VOLUME 71 
1984 


ANNALS > 


" THE 


MISSOURI BOTANICAL GARDEN 


The ANNALS, published quarterly, contains papers, primarily in 
systematic botany, contributed from the Missouri Botanical Garden, 
St. Louis. Papers originating outside the Garden will also be ac- 
cepted. Authors should write the Editor for information concerning 
arrangements for publishing in the ANNALS. 


EDITORIAL COMMITTEE 


Morin, Editor 
Missouri Botanical Garden 


CHERYL В. BAUER, Editorial Assistant 
Missouri Botanical Garden 


MARSHALL R. CROSBY 
Missouri Botanical Garden 


DAVIDSE 
Missouri Botanical Garden 


OHN D. DWYER 
Missouri Botanical Garden & St. Louis University 


ER GOLDBLATT 
Missouri Botanical Garden 


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© Missouri Botanical Garden 1985 


ISSN 0026-6493 


ANDERSON, GREGORY J. The Evolution of Dioecy — Introduction ____ E 
ARMBRUSTER, W. SCOTT & ANN L. HERZIG. Partitioning and Sharing of 
Pollinators by Four Sympatric Species of Dalechampia (Euphorbi- 
aceae) in Panama 
ATWOOD, JoHN T. A Floristic Study of Volcán Mombacho Department 
of Granada, Nicaragua 
AVERETT, JOHN E. (See Shirley A. Graham & John E. Averett) ______ : 
AVERETT, JOHN E. & PETER Н. RAVEN. Flavonoids of Onagraceae ......... 
AVERETT, JOHN E. & SHIRLEY A. GRAHAM. Flavonoids of Rhynchocaly- 
caceae (Myrtales) 
BAAS, PIETER. (See Ger J. C. M. van Vliet & Pieter Baas) 
BAKER, HERBERT G. & PAUL ALAN Cox. Further Thoughts on Dioecism 
and Islands 
BARRETT, SPENCER С. Н. Variation in Floral Sexuality of Diclinous Aralia 
(Araliaceae) 
BARRINGER, KERRY. A New Species of Guatteria (Annonaceae) from Pan- 


BAUM, BERNARD R., THOMAS DUNCAN & RAYMOND B. PHILLIPS. A Bib- 
liography of Numerical Phenetic Studies in Systematic Botany ____ 
Bawa, К. S. The Evolution of Dioecy — Concluding Remarks _____-_-- 
Bawa, К. 5. (See W. A. Haber & K. S. Bawa) 
BEHNKE, H.-DiETMAR. Ultrastructure of Sieve-element Plastids of Myr- 
tales and Allied Groups 
BERNHARDT, P., J. KENRICK & R. B. KNox. Pollination Biology and the 
Breeding System of Acacia retinodes (Leguminosae: Mimosoideae) _. 
BERRY, PAULE. (See Joan W. Nowicke, John J. Skvarla, Peter H. Raven 
& Paul E. Berry) 
BOUFFORD, DAVID Е. Circaea alpina L. (Onagraceae) in Thailand _____. 
BRIGGS, B. О. (See L. A. S. Johnson & В. О. Briggs) 
CARLQUIST, SHERWIN. Wood and Stem Anatomy of Bergia suffruticosa: 
Relationships of Elatinaceae and Broader Significance of Vascular Tra- 
cheids, Vasicentric Tracheids, and Fibriform Vessel Elements .................. 
COETZEE, J. A. & J. MULLER. The Phytogeographic Significance of Some 
Extinct Gondwana Pollen Types from the Tertiary ofthe Southwestern 
Cape (South Africa) 
Cox, PAUL ALAN. (See Herbert С. Baker & Paul Alan Cox) ____------- 
CRANE, PETER R. (See David L. Dilcher & Peter R. Crane) 
CRANE, PETER В. & DAVID L. DitcHER.  Lesqueria: An Early Angiosperm 
Fruiting Axis from the Mid-Cretaceous 
CREPET, WILLIAM L. Advanced (Constant) Insect Pollination Mecha- 
nisms: Pattern of Evolution and Implications Vis-à-Vis Angiosperm 
Diversity __ 


243 


232 


1088 
244 
351 


384 


607 


CREPET, WILLIAM. (See David Dilcher & William Crepet) 


CRONQUIST, ARTHUR. A Commentary on the Definition of the Order 
es 


DAHLGREN, ROLF & ROBERT F. THORNE. The Order Myrtales: Circum- 
scription, Variation, and Relationships 


DANIEL, THOMAS Е. A Revision of Stenandrium (Acanthaceae) in Mexico 
and Adjacent Regions 


DAVIDSE, GERRIT & R. P. ELLIS. Steyermarkochloa unifolia, a New Genus 
from Venezuela and Colombia (Poaceae: Arundinoideae: Steyermark- 
ochloeae) 


DEDICATION 


DILCHER, DAVID & WILLIAM CREPET. Historical Perspectives of Angio- 
sperm Evolution 


DILCHER, DAVD L. (See Peter К. Crane & David L. Dilcher) ______ Зи 


DILCHER, DAvID L. & PETER R. CRANE. Archaeanthus: An Early Angio- 
sperm from the Cenomanian of the Western Interior of North 
America 


DOEBLEY, JOHN Е. Maize Introgression into Teosinte — A Reappraisal __ 


DUNCAN, THOMAS. (See Bernard R. Baum, Thomas Duncan & Raymond 
B. Phillips) 


DUNN, DAvip B. (See Ana Maria Planchuelo & David B. Dunn) _____. : 
ELLIS, R. P. (See Gerrit Davidse & В. P. Ellis) 


FREEMAN, D. C., E. D. MCARTHUR & K. T. HARPER. The Adaptive Sig- 
nificance of Sexual Lability in Plants Using Atriplex canescens as a 
Principal Example 


FRus, E. M. Preliminary Report of Upper Cretaceous Angiosperm Re- 
productive Organs from Sweden and Their Level of Organization 


GADELLA, T. W. J. Notes on Symphytum (Boraginaceae) in North Amer- 
ica 


GENTRY, ALWYN Н. Klainedoxa (Irvingiaceae) at Makokou, Gabon: Three 
Sympatric Species in a Putatively Monotypic Genus 


GENTRY, ALWYN H. New Species and Combinations in Apocynaceae from 
Peru and Adjacent Amazonia .. 


GOLDBLATT, PETER. New Species of Galaxia ideae) and Notes on 
Cytology and Evolution in the Genus _ e: 

GOLDBLATT, PETER. (See Warren L. Nl & Peter Goldblatt) 

GOLDBLATT, PETER, JAMES Е. HENRICH & PAUL RUDALL. Occurrence of 


Crystals in Iridaceae and Allied Families and Their Bisse Sig- 
nificance 


GOLDBLATT, PETER, VIRGINIA WALBOT & oe A. ZIMMER. 
Estimation of Genome Size (C-Value) in Iridaceae - Cytophotome- 
try 


348 


780 


633 


1028 


GRAHAM, ALAN. Lisianthius Pollen from the Eocene of Panama _____ 
GRAHAM, SHIRLEY A. Alzateaceae, A New Family of Myrtales in the 
American Tropics 
GRAHAM, SHIRLEY A. (See John E. Averett & Shirley A. Graham) ......... 
GRAHAM, SHIRLEY A. & JOHN E. AVERETT. Flavonoids of Alzateaceae 
yrtales) 
HABER, W. А. & К. S. Bawa. Evolution of Dioecy in Saurauia (Dillen- 
тасеае) 
HAMPSHIRE, RACHEL & DAVID SUTTON. Alectra aspera (Cham. & Schlecht.) 
L. O. Williams 
HARPER, К. T. (See D. C. Freeman, E. D. McArthur & К. T. Harper) ... 
HAYNES, ROBERT R. Techniques for Collecting Aquatic and Marsh 
Plants 
HENRICH, JAMES E. (See Peter Goldblatt, James E. Henrich & Paul 
Rudall) 
HERZIG, ANN L. (See W. Scott Armbruster & Ann L. Herzig) ... 
HOCH, PETER C. & PETER Н. RAVEN. A New Combination for a North 
American Epilobium 
HOLM-NIELSEN, L. В. (See P. M. Jorgensen, J. E. Lawesson & L. B. Holm- 


Nielsen) 

Hurr, MicHAEL J. A New Combination in Dalechampia (Euphorbia- 
ceae) 

Hurr, MICHAEL J. A Review of Euphorbia (Euphorbiaceae) in Baja Cal- 
ifornia 


HUGHES, NORMAN Е. Mesosperm Palynologic Evidence and Ancestors of 
Angiosperms 
JORGENSEN, P. M., J. E. LAWESSON & L. B. HOLM-NIELSEN. A Guide to 
Collecting Passionflowers 
JOHNSON, L. A. S. & В. С. BRIGGS. Myrtales and Myrtaceae—A Phylo- 
genetic Analysis 
Jones, ALMUT G. (See Porter P. Lowry П & Almut С. Jones) ............................ 
KEATING, RICHARD C. Leaf Histology and its Contribution to Relation- 
ships in the Myrtales 
KENRICK, J. (See P. Bernhardt, J. Kenrick & R. B. Knox) 
КМАРР, SANDRA & JAMES MALLET. Two New Species of Passiflora 
(Passifloraceae) from Panama, with Comments on Their Natural 
History 
Knox, В. B. (See P. Bernhardt, J. Kenrick & К. B. Knox) 
KRASSILOV, VALENTIN A. New Paleobotanical Data on Origin and Early 
Evolution of Angiospermy 


LAWESSON, J. E. (See P. M. Jorgensen, J. E. Lawesson & L. B. Holm- 
1 


Nielsen) 


Lowry, PORTER P., П & ALMUT С. JONES. Systematics of Osmorhiza Raf. 
(Apiaceae: Apioideae) 
McARTHUR, E. D. (See D. C. Freeman, E. D. McArthur & K. T. Har- 
per) 
MCDADE, LUCINDA A. Systematics and Reproductive Biology of the Cen- 
tral American Species of the Aphelandra pulcherrima Complex (Acan- 


thaceae) 
MALLET, JAMES. (See Sandra Knapp & James Mallet) 
MEAGHER, THOMASR. Sexual Dimorphism and Ecological Differentiati 


of Male and Female Plants 


MORLEY, THOMAS. An Index to the Families in Engler and Prantl’s “Die 
Natürlichen Pflanzenfamilien” 


MULLER, J. (See J. A. Coetzee & J. Muller) 
MULLER, JAN. Significance of Fossil Pollen for Angiosperm History ............ 


МОМСКЕ, JOAN W., JOHN J. SKVARLA, PETER H. RAVEN & PAUL E. 
BERRY. А Palynological Study of the Genus Fuchsia (Onagraceae) _ 


PATEL, VARSHA C., JOHN J. SKVARLA & PETER H. RAVEN. Pollen Char- 
acters in Relation to the Delimitation of Myrtales 


PHILLIPS, RAYMOND B. (See Bernard R. Baum, Thomas Duncan & Ray- 
mond B. Phillips) 


PLANCHUELO, ANA MARIA & DAVID B. DUNN. The Simple Leaved Lu- 
pines and Their Relatives in Argentina 


RAVEN, PETER H. The Order Myrtales: A Symposium 
RAVEN, PETER H. (See Hiroshi Tobe & Peter H. Raven) 
RAVEN, PETER H. (See Hiroshi Tobe & Peter H. Raven) 
RAVEN, PETER H. (See Peter C. Hoch & Peter H. Raven) 


RAVEN, PETER H. (See Varsha C. Patel, John J. Skvarla & Peter H. Ra- 
ven) 


RAVEN, PETER Н. (See Joan W. Nowicke, John J. Skvarla, Peter Н. Raven 
& Paul E. Berry) 


RUDALL, PAUL. (See Peter Goldblatt, James E. Henrich & Paul 
Rudall) 


SCHAARSCHMIDT, FRIEDEMANN. Flowers from the Eocene Oil-Shale of 
Messel: A Preliminary Report 


SCHMID, RUDOLF. Reproductive Anatomy and „ы of Myrtales 
in Relation to Systematics 


SKVARLA, JOHN J. (See Varsha C. Patel, John J. Skvarla & Peter H. Ra- 
уеп). 


SKVARLA, JOHNJ. (See Joan W. Nowicke, John J. Fast Peter H. Raven 
& Paul E. Berry) 


STEYERMARK, JULIAN A. Flora of the ME ШО Gun: 
STEYERMARK, JULIAN A. New Rubiaceae from Venezuela . 


1128 


1068 


1088 


1013 _ 


1175 | 


SUTTON, DAVID. (See Rachel Hampshire & David Sutton) 
TAYLOR, CHARLOTTE M. Psychotria hebeclada DC. (Rubiaceae), an Over- 
looked Species from Central America 
THANIKAIMONI, K. Principal Works on the Pollen Morphology of Myr- 
tales 
THORNE, ROBERT Е. (See Rolf Dahlgren & Robert Е. Thorne) _______ 
TIFFNEY, BRUCE H. Seed Size, Dispersal Syndromes, and the Rise of the 
Angiosperms: Evidence and Hypothesis 
TOBE, HIROSHI & PETER Н. RAVEN. The Embryology and Relationships 
of Alzatea Ruiz & Pav. (Alzateaceae, Myrtales) 
TOBE, HIROSHI & PETER Н. RAVEN. The Embryology and Relationships 
of Rhynchocalyx Oliv. (Rhynchocalycaceae) 
UPCHURCH, GARLAND R., JR. Cuticle Evolution in Early Cretaceous An- 
giosperms from the Potomac Group of Virginia and Maryland _____ 
UPCOMING MEETINGS 
AETFAT 
Second International Legume Conference 
VLIET, GER J. C. M. VAN & PIETER BAAS. Wood Anatomy and Classifi- 
cation of the Myrtales 
WAGNER, WARREN L. Reconsideration of Oenothera Subg. Gauropsis 
(Onagraceae) 
WAGNER, WARREN L. & PETER GOLDBLATT. A Survey of Seed Surface 
Morphology in Hesperantha (Iridaceae) 
WALBOT, VIRGINIA. (See Peter Goldblatt, Virginia Walbot & Elizabeth A. 
Zimmer) 
WALKER, AUDREY С. (See James W. Walker & Audrey С. Walker) ____ 
WALKER, JAMES W. & AUDREY G. WALKER. Ultrastructure of Lower Cre- 
taceous Angiosperm Pollen and the Origin and Early Evolution of 
Flowering Plants 
WERFF, HENK VAN DER. Notes on Neotropical Lauraceae 
ZAVADA, MICHAEL $. Angiosperm Origins and Evolution Based on Dis- 
persed Fossil Pollen Ultrastructure 
ZIMMER, ELIZABETH A. (See Peter Goldblatt, Virginia Walbot & Elizabeth 
A. Zimmer) 


1184 


1114 


ANNALS 


ISSOUR] BOTANICAL GARDEN 


UME 71 1984 NUMBER 1 


А CORNUS KOUS. 
СОМТЕМТ5 


Partitioning and Sharing of Pollinators by Four Sympatric Species of Dal- 
echampia (Euphorbiaceae) in Panama W. Scott Armbruster & Ann 


Г. Herzig _ 1 
Pollination Biol and the Breeding System of Acacia retinodes e 

nosae: Mimosoideae) P. Bernhardt, J. Kenrick & R. B. Knox ____ 17 
Flavonoids of Onagraceae John E. Averett & Peter H. Raven .. we W 
A Palynological Study of the Genus Fuchsia (Onagraceae) Joan w. Now 

icke, John J. Skvarla, Peter H. Raven & Paul E. Berry 35 
The Simple Leaved Lupines and Their Relatives in Argentina Ana Maria 

Planchuelo & David B. Dunn 92 


Systematics and Reproductive Biology of the Central American Species of 
the Aphelandra pulcherrima Complex (Acanthaceae) Lucinda A. 
d 


McDade ____ 104 
Klainedoxa (Irvingiaceae) at Makokou, Gabon: Three Sympatric Species in 

a Putatively Monotypic Genus Alwyn Н. Gentry 166 
Psychotria hebeclada DC. (Rubiaceae), an Overlooked Species from Central 

America Charlotte M. Taylor 169 
Estimation of Genome Size (C-Value) in Iridaceae by Cytophotometry 

Peter Goldblatt, Virginia Walbot & Elizabeth A. Zimmer 176 


Contents continued on back cover 


VOLUME 71 


NUMBER 1 


ANNALS 


MISSOURI BOTANICAL GARDEN 


The ANNALS contains papers, primarily in systematic botany, 
contributed from the Missouri Botanical Garden. Papers originating 
outside the Garden will also be accepted. Authors should write the 
Editor for information concerning arrangements for publishing in 
the ANNALS. 


EDITORIAL COMMITTEE 


NANCY Morin, Editor 
Missouri Botanical Garden 


CHERYL В. BAUER, Editorial Assistant 
Missouri Botanical Garden 


MARSHALL R. CROSBY 
Missouri Botanical Garden 


GERRIT DAVIDSE 
Missouri Botanical Garden 


JOHN D. Dwyer 
Missouri Botanical Garden & St. Louis University 


PETER GOLDBLATT 
Missouri Botanical Garden 


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© Missouri Botanical Garden 1984 


VOLUME 71 
1984 


ANNALS 


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MISSOURI BOTANICAL GARDEN 


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This volume of the ANNALS is dedicated to George Engelmann (1809-1884), 
who, though never formally associated with the Missouri Botanical Garden, was 
influential in establishing a program of scientific research here. 

Engelmann was born in Frankfort-am-Main in the same year that Abraham 
Lincoln was born southwest of Frankfort, Kentucky, and Charles Darwin was 
born in England. His involvement with the Burchenschaft, a liberal German 
fraternal organization, caused his migration from the University of Heidelberg, 
to Berlin, to Wiirzburg, where he received his medical degree in 1831. He then 
spent a few months in Paris renewing old university acquaintances with Louis 
Agassiz, Karl Schimper, and Alexander Braun; botanizing in the Bois du Boulogne; 
and studying the latest cholera epidemic, before departing for the United States 
in the fall of 1832 as an emissary for his family, to investigate the advisability 
and feasibility of immigration to Das Westland. 

he next two plus years were spent investigating and exploring western Illinois, 
Missouri, and Arkansas. By the fall of 1835 he was flat broke and established a 
medical practice in St. Louis with the goal of earning enough money in a few 
years to return permanently to Germany. But he never did. His medical practice 
boomed, because the population was growing rapidly, doubling every few years, 
due in no small part to German immigration, and, probably, because his European 
training was better than that of most local practitioners. In 1840 he returned to 
Germany to marry his long-time sweetheart, Dorothea Horstmann. On the return 
trip to St. Louis, Engelmann met Asa Gray in New York, establishing a close 
working relationship that would last the rest of his life. 

The first of Engelmann's many publications on North American botany ap- 
peared in 1842, *A monography of North American Cuscutinae," in the American 
Journal of Science, *Silliman's Journal." Engelmann participated in the foun- 
dation of St. Louis's Western Academy of Science in 1835, and he, Adolphus 
Wislizenus, William Greenleaf Eliot, and Marie P. Leduc attempted to establish 
a botanical garden near the southwestern edge of the city in 1843. These ideas 
were, perhaps, just a bit ahead of their time: neither institution lasted long or 
contributed significantly to the advance of knowledge. However, by the late 1850's 
things had changed: in 1856 Engelmann was a founder of the St. Louis Academy 
of Science, which survives today as the St. Louis Museum of Science and Natural 
History, and he helped mold Henry Shaw's concept of a Botanical Garden to 
include a herbarium and library. Shaw opened his Missouri Botanical Garden to 
the public in 1859, and among its most handsome features was the Botanical 
Museum & Library, in which was installed the herbarium of J. J. Bernhardi of 
Leipzig, which Engelmann had purchased on Shaw’s behalf for $400 while on an 
extended trip to Europe. The Bernhardi herbarium contained about 68,000 spec- 
imens. 

Engelmann maintained a demanding medical practice. A reflection of his de- 
votion to medicine is the fact that though he was one of the 50 original “incor- 
Porators” of the Congressionally established National Academy of Sciences in 
1863, he resigned his membership four years later because his practice would not 
allow him to attend its sessions. 

Monographic publications continued to pour from his steel pen until shortly 
before his death. Cuscuta was not the only difficult, tedious group on which he 
worked. Indeed, he concentrated his efforts on such groups: Quercus, Vitis, Cac- 
laceae, conifers, /soétes. His detailed studies of these and other taxa laid the 
foundations for future workers. 


Engelmann also contributed indirectly to our understanding of plants by acting 
as a middle-man between the West and the East. Strategically positioned in St. 
Louis, the gateway to much western trade, exploration, migration, and adventure, 
he hired and trained individuals—Joshiah Gregg, Ferdinand Lindheimer, Au- 
gustus Fendler— to collect and advised military leaders—John Charles Frémont, 
William Emory— as they lead their troops west, assuring a steady flow of spec- 
imens moving from the hitherto unexplored West to the botanical centers of the 
East, especially into the hands of John Torrey and Asa Gray. 

The Thirtieth Annual Systematics Symposium, held at the Missouri Botanical 
Garden on 19 and 20 October 1984, also commemorated George Engelmann, 
concerning itself with our current knowledge of many of the taxa he studied, 
southwestern floristics, and his life and relations with contemporaries. The pro- 
ceedings of the Symposium will appear in a future issue of the Annals. 


Siu nt ни сви a ee es ee eee сеје РРА 


ANNALS 


MISSOURI BOTANICAL GARDEN 


1984 NUMBER 1 


VOLUME 71 


PARTITIONING AND SHARING OF POLLINATORS BY 
FOUR SYMPATRIC SPECIES OF DALECHAMPIA 
(EUPHORBIACEAE) IN PANAMA! 


W. SCOTT ARMBRUSTER? AND ANN L. HERZIG? 


ABSTRACT 


Observations were made on distribution, рот! morphology, and о нов нА four species of 
Dalechampia (Euphorbiaceae) in central Pan . The four species r sympatrically in various 
combinations throughout Panama and are Se lineal by ерее оао" bees, and resin- 

and/or pollen-collecting stingless bees and megachilid bees. With one exception, these plant + pense 
pre very little in pollinators or time of pollination еа 
in the day by Tune and Бурачка whereas a sympatric congener, D. scandens, is satan 


by the same species of bees late in the day. A 


by euglossine bees. GY e also oc 
Individuals of DUMO dioscoreifolia and D. tiliifolia were 


oe by euglossine bees. 


rved occurring together at only one " here they s 
of day. Interspecific pollen flow was substantial and d 


receptive to pollination at the same tim 


third брате ессе Р. dioscoreifolia, is pollinated 


patrically with D. tiliifolia; the latter 


shared pollinators (euglossine bees) and w 


have resulted in depressed seedset in D. pores, 


A number of authors have suggested that plant 
communities are likely to be organized in ways 
that minimize reproductive interference (Levin, 
| 1970; Levin & Anderson, 1970; Mosquin, 1971; 
| Straw, 1972; Reader, 1975; Heinrich, 1975). [We 
| here define the term "reproductive interference" 
| to include all plant-plant interactions that have 
| direct detrimental effects on reproductive pro- 
| cesses, including competition for pollinator ser- 
| vice, interspecific pollen transfer, and competi- 
tion for agents of seed dispersal; this is more 


ыт 
UWw 

e wish 

Dressler for assistance in Panama, 


inclusive than the phrase "competition for pol- 
lination" used by Waser (1982).] There have been 
a reed of ne that indicate such organi- 
natural communities (Snow, 
1966: Frankie, 14005; Reader, 1975; Heinrich, 
1976a; Stiles, 1975, 1977; Feinsinger, 1978; Wa- 
ser, 1978a; Brown & Kodric-Brown, 1979; Par- 
rish & Bazzaz, 1979). However, as several au- 
thors have pointed out, before claiming that 
organizing processes have affected community 
structure it is necessary to show statistically that 


to thank the Smithsonian Tropical Research Institute for the use of their facilities, Don Windsor 
Irene Baker for information on the 


paints, Kim Steiner and 


| Robbin Foster for information on distribution and phenology, Robert Dressler for identifying euglossine bees, 
ave Roubik for identifying the Trigona, Karen Harris for — in making greenhouse crosses, and Jim 


, John Bryant, Terry Chapin, Steve cad Kim Ste 


С 
TOwder, and an anonymous reviewer for reading the m 


| during ies hon supported by grant #DEB78-24218 ini the National Science Foundation. 

y, University of California, Davis, California 95616. Present address: Departmen 

Biology, University of Alaska, Fairbanks, Alaska 99701. 
Fairban 


x Depart nt of Botan 
1010ру, рые and Wildlife and Institute of Arctic 


> Institute of Northern Forestry, USDA Forest Service, 308 Tanana Dr., 


_ANN. MISSOURI Bor. GARD. 71: 1-16. 1984. 


iner, Ed Murphy, Grady Webster, Cheryl 
uscript and making valuable suggestions. Field work 


of 


ks, Alaska 99701. 


2 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


niche overlap in a community is less than that 
of a randomly generated assemblage of species 
(Connor & Simberloff, 1979; Poole & Rathcke, 
1979; Strong et al., 1979). Further, as Gran 
(1972), Roughgarden (1976), Feinsinger (1978), 
Slatkin (1980), Waser (1983), and others have 
pointed out, the observed organization may be 
either the result of evolution of the component 
species in response to their biotic environments 
or the result of the sorting of preadapted species 
into “compatible” associations. It is difficult, at 
best, to distinguish between these two processes. 

These limitations notwithstanding, we believe 


e 


relationships between members of species as- 

semblages. While detailed studies of a single 

community usually cannot demonstrate com- 

munity organization, they may reveal the selec- 

tive pressures that have been operating and the 
"cost" of not being adapted to sympatry. 

We have been interested in how assemblages 
of sympatric species of Dalechampia (Euphor- 
biaceae) are organized, especially with respect to 
use of the pollinating fauna and to potential in- 
terspecific pollen flow. The pollination systems 
of three gg UY id bec] gsm of 
been discussed D eo and Webster (1979, 
1981, 1982). In each case the pollinators were 
effectively partitioned, and there was very little 
interspecific pollen flo 


Dalechampia (D. dioscoreifolia, D. heteromor- 
pha, D. scandens, and D. tiliifolia) that occur in 
several combinations of sympatry in Panama and 
examine the relationships with pollinators, the 
extent of resource partitioning, and the amounts 
of interspecific pollen flow 

Dalechampia contains about 100 species, most 
of which are small to moderate-sized lianas of 
lowland neotropical habitats. All species are 
monoecious; the unisexual flowers are grou 
together into functionally bisexual LM 
inflorescences (Webster & Webster, 1972). I 

most species studied, including those и 

е 


structure that secretes resin (Armbruster & Web- 
ster, 1979). The whole inflorescence is subtended 
by two usually large and showy bracts 

In most species of Dalechampia, including the 
subjects of this study, the pistillate flowers are 
receptive several days prior to anthesis of the 
staminate flowers in the same inflorescence. Sub- 


(Мог. 71 | 


sequently there is а bisexual phase during which 
the pistillate flowers are still receptive, but the 
staminate flowers are also open and pollen is 
being shed. During the bisexual phase зен -рој- 


that have’ = tested are self-compatible, self- 
fertilization may result (Armbruster, unpubl.). 
During pistillate phase iiag cross-pollination 
is possi 
Most gene of Dalechampia are pollinated 
by female bees that collect the resins secreted by 
with the sta- 
minate flowers (Armbruster & Webster, 1979, 
1981, 1982). The amount of resin secreted de- 
termines the size of the largest floral visitors. 
Apparently due to energetic constraints on for- 
aging behavior, only small bees visit Dalecham- | 
pia species that secrete small amounts of resin, | 
whereas large bees (euglossines) visit only those 
species of Dalechampia bearing larger amounts 
of resin (Armbruster & Webster, 1981, 1982; 
Armbruster, in prep.). 
Because of the viscous, sticky nature of floral _ 
resins, it is very difficult to measure the rate of _ 
resin secretion. Experimental removal of resin — 


open, and about 0.5-1.5 mm (depth) of resin 
accumulates across the surface of the gland daily 
Armbruster, unpubl.). Dalechampia dioscorei- 
folia appears to follow this pattern as well. 
cause the rates of secretion are similar in all | 
soi studied and because of the difficulties in 
measuring secretion rates, the area of secretion 
is is probably the best singe field Measurement of | 


2 
БУ Ч tity wiv aging | 


bees. 
he arrangement of the staminate and pistil- - 


champia in which the gland-stigma and gland- | 
anther distances are smaller («ca. 4 mm) can be \ 
pollinated by smaller bees (Armbruster & Web- | 
ster, 1981, 1982; Armbruster, in prep.). q 


MATERIALS AND METHODS 


Observations on the reproductive biology 0 
Dalechampia species were made in the 
Zone of the Republic of Panama during three . 


1984] 


separate periods: 30 Јипе–3 July 1978, 14-18 
November 1978, and 9—27 January 1980. Inten- 
sive observations were made on three species, 
D. dioscoreifolia Poepp. & Endl., D. heteromor- 
pha Pax & Hoffmann (Pax & Hoffmann, 1919; = 
D. cissifolia subsp. panamensis, Webster & Burch, 
1968; Croat, 1978), and D. scandens L., where 
they occurred together at km 13 Pipeline Road. 
Intensive observations were also made on 
dioscoreifolia, D. heteromorpha, and D. tiliifolia 
Lam. where they occurred together at km 15 
Pipeline Road. Additional observations were 
made on these species at 10 other sites in the 
Canal Zone, including elsewhere along Pipeline 
Road (as far as Rio Casanga), Madden Dam, 
Madden Reserve, Barro Colorado Island, and 
near the Summit Gardens. 

For each species we tagged 19—52 inflores- 
cences on 5—7 plants and daily monitored changes 
in number of staminate flowers open, amount of 
resin present, and the amount and, when pos- 
sible, type of pollen on the stigmas. Resin amounts 
were estimated by observing the depth on the 
gland. Pollen grains, which are large (ca. 50—150 
um), were counted with the aid of a hand 
lens; we were able to distinguish between the 
Pollen of D. tiliifolia and D. dioscoreifolia on the 
basis of size. Dalechampia pollen was distin- 
guishable from pollen of other plants common 
in the area on the basis of size and color. At half- 
hour or hour intervals the position of the invo- 
lucral bracts was assessed. Measurements were 
made of the gland size and minimum distances 
between the gland and stigmas, the gland and 
anthers, and the anthers and stigmas, using dial 
calipers accurate to 0.05 mm. 

Observations on pollinators included counting 
floral visitors, noting the amount and color of 
their corbicular/scopal loads, recording their be- 
havior and monitoring their movements. To fa- 
cilitate these Observations some bees were cap- 
tured, marked on the scutum with correction 
fluid, and released. Effectiveness of pollinators 
Was determined by monitoring changes in num- 
ber of pollen grains on the stigmas of each species; 
effective pollinators (Table 3) are those that were 
observed to regularly transfer Dalechampia pol- 
€n to Dalechampia stigmas. Visitation rates were 
calculated for each pollinator species by sum- 
ming the number of visits observed and dividing 
by the number of days of observation and by the 
mean number of inflorescences open in the ob- 
Servation area during the period of observation. 

Y days in which observations were made 


ARMBRUSTER & HERZIG— DALECHAMPIA 3 


throughout the period of bract opening were in- 
cluded in calculating means. To assess the move- 
ment of pollen within and among species, sta- 
minate flowers of each species were dusted at 
short intervals with specific colors of powdered, 
non-toxic, fluorescent paint; transfer of paint 
granules was recorded periodically. Vouchers of 
plant species and floral visitors were collected. 
In the lab pollen loads were removed from vis- 
itors, slides made using Hoyer's medium, and 
pollen identified with a microscope. Plant vouch- 

ers have been deposited at DAV and SCZ. 
Experimental intraspecific and interspecific 
crosses, measures of selfing ability and stigmatic 
receptivity, and tests of self-compatibility were 
erformed on cultivated material of all four 
species in the greenhouses at the University of 
California, Davis from 1975 until 1980. Crosses 
were made by removing all staminate flowers 
while in bud and manually transferring pollen 
with a small camel's-hair brush. Stigma recep- 
tivity was tested by pollinating stigmas in emas- 
» ьа майин 


> ттүү 


peroxidase activity with Peroxtesmo KO paper. 


RESULTS 
DISTRIBUTION AND FLOWERING TIME 


Dalechampia dioscoreifolia, D. heteromorpha, 
D. scandens, and D. tiliifolia are all locally com- 
mon in forested and/or open areas of the Canal 
Zone and other parts of Panama. While at the 
majority of the 12 study sites only one or two 
species were present, at two sites we were able 
to observe three species occurring sympatrically 
(Table 1). Dalechampia dioscoreifolia occurred 
sympatrically with D. heteromorpha at four sites, 
and with D. scandens at three sites. Dalechampia 
heteromorpha occurred with D. scandens at one 
site and with D. tiliifolia at two sites. Dalecham- 
pia dioscoreifolia and D. tiliifolia occurred to- 
gether at one site, but D. tiliifolia was restricted 
to the open scrub, whereas D. dioscoreifolia oc- 
curred in the forest (Table 1). The two species 
grew close together only at the ecotone of the 
forest and scrub communities. 

The data on flowering phenology of Panama- 
nian Dalechampia are limited; however, it is pos- 
sible to make a first approximation based on our 
observations in 1978 and 1980, on available col- 
lections, and from the literature. The phenolog- 
ical data presented in Table 2 are based on our 
observations made in Panama during July, No- 


4 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 
TABLE 1. Observed co-occurrence and ecological distribution of four species of Dalechampia in central 
апата 
D. dioscoreifolia D. heteromorpha D. scandens D. tilüfolia 
Site: 
km 13, Pipeline Rd. F + + 
km 15, Pipeline Rd. + + + 
km 17, Pipeline Rd. + Е 
Madden Reserve + + 
Madden Dam + + 
Summit Garden + + 
Barro Colorado mel + + 
Habitat: 
Closed Forest + + ? 
Open Forest + = Е 
Forest Edge + + + + 
Secondary Scrub + ? + 
Open Fields Tu + 


vember and January, nearly ipei ste obser- 
vations of K. E. Steiner (pers. comm.), Croat’s 
observations (197 8), and занн" of Pana- 

manian specimens from ; an H 
(Dalechampia dioscoreifolia: 5 sheets; D: hetero- 
morpha: 4 sheets; D. scandens: 3 sheets; D. ti- 
liifolia: 18 sheets). These data are further cor- 
roborat y our observations made on these 
four species i in other parts of Mesoamerica and 
1975 
to 1980. eremi phenological information 


of the population ipn new flowers 
боной the blooming se 
ree of the shaper of зечеве bloom 
primarily during the late wet and dry seasons 
and ано interference between members 
of each sympatric species could be occurring at _ 
this time. Thus, there is potential reproductive — 
oe with congeners affecting D. tiliifolia, 
candens, and possibly D. dioscoreifolia 
кенен the flowering season of each. How- 
ever, since р. heteromorpha blooms year-round, 


can be glean р- 
ulations, even at a few times of the year: Mee 
previous 1–3 months’ flowering activities аге re- 
corded in fruits of various stages of maturation 
or dehiscence; the future month of flowering ac- 
tivities can be predicted by examining plants for 
inflorescence buds. In all four (as studied 
throughout the Neotropics), all “mature” mem- 


from tier species for about half of the year (cf. 
Table 2). 


BREEDING SYSTEMS 


ws Ta 32.137 ex ~ 


shown that Р. dioscoreifolia, D. heteromorpha, 
D. scandens, and D. tiliifolia are self-compatible. 


Flowering phenology of Dalechampia species in central Panama. Table is based on 


TABLE 2. 
observation, herbarium 5 
) 


imens, information presented in Croat, 1978, and verbal reports (K. Steiner, pers. 


comm.). Seasonal assignments follow Ackerman, 1984. (+ indicates abundant flowering occurs during that 
month.) 
Season and Month 
Dry Early Wet Mid Wet Late Wet 
Species Jan Feb Маг Apr May Jun Jul Aug Sep Oct Nov Dec | 

D. dioscoreifolia + + + + +? + + 
D. heteromorpha + + + + + + + + + + + + 
D. scandens + + + a + T 
D. tiliifolia * + + + + 


1984] 


ARMBRUSTER & HERZIG—DALECHAMPIA 


TABLE 3. Floral morphology of Panamanian Dalechampia. Numbers in table are means + s.d. with N in 


parentheses. 

Number 

of Sta- Gland-Stigma Gland-Anther Anther-Stigma 

Dalechampia minate Gland Area Distance Distance Distance 
Species owe (mm?) mm) (mm) (mm) 

D. dioscoreifolia 8-10 30.1 + 12.3 (20) 5.52 34-020) 6.7 + 1.5 (10) 10.2 + 2.0 (9) 
D. heteromorpha 8-10 Due (16) 3.1 + 0.6 (16) 2.2 + 0.4 (9) 0.5 + 0.6 (9) 
D. scandens -10 87 = 30. 00) 3.1 + 0.8 (29) 2.8 + 0.8 (20) 1.8 + 0.8 (20) 
Р. tiliifolia 9-10 22.0 + 4.8 (20) 8.9 + 1.7 (20) 8.2 + 1.0 (15) 30 E 2.1: (15) 


All four of these species set nearly full comple- 
ments of seeds when inflorescences are manually 
self-pollinated and screened from pollinators. 

here are, however, differences among species 
with respect to the ability of each to self-pollinate 
and set seed in the absence of pollinators. Ob- 
servations of pollen movement in a number of 
species have shown that the distance between the 
stigmas and the anthers is a primary determinant 
of the ability of a species to self-pollinate (Arm- 
bruster, in prep.). Accordingly, D. heteromorpha 
with a mean anther-stigma distance of only 0.5 
mm (Table 3) sets abundant seed in the absence 
of pollinators. Plants screened from pollinators 
in greenhouse experiments produce 68% of the 
maximum possible seedset (N = 279). Manually 
selfed material had seedsets of 85% of maximum 
(N = 603), so depression of seedset by the lack 
of insect-mediated pollination, while significant 
(P < 0.001, d = 5.90, normal approximation of 
a distribution; Bailey, 1959), is relatively 

п1 


Dalechampia scandens also has a relatively 
small mean anther-stigma distance (1.8 mm, Ta- 
ble 3); Panamanian material of this species grown 
in the greenhouse set abundant seed in the ab- 
sence of pollinators. A population of D. scandens 
ш Costa Rica with a mean anther-stigma dis- 
tance of 3.6 mm produced 63% of maximum 
Possible seedset (N = 27) when screened from 
pollinators, 

Dalorh Ju y Ec! 3 24. 11 


J Ossie 


tance (3 mm, Table 3) 
and self-pollination when pollinators are absent 
May be relatively frequent. In a population in 
Costa Rica with a mean anther-stigma distance 
hit mm, inflorescences screened from pollina- 
Ors produced 93% of maximum possible seed- 
Set (N = 84). 
P «20есһатріа dioscoreifolia differs from the 
Tee species in having a relatively large 


mean anther-stigma dis 


mean anther-stigma distance (10.2 mm, Table 
3). This strongly suggests that self-pollination in 
the absence of pollinators is rare. In one plant 
screened from pollinators in the greenhouse only 
two out of eight inflorescences set seed. A closely 
related species, D. aristolochiifolia H.B.K. has a 
similar inflorescence morphology (distances be- 
tween gland-stigma = 5.8 mm, gland-anther = 
9.1 mm, anther-stigma = 7 mm; compare with 
Table 3) and set no seed when grown in the green- 
house and screened from pollinators (N = 108). 


FLORAL DEVELOPMENT 


The four species of Dalechampia considered 
in this study follow similar patterns of inflores- 
cence development (Table 4). The involucral 
bracts remain closed when the inflorescences are 
in bud. On the first day that the bracts open, the 
stigmas of all four speci ptive. Seed was 
set in greenhouse material of D. heteromorpha, 
D. scandens, and D. tiliifolia that was pollinated 


on the first day ol p 8 1 у 
emasculated and screened from pollinators. All 
four species show positive peroxidase reactions 
on the first day of bract opening. Similar tests 
show that the stigmas remain receptive through- 
out the period of anthesis of the staminate flow- 


Ts. 
Anthesis of the first staminate flower occurs 
on the second to fourth day after the bracts first 
open. Each day for the next four to seven days, 
one to two additional staminate flowers open. 


anthesis and then abscise. Anthesis of the 
ture" staminate flower(s) occurs shortly after the 
bracts open each day (Table 4). In all four species, 
the anthers dehisce shortly after anthesis. 

The involucral bracts open and close in a diur- 
nal cycle characteristic for each of the four species. 
The bracts of D. heteromorpha open daily in the 
early morning, those of D. scandens in the early 


TABLE 4. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


Inflorescence development and behavior. Numbers in columns | and 2 аге means rounded to the 
nearest day with range and sample size in parentheses. 


Time of 
Anthesis of 
Staminate Period Bracts 
Duration of Duration of owers Are Open 
Species 9 Phase (days) $ Phase (days) (hrs) (hrs) 

D. dioscoreifolia 3 (2—5; 8) 4 (3—6; 4) ca. 1500 (1400) 1500-1830 
D. heteromorpha 3 (2—4; 9) 5 (4—6; 7) са. 0700 0600–1900(+) 
D. scandens 2 (1-3; 10) 6 (5—6; 8) ca. 1330 (1300) 1330-1830 
D. tiliifolia 2 (1-3; 6) 5 (5-6; 11) ca. 1430 1400-1800 


afternoon, and those of D. tiliifolia and D. dios- 
E in the c to mic-afternoon: The bracts 
ofall fo 
4). 

In all four species, after ca. seven to nine days 
of receptivity, the inflorescence passes into the 
fruiting phase. The staminate cycle, including the 
resin gland, abscises. The bracts in D. hetero- 

morpha, D. scandens, and D. tiliifolia close 
tiie: the developing capsules. In the last two 
species the bracts suffuse with chlorophyll. In D. 
dioscoreifolia the bracts abscise when the fruits 
begin to develop (cf. Armbruster, 1982). 


„+1 


у after sunset (Table 


INFLORESCENCE MORPHOLOGY 


The basic number and arrangement of sta- 
minate and pistillate flowers in the inflorescences 
is similar in all the four species considered in this 
study (Table 3, Figs. 1—4). However, there is con- 
siderable variation in the color and size of bracts, 
in the size of the resin glands, and in the distances 
between floral structures. Dalechampia hetero- 
morpha has relatively small green bracts (10-25 
mm), and relatively small resin glands (ca. 6.5 
mm7?), gland-stigma distances (ca. 3.1 mm), and 
gland-anther distances (ca. 2.2 mm, Table 3). 
Similarly, D. scandens has relatively small, pale- 
green bracts (10-25 mm), and relatively small 
resin glands (са. 8.7 mm?), gland-stigma dis- 
tances (ca. 3.1 mm) and gland-anther distances 
(ca. 2.8 mm, Table 3). 

In contrast D. tiliifolia has relatively large white 
bracts (20-50 mm), and relatively large resin 
glands (ca. 22 mm"), gland-stigma distances (са. 
8.7 mm), and gland-anther distances (ca. 8.2 mm, 
Table 3). Similarly, D. dioscoreifolia has rela- 
tively large pink bracts (40-50 mm), relatively 
large resin glands (ca. 30.1 mm?), and moderately 
large gland-stigma distances (ca. 5.5 mm), and 
gland-anther distances (ca. 6.7 mm, Table 3). 


The size of the stigmatic tip of the stylar col- 
umn also varies considerably among the four 
species. In Dalechampia heteromorpha this 
structure is relatively small (ca. 0.7 mm?); in D. 
scandens it is slightly larger (ca. 0.8 mm?). In 
Dalechampia tiliifolia and D. dioscoreifolia the 
stigmatic tips are considerably larger (ca. 4 тт? 
and ca. 6 т, respectively). 


POLLINATION AND SEEDSET 


As predicted from studies of other species of | 
Dalechampia (cf. Armbruster & Webster, 1981, 
1982), D. heteromorpha and D. scandens (both | 
with small resin glands) were visited only by small - 
bees, including Hypanthidium panamense and | 
Trigona spp. (Table 5). These bees collected resin 
and/or pollen. We observed no visits by the larg- 
er euglossine bees during 42 hours of observation 
at the Pipeline Road study sites, although these 
bees were active in the area. Because the gland- _ 
stigma and gland-anther distances are small in — 
both of these Dalechampia species, the small bees 
effectively transferred pollen to the stigmas. Pol- — 
len was deposited on the legs and ventral surface _ 
of the thorax and abdomen. The same species 
pollinated D. scandens and D. heteromorpha at _ 
other study sites where these plants were ob- 

rved. 


l4 
e 


At the Pipeline Road study site, D. tiliifolia _ 
and D. dioscoreifolia were visited and pollinat 
by medium-sized to large euglossine bees (EU | 
laema spp., Euglossa bursigera), which collected _ 
resin from the large resin glands (Table 5). Pollen _ 
was deposited on the legs and on the ven | 
surface of the thorax and abdomen. These bee _ 
g D. tiliifoliaand _ 
р. dioscoreifolia at a number of different study | 
sites in Panama and also in Costa Rica (Arm- - 
bruster, unpubl.). Because of the large gland-stig- 
ma and gland-anther distances, smaller bees (such 


ARMBRUSTER & HERZIG— DALECHAMPIA 


Ff 
—1. D. heteromorpha in 
edition, Pointers indicate 
andens in bisexual condition 

ited by Eulaema cingulata. 


Fic 


mars 14. Pa anamanian Dalechampia and ad Scale bars are 5 m 
bisexual condition n being vi igona jaty.— ко їп wwe co 
.D.s 


ted rigona jaty.— 2. D. 
еа бзэ d (to Hi stamin Dale [ee ex isti om).— 


ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


TABLE 5. Floral visitors to Panamanian Dalechampia. Visitation rates based on observations from 9-27 Jan. 
1980. Numbers in column 5 are means + s.d. with N in parentheses. 


Number 
Dalechampia Effective Visitation Rate in of Hours 
i Floral Visitor Polli- Material Visits- Inflores- of Obser- 
(Locality) (Size in mm) nator? Collected cence^!:day^! vation 
D. dioscoreifolia 
(km 13, Pipe- Eulaema cingulata + resin 0.35 + 0.47 (4) 8 
line Rd.) (Fabricius) d 
Eulaema cf. meriana t resin 1.22 + 0.80 (4) 8 
(Olivier) Q9. 
Euglossa sp. (11) + resin 0.05 + 0.08 (4) 8 
(km 15, Pipe- Eulaema cingulata (22) + resin 0.81 + 0.25 (5) 20 
line Rd.) Euglossa sp. (11) Е геѕіп 0.08 + 0.08 (5) 20 
D. heteromorpha 
(km 13, Pipe- Hypanthidium panamense + resin and 0.97 + 0.48 (3) 42 
line Rd.) Cockerell (7) pollen 
Trigona perangulata + pollen 4.52 + 1.54 (3) 42 
Cockerell (6) 
Trigona jaty Smith (5) + resin 0.05 + 0.09 (3) 42 
Trigona fulviventris = pollen 0.02 + 0.03 (3) 42 
Guerin (6) 
Trigona sp. (3) — resin 0.12 + 0.06 (3) 42 
D. scandens 
(km 13, Pipe- Hypanthidium panamense + resin and 0:32 += 026: (3) 42 
line Rd.) (7) pollen 
Trigona perangulata + pollen 5.25 + 2.39 (3) 42 
(6) 
Trigona jaty (5) + resin 0.08 + 0.14 (3) 42 
Trigona sp. (3) – геѕіп 0.10 + 0.10 (3) 42 
Р. tiliifolia 
(кт 15, Ріре- Eulaema cingulata (22) + resin 1.31 £ 0.86 (5) 20 
line Rd.) Euglossa bursigera + resin 0.005 + 0.012 (6) 20 
Moure (11) 
Tetrapedia sp. (8) – pollen 0.05 + 0.07 (5) 20 


This bee was only observed with binoculars. Due to extreme similarity of mimetic euglossines, we cannot - 


i certain that this is E. meriana (cf. Dressler, 1979). 


as Paratetrapedia, Table 5) are not effective pol- 
linators of D. tiliifolia or D. dioscoreifolia. 

n these four species of Dalechampia, a full 
complement of nine seeds usually develops if 
pollination is adequate (cf. Armbruster, 1982). 
There is no evidence suggesting that selective 
abortion occurs or that, in healthy plants, ab- 
scission of inflorescences is due to anything other 
than lack of pollination. In D. dioscoreifolia, of 
19 pistillate flowers that had been tagged and 
monitored and later abscised, 16 (8496) lacked 
pollen on the stigmas, 3 (1696) had <5 grains per 
stigma and none had >5 grains per stigma. In 
D. scandens, of 15 monitored inflorescences that 
abscised, 8 (53%) had <5 grains per stigma, 6 


(40%) had between 5 and 10 grains per stigma 
and 1 (7%) had >10 grains per stigma. | 
The proportion of tagged pistillate flowers set- 
ting seed varied considerably among species: 
Dalechampia heteromorpha had 100% seedset 
(N = 30) at km 13 Pipeline Road; at this site D. 
scandens had 76% seedset (N = 87). At km 15 
Pipeline Road, Dalechampia tiliifolia had 100% | 
seedset (N = 48), е D. dioscoreifolia had 
only 42% seedset (N = 24). 


POLLINATOR MOVEMENTS BETWEEN SPECIES 


А ће study site by km 13 Pipeline Road, D. 


"ега. 
together ап” 


were pollinated vius the same bee species (Table | 


ae ee oat Ie кали“ са t аи г o 


1984] 


5). In the morning hours Hypanthidi d Tri- 
gona visited and pollinated D. heteromorpha (Fig. 
5). On a number of occasions bees that had just 
visited D. heteromorpha attempted to visit in- 
florescences of D. scandens, however, the bracts 
of the latter were closed in the morning and suc- 
cessful foraging from, and pollination of, this 
species was usually not possible before 1300 hrs. 
Thus there was little potential for interspecific 
pollen flow in the morning hours. 

The majority of attempted visits by Hypan- 
thidium and Trigona during the morning hours 
were to D. heteromorpha. Out of 599 recorded 
inflorescence visits during the period from 0800 
to 1300 hrs, 535 (89.3%) were successful visits 
to D. heteromorpha, 39 (6.5%) were attempted 
visits to inflorescences of D. scandens that were 
closed, 13 (2.2%) were visits to old inflorescences 
of D. scandens that had ceased bract movement 
(and lacked pollen and resin resources), and 12 
(2%) were to the rare inflorescences of D. scan- 
dens that were receptive and slightly open. 

In the afternoon (after 1330 hrs) when the in- 
florescences of D. scandens were open, the pol- 
linating bee species “switched” from foraging 
primarily from D. heteromorpha to foraging pri- 
marily from D. scandens. Of 483 recorded inflo- 
rescence visits during the period from 1330 to 
1700 hrs, 429 (88.8%) were to D. scandens and 
only 54 (11.2%) were to D. heteromorpha. That 
the bees “preferred” D. heteromorpha in the 
morning and D. scandens in the afternoon is sta- 
ена highly significant (Р < 0.001, x? = 

4). 


As a consequence of this daily shift in bee 
preference, the number of interspecific moves by 
Pollinators was surprisingly low. Dalechampia 
heteromorpha and D. scandens grew together in 
the same hedgerow at the km 13 study site; they 
were frequently intertwined. The inflorescences 
were of approximately equal number (Table 6) 
and not spatially segregated to any great extent. 
Yet out of 576 recorded pollinator moves, only 
32 (5.5%) were interspecific (Table 6). 

Observations of the movement of paint gran- 
ules that had been dusted on staminate flowers 
of both species of Dalechampia also suggest a 
low level of interspecific pollen flow. The fre- 
quency was somewhat higher than noted above; 
3 (11.6%) of 43 paint transfers were interspecific. 
(However, the sample size is small and 11.6% is 
Dot significantly different from 5.5% (binomial 
Probability, 8 (5; 43, 0.055) = 0.06).] The aver- 
зве distance of paint transfer was 1.45 m (N = 


ARMBRUSTER & HERZIG— DALECHAMPIA 


w 
o o 
T 1 
лш 
QU 


ч 
{ 
: 


I 
D heteromorpha | 
Д 

Д 

I 

I 

! 

I 


pant” ачай 


Visitation by Pollinators 
о 
T 


(mean number inflorescence-visits per y, hr) 


\ 
\ 
A 
\ 


o 
T 
- 
Lia 
І 
> 


1 
ارو 4 


o 
f 


1 d Ve n J 
1500 1600 1700 


Qd н uo ЕРА О o РАИ АЛА 
0900 1000 поо 1200 1300 1400 
Time of Day (hr) 


FIGURE 5. Rates of effective visitation by pollina- 


D. scandens at 
13 Pipeline Road, Canal Zone, Panama, 13-26 
January, 1980. Bars are + one standard deviation. 


24) with a large standard deviation (1.87) and a 
range of 0.025 m to 7.62 m. Of 27 observed 
paint transfers in which both the source and des- 
tination were known, carry-over of paint (here 
defined as transfer of paint to inflorescences vis- 
ited subsequent to the bee’s first stop after vis- 
iting the source) was observed only twice (=7.4%). 
Presumably pollen carry-over is correspondingly 
low (cf. Waser & Price, 1982). 

At the study site at km 15 Pipeline Road, D. 
tiliifolia and D. dioscoreifolia occurred near one 
another and were pollinated by the same bee 
species and individuals. Despite the fact that these 
two species of Dalechampia differ in bract color 
and morphology and in resin color (D. tiliifolia: 
white bracts, yellow resin; D. dioscoreifolia: pink 
bracts, maroon resin), on many occasions we ob- 
served individual Eulaema cingulata visit both 
species “indiscriminately” and to have mixed 
corbicular loads of yellow and maroon resin. The 
two plant species were highly segregated. An av- 
erage of 82 open inflorescences of D. tiliifolia 
were present in an open grassy area, whereas an 
average often open inflorescences of D. dioscore- 
ifolia were present at the edge of the forest. Thus 
even indiscriminate foraging on the part of the 
bees would result in fewer interspecific moves 
than would be expected were the plants evenly 
distributed. Out of 670 recorded moves between 
inflorescences, 23 (3.496) were interspecific 
moves. This is considerably less than would be 
expected were the plants not spatially segregated 
(Table 7). d 

The small proportion of interspecific pollina- 
tor moves belies the significance of its effect on 


10 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


TABLE 6. Observed movements of pollinators between ca. 20 inflorescences of — наи heteromorpha 


and ca. 20 inflorescences of D. scandens, 13-26 Jan. 1980, Canal Zone, Panama. E 


pected values are calculated 


using 2 x 2 contingency — no pollinator constancy or spatial segregation of стат Observed differs from 
445.9). 


expected at P < 0.001 (x? = 


Hypan- Total Observed Total Expected 
By Trigona АУ е Pollinator Pollinator 
spp. panamense Movements (%) Movements 
Intraspecific movements: 
D. heteromorpha 276 58 334 (58.0%) 213 
Intraspecific movements: 
scande: 204 6 210 (36.5%) 89 
Inte ific movements: From 
D. heteromorpha to D. scandens 13 2 15 (2.6%) 136 
Interspecific movements: From 
. scandens to D. heteromorpha 13 4 17 (2.9%) 138 


D. dioscoreifolia. A comparison of the number 
of pollinator moves from inflorescences of D. 
tiliifolia to inflorescences of D. dioscoreifolia with 
the nu intraspecific moves among D 
сеа oan (Table 7), indicates 
that nearly one-third of the visits to D. dioscorei- 
por че E. cingulata are likely to have resulted 
in the deposition of pollen of D. tiliifolia on the 
stigmas of D. dioscoreifolia. The pollen grains of 
D. tiliifolia are much larger than those of D. dios- 
coreifolia. Stigmas of these two species were ex- 
mined with a hand lens and pollen grains were 
identified and оте АП the stigmas aded 
en 
visited by a bee coming from D. tili. ifolia ы 
8) bore large amounts of pollen of D. tiliifolia. 
In two observations of the reverse interspecific 
move there was no transfer of D. dioscoreifolia 
pollen to the stigmas of D. tiliifolia 
The D. dioscoreifolia at this locality was thus 
subject to a substantial influx of pollen from D. 
tiliifolia. Of 15 stigmas of D. dioscoreifolia ex- 


able 7) and was visited at a 
higher rate (Table 5). Of 51 stigmas of D. tiliifolia 
examined on 22 January 1980, 42 (8296) bore D. 

јава ~~. and 9 (18%) bore none; no stig- 

D. dioscoreifolia pollen. Thus, at least 
as in! to D. tiliifolia, D. dioscoreifolia 
showed substantial stigmatic contamination by 
heterospecific pollen and relatively low levels of 
conspecific pollination. However, part of the lat- 
ter difference between the two species may be 


attributed to the fact that D. tiliifolia self-polli- 
nates fairly readily and D. dioscoreifolia does not. 


HYBRIDIZATION AND INTERSPECIFIC CROSSES 


Despite extensive searches in numerous lo- 
cations in Central and South America, we have 
never found any evidence of natural hybridiza- 
tion pean: species of doit Experi- 
mental g ve been performed 
between. D. scandens and D. sli. Out 
of 45 crosses made with D. scandens as the pis- 
tillate parent, only two produced seed. When these 


found that neither the F,s nor F,s were distin- 
guishable from the pistillate parent; apparently 
these were the result of pollen contamination 
from the pistillate parent. 

e reverse cross (D. heteromorpha as the 
pistillate parent), of 51 crosses only three pro- 
duced seed. These again appeared to be the result 

of contamination by pollen from the pistillate 
arent. 

А has not been possible to make the combi- 

uic two species 

in this study. However, unsuccessful crosses made 

Syse four additional NM | American species 


ана barriers are common among sympatric 


о been performed to 
measure how contamination (“clogging”) of stig- 
mas with heterospecific pollen affects seedset. In 
one experiment using D. scandens as the pistil- 
late parent, stigmas were pollinated with the pol- 
len of D. heteromorpha; two days later they were 
manually self-pollinated. Other stigmas were 


1984] ARMBRUSTER & HERZIG— DALECHAMPIA 11 


TABLE 7. Observed movement of ва between ап average of 82 inflorescences of Dalechampia 
tiliifolia and an average of 9.6 i 20-27 Jan. 1980, Canal Zone, Panama. Expecte 


values are calculated using 2 х 2 contingency assuming no pollinator constancy or spatial segregation of plants. 
4.6) 


Observed differs from expected at P < 0.001 (x? = 31 


Total Observed Total Expected 
By Eulaema By Eu- Pollinator Pollinator 
cingulata glossa sp. Movements (%) Movements 

Intraspecific movements: 

D. tiliifolia 617 1 618 (92.2%) 591 
Intraspecific movements: 

D. dioscoreifolia 27 2 29 (4.3%) 2 
Interspecific m ents: 

D. tiliifolia to D. crei 13 0 13 (1.9%) 40 
Interspecific movemen 

D. dioscoreifolia to D. vilifolia 10 0 10 (1.5%) 37 


pollinated with a mixture of roughly Е ч 
of Р. scandens and D. heteromorpha р 

а control, stigmas were manually inert 
The results (Table 8) indicate significant depres- 
sion of seedset (relative to the control) by het- 
erospecific pollination prior to self-pollination 
(P < 0.0 001). Pollination with the two-species 
pollen mixt tly more seeds 
than heterospecific pollination followed by self- 
pollination (P < 0.05). Pollination with the mix- 
ture produced fewer seeds than the control treat- 
ment, but the difference was not significant (P = 
0.076). 


In a similar experiment on D. heteromorpha, 
the stigmas were pollinated with heterospecific 
pollen followed by manual self-pollination two 
days later. The source of heterospecific pollen 


was D. magnistipulata Webster & Armbruster, 
a relative of D. scandens in sect. Scandentes. The 
control treatment was manual self-pollination. 
The experimental treatment again resulted in 
depression of seedset relative to the control (P < 
0.01, Table 8 


DISCUSSION AND CONCLUSIONS 
FLORAL CONSTANCY AND FORAGING STRATEGIES 


There is considerable literature indicating that 
flower constancy is common or even the rule 
among wild bees (Chambers, 1946; Grant, 1950; 
Manning, 1956; Sprague, 1962; Free, 1966; 
Proctor & Yeo, 1972). These authors have sug- 
gested that individual bees that learn how to ma- 
nipulate a flower species will forage most effi- 


TABLE 8. Effect of heterospecific pollination on seed production. Numbers in rows 1 and 2 indicate the 
number of inflorescences in each class. Column 1 differs significantly from column 2 at Р < 0.05, column 1 
from 3 at P < 0. 001, column 4 from 5 at P < 0.01; columns 2 and 3 are not significantly different, P = 0.076; 


х? analysis. 
ыыы 


D. heteromorpha (9) х 


Р. scandens (2) х по 
D. heteromorpha (8) D. magnistipulata (8) 
Het - Heterospe- 
cific pede ври cific pollina- 
tion followed Pollination Se Е. tion followed Self- 
by self-pol- with mixture pollination by self-pol- pollination 
lination of two pollens (Control) lination (Contro!) 
0-4 seeds produced 
per inflorescence 26 11 8 8 10 
5—9 рг 
Per inflorescence 9 15 34 2 30 
Mean number seeds 
per inflorescence 1.97 3.95 6.93 4.6 8.0 


a ЕО 


12 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


ciently if they restrict their activities to that 
species, at least as long as it is abundant. Some 
authors, however, have argued that the foraging 
strategies of polylectic bees are not adequately 
described by the concept of simple temporary 
constancy, but that many bees are inconstant, 
атара constant, or have “majors” and 
“minors” (e.g., Hobbs, 1962; Macior, 1966; 
Mosauin, 1971; Heinrich, 1975, 19766). | 
Тће 


эс 


оер 
1 z 1 + Pad. 35. >> ofa 


D. dioscoreifolia without apparent “‘regar 
species; yet these bees could surely distinguish 
between these markedly dissimilar Dalechampia 
species. Similarly, we observed individual Hy- 
panthidium and Trigona on inen Occasions 
visit D. scandens and D. heteromorpha indis- 
criminately, moving to nearest neighbors as en- 
countered on their foraging routes. 

Yet bees did distinguish between species of 
Dalechampia under certain conditions. Trigona 
and perhaps Hypanthidium appeared to distin- 
guish between D. scandens and D. heteromorpha 
when there were differences in the available re- 
sources. When inflorescences of D. scandens were 
closed in the morning and pollen and resin re- 
sources were нін и to foraging bees, Tri- 
gona and Hypanthidium foraged from D. het- 
eromorpha on 89.3% of the inflorescence visits 
(N = 599). In the afternoon when the pollen and 
resin resources were depleted in D. heteromor- 
pha, these same bee species foraged “‘preferen- 
tially” from D. scandens, visiting this species on 
88.8% of all inflorescence visits (N = 483). 

Similar observations were made by Armbrus- 
ter and Webster (1982) on the behavior of Hy- 
panthidium nr. melanopterum foraging on Dale- 
champia scandens and D. affinis Muell.-Arg. in 
Brazil. In this community D. scandens opened 
in ба morning and D. affinis пн іп the after- 


sited only 
D places of 19 visits observed ics to 1400 


were depleted, the same individual bees **pref- 
erentially" visited D. affinis; after 1430 hrs 21 
(8496) of 25 observed visits were to D. affinis 
even though inflorescences of D. scandens were 
still open (cf. Fig. 2 in Armbruster & Webster, 
1982). 


When there are differences in the resource 
available, te ic bees, as well, forage pref- 
erenti 


that euglossine bees (of medium to large size) 
collect resin preferentially from Dalechampia 


ster, 1981, 1982). This behavior was exhibited _ 


during this study as well 

Thus it appears that at least some species of 
the diverse genera Eulaema, Euglossa, and Hy- 
panthidium employ a "strategy" of facultative 
constancy which “maximizes” resource harvest. 
They do not discriminate between similar flower 
species when there is no advantage in doing so. 
bees do discriminate between 


sources available. Zimmerman (1981) has sug- 
gested that bumblebees employ this same strat- 
egy, and Simpson and Neff (1981) have drawn 
ме о conclusions from their studies of Centris 
foraging oils in Texas. This pattern may also hold 
for individual Trigona (a social species); how- 
ever, because of the possibility of sequential for- 
ng on different Dalechampia species by dif- 
ferent workers from the same hive, many more 
marked individuals need to be observed. 


ER 


REPRODUCTIVE INTERACTIONS BETWEEN 
PLANT SPECIES 


Recently there has been considerable interest 
in the nature of reproductive interactions be- 
tween sympatric plant species (Waser, 1983). 
ne certain conditions, co-occurring plant 
species may mutualistically facilitate each oth- 
er’s е (Масіог, 1971; Brown & Ko- 
dric-Brown, 1979; Waser & Real, 1979; 
Schemske, 1981). Perhaps more common, how- 
ever, is reproductive interference between со- 

ies. Reproductive interference is 


enough to effect full pollination af. all flowers of _ 


both species (Levin, 1970; Levin & Anderson, 
1970; rosas 1971). Ifa pollinator is constant 
and prefers one species over another, the second 
species will suffer from lower rates of pollination 
as a consequence of its sympatry with the first 
species. Even if a pollinator does not “prefer” 
one flower species over another, both species may 


m one species of Dalechampia over 
another. It has been pointed out several times _ 


па. oS ee ee i ЛҮ УТУЛ ES а ate me 


; 


{ 


1984] 


have lower rates of effective pollination as a ге- 
sult of the large number of wasted interspecific 
pollinator moves. This has especially dire con- 
sequences on the numerically minor species 
(Levin & Anderson, 1970; cf. Lewis, 1961). 
Another detrimental effect may accrue from 
ficiently abundant to adequately pollinate all 
flowers of both species. If shared pollinators re- 
sults in interspecific pollen flow, the reproductive 
fitness of sympatric plants may be depressed in 
several ways. If the species are cross-compatible 
but produce sterile hybrids, reproductive fitness 
is lowered and severe selection operates against 
individuals sharing pollinators (Lewis, 1961; 
Grant, 1966). Interspecific pollination also rep- 
resents a major loss of genomic copies (pollen); 
any plant that is effective in getting its pollen to 
conspecific stigmas will be at a substantial selec- 
tive advantage (Charnov, 1979). We have pre- 
sented evidence of a third consequence of inter- 
specific pollen flow: seedset is depressed by the 
presence of heterospecific pollen on stigmas, even 
if there is adequate conspecific pollination (also 
cf. Waser, 1978a, 1978b; Sukada & Jayachandra 
1980; Thomson et al., 1981). One or several of 
these processes presumably generates selective 
pressures that may lead to partitioning of polli- 
nator resources by coexisting plant species, and 
thereby reduction of competition for pollinator 
ا‎ and/or reduction of interspecific pollen 
ow 


~ 


Several of these selective pressures may ђе op- 
erating in assemblages of Dalechampia species. 
We have shown that one consequence of polli- 
nator sharing by D. tiliifolia and D. dioscoreifolia 
Is substantial interspecific pollen flow, and that 
interspecific pollen flow between D. scandens and 
D. heteromorpha can reduce the number of seeds 
Produced by members of both species. It thus 
Seems likely that populations of sympatric species 
will have adapted to coexistence with their con- 
eners, at least if their ranges overlap substan- 
ually and they have co-occurred for a sufficiently 
long. Period of time. Previous studies of two- 
Species assemblages of Dalechampia supported 
this expectation (Armbruster & Webster, 1979, 
1981, 1982). In the present study we found that 
most of the coexisting species partition pollina- 
lors in ways that result in low levels of interspe- 
Cific Pollen flow. At km 13 Pipeline Road, D. 
concen eifolia was the only species that produced 
i quantities of resin and had relatively large 

nterfloral distances; it alone was pollinated by 


ARMBRUSTER & HERZIG—DALECHAMPIA 13 


euglossine bees. Dalechampia heteromorpha and 
D. scandens, with smaller resin glands and small- 

interfl 1 dist were not visited by euglos- 
sines, but instead were pollinated by small me- 
gachilid and meliponine bees. Although these two 
species were visited by the same bee species and 
individuals, the levels of interspecific bee move- 
ment, and presumably pollen flow, were rela- 
tively low; D. heteromorpha was pollinated pri- 
marily in the morning, D. scandens in the 
fternoon. 

Dalechampia tiliifolia and D. heteromorpha 
occurred together at several sites. These species 
utilized different pollinators as well; D. tiliifolia 
was pollinated by euglossine bees, D. hetero- 
morpha, again, by megachilid and meliponine 
bees. We did not observe D. tiliifolia and D. 
scandens growing together in Panama. It is pos- 
sible that they do occasionally occur together; if 
so, they probably do not share pollinators. 

At km 15 Pipeline Road, we observed D. tili- 
ifolia and D. dioscoreifolia growing together. Both 
species have large resin glands and relatively large 
interfloral distances; they are both pollinated by 
species of euglossine bees. The most frequent 
pollinator of these two species at this site, Eu- 
laema cingulata, moved between the two species 
with sufficient frequency to effect considerable 
interspecific pollination. 

Dalechampia dioscoreifolia was less abundant 
than D. tiliifolia at this site (with averages of ten 
and 82 inflorescences, respectively). As a con- 
sequence it was subject to substantial pollen flow 
from D. tiliifolia and must have lost much pollen 
to foreign stigmas. The effects of interspecific 
pollination on D. tiliifolia were diluted among a 
larger number of inflorescences and were prob- 
ably of minor significance. 

This relationship may have detrimentally af- 
fected the reproductive output of individuals of 
D. dioscoreifolia at this site. With respect to the 
male component of fitness, probably over 25% 
of the pollen was lost to heterospecific stigmas 


e 


ccinn 


14 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


may be more sensitive to stigma contamination 
and/or stylar “clogging” than D. dioscoreifolia. 
Only a small proportion of the stigmas of D. 
dioscoreifolia at km 15 bore significant amounts 
of conspecific pollen (e.g., 20% on 25 Jan. 1980). 
stigmas lacking conspecific pollen were 
either devoid of pollen (53%, 25 Jan. 1980) or 
5 ге pollen of р. tiliifolia (27%, 25. Jan. нан 


аз 
in short s supply; in view of t the rarity of bei ol. 
lination in D. dioscoreifolia, reduced pollinator 
service probably resulted in reduced seed pro- 
duction 
ere is some evidence that D. dioscoreifolia 
suffered from lower rates of effective pollination 
as a result of its proximity to D. tiliifolia. Nearly 
one-third of the pollinator visits to D. dioscorei- 
folia were “wasted,” bringing loads of D. tiliifolia 
pollen. When we factor the “wasted” visits out 
of the visitation rates, we find that D. dioscor- 
eifolia at km 15 Pipeline Road had significantly 
lower rates of effective visitation than did D. 
dioscoreifolia at km 13 P ne Road. During 
three hours of bli us ig on siis of two days 
when the number of open inflorescences were the 
same in the two populations, we observed 19 
visits by Eulaema cingulata and 24 visits by E. 


of effective visitation to D. dioscoreifolia, even 
by E. cingulata alone, was significantly lower at 
km 15 than at km 13 (7 < 19, P< 0.015, as- 
suming Poisson distribution, Pearson & Hartley, 
1958). 

Additional evidence suggests that D. dioscorei- 
folia was at a competitive disadvantage relative 
to D. tiliifolia at the Pipeline Road study site, 
and that this contributed to lower rates of pol- 
linator visitation. If bees visit these two species 


tial distribution of the two species, w we оин 


inflorescences of each species. The frequency of 
visits to D. tiliifolia, then, should have been 0.895 
(its average floral frequency) and the frequency 
of visits to D. dioscoreifolia should have been 
0.105. The observed frequencies of visits were 
0.937 and 0.063 respectively, which are signifi- 
cantly — from the expected at P < 0.001 
(N = 670; normal approximation of binomial 
distributiónd Bailey, 1959). Thus the rate of vis- 
itation to D. dioscoreifolia is significantly lower 


[Vor. 71 


than expected; apparently the bees either havea — 
weak “preference” for D. tiliifolia or they are 
foraging in a manner that causes them to en- 
counter D. tiliifolia more frequently. 

e expected consequence of sharing polli- 
nators with D. tiliifolia is reduced seedset in D. 
dioscoreifolia. Seedset is much lower in the po 
ulation of D. dioscoreifolia at km 15 Pipeline 
Road than is the seedset for other species. How- 
ever, the truly critical -— are lacking. We have 
only subjective comparisons between popula- 
tions of D. енед» the population of D. 
dioscoreifolia at ipeline Road appeared 
to produce less fruit than did the populations of 
similar size we observed at km 13 Pipeline Road, 
and on Barro Colorado Island, where D. tiliifolia 
was absent 

A puzzling question emerges from this study. 
There appears to be ample evidence of selective 
disadvantage to individual plants sharing polli- 
nators and exchanging pollen with members of _ 
other species. Most species of Dalechampia con- 
sidered in this study appear to be adapted (or 
preadapted) to coexisting with each other. Dale- 
champia tiliifolia and D. dioscoreifolia, however, 
share pollinators, exchange pollen, and do not 
appear to be adapted to coexistence. 

The adaptive explanation of pollinator sharing 
leading to higher rates of pollination for rela- 
tively rare or few-flowered species (Schemske, 
10911 4 a Xs 3. Ww 1 1 +h 


species of Dalechampia are fairly common and 
produce relatively large numbers of flowers; also 
D. dioscoreifolia appears to have suffered re- 
duced rates of effective pollination and possibly | 
lower reproductive output as a consequence of 

its proximity to D. tiliifolia. Instead, the expla- | 
nation may be that these two species are not 
adapted to coexistence because they rarely occur 
together. We have observed D. tiliifolia at 14 
sites and D. dioscoreifolia at nine sites in Central 
and South America (Armbruster, unpubl.), but 
only at the Pipeline Road site were the two species 
growing together. The two species usually occur 
in different habitats; in Panama D. dioscoreifolia 
occurs predominately in forest, and D. иа 
occurs predominately in open scrub (Table 1). 
Thus the distribution of these two species is set 


patry with D. tiliifolia. Local adaptation would 


i EE RE IE: 


1984] 


be possible only if gene flow were very localized, 
which seems unlikely in this species (cf. Janzen, 
1971). 


RESOURCE PARTITIONING AND 
COMMUNITY STRUCTURE 


The four species of Dalechampia we observed 
in Panama may be an important part of this 
tropical forest ecosystem. While the flowers pro- 
vide resin resources for only four genera of bees, 
to be important pollinators of many other trop- 
ical plants (cf. Gilbert, 1980). Female euglossine 
bees visit a large variety of plants for nectar and 
pollen resources, while the males visit and pol- 
linate dozens of species of orchids (Ackerman, 
1984; Dressler, 1982). Similarly, Trigona and 
Hypanthidium visit numerous other plant species 
for pollen and nectar. We observed both Trigona 
and Hypanthidium visiting a number of weedy 
roadside species in our study areas. 

Most of the literature addressing pollination 
at the community level concludes that plant 
species that coexist in stable communities oc- 
сиру different “pollination niches” (Levin, 1970; 
Levin & Anderson, 1970; Mosquin, 1971; Fran- 
kie, 1975; Heinrich, 1975, 1976; Reader, 1975; 
Stiles, 1975, 1977; Feinsinger, 1978; Waser, 
1978). However, some auth ggest that niche 
separation is not the only expected outcome of 
ecological processes (Brown & Kodric-Brown, 
1979; Grant & Grant, 1968; Proctor & Yeo, 1972; 
Macior, 1971; Schemske, 1981), and others ar- 
gue that observing niche separation in a single 
community does not demonstrate that any eco- 
logical or evolutionary processes have occurred 
(Connor & Simberloff, 1979; Strong et al., 1979; 
Poole & Rathcke, 1979; Waser, 1983). 

Most of the species of Dalechampia that occur 
‘ogether at our study sites in Panama are either 
pollinated by different bees or are pollinated at 
different times of the day. This is consistent with 
theoretical expectations. The only exception, 
pollinator sharing between D. dioscoreifolia and 
D. tiliifolia, may be a case of two species lack- 
‘ng adaptation for sympatry because they rarely 
occur together; when they do occur sympatrically 
!t may impact only a small portion of each pop- 
ulation. If 50, this is compatible with the re- 
n pertitioning theory as well. Before we can 
Rede claims of community organization, 
ой r, it will be necessary to collect more data 
E relative frequency of co-occurrence of 

Pecies, pollen-flow dynamics, reproductive con- 


ARMBRUSTER & HERZIG—DALECHAMPIA 15 


sequences of interspecific pollination, and com- 
parative reproductive performance of popula- 
tions of each species as they occur with and 
without sympatric congeners. Especially useful 
would be establishment of experimental popu- 
lations of D. tiliifolia and D. dioscoreifolia in 
varying ratios, to determine the effects of sym- 
patry on pollination rates and reproductive per- 
formance. 
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ACKERMAN, J. D. 1984. Phenological relationships of 
male Euglossini (Hymenoptera, Apidae) and their 
nectar and fragrance hosts. In W. D’Arcy (editor), 
Botany and Natural History of Panama. Ann Mis- 
souri Bot. Gard. (in press). 
ARMBRUSTER, W. S. 1982. Seed production and dis- 
persal in Dalec/ (Euphorbiaceae): divergent 


= 


ical ] Amer J. Bot 


69: 1429-1440. 
. L. WEBSTER. 1979. Pollination of two 
species of Dalechampia (Euphorbiaceae) in Mex- 
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& i . Sistemas de polinização de 
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zonica 11: 13-17. 


1982. Divergent pollination sys- 

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Dalechampia (Euphorbiaceae). Amer. Midl. Nat- 
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ВАЦЕУ, N. T.J. 1959. Statistical Methods in Biology. 
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Brown, J. H. & A. Kopric-Brown. 1979, Conver- 
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Ecology 60: 1022-1035. 

CHAMBERS, V. Н. 1946. An examination of the pollen 
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CHARNOV, E. L. 1979. Simultaneous hermaphrodit- 
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Connor, E. Е. & D. 51МВЕКТОРЕ. 1979. The assembly 
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Croat, T. B. 1978. Flora of Barro Colorado Island. 
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DRESSLER, R. L. 1979. Eulaema bombiformis, E. 

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—— 
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16 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


GILBERT, L. E. 1980. Food web organization and the 
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olutionary Ecology Perspective. Si- 
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ee а eem 


POLLINATION BIOLOGY AND THE BREEDING SYSTEM ОЕ 
ACACIA RETINODES (LEGUMINOSAE: MIMOSOIDEAE)! 


P. BERNHARDT, J. KENRICK, AND К. B. KNox? 


ABSTRACT 


Coastal populations of Acacia retinodes Schldl. var. uncifolia J. M. Black are protogynous and 
highly self-incompatible. Flowers are nectarless but insects appear to be attracted to the inflorescences 
both by the yellow floral color and distinctive fragrance. Neutral red tests suggest that the scent 
originates from the stigma and epidermal cells of the anthers. Floral foragers represented three insect 
orders but interpretations of field observations and pollen load analysis of insects indicate that solit 
bees in the Colletidae and Halictidae are the major pollen vectors. The method for removal of pollen 
from the anthers is via thoracic vibration. Because female phase flowers offer no pollen, foraging by 
bees on such flowers is interpreted as a trend towards partial pollination by deceit. 


In Australia, the large number of Acacia species 
(ca. 900, Pedley, 1978, 1979), suggest that this 
country is a center of speciation and evolution; 
taken together with the fact that Acacia repre- 
sents the largest genus of angiosperms, we might 
expect its reproductive biology to be well known. 
Regrettably, this is not the case. Research into 
the mechanisms of pollination and seed-setting 
of Australian species of Acacia has been spas- 
modic and fragmentary. Variation in the number 
of grains per polyad was documented by Mueller 
(1887-1888), but it was not until the 1930s that 
the first cytological studies of pollen germination 
and Pistil interactions were carried out, based 
Primarily on 4. baileyana F. Muell. (Newman, 
Loe 1934b). Later, with the advent of 

n microscopy, the structural relationships 
and taxonomic significance of the polyad was 
established for many species (Guinet & Lugar- 
don, 1976; Guinet, 1981). 

Pioneering Studies of the breeding system of 
је ста species of Acacia were carried out 
id uth African Wattle Research Institute. 
7 H tea Sherry (1946, 1949) established that 
di дыы апа A. mearnsii ате only partially 
Е: mpatible, and are largely outbreeding. The 
Re ors that assure effective pollination have not 
Nis fined, although several brief reports 
vals n published suggesting that bees are in- 

(Armstrong, 1979), or birds in some 


о ЕИ 


species (Ford & Forde, 1976). Vogel (1978) con- 
siders that Acacia is melittophilous. 

The question arises whether research into the 
pollination biology of other mimosoids is further 
advanced. Arroyo (1981) noted that the basic 
unit of reproduction in the Mimosoideae is the 
inflorescence not the individual flower, because 
the flowers tend to be tiny, numerous, and dense- 
ly massed. Furthermore, floral sexuality, within 
a single inflorescence, may intergrade subtly from 
functionally 1 phroditic through the various 
forms of decliny (Lewis & Elias, 1981). There- 
fore, the basic floral morphology of the Mimo- 
soideae offers several obstacles in attempts to 
interpret pollinator-flower interactions and 
breeding systems. Modification of the size, floral 
attractants, and sexuality of the flowers, com- 
posing the mimosoid inflorescence, has permit- 
ted the exploitation of all animal groups com- 
monly associated with the major trends in pollen 
dispersal. This includes bees e.g., in Prosopis 
(Simpson et al., 1977) and Mesoamerican Acacia 
(Janzen, 1974); bats e.g., in Parkia (Baker & Har- 
ris, 1957; Hopkins, 1981); birds e.g., in Callian- 
dra (Arroyo, 1981) and Inga (Koptur, 1983); and 
marsupials e.g., in Inga and Acacia (Turner, 
1983). Zoophilous syndromes intergrade in the 
Mimosoideae. Generalist entomophily occurs in 
Acacia macracantha Humb. & Bonpl. ex Willd. 
(Zapata & Arroyo, 1978) while some Inga spp. 
are pollinated by hummingbirds and Lepidop- 


1 
Research funded by Australian Research Grants Scheme and Australian Department of Education (СРРЕК); 


we Mr. A 
NaYtn- Greene, Mrs. G. Beresford, M 


ANN, Misso 
URI Bor. Garp. 71: 17-29. 1984. 


: , Mrs. R. 
ational pee of Vitoria for the identificatio 
? Plan “a unknown reviewer for helpful comm 

t 
Cell Biology Research Centre, School of Botan 


А. Heisler and rangers of the National Parks Service, Victoria and Mr. C. Campbell for cooperation; 

arginson, and alker 

n of Hymenoptera; Ms. 

ent 
y, 


Mrs. B. Wright for assistance; Dr. K. 
J. Gilbert for skilled secretarial 


s. 
University of Melbourne, Parkville, Victoria 3052. 


18 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


tera (Koptur, 1983). Reliable information per- 
taining to the есте systems remains frag- 

mentary and inconclusive. Neptunia and Parkia 
are probably self-compati tible (Windler, 1966; 
Baker & Harri 7), while self-incompatibility 
has been vies d shown to occur in a few 
neotropical Acacia species (Janzen, 1974; Zapata 
& Arroyo, 1978). 

There is therefore an urgent need to explore 
the reproductive biology of Australian species of 
Acacia. At Melbourne, we have initiated a long- 

the role of the polyad 

in seproduction, using a multi-disciplinary we 
ach. We have established that variation 

polyad grain HUE (4-16 i in different species) 


Ao Ла КЛИКНИ 


in tl 1C OValy (Ken- 


rick & Клек. 1982). However, the polyad grain 


in mimosoids with free pollen grains (Cruden, 
1977). This suggests that the polyad of Acacia 
has a considerable selective advantage, and is a 
highly efficient reproductive unit. The com- 
pound grains also make for efficient use of avail- 
able pollinators. 

In the present paper, we have investigated the 
nature of the jab Pe in a summer-flow- 
ering species of Acacia, A. retinodes, and ex- 
plored its pollinator relationships. We have рге- 
that this species is  self-incompatible (Knox & 
Kenrick, 1983). We now confirm this finding, 
and relate our results to work on other Mimo- 
soideae. 


MATERIALS AND METHODS 


Acacia retinodes Schldl. var. uncifolia J. M. 
Black is restricted to coastal sites in South-east- 
ern Australia where it is locally abundant on cal- 
careous sands and is commonly called the Wir- 
rilda. Henceforth, in this paper, it is referred to 
as A. retinodes. This study was conducted in an 
area towards the eastern end of its distribution 


second about 2.5 km away at the Cape Country 
Club. Both sites are naturally occurring popu- 
lations 


Breeding system analysis. The peak of flow- 
ering of Acacia retinodes in the populations at 
Cape Schanck is from early December until late 


Tal 


, occasional trees may be found _ 


sparsely Зале at any time of the year. Thirty 
trees were tested in this study, and each was la- 
1 g. Immature flowering 


pollination when the majority of buds were ap- 
proaching the yellow bud stage (Newman, 1933). 

pen flowers and phyllodes were removed. The · 
shoots were enclosed in cellulose acetate bags. 
These were 180 mm by 115 mm in size with 30 
mm gussets on either side, and were tied on with 
plastic covered wire ties. These bags are perme- 
able to air and water molecules, and provide suit- 
able protection from pollinators. 

r three days later, the shoots were un- 
covered either for pollen collection, or for pol- 
lination. For manipulated pollinations, e 

flowers and unopened 
buds following the method of Philp and Sherry 
(1946, 1949). The aim was to pollinate when the 
maximum number of inflorescences were at the 
female phase (see Results, Floral Behavior and 
Dichogamy) with anthers still folded but styles 
extended. 

For each series of crosses, all bagging was done 
at the same time and five replicate bagged flow- 
ering shoots were employed for each type of cross. 
Several types of pollination were undertaken: 


1. Control, pollinators excluded. Because of the 
small size of the inflorescences, it is quite im- 
practical to emasculate the flowers to prevent 
accidental self-pollination. Accordingly, to 
determine whether mechanical autogamy oc- 
curred in the absence of pollinators, five sam- 
ples of flowering shoots on each tree remained 
bagged during the зи of the flowers, 1.е., а 
total of ten to 12 da 

2. Manipulated ил. When the ma- 
jority of inflorescences in a bag reached early 
anthesis (see Results for description), the bag 
was taken off and fully open male phase flow- 
ers and unopened buds removed before the 
inflorescences were self-pollinated. Pollen was 
applied to the stigmas from the inner surface 
of 2 ml specimen vials, made of polyvinyl 
chloride, which had been coated with pollen 
= pressing fully open flowers against the in- 

е of the vial, to retain only the polyads. 
The shoots were bagged until the flowers were 
senescent. 

3. Manipulated cross-pollination. These were 
carried out as described for self-pollinations, 


1984] 


TABLE 1. Variation in number of floral organs in two populations of Acacia retinodes at 
Victoria. Explanation of abbreviations: Х, mean; s.d., standard deviation; N, number in sample 


BERNHARDT ET AL.—POLLINATION AND BREEDING OF ACACIA 


19 


Cape Schanck, 


Population 1 


Population 2 


Tree Overall 
Number: 1 3 5 6 20 23 31 34 Data 
A. Number of Flowers/Inflorescence 
x 22:2 20.2 23.6 21.6 23.0 23.0 30.8 24.2 23.9 
s.d. 2.05 0.84 3.44 0.89 1-73 2.86 2.28 2.68 3.73 
N 5 5 5 5 5 5 5 40 (total) 
B. Number of Anthers/Flower 
X 52.9 56.8 59.2 8.7 62.2 78.0 71.6 72.0 63.5 
s.d 4.03 11.06 7.10 6.03 5.97 8.88 6.08 6.76 10.84 
N 25 25 25 19 25 20 25 21 160 (total) 
С. Number of Ovules/Ovary 
Р 12:7 13.7 11.9 11.8 12:7 13.2 12.5 12:3 12.6 
s.d 0.82 0.67 0.74 1.03 0.95 1.14 0.53 1.16 1.05 
10 1 10 10 10 10 10 10 80 (total) 


except that the pollen was from another nom- 
inated tree. 


Pod counting. Pods were counted ten to 28 
days after pollination. The number of pods set 
per infructescence was scored. A comparison was 
made between pod set following open-pollina- 
tion and that following controlled pollination in 
one tree (number 23). 


Floral statistics. Data for number of flowers/ 
inflorescence and number of anthers/flower were 
counted in the laboratory using a high power 
binocular dissector on fresh or FAA-fixed ma- 
terial. Number of ovules/ovary was observed by 
fluorescence microscopy after ovaries, dissected 
from FAA fixed material were stained with de- 
colorized aniline blue (Linskens & Esser, 1957; 
as modified by Kenrick & Knox, 1981a). The 
number of polyads/style was scored from open- 
po llinated, FAA-fixed flowers, which were rinsed 
in distilled water and stained with Calberla's so- 
lution (Ogden et al., 1974) and observed by bright 
field microscopy. Neutral red staining for detec- 
Поп of osmophores was employed as described 
by Boyer (1963). 


Pollen vector analysis. To determine the pol- 
len vectors of Acacia retinodes, insects were se- 
lectively collected, from 15 Dec. 1981 to 12 Feb. 
1982 from 7:00 A.M. to 4:00 p.m. Collecting pe- 
nods from 1:00 p.m. to 4:00 р.м. were finally 
ы because no insect activity was recorded. 
tha а were collected on/y when they foraged on 

©wers of A. retinodes. Foraging is defined 


here as the active removal of pollen or the prob- 
ing of floral structures with insect mouthparts. 
Insects were killed together in jars containing 
ethyl acetate vapor. To determine the presence 
of pollen, insects were first observed under dis- 
secting microscopes. To analyze pollen species 
th i ts were gently pressed against glass 
slides, to dislodge grains. Samples were stained 
with Calberla’s solution and observed under light 
microscopy. Because insects had been killed in 
the same jar there was a continual danger of con- 
tamination. Therefore, pollen species were not 
recorded on a particular insect as present unless 
25 individual polyads (for A. retinodes) or 25 
separate grains (for all other species) could be 
counted in a single, stained sample. Foraging be- 
havior of insects was noted on А. retinodes and 
on co-blooming species within the study sites. 


RESULTS 


Floral morphology. The globose inflores- 
cences of A. retinodes contain 18 to 34 flowers 
(Table 1A). Inflorescences are arranged in “га- 
cemes" of five to seven inflorescences in the axil 
of a phyllode; however, at peak flowering, de- 
velopment of the phyllodes is evidently sup- 
pressed, and the apices of branches appear to be 
panicles of globose inflorescences (Fig. 1). дч 

1 1 11 4 4 РА a ап 


. 


new vegetative growth may occur even from the 
tips of the racemes. 
Each inflorescence bud develops in the axil of 


a reddish bracteole that ceases expansion at an 


20 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


Ficures 1, 2. A flowering shoot of А. retinodes var. 


uncifolia.—1. Note that there is usually more than one 
+h te . oa 32 n 11 ГА l'a! 3 ns 


2 Inflorescence in the female phase (x10). 


early stage (Jobson et al., 1985). The calyx has 
five fused, reduced red sepals and the corolla has 
five yellow petals, that are reflexed at anthesis. 
The 34 to 91 stamens in each flower (Table 1B) 
have anthers that contain eight, 16-grain polyads 
that dehisce through longitudinal slits (Kenrick 
& Kn 979). The single ovary contains ten to 
14 ovules (Table 1C). 
ong, narrow style is generally equal to or 
exceeds the length of the stamens. The terminal 
cup-shaped stigma is of the wet type (WN) in the 
classification of Heslop-Harrison (1981). The 
flowers on most trees examined were hermaph- 
rodite although in 2596 of trees, some occasional 
flowers had undeveloped pistils. No nectaries 
have been found on the floral axis around the 
ovary, as occurs in some African species (Rob- 
bertse, 1974) 
Floral behavior and dichogamy. 


tall 


Inflo- 
n 


petally and о 
synchronously within an inflorescence. The ma- 
jority of styles emerged before 8:00 A.M., and are 
at first folded in a zigzag pattern, but soon 
straighten (Kenrick & Knox, 19812). At this stage, 
the flower petals are only partially exserted and 
stamens are compressed beneath the petals. An 
inflorescence can be said to be truly protogynous 
since flowering is synchronous. At this point the 
inflorescence resembles a spiked club, and is re- 
ferred to as a female phase inflorescence (Fig. 2). 

Stamens normally do not fully extend until 
after mid-day, depending on the weather con- 
ditions. When the anther filaments are fully ex- 
tended the styles are generally hidden. This state 


заше аст opetally t 


marks the beginning of the male phase, although 
dehiscence usually does not take place until the 
following day. Rate of floral development may 
vary according to the prevailing climatic con- 
ditions: dry sunny conditions accelerating and 
cool dudy weather retarding development. 

A fruity poon. reminiscent of Пре cantaloupe 


R 


mel 
Neutral red tests for detection of osmophores, 
during this phase, stain the stigma only. How- 
ever, scent is most pronounced during the male 
phase, when the anther epidermal cells stain in- 
tensely. 


Breeding systems. The data obtained from 


controlled pollinations demonstrate that re 
tinodes is highly self-incompatible (Table 2) 
ross-pollinations wi trees resulted 


high levels of pod set, while self-pollinations gave 
few or no pods. Higher levels of pod set resulted 
from interpopulation crosses than intrapopula- 
tion crosses. 

The self-sterility is almost complete. Control 
flowering shoots, kept in bags during the flow- 
ering period to exclude gregi showed sim- 
ilar low levels of pod set. In fact, the level is 
approximately 1096 of that of the идо self- 
pollinations (Table 2). These controls involved 
a much larger sample of trees in both populations 
than the manipulated pollinations. These 


ares 


to be transferred from one tree to another. Trees 
existing very close together, suggesting a com- 
mon origin from a single parent by root coppic- 
ing, were tested for the presence of self-incom- 


DIT 


чут rpm mm 


1984] 


BERNHARDT ET AL.—POLLINATION AND BREEDING OF ACACIA 


21 


TABLE 2. Comparison of the breeding systems of two populations of Acacia retinodes from Cape Schanck, 


Victoria following controlled pollinations. 


уље а ee eae ee aaa Ter t ventre qur ote nne m Prem EROR PST ы mee РНЕ ЫНЫ gus nr como 


Number of Number of Number of Total 
Trees Inflorescences Infruc- Number of Pod Set 
Pollen Source Tested Pollinated tescences Pods Set Ratio (4/2) 

Female Trees of Population 1: 

Population 1 6 912 209 665 0.73 

Population 2 4 581 199 863 1.49 

Same tree (selfed) 6 393 4i. 5 0.013 

Control, pollinators excluded 7 3,360“ 5 12 0.001 
Female Trees of Population 2: 

Population 2 8 1,879 320 1,012 0.54 

Population 1 3 1,612 355 1,256 0.78 

Same tree (selfed) 4 573 12 15 0.03 

Control, pollinators excluded 20 4,104“ 9 37 0.009 
Total: 27° 13,414 1,113 3,865 0.29 


* Estimated by using the number of shoots enclosed times 24 (the mean number of inflorescences pollinated 
shoot 


per shoot). 
° Actual number of trees employed. 


patibility. In one such system (20A, B, C), the 
individuals were reciprocally cross-incompati- 
ble. 


e 41 


Natural pollination It igni y low 
er levels of pod set (P = 0.001), than controlled 
pollination (Fig. 3). Six pods/infructescence were 
the greatest number set after open-pollination, 
compared with 13 after controlled pollination on 
the same tree. It is important to establish the 
Probable frequency of natural pollination to de- 
termine the effectiveness of the pollination 
mechanism(s). Observations of the presence of 
polyads on random samples of pistils from six 
different trees showed that there is considerable 
variation (Table 3), with pollination ratios vary- 
"res 0.1 through 0.9, and a mean ratio of 


Diversity of floral foragers. Floral foragers 
Were active between 7:00 A.M. and noon with the 
greatest density observed between 8:00 A.M. and 
11:00 a.m. Foragers represented three insect or- 
ders (Table 4). While dipterans (flies) and hy- 
menopterans (bees) were collected throughout the 
duration of the field study, coleopterans (beetles) 
Were found visiting flowers only from 15 Dec. 
1981 to 4 Jan. 1982. 

ative species of solitary bees, and the intro- 
- Apis mellifera (feral Caucasian strains) 
кез. ир more than 70% of the insect collection 
be Were the dominant polyad vectors. Over 5596 
the bees collected were Lasioglossum (subg. 


Parasphecodes) spp. ofthe family Halictidae (Ta- 
e 4). 


Insect foraging behavior. Beetles usually 
ploughed through individual inflorescences in 
male phase eating pollen and stamens. Acacia 
polyads were deposited sterno- and nototribi- 
cally with the greatest density confined to the 
thoracic region. Whole stamens were found in 
the mandibles of Stenoderus suturalis (Coleop- 
tera). Flies landed on inflorescences in male (sta- 
minate) and female (pistillate) phase and probed 
stamens and styles with their probosces. Acacia 
polyads were found infrequently on these insects 
(Table 5) and were deposited sternotribically on 
the legs, thorax, and abdomen. Larger bees such 
as Lasioglossum spp., Apis mellifera, and Meg- 
achile sp. landed on inflorescences and crawled 
over the entire hemisphere continuously scrap- 
ing the anthers with the two pairs of forelegs and 
raking with the hind legs. Thoracic vibration was 
audible at this time suggesting that polyads were 
harvested by the wing vibration technique as de- 
scribed in Bombus (Heinrich, 1976; Bernhardt 
& Montalvo, 1979) and on other members of the 
Mimosoideae (Arroyo, 1981). The smallest bees 
in the genera Leioproctus (Colletidae) and Hom- 
alictus (Halictidae) appeared to visit each male 


phase flower on an inflorescence sequentially. 
толса ВР НОА РИА ded as observed for 


4 уе 


larger bees. Acacia polyads were deposited ster- 
notribically on all bee taxa, on the legs, thorax, 


22 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


о 2 4 6 8 170 12 о 2 4 6 8: 10 12 


URE 3. Histograms of the percentage frequency 
) 


of pois t under (a) natural open pollination and (b 
quis ipulated cross pollination | on the same tree > (num- 
23).D 


e^ J 


different (D = 7.97, P = 0.001). 


and abdomen (Fig. 4). Pollen was eventually 
transferred to the abdomen or scopae of the hind 
legs of bees (Fig. 5) belonging to asocial families 
(Colletidae, Halictidae, Megachilidae) or to the 
corbiculae in Apis mellifera 

The amount of time a Gee spent on an inflo- 
rescence appeared to be directly proportional to 
the number of flowers in the male phase. Apis 
mellifera and Lasioglossum spp. attempted to 
forage on inflorescences in the female phase but 
normally abandoned them before covering the 
full circumference. Small halictids and colletids 
usually visited all flowers on an inflorescence 
providing at least one-third of them had just 
emergent anthers. Undehisced anthers were found 
in the scopae and corbiculae of all bee taxa col- 
lected suggesting that insects did not regularly 
distinguish between polyads and indehiscent an- 
thers 


Pollinator fidelity and co- blooming plants. Over 
62% of bees, the largest group of pollen vectors, 
carried Acacia polyads in association with one 
or two other species (Table 4). Four pollen species 
were counted on one Homalictus brisbanensis 
and one Lasiogiostum ее sp. All 
1 the pol- 
len of other s species bore, at least. с one species of 
pollen from a flower that also produced nectar 
(Table 4). A total of eight different pollen taxa 
were found on insects collected (Table 5). At least 
four pollen species came from angiosperms that 
were introduced to Australia and had become 


(Мог. 71 


Е 3. Frequency of natural pollination of Aca- 
cia retinodes at Cape Schanck, Victoria. 


Number of 
of Pistils Pistils 
Tree Number Pollinated Scored 
Population 1: 
1 60 90 
3 7 114 
6 31 96 
Population 2: 
54 37 
23 24 89 
34 88 52 
Total X= 37 478 


naturalized on the Cape Schanck peninsula and 
sues Victoria (Willis, 1972). 

and flies observed foraging on Hypo- 
chaeris radicata, aeos ferocissimum, Salpi- 


a 


found to collect nectar from these plants before 
attempting to remove their pollen. Hypochaeris 
radicata was in flower when the field study began 
and was collected on insect bodies until 19 Jan. 
1982 when its flowering season appeared to con- 
clude on Cape Schanck. The two species of So- 
lanaceae (L. ferocissimum and S. origanifolia), 
were also in flower when the field study be 

and their pollen was found on insects’ bodies 
until the end of the field study. Melaleuca lan- 


ceolata was not found in flower until mid-Jan- - 


uary and the first insect bearing its pollen (Leio- 
M metallescens) was not collected until 18 
Jan. 1982. 


DISCUSSION 


Self incompatibility and the breeding sve | 


rt acia retinodes vat. 
uncifolia i is highly self-incompatible. The anal- 
ysis is based on experiments involving nearly 
6,000 inflorescences from trees in two popula- 
tions. Following self-pollination, less than 2% of 
inflorescences set any pods; while following in- 
таро 


e 
e 
2 
o 
3 
S8 
o 
e 
© 
i 
[= 
ке) 
e 
o 
N 
~ 
= 
о 
m 
_ 
3 
2 
а 
oO 
a 


same conditions as unmanipulated controls. 
A summary of published information on the 


1984] 


BERNHARDT ET AL.—POLLINATION AND BREEDING OF ACACIA 


23 


TABLE 4. Pollen load analysis of insects collected while foraging on Acacia retinodes var. uncifolia.* 


Pollen Load 


Acacia 


Insect (Order and Species) Only 


Acacia and 


Other spp. No 
Other spp. Only Pollen 


Coleoptera: 
Automolus depressus TE 
Belidae id 
Cleobora mellyimules +" 
Rhyparida polymorpha psa 
Stenoderus suturalis 1 
Total: 1 
Diptera: 
Eristalis copiosus 1 


Pyrellia sp. T 
Musca vetustissimus ES 
Senostoma sp. M 
Stomorhina subapicalis kr 
Syrphus damaster 1 
Trichareae brevicornis l 
Xanthogramma grandicornis азы) 
Total: 

Hymenoptera: 
Anthobosca spp. 
Apis mellifera 
Homalictus brisbanensis 
Н. oxoniellus 
Lasioglossum (Chilalictus) sp. 
Lasioglossum (Parasphecodes) sp. 
Leioproctus metallescens 
L. plumosus 
Megachile spp. 
Total: 


Grand Total: 


\ 
س‎ 
aS ш мої 


о ME 

О س‎ ьм NWN м 
~ 
-— 


oo ~ 
~ 
Un 


* Combines collections made at both study sites. 


breeding System and occurrence of self-incom- 
patibility in Acacia and other Mimosoideae is 
уеп in Table 6. Very little data are available; 
only 12 species of Acacia and five other genera 
of Mimosoideae are listed. Data are often brief, 
and entirely qualitative, and the methods an 
results are frequently not given. Evidence sug- 
gesting the existence of self-incompatibility is 
8iven for А. decurrens, A. harpophylla, A. macra- 
сатћа, А. mearnsii and now, A. retinodes, and 
for three other mimosoid taxa, Calliandra laxa, 
Enterolobium cyclocarpium, and Pithecellobium 
saman (Table 6). 


Bawa (1974) developed criteria of self-incom- 
patibility: (a) either no more than a third of the 
individuals are self-compatible and/or (b) cross- 


24 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 
TABLE 5. Pollen analysis of those insects collected bearing Acacia mixed with other species. 
Pollen Species* 
Insect 
(Order and Species) Ac Hyp Lyc Sal Mel Pol Euc Mal 
Coleoptera: 
Automolus depressus 1 1 س‎ E = E = zl 
Cleobora mellyimules 1 1 — س‎ se a an 
Stenoderus suturalis 1 E 1 = = = = ub 
Diptera: 
Eristalis copiosus 1 — ES 1 = =. E dm 
E. punctulatus 2 — 1 1 Ба us = 2 
Melanguna viridicens 1 — _ ES = 5 = 1 
Hymenoptera: 
Anthobosca spp 2 2 1 = = ae res = 
Apis mellifera 4 1 2 — 2 — с ХЕ 
Homalictus brisbanensis 2 1 1 2 — — — — 
Н. oxoniellus 2 1 — 1 = = = = 
preces (Paraspe- 
chodes) sp: 52 17 9 8 28 1 — — 
Leioproctus cies 14 — 2 — 12 — 1 — 
L. plumosus 1 — — 1 чы ees 555 ы 
Megachile spp. 2 2 E = iE = iex км 
а Pollen species: Ac = зада retinodes маг. uncifolia J. М. Black; hepa? Hypochaeris radicata L 
Lycium ferocissimum Miers; Sal = Salpichroa и (Lam.) Baill.; Mel = M leuca раан jy ж 


Pol = Polygala myrtifolia gn "Бис = Eucalyptus 


self- and cross-pollinated gave overall ratios of 
self- to cross-pollinated fruit set in populations 
1 and 2 of 0.01:0.73, and 0.03:0.57, respec- 
tively. This level is also consistent with experi- 
mental results from etophytic self-incom- 
patible cultivars of Lolium perenne L. with ratios 
of 0.26: 10.88 pistils pollinated which produced 
seed (Cornish et al., 1980) and Trifolium pra- 
tense L. in which only 0.2% of selfed pistils pro- 
duced seed (Denward, 1963). The overall results 
with A. retinodes give an ISI score of 0.03 ona 
set basis indicating a high level of self-in- 
— је in Hee a score that is seven times 
lower than г 
The existence p^ Bfotógyav has now been re- 


(Newman, 1934a), A. decurrens, A. mearnsii 
(Philp & Sherry, 1946), A. subulata (Kenrick & 
Knox, 1981a). Our data extend these observa- 
tions to A. retinodes, and further demonstrate 
the existence of a female phase at stigma exser- 
tion which is especially favorable for cross-pol- 
lination. In this summer-flowering species, the 
female phase is coincident with the period of 
greatest activity of insect pollinators, and may 
be as short as 2-3 hr. Pollinations made follow- 
ing days of temperatures > 30°C show drastically 


з Ма! = е Matvace 


reduced pod set (Kenrick & Knox, unpubl. data). 
It appears that high temperatures may intensify 
the expression of self-incompatibility in the stig- 
ma and style, or make pollen inviable or stigma 
unreceptive. The data indicate that for successful 
pod set, pollen must be transferred from one tree 
to another. 


Pollination biology of Acacia. Bees appear to 
be the only consistent pollen vectors of A. reti- 
al foragers 

representing two more insect aois ers. „ Аса | ге- 
tinodes should be regarded as a “generalist” mel- 


litophile, as pollinating bees span three native _ 


families of soli idea as well as the nat- 
uraliz 


tary 
ed, eusocial Apis mellifera (primitively el | 
ia; С 


social Halictidae do not occur in 

D. Michener, pers. comm.). These results parallel 
observations by Janzen (1974) concerning the 
swollen thorn acacias of Mesoamerica. Although 
the polyads of Acacia are not shed, as in annon- 


alian or aroid taxa (Vogel, 1978), they do pro- _ 


trude during dehiscence and remain exposed on 
= surface of the anther (Kenrick & Knox, 1979). 


їп мо American Prosopis species (Simpson et ај, 
1977; Arroyo, 1981), as specialized foraging hab- 


1984] 


Em. 


Лесе 
> 


brushlike inflorescences. Acacia retinodes, 

though, receives a less varied spectrum of pol- 
linators than Prosopis as it lacks floral nectaries. 
Acacia retinodes is of little interest to moths, 
most butterflies, wasps, carrion, and dung flies 
etc. that do not require the protein and lipids in 
pollen for ovulation or as a food source for lar- 
vae. Post-pollination exudate is not a nectar sub- 
stitute! Secretions occur very briefly after polli- 
nation has occurred and if insects were attracted 
to the fluid they would undoubtedly interfere with 
the polyad-stigma interface (Kenrick & Knox, 
1981b) 

Furthermore, female phase inflorescences of 
A. retinodes offer no edible reward but they do 
offer color and scent as floral attractants. Cross- 
pollination must occur most frequently via “раг- 
tial pollination by deceit" (sensu Vogel, 1978; 
Bernhardt & Montalvo, 1979). The discrepancy 
between natural and artificial (hand-pollinated) 
pod set may be based in part, on the foraging of 
bees that learn to discriminate between male and 
female phase inflorescences. Bees typically do 
not visit all of the flowers on a female phase 
inflorescence but an objective, artificial cross- 
pollination will probably result in a higher num- 
ber of successful fertilizations. 

Self-incompatibility undoubtedly limits the 
success of pod set between siblings or parents 
and their progeny. Interpopulational crosses are, 
therefore, superior to intrapopulational crosses. 
Long distance pollinations seem most unlikely 
with primary pollinators belonging to the Halic- 
tidae and Colletidae. Ironically, if such pollina- 
tions occur naturally in this region, they woul 
be effected only via the **trap-line" foraging of 
the introduced honeybee! 

Is natural seedset lowered in A. retinodes by 
competition for pollinators with so many natu- 
ralized plant species? Simpson et al. (1977) and 
АЕ (1981) suggested that the most efficient 
bee р of many Leguminoseae were those 
with polylectic-oligolectie (not monolectic) for- 

aging patterns. This increases the frequency of 
cross-pollinations as small bodied bees, depen- 
dent on only one plant species for pollen, rarely 
visit more than one large shrub during a foraging 
bout. Narrow polylectic foraging seems to be the 
norm in bees associated with Australian Acacia 
species as these insects must obtain their chem- 
ical energy (floral nectar) from co-blooming taxa 
(Bernhardt, 1983; Bernhardt & Walker, 1983a, 
1983b). The only established competitor for the 


its are not requ ired t 


BERNHARDT ET AL.—POLLINATION AND BREEDING OF ACACIA 25 


„| 
€ 5 


Ficures 4, 5. 4. Ventral view of Leioproctus me- 
tallescens caught on A. retinodes showing the build-up 
of pollen on the е legs and е in contrast to 
the forelegs and thorax (x 9.4). — 5. Scopal hair of Lasi- 
MEAE oe des od А sp. ти а mixed load of 

lyads of A. retinodes and grains of Melaleuca lan- 
pb s (x640). 


A 2 +h 


Acacia 
со (Bernhardt, 1983; Bernardt & Walker 
1983a). True “роПеп flowers” (sensu Vogel, 1978) 
posh overlapping flowering periods with sym- 
d by the same 
jeté Heinrich, 1976; Bernhardt & Montalvo, 
1979; Bernhardt, 1984). This has been inter- 
preted as се advantageous as the limited 
pollinato like 
that the invasion of European and South African 
plants has not put pressure on A. retinodes but 
has supplanted the ori tar flora, exclud- 
ing Melaleuca lanceolata (Willis, 1972). 
ое the majority of mimosas studied so 
“Ра- 


llanatare nf an 


n Type" pollen flower (sensu Vogel, 1978) 
due to the absence of floral nectaries and the 
accessibility of polyads retained on the anthers. 
Self-incompatibility and synchronous protogyny 
encourage cross-pollination in A. retinodes but 
also reduce the success of bee-mediated geito- 
nogamy. The absence of floral and extra-floral 
nectar reduces the spectrum of potential pollen 


TABLE 6. Breeding system of selected species of Acacia and other genera of Mimosoideae. 


Number of | Number of Flowers 
Trees Tested per Polli- 
Species Interpretation? Sampled* nation per Tree* Pollination Tests’ Reference 
1. Acacia 
A. aroma Hook. & Arn. SI >] 1 flowering cross, self, control Simpson, 1977 
ranc 
A. constricta Benth. SI >] 1 flowering cross, self, control Simpson, 1977 
branch 
A. cornigera L. outbreeding NG NG seed set in glass- Janzen, 1974 
house 
A. decurrens Willd. outbreeding 14 flowering open 71.9%, self Philp & Sherry, 1946; 
branches, 26.8%, 400 Moffett & Nixon, 1974 
8.3/tree ovules/tree 
A. drepanolobium SI 42 seed set in glass- Hocking, 1970 
Harms. ex Sjéstedt ouse 
A. furcatispina Burk. SI >1 1 flowering cross, self, control Simpson, 1977 
branch 
A. greggii Gray SI >1 1 flowering cross, self, control Simpson, 1977 
branch 
A. harpophylla outbreeding 17 NG number of pods/ Coaldrake, 1971 
F. Muell. ex Benth. cluster, cross 
0.47%, self 
0.19%—0.26% 
А. тастасатћа Н. & В. 51 6-7 3,786-15,780 cross 0.19%, self Zapata & Arroyo, 1978 
096, control 096 
A. mearnsii De Wild. outbreeding 24 flowering number of viable Moffett, 1956 
(syn. A. mollissima) branches seeds/pod, open 
6.8%, self 2.7% 
. Other Mimosoidea 
Calliandra laxa Benth. SI 5-6 136-139 cross 11.76%, self Zapata & Arroyo, 1978 
: 0%, control 0% 
С eriophylla Benth. SI >i Simpson, 1977 


1 flowering 
branch 


9c 


N3G3IVD TVOINV.LOS IMNOSSIW AHL 40 STVNNV 


IL 10A] 


TABLE 6. Continued. 


Number of Number of Flowers 
Trees Tested per Polli- 
Species Interpretation* Sampled nation per Tree Pollination Tests? Reference 
Enterolobium cyclo- SI 3-5 15—100 number of flowers Bawa, 1974 
carpum (Jacq.) setting seed, self 
Griseb 0%, cross 0.28% 
Leucaena trichodes SI NG NG NG Hutton & Eddie, 1982 
(Jacq.) Benth. 
L. esculenta (MCC & SI NG NG NG Hutton & Eddie, 1982 
Sesse) Benth 
L. collinsii Britton & SI NG NG NG Brewbaker, 1982 
Rose 
L. lanceolata 8. Watson SI NG 15 NG Brewbaker, 1982 
L. macrophylla Benth. SI NG 4 NG Brewbaker, 1982 
L. pulverulenta SI NG 18 NG Brewbaker, 1982 
(Schlecht.) Benth 
L. shannoni Donn. Smith SI NG 15 NG Brewbaker, 1982 
Pithecellobium saman SI 3-5 15-100 self 0%, cross Bawa, 1974 
Jacq. 0.28% 
Prosopis chilensis Mol. SI >1 1 flowering cross, self, control Simpson, 1977 
tuntz emend. Burk. branch 
P. flexuosa DC. SI >1 1 flowering cross, self, control Simpson, 1977 
branch 
P. velutina Woot. 51 >1 1 flowering cross, self, control Simpson, 1977 
branch 
P. torquata (Lag.) DC. SI >1 1 flowering cross, self, control Simpson, 1977 
branch 


* SI = self-incom 


patible. 
* Control ар ong inflorescences bagged but unmanipulated. 


* NG = not give 


[7861 


VIOVOF AO омазача аму NOLLVNITIOd — "IV ІЯ LO VHNOIS 


28 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


vectors, excluding vertebrates like arboreal m. 
supials (Turner, 1983) and birds (Ford & Forde, 
1976; Kenrick et al., 1983), but it may also en- 
courage cross-pollination as bees are forced to 
leave individual plants periodically when their 
supply of chemical energy is depleted. 


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BAKER, H. G. & B. A Harris. 1957. The are cuento 
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BA К. S. 74. Breeding systems of tree species 

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CRUDEN, R. W. 1977. Pollen ovule ratios: a conser- 

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DENWARD, T. 1963. The factio of the incompati- 
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24: 793-7 


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P. H. Raven vc esee in T а 
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У ARA 


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ds 6. Diversite cds weit 


[VoL. т | 


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Hopkins, H. С. 1981. 

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fram ct 


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BERNHARDT ET AL.—POLLINATION AND BREEDING OF ACACIA 29 


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230. 


FLAVONOIDS OF ONAGRACEAE! 


JOHN E. AVERETT? AND PETER H. RAVEN? 


ABSTRACT 


A 1 frnl а * +“ 1 1 


3 t ж ‚= RM t 


f Onagraceae 


and prel iminary surveys have bee 


J 


of the 17 genera. 1. Some 


apum Pr 
40 flavonoids, including elycoflavones, уон, еи со have v isolated and ident ified. 


or co-occurring "n flavonols, characterize the more generalized tribes, whereas only flavonols are 


, ОССТ iri 


found in the pda 
members of al 
Fuchsieae, and Onagreae. In 


n some 
aged except Кейин and Epilobieae, whereas flavones occur only in Gincana 
fro 


other lines of phylogenetic ету about the relative degree of advancement of taxa, but на 
do not provide strong indications of phylogenetic relationship between genera or tribes. 


AA РБ. els £n 238 z ry 1 


concentrated on the compounds found in the 
leaves of these plants, and this paper will em- 
phasize such studies. First, however, it seems 


concerned with the floral pigments of this family. 
In the later sections of the paper, when dealing 
with foliar flavonoids, we shall not concern our- 
selves with anthocyanins. The anthocyanins of 
the flowers of Fuchsia and their influence on 


The 3-glucosides and the 3,5-diglucosides of all 
six common anthocyanins are responsible for 
flower color in this genus. Variants in color ap- 
pears to be almost wholly determined by these 
anthocyanins (Crowden et al., 1977). One of them, 
malvidin 3,5-diglucoside, also has Лаа reported 
from the flowers of Epilobium and Clarkia, and 
ucoside, also from the 


a 
cyanins of 12 genera of the family. They found 
four widespread anthocyanins, and noted that 
several other anthocyanins seemed to have 
evolved independently in several lines. Cyanidin 
3-glycoside was the most commonly encoun- 
tered anthocyanin in Onagraceae, being present 
in Calylophus, Gaura, Gongylocarpus, Hauya, 
and Xylonogra. 

A member of another class of floral pigments, 


1 WW. *a4. n 4 с ыз мт. 


the chalcone isosalipurposide, was reported as а 


floral pigment in 13 species from five genera of _ 


Onagraceae by Dement and Raven (1973, 1974). 
This chalcone is of particular interest because it 


represents a class of flavonoids that is apparently 


not found in the leaves of any Onagraceae. This — 


chalcone plays an important ecological role in 


yellow-flowered Onagraceae, not reflecting light — 


in the ultraviolet wavelengths so conspicuous in 
the portions of the 


formation of floral markings strikingly visible 
under ultraviolet light, and thus to the insects 
that visit he flowers of these plants. 

A each genus and most 


не лае within the family have been analyzed | 


for its foliar flavonoids. S 


ceae, not including anthocyanins. These include 
seven glycoflavones and six flavones. The re- 
mainder are flavonols based on kaempferol (5), 


atively few exhibiting seven or B-ring (3' 0 
substituents. At least four sulphated compounds, 
occurring in two different tribes, have been de- 
tected in the family. These data are summarized 

a Bao EC E 1 d eve 


pate 
5 


tems are shown in Figure 1. Results for the in- 
dividual tribes (summarized in Table 2) follow. 

Jussiaeeae. Jussiaeeae include the single ge- 
nus Ludwigia, with about 80 species. The species 


c 


D 


rc “ине, e ae" 1 4 J.E. À. 
R. Presented at ata symposium on rre II Int ional Congr f Svst i di Evolutionary 
1980. у 


same flowers where carot- . 
enoids predominate. Here it contributes to the - 


and P НЕ 
oe. Vancouver, B.C., Augu 
? Departm 


ent of Bio ology, University of Missouri-St. Louis, St. Louis, Missouri 63121. 
3 Missouri у гарда Garden, P.O. Box 299, St. Louis, Missouri 63166. 


ANN. MISSOURI Bor. GARD. 71: 30—34. 1984. 


| сетед 


19841 AVERETT & RAVEN—FLAVONOIDS OF ONAGRACEAE 31 
TABLE |. Flavonoids in the Onagraceae.* 
Flavonols Glycoflavones Flavones 
kaempferol quercetin myricetin vitexin apigenin 
3-O- 3-O-gal 3-O-gal isovitexin 7-O-glu 
3-O-glu 3-O-glu 3-O-glu orientin 7-O-glucuronide 
3-O-rha 3-O-rha 3-O-rha isoorientin 7-O-glucoronide- 
3-O-ara 3-O-ara 3-O-ara orientin-o- sulphate 
3-O-rha-glu 3-O-rha-glu 3-O-rha-glu acylate luteolin 
3-O-rha-gal 3-O-diglu itexin-o- 7-O-gl 
3-O-diglu 3-O-me-7-O-glu acylate 7-O-glucuronide 
3-7-O-diglu lucinin tricinin 
7-O-rha 7-O-glucuronide- 
3-O-me, 7-O-glu sulphate 
3-O-xyl-gal 
3-O-sulphates 
3'-O-me 


3-O-glucuronide 


ХАО те 
* Gal = galactose, glu = glucose, rha = rhamnose, ara 


are unevenly divided among 17 sections. As 
demonstrated by Eyde (1978, 1979), Ludwigia 
represents a phylogenetic line distinct from all 
other genera, which are, therefore, more closely 
related to one another than any one is to Lud- 
wigia. All but a few of the species of this genus 
have been examined for their foliar flavonoids 
(Averett et al., unpubl. data). 
Eight flavonoids, includi g three gly 
based on orientin and isoorientin and five fla- 
Yonol 3-O-glycosides, all based on quercetin, have 
been identified in Ludwigia. Both classes of fla- 
vonoids are found among the more primitive 
Мир. Myrtocarpus, Michelia, апа Pterocau- 
on. Only flavonols are found in sections Tecti- 
e кош, Oligospermum, and Cary- 
: lic oidea; only glycoflavones are found in the 
саш ve ten sections. Even within sect. Ptero- 
v d two of the five species have fla- 
tha шы us, with increasing specialization of 
је » there is evidently a corresponding loss 
Ee lycoflavones or flavonols. Overall, gly- 
nod Age predominate. Another point to be 
cd that all of the flavonols are based on 
a 1n and that all of the substituents are rel- 
e Y simple 3-O-glycosides. 
clear ай. 8 The only genus, Circaea, has no 
family. It ; T to any of the other tribes in the 
Phyletic У ~ ч Owever, clearly a generalized early 
al. 1978) Shoot. Previous studies (Boufford et 
and the reported the presence of glycoflavones 
study bie presence of flavones. The earlier 
15 considered preliminary, was con- 
With hydrolysates, and included a limited 


1 a 


= arabinose, xyl = xylose. 


number of species. Subsequent work with ad- 
ditional species, especially Asian ones, has con- 
firmed the presence of some 14 compounds 
among the species of Circaea. These include eight 
glycoflavones, four flavones, and two flavonols. 
Fuchsieae. Fuchsia is the only genus of the 
tribe. Eighteen flavonoid glycosides have been 
identified from si tal species of Fuchsia 
and seven of their hybrids by Williams et al. 
(1983). The compounds include 11 flavonol gly- 
cosides and six flavone glycosides. Three of the 
six flavones are sulphates. Among the approxi- 
mately 100 remaining species of Fi uchsia, we have 
identified 12 flavonoid glycosides, including four 
flavones and eight flavonols. The flavones in- 
clude two sulphates. The flavonols include six 
3-O-glycosides based on kaempferol, quercetin, 
or myricetin; and two methyl ethers. Flavonol 
glycosides are found in each of the species ex- 
amined. Flavones are consistently present in each 
of the four species of sect. Skinnera, occasional 
in the single species of sect. Kierschlegeria, and 
sporadic among one or a few species of sections 
Fuchsia, Ellobium, and Quelusia. The flavone 
sulphates are restricted to sect. Skinnera. With 
this feature, coupled with the consistent presence 
of other flavones, sect. Skinnera is the most dis- 
tinct of the genus with respect to its flavonoid 
chemistry. This New Zealand-Tahitian group of 
what is otherwise an American genus 1s equally 
distinctive morphologically, although clearly a 
member of the genus, which is quite diverse even 
excluding sect. Skinnera. 
Although both fl 


nrag 


32 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


FLAVONOID SKELETON 


R R 
APIGENIN H он 
AND NUMBERING SCHEME OH 


LUTEOLIN OH 


R 
ISOVITEXIN KAEMPF EROL н он 
VITEXIN QUERCETIN OH OH H 
MYRICETIN OH 


UR se structures and a scheme 
Poe или discussed in the tex 


ent in Fuchsia, the flavones occur only in a few 
scattered species. In contrast to this pattern, fla- 
vonols are аи of the genus, occurring 
in every speci 

она Preliminary data indicate the 
presence of six flavonol 3-O-glycosides and at 
least four glycoflavones in Lopezia, the only ge- 
nus of the tribe. To date, glycoflavones have been 
detected in one of the more primitive sections 
of Lopezia, sect. Jehlia, and in both species of 
the very distinctive sect. Riesenbachia, which is 
evidently an early offshoot. Flavonols occur in 
both sections but are absent in one of the two 
species of sect. Riesenbachia, L. riesenbachia. 
Only flavonols are present in the remaining sec- 
tions. Neither methylated nor ud flavo- 
noids have been detected in Lopez 

Hauyeae. Hauya, the single ane jo the tribe, 


Rica. In all taxa of Hauya, four flavonol 3-O- 
prone are typically present, with an addi- 
tional t In at least some 

populations each of the four copped alsin of H. 
ele: egans, how resent. 
The inf species, the diploid H. hevdeana 
Donn. Sm. & Rose, lacks glycoflavon 

Onagreae. Flavonoid analyses af Gusts 
have been confined largely to Oenothera, but at 


[VoL. 71 


TABLE 2. Distribution of flavonoids among the 
tribes of Onagraceae 


Glyco- 
Flavonols flavones  Flavones 
Tribe: 
Jussiaeeae E] * 
ircaeeae Е] • e 
Fuchsieae LJ а 
pezieae e e 
Hauyeae e • 
nagreae * * LÀ 
Epilobieae e 
least some dat ilable for each of the other 


genera (Kagan, 1967; Zinsmeister & Bartl, 1971; 
Zinsmeister et al., : 
Averett et al., 1982; Averett & Raven, 1983a, 
1983b). Only flavonols have been reported for 
this group but studies in progress have identified 
glycoflavones and flavones, as well, in a few 
species of Oenothera and Gaura. Some 20 com- 
pounds, including compounds with 3; 3,7; 7; and 
B-ring catia eagle sg been isolated and iden- 
tified from the e substituents include 
monoglycosides, pu eren sulphates, and 
methyl ethers. Typically, four to six compounds 
are found in any one genus but these range from 
three in Stenosiphon to more than 15 in Oeno- 
thera, taking the genus as a whole. Additional 
chemosystematic analyses in the tribe are need- 
ed, especially in Calylophus, Camissonia, Clark- 
ia, and Gaura, in view of the diversity of com- 
pounds in this tribe. Preliminary surveys both 
of Gaura and of hitherto unexamined species of 
Oenothera indicate the presence of a great di- 
versity of systematically interesting flavonoids, 

both unusual flavonols and glycoflavones. 
Epilobieae. n. compounds, all 3-0- 
mpferol, quercetin, or my- 


ricetin, are iid a among the species of Epilo- ' 


a and Boisduvalia, the two genera of this tribe. 
compounds, the 3-O-rhamnosides and 3-O- 
егы of quercetin and myricetin, are typi- 


Chamaenerion (Averett et al., 1978, 1979). 


The lack of flavonoid diversity among so many | 
species is striking, with only seven compounds, : 


1984] 


each a simple monoglycoside, present. Variation 
is largely in the presence or absence of glycosy- 
lation by an arabinosyl moiety and in the pres- 
ence or absence of the single kaempferol com- 
pound. In general, the more advanced taxa have 
fewer compounds, representing the absence of 
molecules with one glycosidic substitution and/ 
or the absence of kaempferol-based compounds. 
Epilobieae are highly specialized in other char- 
acteristics; the flavonoids they exhibit seem to 
represent an example of secondary loss of sub- 
stituents; i.e., highly advanced in the terminol- 
ogy of Gornall and Bohm (1978). The trend is 
apparent both within the tribe and in compari- 
sons between it and other tribes. 


DISCUSSION 


Harborne (1966, 1976, 1977) has considered 
complex glycosylation and methylation as ad- 
vanced characters and the presence of glycofla- 
vones as primitive. Gornall and Bohm (1978), 
although in general agreement with the primitive 
nature of glycoflavones, have suggested a third 
State, highly advanced, where substituents, once 
gained, are then lost. We also have suggested that 
a loss of substituents may be correlated with evo- 
lutionary advancement within a given taxon 
(Averett, 1973; Averett et al., 1978, 1979). The 
distribution of flavonoid types in Onagraceae 
(Table 2) is interesting in relation to these sug- 
gestions, 

Jussiaeeae, as mentioned above, represent a 
је line within the family, a line that is char- 
—! by the presence of glycoflavones. Fla- 
abi are widespread in Jussiaeeae, but are rel- 

Y Simple glycosides of only one base 
heus, Glycoflavones and flavonols in Lud- 
itive site found together only in the more prim- 
secas 2 The sections considered to be more 
tes de ave lost one or the other of these 

5 of flavonoids. 
we hee of the famil y itut d main 
din rn in the family. Within this line, 
M dod Md TAM сый 

. о Б C tribe e" TO - 
Ne &eneralized in their characteristics, On- 
he m. Соо more specialized. Lopezia 
nols. In E ave both glycoflavones and flavo- 
stricted to dm however, glycoflavones are re- 
apparent] x ew of the most generalized taxa, 
evolutio У having been lost during the course of 

n of the genus. Flavonols, on the other 
occur in every species examined of both 


AVERETT & RAVEN—FLAVONOIDS OF ONAGRACEAE 33 


Lopezia and Hauya except for one species of 
Lopezia, L. riesenbachia, which is obviously spe- 
cialized. Thus, flavonols clearly predominate in 
these two genera, but the ones that are present 
are generally simple in structure, and glycofla- 
vones are frequent in the generalized species. 

Fuchsia has both flavonols and flavones but 
no glycoflavones, whereas Circaea has all three 
classes of compounds. In contrast, the two more 
specialized tribes, Onagreae and Epilobieae, dif- 
fer markedly in their flavonoid constituents. On- 
agreae, like Circaea, have glycoflavones, fla- 
vones, and flavonols, whereas Epilobieae have 
the least diverse pattern of any tribe, having only 
flavonol 3-O-monoglycosides. 

If the presence of glycoflavones is a primitive 
characteristic, as Harborne (1976) has postulat- 
ed, the fact that this class of compounds occurs 
in all groups except Fuchsia and Epilobieae is 
notable. Epilobieae is a group that is clearly ad- 
vanced in many of its characteristics, and one 
might assume that glycoflavones have been lost 
in the evolution of Fuchsia also. 

Especially noteworthy in considerations of fla- 
vonoid evolution in Onagraceae is the presence 
of flavones in Circaea, Fuchsia, and the tribe 
Onagreae. Extensive surveys of flavonoids have 
not been completed in other families of the order 
Myrtales, but thus far, flavones have not been 
detected in any family other than Onagraceae 
(Gornall et al., 1979; Dahlgren & Thorne, 1984). 
This pattern suggests that ability to synthesize 
flavones may have evolved within Onagraceae, 
possibly in the ancestor of the “non-Ludwigia” 
branch of the family. If this hypothesis is correct, 
flavones were subsequently lost in most species 
of the family, including all of Hauya, Lopezia, 
and the tribe Epilobieae. It seems very unlikely 
that the biochemical pathway leading to the syn- 
thesis of flavones originated independently in the 
three groups in which they occur. Despite this, 
it also seems unlikely that these groups could 
share an immediately common ancestor in view 
of the major differences between them. Thus, if 
it can be interpreted properly, the occurrence of 
flavones in these three tribes might offer valuable 
clues to relationships within the family. 

Overall, the pattern of distribution of glyco- 
flavones and flavones in Onagraceae tends weak- 
ly to support the hypothesis that Fuchsia and 
Circaea might be early offshoots of the phylo- 
genetic line leading to the tribe Onagreae, and 
that Hauya, Lopezia, and the tribe Epilobieae 
might not belong to this same line. Furthermore, 


34 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


there is some suggestion in its diversity of com- 

pounds that the tribe Onagreae might be heter- 

opan 5 origin, and new detailed information 

the species 

and genera that make up this large tribe might 
be helpful in evaluating this possibility. 

ite moni for the family ; asa whole (Table 


73 
1 


t i all tribes 
except Fuchsieae and ETE Onagreae ex- 
hibit the greatest diversity of compounds, in- 
cluding flavonol 7-O-glycosides and B-ring sub- 
stitutions. The Epilobieae exhibit the least diverse 
pattern, having only flavonol 3-O-monoglyco- 
sides. If these data represent, as indeed we be- 
lieve they do, a proliferation of compounds dur- 
ing the course of evolution of the family with a 
reduction of compounds with further advance- 
ен they: are in general agreement with assess- 

ary States of sir taxa 
derived from other lines of invest con- 
text, however, the lack of aa in ue uch- 
sia is unexpected in view of the ubiquitous dis- 
tribution of this class of compounds among all 
other genera of the family with relatively prim- 
itive characteristics. 


LITERATURE CITED 


AVERETT, J. E. 73. Biosystematic study of Cha- 
mesaracha eee Rhodora 75: 325-365. 
& P. 


. RAVE 983a. Flavonoids of Xylo- 
Hm Повага Ген рабин 22: 1679- 
1680 
Барча ЕЕ 19835. Flavonoids of Stenosiphon 
(Onagraceae). Pe Ar grid 22: 168 T 
———, 1982. The oe 
M Y Hetrogaura (Onagraceae). а 
istry 21: 
— B. de P. H. RAvEN. 1978. The flavo- 
noids of Onagraceae, tribe Epilobieae: r 
sect. Ses Amer 
„К. Н. N & Н. 'BECKE KER. 1979 PA Fla- 
vonoids of ваша Tribe Epilobieae. Amer. 
J. Bot. 66: peer 11 к 
BourroRp, D. E., м & J. E. AVERETT. 1978. 
E in vps soe Biochem. Syst. Ecol. 6: 
59-60. 


WRIGHT & J. B. HARBORNE. 1977. 
ocyanins of Fuchsia (Onagraceae). Phyto- 

chemistry 16: 40 

DAHLGREN, R. & R. F. THORNE. 


CROWDEN, R. K., J. 
An 


1984. The order 


[Von 71 


=, K. Pur 
glycosides in авс uth Am 


Myrtales: circumscription, variation, and relation 
ships. Ann. Missouri Bot. Gard. 71: (in press). - 
DEMENT, W. A. & P. Н. RAVEN. 1973. Distribution 
of the chalcone, isosalipurposide, in the e Onagra- 
сеге. Phytochemistry 12: 807—808. 


19 igments responsible for ш. 
pine patterns in flowers of Oenothera (Ona 
ceae). Nature 252: 705-706. 
EYDE, К. Н. 1978 (1977). _Reproductive structures 
( 


ae). I. An- 
m. Ani Misso 


evolution in Ludwigia (Onagraceae). II. Fruit and 
issouri Bot. Gard. 65 5 
GORNALL, R. OHM. 05 


78. Angiosperm 

flavonoid evolution: a reappraisal. Syst. Bot. 3: 
353-368. | 

—— ——, == & R. DAHLGREN. 1979. The dist 
butio on fe ae in the angiosperms. Bot - 
132: 1-29. 


pigments in plants. Pp. 271-29 T. Swain (ed- 
itor), Comparative isa изаћи ы Academic 
€ ndon 


1967. Comparative eprint: of the Fla- 
vonoids. Academic Press 
197 


tabolis 
Coevolution. Nova Bu Leopoldina Supp. "Nr. 
Barth Verlag, Leip: 
1977 сно а and the evolution of an- 


giosperms. Biochem. Syst. Ecol. 5: 7-22. 
HOWARD, T. H. MABRY & P. H. RAVEN. 1972. 
Di on of flavonoids in twenty-one species 

291 


hytochemistry 6: 317-318. E 
Flower color in Fuchsia cul- | 
ars. Canad. J. Bot. p 1215-1217. | 
Wass C A ТИ Рим & J. В. HARBORNE. 
1983. Leaf flavonoid ма оїһег phenolic p ; 
sides as indicators of parentage in six ornamental 
species of Fuchsi their hybrids. Phy- - 
tochemistry 22: 1953-1957. i 
YAZAKI, Y. & K. HAYASHI. 1967. Analysis of flower | 
colors in Fuchsia hybrida with reference to the 
concept of copigmentation. Proc. Japan. Acad. 43: 


316- 
амино н. D. & S. BARTL. 1971. The phenolic 
mpounds of Oenothera. Phytochemistry 10: 
3129 3132. 
о & Н. wrona е Flavonoid | 
s of Oeno- _ 
era sect. Coe. матаган 16: 497. 


| 


А PALYNOLOGICAL STUDY OF THE GENUS 
FUCHSIA (ONAGRACEAE)! 


JOAN W. NOWICKE,? JOHN J. SKVARLA,? PETER Н. RAVEN,* 
AND PAUL E. BERRY? 


ABSTRACT 


The pollen of 76 collections representing 48 of the ca. 100 species and all nine sections of Fuchsia 
was examined in light (LM) and scanning electron microscopy (SEM), and a selected group in trans- 
mission electron microscopy n of Fuchsia is shed ds and is mostly 2-aperturate 
or very rarely 3-aperturate; the exine sculpture is composed of globular elements, or more rarely 
elongated elements; the viscin threads are segmented, more rarely smooth; the exine is composed of 
two layers, an outer spongy undifferentiated ektexine, and an inner solid, massive endexine. The 


polyploid sects. Quelusia (eight species) and Kierschlegeria (one) are characterized by 3-aperturate 
ис 


pollen as are several tetraploid species in sects. 


Asia and Hemsleyella. As far as is known, 3-aperturate 


grains usually occur only in polyploid species; but not all polyploids have 3-aperturate pollen. Two 


represent the condition of the diploid ancestors. It may be con 


. Two- 
n both sects. Kierschlegeria and Quelusia, where they doubtless 


cluded that the common ancestor of 


all extant sections of Fuchsia had 2-aperturate pollen, although ultimately, within the Onagraceae, the 


2-aperturate condition must have been derived from 3-aperturate pollen. 


Most species of Fuchsia 


have a globular-type sculpture element, but sects. Encliandra (six species) and Kierschlegeria have 
diti isci 


elongated elements, a derive 
threads, but sects. Sc 


nted-beaded viscin 


ufia (two species), Jimenezia (one) and Kierschlegeria (one) and some species 


of sect. Encliandra have smooth viscin threads, another derived condition. A combination of aperture 
H : 4 R Ё. to th 1 ti f Fi 


hsia, 


number, sculpture element, and viscin th 


although palynology provides, at best, only weak evidence for distinguishing sections. 


In the already highly distinctive Onagraceae, 
mis genus Fuchsia L. (100 species; Munz, 
iin Breedlove, 1969; Breedlove et al., 1982; 
2 1982) is further distinguished by 
уш hae pollen in most species and a berry- 
Кай: » two characteristics not found іп any 
4 Ing taxa. Most species of this genus are 

Tubs and trees with red, tubular, bird-polli- 
we although a few have shorter flow- 
a id EU colored, yet still red or reddish 
bán i ме of the distinctive flowers and 
E uchsia has traditionally been treated as 
E ogeneric tribe of Onagraceae. In fact, it has 

је vious relationships to any other genus. 
= па all the distinctive features of Fuchsia 
Padel. > advanced, in overall characteristics, 
эш us of the less specialized of the 17 
omy (E graceae. Evidence from floral anat- 

yde & Morgan, 1973), wood anatomy 


(Carlquist, 1975), cytology (Kurabayashi et al., 
1962), and leaf architecture (Hickey, 1980) sup- 
port this conclusion. The ovary of Fuchsia is 
4-locular with a biseriate row of ovules in each. 
The placentation is axile but more importantly 
the placentas are deeply cleft, a primitive con- 
dition. Fuchsia is one of only three genera, Hauya 
Moc. & Sesse and Ludwigia L. being the other 
two, that lack interxylary phloem, a clearly prim- 
itive condition. Most species of Fuchsia are dip- 
loid, with a gametic chromosome number of n = 
11, basic in Onagraceae. In addition, the chro- 
mosomes are relatively large for Onagraceae, lack 
reciprocal translocations as a regular part of the 
adaptive system, and are poorly differentiated 
into heteropycnotic and eupycnotic segments 
(Kurabayashi et al., 1962). In addition, Baker 
and Baker (1983) characterized the starchless 
condition found in the pollen grains of Fi uchsia 
and Lopezia Cav. as the ancestral one, and sug- 


1 
thang PPorted in part by National Science Foundation grants to Peter Н. Raven and to John J. Skvarla. We 


2 
3 


s гу ouri Botanical Garden, Р.О. Box 299, St. Louis, Missouri 63166. 
ү E *nto de Biología de Organismos, Universidad Simón Bolívar, 


ANN. 
Missouri Bor. GARD. 71: 35-91. 1984. 


Р. С. Hoch, J. Bittner, S. Braden, W. Chissoe, M. J. Mann 
Пере У Department, Smithsonian Institution, Washington, D.C. 20560. 


‚ and 5. Nelson for their technical assistance. 
Oklahoma 73019. 
Apartado 80659, Caracas 1080, 


36 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


TABLE 1. Fuchsia specimens illustrated, with collector, locality to country, and Figure number(s). 


Sect. Ellobium 
Fuchsia decidua Standley 
F. fulgens DC. 


F. splendens Zucc. 


Sect. Encliandra 
F. cylindracea Lindley (F. par- 
viflora sensu Breedlove, 
non Lindle 
F. cect aaa Steudel subsp. 
encliandra 


F. encliandra Steudel subsp. 
tetradactyla (Lindley) 


reedlove 

F. microphylla H.B.K. subsp. 

aprica (Lundell) Breedlove 

F. microphylla H.B.K. subsp. 
п & 


F. microphylla =ч В.К. subsp. 
hidalgensis (Munz) Breedlove 

F. microphylla H.B.K. subsp. 
microphylla 

F. microphylla H.B.K. subsp. 
quercetorum Breedlove 

F. obconica Breedlove 


F. ravenii Breedlove 


F. thymifolia H.B.K. subsp. 
minimiflora (Hemsley) 
reedlove 
F. thymifolia H.B.K. subsp. 
thymifolia 


Sect. Fuchsia 

F. ayavacensis H.B.K. 
F. boliviana Carriére 
F. corollata Benth. 

. cuatrecasasii Munz 
F. dependens Hook 
F. gehrigeri Munz 
F. hartwegii Benth. 


F. hirtella H.B.K. 
F. macrophylla Johnston 


— Á—M——À e 


Boutin 3036 (MO) 

Oliver & Voerhoek- 
Williams 562 (MO) 

Burger & Stolze 5969 
MO 


Croat 515 (MO) 


Breedlove 36037 (MO) 
Breedlove 15831 (DS) 


Davidse & Davidse 
Kalin 7089 (MO) 
Breedlove 15849 (DS) 
Breedlove 25920 (MO) 
Breedlove 31744 (CAS) 


Utley 4297 (MO) 
Raven 20975 (DS) 


Breedlove 15881 (US) 
Arizmendi 259 (MO) 
Breedlove 22959 (CAS) 
Breedlove 18711 (CAS) 
Ventura 1457 (MO) 
Kalin 7090 (MO) 
Breedlove 22788 (CAS) 
п & Laskow- 


ski 3993 (MO) 
M. 9794 (MO) 


Berry & Escobar 


Bristol 876 (DS) 

Berry 3543 (MO) 

Berry & Aronson 
3080 (MO) 


Mexico 
Mexi 


Costa Rica 


Costa Rica 


Mexico 
Mexico 


Mexico 
Mexico 
Mexico 
Mexico 
Mexico 


Costa Rica 
Mexico 


Mexico 
Mexico 
Mexico 


Mexico 


Mexico 
Mexico 
Peru 


Colombia 
eru 
Colombia 


Colombia 
Colombia 


7-9 
10-12 
13-14 


15, 115-117 


67. TA 
144-146 


69 

59, 60 
138-141 
135-137 
120-123 


64, 65 
129, 130 


124-128 

66 

131-134 

70, 142, 143 

58 

61-63, 71, 
118-119 

147-150 

57 


55, 56, 68 


103, 104 


1984] NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 


TABLE 1. Continued. 


F. macrostigma Benth. 
F. mathewsii Macbride 
F. pallescens Diels 

F. petiolaris H.B.K. 


F. pringsheimii Urban 
Е. putumayensis Munz 
F. scabriuscula Benth. 

F. tincta Johnston 

F. triphylla L. 

F. verrucosa Hartweg 


Sect. Hemsleyella 
F. apetala Ruiz & Pavón 


F. chloroloba Johnston 


F. garleppiana Kuntze & Wittm. 


F. inflata Schulze-Menz 


F. juntasensis Kuntze 
F. membranacea Hemsley 
F. tillettiana Munz 


Sect. Jimenezia 
F. jimenezii Breedlove, Berry & 
Raven 


Sect. Kierschlegeria 
F. lycioides Andrews 


Sect. Quelusia 
F. bracelinae Munz 
F. campos-portoi Pilger & 
Schulze 


F. coccinea Sol. 
F. magellanica Lam. 


F. regia (Vand. ex Vell.) Munz 
Sect. Schufia 


F. arborescens Sims 
F. paniculata Lindley 


Escobar 1094 (MO) 
Berry 3603 (MO) 
Berry 3570 (MO) 
Berry 3539 (MO) 
Berry 3560 (MO) 
Tuerckheim 3151 (MO) 


Berry 3562 (MO) 
Berry 3593 (MO) 
Berry et al. 2597 (MO) 
Davidse 2689 (MO) 


Berry 3286 (MO) 
Grant 10260 (US) 


Berry & Aronson 

3033 (MO) 
Berry & Aronson 

3070 (MO) 
Berry et al. 2599 (MO) 
Linderman 2030 (MO) 
Berry & Aronson 

2 (МО 

Berry 3638 (MO) 
Berry 3278 (MO) 
Berry 3267-B (MO) 
Berry 3463 (MO) 


Allen 4965 (MO) 
Croat 36223 (MO) 


UC Bot. Gard. Berk. 
53.1303-S2 (RSA) 
(from Hartweg in 


19 
Zóllner 8089 (MO) 


Mexia 4013 (US) 
Brade 18008 (S) 


Irwin et al. 30326 (NY) 

Solomon & Solomon 
4599 (MO) 

Raven 20560 (MO) 

Davidse et al. 11076 


(MO) 
Hoehne 19661 (RSA) 
Ramamoorthy 680 (MO) 


Feddema 2872 (MO) 
Croat 35428 (MO) 
Allen 713 (MO) 


Ecuador 
Peru 
Colombia 
Colombia 


Colombia 


Peru 


Peru 
Peru 
Bolivia 


Bolivia 

Venezuela 
Venezuela 
Venezuela 


Panama 
Costa Rica 


Chile 


Chile 


Brazil 
Brazil 
Brazil 
Chile 
New Zealand 
Brazil 
Brazil 


Brazil 


Mexico 
Costa Rica 
Costa Rica 


102 

107 

100, 105, 106 
94 

111, 155-157 

109, 110 

74, 75, 78, 84 

73 

82, 86, 87 


160-163 


83 


79-81, 164-167 
77 


1, 2, 168, 169 
3 


4, 5, 170-173 
17, 18 
19, 25 


31-33 
20-24, 175 


174 
34-36 


26-30 
16 


37—40, 191, 192 
41, 42 


193, 194 


38 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


TABLE 1. Continued. 


Sect. Skinnera 
F. cyrtandroides Moore 


F. excorticata (J. R. Forster & 
G. Forster) L. f. 


Carse 2312 (МО) 
Raven et al. 25212 


F. perscandens Cockayne & 
Allen 


F. procumbens Cunn. 


van Balgooy 1785 (MO) 


McMillan 65/91 (MO) 


(MO) 
Walker 4730 (MO) 
Cultivated Univ. of 


Tahiti 46, 49, 50, 
181-18 

New Zealand 43, 44, 51, 54, 
178, 180 

New Zealand 176, 177, 178 

New Zealan 45, 53, 186, 187 

New Zealand 47, 48, 52 

New Zealand 188-190 


California Botanical 
Garden, Berkeley 
UCB 49.812 (UC) 


gest that the starchy condition found in all re- 
maining genera may be derived. The geograph- 
ical distribution of Fuchsia could also be cited 
as evidence of its relative primitive position 
within the su паре ae it clearly centers in 
South America (wh e family almost cer- 
tainly originated; т k Axelrod, 1974; Ra- 
ven, 1979), with others in New ae 
and in Central America-Mexi 

Fuchsia is modally ий. largely be- 
cause of a combination of protogyny and spatial 
separation of anthers and stigma (Raven, 1979; 
Berry, 1982). In addition, male-sterility occurs 
in the sects. Encliandra, Kierschlegeria, Schufia, 
and Skinnera, and, together with female-sterility 
in most of the same species enforces outcrossing 
by dioecism, subdioecism, or, in two species of 
sect. ali by gynodio 

Advanced features in chus include those 
ameter with bird ролна o OE eval 
flowers—and bird dispersal of se 
These features make it very шше ы = 
with the characteristics of Fuchsia could have 
evolved before the Eocene (Raven, 1979; Suss- 
man & Raven, 1978), whereas the known fossil 
record of the family extends back to the upper- 
most Cretaceous (Eyde & Morgan, 1973). The 
2-aperturate pollen of most species of Fuchsia is 
unique in Onagraceae and nearly so in all of the 
Myrtales, and is a clearly derived feature. The 
nine sections of Fuchsia may be summarized as 
follows: 

Sect. Ellobium consists of three species in 
Mexico and Central America formerly assigned 
to sects. Fuchsia and Hemsleyella (Breedlove et 
al., 1982). Sect. Ellobium combines character- 


istics of each of these basically South American 
sections, having petals as in sect. Fuchsia and 


gave rise to these 
Sects. Е ncliandra ( ао 1969), Jimene- 
,and 5 опе, and two species 
respectively, ‘and occur in Mexico a 
he presence of small ае, lobed- 


ч 
~. 


шл саа and smooth viscin threads sug- | 


gest a common ancestry (Berry, 1982), as does 


the geographical proximity of these sections. All | 
nine species are diploid, with n = 11 (Breedlove, _ 
1982). Sect. Schufiacan | 
be easily distinguished from all other species of 


1969; Breedlove et al., 


Fuchsia by the large, many-flowered, terminal 
panicles in which the small flowers have stamens 
exserted beyond the floral tube. These three sec- 
tions apparently represent an earlier invasion of 
Central and North а than that which рауе 
rise to sect. Ellobiu 


Sect. Fuchsia disi 61 species, 59 from thè | 


tropical Andes of South America, and the other 
two in Hispaniola (Berry, 1982). This is the only 

ion with annular nectaries in all but three 
species. The flowers have petals, in contrast 10 
those of the sympatric sect. Hemsleyella, and the 
floral tubes are longer than the sepals, F. verru- 
cosa excepted. Of the 43 species in sect. Fuchsia 
for which chromosome numbers have been ге- 
ported, 37 were diploid with n = 11, five were 
tetraploid with n — 22, and one included both 
diploid and tetraploid individuals. 


Sect. Hemsleyella, the second largest with 14 
species, is found in the tropical Andes, as is sect. | 


(Мог. 71 | 


bI 


1984] 


Fuchsia. It differs from the latter by the absence 
of petals and its adaptations to a largely epi- 
phytic habitat: tuberous stems and dry-season 
flowering and leaf drop (Berry, 1982). In fact, 
most herbarium specimens of sect. Hemsleyella 
lack leaves. Some species are polyploid (Berry, 
unpubl. data). 


Sect. Kierschlegeria has a single species, the 
only one in the genus to occur in a seasonally 
dry habitat (Berry, 1982). Fuchsia lycioides has 
small deciduous leaves, spinose leaf bases, and 
thick seed coats, characteristics associated with 
xerophytic conditions. The flowers are small and 
solitary in the axils of leaves on (mostly) un- 
branched, peculiarly straight stems. It is sub- 
dioecious (Atstatt & Rundle, 1982). Like sect. 
Quelusia, it is tetraploid and has 3-aperturate 
pollen. 

Sect. Quelusia exhibits a common pattern of 
disjunct distribution, seven species in southeast 
coastal Brazil, and an eighth, the widely culti- 
vated F. magellanica, in the southern half of 
Chile and ойт, мп the western slopes of the 
Andes in Argentin 
all have 3- Palen. pollen. 

The four species of sect. Skinnera are the only 
representatives of the genus that occur in the Old 
World, three in New Zealand and one in Tahiti. 
These species are characterized by reduced pet- 
als, band-type nectaries, and the smallest and 
most ni the genus. It s likely 
that sect. Skinnera separated in Paleogene time 
from the ancestral stock, as judged from fossil 
evidence and the time needed to produce the 
present diversity in habit among the three New 
Zealand species, one a creeper, the second a liana, 
and the third a tall forest tree (see discussion in 
Berry, 1982). 

This paper is intended to be a companion re- 
port to Praglowski et al. (1983), which comprises 
a survey of Fuchsia and Ludwigia pollen using 
predominantly light microscopy. 


Jr 


MATERIALS AND METHODS 


Anthers were removed from herbarium spec- 
imens; all material for LM and Me а асе- 
man eri Samples! for! SEM were either sputter 
or vacuum coated with gold and examined wit 
an ISI Super II, a Cambridge Stereoscan MK Ila 
and S410, or a Coates and Welter 106B Field 
Emission Microsc scope 

The species ت‎ collection data, and fig- 


NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 39 


ure number(s) are given in Table 1. Most of the 
collections used in this study were also reported 
in Praglowski et al. (1983), and there are pre- 
sented both illustrations and extensive pollen 
morphological data on all collections. Althou 
virtually all of the collections cited in the earlier 
study were examined for this report, not all spec- 
imens are illustrated here, either because of closely 
similar morphology (especially in sect. Fuchsia) 
or because they were illustrated already in Prag- 
lowski et al. (1983). 

For TEM, pollen samples were acetolyzed or 
rehydrated (unacetolyzed). In the former, the res- 
idue was incorporated into agar, dehydrated 
through a graded acetone series and embedded 
in Araldite-Epon resins. Prior to incorporation 
in agar, the pollen was stained in 1–2% OsO, 
buffered with sodium cacodylate at pH 7.2-7.4 
for 1-2 hours at room temperature. Unaceto- 
lyzed pollen was rehydrated by Alcian blue 
(Rowley & Nilsson, 1972) or by softening in Vat- 
sol (Pohl, 1965), soaking for 2-3 days in 2.5% 
sodium cacodylate buffered (pH 7.2) glutaral- 
dehyde. Dehydration and embedding follows that 
described above, except that agar was not used. 

Sections approximately 10 nm thick were cut 
with diamond knives, collected on uncoated cop- 
per grids, and stained for 5 minutes each in 0.5% 
aqueous uranyl acetate and lead citrate, or in 
rehydrated pollen only in lead citrate. Ober- 
either a Philips epe 200 or ien 10 electron 
microscope at 40 k 

The terms for uM elements that are used 
in the palynological description of Fuchsia in this 
paper are documented elsewhere (Praglowski et 
al., 1983). 

Light slides of all samples are deposited at the 
Palynological Laboratory, Department of Bota- 
ny, Smithsonian Institution. 

RESULTS 

Mature pollen of Fuchsia is shed as monads, 
is paraisopolar to heteropolar, 2-aperturate and 
bilaterally symmetrical (Figs. 1, 7, 10, 13, 37, 40, 
41, 43-48, 55, 58-61, 64, 73, 74, 79, 82-86, 88- 
92, 103-107, 109, 112-114), or, more rarely, 
3-aperturate and radially symmetrical (Figs. 4, 
16-21, 33-36, 76, 108, 180, 181). 

SHAPE 

The shape in polar view is + elliptic in 
2-aperturate grains (e.g., Figs. 1, 10, 40, 59, 89, 
92, 109, 114), or triangular in 3-aperturate grains 


40 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


(e.g., Figs. 4, 17, 19, 20, 36, 76, 108). The shape 
in aperture-centered equatorial view is + ovoid 
in 2-aperturate grains (Figs. 85, 86, 103, 105), or 
apiculate in 3-aperturate grains (Figs. 18, 21). 
The shape in mesocolpus-centered equatorial 
view is + apiculate in both 2- and 3-aperturate 
grains (Figs. 34 uppermost grain, 43, 55, 58, 84, 
104, 106). 


APERTURES 


The apertures protrude and are formed by a 
cone-like extension of the exine (Figs. 35, 93, 
122; 128, 132, 136, 143,159, 171, 176, 175 191, 
193). The endoaperture is complex and consists 
of a massive deposition of endexine in the form 
of ring(s). The chamber-like ares delimited by 


y and by the ec- 
toaperture (see below) distally, has been desig- 
nated as the vesti kiet al., 1983). 


At the base of the cone ‘and | partially extending 
into the body of the grain the endexine is coarsely 

ular; within the vestibulum it is also finely 
channeled (Figs. 119, 122, 128, 132, 136, 143, 
155, 163, 171, 174, 176, 177, 188, 191, 193). 
The ectoaperture is irregular in shape (Figs. 38, 
51, 85, 86, 103, 105), only rarely a well-defined 
pore (Figs. 28, 93) ora "а horizontally-oriented col- 


Rare 
us. Kare 4 


22 in the 3-aperturate sect. Quelusia, dad 
n F. inflata 
(uit. пи. and F. Роси F. ех- 
corticata (Fig. 180), and F. cyrtandroides (Fig. 
181) of sect. Skinnera, which is characterized by 
2-aperturate pollen. 


EXINE 


The exine is distinctly bizonal (cf. many ex- 
amples illustrated in Figs. 115-194), composed 
of ektexine and endexine. The ektexine consists 
ofan outer spongy o or paracrystalline- “beaded sA 


er without 


umellae, and f foot layer components. The sei 
ine is the mostly solid and continuous layer. The 
inner surface is finely granular in the body of the 
grain and very coarsely granular and/or lamellate 
within the apertures (see numerous examples in 
Figs. 115—194). The two exine layers are closely 
associated with one frequently appearing to ex- 
tend into the other (e.g., Figs. 121, 124, 125, 130, 
133-135, 138, 142, 149, 150, 160, 161, 168-170, 
172, 178, 179, 183, 186, 189, 192, 194). 
Sculpturing of the ektexine consists of ele- 
ments which are primarily globular or irregular 


spheres (Figs. 2, 3, 14, 15, 27, 30, 53, 54, 57, 95, 
98-102, 126, 147, 182), or elongated units (Figs. 
56:36; vie ње 70-72, 129). Sometimes the 
elements w iti 
to pues ; d. e., Fig. 144). 


VISCIN THREADS 


Viscin threads are extensions of the ektexine _ 


(Figs. 126, 130, 138, 141, 142, 144, 145, 147, 
152,153,158-161, 164, 172, 178, 179, 182,183, 


186, 190, 192). While they are usually located - 
near or about the central region of the proximal | 


face (Figs. 1, 10, 17, 59, 73, 88, 89, 92, 109, 112, 
114, 181), they have also been noted to or on, 
the apertural protrusion (Figs. 141, 145, 188, 
190). In freshly collected or rehydrated pollen, 
the viscin threads are enclosed by a membrane 
(Figs. 117, 152-154, 164-167, 172, 173, 178, 
192). Threads are mostly segmented-beaded (Figs. 
9, 12, 14, 15, 22-27, 52-54, 75, 87, 94—97, 101, 
102, 117, 153, 154, 158-161, 165-167, 178, 182- 
187, 190) to segmented-ropy (Figs. 57, 98-100, 
126, 147), or less commonly smooth (Figs. 2, 3, 
5, 6, 31, 39, 42, 49, 50, 62, 63, 65, 66, 69-72, 
110, 111, 123, 130, 131, 138-141, 144, 145, 157, 
173) 

In some species it is difficult to recognize the 


morphological pattern and the threads consist of | 
both smooth and segmented portions (see, for _ 
ntation | 


— Е. ravenii, Fig. 71). 1 
F. cyrtandroides, Figs. 49, ‚ 50, 182, 185; F. 

Brest du Fig. 187) characterizes some species 
and usually requires supporting evidence from 
y (Figs. 183, 184, 


o 


e 


186). 

Localized distenti tribute to thread 
morphology. One type, illustrated by F. cyrtan- 
droides (Fig. 50) and Е. verrucosa (Fig. 1 11) shows 
inflated bases and results from several threads 
originating from the exine surface within a con- 
fined area. This is common throughout Onagra- 
ceae, most notably in Epilobium (Skvarla et al., 
1978). Another type is that of nodular disten- 
sions along the threads (e.g., F. coccinea, Fig. 31; 
F. cyrtandroides, Fig. 49), which probably rep- 
resents a “rolling up" of certain thread regions. 
Threads characterized by nodular or “‘ball-like” 
distensions are usually associated with the more 
complex compound threads of Epilobium and 
Boisduvalia. The last type of distension occurs 
on smooth threads and appears cylindrical. This 


is observed on most smooth threads throughout 
) É 


the family (Skvarla et al., 1978 


1 and therefore difficult | 


1984] 


TABLE 2. Pollen morphology in Fuchsia. 


NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 


41 


Number of Pollen € 
Species in Aper- Ekte 
Sections Section tures Берге Viscin Threads? 
Ellobium 3 2 globular-type segmented-beaded . 
Encliandra 7 2 elongated smooth, sparsely segmented 
(segmented-ropy) 

Fuchsia 61 2 (3) globular-type^ segmented-beaded* 
Hemsleyella 14 2 (3) globular-type segmented-beaded 
Jimenezia 1 2 globular-type ooth 
Kierschlegeria 1 3 elongated smooth 
Quelusia 8 3 globular-type segmented-beaded 
Schufia 2 2 globular-type 
Skinnera 4 2 (3) globular type segmented-beaded 


Term for viscin ге errs rics follows Skvarla et al. (1978). 


В но ted іп F. v 
* Smooth in F. citm 


The pollen morphology of the sections of 
Fuchsia is characterized briefly as follows, and 
summarized in Table 2: 


Sect. Ellobium (Lilja) Breedlove, Berry & Raven. 
Figures 7-15, 115-117. 
Three species, Mexico and Central America. 
Pollen was similar, 2-aperturate with a glob- 
ular type ektexine sculpture and segmented- 
beaded viscin threads. 


Sect. Encliandra (Zucc.) Endl. Figures 55-72, 
118-150. 

Seven species, Mexico and Central America. 

Pollen of sect. Encliandra was predominantly 
2-aperturate with an elongated type of ektexine 
sculpture. Viscin threads in this section were pri- 
marily smooth (Figs. 65, 66, 69, 71, 144), al- 
though sparsely segmented (Figs. 62, 63, 67, 68, 
70-72), and келел н (Figs. 57, 147) 
threads were also comm 


Sect. Fuchsia. Figures 88-114, 151-161. 

Sixty-one species, tropical Andes and Hispan- 
iola. 

Almost all species examined in sect. Fuchsia 
had similar pollen: 2-aperturate (Figs. 88—92, 
103-107, 109, 112-114) with globular type ekt- 
exine кише апа segmented-beadeg viscin 
threads, d best at high 
magnification ( x 15,000), Figures 100-102. One 
collection of Fuchsia corollata, Berry 3173, had 
predominantly 3-aperturate grain 

The type species for this section and thus for 
the genus is F. triphylla (Figs. 88, 94) endemic 
to Hispaniola, as is one other species F. prings- 
heimii (Fig. 89). Both are tetraploid, but have 


2-aperturate grains (for discussion, see Berry, 
1982: 37). 

Fuchsia verrucosa (Figs. 109-111) differed in 
thread type and ektexine sculpture. The threads 
were smooth and usually originated from a 

*whorled ам ры “899 the sculpture element i in the 
110), and 
more а а shaped in the ава col- 
lection (Fig. 111). Berry (1982) considered this 
species one of the most distinctive in the section 
on the basis of its short floral tubes, antesepalous 
nectary lobes, and tetraploidy with 2-aperturate 
pollen grains. 


Sect. Hemsleyella Munz. Figures 73-87, 162— 
167. 


Fourteen species, tropical Andes of South 
America. 

Pollen of all species of sect. Hemsleyella was 
similar: predominantly 2-aperturate, segmented- 
beaded viscin threads and with a globular type 
sculpture element. In one collection of F. inflata, 
Berry & Aronson 3012 (Fig. 76), approximately 
three-fourths of the grains were 3-aperturate. An 
equatorial ridge appeared particularly pro- 
nounced in some species of sect. Hernsleyella, 
e.g., F. tillettiana, Figure 79 (see Praglowski et 
al., 1983: 5). 


Sect. Jimenezia Breedlove, Berry & Raven. Fig- 
ures 1—3, 168, 169. 

One species, Costa Rica and Panama. 

Pollen of F. jimenezii was 2-aperturate with a 
globular type sculpture and smooth viscin threads 
that can be single or compound. In this species 
the viscin threads originated over a wide area of 
the proximal surface 


42 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


Sect. Kierschlegeria (Spach) Munz. Figures 4-6, 
170-173. 

One species, coastal Chile. 

Pollen of F. /ycioides, a tetraploid species, was 
3-aperturate with an ektexine that had an elon- 
gated element sculpture and smooth viscin 
threads. 


= Quelusia (Vand.) DC. Figures 16-36, 174, 
173. 


Eight species, SE coastal Brazil, Chile, and Ar- 
gentina 

Pollen of sect. Quelusia was 3-aperturate (Figs. 
16, 17, 33-36) with a globular type of ektexine 
sculpture. Rare 4-aperturate grains were noted 
(Fig. 32). The viscin threads were segmented- 
beaded (Figs. 22-27, 29, 30). In F. coccinea (Fig. 
31) the threads were only slightly segmented and 
had nodular distensions (see also F. cyrtan- 
droides, Fig. 49). All species of this section are 
polyploid. 


Sect. Schufia (Spach) Munz. Figures 37-42, 191- 
194, 


Two species, Mexico to Panama. 
Pollen ofthe closely related F. arborescens and 
F. paniculata was ‘similar: 2-aperturate with a 


globular 
cin threads. 


R^. Skinnera (Forster) DC. Figures 43-54, 176- 


d smooth vis- 


Rs species, three in New Zealand and one 

in Tahiti 

The pollen of sect. Skinnera was 2-apertura 
(a few 3-aperturate grains in F. памте 
Fig. 181; F. excorticata, Fig. 180; and F. р 
cumbens) with a mostly globular type ind 
sculpture (slightly elongate in F. cyrtandroides, 
Fig. 50). A trend in viscin thread segmentation 
was evident: prominent segmented-beaded 
threads in F. excorticata (Figs. 54, 163, 164) and 
F. procumbens (Figs. 52, 190), less prominent 
segments in F. perscandens (Figs. 53, 186, 187), 
and light segmentation in F. cyrtandroides (Figs. 
49, 50, 182-185). At low-intermediate SEM 
magnifications (Figs. 49, 50) segmentation in F. 
cyrtandroides was not clearly evident and thread 
morphology appeared smooth (see Praglowski et 
al., 1983: 21). At higher SEM magnification light 
segmentation was evident in the threads (Figs. 
182, 185). These segments were better defined 
with TEM (Figs. 183, 184). 


DISCUSSION 


The most conspicuous variation in the pollen 
of Fuchsia is that of aperture number, which also 


[VoL. 71 


determines shape of the grain and the type of 


symmetry. Most of the species in the largest sec- | 
tion, sect. Fuchsia (Figs. 88-92, 103-107, 109, 


112-114) have predominantly 2- -aperturate | 


grains, as do the species of sects. Jimenezia (Fig. 
1), Ellobium (Figs. 7, 10, 13), Schufia (Figs. 37, 
40, 41), Skinnera (Figs. 43-48), Encliandra (Figs. 


55, 58-61, 64), and Hemsleyella e 79 74, 
79, 82-86). The entirely polyploid s 


lusia (Figs. 16-21, 32-36) and Kircher (Fig. | 
as аге 
| ione polyploid species in sects. joe and | 

eyella. In one collection of F. inflata (sect. 


4) are characterized by 3-aperturat 


Hemslevella) Berry & Aronson 3012, the ma- 
jority of the grains were 3-aperturate (Fig. 76). 
In many other plants the number of apertures in 


the pollen is affected by level of polyploidy. Ош - 


data (for the entire family) support this conten- 
tion: deviations from the standard 3-aperturate 
conditions—i.e., four or five—are found in poly- 
ploids. Warth (1925) reported that a single tet- 
raploid individual of sect. Encliandra had about 
50% 3-aperturate pollen in contrast to the con- 


sistently diploid and 2-aperturate condition of | 
ther 


Similarly, Berry (1982: 


Eam tb. if 3- 


pollen i in two of the six wholly or partly tetraploid — 


taxa of sect. Fuchsia 

The wide distribution of 2-aperturate pollen 
in diverse sections of Fuchsia, including the very 
distinctive and only Old World section, sect. 
Skinnera, would favor the hypothesis that the 
3-aperturate condition of a few species in the 
genus is directly associated with polyploidy and 
derived wherever it occurs. 

In F. lycioides (sect. Kierschlegeria), about 25% 
of the grains examined by Praglowski et al. (1983) 
were 2-aperturate, as were occasional grains of 
one sample of F. magellanica (sect. Quelusia). 
Most likely these examples represent reversions 
to the ancestral condition of the diploids from 
which the tetraploids were derived, rather than 
separate origins of a character that is otherwise 
unknown in the family. We may conclude that 
the common ancestor of all extant species of 
Fuchsia had 2-aperturate pollen 

The predominant е: exine sculpture in Fuchsia 
an type 


elements, и EY have varying degrees of distinc- 
tion, e.g., in Figures 2 and 3 (F. jimenezii) the 
elements protrude, some even appear to be dis- 
crete spheres, whereas in Figures 27 (F. regia) 
and 77 (F. tillettiona p elements appear more 

"submerged." This condition, globular-type ele- 
ments, is probably primitive for the genus. The 


P a == 


- 


1984] 


second sculpture type consists of elongated ele- 
ments and is illustrated best in Figures 5 (F. /y- 
cioides), 65 (F. microphylla subsp. hemsleyella), 
and 70 (F. obconica). In general, the six species 
of the advanced sect. Encliandra and the only 
species in sect. Kierschlegeria mainly have elon- 
gated exine elements. 

Judging from the data presented in this paper, 
as well as that of Skvarla et al. (1978), the viscin 
threads of Fuchsia are among the most copious 
in Onagraceae (Figs. 29, 75, 77, 78, 86, 96, 106, 
112) and their interpretation as extensions of the 
ektexine (Skvarla et al., 1978) is strikingly illus- 
trated (e.g., Figs. 130, 138, 141, 142, 145, 152, 
153, 158-161, 178, 179, 186, 190, 192). These 
threads hold large masses of pollen together, pre- 
sumably for more efficient pollination. The co- 
pious aspect of Fuchsia threads may be associ- 
ated with bird pollination. The fact that these 
threads maintain the pollen in masses even after 
acetolysis would substantiate their effectiveness 
in nature. As pointed out by Raven (1979), sparse 
development of viscin threads is associated with 
pollination by bees, which are actually concerned 
with gathering pollen as food. 

As shown in Table 2, segmented viscin threads 
are characteristic of most species of Fuchsia, and 
this is clearly the primitive condition in the ge- 
nus. Smooth viscin threads of the derived and 
presumably directly related sects. Encliandra, Ji- 
menezia, and Schufia, as well as those of the 
unrelated but still clearly derived sect. Kierschle- 
geria, clearly represent an advanced condition in 
these groups. There is a considerable amount of 
variability in viscin thread morphology in Fuch- 
sia microphylla (sect. Encliandra): one subspe- 
cies, F. microphylla subsp. hidalgensis (Fig. 126), 
had segmented-ropy viscin threads; while others, 
subspp. aprica (Fig. 123), hemsleyana (Figs. 64, 
130), microphylla (Fig. 66), and quercetorum (Fig. 
131), had smooth threads. 

In a recently published paper, Hesse (1982) 
described the development of viscin threads in 
Epilobium angustifolium and an unnamed species 
of Fuchsia. According to him, viscin threads de- 
velop in a granular matrix, and then the threads 
“approach towards” the microspores and “tend 
to fuse with the ektexine.” In all Onagraceae the 
viscin threads are attached on the proximal face 
near the pole. In the case of pollen that is shed 
as tetrads, it is difficult for us to visualize a mi- 
gration of threads between closely associated tet- 
rad members, and their subsequent attachment 
to the pole. 

The structure of the exine in Fuchsia and in 


NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 43 


most other Onagraceae (Skvarla et al., 1976) is 
unique within the angiosperms (Patel et al., 1984). 
The ektexine is not differentiated into tectum, 
columellae, and foot layer units; instead, it con- 
sists of a spongy or paracrystalline layer, which 
is united with the endexine at numerous points 
along the ektexine-endexine interface. This se- 
lected union (rather than a total union or blan- 
keting which would be expected in columellaless 
pollen) can result in a misleading impression that 
vestigial or incipient columtellac are present. 
These structural relat are clearly evident 
by perusal of many of the TEMs i in Figures 115- 
194 as well as in SEM of fractured pollen (see 
particularly Figs. 120, 129). The ektexine is rel- 
atively uniform within a grain, differing some- 
times in thickness between the distal and prox- 
imal faces (Praglowski et al., 1983; e.g., Figures 
115, 116, 124, 125, 145, 146, 189, 190), and in 
the degree of fusion of the spongy elements. Or- 
ganization of the spo 
suggests that some ektexines are more “com- 
plete" than others. For example, the ektexine in 
F. microphylla subsp. hidalgensis (Figs. 124, 125) 
seems to have more fused elements, hence more 
ektexine area than F. garleppiana (Fig. 162). Al- 
though this has certain validity, examination of 
the included TEMs (Figs. 115-194) will show 
that “completeness” or “incompleteness” of the 
ektexine will vary within the nine sections of 
Fuchsia and possibly even within species (com- 
pare TEM of subspecies of F. microphylla, Figs. 
121, 122, 124, 125, 128, 130, 132-134). The 
second exine layer, the endexine, is primarily 
massive and uniform. As mentioned elsewhere, 
the lower or inner margin is usually finely gran- 
ular throughout the pollen grain body, while in 
the aperture protrusions the endexine is extraor- 
dinarily channeled as well as being coarsely gran- 
ular. 
These results agree with previous work which 
considered the ektexine pattern of Fuchsia as 
having “tectum and columellae virtually indis- 
tinguishable" (Skvarla et al., 1976: 452). In this 
earlier study the ektexine pattern of F. micro- 
phylla subsp. quercetorum was described and il- - 
lustrated (p. 51 and pl. 1F) as having “tectum 
and columellae distinct." Reexamination of this 
taxon clearly shows that the **columellae" were 
enhanced because the sectional view was exactly 
at the junction of the exine and cone-like aper- 
ture protrusion. Therefore, it is now more ap- 
prie to recognize this exine layer simply as 
ektexin 

In che pollen of Fuchsia, two characteristics 


25 ANNALS ОЕ THE MISSOURI BOTANICAL GARDEN [VoL. 71 


FiGu 1-3. Scanning electron тиим of Fuchsia sect. Jimenezia, Е. jimenezii.—1. Slightly oblique 
„ы view.—2. Ektexine with globular element коро е and smooth viscin threads. — 3. See legend of Fi 
2. The scale equals 2 um, unless otherwise indica 


FIGURES 4-6. Scanning electron зубе of Е. мша» ea Kierschlegeria, Е. lycioides. —4. Distal polar 
view. — 5. Ektexine with el h viscin threads. —6. See legend of Figure 5. The 


scale equals 2 um, unless indicated. 


NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 


FIGURES 7-12. Scanning electron micrographs of Fuchsia sect. Ellobium. 7-9. F. decidua.— 


Lo 
fication of group.—8. Ektexine with globular-elongated element sculpture. — 9. ented viscin threads. 10- 
12. F. fulgens.—10. Proximal polar view illustrating thread attachment.—11. See legend of Figure 8.— 12. 
Segmented viscin threads. The scale equals 2 um, unless indicated. 


46 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Vor. 71 


FiGURES 13-15. ae electron micrographs of Fuchsia sect. Ellobium, Е. splendens. — 13. Slightly oblique 
r view.—14. Proximal pole with attached threads.— 15. Exine fracture illustrating spongy ektexine and 
massive, solid des The = equals 2 um, unless indicated. 


2 
шщ 
Q 
24 
< 
о 
У 
< 
Ы 
Z 
< 
= 
О 
& 
z 
= 
О 
N 
a 
= 
щ 
I 
= 
ш. 
о 
M 
Я 
< 


NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


Q- = 


FIGURES 37—42. Scanning electron pectin of Fuchsia sect. Schufia. 37—40. Е. arborescens.—37. Sli m 
oblique polar view.—38. P —39. Sm 


n 


Pore with ragged mar ooth о Shae cs segmented (?) I leues W: 
an ektexine sculpture of both globular and dorse elements. view. 41, 42. F. paniculata. A 
Slightly oblique view.—42. See legend of Figure 39. The scale nr 4 p iieri indicated. 


E 


FIGURES 31-36. Scanning electron micrographs of Fuchsia sect. Quelusia. 31-33. F. coccinea.— 
— viscin threads showing localized nodular distensions (see also 


Fig. 49).— 
ghtly oblique polar view. 34-36. F. г 


—3l. Se 

—33. Sli га. — 34. Group of 3-ape rturate grains.—35. Equ 
Made, note thickened endexine around endoapertures. — 
um, unless indicated. 


36. Slightly oblique polar view. The scale nies 10 


NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 


FIGURES 43-48. Scanning ee micrographs of Fuchsia sect. Skinnera. 43, 44. F. excorticata. ln Me- 
socolpus-centered equatorial view. — 44. Slightly oblique polar view. —45. F. perscandens, oblique polar 

46. F. cyrtandroides, mesocolpus- pers equatorial view. 47, 48. F. айне — 47. Slightly oblique ой 
polar Jew. —48. Slightly oblique polar view. The scale equals 10 y 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


FiGures 49-54. -m electron micrographs of Fuchsia sect. Skinnera. 49-50. F. rr —49. 
Viscin threads with various sized nodular di Voi (arrows).— 50. Ektexine at proximal pole with attachment 
of threads from infla “за hd n: elongated surface elements (arrows). Note that at this magnification 

о be mostly smo oth wi 


5, attachment са ийне нса. segmented visi 
oats wi перове ејетеп! sculpture. Sd, Е. С ѕее сосна of Figure 53. The scale equals | 


NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 


Е 


10 ип 


& 


FIGURES 55-60. Scanning electron micrographs of Fuchsia sect. Encliandra. 55-57. F. thymifolia subsp. 
thymifolia.—55. Oblique view.— 56. Ektexine with elongated element sculpture and sparsely segmented viscin 
threads. — 57. Ektexine with globular element sculpture and segmented-ropy viscin thread (see also Fig. 147 of 
F. thymifolia subsp. minimiflora).— 58. Е. obconica, slightly oblique equatorial view. 59, 60, F. encliandra subsp. 
encliandra.— 59. Proximal polar view.—60. Low magnification of group of pollen grains. The scale equals 2 um, 
unless indicated. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


64, 65. F. m 
gated elements and smooth threads. — 66. Е. microphylla subsp. оа ѕее sim of Figure 65. The scale 
equals 2 um, unless indicated. 


1984] NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 55 


FIGURES 67-72. Scanning electron micrographs of Fuchsia sect. Encliandra. Viscin threads. —67. F. су 
dracea, very sparsely segmented threads, with globular-elongated element sculpt ure.—68. F. thymifolia subsp, 
—69. F. 


thymifolia, very sparsely ке threads, with gl . encliandra su 
Ma smooth threads. — 70. F. obconica, segmented viscin threads, ektexine with globular element о. 

. Е. ravenii, viscin thread forked at exine surface and then inflated and smooth in area immediately 
зен other parts of thread are segmented-ropy (upper right corner).—72. F. cylindracea, sparsely segmente 
threads with elongated element sculpture. The scale equals 1 um 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


view.—74. Low magnifica of group.—75. Ektexine with g 
threads. — 76. F. inflata, nen pa oia (Berry & Aronson 301 ta 


jam, unless indicate 


NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 


© 


10um 


Mr tma 
p-— 


FIGURES 79-81. Scanning electron nie of Fuchsia sect. Hemsleyella, Е. tillettiana. — 79. Slightly 
oblique mesocolpus-centered equatorial view, equatorial thickening (see also Figs. 73, 74, 76) is very prominent.— 
80. Pore.—81. Ektexine with globular diria. element and segmented threads. The scale equals 2 um, unless 
indicated. 


ка 82-84. Scanning electron micrographs of Fuchsia sect. Hemsleyella.—82. Е. chloroloba, oblique 
iew. —83. Е. juntasensis, oblique view.— 84. F. apetala, mesocolpus- centered equatorial view. The scale equals 
m. 


58 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


FIGURES 85-87. Scanning electron micrographs of Fuchsia sect. Hemsleyella.—85. F. membranacea, aper- 
ture centered equatorial view, note elliptical shape of vestibulum. 86, 87. F. chloroloba. —86. Aperture- -centered 
uatorial view.—87. Ektexine with globular element sculpture and segmented viscin чер а The scale equals 

10 um, unless indicated. 


NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 


гит 93 


FIGURES 88—93. Scanning electron micrographs of F иса sect. Азыз —88. F. са ЕН grani 
proximal polar view.—89. F. pringsheimii, proximal polar view.— F. gehrigeri, oblique v aya- 
vacensis, oblique distal view. 92, 93. F. macrostigma. —92. Proumii polar view.—93. Aerie. ‘alin view. 
The scale equals 10 ит, unless indicated. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


"њи — 


— MÀ 


h 


FIGURES 94-99. Scanning weg micrographs of Fuchsia sect. Fuchsia. Globular element sculpture with 
segmented viscin threads.— 94. F. triphylla. kt. < hirtella.—96. Е. gehrigeri.—97. Е. cuatrecasasii.—98.- F. 
pallescens. —99. Е. petiolaris. The scale equals 


1984] NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 61 


Ficures 100-102. Scanning electron micrographs of Fuchsia sect. Fuchsia. Globular element sculpture with 
segmented viscin threads.— 100. F. tincta.—101. F. boliviana.—102. F. putumayensis. The scale equals 1 um. 


62 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


FIGURES 103-108. Scanning electron micrographs of Fuchsia sect. Fuchsia. 103-104. F. macrophylla. —10% 
ye сүнөт equatorial view, colpus slightly distorted.— 104. Mesocolpus-centered equatorial view. 105, 
106. F. t — 105. Aperture-centered equatorial view. — 106. Mesocolpus-centered equatorial view. — 107. E 
seabriuseuda Te grains held together by threads.— 108. F. по одане а 3-aperturate grain. The scale equals 10 


ль а 


64 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


, 
е. 


саз: 
: SY وو‎ м 
О >. 


~ #® 


S oai 5: 


JO P ox 
om. 


FIGURES 115-118. Transmissi f Fuchsi hat иу sect. Ellobium (Figs. 115-117) and 

sect. Encliandra (Fig. 118). All satin емна Ts 117. Е. splendens.—115. Section from approximately 

the middle of the distal polar face (at right) to the junction of the central auth and apertural protrusion (tapered 

part of the endexine at left).—116. Same pollen grain 1 1 i 

жо proximal), Note the comparatively thinner ektexine. — 117. Section through 
r 


1984] NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 65 


ektexine, the thick and massive-homogeneous-uniform part of the endexine, and the highly irregular lower 
gran е oo which is roughly equivalent to the large endexine granules in Figures 119 and 122. The scale 
equals 


66 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


hi 
protrusion. The acetolyzed exines of Fuchsia (Figs. 124, 125, 133-135, 137, 158- 162. 174, 179, 194) alway 
appear extremely opaque with both ektexine and endexine ри tely of equal electron density. In contrast 
the Agere exines (Figs. 115, 116, 118, 119, 151-154, 164-173, 175, 178, E -— the possible exception 
of F. rucosa (Figs. 155, 156) are стоне less dense. —122. Section of a ral protrusion, includi 4 
домена tef channel. Comparison of apertural protrusions in the acetolyzed | (Figs. 128, КЕ 136, 163, 1747 Ee 
us 193) and unacetolyzed (Figs. 119, 155, 171, 19 v 
n all structural features, although the highly channeled or honeycombed endexine i is more > clearly о 
ihor acetolysis. The scale equals 1 


| 
| 


67 
NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 
1984] 


i hs of Fuchsia 
issi i 124, 125) electron micrograp 4 
i ig. 123) and transmission (Figs. ‚54 : iew of this fractured 
seg d а 123. Е. microphylla subsp. aprica, p oe es ed да 
рое sect. л аф oarse globular elements of the apertural protrusion -— у садыш 124. Section near 
relatively smooth endexine af the central bye Eom ee : oye E pe һана from opposite face (either 
llen grain as in Figure А í ine. The scale 
e - Pe Nee sacra i сода component as well as slightly thicker ektexin 
polar or lateral). 
equals 1 um. 


68 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


pollen, sect. Е ncliandra, F. microphylla subsp. наета sis. Pollen acetolyze 6. Scanning electron micro- 


graphs of grou wW : 

thymifolia (see Figs. 56, 57 and Pl. 5, Fig. 1 of Skvarla et al., 1978) and F. thymifolia subsp. minimiflora ( 1B 
147) and which contrast with the smooth (Fig. 131) or beaded threads more typical of Fuchsia.— 127. S ection 
through a group of threads.— 128. Section through apertural protrusion but not including pore ог інг 
channel. The channeled endexine clearly underlies the vestibulum or aperture chamber. The scale equals ! ит. 


— a 


| 
| 


1984] NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 69 


FIGURES 129, 130. Scanning (Fig. 129) and transmission (Fig. 130) electron micrographs of Fuchsia pollen, 
sect. . Encliandra, F. microphylla subsp. hemsleyana. Pollen acetolyzed. — 129. Po rtion of a broken pollen grain 
he massive endexine 
ME sa highly irregular lower margin.— 130. Section through proximal surface M t an oblique view of a 
smooth viscin thread connected with t the ektexine surface. The scale equals 1 


70 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


FIGURES 131, 132. Scanning (Fig. 131) and transmission (Fig. 132) electron (норм of Fuchsia рођену 
. Pollen 131. Scan 


sect. Е ncliandra, F. microphylla subsp. quercetorum. Po acetolyzed.— ing electron micrograp ph o 
a great mass of smooth viscin threads. — 132. Somewhat oblique section through El protrusion. The scale 
s ] um 


1984] NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 44 


FiGures 133-137. Transmission electron micrographs of Fuchsia pollen, sect. Encliandra. Pollen acetolyzed. 
133, 134. F. microphylla subsp. quercetorum.—133. Section through middle of central body. Although the 


appears to be common for this taxon (see also Pl. 1, е et al., 
endexine is ы НЕ “ in this print the fractured ektexine was emphasized at the expense of the granular 


endexine.— 134, The е comments apply as discussed in ponen 135. 135-137. F. encliandra subsp. tetra- 
а — 135. Section. through middle of central body and somewhat oblique to the surface.— 136. Section 
hrough portion of the central body and apertural protrusion.— 137. Section near middle of central body. The 


iE of the кыы! as the top) pate with the section in Figure 135. The scale equals 1 um. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


FIGURES 138-141. Transmission electron micrographs of Poles pollen sect. Encliandra, F. encliandra 
subsp. encliandra. pu ара -— 138. Section through prox surface.— 139. Longitudinal section de 
parts of two smooth viscin threads. — 140. Section through a ping viscin threads with various orientatio 
= Somewhat ак дыны о, through proximal surface near region of aperture protrusion. The scale ан. 

pm. 


1984] NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 73 


FIGURES 142, 143. Transmission electron micrographs of Fuchsia pollen, sect. Encliandra, Е. obconica. 
is acetolyzed.— 142. View at proximal surface with prominently segmented viscin threads attached to exine 
ace.— 143. жср ес apertural protrusion and vestibulum but not including роге ог aperture channel. 

The scale equals 1 


74 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


nage ын Scanning (Fig. 144) and р (Figs. 145, 146) electron micrographs of Fuchsia 
pollen, se . Encliandra, Е. cylindracea. Pollen ac etolyzed. — 144. Smooth viscin threads are attached to the 
exine Saut apenas ng of slightly elongate r mie elements.— 145. Oblique view of proximal surface 
toward aperture protrusion with portion of a smooth viscin rd — 146. Same pollen grain section as Figure 
145 but of directly opposite distal surface. The s scale equals 1 u 


—— 


1984] NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 75 


FIGURES 147-150. Scanning (Fig. 147) and meom d (Figs. 148-150) of Fuchsia pollen, sect. Encliandra, 
Е. thymifolia subsp. minimiflora. Pollen acetolyzed.— 147. The segmented-ropy viscin threads and a coarsely 
iic surface are similar to F. thymifolia subsp. thymifolia (Figs. 56, 57).—148. Longitudinal section through 

gmented thread. — 149. Center of the proximal polar face.— 150. Same pollen section as Figure 149 but directly 
iso distal polar face. The scale equals 1 um. 


76 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


~ У 


enr e e+ glass 
el 2 
va Vy r^ x pw 


Figures 151-154. Transmission electron micrographs of Fuchsia pollen, sect. Fuchsia, Е. boliviana. А 
gure 15 
thinner.— 


1984) NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA TET 


pollen rehydrated.— 155. Oblique section to include just one apertural protrusion. — 156. Section through parts 
of two pollen grains bound together by pollenkitt or some other extra-exinous substance. Note the thicker 
concentration of granular endexine in the lower exine.— 157. Longitudinal section through a smooth viscin 
thread. The scale equals 1 um. 


78 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


vt . 
EEE 254 Bria eee 


“er 


EE 


5 161. Transmission electron micrographs - ped pollen, е Fuchsia (Figs. 158, 159) and 

e 2 F. hartwegii. — 158. Section along proximal: face 

reads and d surface. — 159. за s section along the proxim mal 
A thin basal granular endexine € component is comm 


160, 161. 4 is section the 
a is clearly seen to be an integral part of the viscin threads. — 161. = чер паре Mee agent 


Similar to Figure 160. The scale equals 


79 
NOWICKE ЕТ AL.—PALYNOLOGY OF FUCHSIA 
1984] 


i leyella, F. garleppiana. 
FIGURES 162, 163. Transmission electron micrographs of Fuchsia рохе “ ae мел er uen 
Pollen acetolyzed.— 162. High magnification of section through centra y. 
trusion. The scale equals 1 um. 


80 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


AO 


Ficures 164-167. Transmission electron micrographs of Fuchsia pollen, et. амаи ella, Е. tillettiana. 
All pollen rehydrated. — 164. Section at proximal polar surface. Note con spicuous membrane around threads ! 
all Гер! їп this plate.—165. pce section through four viscin threads. — 166. Cross M lion through â à 


1984] 


NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 


f Fuchsia жещ sect. Jimenezia (Figs. 168, 169) 
Transmission acis nee ae of Fu аа lass 
urface 


granular endexine. The dense fibrous material on the ektexine s 


Ficures 1 168- 170. 

and sect. Kierschlegeria (Fig. 170). All pollen rehydrated. 168, 169. F. jimenezii.— 
of central body. Note the e loosely form ul 

is a precipitate from staining.— 169. Section similar to Figure 115 in that the endexine is tapered at the junction 
of the apertural protrusion and central body. In this section the granular н ine component is not evident. — 
170. F. lycioides, section at middle of central body. The scale equals 1 и 


mm 


82 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


od |: 5, 
3 


FıGuRES 171-173. Transmission electron micrographs of Fuchsia pollen, sect. куйше spine d e 
All pollen rehydrated. — 171. Section through apertural protrusion with ора sm extending fro e central 
body (at bottom) through aperture channel and into the vestibulum o apertur e chamber. де =; ection at 
proximal polar surface showing at least six viscin threads in cross ома view.— 173. Longitudinal section 
of smooth viscin thread group along surface of the ektexine. The scale equals 1 и 


1984] NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 83 


FIGURES 174-177. Transmission electron EE: of Fuchsia pollen, sect. не (Figs. 174, 175) = 
sect. Skinnera (Figs. 176, 177). Acetolyzed (Figs. 174, 176, 177) and rehydrated (Fig. 175) pollen. 174, 175. 
magellanica.—174. Section of apertural protrusion (at left) and central body (at right). —175. This кон 
еп ргаіп 15 similar to the acetolyzed grain in Figure 174 except that the ektexine appears to be partially 
enclosed by a membrane (as noted for the viscin thread) and does not show any granular endexine. 176, 177. 
510 


· €xcorticata.— 176. This figure ан the following (Fig. 177) are sections of the apert protrusion at different 
levels In Figure 176 the hone е appears to line the aperture chamber, at least in part 
In this figure the section is сна л at mid-level through the center of the ape protrusion and shows the 


rtura 
pore area at the ektexine surface and the apertural channel through the e ~ Note apertural protrusion- 
central body junction (at right; also see Figs. 115, 169). The scale equals 


84 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


FIGURES 178, 179. Transmission electron micrographs of Fuchsia pollen, sect. Skinnera, F. excorticata. 
Rehydrated (Fig. 178) and срт ч 179) pollen.—178. Section through proximal polar face showing 
viscin thread attachment with ektexine.— 179. Section similar to Figure 178 and included for purpose of com- 
paring acetolyzed and кч) aie The very fine dense granules are probably ринде from osmic 
acid stain. The scale equals 1 ш 


1984] NOWICKE ЕТ AL.—PALYNOLOGY OF FUCHSIA 85 


182. F. cyrtandroides.—181. А 3-aperturate grain (compare with more common 2-a rturate grains in Figs. 46, 
49, 50).—182. Enlargement of proximal surface of Figure 181. Note faint but distinct lightly segmented nature 
of viscin threads. In Figures 180, 181 the scale equals 2 um; in Figure 182 the scale equals 1 um. 


86 ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL. 71 


FIGURES 
pollen, sec 


viscin threads is evident in some of the threads in the group attached to the ektexine (at right). In the a 
section of the thread cluster (at left) the segmented nature of the individual threads is not apparent. — 18 ' 
Longitudinal section clearly indicating seg 1 fthread.— 185. Group of threads from typical 2-aperturate 
grain showing their lightly segmented nature (compare with Figs. 49, 50, 182). The scale equals 1 um. 


1984) NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 87 


FIGURES 186, 187. Transmission (Fig. 186) and scanning (Fig. 187) electron micrographs of Fuchsia pollen, 
sect. Skinnera, F. perscandens. Pollen acetolyzed. — 186. Section through proximal face. The longitudinal section 
through the viscin threads indicates their light segmentation (see also Figs. 183, 184).— 187. A cluster of threads 
(approximately equivalent in section view to cross section of thread cluster in Fig. 183). Segmentation of the 
threads is extremely light. The scale equals 1 um. 


86 ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL. 71 


FIGURES 183-185. Scanning (Fig. 183) and transmission (Figs. 184, 185) electron micrographs of Fuchsia 
pollen, sect. Skinnera, F. cyrtandroides. Pollen acetolyzed.— 183. Section includes exine on distal (at bottom) 


viscin threads is evident in some of the threads in the group attached to the ektexine (at right). In the cross 
section of the thread cluster (at left) the segmented nature of the individual threads is not apparent. — 184. 
Longitudinal n clearly indicating seg 1 fthread.— 185. Group of threads from typical 2-aperturate 
grain showing their lightly segmented nature (compare with Figs. 49, 50, 182). The scale equals 1 um. 


1984 NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 89 
] 


x equites 


$5. 


Ё: > ~ ee E E T j J - & à 


FIGURES 191, 192. Transmission electron micrographs of Fuchsia pollen, sect. Schufia, F. arborescens. All 
pollen rehydrated. — 191. Section through apertural protrusion showing cytoplasm from central body extending 
through the aperture channel and into the aperture chamber. Note well-defined intine.— 192. Section at proximal 
polar face showing viscin thread attachment with ektexine. The scale equals 1 um. 


90 ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL 71 


FiGURES 193, 194. Transmission electron micrographs of Fuchsia pollen, sect. Schufia, F. paniculata. Pollen 


acetolyzed.— 193. View of apertural protrusion and a 
y. The scale equals 1 y 


portion of the central body.— 194. Section through cen ntral 


1984] 


clearly have taxonomic value, aperture number 
(two versus three) and viscin thread morphology 
(smooth versus segmented). By using a combi- 
nation of these features, most sections can be 
distinguished. Table 2 attempts to correlate these 
at the sectional level. 


LITERATURE CITED 


АтѕАТТ, Р. R. & P. RUNDLE. 1982. oe main- 
tenance vs. fruit production: partitioned repro- 
ductive effort in subdioeciou тни lycioides. 

—208. 


. 1983. Starchy and starch- 

less pollen in the —— Ann. Missouri Bot. 

Gard. 69: 748-7 

982: = اش د‎ evolution of 
ae). Ann. Mis 


· 1969. The systematics of Fuchsia 
sect. Encliandra (Onagraceae). Univ. Calif. Publ. 
Bot. 53: 1-69. 

‚ P. E. BERRY & P. Н. RAVEN. 1982. The Mex- 
ican and Central American species of Fuchsia Cr 
agraceae) except sect. Encliandra. Ann. Misso 
Bot. Gard. 69: 209-233. 

CARLQUIST, S. 1975. Wood anatomy of Onagraceae, 

with notes on alternative modes of үн 
movement in Core wood. Ann. Missou 
Bot. Gard. 62: 386—4 
ERDTMAN, G. 1966. mt Morphology and Plant 
axonomy: Angiosperms (An Introduction to Pal- 
ynology. I). Hafner Publishing Company, New 


ork. 

EYDE, R. Н. & J. T. MORGAN. 1973. Floral structure 
and evolution in Lopezieae (Onagraceae). Amer. 
J. Bot. 60: 771-787. 

Hesse, М. 1982 [1981]. Pollenkitt and viscin threads: 
their н in cementing pollen grains. Grana 20: 


145- 
HICKEY, : T . 1980. Leafarchitecture of Onagraceae. 


NOWICKE ET AL.—PALYNOLOGY OF FUCHSIA 91 


P. 69 in Abstracts of the 2nd International Con- 
gress of Systematics and Evolutionary Biology, 
Vancouver, Canada, dd 17—24, 1980. 
BURMA M., H. Lew 5 & Р. Н. КАУЕМ. 1962. 
nitosis in the Onagraceae. 
Amer. J Bot. 49: 1003- 1026. 
1943. 


Мом2, P. А. А revision of the genus aera 
(Onagraceae). Proc. Calif. Acad. Sci. ТУ 25: 1-138. 
РАТЕ, У. С., VARLA & P. Н. RAVEN. 458 


Pollen characters in relation to the delimitation of 
es. Ann. Missouri Bot. Gard. 71: (in press). 

PoHL, R. W. 1965. Dissecting equipment and ma- 
terials for the study of minute plant structures. 
Rhodora 67: 95—96. 

PRAGLOWSKI, J., Р. H. RAVEN, J. J. SKVARLA & J. W. 
МОМСКЕ. 1983. Angiospermae: agraceae Juss. 
Fuchsieae & Jussiaeeae. World Pollen and Spore 
Flora 12: 1-41. 

RAVEN, Р. Н. 1979. A survey of reproductive biology 
in E New Zealand J. Bot. 17: 575-593. 

. I. AXELROD. 1974. Angiosperm bio- 
Ee and past continental movements. Ann. 
sing Bot. Gard. 61: 539—673. 

ROWLEY, J. В. & S. NILSSON. 1972. Structural sta- 
bilization for electron microscopy of pollen from 
herbarium specimens. Grana 12: 23-30. 


SKVARLA, J. J., P . PRAGLOWSKI. 1976. 
Ultrastructural survey of Onagraceae pollen. Pp. 
447-479 in I. K. Ferguson & J. Muller (editors), 
The Evolutionary Significance of the Exine. Aca- 
demic Press, London. 
Е. ОЕ & М. SHARP. 1978. 
Ап ultrastructural ener of viscin threads 1 in On- 
agraceae pollen. Pollen & Spo: 
SussMAN, R. W. 1978. Pollination 
by lemurs and marsupials: an archaic coevolu- 
ionary system. Science 200: 731-736. 
WARTH, G. 1925. Zytologische, histologische und 
stammesgeschichtliche Fragen aus der Gattung 
Fuchsia. Z. Indukt. Abstammungs-Vererbungs. 28: 
200-257 


THE SIMPLE LEAVED LUPINES AND THEIR 
RELATIVES IN ARGENTINA! 


ANA MARIA PLANCHUELO AND DAVID B. DUNN? 


ABSTRACT 


Arguments are presented to support the thesis је к of lupines with a single blade аге as 


ated species with 
aureonitens, and L. multiflorus. 


The species of Lupinus are restricted to the 
New World, with the exception ofa limited num- 
ber in the Mediterranean region, and a few 
Africa, reviewed by Gladstone 1974, апа Pu 
mann (1981). The major speciation centers are 
in the montane western area ad North America, 
Mexico, and in the Andean region of South 
America: Пе simple-leaved lupines occur main- 
int f Brazil 


Four species were treated by Small ( (1933) as the 
Simplicifolii in Florida. Dunn (1971) contended 
that the four taxa of the complex originated in 
Brazil and reached Florida by long range dis- 
persal. 

The species treated in this paper are the only 
known biennial or perennial lupines in north- 
eastern Argentina that are related to lupines of 
Brazil, Paraguay, and Uruguay. Their floral or 
vegetative characteristics are not remotely sim- 
ilar to those of Andean lupines. The other three 
native species that grow in the area are annuals. 


DISCUSSION OF LEAF CHARACTERISTICS 
IN LUPINUS 


Different terminology has been used to de- 
scribe the mapie Wade oe о lupines. Whether 
they should be c ple-leaved or uni- 
foliolate has been an unresolved question. 


i 
e characteristics 
“leaves simple or жене ураа y in the same state- 
ment of the key, without any subsequent sepa- 
ration or explanation about the difference. How- 


! The work was a portion of ss problems encountered by A. M. Planchuelo (1978) in her doctoral dissertation 
at the University of Missouri-Columbia. | 

? Division of Biological uA University of Missouri-Columbia, 202 Tucker em = Missoufi 
65211. The au thors wi wish to express their appreciation to the curators of the herbari ted in the 


under the direction of D. B 


distributions. Wi 


a whereas L. 


ve all or some of their leaves simple. L 
paraguariensis has simple i 
ranch but the others are palmately compound. 


almately compound leaves are treated in this paper: L. albescens, І. 


ever, in the following genus, Crotalaria, he clearly 

separated simple-leaved species from unifolio- 

e defined “‘Simplicifoliae” as those 
» 1 Е 


E 


w petiole wi 
e“ “Foliolatae” are defined as having leaves with 
one to three leaflets, with the petiole articulate 
at the apex. 

Smith (1945) recognized 21 simple-leaved lu- 
pines for Brazil and referred to them as unifoli- 
ate. Burkart (1952, 1967) also used the term un- 
ifoliolate in his description of Lupinus. 

Hutchinson (1964), in the key to the tribe Lu- 
pineae, separated Lupinus by the characters 
“leaves simple, digitately several to many-fo- 
liolate or 1-foliolate.” Later in the description of 
the genus he stated Padi rarely digitately 3-fo- 
liolate or 1-foliolate." 

Polhill (1976) нола the leaves of Lupinus 

*5-1 1(-17)-foliolate or less often (in Central and 


only one genus, Lupinus) with “leaves 5-17-f0- | 
liolate, palmate, rarely simple." | 
This literature review shows that there is not | 
an unanimous opinion in the use of appropriate 
e to describe the simple-blade leaves 
of Lupinus. To resolve the problem, we studi 
the morphology of the leaves using the same cri- 
teria of the articulation or abscission of the pet 
iole introduced by Bentham (1859) in C rotalaria. 
The position of the abscission layer can rea ily 
bed d from old leaves of preceding yea’: 
The perennial species of Lupinus with digi- 


, the oo. oem ign «uta bein a possil 


P 


ANN. MISSOURI Bor. GARD. 71: 92-103. 1984. 


EN. Дд 


С ЖРТ 


пир" _ dí 


== 


1984] 


tately compound leaves commonly have the ab- 
scission layer at each petiolule or base of each 
leaflet, at the top of the petiole. In many species 
the petioles remain attached to the plant at least 
one year before finally weathering away. In other 
species the petiole is lost shortly after the fall of 
the leaflets, by a later abscission at the base of 
the petiole. In contrast, in the simple-leaved 
species of Lupinus, abscission occurs only at the 
base of the petiole or where the petiole becomes 
free from the fusion of the stipules. After ab- 
scission there is often a flange-like remnant re- 
maining at the node where the leaves from the 
previous year were attached. However, there is 
no visible indication of an abscission zone at the 
top of the petioles of the 18 species of simple- 
leaved lupines that we have been able to study 
from Brazil, Paraguay, and Argentina. There are 
several species that have completely lost the en- 
tire petiole, in which case there is an abscission 
below the sessile blade. 

We concluded from this study that the term 
unifoliolate is not appropriate for the genus Lu- 
pinus, hence, we considered the simple-blade 
leaves as truly simple. 

An interesting condition in L. paraguariensis 
shows a transitional stage between simple and 
compound leaves. The juvenile basal leaves from 
the caudex, and the first leaf produced on the 
lateral branches, are simple. The other leaves of 
the main stems and branches are digitately com- 
pound with three to five leaflets. The compound 
leaves do not show any sign of abscission zone 
at the base of the leaflet or at the top of the 
petiole, and the petioles do not remain attached 
to the plant as in other species. Lupinus para- 
guariensis is the only known species with the 
combination of simple and compound leaves in 
mature plants. 

We were able to obtain some viable seeds of 
L. albescens, and all of the seedlings in the colony 
we planted produced one simple elliptical leaf 
blade on the first leaf above the cotyledons. The 
second leaf had three leaflets, the third had five 
leaflets, and the number of leaflets increasd as 
the vigor of the seedling increased, until the typ- 
ical number of the mature plants developed, as 
cited in the section on taxonomy. We are con- 
fident that the same situation will occur in L. 
aureonitens and L. multiflorus, because they are 
morphologically closely related to L. paraguar- 
iensis. None of the North American lupines that 
we have grown experimentally have germinated 
with the first leaf simple. 


PLANCHUELO & DUNN—SIMPLE LEAVED LUPINES 93 


TAXONOMY 


Only the perennial or biennial species of north- 
eastern Argentina, adjacent Brazil, Paraguay, and 
Uruguay are treated in this paper (Fig. 1). There 
are three native annual species (L. bracteolaris 
Desr., L. linearis Desr., L. gibertianus C. P 
Smith) and three annuals sometimes cultivated 
(L. albus L., L. angustifolius L., L. luteus L.) in 
this area that are not included. The leaves in this 
group are simple or compound with well-devel- 
oped pinnate lateral venation. The plants are her- 
baceous and generally die back to a perennial 
caudex, with the exception of L. guaraniticus 
(Hassl.) C. P. Smith, which may become sprawl- 
ing and suffruticose. The stipules are well de- 
veloped in all of the species except L. guarani- 
ticus, in which the free tips are absent. The tapered 
base, as well as the absence of a gibbous base of 
the upper-lip of the calyx, is very similar in all 
of the species of this group, and sets them apart 
from the Andean lupines, in which the gibbous 
base is often well developed. The tooth-like tip 
of the wings and the conformation of the banner 
also suggest that the species in the group are 
closely related. 


KEY TO THE SPECIES 


la. Leaves all or some simple. 
2a. Leaves all simple. 
3a. Stipules with free tips absent; stems 
5 


flowers 13-16 mm long 

a Se guaraniticus 
. Stipules with free tips present; stems 
на оона shaggy-lanate; petioles 
m long; flowers 10-12 mm 

long 2. L. sellowianus 
2b. Leaves simple at the base of the plant 
and the first leaf of each lateral branch, 
the others palmately compound ..................... 

paraguariensis 


~ 
= 


1b. Leaves all compound 
4a. Wing tips rounded, without a tooth-like 
tip; keel angle over 90° ___. 5. L. multiflorus 
4b. Wing tips with an — tooth-like 
tip; keel angle 90° or les: 


5a. Leaves primaril eem stems with 


leaves gene t ets; 
leaflets complanat L. aureonitens 
5b. Leaves primarily cauline; stems 
erect, branching above; all leaves of 
mature plants with 5-12 leaflets, 
conduplicate . 6. L. albescens 


1. Lupinus guaraniticus (Hassl.) C. P. Smith, Sp. 
Lup. 325. 1943. (Fig. 2). L. attenuatus Gardn. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


94 
۱ ! 
t 
J Harto Grr орао 
~ 
x ۵ ~. ~ шер а, ce 
id 4 \ 
ГА. к ) 
LI 
' . l 
eS с ? 
Mo ù \ 
' мыр 4 X SUMA 
f ы: СА 
о. = У 
По om 
7 “u, Formosa ~ А • / 4 "en 
Де : 1 
Mr На e ~ y E 1 " 
^ ` 6 of 
: Chaco Y / , 
: IN 
' key] Је РА 
' ~» . US E 
. * è ‹“, 
i : ~ Misiones EER 
а э шай а НА 
Santiago а. ar m Santa Catarina 
del Estero: a d^ T Uis 
hare EI > 
Н 
LI 
rs is 
| ы 
iS 
' 


'e 


— 


1 Santa Fe 


ӯ 


ЧЕ 
-. 


Córdoba 


j 
BUS Бесе 


V 


L. guaraniticus 


Buenos Aires 
L. sellowianus 


V 


L. paraguariensis 


aureonitens 


L. multiflorus 


Eg + {> XxX © 
t 


L. albescens 


400 


$cale 1: 6,930,000 
0 100 2 300 


= i lometer 
60 55 50 


| 
d. | 
FIGURE 1. Distribution of the simple leaved lupines of Argentina and their relatives as listed in the lege? | 


1984] 


Lupinus guaraniticus (Hassler) С.Р, Smith 


PLANCHUELO & ООММ —SIMPLE LEAVED LUPINES 95 


17 
n 


ON 
M 
\ 


Illustration of typical structures of Lupinus guaraniticus. The floral and vegetative parts, with the 
Ppa дон te н реми у ак 


IGURE 2. 
exception of the leaf, are drawn to the scale shown from the mean 


lateral veins drawn from the lower surface view; inse 
stem structure showing the flange left after abscission 
no free portion present; W = wing petal. 


var. guaraniticus Hassler in Fedde, Repert. 
Spec. Nov. Regni Veg. 16: 158. 1919. TYPE: 
Paraguay. In fields, Alto Paraná, Fiebrig 5681 
(holotype, G; isotype, SI; photo, UMO). 


Plants perennial, 3-7 dm tall, several stems 
from a branched caudex; stems herbaceous, or 
becoming ligneous, suffruticose, hollow, 3-6 mm 
diam., sericeous, hairs of several sizes, tawny in 
age, the longest hairs 2-3 mm long, internodes 

-4 cm long; stipules with the free tip absent, 
connate portion sheathing half of the diameter 
of the stem; petioles 8-13 mm long; leaves sim- 
ple, entire, lance-elliptic, complanate at matu- 
rity, minutely strigose to thinly sericeous above, 

nely to densely sericeous below, the largest 
blades 7-9.5 cm long, 1.7-3 cm wide wit 
lateral veins on each side arcing forward, tips 


ber of ovules 
llustrates the thinly strigose hairs of upper surface; S = 
of the leaf; St — stipular portion fused to the petiole with 


Ca = calyx, cut at the left lateral sinus and 


drawn; L = typical leaf (not to scale), the 


acute to obtuse, the base as a narrow wing along 
the entire petiole, abscission of the leaf near the 
base of the petiole; peduncles 3.5—6.5 cm long at 
anthesis, sericeous; racemes 7-11 cm long, flow- 
ers scattered; bracts caducous, ovate, sericeous 
dorsally, 4-6 mm long, 2-2.8 mm wide at the 
base, tips attenuate; pedicels 2.5-3 mm long at 
anthesis, 5-6 mm long in fruit, sericeous; calyces 

riceous outside, glabrous within, base 
slightly or not gibbous above, lower-lip lanceo- 
late, 12-17 mm long, 3-5 mm wide, the пр trifid, 
central tooth ca. 2 mm long, 1 mm wide, the 
lateral teeth much shorter and curved outward, 
upper-lip 8—12 mm long, 3—4 mm wide below, 
bifid, the notch 2–3.5 mm deep, the lobes 1.5 
mm wide, lips connate 1.5-2.5 mm, bracteoles 
lanceolate, 2-3.5 mm long, 0.7-1 mm wide, at- 
tached 0.3–0.6 mm below the lips of the lateral 


96 


sinuses; corolla glabrous; banner oval-ovate with 

w, 12-15 mm long, 10-13 mm wide, 
appressed 2—4 mm, reflexed 10-13 mm, re- 
flexed/appressed ratio 3-5, the blade arching out 
and upward with the sides hardly reflexed; wings 
arcuate, 13—16 mm long, 5—6 mm wide, the claw 
1.5-2 mm long, the lobe above the claw poorly 
developed; Кее! arcuate, 3.5-5 mm wide in the 
middle, tip acute, curved backward; ovules 6-8; 
legumes 5.5-6.5 cm long, 9-10 mm wide, as- 
cending lanate; seeds 6–6.5 mm ime 4-5 mm 
wide, dark brown mottling and speckles on tan, 
funicular pit elongate, 2 mm long. 

T pecies is reported from grassy areas in 
open places or slopes from Paraguay, southern 
Brazil, and Misiones and Corrientes in Argen- 
tina. It is viewed as the most primitive species 
of those treated in this paper, due to the ligneous 
sprawling stems, which often persist more than 
one year: other species die back to a woody cau- 
dex or function as biennials. The lack of the free 
tips of the stipules places it out of the direct 
lineage to the other species treated here. 


Representative. specimens. ARGENTINA. COR- 
RIENTES: Santo Tomé, Ruta 40 y Arroyo Chimiray, 
poe coke e 10323 (CTES, MO, UC), Quarin 

02 (CTES). MISIONES: San Pedro, En la picada a La 
Сы. , Perrone s.n. (BA #54259, SI); San Pedro, 
Niederlein 1129 6. 

i, Fda. do Tigre, Hatschbach 
72064 (оу с ‘Clans Carat, ои 35482 (ВН, 
ES); Guarapua , Hatschbach 30851 


(UC); Lara ра 46 Sul, Hanks 4238, 4239 (US); 
Hatschbach 35213 (BH, CTES, MO, UC); Tibagi, Fda 
Mt. , Invernada Miranda, Hatschbach 2822 (US) 


RI DO SUL: Canabara, S Fr. de Paula, Rambo 
36207 (MO); Caxias do Sul, no Strede To V. Oli 
va, Valls 1431 (CTES); St. Loureuro Gom , Born- 
muller 325 (GH); S Angelo, S Joao Velho, Pedersen 
i ES, SI). SANTA CATARINA: Ag e, Cam 

s de о Smith & Klein ке Оз), "Curitiba. 
in Campo 11 km S о mith & Klein 
12202 (US), ске Alegre, Reitz & Е 5267, 6165 
(U 


PARAGUAY. Itaqugry, alto Parana, Fiebrig 5881 
ena аса alto Parana, Fiebrig 5681 (С, SI). 


2. Lupinus sellowianus Harms in Fedde, Repert 

pec. Nov. Regni Veg. 17: 5. 1921. TYPE: 

Brazil. Location unknown, Sello 4866 (ho- 
lotype, B, not seen) (Fig. 3). 


Plants perennial, herbaceous, seasonal stems 
arising from a subsurface root- Stalk; stems 2.5— 
4.5 dm tall, hollow, slightly fistulose, loosely 
shaggy-lanate, lower internodes very short, up- 
per 2-3 cm long, ridged from the veins of the 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


petioles, 3-6 mm diam.; stipules 2-4 cm long, 
free tips 1.5-2 cm long, caudate-attenuate to sub- 


simple, lanate on both sides, the blades of the 
largest leaves 8-11 cm long, 1—2 cm wide, small- 
er above, not abscissing from the petioles, with- 
ering in age and the petioles breaking near the 
base, without a clear-cut abscission layer, prom- 
inent lateral veins raised below, arcing out and 
toward the tip, 5-8 pairs; peduncles 4—6.5 cm 
long, lanate as stems, hairs 4—7 mm long; ra- 
cemes 10—20 cm long, flowers scattered to sub- 
verticillate; bracts lance-shaped, tips attenuate, 
caducous, 8-10 mm long, 2-2.8 mm wide below; 
pedicels 1-2 mm long, densely e lana 
calyces densely lanate outside, glabrous within 
except the margins of the lips, upper-lip bifid, 6- 
8 mm long, the notch 2.8-3.5 mm deep, lower- 
lip tridentate to trifid, 8-10 mm long, the teeth 
1.5-2.5 mm long, lips connate 2 mm, bracteoles 
lanceolate, 2-3 mm long, 0.6-1 mm wide; corolla 
glabrous; banner ovate to oval, slightly emargin- 
ate at the tip, with a short claw at the base, 9.8- 
11.6 mm long, 6.4-8 mm wide, reflexed 6-7 mm, 
appressed 4.3-5.5 mm, reflexed/appressed ratio 
1.3, the angle 120-135°; wings narrow, lower 
margin arcuate, tip pointed, weakly fused distally 
below the tip, 10.5-11.5 mm long, 3.3-4.7 mm 
wide, claw 1.5-1.8 mm long, tooth above the 
claw 1.4-2 mm wide; keel 2.5-3.4 mm wide in 
the middle, the angle 85—90°; ovules 4; legumes 
immature, 25 mm long, 6 mm wide, shaggy- 
anate. 


1 ta those 
тар imil ar LO шох 


he flo 

of L. multiflorus as well as the leaf venation and 
indument of vegetative parts. nos d is re- 
ported for the first time for Argen 

Smith (1945: 492) cited three E of L. 
sellowianus from the Berlin herbarium. One iS 
the type specimen Sello 4966, from Brazilia; the 
second is Dusen 13173, from Parana; the thi 
is Dusen 7261, from Espirito Santo, which was 
photographed by mistake as the type specimen. 
and the picture is filed in the New York herbar- 
ium. These three specimens were apparently de- 
stroyed by fire in Berlin in WWII 


Representative specimens. ARGENTINA. MISIONES 
Bernardo de Irigoyen, 7 km en camino a San Pedro 
Krapovickas et al. 23381 (CTES). 261 
BRAZIL. ESPIRITO decida Villa Velha, Dusen 7 M 
(photo NY); eiras a 3521 
(UC); Ponta гран 
PAULO: 5 Pedra Campos, e e 319 (RB 


o a 


1984] 


PLANCHUELO & DUNN—SIMPLE LEAVED LUPINES 97 


Lupinus sellowianus Harms 


FIGURE 3. 
own from the mean 


number of ovules drawn 


Illustration of typical structures of Lupinus sellowianus. The floral parts and the section of the 
о ale 5 fi values from dissections of specimens cited. B = banner petal 
Ca = calyx, cut at the left lateral sinus and opened to show the inside surface; F = lateral 


wn on the lower half; S = stem structure, first year growth, vascular traces from petiole above; St — 
1. 


surfa 
stipules, detached at the node (drawn to У of the scale shown); W = wing peta 


3. Lupinus paraguariensis Chodet & Hassler, 
Bull. Herb. Boissier, Ser. 2, 4: 836. 1904 
TYPE: Paraguay. Regione fluminis, Capi- 
bary, Hassler 4430 (holotype, G; isotypes, 
GH, LIL, MO, NY, UC; photos, F, GH, 
UMO) (Fig. 4). 


L. paraguariensis var. missionum Hassler in Fedde, 
Repert. Spec. Nov. Regni Veg. 16: 159. 1919. 
ТҮРЕ: Argentina. Misiones: fields near San Igna- 
cio, Hassler 445 (holotype, С). 

I3 eet (Hassler) C. P. Smith, Sp. Lup. 325. 


Plants perennial, possibly biennial, 4–8 dm tall; 
stems fistulose, 6-8 mm diam., appressed woolly 
pubescence to 5 mm long, with an undercoat of 
shorter hairs, internodes 2-8 cm long; stipules 
2-5.5 cm long, the free tips slender, 1.5-4.5 cm 
long, lanate; longer petioles 6-12 cm long, lanate; 
leaves simple at the base of the plant and the first 


leaf on each branch, the others 3—5 palmately 
compound, leaflets broadly elliptical to elliptical- 
oblanceolate, complanate at maturity, appressed 
lanate on both surfaces, the largest 10-13 cm 
long, 1.8-4.5 cm wide, midribs and pinnate lat- 
eral veins conspicuous, tips obtuse, mucronate; 
abscises near the base of the petiole or at the 
point where the stipules become free; peduncles 
4—7 cm long, lanate; racemes 12—30 cm long or 
little longer after fully developed, flowers scat- 
tered or subverticillate; bracts deciduous, nar- 
row, lanceolate, 8—15 mm long, 1–2.5 mm wide 
below, lanate dorsally, tips long-attenuate; ped- 
icels 2-4 mm long at anthesis, 6-7 mm long in 
fruit, lanate; calyces appressed lanate outside, 
glabrous within, except the tips and margins of 
the lips, lower-lip oblong, arcuate, 13-18 mm 
long, 4-6 mm wide, tips trifid, the teeth similar, 
1-3 mm long, 0.4–0.8 mm wide, upper-lip 9-13 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


Lupinus paraguariensis Chodet & Hassler 


FIGURE 4. 


Illustration of the typical structures of Lupinus paraguariensis. The floral and vegetative parts, 


except the leaves, are drawn to the scale shown, from the mean values of a set of multiple dissections, from the 


geographic range of the species 
не 


from specimens cited. В = banner petal flattened, dorsal view; Вг = bract, orsal 


= calyx, cut at the left lateral sinus and opened to show the inside surface; F = lateral view of the left 


side of the flower; K = 


the mean number of ovules drawn; 


, A о = 2 wi . 
L = leaflet and trifoliolate leaf (not drawn to scale), note leaflets often connected by lamina at base, petiole often 


with a wing; S = stems fistulose, with flanges left where leaves abscissed, in some areas they weather away; Wa 
i 1. 


wing peta 


mm long, bifid, the notch 3.5-6 mm deep, each 
lobe 2 mm wide, lips connate 2.5-3.5 mm, brac- 
teoles lanceolate, tips attenuate, 2.5—4 mm long, 
0 m wide, attached at the lips of the 
lateral sinuses, both lips elongating after fertil- 
ization; corolla glabrous; banner oval, 14—15 mm 
long, 10-13 mm wide, appressed 4.5-5.5 mm, 
reflexed 8-9 mm, reflexed/appressed ratio 1.8, 
the angle 113°, the top part arcing forward; wings 
13-15 mm long, 5-6 mm wide, the claws 2-3 
mm long, the lobe above the claws poorly de- 
veloped, the blade arcing upward distally as a 
broad blunt tip; keel 3.5-4.5 mm wide in the 
middle, the tip strongly hooked backward; ovules 
6-7; immature legumes to 4 cm long, 8 mm wide, 
densely shaggy-lanate; seeds not seen. 

The species occurs in southern Brazil, Para- 
guay, and Argentina. It is found in open areas or 
along river banks, and flowers in early spring. 
The similari "Pn 


га 1 4 +1 
1 


ty Oll UO OSC ОГ . на 
niticus and L. velutinus of Brazil clearly suggests 


that they are all related. The variety missionum, 
named by Hassler, represents only younger plants 
or those in less favorable ecological situations. 
Field studies are needed to verify this. 


arenal alto de Yatay-pony, Schinini & Ahumada 14 - 
do, Río Empedrado, ruta 12, 


CD int 
Carnevalli 3368 (CTES); Ituzaingó, Isla AP! Н 
Grande, Schinini & Vanni 15784 (СТЕ); Lavalle, » 
12, 7 km N de Enpalme con ruta 120, Tressens € 2: 
651 (CTES); Santo Tomé, Estancia San Juan Ba us 
Krapovickas et al. 26015 (CT 
Pu 


F); San Ignacio, Alrededores, РЕЈ 
sadas alrededores, Spegazzini 10 Г 
(BAF); San Ignacio, Hassler 445 (С, type of var. ie 
sionum), Muniez 114 (BAF); 5 km de San pec 
camino al Teyu-Cuare, Quarin 3477 (CTES); San 


[Von | 


оваа eS 


1984] 


y | 


W 


Lupinus aureonitens Gillies 


FIGURE 5. 
drawn to 
flattened, dorsal view; Br = brac 


PLANCHUELO & DUNN—SIMPLE LEAVED LUPINES 99 


specimens cited. B = 
yx, cut at the left lateral sinus and opened so tha 
i tiple sizes; K = keel petals, enclosing the 


Illustration of the typical structures of Lupinus aureonitens. The floral and vegetative parts are 
the scale shown from the mean values of the limited number of spec er pe 
1 ract, dorsal surface; Ca — cal 

inside surface shows; F — flower, left lateral view; H — stem hairs, m 


staminal tube and pistil, with the average number of ovules drawn; L — average largest leaflet (not drawn to 


scale), lateral veins of lower surface shown; S = stem structure, 


first year, varies to fistulose, vascular traces show 


on the internodes from the petiole above; St — stipule, detached at the node, not abscissing; W — wing petal 


vier, 11 km NE de San Javier, Krapovickas & Cristobal 
28870 (CTES). 

RAZIL. PARANA: Entrada Curitiba, Ponta Grossa, 
Proxima Rio Papagaio, Pereira 6112 (RB); Ponta 
Grossa, Parque Villa Velha, Hatschbach 8752 (RB). 
RIO GRANDE DO SUL: Sao Lepoldo, Leite 553 (NY). 

PARAGUAY. Condillere de Peribebui, Balansa 3109 
(BAF); Regione Fluminis, Yhu, Hassler 9498 (F, NY, 
UC); Sierra de Магасауй regione fluminis, Capibary, 
Hassler 4430 (F, GH, LIL, MO, NY, UC); Valenzuela, 
Rojas 12841 (BAF) 


4. Lupinus aureonitens Gilles in Hooker, Bot. 
Misc. 3: 201. 1833. TYPE: Argentina. Buenos 
Aires: Pampas near Cabeza del Tigre (K, not 
seen) (Fig. 5). 

L. purolantus C. P. Smith, Sp. Lup. 343. 1944. TYPE: 
Argentina. Buenos Aires: Sierra Tampé, Sierra de 
la Ventana, Lorentz 3 (holotype, US; isotypes, 
CORD, F). 


Plants biennial, or possibly sometimes annual, 


or a short lived perennial, 15—20 cm tall in fruit, 
branches mostly basal; stems ligneous and hol- 
low, 6-10 mm diam., densely soft subappressed 
to spreading lanate throughout all vegetative 
parts, tawny in age, longer hairs 5-7 mm long, 
with a dense undercoat of kinky hairs 2.5-4 mm 
long, upper internodes 1.8–3 cm long at fruiting, 
the lower not elongated; stipules 2.5-4 cm long, 
free tips 1.5-2 cm long, the lower ones imbri- 
cated for ca. 7 cm; petioles 5-8 cm long, persis- 
tent long after the leaflets drop; /eaflets 3-6, ob- 
lanceolate, mostly complanate, 4—6 lateral veins 
on each side of the midrib, hidden in the dense 
lanate hairs, largest leaflets 4—6 cm long, 8-18 
mm wide, tips obtuse, mucronate; peduncles 2- 
4 cm long; racemes 12-20 cm long in fruit, flow- 
ers scattered; bracts deciduous, densely lanate 
dorsally, lanceolate, tips caudate, 6 mm long, 2 
mm wide below; pedicels 2—5 mm long at ап- 
thesis, 6-8 mm long in fruit; calyces densely la- 


100 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Уог. 71 


nate outside, glabrous within except at the tips 
of the lips, lower-lip lance-oblong, 9-10 mm long, 
3-4 mm wide, tridentate, the central tooth 1.5 
mm long, 0.5 mm wide, the lateral teeth shorter, 
upper-lip 7-8 mm long, 4—5 mm wide, bifid, the 
notch 1.5-2 mm deep, the lobes 1.5-2 mm wide, 
lips connate 2.5-3 mm, bracteoles MES atten- 
uate, 3-4 mm long, 0.7-1 mm wide, attached 
0.5 mm below the lips of the lateral sinuses; co- 
rolla glabrous; banner oval-obovate, 3mm 
long, 8-12 mm wide, appressed 6–6.5 mm, ге- 
flexed 7 mm, reflexed/appressed ratio 1.1, the 
angle 120-135°, the tip bilobed, or entire, the 
teeth 0.5 mm long, 1 mm wide; wings 12-14 mm 
long, 5.5-6 mm wide, the tip ending as a lobe or 
tooth-like, the claw 2-2.5 mm long, the lobe 
above the claw 1.5-2 mm wide; keel 3.5-4 mm 
wide in the middle, the angle 85—88°; ovules 6; 
legumes 4-5 cm long, 8-9 mm wide, densely 
shaggy-lanate; seeds light tan, much dark mot- 
tling, 5 mm long, 4 mm wide, the funicular pit 
1.3-1.5 mm diam., angle mark not observed. 
The species appears more similar morpholog- 
ically to L. paraguariensis in many traits but has 


paraguariensis. The distribution is primarily 
south of Buenos Aires. The leaves with three 
leaflets are generally basal or the first leaves on 
the lateral branches. The reduction in the num- 
ber of the leaflets in the basal leaves suggests 
relationship with L. paraguariensis. 


Representative specimens. ARGENTINA. BUEN 
uus а Cerros, Grondona 8016 (BAA); С 
у Clavez, Hicken s.n. (SI #5883); General Vil- 
oor "Parodi 1 3385 (BAA, SI); Cabera 5694 (SI); Sier- 
ra Tam ierra dı 


Gomez et al. s.n. (BAA #11346). 


5. Lupinus multiflorus Desr. in Lam. т 

рейіа 3: 624. 1789. туРЕ: Uruguay. Моп- 

tevideo, Commerson (holotype, Р; Bowers 
and leaflets loaned) (Fig. 6) 


i пе Desr. 8. А Benth. in Mart., Fl. 
16. 1859. Tv nknown 

L aria e Desr. E tus Benth. in Mart., 

Fl. Brasil. 1: 16. 1859 (holotype, K; photo, UMO). 


Plants perennial, short lived, branching basal, 
with the leaves primarily basal, rosette at ground 
level when the primary raceme reaches anthesis: 
stems elongate some by fruiting, usually only the 
upper 2-4 internodes, 5-7 mm diam., hollow, 


somewhat ligneous in age, pubescence tawny in 
age, the longer hairs 2-4 mm long, appressed 


anthesis, 2.5-3.5 cm in fruit, three ridged from 
the veins of the petioles; stipules densely pubes- 
cent dorsally, sparsely pilose ventrally, 15-26 mm 
long, free tips narrowly triangular-subulate, 8- 

mm long, 2 mm wide, the lower ones imbri- 
cate; longest petioles 8-11 cm long, persisting 
into the second season after the leaflets abscise; 
leaflets 5-8, elliptic-oblanceolate, conduplicate 


appressed sericeous to sublanate below, with 4- 
6 lateral veins on each side of the midrib, visible 
after removing the hairs below, the largest 4-7 
cm long, 6-15 mm wide, tips acute, mucronate; 
peduncles 3-8 cm long, sericeous; racemes 8-25 
m long, flowers scattered; bracts deciduous, 
lance-caudate, 6-7 mm long, 1.5-2 mm wide, 
sericeous dorsally; pedicels 2 mm long at anthe- 
sis, 5-8 mm long in fruit, densely sericeous; ca- 
lyces densely appressed sericeous outside, gla- 
brous within, the base tapering into the pedicel, 
not gibbous, lower-lip lance-shaped, 8-11 mm 
long, 2-3 mm wide, tridentate, the teeth 1.5-2 
mm long, central largest, upper-lip 6-8 mm long, 
3 mm wide, bifid, the notch 1-1.5 mm deep, 
lobes 1-1.5 mm wide, lips connate 2 mm, brac- 
teoles lanceolate, 2.5-3 mm long, 0.5-0.8 mm 
wide, attached close to the margins of the lateral 
sinuses; corolla glabrous; banner oblong-ovate, 
12-16 mm long, 7.5-10 mm wide, appressed 6- 
7.5 mm, reflexed 5.5-7 mm, reflexed/appressed 
ratio 0.88–0.92, the angle 120-130*; wings 12- 
16 mm long, 5-7 mm wide, the claw 2-2.5 mm 
long, lobe above the claw ca. 2 mm wide; keel 
2.5-3.5 mm wide in the middle, the angle 95- 
105°; ovules 6-8; legumes 4—5.5 cm long, 7-8 
mm wide, subapressed sericeous to lanate; seeds 
5-6 mm long, 4-5 mm wide, tan with brown 
mottling, funicular pit 1.5 mm diam. 

e species occurs in Uruguay and Corrientes, 
Argentina, growing in sandy or gravelly soils. 
Only one specimen has been seen from Be d 
Th hi X "n ntin this 


O 


species, which is mostly sericeous. 


шшер ышын Ж specimens. ARGENTINA. pni 
ENTES: La Сп 9 (SE), Parodi 12548 (В 
GH). 


BRAZIL. SANTA CATARINA: Laguna, Hatschbach 272 05 


Uruauay. Colonia, Coll. unknown (ВАА #1047); 


а. ee анат р 


1984] 


у ћ values о 
Specimens cited. B = banner petal flattened, dorsal view; Br = 
ace; F = 
enclosing the staminal tube and pistil, with the mean number of ovules dra 


veins Prominent, distal third—upper surface; S = stem structure, first year growt 


PLANCHUELO & DUNN—SIMPLE LEAVED LUPINES 


Е bract, dorsal surface; Ca = calyx, cut at the left 
lateral view of the left side of the flower; K = keel petals, 
wn; L = average largest leaflet (drawn 
at У; the scale shown), lower portion —lower surface sublanate, middle portion—lower surface sericeous, lateral 


, vascular traces from petiole 
petal. 


forming ridges on the internode below; St — stipules, detached at the nodes; W — wing 


Florida, Cerro Colorado, Ea. San Pedro, Gallinal et al. 
Pérez, Herter 


(MO); Montevideo, Commerson s.n. (Р); Mon- 
tevideo, Barattini s.n. (MO #1224502), Berro 1902 
(BAF); Independencia, Osten 5632 (SE), Isabelle s.n. 
(F #153885, NY). 


6. Lupinus albescens Hooker & Arnott, Bot. 
Misc. 3: 201. April 1833. TYPE: Uruguay. 
Unknown, Baird s.n. (holotype, K; H-82/ 
77-7, only the two plants on the right side 
of the herbarium sheet) (Fig. 7). 


L. incanus Graham, Edin. Phil. Jour. 16: 178-179. 
Dec. 1833. 


L. parodianus C. P. Smith, Sp. Lup. 208. 1940. TYPE: 
Argentina. Buenos Aires: Isla Martin Garcia, Pa- 
rodi 2530 (holotype, GH; isotype, BAA). 


Plants perennial, herbaceous 3—6 dm tall, erect, 
ramose above; stems hollow, ligneous to fistu- 
lose, angular, 5-10 mm diam., the hairs yellow- 
ish brown, app d seri to sublanate, felt- 
like mat, longer hairs 2-3 mm long, with a dense 
undercoat of shorter hairs, upper internodes 2- 
7 cm long; stipules 10-30 mm long, shortest 
above, both surfaces densely pubescent, subu- 
late-caudate free tips 7-15 mm long, 1.5 mm 
wide below; /eaves primarily cauline; petioles 7— 


102 


SS 


Lupinus albescens Hooker & Arnott 


Ficure 7. Illustration of the typical structures of 
drawn to the scale shown, from the mean values of 
distribution of the species. B = banner petal flattened, 
1 = keel petals, ] 


several sizes; К. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


at the left lateral sinus and opened to show the inside surface; F = lateral view of the left side of the flower; 


[VoL. 71 


SS 
SF a 


Кы: 


Lupinus albescens. The floral and vegetative parts аге 
select specimens dissected from within the geographic 
dorsal view; Br = bract, dorsal surface; Ca = cal А 

mean number of ovules shown; 


h 
L 
stem structure, first year growt 
detached at the node; W = wing petal 


16 cm long, pubescent 


d z e. PA E 
season after the leaflets abscise; leaflets 5—12, 
, р lata A 14 + 1 + 4 age 


Е 


densely sericeous to sublanate on both surfaces, 
the lateral veins 4–6 pairs, visible below after 


tered; bracts caducous, ovate-caudate, 6-10 mm 
long, 2–2.4 mm wide, densely sericeous to lanate 
dorsally; pedicels 4–6 mm long at anthesis, 8-10 
mm long in fruit; calyces densely sericeous to 
lanate outside, glabrous within, the base not gib- 


— 


М р g p ‚ with t 
= average largest leaflet (drawn to % scale shown), lower half—lower surface, upper half—upper surface; S = 
h, vascular traces form ridges on the internodes below the petioles; St 


= stipule, 


bous above, lower-lip lanceolate, 7-10 mm long, 
2.5-4.5 mm wide, tip tridentate, the central tooth 
2 mm long, 0.6 mm wide, lateral teeth shorter, 
upper-lip 6-9 mm long, bifid, the notch 1.5-3.5 
mm deep, lips connate 1.5—2.5 mm, bracteoles 
lanceolate, 2-3 mm long, 0.8-1 mm wide, ab 
tached from near the lip to ca. 1 mm below the 
lips of the lateral sinuses; corolla glabrous; ban- 
ner obovate, 9-14 mm long, 8-11 mm wide, ЇР 
bidentate, the teeth 0.5 mm long, 0.8 mm wide, 
the angle 130-150*; wings 9.5-14.5 mm long 
4.5-6.5 mm wide, the tip with a small tooth-like 
lobe, the claw 2-3 mm long, lobe above the claw 
1.5-2 mm wide; keel 3—4 mm wide in the middle, 


1984] 


the angle 80-88°; ovules 7-8; legumes 6-8 cm 
long, 8-10 mm wide, densely sericeous; seeds 
5.8-6.5 mm long, 4.5-5.7 mm wide, sides con- 

x but seeds rather flat, generally dark brown 
to blackish, stippled and mottled with areas, oc- 
casionally more tan and buff than darker colors, 
funicular pit with large projecting rim, the pit 
oval 1.2-1.6 mm long. 

The species occurs in Uruguay and northeast- 
ern Argentina, where it grows in sandy soils and 
dunes. It is common near Paraná River and on 
islands. It appears to be the most common pe- 
rennial species in eastern Argentina. The erect 
habit clearly separates it from L. aureonitens, 
which also has a tooth at the tip of the wings. 

The Hooker Herbarium at Kew has three her- 
barium sheets (H82/77—6; Н82/77-7; H82/77- 
8) with plants labeled as L. albescens Hook. Only 
the H82/77-7 can be considered the holotype of 
the species because it specified “Banda Oriental, 
Baird," as Hooker and Arnott cited in the orig- 
inal description. The two plants and the leaves 
on that herbarium sheet are L. albescens, but the 
inflorescence in the left upper corner belongs to 
another species. 


Representative specimens. ARGENTINA. BUEN 
AIRES: Isla ín Garcia, Cabrera 2874 (SI), Parodi 
2526 (CTES), 2530 (BAA, GH). CHACO: 

Antequera, Krapovickas & Cristobal 20066 (CTES, 
GH); Isla Soto, Burkart 30853 (CTES, SE), Schinini 
16157 (CTES); Acceso al puente Manuel Belgrano, 
Schinini 16024 (CTES). CORRIENTES: Capital, Alrede- 
ores de la Ciudad de ER Alboff s.n. (NY); 

ente Pesoa, Fernandez 205 (CTES); Río Kinch 
Crovetto 11116 (CTES); Bella Vista, 10 km S of Bella 

Vista, Schinini & Ahumada 15918 (CTES, MO); Em- 
pedrado, “Las Tres M о Paraná, Pedersen 3049 


| ES, M 
Ituzaingó, Arbo et al. 2129 (CTES), Daciuk 4 (CTES), 
Holmberg 219 (51), Krapovickas et al. 24471, 24472 
(CTES), Meyer 6038 (GH, U), Spegazzini 10057 (SI); 
Villa Olivari, Schinini & Vanni 15663 (CTES); Paso 
de los Libres, Paso de los Libres, Burkart et al. 29917 
(CTES, SI); Laguna Mansa, Schinini 7604 (CTES, MO), 


PLANCHUELO & DUNN— 


SIMPLE LEAVED LUPINES 103 


7730 (CTES), Faggi et al. s.n. (BAA #13983, CTES); 
Goya, Goya, = 1510 (SI). ENTRE Rios: Federa- 
Burkart 28652 (SD, и (СТЕ); 8 
km N, oh a 22588 (SI). SANTA FE ital, San José 
del Rincón, Burkart 9056 (SI), Pio 244 1b, 3617 
(SD; Altoverde, Donnet 2088 (SI); Isla Timbé, en el 
cruce de balsa de Santa Fe a Paraná, Burkart et al. 
23699 (SI, UC); Isla Расага, frente a Ја capital, Boelcke 
& Correa 9103 (BAA, CTES); Rosario, Rosario, Bur- 
kart 8774 (F). 

PARAGUAY. Puerto Bartoni, alto Parana, Jimenez 
7884 (SI). 

URUGUAY. Colonia, Riachuelo, Cabrera 3938 (F); 
San José, Arazoti, LeGrand 1697 (SI); Soriano, Arenal 
Grande, Cabrera 257 1 (NY); unknown, Baird s.n. (K, 
#82/77–7, specimen on right only). 


LITERATURE CITED 
"e кы 1859. Leguminosae. Jn C. Martius, Fl. 
Bra: 


0- 
BisBv, F S Tribe 32, Genisteae. Рр. 409-425 in 
R. M. Polhill & P. H. Raven (editors), Advances 
in Legume Systematics. Royal Botanic Gardens, 


ew. 
BURKART, A. 1952. Las Leguminosas Argentinas Sil- 
biti y Cultivadas, 2nd edition. Acme Agency 


967. Leguminosas. Pp. 535—542 іп A. L. 


rapid speciation. Trans. Missouri Acad. Sci. 5: 26– 


GLADSTONE, Ls 
region of Africa 
Agric. 26. Моши. Australia. 
HOLMGREN, Р. & W. KEUKEN. 1974. Index Herba- 

riorum. 6th edition. Regnum Veg. 92: 1-397. 
HUTCHINSON, J. 1964. The Genera of Flowering 

Plants, Volume 1. Clarendon Press, Oxford. 
PLANCHUELO, A. M. 1978. A monograph of Lupinus 
for Argentina. Ph.D. dissertation. Univ. of Mis- 


1974. Lupines bes the Mediterranean 
echn. Bull. W. Austral. Dept. 


bia. 
1981. Evolutionary history of the old 
world lupines. Taxon 
иа В. M. 1976. Genisteae (Adans. ) Benth. and 
ted tribes (Leguminosae). Bot. Syst. 1: 143- 


1933. Manual of Southeastern Flora. 

t. Press, Lancaster, Pennsylvania. 

1938-1953. жазда арабдын Sig- 
5 1—44. Saratoga, California 


Pe 
SMALL, J. x 


Sci. 
-— шы Р. 


SYSTEMATICS AND REPRODUCTIVE BIOLOGY OF THE 
NTRAL AMERICAN SPECIES OF THE 
APHELANDRA PULCHERRIMA COMPLEX (ACANTHACEAE)! 


LUCINDA A. MCDADE? 


ABSTRACT 


Maie agi (Acanthaceae) is a neotropical genus of about 170 species of herbs, shrubs, and small 
trees. The A. pulcherrima comple x is a monophyletic group of about 40 species distinguished by the 
einer of bracteal nectaries and a unique неба morphology. Thirteen Central American species 
belonging to this complex are recognized based on herbarium, field, and greenhouse studies; pollen 
enin du and artificial hybridizations. The genus Aphelandra and the A. pulcherrima complex 
probably originated in South America. Central American species have evolved from South American 
or intermediate Central American ancestors. The species treated here are diffusely поема бе 
ог vate! ranched, monocaulous plants. They are found in primary forest to disturbed secondary 
and edge habitats, and from low to middle Lagann Field observations ee that all ји: 
BOR ie odorless flowers uns last a single day, produce copious, rather dilute nectar, and are hum- 
mingbird резне. All but 4. deppeana are чыка аз by large hermit ссы (Trochilidae: 
pers site rmitdike species. The long, decurved bills and traplining foraging habits of these 
birds co to ge floral morphology and spatial distribution of the plants. Chromosome data 
are not шигыре: д: useful within the group studied. АП 12 species for which counts were obtained 
have n = 14 chromosomes. The 13 species are variable palynologically, showing three distinct pollen 
types, as well as significant variability in pollen size (length and width). Pollen characters resolve all 
two species and provide evidence for patterns of phylogenetic relationships among the species. 
ids п many spe pair: i i ids i Ы 


PA о 

disturbance has apparently been important in creating situations favorable for hybridiza ation between 

at least one of these pairs of species. Phylogenetic analysis identifies two main lineages within the 

group: Group I (A. terryae, A. sinclairiana, A. storkii, A. gracilis, A. T буна c: A. panamensis, 

and A. deppeana) and Group II (A. lingua- bovis, A. leonardi i, A. laxa, A. campanensis, A. hartwegiana, 
and A. darienensis). These results are in accord wit th data from artificial hybridizations, except t that 


L whereas e indices suggest that these species are much more distantly related. Genetic 
пелена may be an important barrier to interbreeding between species of Group II such that 
the results of а hybridizations do not provide reliable estimates of the degree of relationship 
among these species. 


Aphelandra (Acanthaceae) is a morphologi- 160 species are confined to the New World trop- 
cally diverse genus traditionally distinguished by ics, ranging from northern Argentina and Bolivia 
its lack of cystoliths and possession of four to northern Mexico. Over two-thirds of the taxa 
monothecous anthers, bilabiate corollas, and are confined to South America with notable con- 
elongate, tricolpate pollen grains. The more than centrations of species in southeastern Brazil, Co- 


! This paper represents part of a dissertation submitted to Duke University. Field work in Central Ame erica 


was greatly facilitated by the Organization for Tropical Studies, the Smithsonian Tropical Research iste 
raduate ool Research award from Duke University, and nt 


Duke University. I thank the curators of the following herbaria for generous loan imens of Aphel ndra 
for my c As F, FSU, GH, TUS WIS. Ms. Sherri Herndon aided анау in all aspects 0 
m work. The assistance of s. rner, L. Eibest, and d i rious aspects of this 
work is раи appreciated. Paulette ы executed the drawings that appear in the comparative morphol 
section. The critical com on, J. Antonovics, D. E. Stone, R. L. Wilbur, J. С. Lundberg: 
L. H. Durkee, and T. F. Daniel are * gratefully acknowledged. I thank especially Dr. Donald Stone for = 
t. Publication of this paper was made possible 


by a grant from the National Science Foundation (No. BSR-830 03071). 
2 Department of Botany, Duke University, Durham, North Carolina 27706. 


ANN. MISSOURI BOT. GARD. 71: 104-165. 1984. 


1984] 


lombia, and Peru (Wasshausen, 1975). Thirty to 
40 species are found in Central America and 
Mexico 

јр has been treated in several region- 
al floras (Leonard, 1938, 1953, 1954; Gibson, 
1974; Durkee, 1978), and in a recent monograph 
(Wasshausen, 1975). Knowledge of many of the 
species and of phylogenetic relationships among 
species, however, remains fragmentary. Many 
taxa are known only from one or very few, fre- 
quently incomplete specimens, and data from 
field and experimental studies are essentially 
lacking. 

This study is a systematic investigation of the 
Central American species of the Aphelandra pul- 
cherrima complex. The complex is an apparently 
monophyletic assemblage of about 40 species. 
As treated here, 13 of these species occur in Cen- 
tral America. New data from several sources have 
been gathered: comparative morphology of liv- 
ing plants, field observations, chromosome 
counts, palynology, studies of floral biology, and 
artificial hybridizations. The taxonomic treat- 
ment is based on these data and portrays the best 
hypothesis for the phylogenetic relationships 
among these species. 


SYSTEMATIC POSITION AND 
TAXONOMIC HISTORY 


The Acanthaceae are a large, predominantly 
tropical family with about 250 genera and 2,600 
species (Long, 1970; Heywood, 1978). The fam- 
ily is pantropical with four centers of distribu- 
tion: Indomalaysia, Africa, Brazil, and Central 
America (Long, 1970). Whereas most acanth 
genera are restricted to one continent, a few are 
pantropical (e.g., Justicia, Ruellia). 

axonomists have almost unanimously con- 
sidered Acanthaceae to be closely related to 
Scrophulariaceae. These two families, along with 
Bignoniaceae, Lentibulariaceae, Gesneriaceae, 
Pedaliaceae, several other small families, and a 
varying group of families of disputed affinities, 
have usually been classified together at the or- 
dinal level (e.g., Scrophulariales: Stebbins, 1974; 
Takhtajan, 1969; Cronquist, 1968, 1981; Big- 
noniales: Thorne, 1976; Tubiflorae: Engler, 1964; 
Personales: Hutchinson, 1973). Although the 
phylogenetic relationships of all of these families 
have not yet been fully studied, it is likely that 
several families are not strictly monophyletic 
(sensu Hennig, 1966: strictly monophyletic taxa 
must include all and only the descendants of a 


McDADE—APHELANDRA PULCHERRIMA 


105 


common ancestral species). For example, be- 
cause Orobanchaceae are probably derived from 
within Scrophulariaceae, the latter family is not 
strictly monophyletic. Confident recognition of 
strictly monophyletic families and placement of 
disputed groups must await phylogenetic anal- 
ysis at the hue level. 

t ae provide an excellent example of 
the unresolved relationships encountered in the 
order. C t exists as to the 
taxonomic placement of the groups recognized 
by Lindau (1895) as subfamilies of Acanthaceae: 
Nelsonioideae, Thunbergioideae, Mendoncioi- 
deae, and Acanthoideae. Bremekamp (1953, 
1965) systematically reviewed the evidence for 
taxonomic placement of these groups and con- 
cluded that Nelsonioideae should be transferred 
to Scrophulariaceae (near Rhinantheae) and that 
the remaining three subfamilies should be rec- 
ognized at the familial level. Mohan Ram and 
Wadhi (1964, 1965) favored retention of Nel- 
sonioideae in Acanthaceae on the basis of em- 
bryological characters, and emphasized similar- 
ities between this group and Andrographideae. 
Thunbergioideae are embryologically distinct 
from Acanthaceae, justifying, in their view, Bre- 
mekamp’s recognition of the group as a family. 
Embryological data are lacking for Mendoncioi- 
deae. After morphological and anatomical study 
of the genera comprising Nelsonioideae (sensu 
Lindau), Hossain (1971) returned this group to 
Acanthaceae as a tribe (Nelsonieae) near Andro- 
graphideae. Hossain also took exception to Bre- 
mekamp's removal and elevation to familial sta- 
tus of Mendoncioideae and Thunbergioideae, but 
presented no new evidence. Cuticular studies 
demonstrate that all four of Lindau's subfamilies 
share diacytic stomates (Ahmad, 1974a, 1974b). 
This evidence suggests recognition of a mono- 
phyletic taxon composed of the four groups, but 
diacytic stomates occur sporadically throughout 
the Scrophulariales | (Metcalfe е. Chalk, 1950). 

trichomes 
suggests а relationship between Thunbergioideae 
and Nelsonioideae (Ahmad, 1978). Based on a 
study of epidermal hairs of 109 species in 39 
genera from all subfamilies, Ahmad (1978) fa- 
vored retention of Lindau’s subfamilies within 
Acanthaceae. There is thus considerable dis- 
agreementas to the exact familial limits of Acan- 
thaceae, as well as lack of consensus regarding 
relationships among the four clearly circum- 
scri groups. 
There is little doubt, however, that Acantha- 


106 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 
TABLE 1. Characters distinguishing Bremekamp’s subfamilies of Acanthaceae. 
Character Acanthoideae Ruellioideae 
Shoots Never articulated Always articulated 
Cystoliths Absent Present* 
Stamens 4 2 or 4 
Anthers Monothecous? At least 2 bithecous 
Pollen Colpate Colporate or porate? 
Tribes included Hasselhoffieae Trichanthereae 
Rhombochlamydeae Whitfieldieae 
Stenandriopsideae teri 
Apheland Ruellieae 
Acantheae Lepidagathideae 
Andrographideae 
Justiceae 
* Hypothesized derived character states. 
ceae (sensu Bremekamp, Lindau's Acanthoi- іп Acanthoid tolith d colporate or por- 


deae) are a closely related group sharing several 
derived characters: ovary bilocular with two 
longitudinal rows of ovules in each locule, cap- 
sule loculicidal and explosively dehiscent with 


delimited are strictly monophyletic will be de- 
termined only by analysis of sister group rela- 
tionships at the family level within the order. 
Several systems of classification for subdivi- 
sion of Acanthaceae (sensu Bremekamp) have 


"suborder" Echmata- 
cantheae, which included the genera currently 
placed in Acanthaceae sensu stricto. Bentham 


and Imbricatae (corolla aestivation usually im- 
bricate) with ten tribes. More recently, Breme- 
kamp (1965) recognized two subfamilies, Acan- 
thoideae and Ruellioideae, that are distinguished 
by differences in several characters (Table 1), and 
comprise five and seven tribes, respectively. Al- 
though intrafamilial classification of Acantha- 


ate pollen in Ruellioideae). 

Of the tribes comprising Bremekamp's Acan- 
thoideae, the Acantheae and Aphelandreae are 
well-defined groups of genera that share p" 

A i 4 3 + ГА э! 1 1 


and аге probably monophyletic. The remaining 
tribes, however, bear further investigation. All 
three resemble either Acantheae or Aphelan- 
dreae and are separated from these only by om 
or a few character states that appear to be prim- 
itive within the subfamily. Stenandriopsideae, 
for example, are separated from Aphelandreae 
by possession of a subactinomorphic corolla 
(versus a strongly zygomorphic corolla in the lat- 
ter tribe), and from Acantheae by lack of the 
characteristic incision at the adaxial side of the 
corolla. Further с, of these small, geograph- 
ically restricted groups might iiM evidence 
that they are сину primiti bers of 
either Acantheae or Aphelan vend These latter 
two tribes are probably sister groups (sensu Hen- 
nig, 1966), but the phylogenetic relationships 
within the subfamily bear further study. 

There is little disagreement as to taxonomic 
placement of Aphelandra. It is related to the old 
World genus Acanthus and these, together with 


Esenbeck (1847a) recognized two adjacent tribes, 
Aphelandreae and Acantheae, in his “series” (= 

supertribe) Imbricatae. Bremekamp (1965) fol- 
lows this alignment, placing both tribes in his 
subfamily Acanthoideae as discussed above (Та- 


о овако: оса == DC 


1984] 


ble 1). Neotropical genera allied with Aphelandra 
in Aphelandreae include Cyphacanthus, Neria- 
canthus, Encephalosphaera, Stenandrium, and 
Holographis. The phylogenetic relationships 
among these genera, however, have yet to be 
rigorously investigated and one or more might 
be more correctly placed within Aphelandra. En- 
cephalosphaera, for example, has been distin- 
guished from Aphelandra only on the basis of 
pollen characters. A broader palynological sur- 
vey of Aphelandra (Wasshausen, 1975; McDade, 
unpubl. data) indicates that pollen variability is 
much greater than was known to Lindau when 
he described Encephalosphaera. 

Plants currently placed in Aphelandra were first 
described in Justicia by Jacquin in 1762 and Vahl 
in 1794 (Wasshausen, 1975). Aphelandra was first 
proposed as a distinct genus by Robert Brown 
(1810) to include J. pulcherrima Jacq., J. scabra 

аһ, and J. cristata Jacq. These species were 
distinguished from Justicia by their four uniloc- 
ular anthers and calyx of five unequal segments. 
Rafinesque (1838) appears to have recognized 
the same differences when he erected the genus 
Amathea based on J. pulcherrima Jacq. In the 
first half of the nineteenth century, five addi- 
tional genera were d d that have since been 
considered congeneric with Aphelandra: Syn- 
andra Schrader (1821), Strobilorhachis Klotzsch 
(1839), Hydromestus Scheidweiler (1842a), 
Hemisandra Scheidweiler (1842b), and Lago- 
chilium Nees von Esenbeck (1847a). A more de- 
tailed discussion of these segregate genera and 
relevant taxonomic decisions is found in Wass- 
hausen (1975). 

Many species have been described in Aphe- 
landra, with notable contributions by Nees von 
Esenbeck (1847a, 1847b), Lindau (1893, 1895, 
1904), Leonard (1938, 1953, 1961), and Wass- 
hausen (1973a, 1973b, 1975). A recent revision 
of the entire genus (Wasshausen, 1975) recog- 
nized 165 species and two varieties. Two addi- 
tional species were described by Durkee (1978). 
Three new species were recognized in the course 
of ol обу (McDade, 1982) апд а илк 
Mos regional treatments of the. genus are 
available, including those for Costa Rica (Leon- 
ard, 1938), Colombia (Leonard, 1953), Guate- 
mala (Gibson, 1974), and Panama (Durkee, 
1978). 

In the only published supraspecific classifica- 
tion of this large and variable genus, Nees von 
Esenbeck (18472) recognized two sections based 


McDADE—APHELANDRA PULCHERRIMA 


107 


FIGURES 


1, 2. Floral bracts and bracteal nectaries 
in the Aphelandra pulcherrima complex. — ( 
10), individually large, circular to oval glands char- 
acteristic of species of Group I: (1) A. terryae, (2) A 
pipa ana, (3) A. storkii (figured), (4) A. gracilis, (5) 


Безем — 2. Oblong patches composed of many (> 100) 
minute glands characteristic of species of pee IT: (8) 
A. lingua-bovis, (9) A. leonardii, P (10) A E СУ A: 
campanensis, (12) A. hartwegiana Da and (13) 
A. darienensis. 


on relative length of the middle and lateral lobes 
of the lower corolla lip. In Stenochila, the lateral 
lobes were less than one-fourth as long as the 
middle lobe. Section Platychila included species 
with lower corolla lobes more nearly equal. The 
latter section was divided further into two sub- 
sections, Genuinae and Acanthoideae, with en- 
tire and serrate or pinnately lobed leaves, re- 
spectively. Although Lindau (1895) followed Nees 
von Esenbeck’s system in his treatment of the 
genus, subsequent systematists have not. It is 
apparent that there are several monophyletic 
groups within the genus, each of which can be 
recognized by several derived character states 
[e.g., the А. pulcherrima complex referred to by 
Leonard (1953) and treated in part here]. Several 
difficulties, however, have thus far frustrated at- 
tempts to devise a valid infrageneric classifica- 
tion of the genus. Many species are poorly known 
and are represented in herbaria by one or few 
specimens, which frequently lack mature inflo- 
rescences and flowers. In addition, several as- 
pects of corolla morphology (including relative 
size and degree of fusion of the lobes, morphol- 
ogy of the upper lip at anthesis, and position of 
the anthers in relation to the corolla) are poorly 
preserved in most herbarium specimens and dif- 
ficult to observe. Establishment of a natural su- 
praspecific classification of the genus Aphelandra 


108 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


5 3-5. Corolla morphology in ai rar s complex.— 3. Lateral view, anthers à 


FiG 
BP sees concealed within folded lobes of up 
and 


nd 
1 view, note reduction of lateral lobes of lower lip, 


anther pocket formed by sensei he of “i ‘Of upper Tip. —5. porai pocket opened to reveal anthers and 


exserted stigma, note bilobed upper lip 


will be a valuable contribution to systematic 
knowledge of Acanthaceae. 
DELIMITATION OF THE 
APHELANDRA PULCHERRIMA SPECIES COMPLEX 
This group of about 40 species forms a mor- 
phologically well-defined, monophyletic com- 
plex, with all members sharing several derived 
features including extrafloral nectaries on the 


along both margins of the abaxial surface of the 


floral bracts, and are of two distinct types: clumps 
of 1-10 relatively large (0.5-1.25 mm diam.) 
glands, or oblong patches (several mm diam.) of 
many (> 100) extremely minute glands (Figs. |, 

2, respectively). Necta 
after the inflorescences are initiated and contin- 
ues throughout the flowering period. 
consumed by ants of many species and ants are 
rarely absent from inflorescences. Several un- 
usual features of the corolla result in a very dis- 
tinctive structure: the edges of the bilobed upper 
lip are laterally folded to form a pocket that pal 


r production begins soon 


Nectar i$ 


TABLE 2. Central American members of the Aphelandra pulcherrima species complex. 


a NM 
Species (Abbreviation) Range BEES _ 

1. A. terryae Standley (TE) E Panama and eee 

2. A. sinclairiana Nees (SI) seri Panam 

3. A. storkii Leonard atl Limón and Heredia, Costa Rica 

4. A. gracilis Leonard ( сеш Рапат 

5. A. golfodulcensis ak (GO) SW Costa = and adjacent Panama 

6. A. panamensis McDade (PA Central Panama 

7. A. deppeana Schldl. & Cham S Mexico to N South America 


. (DE) 
A. dukei Wassh. (= A. deppeana Schldl. & Cham.) 
8. A. lingua-bovis Leonard (LB) 

9. A. leonardii McDade (LE) 

10. A. laxa Durkee (LA 

11. A. campanensis Durkee (CA) 

12. A. hartwegiana Nees ex Benth. (HA) 

13. A. darienensis Wassh. (DA) 


SW Costa Rica, Panama, and Colombia 
a 


E Panama aa Бан 
Darién, Panam EDD | 


1984] 


tially or completely conceals the anthers at an- 
thesis, and the lateral lobes of the lower corolla 
lip are extremely reduced (to only 1-2 mm long) 
and flattened in a plane perpendicular to the tube 
so that they almost contact one another across 
the mouth of the tube (Figs. 3-5). This closed- 
mouth, concealed-anther morphology functions 
in pollination. A hummingbird inserts its bill 
into the corolla by using the tip of the bill to force 
apart the lateral corolla lobes. As the broadest, 
basal portion of the bill enters the corolla, the 
upper lip opens, bringing the anthers and exsert- 
ed stigma into contact with the bird’s head. 

о other species of Aphelandra have both 
bracteal nectaries and the distinctive corolla 
morphology that characterize this complex. 
Shared possession of these derived morpholog- 
ical features provides strong evidence for a 
monophyletic origin of this group of species. 
Three South American species outside this com- 
plex possess bracteal nectaries: A. дем 
Leonard, A. impressa Lindau, and A. hylae 
Leonard. These species are probably the a 
living relatives of the A. pulcherrima group, with 
one or more constituting the sister group of the 
A. pulcherrima complex 

The species belonging to this complex are 
identified in Appendix A. Nine species restricted 
to Central America and four found both in Cen- 
tral and northern South America are recognized 
as belonging to the А. pulcherrima complex (Ta- 
ble 2). The comparatively recent origin of the 
Central American isthmus compared to the older 
continent of South America, along with the clear 
Gondwana distribution pattern of Acanthaceae 
and the presence of close relatives of Aphelandra 
in Africa suggest a South American origin of the 
genus and of this species complex. The wholly 
Central American species are thus derived di- 
rectly or through intermediate Central American 
ancestors from South American ancestors. Species 
found in both areas probably represent exten- 
sions of older South American ranges to include 
adjacent eastern Central America. 


COMPARATIVE MORPHOLOGY 


Habit and branching. The species of Aphe- 
landra treated here have two distinct growth 
forms that are associated with distinctive ar- 
rangements of the inflorescences. Individuals of 
six species are relatively low plants characterized 
by a very soft-wooded central axis that branches 
only after differentiation of the growing point 
into an inflorescence (Fig. 6). The one or two 


McDADE—APHELANDRA PULCHERRIMA 


109 


. ha 
(13) А. darienensis. (Aphelandra storkii, Finca La Sel- 
va, Heredia, Costa Rica.) 


lateral branches subsequently formed are equal 
and, again, branch only after flowering. This pat- 
tern has been described by Troll (1935) as di- 
chasial sympodial branching. Because the stems 
are soft-wooded (sometimes rather succulent), 
the branches invariably break after at most three 
branching points. As a consequence, individuals 
of species with this monocaulous growth form 
are mostly 1–2.5 m tall and very rarely larger 
than 3 m. The remaining seven species form true 
shrubs with generally profuse lateral branching 
(Fig. 7). Individuals of four species are soft- 
wooded shrubs that attain heights of 4—5 m. 
Aphelandra gracilis and A. panamensis are small 
trees to 7 m tall and 12 cm DBH. Individuals of 
A. deppeana tend to sprawl, forming horizontal 
branches close to the ground, and reach heights 
of 3-4 m. Plants of all species retained their char- 
acteristic habits when grown in greenhouses and 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


FIGURE 7. d habit characteristic of seven Cen 
eese. :)1( A.t 
and (9) A. ee: а вино panamensis, Cerro Jefe 


were unusual only in their tendency to flower 
profusely while very small 


Leaves. АП species treated here have орро- 
site, isophyllous leaves, with the exception of 
ipd alternate- leaved individuals (or 

iduals) of A. terryae and A. gol- 

bes s. The leaves of most species have a 
well- prre Брине blade and petiole, but those 
a A. panamensis and occasionally A. deppeana 
are sessile. Petioles are slender and similar in 
vestiture to the veins of the abaxial leaf surface. 
Leaves are simple, with entire, undulate or cren- 


(most species) to obovate. Texture of the blades 
ranges from membranous to coriaceous to very 
slightly succulent, and from glabrous through 
moderately scabrous to densely pubescent. Tri- 


costa generally depressed below the adaxial sur- 
face and protruding on the abaxial surface. Leaf 
surfaces are generally plane, but are slightly bul- 


e, (2) A. sinclairiana, (4) A. gracilis, (5) A. алено на (6) А. panamensis, (7) A. dep, 
ma.) 


al American species of the Aphelandra pulcherrima 
peana, 
, Panamá, Pana 


late in A. storkii and occasional individuals of 
A. sinclairiana. Except for variability in size, leaf 
variation over the range of each species appears 
to be minimal. However, Costa Rican plants of 
A. leonardii have leaves that differ from those of 
Panamanian plants in shape (narrower), vesti- 
ture (trichomes more dense), and texture (mem- 
branous rather than slightly succulent). 


Vestiture. Two types of trichomes occur in 


structures (Figs. 8, 9). The terminal cells аге ust- 
ally smooth, but may be short barbellate. In ad- 
dition, multicellular, capitate to turbinate, pr 
suma 
species (Fig. 
widely — in Acanthaceae (Ahmad, ! 78, 
Singh & Jain, 1975). Of taxonomic significante 
in the species treated here are the density, length 
and posture of simple trichomes on different ри 
Structures, as well as the presence ог absence 0 
glandular trichomes. 


1984] 


Inflorescences. Aphelandra has spicate inflo- 
rescences with distichously arranged flowers, each 
subtended by a floral bract and two bracteoles. 
In the species treated here, two distinct arrange- 
ments of spikes are found that are correlated with 
plant habit. Species that branch freely to form 
true shrubs produce many spikes in a terminal, 
paniculate inflorescence. In species that branch 
rarely or not at all, inflorescences are simple or 
rarely composed of up to five spikes. Individual 
spikes of shr ubby ly st rt (10- 
20 cm) and few-flowered (12—40 per spike). Those 
of sparsely branched species are much longer (to 
70 cm) and have many more flowers (to over 200 
per spike). The arrangement of flowering spikes 
is of taxonomic significance and may have im- 
portant implications for plant breeding systems 
as it relates to the number of flowers open daily 
per plant. 


Floral bracts. The usually large and conspic- 
uous bracts that subtend flowers of Aphelandra 
are highly variable among ‘Species and are e 
ditionally important in id 
(Leonard, 1597 Wasshausen; 1975). All species 
treated here fl nectaries located lat- 
erally and usually medially along both margins 
of the floral bracts. As described above, two dis- 
tinct types of nectaries occur (Figs. 1, 2). Addi- 
tional taxonomically significant features of floral 
bracts are size, texture, color, apical shape, po- 
sition of the nectaries and disposition along the 
rachis. 

Species with nectaries composed ofa few, large 
glands have bracts that are membranous and di- 
vergent from the rachis. Aphelandra panamensis 
and A. deppeana share imbricate bracts that are 
green and marginally toothed. Aphelandra gra- 
cilis and A. golfodulcensis have entire, green to 
dull orange, rather small and narrowly ovate 
bracts that are barely imbricate in the latter and 
quite lax in the former. The remaining species, 
A. terryae, A. sinclairiana, and A. storkii, have 
orange bracts that are closely imbricate. Bracts 
of A. sinclairiana and A. terryae are obtuse at 
the apex whereas those of the remaining species 
are acute. Bract size is an important character 
among these species, ranging from 5 mm long in 
A. gracilis to 25-30 mm long in A. storkii. Aphe- 
landra storkii differs from the other species shar- 
ing large glands in having bracts that are coria- 
ceous 

The floral bracts of species with minute glands 
are characteristically entire and leathery in tex- 


McDADE—APHELANDRA PULCHERRIMA 


mes of Central American 


FIGURES 8-10. 
species of "iie а: pulcherrima complex (ѕсап- 
ning electron photomicrographs, A. hartwegiana, 
McDade 425, DUKE).—8. Uniseriate and glandular 
trichomes of adaxial leaf surface.—9. Uniseriate tri- 
homes showing basal cells and part of barbellate ter- 
minal cell, adaxial leaf surface.— 10. Glandular turbi- 
nate trichome, abaxial leaf surface. 


о 


ture. Among these species, A. lingua-bovis, A. 
leonardii, and A. campanensis have rhombic- 
ovate bracts that are appressed to the rachis and 
nested among adjacent bracts, overlapping only 


112 ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL. 71 


Ficures 11,12. Bracteoles of the Aphelandra pul- 
cherrima c еа x.— 11. Lanceolate, apically acute, se- 
pal-like bracteoles most соттоп in the group.—12 
Falcate, keeled bracteoles found only in (11) A. cam- 
pest (12) A. hartwegiana (figured), and (13) A. 
darienensis. 


slightly. Aphelandra laxa shares this pattern ex- 
cept that the bracts are laxly disposed. Flowers 
of these species wither and dry before falling from 
the plant because they are held tightly between 
the rachis and the close-fitting bracts. Aphelan- 


above species, A darienensis has bracts that are 


ovate, E 3 ai ched a way 
from the raids. 


Bracteoles. А pair of conspicuous lateral 


of pieds [in the aranning k species, these 
structures are rudimentary (Leonard, 1953; 
Wasshausen, 1975)]. With three exceptions, 
bracteoles of the species treated here are lanceo- 


darienensis are similarly falcate, but do not over- 


Ficures 13, 14. Capsule morphology and dehis- 
cence in Aphelandra.—13. pane fruit opened to 
fis ат id two rows of two sed seeds.— 14. 

psule with seeds held by Ves retina 
зе seman figured). 


Calyx. Species of Aphelandra have a five- 
hts polysepalous calyx with a wide adaxial 
ent, narrower paired abaxial segments and 


shape (oblong or lanceolate), shape at the apex 
(acute or obtuse and apiculate), and color (green 
to brightly colored). 


Corolla. As described above, species of the 
A. pulcherrima complex share a unique and de- 
rived morphology of the upper and lower corolla 
lips (Figs. 3-5). The corolla tube in these species 
is constricted to 1-2 mm in diam. just above 

he ovary, which may protect the nectaries and 

ovary from sharp, probing bills of pollinating 

hummingbirds. This narrowed section is further 

congested and strengthened by the bases of the 
laments, which are inserted in the tube just 

above the narrowest point. In five of the species 

treated here (A. leonardii, A. laxa, А. сатра 
e 


open by an abrupt downward movement of the 
lower lip. The lower lip remains plana and is 
afi 


1 + the 


ә trongly у VY 

In the remaining eight species, the , corolla lobes 
are more tightly imbricate in the bud and flower 
open gradually or when visited by a pollinator. 


length (36-75 mm), color, pubescence (glabrous 
to pilose), texture (membranous to quite cori" 
ceous), and dimensions of the upper lip. 


Androecium. АП ѕресіеѕ of Aphelandra pos- 
sess four s. The 
anthers are basifixed, poe and held paralle 


110 


а авина 


1984] 


McDADE—APHELANDRA PULCHERRIMA 


113 


FicunEs 15-17. Capsule and кеб лабаа in the Aphelandra pulcherrima complex.— 


flattened, stipitate capsule (a, fron 
Group II: (8) A 


teral view) and flatte 
. lingua-bovis, (9) A. gene: Pare (10) A. laxa, (11) A. campanensis, (12) A. Posada 
and (13) A. darienensis. — 16. Stipitate, terete capsule (a) and erc n seeds (b) chara 


(2) A. sinclairiana, (3) A. anite (figured), (4) A. gracilis, and (5) A 


— 15. Mog gs 
ned seeds (c) characteristic of species of 


cteristic of: (1) A. terryae, 
golfodulcensis.— 17. Sub-globose, terete 


capsule lacking a distinct stipe (a) and sub-globose seeds (b) cha ан of (6) A. panamensis and (7) A. 


deppeana (figured). 


the adaxial side of the corolla tube. In the A. 
pulcherrima complex, the anthers are concealed 
within the folded lobes of the upper lip at an- 
thesis and emerge only when the flower is visited 
by a pollinator. Within the group, anther length, 
which ranges from 3 mm in A. deppeana to 10 
mm in A. hartwegiana, is taxonomically useful, 
as is pollen color, which varies from cream (e.g.. 
A. gracilis) to yellow (e.g., A. leonardii) and or- 
ange (e.g., A. sinclairiana). 


Gynoecium. Species of Aphelandra charac- 
teristically have a bilocular ovary with four 
ovules. In the Central American group dealt with 
here, the ovary is uniformly green and glabrous, 
except that occasional individuals of A. terryae 
have red-tipped ovaries. The style is filiform and 


extends to, and usually slightly beyond, the adax- 
ial pair of anthers (Fig. 5). Most species have 
shallowly bilobed stigmas that may be red or 
pink. Aphelandra deppeana and A. panamensis, 
however, have oblique stigmas that appear to be 
hollow and are not и colored. 


P Lh Aah: 
dehiscent 


Fruits. | 
capsules in which the four (or fewer) seeds are 
borne on membranous to woody, hook-like ret- 
inacula (Lindau, 1895; Long, 1970; Figs. 13, 14). 
In six of the species treated here, the capsules are 
clavate with a narrowed stipe below the seed- 
bearing portion of the fruit. They are dorsiven- 
trally flattened and thus oval in cross-section (Fig. 
15a, 15b). Five species have capsules that are 
stipitate and terete (Fig. 16a). In A. deppeana 


114 


Seed ernie patterns in the 

18. ey ger- 

n characteristic of species of Group poke А. 

pus -bovis, (9) A. leonardii, (10) A. laxa, (1 ЈИ са 

panensis, (12) А. hartwegiana, and (13) A darienen- 

i 1 germ rmination, with ‘only slight 

of the eg — of species‏ ا 

I: (1) A. terryae, (2) A lairiana, (3) A. 

storkii, (4) 4. суын 0 4  solfoduleensis (6) A. pan- 
amensis, and (7) A. а. 


FIGURES 18, 19. 
aphe andre pulcherrima complex. — 


and A. panamensis, fruits are sub-globose, lack 
a distinct stipe, and are terete (Fig. 17a). All 
species have capsules that are elliptic in outline, 
except A. sinclairiana has capsules that are lat- 
erally narrowed between the pairs of seeds and 
are sinuate in outline. Capsules of most species 
are green when immature, but those of A. sin- 
clairiana are black, and those of A. panamensis 
and A. lingua-bovis are dull orange-brown. 
Among species, capsule length ranges from 13 
mm (A. deppeana) to 35 mm (A. darienensis). 


Seed and seed germination patterns. As is 
characteristic of Acanthaceae, Aphelandra seeds 
are exalbuminous (Bremekamp, 1965). Mature 
seeds are various shades of brown, glabrous and 
orbicular to irregularly angular in outline (Figs. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


15c, 16b, 17b). Of the 13 species treated here, 
seven have seeds that are only slightly flattened 
(diameter/width ratio < 2) and six have strongly 
flattened seeds (diameter/width ratio > 2). Rel- 
ative seed wi is associated with fruit mor- 
phology: sub-globose seeds occur in species with 
terete fruits (Figs. 16, 17), and strongly flattened 
seeds occur in species with similarly flattened 
fruits (Fig. 15). 

Epigeal and semi-hypogeal germination pat- 
terns are found among the species studied here. 
In epigeal germination, the cotyledons are raised 
above the surface by elongation of the hypocotyl 


level of the substrate because no (or very little) 
elongation of the hypocotyl occurs (Ng, 1978; 
Fig. 19). Seed morphology is correlated with ger- 
mination pattern: flattened seeds germinate epi- 
geally (six species), and sub-globose seeds ger- 
minate semi-hypogeally (seven species). 


SYSTEMATIC IMPLICATIONS 


Comparative morphology provides evidence 
for the four taxonomic changes resulting from 
this study. Aphelandra dukei is considered con- 
specific with A. deppeana and three new species 
were described (McDade, 1982): A. panamensis, 
A. golfodulcensis, and A. leonardii. Detailed jus- 
tification for these changes is provided in the 


also prov 
logenetic relationships among these species. The 
14 P.L : 1 H р ed here 


in summary form to facilitate discussion of in- 
The C 


tral American species treated here belong to two 

lineages, referred to hereafter as Groups I (species 

1-7) and II (8-1 3) (Table. 3). Species of each 
states (see 


Phylogenetic Analysis) and may be readily rec 
ognized by suites of distinguishing features (Ta- 
ble 3). 


CHROMOSOME DATA 


In the most thorough cytogenetic survey of 
Acanthaceae to date, Grant (1955) reported ар" 
proximately 100 new chromosome Sein for the 
family and suggested that chromos e da 
would be useful in studying interretationship? 

within the group, especially at lower taxonomi® 
levels. Altho m w counts hav " 
reported subsequently, systematic applications 


1984] 


McDADE—APHELANDRA PULCHERRIMA 


115 


TABLE 3. Morphological characters distinguishing groups of species within the Central American members 
of the Aphelandra pulcherrima complex. NA denotes data not available. 


Bracteal Germination 
Species Nectaries Capsule Seed Pattern Habit 

Group I 

l. A. terryae (TE) Large Terete Sub-globose Semi-hypogeal Shrub 

2. A. sinclairiana ($1) Large Terete Sub-globose Semi-hypogeal Shrub 

3. A. storkii (ST) Large Terete Sub-globose — Semi-hypogeal — Monocaulous 
4. A. gracilis (GR) Large Terete Sub-globose Semi-hypogeal Shrub 

5. A. golfodulcensis (GO) Large Terete Sub-globose -hypogeal Shrub 

6. A. panamensis (PA) Large Sub-globose, Sub-globose Semi-hypogeal Shrub 

terete 
7. A. deppeana (DE) Large Sub-globose, Sub-globose Semi-hypogeal Shrub 
terete 

Group II 

8. A. lingua-bovis (LB) Minute Flattened Flattened Epigeal Monocaulous 

9. A. leonardii (LE) Minute Flattened Flattened Epigeal Shrub 

10. A. laxa (LA) Minute Flattened Flattened NA Monocaulous 
11. A. campanensis (CA) Minute Flattened Flattened Epigeal Monocaulous 
12. A. hartwegiana (HA) inute Flattened Flattened Epigeal Monocaulous 
13. A. darienensis (DA) Minute Flattened Flattened Epigeal Monocaulous 
of cytological data are essentially lacking. The of Hoyer’s solution (Anderson, 1954; Beeks, 


chromosome numbers reported previous to this 
study for four species of Aphelandra (n = 14, 14, 
28, 34; Table 4) suggested that cytology might 
be valuable in elucidating relationships within 
the group treated here. 


MATERIALS AND METHODS 


Flower buds were collected from both field 
populations and greenhouse plants (grown from 
cuttings taken from field populations) for study 
of meioti + Rootti Р. cuttinoc 


and from young seedlings were used to determine 
mitotic chromosome numbers. Suitable cytolog- 
ical material was obtained from at least one lo- 
cality of all species except A. laxa. Chromosome 
vouchers are deposited at DUKE. All materials 
were fixed in Carnoy's solution (3 absolute al- 
cohol: 1 glacial acetic acid) for 24 hours at room 
temperature or for four hours at 60°C. Material 
not processed immediately was stored in 7096 
ethanol and kept refrigerated when possible. 
Anthers or root tips were gently boiled for about 
five minutes in acetocarmine (saturated solution 
of carmine in 4596 acetic acid). A single anther 
or root tip was then transferred to a drop of 4596 
acetic acid. The root cap was removed and the 
distal 1-2 mm of the meristem was excised. The 
root tip or anther was then placed in a small drop 


1955) on a clean ANE. The tissue was gently 
broken apart О 

pel edge, a cover - glass was added and pressure 
applied to spread and flatten the preparation. 


= 
№ 
= 
[^7 
[e] 
e 
= 


RESULTS 


The haploid number of all 12 species is 14 
(Table 5). Karyotype analysis proved impossible 
due to the small size of the chromosomes (2-3 
се and their tendency to clump in к перне 

lis. The same by Grant 

(1955) in his work with the closely related tribe 
Acantheae 

The previously reported meiotic count of п = 


TABLE 4. Published reports of chromosome num- 


bers of species of Aphelandra. 
Species n Source 

А. aurantiaca 14 Takizawa, 1957 
А. chamissoniana 14 Takizawa, 1957 
А. ји 

(= А. deppeanay 28 Ра!, 1964 
A. crist 

(= А. tetragona) 34 Магауапап, 1951 


а Species included in this study. 
>South American member of the A. pulcherrima 


complex. 


116 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


Chromosome numbers of Central American species of the Aphelandra pulcherrima complex. МА 


TABLE 5. 
denotes data not available. 


Species n 2n Voucher 
1. A. terryae Standley NA 28 Panama. Darién: along Rio Pirre ca. 10 
km S of El Real, McDade 431. 
2. A. sinclairiana Nees 14 NA Panama. Colón: ca. 14 km from Colón 
along hwy. to Panamá, McDade 384. 
14 NA Panama. Colón: along Pipeline Rd. 
McDade 280. 
3. A. storkii Leonard 14 NA Costa Rica. Heredia: Finca La Selva, near 
Pto. Viejo, McDade 350 
4. A. gracilis Leonard NA 28 Panama. Panamá: slopes of Cerro Jefe, 
McDade 420 
5. A. golfodulcensis McDade 14 NA Costa Rica. Puntarenas: San Vito de Java, 
McDade 251 
14 28 Costa Rica. Puntarenas: Corcovado Na- 
tional Park, McDade 401 
6. A. panamensis McDade NA 28 Panama. Colón: Sta. Rita Ridge, ca. ? 
km from hwy. between Panamá and 
Colón, McDade 388. 
14 NA Panama. Darién: slopes of Cerro Pirre, 
McDade 428. 
7. A. deppeana Schldl. & Cham. NA 28 Costa Rica. Puntarenas: ca. 18 km SE of 
Palmar N., McDade 290 
8. A. lingua-bovis Leonard 14 NA Costa Rica. Puntarenas: Corcovado Na- 
tional Park, McDade 402 
NA 28 Panama. Darién: summit and upper 
slopes of Cerro Pirre, McDade 429. 
9. A. leonardii McDade 14 28 Costa Rica. San José: Río Tarrazü near 
Frailes, McDade 310. 
11. A. campanensis Durkee NA 28 Costa Rica. Limón: ca. 5 km N of Bribri, 
McDade 242. 
12. A. hartwegiana Nees ex Benth. NA 28 Panama. Darién: along trail between El 
Real and Pirre, McDade 425 
13. A. darienensis Wassh. NA 28 Panama. Darién: upper slopes of Cerro 


Pirre, McDade 430 


28 for A. fulgens (= A. deppeana) (Pal, me is 
i conflict with my determinauon of 2n = 28 fo 


к 


from Costa Rica. Pal d t indicat 

of the plant(s) from which the counts was i ob. 
tained, but the species was apparently cultivated 
in a botanical garden. Study of this species 
throughout its extensive range will be required 
to document and described this possible varia- 
tion in chromosome number. The 27 = 68 report 
for A. tetragona (Narayanan, 195 1), a Venezue- 
lan species belonging to the A. pulcherrima com- 
plex, suggests that chromosomal differentiation 


has occurred at least to some extent in the South 
American members of the complex and that fur- 
ther cytological work is warranted. 

though chromosome numbers have been 
determined for a small ан of A phelandrà 
species (15 of about 170), counts of n = 14 for 
representatives of three eid акай species 
groups [4. aurantiaca (Scheidw.) Lindl., А 
chamissoniana Nees, А. pulcherrima group] 598" 
gest that 14 is the base number of the genus: 
This same number has been reported for species 
belonging to most other tribes within Acanth® 
ceae (Grant, 1955). 


کے یھ ——— ———— 


1984] 


POLLEN 


The diversity of pollen morphology in Acan- 
thaceae is well-known (Erdtman, 1966) and its 
taxonomic importance has long been empha- 
sized (Radlkofer, 1883; Lindau, 1895; Breme- 
kamp, 1944; Raj, 1961). Although the results of 
a somewhat restricted survey of pollen mor- 
phology served as the basis of Lindau’s (1895) 
classification of the family at the suprageneric 
evel = recent -— complete studies using 


A 


considerable variation within Lindaa. suppos- 
edly uniform groupings (Bremekamp, 1944; Raj, 
1961; Gibson, 1972; Wasshausen, 1975). To as- 
sess accurately the systematic value of pollen 
morphology at higher taxonomic levels, knowl- 
edge of the infrageneric range of pollen vari- 
ability is necessary. Unfortunately, complete pal- 
ynological surveys have been made of only a few 
small genera of Acanthaceae. Partial surveys of 
several large genera have indicated extensive in- 
frageneric variability (e.g., Aphelandra: Wass- 
hausen, 1975; Justicia: Raj, 1961; Ruellia: Chau- 
bal, 1966). 

Variability in pollen size among taxa in Acan- 

thaceae has received little systematic attention. 

mong species with morphologically in- 
distinguishable pollen, significant differences in 
grain size may exist. Pollen size is readily deter- 
mined and is commonly reported in palynolog- 
ical descriptions. 

In an SEM survey of pollen of 60 species of 
Aphelandra, Wasshausen (1975) found consid- 
erable diversity in shape (spheroidal to perpro- 
late) and sculpturing (verrucose, reticulate, psi- 
late). Although indicating that pollen characters 
should be useful in classification of Aphelandra 
at the species level, Wasshausen found that evi- 
dence from pollen analysis conflicted with his 
interpretation of the affinities of several species 
based on morphological studies. Resolution of 


thac “a 


liv thor чы 
analysis of the relationship within Aphelandra, 
as well as a complete palynological survey of the 
genus. For the 13 species treated here, analysis 
of pollen size, shape, and uitrasculptüsing using 
both light and py was 
conducted. 


MATERIALS AND METHODS 


* | СТСЋАЋ 
J МОЛУ 


pollen was obtained from two or more plants 


For scanni 


McDADE—APHELANDRA PULCHERRIMA 


7 


aa 3 


from each of one to five p 
the geographic range of each species (Appendix 
B). Anthers were collected from field and green- 
house plants from flower buds one to three days 
prior to anthesis and fixed initially in FAA (for- 
malin: acetic acid: alcohol). Fresh or fixed pollen 
of A. laxa was not available and thus dried an- 
thers were removed from herbarium specimens 
and rehydrated for 24 hours in Aerosol OT so- 
lution. Following a dehydration series through 
10096 ethanol to 100% freon, the anthers were 
dried using carbon dioxide as a transitional fluid 
in a BOMAR PS 900/EX critical point dryer. 
T £ of glass coat- 
ed with polyvinyl chloride (n methyl ethyl ke- 
tone solution) was attached to the stub surface 
using low resistance cement. Pollen grains were 
extracted by slicing a dried anther and gently 
tapping it over a prepared stub. Stubs were then 
coated with a 250 angstrom layer of gold-pallad- 
ium using a sputter coater. The samples were 
viewed and photomicrographs taken using a 
JEOL J SM- T20 scanning electron microscope. 


g,a small р 


for 


were collected from several sources including 
dried herbarium specimens, field populations, 

and greenhouse plants (Appendix B). One to sev- 
en localities from throughout the range of each 
species were sampled. Fresh specimens were fixed 
initially in FAA and stored for varying lengths 
of time. Both dried and FAA-fixed anthers were 
acetolyzed by boiling in 9:1 acetic anhydride: 
sulfuric acid, straining to remove anther debris, 
boiling in 10% KOH, and eventual storing in 
70% ethanol (Livingstone, pers. comm.). Two 
sub-samples of at least 25 grains were taken from 
each sample and mounted in aniline blue in lac- 
tophenol solution. Length and width of each grain 
were measured under high dry magnification of 
400 x (bright field light microscopy). These data 
were analyzed by Analysis of Variance (ANO- 
VA), followed by Duncan Multiple Range a pos- 
teriori test for significant differences among 
species means (Sokal & Rohlf, 1969; SAS User’s 
Guide, 1979). 


RESULTS 


Pollen of all 13 Aphelandra species studied is 
isopolar, radiosymmetric, tricolpate, and prolate 
(4. panamensis) to perprolate (remaining 12 
species). With few exceptions as noted below, 
there is little variability at either the individual 
or population level among grains of the same 


118 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


Pw. 


species. Three pollen types are distinguished on 
the basis of morphology (shape and sculpturing). 


Type I (Figs. 20—26). Pollen perprolate and 
poles (Fig. 25). Sculpturing gemmate to verru- 
cose over colpi, finely reticulate elsewhere with 
the beni apie of longit ш end of vermic- 

dge ach colpus, 
these extending from the equator bus halfway 
to each ai 


A a terryae, A. sinclairiana, A. storkii, 
A. Mieres and A. gracilis (species 1—5, 
Figs. 20-26) have pollen of Type I. Among these 


1. (1) A. terryae, McDade d Sa 
3, (5) 4 а McDade 401 (ОКЕ). 
Бу polar view, McDade 350 (DUKE). 


ea McDade 389 (DUKE).— 


— 26. (5) A tres polar view, McDade 251 (DUKE). 


species, there is little difference in pollen тог 
phology although grain size differs markedly (зе 
below). А few individuals of А. golfodulcen sis 
show unusual colpi that bifurcate near the poles 
and meet, leaving a triangular shield of typical 
finely reticulate exine at the pole (Fig. 26). 


Type II (Figs. 27-34). Grains similar to Bie 


elsewhere, except longitudinal bands ж и 
olnus. 


nds вв вене and bordered with regions of 


1984] 


McDADE—APHELANDRA PULCHERRIMA 


FIGURES 27-34. Apure pollen of Type II (scanning electron photomicrographs). — 27. (10) A. ipa Mori 
et al. 6854 (MO).—28. (9) A. leo nan McDade 310 (DUKE).—29. (9) A. leonardii, McDade 432 (D 

30. (11) A. ia McDade 273 (DUKE).—31. (12) A. hartwegiana, McDade 425 (DUKE). hey TE 3) A. 
darienensis, McDade 430 (DUKE).— d. (11) A. campanensis, McDade 273 (DUKE).— —34. (11) A. campanensis, 
McDade 242 (DUKE). 


119 


120 


FiGURES 35-37. Ultrastructure of Aphelandra pol- 
len (transmission electron photomicrographs, prepa- 
ration after Stone etal., 1979). —35. € 


sed 
eduction of wall 
ularly of pons layers) over colpus. (Aphelandra 
от. McDade 350.) 


vermiculate ехте (Fig. 33) and extending from 
the equator approximately half the distance to 
each pole. 

Aphelandra leonardii, A. laxa, A. campanen- 
sis, A. hartwegiana, and A. darienensis (species 
9-13, Figs. 27-34) have pollen of Type II. Among 
these species, there are differences with respect 
to width of unsculptured bands (narrow in A. 
leonardii and A. laxa, quite broad in A. dari- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


enensis), as well as in size (see below). Structur- 
ally, the unsculptured regions probably are the 
exposed foot layer of the exine, with the colu- 
mellae and tectum lacking (Figs. 35-37). 


Type III (Figs. 38—43). Pollen prolate to 
barely perprolate, tapering very little from equa- 
tor to the poles so that grains are somewhat rect- 
angular, syntricolpate (colpi meeting at the poles: 
Figs. 40, 43). Exine finely reticulate to vermic- 
ulate over colpi, elsewhere finely reticulate. Lon- 
gitudinal bands along colpi may be quite indis- 
tinct (Fig. 42) or may be well-defined dene 
bearing vermiculate sculpturing (Figs. 40, 41). 

Aphelandra deppeana, A. panamensis, Es A. 
lingua-bovis (species 6-8; Figs. 38—43) have pol- 
len of Type III. Pollen of the last species is some- 
wit اوو‎ 8 populat ith respect to 
degree of sculpturing relief (from quite smooth, 
extremely finely reticulate grains with ill-defined 
colpi, to rather coarsely reticulate grains with 
vermiculate colpi; i.e., contrast Figs. 41, 42). Al- 

ough grains of these species are quite similar 
in shape, there is significant size disparity be- 
tween A. lingua-bovis and the other species. 

Pollen grains of the 13 species range in length 
from 45.6 um (А. panamensis) to 88.6 um (А. 
hartwegiana), and in width from 24.8 um (4. 
е) to 40. 0 ит (A. lingua- bovis). Analysis 


сес in both length ( (F, = 375.83; 13,3083 df 
P « 0.00001), and width (F, = 321.00; 13,3083 
df; P < 0.0001). Duncan Multiple Range test for 
differences among means permitted further res- 
olution oft lly distinguis 
able groups of means (Tables 6, 7). “All species 
can be distinguished on the basis of pollen length, 
width, or both, with the exception of two species 
pairs: A. darienensis—A. lingua-bovis, and A. gol- 
fodulcensis-A. sinclairiana. When both mor- 
phology and size of pollen are considered, only 
. golfodulcensis and A. sinclairiana remain in- 
distinguishable. 


SYSTEMATIC IMPLICATIONS 


Pollen characters support three of four taxo- 
nomic changes made in this treatment. Pollen 
morphology Magy A leonardii, with pollen 
of Type II, which h has pollen 
of Type I (Figs. 44, 45). Although grains of А. 
deppeana and A. panamensis are not distinguish- 
able by shape and sculpturing, pollen length and 
width differ (Tables 6, 7). The results of pollen 


1984] 


McDADE—APHELANDRA PULCHERRIMA 


FIGURES 38-43. ac pollen of Type III (scanning electron € — 38. (7) A. deppeana, 


McDade 533 (DUKE).— 


(DUKE).—41. (8) A. ingia. bovis, McDade 399 


analysis also support the inclusion of A. dukei 
within A. deppeana: the grains are indistinguish- 
able both morphologically (Figs. 46, 47) and in 
length and width (Tables 6, 7). However, pollen 
characters provide no additional basis for the 
recognition of A. golfodulcensis as distinct from 
A. sinclairiana. 

Pollen morphology also provides evidence for 
the recognition of interrelated groups among these 
13 species. With the exception of A. lingua-bovis, 
the species of Group II (9-13) share pollen of 


deppeana, McDade 
9 (DUKE).— 
(8) A. lingua-bovis, polar view, McDade 399 (DUKE). 


KE).—40. (6 anamensis, McDade 4 e 


— 42. (8) A. lingua- Peia McDade 380 (DUKE).— 


Type II. Species 1-5 (Group I, excepting A. dep- 
peana and A. panamensis) have Type I pollen. 
Of the three remaining species sharing pollen 
Type III, A. deppeana and A. panamensis are 
close relatives. The relationship of these two with 
A. lingua-bovis is less clear and is discussed in 
more detail subsequently. 

Preliminary surveys of additional species of 
Aphelandra (Wasshausen, 1975; McDade, un- 
publ. data) suggest that pollen morphology, to- 
gether with size analysis, has considerable sys- 


122 


TABLE 6. Pollen length variability among Central American species of the Aphelandra pulcherrima complex. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(VoL. 71 


N (Populations, Pollen Length? 
Species Grains) (Mean + 1 s.d.) Pollen Type? 
12. A. hartwegiana 4, 162 88.6 + 10.59 II 
10. A. laxa Бао 82.1 = 4.36 II 
13. A. darienensis 1, 65 80.9 + 3.74 II 
11. A. campanensis 4, 407 79.0 + 9.04 II 
9. A. leonardii 7, 344 2417 = 720 Il 
8. A. lingua-bovis 6, 273 78.5 + 9.48 III 
4. A. gracilis 3; 212 747 X 7.44 
l. A. terryae 37107 74.1 + 10.53 I 
5. A. golfodulcensis 7, 361 70.6 + 7.94 I 
2. A. sinclairiana 8, 451 69.5+ 8.43 I 
3. A. storkii 1, 93 ОЛСЕ 3.49 
A. “duker” 1, 34 49.8 + 2.70 III 
7. A. deppeana 7, 239 49 T4 722 IH 
6. A. panamensis 3, 138 45.6 + 8.12 III 


b 


tematic potential. At least three additional 
morphological types are recognizable that may 
clarify relationships within the large and heter- 
ogeneous genus. 


REPRODUCTIVE BIOLOGY 


Field investigations were undertaken to char- 
acterize the floral biology of the Central Amer- 
ican species of the Aphelandra pulcherrima com- 
plex (McDade, 1980). Aspects of particular 
systematic significance discussed here are sea- 


а Bars connect means not significantly different (P > 0.05). 
See text. 


sonality and phenology of flowering, pollinator 
relationships, and seed dispersal. 


Seasonality and phenology. Flowering sea- 
sonality was determined for 12 species of Aphe- 
landra over the course of 18 months of field work, 
augmented by study of herbarium specimens. 
Four species flower during the Central American 
dry season (late Dec. through March or April), 
and eight flower during the wet season (April or 
May to Dec.) (Table 8). At least five of the wet 
season flowering species (A. panamensis, A. stor- 


TABLE 7. Pollen width variability among Central American species of the Aphelandra pulcherrima complex. 
ы 


N (Populations, Pollen Width? 
Species Grains) (Mean + 1 s.d.) Pollen Type? 
8. A. lingua-bovis 6, 273 40.0 + 5.76 ш 
13. A. darienensis 1, 65 | 38.7 + 2.72 П 
12. А. hartwegiana 4, 162 | 38.1 + 4.79 П 
11. А. campanensis 4, 407 35.4 + 5.42 П 
9. A. leonardii 7, 344 32.1 + 4.24 П 
10. А. laxa 1.50 31.2 + 2.54 П 
4. А. gracilis 5,212 29.7 + 4.08 1 
3. А. storkii 1, 93 29.6 + 2.84 1 
2. А. sinclairiana 8, 451 28.0 + 7.96 1 
1. А. terryae 5, 168 27.1 + 3.31 I 
5. A. golfodulcensis 7, 361 27.1 + 3.16 1 
6. А. panamensis 3, 138 27.1 + 3.08 Ш 
7. А. deppeana 7, 239 24.8 + 3.01 Ш 
А. “duker” 1, 34 22.2 + 1.43 з coss ВИ 


b 


* Bars connect means not significantly different (P > 0.05). 
See text. 


a M al 


nee 


—— 


1984] 


McDADE—APHELANDRA PULCHERRIMA 


123 


FIGURES 44-47. Pollen Site rro of two taxonomically пар pairs of reme species (scanning 


electron photomicrographs).— 44 (9). 4 
(US).—46. A. dukei, Duke 14397 (US). 


kii, A. lingua-bovis, A. leonardii, and A. hartwe- 
giana) mature fruits during the following dry sea- 
son. This fruiting pattern may have adaptive 
value since Aphelandra fruits must desiccate be- 
- dehiscence and seed dispersal can. occur. 


+ Pt } 


= that 


flowers open at or shat. after dawn and fall in 
the late afternoon or night of the same day. Re- 
lease of pollen coincides with floral anthesis; by 
late afternoon, the anthers are empty and dis- 
colored. Controlled pollinations of greenhouse 
plants indicate that the stigma is receptive im- 
mediately following anthesis and that there is no 
temporal separation of male and female phases. 
There is, however, considerable spatial separa- 
tion: the stigmas of all species are exserted 3—10 
mm beyond the anthers. This separation effec- 
tively prevents autogamy (McDade, 1980). 
Aphelandra flowers secrete nectar beginning 
just prior to anthesis and continuing until late 
afternoon (McDade, 1980; McDade & Kinsman, 
1980). Sugar concentration in the nectar of six 
species ranged from 24% to 36% (McDade, 1980). 
Flowers of the species treated here are odorless, 
at least to human sensitivities. However, inflo- 


. leonardii, McDade 432 
—47. (7) A. deppeana, ГУА А 290 (DUKE). 


А. pulcherrima, Blum 3523 


KE).—45 


rescences of A. sinclairiana have a sweet, citrus- 
ike aroma. 


Flower visitors. Observations were made to 
identify animals that consume the floral re- 
sources (nectar and/or pollen) of Aphelandra, and 
to characterize the behavior of each species vis- 
iting the flowers. A visit was defined as actual 
physical contact of the animal with at least one 
flower. In a “legitimate” visit, an animal gained 
access to the nectar through the natural opening 
at the gu end of the corolla tube. All other 
means xtracting nectar or pollen were con- 
sidered ‘ Понта mate." Observation periods of 45 
minutes or longer were scheduled to cover day- 
light hours as fully as possible, and were con- 
ducted at 14 localities of ten species (Table 9; 
Appendix C). Data were not obtained for A. dar- 
ienensis, A. terryae, or A. laxa 

summary of the observed animal visitors is 
presented by species of Aphelandra in Table 9. 
Flowers of all species observed were pollinated 
by hummingbirds. The complex and extremely 
consistent floral morphology and phenology of 
all 13 species treated here suggests that the three 


124 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


TABLE 8. Flowering seasonality of Central Ameri- 
can species of the Aphelandra pulcherrima complex. 


Wet Season Dry Season 


paa PR 
gracilis 


A E 

A 2 А 

А 4. А. 

А. 5. А. golfodulcensis 
9. А. 

А 

А 

А 


. darienensis 


species not studied in the field have the same 
poo е distinctive morphology of En 
upper c 


aes pun mouth parts sufficiently 2l to 
open the upper lip and bring the anthers and 
stigma into contact with the visitor's body. An- 
es with narrow mouth parts (e.g., Lepidop- 
, Hymenoptera) would never contact the 
e floral organs and thus could not be 
effective pollinators. 
ith two exceptions, flowers were pollinated 
virtually exclusively by two species of large her- 
mit hummingbirds (Trochilidae: Phaethorni- 
nae): Phaethornis superciliosus (long-tailed her- 


Amazonian Brazil (P. superciliosus), and from 
Costa Rica to northern Venezuel 
Peru (P. guy). Phaethornis superciliosus occurs 
from sea level to about 900 m, and P. guy re- 
places it at mid-elevations (to about 1,700 m). 
Flowers of A. lingua-bovis and A. campanensis, 
which range from the lowlands to over 1,000 m, 
are pollinated by both birds. Most species, how- 
ever, have more restricted elevational distribu- 
tions and have only one pollinator. There is a 
close correspondence between the corolla tube 
length (35-45 mm above basal constriction) and 
curvature, and the bill length (35-44 mm) and 
curvature of both species of Phaethornis. Thus, 
these birds are able to gain access to nectar near 
the base of the corolla and to effect pollination 
in a “legitimate” visit (i.e., hovering in front of 
the flower and inserting the bill at the mouth of 
the corolla tube, causing the pocket-like corolla 
lip to open, thus bringing the anthers and stigma 
into contact with the bird's head). Three addi- 
tional lines of evidence suggest that these birds 
are effective pollinators: (1) pollen of A. storkii 
was removed from the crown feathers of several 
individuals of P. superciliosus at La Selva, Costa 


Rica; (2) hummingbirds that visit Aphelandra 
usually have a clearly visible crown patch of pol- 
us following flower probing; and (3) all of the 

pecies observed in the field set fruit and seed 
(Meade, 1980). 

In addition to close morphological correspon- 
dence between Bowers of Aphelandra and their 
pollinators, there i coincidence between 
hermit foraging behavior and: the spatial. distri- 
bution ofthe plants. I 
plants occur as isolated individuals or small 


(e.g., tree falls, stream edges). Similarly, most 
hermit hummingbirds forage on established cir: 


small clumps of species with distinctive floral 
morphologies (Skutch, 1964; Snow & Snow, 1972; 
Stiles, 1975, 1977; Feinsinger & Colwell, 1978). 
My observations agree with this view of hermit 
foraging: there was none of the agressive behav- 
ior associated with defense of territories by other 
hummingbird species (Stiles, 1975, 1977; Fein- 
singer, 1976). Except for brief periods of resting 


flowers. Within a patch or individual, pollinators 
generally visited avery accessible бои Ne 


1h 1 ps 
lar БУ UF Lic 19 


was disturbed in some way. 

Aphelandra leonardii was the only long-flow- 
ered species not visited by one or both species 
of large Phaethornis hummingbirds. Flowers of 
this species at Frailes, Costa Rica were visited 


and Feinsinger =ч have characterized this 
bird’s foraging behavior as hermit-like. It is cleat 
that pollen was transferred effectively at this site 
because high levels of fruit and seed set were 
observed (McDade, 1980). 

Aphelandra deppeana, with corollas only 36- 
42 mm long, was pollinated by a different gr oup 
of hummingbirds (Table 9). Although euglossine 
bees have been reported to pollinate flowers 0 
this species (Deuth, 1977), hummingbirds of the 
subfamily Trochilinae were the most frequent 
flower visitors at my study site. Mies be- 
havior by male blue-tailed I ds (Ama 
zilia cyanura) foraging in large ie of 4 
deppeana was observed. More sporadic, non-ter- 
ritorial feeding by members of both this species 
and A. rutila gbird) occu 
at small clumps and isolated plants. Bill length 


m—— T 


ا ا ا و و ق Sa aan. a‏ 


эзе г 


a ee ee 


— ни 


1984] McDADE—APHELANDRA PULCHERRIMA 125 


TaBLE 9. Animal visitors to flowers of Central American species of the Aphelandra pulcherrima complex. 


NA denotes data not available. 


Illegitimate Visitors 


Species and Location Legitimate Visitors Nectar Robbers Pollen 
(Total Hr. Observed) (Pollinators) Birds Insects Robbers 
1. A. terryae NA NA NA NA 
2. A. sinclairiana Phaethornis P. longuemareus Trigona sp. Trigona sp. 
superciliosus Chalybura buffoni? Xylocopa sp. 
3. A. storkii P. superciliosus P. longuemareus Trigona sp. Trigona sp. 
Pto. Viejo (31.5) 
4. A. gracilis P. guy P. longuemareus — – 
El Valle (3) 
5. A. golfodulcensis 
Corcovado (12) P. superciliosus P. longuemareus* Trigona sp. Trigona sp. 
Heliothrix barroti* Xylocopa sp. 
Thalurania furcata 
Amazilia tzacatl 
Coereba flaveola 
San Vito (11.25) P. guy P. longuemareus — -— 
6. A. panamensis P. guy P. longuemareus — “ 
Cerro Pirre (2.5) 
7. A. deppeana A. cyanura A. cyanura — Trigona sp. 
Cañas (11.75) A. rutila Chlorostilbon canivetii 
8. A. lingua-bovis 
Corcovado (6.75) P. superciliosus P. longuemareus = – 
С. flaveola 
Зап Упо (8.75) P. guy P. longuemareus — = 
9. A. leonardii Campylopterus — = E 
Frailes (1.5) hemileucurus 
10. A. laxa NA NA NA NA 
ll. А. campanensis 
El Valle (4.75) P. guy P. longuemareus – EM 
El Copé (1) P. guy Sus = d 
12. A. hartwegiana P. superciliosus — ves = 
io Pirre (4) 
13. A. darienensis NA NA NA NA 


* Primarily robbing species occasionally observed to visit legitimately. 


of both species (17-23 mm) corresponds to со- 
rolla tube length in 4. deppeana (22-24 mm above 
basal constriction). Observation of pollen on the 
crowns of foraging individuals, as well as high 
fruit and seed set (McDade, 1980), indicates that 
these birds are effective pollinators. 

In addition to visits by pollinating humming- 
birds, several other sorts of flower visits were 
observed (Table 9). Eight species were visited by 
birds with short bills that pierced or ripped holes 
near the base of the corolla tube to gain access 
to nectar. Birds visiting in this manner never 
contact the anthers or stigma and are not polli- 
nators. Flowers of four species were also visited 


by bees, particularly Trigona spp. (Apidae: Me- 
liponinae). These bees most frequently collected 
pollen from flowers, but also took nectar from 
two species (A. golfodulcensis and A. storkii). In- 
dividual bees typically settled on the upper co- 
rolla lip, chewed through the ке ved ns 

and collected pollen from the c aled a 
Because the stigma is exserted several mm pde 
yond the anthers, bees are unlikely to contact the 
stigma while gathering pollen. In fact, these bees 
frequently severely damaged or severed the style 
at the level of the anthers, precluding seed set. 
Trigona, as well as occasional carpenter bees 
(Anthophoridae: Xylocopinae, X ylocopa sp.) ex- 


126 


TABLE 10. Comparison of seed set from inter- and 
intrapopulation crosses of Aphelandra species. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


er factors must have spurred speciation and the 
subsequent evolution of isolating mechanisms in 
this grou 


Species Inter Intra Б, ағ 

5. A. golfodulcensis 0.590 0.490 3.478* 7 INTERPOPULATION CROSSES 
6. A. panamensis 0.448 0.210 257.089 1 |. 
7. A. deppeana 0.636 0.535 9528" 9 Perhaps th t ldi t 
8. A. lingua-bovis 0109 0223 ЗӨ" 3 ү 1 applying the biological species concept is that 
9. A. leonardii 0.461 0.614 182.143> 5 g 

ар < 0.01. ат жае 1 д کو‎ РС ESCENA Even 

>P<0.001. 


tracted nectar through holes made near the base 
of the corolla tube. 

Because they affect nectar and pollen resources 
available for pollinators, these non-pollinating 
bird and insect visitors are an important com- 
ponent of the floral biology of some populations 
of Aphelandra (McDade & Kinsman, 1980). The 
extent of their impact in terms of fruit and seed 
set, however, remains to be fully determined. 


Seed dispersal. Seeds of Aphelandra are dis- 
persed by explosive dehiscence of the capsules. 
The two woody lateral ribs are held together at 
the apex in immature fruits by hygroscopic cells. 
As capsules mature and dry, this tissue ruptures 


(Bremekamp, 1965; Sell, 1969; Figs. 13, 14). The 
retinacula, two of which are attached to each 
woody rib of the capsule, each hold one seed and 
insure that the seeds are propelled away from the 
parent plant rather than falling directly to the 
ground. Dispersal distances vary depending upon 
position of the fruit and plant, and surrounding 
vegetation. Limited observations of A. sinclair- 
ian be thrown 
more than 10 m from the parent plant. 


SYSTEMATIC IMPLICATIONS 


Differences in flowering E are an im- 
portant isolating mechanism ween several 
closely related pairs of Aphela г) species (Table 
8). In addition, pollinator relationships of A. de ер- 
peana and А. panamensis provide support for 
recognizing them as distinct species. They are 
morphologically distinct, elevationally isolated 
and are pollinated by different species of hum- 
mingbirds (Table 9). These data indicate, how- 
ever, that diversification of floral morpholo 
and phenology in conjunction with TOP aoa 


has not heen a 


major fe eatu 


in [cub radiation ofthis group of Aphelandra. ok 


with plants that are readily Санча апа r 
pollinated, the logistics of carrying out t 
necessary crosses are prohibitive. Conducting т 
terpopulation crosses to test for reproductive 
continuity within putative species must be re- 
garded as sampling, and the results taken as evi- 
dence for or against, but not proving, potential 
reproductive continuity within species. 


MATERIALS AND METHODS 


Plants were grown in the greenhouse from cut- 
tings or seeds taken from field populations. 
Crosses between sites were carried out for a 
species for which individuals from more than 
one population were available (Appendix О. 

and pollinations were made between 0730 and 

900 ., by placing an excess of pollen on 
the stigma of the ovulate parent. No emascula- 
tions were performed because selfing is prevent- 

ed by exsertion of the stigma well beyond the 
anthers at anthesis. The floral bracts subtending 
all treated flowers were color-coded using acrylic 
paints and observed until just prior to dehiscence 
of fruits or until failure to set fruit was apparent. 
Any inflorescence that did not set fruit, as well 
as distal portions of inflorescences beyond fully 
formed fruits, were not included in the analy 


Fruits were collected as they began | to desiccate, 
opened, and the number of fully filled seeds 
counted. At least 50 interpopulation pollinations 
were attempted between plants from each раї 
of sites. 

Fruit set from each cross was calculated as the 
proportion of treated flowers that produced fruits. : 
Seed set per fruit was expressed as a fraction ? 
the maximum of four. These two indices Wer 
multiplied to yield percent seed set; that at is 


nrannrt 


into. mature seeds. 


RESULTS 


iv- 
Seed set from interpopulation crosses invo 
ing five species is compared with se 


і 
| 
7 
| 
| 


1984] 


TABLE 11. 


McDADE—APHELANDRA PULCHERRIMA 


127 


Crossability indices between Central American species of the Aphelandra pulcherrima complex. 


The larger of the paired indices from reciprocal crosses is presented as the most conservative estimate of degree 
of relationship. The full matrix is presented as Appendix D. NA denotes data not available. Species numbers 


and abbreviations as in Table 


Species ДЕТЕ М ZSF 4 OR O0 .&PÀ 7.DE 8.18 UIE ILCA ти 
2; M 0.66 

3:4 STi 0.59 0.39 

4. GR 0.59 NA 0.62 

5. GO 0.86 0.98 0.51 0.51 

6. PA 0.80 0.99 0.58 0.37 0.64 

7. DE 0.11 0.13 0.29 0.05 017 0.89 

8. LB 0.03 0.07 0 0.45 0.04 0 0.08 

9. ТЕ 0.11 0.16 0.12 0.49 0.27 0.90 тз 0.12 

11. CA NA NA 0 0 0 0 0.07 0 0.17 

12. HA NA NA 0.03 NA 0 0 0 0 0.26 0.04 

13. DA 0.07 0.01 0 NA 0.03 0 0 0 0.39 NA NA 
from intrapopulation crosses [ means Crossability indices for each cross attempted 


of at least 100 attempted pollinations for each 
species (McDade, 1980)] in Table 10. Interpopu- 
lation сом vof A. golfodulcensis, A. italic 
sis, and A tly more 
seeds than did intrapopulation c crosses. The re- 
Verse occurred in A. lingua-bovis and А. leo- 
nardii. In these last two species, however, seed 
set from interpopulation crosses was higher than 
from the most fertile interspecific pollinations 
(Appendix D). 

These data provide no evidence that there are 
reproductive barriers between plants from dif- 
ferent sites of the species tested. In the form of 
step-wise exchange of genes through both pollen 
flow and dispersal events, this lack of reproduc- 
tive barriers may result in reproductive conti- 
nuity within these species. 


ARTIFICIAL HYBRIDIZATIONS 


MATERIALS AND METHODS 


Interen Hd 11: P ed 


D e carried out with 
all species treated here бше А. laxa, using 
greenhouse grown plants from field populations. 
Three to eight individuals from one to three pop- 
ulations of each species were used in the artificial 

ybridizations. Except when the number of flow- 
ers and Overlapping flowering periods were lim- 
iting, at least 50 crosses of each possible com- 
bination were attempted. Controlled pollinations 
Were carried out as described above for inter- 
Population crosses. Hybrid seeds were germi- 
nated on filter paper and formed vigorous, rap- 
idly growing seedlings. Representative seedlings 
of each successful cross were cultivated in the 
greenhouse for use in future studies. 


were calculated from percent seed set from each 
cross. For each ovulate species, percent seed set 
from interspecific crosses was divided by seed 
set from out-crosses within that species (Mc- 
Dade, 1980). This was done to avoid errors in 
comparing results among species due to differ- 
ences in gamete viability, appropriate pollination 
conditions, etc. Crossability indices (CIs) thus 
can range from zero (for crosses yielding no seeds) 
to greater than one (if seed set from an artificial 
hybridization exceeds seed set from intrapopu- 
lation crosses). 


RESULTS 


Crossability indices for each cross attempted 
are presented in Appendix D. Considerable dis- 
parity exists between indices for some species 
pairs, depending upon which species was the 
ovulate parent. For instance, in the cross A. pan- 
amensis9 х A. sinclairiana ё, seed set was 0.986, 
whereas in the reciprocal cross, seed set was only 
0.042. Although there is a significant correlation 
(r = 0.313, 90 df, P < 0.01) between reciprocal 
crossabilities for each species pair, the disparity 
between indices is эрик particularly when 
one cross of a reciprocal pair yielded very high 
seed set. Many factors ла degree т rela- 
tionship can influence seed set from experimen- 
tal hybridizations (e.g., interspecific and intra- 
specific incompatibility barriers, pollen 
germinability, pollen tube growth, and harmo- 
nious growth and development of the hybrid em- 
bryo within the ovary). These may vary mark- 
edly in their influence on the success of 
hybridizations depending on whether a species 
is used as the ovule or pollen parent (Ornduff, 


128 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


F4 п 1 E | Ж. L ЧАРОВ ТИШ! | s. 
12 
HA [ә] 
н 11 
СА fal 
13 
Ева ES 
^ 9 
а 
wes Ema. mm Йй 
с Е 
+ 4 3 
LB | 
[31 [7] [9] [2] a 
DE po “А [519] 2] 1[вјија] | 
: | 
РА E | 
[2] [917] [1] T) fl [4] | 
3 - | 
5 1 E 
I ml m maan] DENE- | 
+ | 
14 
3 [1 a m Ё DETRU | 
: у [519] | 
E Боја в mia rm m. 
o е 13] [12] | 
со 5 Rl [6] 2E [9] [7]. osu | 
i а | 
5 5 fi | 
КЕ n] [3] г9]7] [8] 18 : | 
M 0.90 0.80 0.7 70 0.60 0.50 0.40 030 0.20 0.10 0 NAT 
CRHROSSAHTIUTTY IND Ex 


, FIGURE 48. , Frequency distribution table of crossability indices for 12 Central American species of 


Each square is labelled with the appropri pecies identificati ber. Data not availabl (NA) are e indicated 
at rege far right. 
1969). For example, Lloyd (1965) crossed races vergence. The iarger index for each species раї 


of Leavenworthia and found that seed set was is, therefore, used in all further analyses (Table 


higher when the staminate parent was self-in- k 
compatible and the ovulate parent self-compat- eic Yi are presented in tabular 
ible, than when the reciprocal cross was made. and diagram orm as recommended by 


The goal of this study was to obtain estimates McDade and юр лн (1982). The frequency 
of the degree of relationship among the species — distribution of crossability indices (Fig. 48) shows 
of Aphelandra treated here. During the evolution that, with the exception of a very high cro ossi" 
of these species from a common ancestor, cross- bility between species 9 (A. leonardii) and 6 (4 
ability has decreased from full interfertility to panamensis), all of the CIs above 0.50 are among 
various degrees of incompatibility between each species 1-7 (Group I, Table 3). Crossabilities 
pair of species. The larger of the reciprocal CIs among species 8—13 (Group II), and between 
for each Species pair thus represents the most and species 1—7 are mostly less than 0.20. Sum- 
conser p. The small- — marization ofthe crossability data by ^ oup( 
er index may be a product of various aspects of 49) emphasizes this pattern. Species 7 (4. + 
incompatibility beyond degree of relationship, as peana) is apparently isolated within Group LA ; 
described above, and would over-estimate di- though species 6 and 7 are highly interferti 


| 
| 
| 
| 
| 
| 
| 


№ 


3 


1984] 


(CI = 0.89), of the CIs among species 1-7, all of 
those below 0.30 have species 7 as one member 
of the pair. Species 9 (A. leonardii) appears to be 
intermediate between the two groups. Of four 
crossability indices above 0.20, three involve 
species 9, as do six of seven CIs above 0.11 

Crossability maps, representing the best dn 
dimensional configuration of species based on 
the matrix of crossability indices, were con- 
structed using Multidimensional Scaling (Krus- 
kal & Wish, 1978; McDade & Lundberg, 1982; 
Fig. 50). The locations and relative proximities 
of species on the map are indicative of their in- 
terrelationships based upon the results of artifi- 
cial hybridizations. Subsequent maps display 
connections between species that cross at or above 
five selected crossability levels (Fig. 51—55). 
Crossability mapping emphasizes the close re- 
lationships among species 1-6 of Group I (A. 
terryae, A. sinclairiana, A. storkii, A. gracilis, A. 
golfodulcensis, A. panamensis). Species 7 (A. 
deppeana) is closely related to species 6 (A. pan- 
amensis), but is more distant from the remaining 
five species. Species 9 (A. leonardii) occupies an 
intermediate position between this interrelated 
group and the much less closely linked species 
11, 12, 13, and 8 (А. campanensis, A. hartwe- 
giana, A. darienensis, and A. lingua-bovis). The 
tentative position of species 8 merits further dis- 
cussion. Whereas multidimensional scaling 
placed species 9 between species 1-7 and 8 based 
on all crossing relationships, the first connection 
of species 8 is with species 3 at CI = 0.45. No 
further connections are made until CI = 0.12 with 
species 9 (Fig. 55). It is possible that the cross- 
ability index between species 8 and 3 is the result 
of a sampling error due to the unusually small 
number of crosses attempted (л = 10). An initial 
connection of species 8 (A. lingua-bovis) with 9 
(4. leonardii) would be more in accord with the 
pattern of crossabilities between species 8 and 
all other taxa. 


NATURAL HYBRIDIZATION AND 
ISOLATING MECHANISMS 


Only two combinations of parental species are 
suspected of producing naturally occurring hy- 
brid offspring. Three Panamanian localities host 
putative hybrids between A. sinclairiana and A 
&racilis. All three are mid-elevation sites where 
cloud forest habitat of А. gracilis has been dis- 
turbed and warmer and drier local climates re- 
sult. Aphelandra sinclairiana usually occurs along 


McDADE—APHELANDRA PULCHERRIMA 


129 


WITHIN GROUP JI 


п. 


BETWEEN GROUPS Т 
8- 11-7] AND II [8-13] 


II 1-41 БЕПНЕ ШШ! 


P 
i] 
GOOG 
ЕГП 


WITHIN GROUP I 
Fey 


esL 


CROSSABILITY, 


FIGURE 49. Summary frequency distribution of 
сойылу indices within and between the specie 5 of 


jrouns la 
Н 


in text. 


P 


edges and in gaps in primary lowland to pre- 
montane forest, and may also colonize exten- 
sively disturbed areas at higher elevations. Hy- 
brid plants between these two species are found 
in disturbed areas near El Valle (Coclé), Cerro 
Jefe and El Llano (Panamá) (Fig. 56). They are 
distinctly intermediate in many characters and 
produce distorted, apparently sterile pollen. Un- 
fortunately, I have not attempted this cross in 
the greenhouse. 

Interspecific hybrids apparently between A. 
sinclairiana and A. golfodulcensis occur at var- 
ious localities in the Caribbean lowlands of 
northeastern Costa Rica (Fig. 56). Although the 
ranges of the two parental species are separated 
by the central mountain range in Costa Rica, 
older collections indicate that the two may have 
occurred close together e either slope of the 
central plateau north ofth pd Talamanca pinge. 
TI 


ters at the present time. The ылыа hybrids are 
intermediate between the two parental species in 
many features and, though quite vigorous, are 
pollen sterile. Numerous self- and cross-polli- 
nations between clumps of these plants were at- 
tempted without any successful seed set. Collec- 
tion localities suggest that streams and rivers are 
important in the propogation of this sterile hy- 
brid. Three clumps of the hybrid occur at La 
Selva in Heredia province, all of which are along 
the banks of the Rio Puerto Viejo within the 
flood zone. Branches broken off upstream would 
root quite readily when lodged against the bank 
downstream, giving rise to new “individuals” of 


130 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


=0.5 у 
с! 1 Ф Ф 


FIGURES oo _Crossability mapping of Central American ери of the Aphelandra pulcherrima complex, 
at six successiv ve the indicated CI are резе їп еасһ 
map. Dashed dis indicate conflicting evidence for the position of. species 8 as discussed in t 


the hybrid. Hybrids between A. sinclairiana and With these exceptions, reproductive isolation 
A. golfodulcensis have been made in the green- between Central American species of the A. pul- 
house, and these are indistinguishable from the cherrima карел is apparently comple. b 


putative hybrids from Costa Rica. Field studies sp at are full 
and ioo hybridizations indicate had, id pletely ИЕН (Table 12), further discussion 
the ranges of the t of isolating mechanisms is moot. The results of 
Raduno of flowering times, MT Dol greenhouse crosses using plants from i 4 
linator species, and interfertility would result in ulations, however, 
the production of hybrids. adjacent or sympatric ranges are interfertile: Be- 
dior 25 cov i MN 
А А. sinclairiana 
в A. gracilis 
€ А. golfodulcensis 
• * А.зі X gr 
COSTA хх * NW X 
Se 
. 


100 km 
——— 


E 56. Distribution of Aphelandra sinclairiana, A. gracilis, A. dot meti and the hybrids between 


Pus. dfi iie latter two species, and A. sinclairiana in Costa Rica and P 


— 


mmm amat men 


و چ af‏ 


ТЕТ} 


a 


1984] 


1400 


5 


о Г) 
= UB 
oe (E МИ СВЕ HD БР gam БЕЛЕ ` 


E: 


ELEVATION Imi 
5 
о 


~ 
‚5 


ST GR GO PA DE LB LE CA 
8 РЕ СЕ 8 


ТЕ Si 


i FIGURE 57. Elevational range of the Central Amer- 
elandr ple 


h species are 
n local climatic conditions result in 
habitat atypical of that elevation in this region. 


cause hybrids are rare in nature, further exami- 
nation of barriers preventing hybridizations be- 
tween such species is appropriate. Four 
interrelated factors merit attention: isolation by 
elevational range, habitat differences, flowering 
seasonality, and pollinator specificity 

Isolation by elevation, especially if reinforced 
by similarly restricted pollinator ranges and hab- 
itats, may effectively prevent hybridization be- 
tween species. Several species of Aphelandra are 
restricted to either lowland or mid-elevation lo- 
calities (Fig. 57). Thus, although the ranges of 
several lowland species (e.g., A. deppeana, A. sin- 
clairiana, A. terryae) are adjacent to those of mid- 
elevation species (e.g., 4. panamensis, A. graci- 
lis) (Fig. 56), hybridization events are rare. 

Habitat differences may separate species that 


TABLE 12. Isolat 


McDADE—APHELANDRA PULCHERRIMA 


VECI 


HH 


have adjacent ranges, or can reinforce elevational 
isolation. The species of Aphelandra treated here 
are found in seasonally drought deciduous low- 
land forest, lowland wet forest, and cloud forest. 
Aphelandra deppeana, for example, occurs in 
habitats with a more severe dry season than can 
be tolerated by other species. This habitat dif- 
ference, along with pollinator specificities, ap- 
parently reduces the possibility of hybridization 
involving A. deppeana. Thus, although hybrids 
of A. deppeana and its close relative, the cloud 
forest species A. panamensis, are easily synthe- 
sized (Table 11), naturally occurring hybrids are 
not found. 

Because the wet and dry seasons are quite dis- 
crete in many parts of Central America, temporal 
differences in flowering can be effective as a bar- 
rier to hybridization even between fully sym- 
patric species. Four species of Aphelandra treat- 
ed here flower during the dry season, and the 
remaining nine flower during the wet season (Ta- 
ble 8). For example, А. panamensis and А. gra- 
cilis coexist and share the same pollinators at 
several localities in Panama. Lack ofoverlapping 
flowering seasons effectively prohibits hybrid- 
ization. 

As documented by field observations of flower 
visitors to the species of Aphelandra treated here, 
all but A. deppeana are pollinated by large hermit 
or hermit-like hummingbirds (ТАР Э), Polli- 
nator differences thus 
lation of A. deppeana and species with adjacent 
ranges (e.g., A. sinclairiana). The two ера pol- 
linators of th 
elevational ranges, perhaps reinforcing eleva- 


diff er ent 


Central American species of the Aphelandra pulcherrima 


complex. Pairs not fully allopatric (A) ӨР үги (I) may be isolated by elevation (E), habitat (Н), 
flowering seasonality (FS), or pollinator specificity (P). Species numbers and abbreviations as in Table 2. 


Species 1. ТЕ ZSb RSF. 4 OR 5.GO 6.PA 7.DE 8.LB SLE 11.СА 12. НА 
2. 8l A 

3 SF A 

4. GR A E,H* A 

5. GO A A A A 

6. PA E,FS EH,S А FS A 

7. DE H,SP Н,Е8,Р А ЕНЕР HESE EH, 

8. LB E,FS H,FS АЛ А FS I A 

9. LE A A A E,FS A E A E 

11. CA Аз EH,FS* АЛ 1 АЛ 1 А АЛ А 

12. НА FS: Аг А Аз АЛ 1 АЛ I E A 

13. DA A A A Аг А 1 АЛ 1 Е А ЕН 


* Species pairs for which data from artificial hybridizations are not available. 


132 


tional isolation of geographically proximate 

species. Long-tailed (lowlands) and green her- 

wever, apparently 
e 


land species pollinated by long-tailed hermits, is 
cultivated at 1,200 m at the Las Cruces Botanical 
arden in Costa Rica. Visits to flowers by green 


hermits were EEE eet since these 


tions, pollinator specificities are lost. Hybridiza- 
tion between A. sinclairiana and A. gracilis, a 
species restricted to mid-elevations, results be- 
cause green hermits pollinate flowers of both 
species. 

The paucity of naturally occurring hybrids is 
at first striking given the geographic eyed 
and lack of full sterility between many of thes 


о 
ranges and prevailing weather етен result in 
small scale environmental partitioning. Under 
these conditions, isolating factors that fall short 
of complete intersterility and strict allopatry can 
effectively prohibit hybridization. Such factors 
are clearly important among the species of Aphe- 
landra treated here. 


PHYLOGENETIC ANALYSIS 
INTRODUCTION AND METHODS 


The goal of phylogenetic systematics (sensu 


phylogeny provides the conceptually unifying 
basis for biological classification. Provided that 
only strictly monophyletic taxa are recognized, 
hierarchical Linnaean classification allows exact 
retrieval of phylogenetic сачы Мопо- 
phyletic groups can be d ted only by rec- 
ognition of shared devel RAGES character 
states (Hennig, 1966; Lundberg, 1972; Wiley, 
1981). Character analysis is thus basic to phy- 
logeny reconstruction and involves at least two 
steps: recognition of strictly homologous char- 
acters and formulation of polarity hypotheses. 
The phylogeny supported by the largest suite of 
савана greed character States is the best hy- 
thes 


E 


осу 
апд асе reversals, parallelisms, and err 
in character analysis. Such unreliable didicit 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


may be more numerous than reliable ones in the 
data set, but presumably will not be mutually 
congruent. An incorrect phylogeny will be ac- 
cepted as “ay T hypothesis jou X a set of 
d hom- 
oplasies exists T is caval than the с of cla- 
distically reliable charact 
recently reviewed in B (1980), sev- 

eral criteria may be used to infer evolutionary 
polacas, of character states, including evidence 
fro 9 


ntogeny, d rison 


a out-groups. In this study, primary emphasis 
was on the last criterion because Aphelandra has 
no known fossil record and the ontogeny of most 
characters used in the analysis has not been stud- 
ied. Based upon shared possession of a suite of 
eevee пшне States that result in the dis- 
ar to this group, 
the species of the hi осени complex are 
hypothesized to be monophyletic. These species, 
along with А. hylaea Leonard, A. impressa Lin- 
dau, and А. lamprantha Leonard, are also unique 
within Aphelandra in having nectaries on the 
floral bracts. Shared possession of the extra-floral 
nectaries is evidence that these three species and 
the A. pulcherrima complex are together a mono- 
phyletic group, and that one or more of the three 
is the sister group of the А. pulcherrima group. 
Further resolution of the sister group will require 
udy; all three species were therefore used 
as the out-group in character comparisons and 
polarity decisions. Following study of the distri- 
bution of states of 42 characters (Table 13) among 
these especies; polarity hypotheses were made fol- 
(Watrous & Wheel- 
er, 198 Ix Consideration of Ше three species out- 
group resulted in unambiguous hypotheses for 
35 of the 43 characters (2-10, 12-29, 33, 34, 36, 
39-43). Character states in the out-group wer 
unknown or offered conflicting evidence for de- 
termining evolutionary polarities of the remain- 
ing eight characters and the analysis was © 
panded to consider more distantly related groups: 
Relationships within the genus аге not sufficient- 
ly resolved to permit identification of the sister 
group of the species sharing bracteal nectaries 
and the entire genus was thus used as the next 
level of comparison. Two additional, more dis 
tantly related out-groups are provided by the 1°- 
lationships of Aphelandra within Acanthoide# 
other genera in Aphelandreae and the Old Worl 
Acantheae. The results of character analysis ® 
presented in Table 13 and as a character by 2X0" 
matrix in Appendix E. The value of the phylo- 


1984] 


genetic hypothesis presented for the species of 
Aphelandra treated here rests on the validity of 
this character analysis. Detailed information on 
character state distributions among out-group 
taxa and polarity decisions for each character is 
available from the author. A phylogenetic hy- 
pothesis was constructed from these data using 
the Wagner method (Wagner, 1969; Kluge & Far- 
ris, 1969; Lundberg, 1972). 


RESULTS 


The 13 species fall into two lineages (Fig. 58) 
herein referred to as Group I (species 1-7) and 
Group II (8-13) (Table 3). The species of Group 
I share several uniquely derived character states: 
trichomes of distal stems longer than 0.5 mm 
(character 4); bracteal nectaries of individual, 
large glands (12, 13); terete fruits (30); sub-glo- 
bose seeds (35); and semi-hypogeal germination 
(37) (Fig. 58). Shared possession of these ad- 
vanced states provides strong evidence of a 
monophyletic origin of these species. Aphelandra 
sinclairiana (species 2) and A. чотки (3) are sister 
species, sharing long and erect trichomes on dis- 
tal stems (character 3). Aphelandra terryae (1) is 
hypothesized to be the sister group of these two 
species. Characters providing evidence for this 
relationship are, however, homoplasious (re- 
versed or paralleled elsewhere in the cladogram) 
(Appendix F). Aphelandra deppeana (7) and A. 
panamensis (6) are sister species, sharing three 
uniquely derived character states: dense pubes- 
cence of distal stems (2), villous pubescence of 
lower corolla lip (26), and oblique stigmas (29). 
The relationships of A. golfodulcensis (5) and A. 
gracilis (4) within Group I are tentative. Shared 
possession of green floral bracts (9), along with 
six homoplasious characters (Appendix F), sug- 
gests that these two species share a monophyletic 
origin with 4. deppeana and A. panamensis. In 
conflict with this evidence, A. deppeana and A. 
panamensis share derived states of characters 25 
(pubescence of the corolla tube) and 26 (long 
trichomes on the lower lip of the corolla) with 
die (1), A. sinclairiana (2), and A. storkii 


Evidence in support of a monophyletic origin 
of species 8-13 (Group II) is provided by shared 
Possession of extremely leathery floral bracts 
(character 7) and glabrous corollas (25, 26) (Fig. 
58). The bracteal nectaries composed of many, 
minute glands facilitates recognition of these 
species. This feature, however, is shared by the 
three species out-group (A. hylaea, A. impressa, 


McDADE—APHELANDRA PULCHERRIMA 


133 


А. lamprantha) and is thus hypothesized to be 
primitive for the A. pulcherrima complex. The 
placement of A. lingua-bovis (species 8) is ten- 
tative. All of the derived character states it pos- 
sesses are homoplasious (Appendix F). Derived 
states of characters 23 (narrow upper corolla lip), 
28 (anther length) and 39 (syntricolpate pollen) 
suggest a relationship between this species and 
the sister species A. deppeana (7) and A. pana- 
mensis (6). This relationship, however, is con- 
tradicted by many other characters. Study of 
South American relatives of A. /ingua-bovis may 
provide data for a more satisfactory resolution 
of the phylogenetic relationships of this species. 
Strong evidence for a monophyletic origin of 
species 9—13 (A. leonardii-A. darienensis) is pro- 
vided by shared uniquely derived states of char- 
acters 40 (pollen with unsculptured longitudinal 
bands) and 41 (corolla opening immediate). 
Aphelandra laxa (10) shares leathery and papil- 
late corollas (21, 41) with species 11-13. Shared 
possession of falcate bracteoles (16) and large 
seeds (36) provides evidence that A. campanen- 
sis (11), A. hartwegiana (12), and A. darienensis 
(13) are monophyletic. Aphelandra hartwegiana 
and A. darienensis share anthers longer than 9 
mm (28), as well as three homoplasious derived 
character states (Appendix F). In conflict with 
this evidence are characters 19 (calyx lobes ob- 
tuse and apiculate) and 5 (parallel evolution of 
pedunculate inflorescences), which suggest that 
A. hartwegiana and A. campanensis are sister 
species. Additional data will be required to sat- 
isfactorily resolve these relationships. 

The A. pulcherrima complex includes about 
25 species that occur only in South America (Ap- 
pendix A). These species received only cursory 
attention in the course of this research and have 
not been incorporated into the phylogeny. It is 


all South American species. Rath 
Central American groups described here has 
South American members. The Central Ameri- 
can species thus represent more than one evo- 
lutionary line from the older continent. As de- 
tailed in the taxonomic treatment, several species 
apparently have closer relatives among South 
American members of the complex than among 
species treated here. Further study of South 
American species of this complex will permit 
expansion of the phylogeny to include all species 
of the monophyletic group. The complete clado- 
gram will facilitate formulation of biogeographic 


134 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


TABLE 13. Characters and character states used in TABLE 13. Continued. 
MESE analysis. Asterisks denote hypothesized 


primitive states. For multistate characters with an in- 


14. Bracteal nectaries, position 


termediate state primitive, two-directional evolution 0 Sub-medial 
is hypothesized. *1 Medial 
2 Supra-medial 
1. Habit 15. Floral bracts, orientation 
*0 Plane 
1 Shrub/small tree ] Recurved 
2. Pubescence of distal stem, density 16. Bracteoles, shape 
parse *0 Lance-ovate 
1 Moderate 1 Slightly falcate 
2 Dense | i 2 Falcate 
3; prer of distal stem, orientation 17. Bracteoles, color 
0G 
*1 Upwardly appressed 1 Brightly colored 
Downwardly appressed 
: 18. Calyx, length 
4. Pubescence of distal stem, length *0 6-10 
*0 to 0.5 mm mora 
ists dias ] 11-15 mm 
2 i iig: 2 16-20 mm 
„ым 19. Sepals, E. shape 
. *0 Аси 
à i 
: аа 1 ой and apiculate 
: 20. Sepals, color 
6. Floral bracts, margin *0 G 
*0 Toothed | i 1 1 
1 Occasional minute teeth ER 
2 Entire 21. Corolla, texture 
* 
7. Floral маа texture ы —À 
n ме А Coriaceous 
1 саа маме 
2 the 22. Corolla, length 
8. Floral bracts eee 
*0 Imbricate ELEM 
i Tax $ 6.1-7 cm 
>7 cm 
9. Floral bracts, color . 
90 Caen 23. Corolla, width upper lip 
1 Brightly colored 1 ~ 5 URN 
10. Floral icm length 29.5-11.5 mm 
*1 8.5-14 mm с: 
514.422 0; 24. Corolla, apical shape upper lip lobes 
3 22 5-30 ae *0 Acute to acuminate 
сз 1 Emarginate and apiculate 
и Рита ыны acis 25. Corolla vem pubescence 
*0 Acute 0 Glabrous 
1 Cibtuse *1 «0.25 mm 
2 
12. Bracteal nectaries inpia 
Мау minds 26. Corolla, pubescence of lower lip 
1 Few large 2 и 
à | .25 mm 
13. ME gang diameter 2 0.26-0.75 mm 
1 0.25-0.75 mm OD m 
20.76-1 mm 27. Corolla, color 
3 51 m *0 Red, pb orange 


1 Yello 


1984] 


TABLE 13. Continued. 


28. Anther, length 
0 mm 


*1 3.5-6 mm 
2 6.5-9 mm 
3 >9 mm 
29. Stigma, morphology 
Bilobed 


1 Oblique 
30. Fruit, shape 
*0 Flattened 
1 Terete 
31. Fruit, color (immature) 
*0 Other 


1 Orange-brown 
32. Fruit, color (immature) 
*0 Other 
1 Black 


33. Fruit, length 
*0 <20 mm 


35. Seed, shape 


36. Seed, diameter 
0 <4 mm 
*1 4.5-6 mm 
2 >6.5 mm 
37. Germination pattern 
*0 Epigeal 
1 Semi-hypogeal 
38. Pollen, shape (L/W) 
*0 L/W < 2.1 
1 L/W > 2.1 
39. Pollen, colpi 
*0 Tricolpate 
1 Syntricolpate 
40. Pollen, «€ 
*0 Continuou 


1 анна bands 
41. Corolla opening 
*0 Delayed 
1 Immediate 
42. Corolla, vestiture 
*0 Pubescent, glabrous 
1 Papillate 
43. Fruit, shape 
*0 Stipitate 
1 Sessile 


McDADE—APHELANDRA PULCHERRIMA 135 


hypotheses based on phylogenetic relationships 
and distributional patterns. 


COMPARISON OF RESULTS FROM ARTIFICIAL 
HYBRIDIZATIONS AND PHYLOGENETIC ANALYSIS 


The results of artificial hybridizations can be 
compared with two measures of relationship de- 
rived from phylogenetic analysis: number of hy- 
Mn ds speciation events (cladistic distance) 

r of inferred evolutionary changes 

Co iita distance) between species. Both dis- 
tances are significantly correlated with cross- 
ability indices for each pair of species (r = 0.442, 
cladistic distance; r — 0.560, patristic distance; 
57 df, P « 0.001 for both coefficients). More spe- 
cific comparisons of the results of the two anal- 
yses are made using Figures 55 and 58. Phylo- 
genetic analysis separates the species into two 
lineages (Fig. 58). Crossability indices generally 
support this division but suggest an intermediate 
position for A. leonardii (species 9) between the 
two groups (Fig. 55). Both analyses closely link 
A. terryae, A. sinclairiana, A. storkii, A. golfo- 
dulcensis, A. gracilis, and A. panamensis (species 
1-6). The phylogenetic hypothesis that A. dep- 
peana and A. panamensis are sister species is 
supported by high crossability between the two 
(Table 11). Aphelandra deppeana has several 

: ide denen а E 


uniqueiy E 
it from other species of Group I (Fig. 58). Low 
crossability of A. deppeana with other species of 
Group I corroborates its distinctiveness (Table 
it, Fig. 35) 

The most apparent difference in the results of 
of Group II (species 8—13). Phylogenetic analysis 
suggests that species of Group II are as closely 
interrelated as those of Group I. The available 
results of artificial hybridizations, however, in- 
dicate that these species do not cross readily (Ta- 
ble 11, Fig. 55). This conflict illustrates the dif- 
ficulty encountered in using artificial crossability 
to estimate relationships. The rigidity of genetic 
incompatibility barriers to hybridization be- 
tween species is apparently not reliably чиа: 
ed with phylogenetic relationships. Thee 
of other i 1 
distant relatives separated by effective barriers 
9А, habitat, different pollinators) may remain 

ross-compatible while sister species lacking ad- 
ditional isolating mechanisms may be highly in- 
tersterile. Thus, if genetic incompatibility is rel- 
atively unimportant as a barrier to interbreeding 


136 


1TE 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


йр IL 


[e] 
8LING 9LEON 10 LAX 11 CAMP 12 HART 13 


5 
41 
9 о 40 1 
D 6 1 
1 j 
35-1 
ан ph 26 4-0 
13-9 1 
25-—ў- 0 
key gi 72 
4а - 1 
А à 
3 о 
URE 58. Phylogenetic tl ntral American species of the Ар ЧИ 
Prec complex. . Eac h species is located d the upper horizontal of the diagram. Evolution of uniquely 
derived and unreversed character states is indicated by horizontal slashes, with numerals to the left indicating 


the ye character and those | to the right Мини the state мина ~ у ај terminal intervals are identified 


by letter. Total 1 


for each interval. Appendix F provides a complete listing 


of dad changes by interval. 


among species of Group I, then the results of 
artificial hybridizations may provide reliable es- 
timates of degree of phylogenetic relationships 
among these species. In Group II, genetic incom- 
patibility may be more important, resulting in 
strong intersterility barriers between species. 


TAXONOMIC TREATMENT 


Aphelandra R. Br., Prodr. 475. 1810. LECTOTYPE: 
A. cristata Jacq. 


Synandra Schrader, Gótt. Gel. Anz. 1: 715. 1821, non 

bre 181 
Raf., Fl. “tellur. 10: 65. 1838. 

урина prid Klotzsch in Otto & Dietrich, Allg. Gar- 
tenzeitung 7: 307. 1839. 

на TIE S Otto & Dietr., Allg. Garten- 

ung 10: 285. 1842. 

Hemisandr Scheidw., de Acad. Roy. Sci. Bruxelles 

9:2 


Lagochlun gos in Martius, Fl. bras. 9: 85. pl. 10. 
1847 


trees; stems terete to quadrangular, soft-wooded, 
rarely thick and succulent, glabrous to pubescent, 
nodes frequently swollen. Leaves opposite, rarely 
verticillate or alternate, petiolate; the blades 
membranous to coriaceous, marginally toothed, 
lobed, crenate, undulate or entire; stipules lack- 
ing or present as interpetiolar spines. Inflores- 
cences of terminal spikes, solitary to few, ог nu- 
rous and arranged freely branching 
paniculate inflorescence; each flower subtended 
е 


ing lateral glandular areas (“осе 
two, laterally subtending calyx, usually lan lan ee 
late, similar to sepals in shape and texture, rare y 
rudimentary. Calyx of 5 subequal, usually lan- 
ceolate sepals, the adaxial sepal, and the abaxi 


1984] 


and lateral pairs of unequal width; corolla straight 
or curved, limb 5-parted, nearly regular to 
strongly bilabiate with a basically bilobed upper 
lip (the lobes sometimes partially or completely 
united) and a reflexed 3-lobed lower lip, the lobes 
of the lower lip subequal to strongly dimorphic 
with lateral lobes reduced or essentially lacking; 
stamens four, epipetalous, rarely included within 
corolla tube, usually exserted beyond throat but 
not extending beyond tip of upper lip, anthers 
usually borne erectly, within or closely parallel- 


McDADE—APHELANDRA PULCHERRIMA 


137 


ing upper lip, narrow, one-celled; stigma infun- 
dibular, entire or shallowly bilobed, style fi- 
liform, frequently extending through and slightly 
beyond the adaxial pair of anthers, ovary biloc- 
ular with two ovules per locule. Fruits capsular, 
clavate to sub-globose, terete to strongly flat- 
tened, 4-seeded, explosively dehiscent on drying, 
seeds borne on hook-like retinacula, brown, 
rounded to somewhat angled and strongly flat- 
tened to sub-globose. Seed germination epigeal 
or semi-hypogeal. 


KEY TO THE CENTRAL AMERICAN SPECIES OF THE APHELANDRA PULCHERRIMA COMPLEX 


1. Bracteal nectaries composed of a few (1-10) well-defined glands each 0.5—1.25 mm in diameter; capsules 


terete in cross-section or nearly so; seeds sub-globose аре Aes < UIN 
2. Corolla less than 4.5 cm long; S Mexico to N South Ameri 
n 


2’. Corolla exceeding 5 c 


7. A. deppeana 


ү 


m lo 
3. Bracts consistently bearing 2-3 pairs of marginal teeth, each 1-2 mm long; capsules sessile; 
leaves epetiolate; central and eastern Panama . А. panamensis 
3'. Bracts a entire or sog bearing 1—2 pairs of minute teeth (< 1 mm long); capsules 
stipitate; leaves with distinct petio 
4. Plants profusely нар ched T to signs trees qe many short (to 20 cm) rv ina 
terminal paniculate inflorescence; У о broadly ovate, to 20 mm lon 
5. Bracts green ih. occasionally dull bro , narrowly ovate to ovate, to 7 mm wide. 
6. Bracts 5-8 mm long, виса и internodes 7- 10 mm long; leaves glabrous, 
slightly coriaceous and shiny; central Pan 4. A. gracilis 
6'. Bracts >8 mm long, slightly to closely њива leaves pubescent, membranous, 


and dull. 
7. Bracts sli obtu урау b f distal 
stems erect; corolla на eie entrat Panama... A gracilis x каны 
10 Bracts i mbricate Loe acute, minutely puberalent pubescence of distal st 
downwardly app N Cos indere eu dins 
ama piis cse im 


5'. Bracts bright orange, CE ovate, 8-20 m ide. 
8. Corollas 5.7-6.2 cm long; distal stems, p ides and bracts sparsely pubescent; E 
Panama and Colombi . A. terryae 
8. pio 6.4—7.1 cm long; distal stems, leaves and bracts moderately pubescent to 


9. goes 16-21 mm long, 14-20 mm tide pena pubescent; distal stems рон, 
trichomes erect; anthers 7—8 mm lo р 
S Costa Rica to Е Panama 24 АН 
9'. Bracts 9-13.5 Eee long, 5-9 mm wide, sparsely pubescent; distal stems mod- 


erately pubescent, trichomes downwardly appressed; anthers Ts 6–6.5 mm long, 
shriveled and jere little pollen; plants sterile; P Сома Rick с a 
· golfodulcensis х x sinclairiana 
4'. Di 4 41. 
spikes; bracts | ea و‎ suc >25 mm ego Costa Rica Е апа Heredia) £s 


3. A. storkii 
Bracteal nectaries of many (> 50) minute glands forming oblong patches 2-5 mm in diameter; capsules 
strongly flattened; seeds strongly flattened (diameter/width > 3/1). 
10. Corolla 5.5-6 cm long; plants rarely taller than 1.5 m; immature capsules orange-brown; SW 
Costa Rica, Panama, and Colombia 8. A. lingua-bovis 
. Corolla adio. than 6 cm; plants taller than 1.5 m when reproductive; immature capsules green 
or yellow-green. 
ll. Bracts non-imbricate, separated by internodes 1.5-2 cm long; Panama (San Blas) __ 10. А. /axa 
11’. Bracts imbricate, internodes not visible at anthesis. 
cts r rhombic-ovate, 7-10 mm long, 5-7 mm wide; bracteoles lanceolate; р Rica 
— A. leonardii 
12'. Bracts broadly ovate, 11-40 mm long, 9-26 mm wide; bracteoles slightly to markedly 
alcate. 


, 


© 


13. Bracts to 14 mm long, planar; sepals longer than bracts; capsules to 31 mm long. 
14. Bracts 9-11 mm wide; bracteoles slightly falcate, 11—13 mm long; sepals 15- 


138 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог, 71 


18 mm long; I" orange; capsules 20-24 mm long; S Costa Rica (Limón) 


to central Pan 


. A. campanensis 


= 


. Bracts 11-14 m 


31 mm long; E Pa 


1. Aphelandra terryae Standley, Publ. Field Mus. 
Nat. Hist., Bot. Ser. 22: 381. 1940. TYPE: 
Panama. Darién: Chepigana District, Tu- 
cuti, ca. sea level, Terry & Terry 1377 (ho- 
lotype, F; isotype, GH) 

Ane incarnata Leonard, Contr. p 8. Natl. Herb. 

242. Фан TYPE: Colombia. er: vicin- 
г ‘of B nca Bermeja, Maddis Valley, 100- 
500 m, poe 1315 (holotype, US). 


Shrubs 1—4 m high, profusely branching: youn- 
ger stems subquadrangular, moderately pubes- 
cent, the trichomes downwardly appressed, white, 
about 0.25 mm long, older stems terete, glabrate. 
Leaves opposite (very rarely alternate), oblan- 
ceolate, 20-30 cm long, 6–10 cm wide, apicall 
acuminate (the tip acute or blunt), basally atten- 
uate and decurrent on the petiole, marginally en- 


pubescent, the trichomes appressed, white, about 
.25 mm long; petioles 1-2 cm long, sparsely 
pubescent, the trichomes appressed, white, about 
0.25 mm long; leaves subtending inflorescences 
much reduced, 7-11 cm long, 2.5-4 cm wide 
essentially glabrous. Inflorescences gipa 
spikes numerous, terete, 3-8 cm lon ng, 1-2 с 
wide, arranged in a freely branching асаа: 
inflorescence; the peduncles 2.5-4 cm long, mod- 
erately pubescent, the trichomes erect, white, 
about 0.25 mm long; rachis minutely puberu- 
lous; lowermost 1-2 pairs of bracts leaf-like, 1— 
2 cm long, 0.5-1 cm wide; floral bracts imbricate, 
broadly ovate, Bug obtuse, marginally entire, 
10-12 mm ‚ 8-10 mm wide, orange, fre- 
quently (е ир = green at base, glabrous within, 
moderately pubescent without, the trichomes ap- 
pressed, white, 0.5-0.75 mm long, margins mi- 
nutely ciliolate, the nectaries medial, composed 
of several (5-12) individual glands, each 0.5— 
0.75 mm in diameter; bracteoles narrowly ovate, 
apically acute, 4.5-6 mm long, 2-2.5 mm wide, 
orange fading to green toward base, glabrous or 
with moderately pubescent keel, the trichomes 
appressed, white, about 0.5 mm long. Sepals 6— 
7 mm long, apically acute, greenish orange, es- 
sentially glabrous, the adaxial segment narrowly 


~ 


TRO bracteoles strongly falcate, 7-10 mm long; sepals 17- 
22 mm long; corolla yellow (rarely eha У and extremely coriaceous; capsules 
28- anama and Colo 2. А. 

13’. Bracts 30-40 mm long, apically геси 
anthesis; capsules about 35 mm long; Panama (Dari 


artwegiana 
гуед; itus Е" than bracts, not visible at 
én) 13. A. darienensis 


ovate, 3-4 mm wide, the abaxial pair lanceolate, 
2-2.5 mm wide, the lateral pair narrowly lan- 
ceolate, 1.25-1.5 mm wide; corolla pink or or- 
ange, 5.7—6.2 cm long, sparsely pubescent except 
lower lip moderately pubescent, the trichomes 
erect, white, 0.5—0.75 mm long, the tube 42-45 
mm long, about 3 mm in diameter at base, con- 
stricted to about 1.5 mm above ovary (7 mm 
above base), expanding to 6—7 mm deep at throat, 
the upper lip erect, ovate, 16-18 mm long, 7.5- 
11.5 mm wide, bilobed, the lobes triangular, 8- 
9 mm long, anther pocket well-developed, the 
middle lobe of lower lip broadly lanceolate, 23- 
26 mm long, 7-8 mm wide, minutely apiculate 
at apex, the lateral lobes about 1 mm long an 

6—7 mm wide; filaments inserted 11 mm from 
base of corolla tube, free portion of each about 
4 cm long, the anthers 5-6 mm long, extending 
4—5 mm from tip of upper lip, pollen pale orange; 
stigma pink, minutely bilobed, the style filiform, 
extending 3-5 mm beyond the anthers, the ovary 
apically red, glabrous. Capsules clavate, terete, 
glabrous, green with red-tinged apex when im- 
mature, becoming dark brown to black at dehis- 
cence, 17-19 mm long, 4.5—6 mm wide, 5-6 mm 
thick, strongly constricted 4-5 mm above base 
to form narrow stipe; seeds dark brown, 3-45 
mm in diameter, 1.5-2 mm thick. Seed germi- 
nation semi-hypogeal. 


Habitat and distribution. This species occurs 
in eastern Panama in the provinces of Darién 
and San Blas, and in adjacent Colombia. Aphe- 
landra terryae is found primarily in lowland for- 
ests (occasionally to 500 m elevation) where se 
sonality of rainfall is not pronounced [tropical 
moist and wet forests (Holdridge, 1967)]. Indi- 
viduals of this species are found in n gaps in pri- 
mary f trails) 


Flowering and fruiting. Peak flowering is 
during the driest months ofthe year (Dec. thro 
March). Fruits mature during the late dry se2507 
and early wet season. 

Leonard (1953) described A. incarnata, based 
on Colombian plants, as distinct from A. 57" 
clairiana, and apparently overlooked the earlier 


——————————HÉH——uIÓ——————— —|ÓM4M— YÍÁtÀ EE eeEO m 


1984] 


description of essentially identical Panamanian 
plants as A. terryae by Standley (in Standley & 
Steyermark, 1940). Although I have been unable 
to study Colombian plants in the field, herbar- 
jum specimens are not distinguishable from col- 
lections of A. terryae. I therefore concur with 
Wasshausen’s (1975) decision to synonymize A. 
incarnata Leonard under A: terryae Standley, 

Plants of A. terryae are di 
relatives by their overall sparse vestiture, size 
and color of the bracts, short inflorescences and 
corollas, and green, glabrous capsules. 


from close 


Relationships. Aphelandra terryae is a mem- 
ber of Group I, which includes species with brac- 
teal nectaries of individual, large glands. Phy- 
logenetic analysis indicates that it is most closely 
related to A. sinclairiana and A. storkii (Fig. 58). 
These three species share bright orange floral 
bracts, bracteoles and sepals, and long trichomes 
on the corollas. 


Additional specimens examined. PANAMA. DARIEN: 

slopes of Cerro Pirre, Mori & Kallunki 5516 (MO); 
Rio Pirre near town of Pirre, Gentry & Clewell 6937 
(F, MO); Rio Pirre near crossing of trail from EI Real 
5187 vey trail 
Allen ges (A, MO, US); 
Cerro Piriaque, Tyson et al. 381 5 (DUKE, ory MO): 
trail from Pucuro to Cerro Mali, ridge between Pucuro 
and Tapalisa Rivers, Gentry & Mori 13550 (MO); near 
e at hydrocamp on Rio Morti, Duke 15421 (US). 

SAN BLAS: mainland opposite Achituppu, Lewis et al. 
126 (GH, MO, шыр 

COLOMBIA. ANTIOQUIA: along Rio Anori, Zaragoza, 
500 m, Soejarto & Villa 2734 (GH); Malena, 140-160 
m, ii 3782 (US); between Río Guapá and León, 
10 m, Yepes et al. 18300 (US); La Llorona near Da- 
beiba, highway to Mutatá, Barkley & Guttierez 35442 
Me BOLIVAR: Boca Verde, on Río Sint, Pennell 4581 


E and Colorado Rivers, 100-500 m, Haught 2098 
NY, US). 


2. Aphelandra sinclairiana Nees in Benth., Bot. 
Voy. Sulphur 146. pl. 47. 1844. TYPE: Pan- 
ama. Province not given, Sinclair s.n. (ho- 
lotype, K, not seen). 


Shrubs 2-6 m high, profusely branched; stems 
terete, younger surfaces moderately pilose, tri- 
chomes erect, white, 1-1.5 mm long, older sur- 
faces sparsely pilose to glabrate. Leaves opposite, 
elliptic to oblanceolate, 20–30(–40) cm long, 6– 
1015) cm wide, apically acuminate to atten- 


McDADE—APHELANDRA PULCHERRIMA 


139 


uate, basally attenuate and decurrent on petiole, 
marginally entire to slightly undulate, upper sur- 
face sparsely strigose, the trichomes appressed, 
white, about 1 mm long, sparingly pilose below 
(moderate on veins), the trichomes appressed 
(erect on veins), white, about 1 mm long; petioles 
1–2 cm long, sparingly pilose, the trichomes erect, 
white, 1–1.25 mm long. Inflorescences terminal, 
spikes numerous, terete, 8—15(-20) cm long, 2 
cm wide, arranged in a freely branching panicu- 
late inflorescence; peduncles lacking or to 6 
ст long, moderately pilose, the trichomes erect, 
white, 1–1.25 mm long; rachis densely pubes- 
cent, the trichomes erect, white, about 0.5 
long; lowermost 2—3 pairs of bracts sterile and 
leaf-like; floral bracts densely imbricate, broadly 
obovate, apically obtuse, marginally entire or with 
2-3 pairs of minute teeth, 16—20 mm long, 14- 
20 mm wide, orange, densely minutely puberu- 
lous within, densely pubescent without, the tri- 
chomes appressed, white, about 0.25 mm long, 
margins ciliate, the trichomes white, 0.5–0.75 
mm long, the nectaries medial, composed of sev- 
eral (4-10) individual glands, each about 0.5 mm 
in diameter; bracteoles narrowly ovate, apically 
acute, 7-9 mm long, 2-3 mm wide, orange, mod- 
erately pubescent, the trichomes appressed, white, 
about 0.25 mm long. Sepals 7-9 mm long, api- 
cally acute, orange, striate, very minutely puber- 
ulous, the adaxial segment oblong, 2-3 mm 
wide, the abaxial pair lanceolate, 2 mm wide, the 
lateral pair lanceolate, 1.5 mm wide; corolla pink 
or orange-red (rarely white), 6.5—7 cm long, mod- 
erately pubescent, the trichomes erect, white, 0.5— 
0.75 mm long, the tube 48-50 mm long, 3 mm 
in diameter at base, constricted slightly to 1.5— 
2.5 mm above ovary (8-11 mm above base), 
expanding to 8-10 mm deep at throat, the upper 
lip ovate, 16-20 mm long, 9-10 mm wide, bi- 
lobed, the lobes triangular, 7-9 mm long, anther 
pocket well-developed, the middle lobe of lower 
lip elliptic, 25-29 mm long, 8-10 mm wide, re- 
curled slightly at tip, the lateral lobes 1-2 mm 
long, 8-9 mm wide; filaments inserted about 11 
mm above base of corolla tube, free portion of 
each about 5 cm long, the anthers 7-8 mm long, 
extending to within 2-6 mm from tip of upper 
li , minutely bilobed, 
the style filiform, ‘extending 2-5 mm beyond an- 
thers, the ovary glabrous. Capsules clavate, te- 
rete, dark brown to black when immature and at 
PETES very minutely puberulous, 23-25 mm 
g, 6-7 mm wide, 5-6 mm thick; seeds dark 
pace te orbicular, slightly flattened, 5-6 mm in 


, pollen ink 


140 


diameter, 2-3 mm wide. Seed germination semi- 
hypogeal. 


Habitat and distribution. Aphelandra sin- 
clairiana ranges from southern Costa Rica to 
eastern Panama (Fig. 56). In Costa Rica, nu- 
merous collections of this species have come from 
the wet Caribbean lowlands of southern Limón 
province. A collection from Atirro, Cartago b 
Donnell Smith in 1896 is apparently A. sinclair- 
iana, but lack of collections between this locality 
and southern Limón make it difficult to deter- 
mine the northern limit of this species. This is 
true as well of the eastern distributional limit: in 
addition to numerous collections from central 
Panama (east to Cerro Brewster), one specimen 
from the Pacific coast of the Darién is apparently 
of this species. Additional collections from in- 
tervening areas, particularly the Caribbean low- 
lands of San Blas and Bocas del Toro will help 
to resolve the distributional limits of this species. 

Aphelandra sinclairiana i is primarily a species 

f th ’s (1967) 
tropical moist forest]. Although it is not found 
in areas with severe dry seasons of long duration, 
it does occur in seasonally partially deciduous 
forests that experience a 2-4 mont ип B pen 09 with 
clairiana ос occurs in small to ines gaps in ‘Primary 
forest, b 
Alth d primarily a lowland species, it occurs 
occasionally at mid-elevations (to 1,200 m), es- 
pecially where disturbed cloud forests [premon- 
tane wet forests (Holdridge, 1967)] are located 
at the crest of the central mountain range adja- 
cent to extensive lowland, seasonally dry areas. 


Flowering and fruiting. Individuals flower 
during the driest months ofthe year (Dec. through 
March) with apparently very little variation. Most 
plants have completed fruiting by the onset of 
the wet season. 


Aphelandra sinclairiana may be readily distin- 
guished from other species by its pilose stems, 
leaves and corollas; large, bright orange bracts; 
citrus-like odor of the inflorescences and dis- 
tinctively colored, puberulous capsules. There is 
some variability in bract size and, most notably, 
corolla color in this species. I have found plants 
with pink, red-orange, and white corollas at the 
same locality. These секи аге apparently 
not of systematic importanc 


Relationships. Phylogenetic analysis indi- 
cates that A. sinclairiana is most closely related 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


to A. storkii. These two species share erect, pilose 
pubescence of stems and floral structures. Aphe- 
landra sinclairiana crosses readily with А. ter- 
ryae, A. golfodulcensis, and A. gracilis (Table 11). 
Where geographic and elevational isolation break 
down, it hybridizes readily with the latter two 
species. 


Additional specimens examined. СоѕтА RICA. CAR- 
TAGO: Atirro, 600 m, Donnell Smith 6694 (GH, US). 
py Río 86 а drainage, Shank & Molina 

545 (Р); Ri 


ger et al. 10420(D 
ton 124 (US) 
NAMA. BOCAS DEL TORO: vincinity of Chiriqui La- 
goon, von Wedel 1083 (GH, MO, US); Changuinola, 
0-6 , Lewis et al. 803 (GH, MO, US); pe 


Bratsi, 10– 
UKE, EX Tiu inci Valley, qs 


i 
US); El Copé, 250 m, MeDaniel & Cooke 14831 (FSU, 
MO). COLON: edge of forest along Pipeline Road ca. 10 
km of Gamboa, Wilbur & Teeri 1 3365 (DUKE, 


n 
iin 2239 (F, MO), McDade 289 (DUKE); W end of 
ап Lake Dam, Вит & Tyson 1975 (FSU, МО); 


a 
Hansen 14047 (DUKE, MO, WIS); 5 mi. SW of Cerro 
Brewster, 1,000 ft., Lewis et ‘al. 3316 (DUKE, F, МО, 


); slopes of Cerro Campana, 
2,500–2,900 ft., Wilbur 24367 (DUKE). 


3. Aphelandra storkii Leonard, Publ. Field Mus. 
Nat. Hist., Bot. Ser. 18: 1197. 1938. TYPE: 
Costa Rica. Limon: Livingston, Río Reven- 
tazón, Rowles & Stork 690 (holotype, US): 


Shrubs 1-3 m high, sparsely branched; stems 
нер, younger surfaces moderately pilose, the 
trichomes erect, white, about 1 mm long, older 
surfaces glabrate. Leaves opposite, obovate 10 
broadly ПРЕ, 30-45 cm long, 15-20 cm 
ae ies te (the tip acute or blunt). 
basally long attenuate and decurrent on petiole, 
marginally entire to crenulate, sparsely strigose 
above, the trichomes appressed, white, about 0. 75 


erect, white, about 1 mm long; petioles 1 
long, densely pilose, the trichomes erect, white: 


س ی ٠٦٠٠٨٠٦٠‏ و анааан‏ = 


1984] 


about 1 mm long. Inflorescence terminal, spikes 
usually single (rarely 2—5), terete to subquadran- 
gular, 15-25(-45) cm long, about 2 cm wide; 
peduncles 1-3 cm long (to 5 cm below lateral 
inflorescences), densely pilose, the trichomes 
erect, white, about 1 mm long; rachis densely 
pubescent, the trichomes erect, white, about 0.5 
mm long; bracts imbricate, rhombic oblong- 
ovate, apically acute, marginally entire or bear- 
ing 2-3 minute teeth along each edge (each about 
1 mm long and 0.25 mm wide), orange, 25-30 
mm long, 13-18 mm wide, minutely puberulous 
within, moderately pubescent without, the tri- 
chomes appressed, white, about 0.5 mm long, 
margins ciliate, the trichomes white, about 1 mm 
long, the nectaries medial, composed of 10-15 
individual glands, each about 0.5 mm long and 

mm wide; bracteoles lanceolate, apically 
acute, 9-14 mm long, 2-4 mm wide, pale orange, 
moderately pubescent, the trichomes ascending, 
white, about 0.25 mm long. Sepals 13-17 mm 
long, apically acute, pale orange, striately nerved 
moderately pubescent, the trichomes erect, white, 
about 0.25 mm long, the adaxial segment broad- 
ly lanceolate, 3.5-7 mm wide, the abaxial pair 
lanceolate, 2-4 mm wide, the lateral pair nar- 
rowly lanceolate, 1-2 mm wide; corolla orange, 
6.5-7.5 cm long, moderately tomentose, the tri- 
chomes erect, white, about 0.5 mm long, fre- 
quently twisted, the tube 48-56 mm long, 4—5 
mm in diameter at base, constricted to 2.5-3 mm 
above ovary (8 mm above base), expanding to 
6-8 mm deep at throat, the upper lip erect, el- 
liptic, 17-20 mm long, 10-15 mm wide, bilobed, 
the lobes triangular, acuminate, 8-11 mm long, 
anther pocket well-developed, the middle lobe 
of lower lip elliptic, 27-30 mm long, 9-12 mm 
wide, acute, the lateral lobes about 2 mm long 
and 5-6 mm wide; filaments inserted 9-10 mm 
from base of corolla tube, free portions about 5 
cm long, the anthers 7-9 mm long, extending to 
within 5-6 mm of tip of upper lip, pollen orange; 
stigma very pale orange or uncolored, minutely 
bilobed, the style filiform, extending 1-7 mm 
beyond anthers, the ovary glabrous. Fruits cla- 
vate, terete, glabrous, green when immature, be- 
coming black-brown at dehiscence, 28-32 mm 
long, about 7 mm wide, 5-6 mm thick; seeds 
brown, angularly orbicular, slightly flattened, 5- 
7 mm in diameter, 3-4 mm thick. Seed germi- 
nation semi-hypogeal. 


Habitat and distribution. This species is en- 
demic to the Caribbean lowlands of northeastern 


McDADE—APHELANDRA PULCHERRIMA 


141 


Costa Rica, occurring in forests with slight sea- 
sonal differences in rainfall [tropical wet to pre- 
montane wet forests (Holdridge, 1967)]. Aphe- 
landra storkii is found in the understory of 
primary forest and in gaps of varying sizes, but 
rarely in extensively disturbed areas. 


Flowering and fruiting. Aphelandra storkii 
flowers during the wettest months of the year 
(July through Nov.). Fruits are matured during 
the driest months of the year (Jan. to March). 


This species may be readily distinguished from 
all other Aphelandras by the combination of 
monocaulous growth form and pilose pubes- 
cence of leaves and stems, distinctively colored 
floral bracts and corollas and large size of the 
bracts, calyx, and corolla. The few collections 
known of A. storkii show little morphological 
variability over its limited range. 


Relationships. Among Central American 
species of Group I, A. storkii is most closely re- 
lated to A. sinclairiana. It is a distinctive species 
with many uniquely derived character states. 
پوو‎ of this specum may be found i in 

ith Ameri sp 
ps peor она 4 aristei Leonard, and А. 
trianae Leonard bear at least a superficial resem- 
blance to A. storkii (Leonard, 1953). 


Additional specimens examined. СоѕтА Rica. 
HEREDIA: past town of Pto. Viejo on road to Rio Frio, 
100 m, McDade 232 (DUKE); Finca La Selva, along 
Rio Pto. Viejo near town of Pto. Viejo, 100 m, Grayum 
2361 (DUKE), McDade 350 (DUKE), Opler 988 (F, 
MO), Sperry 650 (DUKE), Sperry 765 (DUKE), Sperry 
831 (DUKE), Wilbur 33599 (DUKE); Rio Bijagual, 2 
km E of Tirimbina, Maas 1324 (US). 


4. Aphelandra gracilis Leonard, Proc. Biol. Soc. 
Wash. 56: 54. 1943. ТУРЕ: Panama. Coclé: 
N of El Valle de Antón, 1,000 m, Allen 2908 
(holotype, US; isotypes, AAH, MO). 


Shrubs or small trees, 2-7 m high, profusely 
branched; younger stems quadrangular, moder- 

ately pubescent, the trichomes upwardly ap- 
pressed, white, 0.25—0.5 mm long, older stems 
terete, glabrate. Leaves opposite, elliptic to ovate, 
10-20 cm long, 5-8 cm wide, apically acuminate 
(tip acute or blunt), basally acute or attenuate 
and decurrent on petiole, marginally entire, 
somewhat coriaceous and shiny, essentially gla- 
brous above (few trichomes on veins), essentially 
glabrous below although sparsely pubescent on 
veins, the trichomes appressed, white, about 0.25 
mm long; petioles 1-2 cm long, moderately pu- 


142 


bescent, the trichomes appressed, white, about 
0.25 mm long. Inflorescences terminal, spikes 
solitary or 2—5, terete, 8—12(—15) cm long, about 
1 cm wide, sessile; the rachis sparsely pubescent, 


long, bracts ovate, apically а acute, marginally en- 
tire, 5—8 mm long, m wide, green, gla- 
brous within, рну ene towards tip of 
midvein without, the trichomes appressed, white, 
about 0.25 mm long, margin sparsely and mi- 
nutely ciliolate, the nectaries medial, quo 
of few (3-7) individual glands, each 0.5 mm 
AT binis е оуаїе, кшй 
cute, 4—6 mm long, 1.5-3 mm wide, green, es- 
duds Ойка or witha iv trichomes toward 
apex, these appressed, white, about 0.25 mm long. 
Sepals 7—9 mm long, apically acute, green, striate 
with narrow hyaline margins, essentially gla- 
brous, the adaxial segment narrowly ovate, 2.5— 
4 mm wide, the abaxial pair lanceolate, 2-3 mm 
wide, the lateral pair narrowly lanceolate, 1—1.5 
mm wide; corolla pink or orange-red, 6.5-7 cm 
long, minutely puberulous with erect trichomes, 
e tube 48—50 mm long, 3 mm in diameter at 
base, constricted to about 1.5 mm above ovary 
(5-7 mm above base), expanding to 8-10 mm 
deep at throat, the upper lip erect, ovate, 16-17 
mm long, 9-12 mm wide, bilobed, the lobes tri- 
angular, apiculate, 6-9 mm long, anther pocket 
well-developed, the middle lobe of lower lip el- 
liptic, 23-26 mm long, 8-10 mm wide, acute, 
the lateral lobes about 1 mm long, 5-6 mm wide; 
filaments inserted about 12 mm above base of 
corolla tube, free portion of each 4.3—4.6 cm long, 
the anthers 5-6 mm long, extending to within 4— 
6 mm from tip of upper lip, pollen cream-col- 
ored; stigma not distinctively colored, very mi- 
nutely bilobed, the style filiform, extending 1-3 
mm beyond anthers, the ovary glabrous. Cap- 
sules clavate, terete, green when Мана a 
at Ce 20-22 mm long, about 6.5 m 
wide and 4.5 mm thick; seeds brown, Өй. 
slightly flattened, 3.5~5 mm in diameter, about 
m wide. Seed germination semi-hypogeal. 


Habitat and distribution. Aphelandra graci- 
lis is restricted to the provinces of Veraguas, Co- 
clé, Colón and Panamá in central Panama (Fig. 
56). It occurs from 700 to 1,200 m elevation in 
wet cloud forest t habitat, and at lower elevations 


frequently ем climate [Holdridge' 5 (1976) 
р forests]. The 


рі emontan 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


species is apparently limited to primary forest 
and is unable to survive in open areas. 


— and fruiting. Flowering occurs 

e driest months of the year (late Dec. 

= jene March), and fruits are matured 
uring the late dry and early wet seasons. 


3 


Aphelandra gracilis is readily distinguished 
from all other Aphelandras treated here by its 
small green bracts that are distantly spaced along 
the rachis and its glabrous, slightly coriaceous 
and somewhat shiny leaves. Both field and her- 
barium studies suggest that hybridization be- 
tween n pua ee A е occurs in 
area occur 
кунуна to seasonally dry ди Mid premontane 
habitats on the Pacific slope of the central moun- 
tain range of Panama. Hybrids between these two 
species are quite vigorous and are intermediate 
in bract size, color, and spacing; leaf texture and 
pubescence; and overall plant pubescence. Col- 
lections of these hybrid plants have previously 
been identified as A. gracilis, A. sinclairiana, ог 
the South American species A. pilosa. The mis- 
PCM i of hybrid plants from El Llano 
m (Durkee, 1978) is readily 


much smaller bracts than are typical of this 
species, resulting in a superficial resemblance of 
these plants to A. pilosa. 


Relationships. The bracteal nectaries, fruit 
and seed shape, and germination pattern of 4. 
gracilis place it in Group I. Within Group |, its 
green bracts ally it with A. golfodulcensis, A. pal 
amensis, and A. deppeana. 


Additional specimens examined. PANAMA. one 
vicinity of El Valle de Antón, 700–1,200 m, ‚Наа 
Allen 311 (US), Allen 1671 (Е, GH, NY), Gentry 


km abo erAm. 

from El Llano to Carti-Tupile, 150- 0-350 m, Kennedy 
& Dressler 2954 (MO), Mori & Kallunki e (MO) 
Cerro Jefe, about 10 km past Goofy Lake, > + 
po 386 (DUKE), Nee 9291 (MO), Gentry f 

90 (MO), Gentry & Mori 13432 (F, MO), Wilbur 
a 1132 #24 “ghee Gorgas Mem orial Labs researe 
camp, km NE of Altos de злива — pe Mori 
& aha 3343 (MO); slopes of Cerro Cam y 
m, Smith & Smith 3356 (F, US), ze 22793 E, МЕ 


ааз & Dressler 726 (МО yau past 
ta Fé, а road past Escuela Aol, По 5 С 
Tute, 800—1,200-m, od: 23038, 34200 (MO), беп? _ 
62 


pg 


| 
1 


47 (МӨ): E 
Putative hybrids between A. gracilis and A. sin¢ | 


1984] 


. COCLE: vicinity of El Valle, 500—700 
m, my 1671, ^300 (US), Dwyer 11845 (МО), Lewis 


n 
Nee et al. 8873 (MO), Croat 22891 (MO). 


5. Aphelandra golfodulcensis McDade, Ann. 
Missouri Bot. Gard. 69: 405. 1982 [1983]. 
TYPE: Costa Rica. San José: vicinity of El 
General, beside Rio Chirrip6, Skutch 2573 
(holotype, MO; isotypes, A, GH, NY, US). 


Shrubs or small trees 1-6 m high, profusely 
branching; stems terete, younger stems densely 
pubescent, oming moderate to sparse on old- 
er surfaces, the trichomes downwardly ap- 
— white, about 0.75 mm long. Leaves op- 
posite (very rarely alternate), elliptic to 

Мел. л, 25-30(-45) cm long, 12-15 cm 
wide, apically acute to acuminate (the tip acute 
or blunt), basally attenuate and decurrent on pet- 
iole, marginally entire or slightly undulate, upper 
surface essentially glabrous, sparsely pubescent 
on veins, the trichomes appressed, white, about 
0.5 mm long, moderately pubescent below, the 
trichomes appressed (erect on veins), white, about 

.75 mm long; petioles to 1 cm long, moderately 
pubescent, the trichomes erect, white, about Чә 
mm long; leaves subtending i 
reduced, 3-6 cm long, 1 1-2.5 cm wide, pubes- 
cence as of cauline leaves. Inflorescences ter- 
minal, spikes numerous, terete, 3-15 cm long, 
0.75—1 cm wide, arranged in a freely branching 
paniculate inflorescence; the peduncles 0.5-10 
cm long, moderately pubescent, the trichomes 
erect to downwardly appressed, white, about 0.75 
mm long; the rachis minutely puberulous, the 
trichomes erect, white; bracts imbricate, rhom- 
bic-ovate, apically acute, entire, 8—13 mm long, 

mm wide, green to dull brown-orange, gla- 
brous to sparsely papillate within, minute puber- 
ulous without, the trichomes appressed, white, 
margin ciliolate, the trichomes white, about 0.25 
mm long, the medial, composed of sev- 
eral (1-7) individual glands, each about 0.75 mm 
long and 0.5 mm wide; bracteoles narrowly ovate, 
apically attenuate, 4–6.5 mm long, 2—4 mm wide, 
green, moderately puberulous, the trichomes ap- 
pressed, white. Sepals 6-9 mm long, apically 
acute, green, finely striate, minutely puberulous, 
the trichomes appressed, white, the adaxial seg- 
ment narrowly ovate, 3—4 mm wide, the abaxial 
pair broadly lanceolate, 2–2.5 тт wide, the lat- 

pair narrowly lanceolate, about 1.5 mm wide; 
corolla orange to red, 6.3-7.3 cm long, minutely 


McDADE—APHELANDRA PULCHERRIMA 


143 


puberulous, the trichomes erect, white, the tube 
about 4.7 cm long, 2—3 mm in diameter at base, 
slightly constricted above ovary (6 mm above 
base), expanding to 6–8 mm deep at throat, the 
upper lip erect, elliptic, 17-19 mm long, 7-11 
mm wide, bilobed, the lobes triangular, acumi- 
nate, 6-10 mm ik anther pocket well-devel- 
oped, the middle lobe of lower lip broadly lan- 
ceolate, 22-26 mm long, 6-9 mm wide, 
acuminate, the lateral lobes 1-3 mm long, 5—7 
mm wide; filaments inserted about 15 mm above 
base of corolla tube, free portion of each about 
4 cm long, the anthers 6-8 mm long, extending 
to within 5 mm from tip of upper lip, pollen very 
pale orange; stigma red, slightly bilobed, the lobes 
about 0.5 mm long, the style filiform, extending 
3-5 mm beyond anthers, the ovary glabrous. 
Fruits clavate, terete, glabrous, green when im- 
mature, turning black-brown at dehiscence, 19— 
23 mm long, 5-8 mm wide, 5.5-7 mm thick. 
Seeds dark-brown, orbicular, slightly flattened, 
4—6 mm in diameter, 2.5-3 mm wide. Seed ger- 
mination semi-hypogeal. 


Habitat and distribution. Aphelandra golfo- 
dulcensis is found primarily in the tropical wet 
forests (Holdridge, 1967) of the Golfo Dulce re- 
gion of Puntarenas province, Costa Rica (Fig. 
56). Its range extends into the adjacent Burica 
Peninsula of Panama (Chiriquí province), to mid- 
elevations above the Golfo Dulce region [pre- 
montane rain forests (Holdridge, 1967)], and to 
the north into Alajuela and Guanacaste prov- 
inces where local conditions result in a climate 
substantially wetter and less seasonal than is typ- 
ical of these areas. The plants occur as understory 
shrubs in primary forests and also colonize 
successional and edge habitats. 


Flowering and fruiting. Peak flowering oc- 
curs during the dry season (late Dec. through 
March). Fruits mature rapidly and few individ- 
uals still bear fruits when the wet season begins 
in this area. 


ІГ. к MA ` 


Plants of A. g been 
referred to A. sinclairiana. Morphological fea- 
tures distinguishing these two species include 
bract size, color, and pubescence; corolla tube 
vestiture; fruit color and pubescence; and overall 
vestiture of the plants. Data from artificial hy- 
bridizations support recognition of the two as 
distinct but closely related (Table 11). Several 
collections of putative hybrids between А. gol- 
fodulcensis and A. sinclairiana are known from 


144 


northeastern Costa Rica. These plants are sterile 
and are morphologically intermediate between 
the two parental species, most notably in vesti- 
ture of leaves, stems and corollas, and bract size 
and color. 


Relationships. Aphelandra golfodulcensis isa 
member of Group I and is phylogenetically most 
closely related to A. gracilis, A. panamensis, and 
A. deppeana (Fig. 58). 


Additional specimens ee Costa RICA. 
ALAJUELA: vicinity of Capulin о о Grande de Таг- 
coles, 80 m, Standley 40160 ae Santiago de San 

Ramon, Brenes 662 E GUANACASTE: El Are- 
it Sta ndley & Valerio 45 105 (US). PUNTARENAS: ca. 


Hwy., Burger & Matta-U. 4646 (F, MO, NY), McDade 
378 (DUKE); Esquinas forest, between Río Esquinas 
and Palmar S., Allen 5775 (F, GH, US); Golfo Dulce 
and Río Térraba, За 5406 (Е, E ohne of Santo 
Domingo de Golfo Dulce, Tonduz 9969 (NY, US); 
Rincón de Osa, рина Gentry 8851 ©, <i 
covado National Park, sea level, McDade 401 (DU 

Canas Gordas, Pittier 111 93 (US); ca. i mi. from ч 
Vito de Java, Las Cruces Botanical Garden, McDade 


5 
~" 


1 KE). SAN JOSE: Rio Ут. vicinity of El Gen- 
eral, Skutch 3941 oe NY, US); Rio Chirripó del 
c dpud and Chimiról, ord Tos. 

ner 7117 (F, M 
AMA. CHIRIQUÍ: Pto. Armuelles, 1 mi. W of air- 
port, Croat 21884 ЧЕ, MO, : i. S of Pto. 
Armuelles, died et al. 13583 (DUKE, F); San Bar- 
tolo Limite nea i border, 12 mi. W of Pto. 


Armuelles, 400-500 m, Croat 22194 (DUKE, MO). 
_ Putative ый between А. golfodulcensis and A. 
Costa Ел 


Guapiles, 280 m, Carpenter 373 (US), eer 1 у 09 
(US), Carlson 3457 (F, US); cg = Santa Clara, 
650 ft., Donnell Smith 4 917 (GH, Santa Clara, 
Las Delicias s, 500 m, Biolley 10669 4 Rio Chirripó, 
hwy. from Rio Frio to Guapiles, Poveda 991 (Е). 


6. Aphelandra panamensis McDade, Ann. Mis- 
souri Bot. Gard. 69: 402. 1982 [1983]. TYPE: 
Panama. Panama: slopes of Cerro Jefe, past 
Goofy Lake and large coffee finca, 800 m 

McDade 411 оне DUKE; isotypes, Е, 

MO). 


~ 


Shrubs ог small trees 1-6 m high, sparsely 

ranched; stems terete, younger stems densely 
pubescent, the trichomes upwardly appressed, 
white, 0.5–0.75 mm long, older surfaces glabrate. 
Leaves EP narrowly elliptic, 15-18(-22) 
cm long, 3–6.5 cm wide, apically acuminate to 
acute, basally attenuate and decurrent on the pet- 
iole, y entire or undulate, the upper sur- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


face of youngest leaves sparsely pubescent, gla- 
brate with age, lower surface moderately 
pubescent, the trichomes appressed, white, about 
0.5 mm long; petioles lacking or to 5 mm long, 
densely pubescent, the trichomes erect, white, 
about 0.5 mm long; uppermost leaves subtendi 
inflorescences frequently reduced. Inflorescences 
terminal, spikes usually solitary (rarely to 5), te- 
г .2 ст wide, sessile; the 


cate, narrowly rhombic-ovate, apically atten- 
uate, marginally with 2-3 pairs of teeth (each !- 
2 mm long), 11-15 mm long, 6-8 mm wide, 
green to pale dull orange, sparsely pubescent 


mm long, the hectaries A compo of sev- 
5-1 bout 0.5 mm 
p and 0.3mm wide; veste. lanceolate api- 
cally acute, 6-10 mm long, 1.5-2. m wide, 
straw-colored or green, glabrous except ore and 
apically sparsely pubescent, the trichomes erect, 
white, about 0.75 mm long. e 8-12 mm 


| 


adaxial segment narrowly ovate, 3-5 mm wide, 
the abaxial pair lanceolate, 2-3 mm wide, the 
lateral pair narrowly lanceolate, 1.5-2 mm wide; 
corolla bright red, 5.5-7 cm long, minutely pu- 
berulous except tip of lower lip sparsely pubes- 
cent, the tube about 5 cm long, 2.5-3 mm in 
diameter at P. constricted to 1.5 mm above 
ovary (about m above base), expanding t0 
—7 mm deep at t throat the upper lip erect, el- 
liptic, 14-20 mm long, 6-8 mm wide, bilobed, 
the lobes triangular, acute, 5-7 mm long, anther 
pocket poorly developed, the middle lobe of low- 
er lip narrowly elliptic, 18-23 mm long, 4-7 mm 
wide, acute, tip strongly curled back toward tube, 
the lateral lobes about 0.5 mm long and 3 mm 
wide; filaments inserted about 5 mm above базе 
of tube, free portion of each about 5 cm long, 
the anthers 4—5 mm long, extending to WI within 2- 
3 mm of tip of upper lip, pollen very pale yellow; 
stigma not distinctively colored, oblique and ар- 


ااا ———" 


=" 


Т0 


"= 


—————" 


1984] 


5.5-7 mm thick; seeds dark brown, irregularly 
orbicular, slightly flattened, 4–6 mm in diameter, 
2-3 mm thick. Seed germination semi-hypogeal. 


Habitat and distribution. Aphelandra pana- 
mensis is known only from central and eastern 
Panama in the provinces of Coclé, Colón, Pan- 
amá, San Blas, and Darién. It occurs in wet cloud 
forest habitats, predominantly above 600 m el- 
evation, but occasionally lower where local cli- 
matic conditions result in high rainfall and fre- 
quent fog cover [Holdridge's (1967) premontane 
wet and premontane rain forests]. Individuals of 
this species are primarily understory shrubs of 
primary forest, but are found in advanced sec- 
ondary forest as well. 


Flowering and fruiting. Peak flowering oc- 
curs in the wet season (Sept. to Dec.) and fruits 
mature during the driest months of the year (late 
Dec. to early March). There is, however, consid- 
erable asynchrony among individuals at some 
sites. Notably, at Santa Rita Ridge, in the prov- 
ince of Colón, flowering individuals can be col- 
lected during most months. 


The combination of toothed bracts with extra- 
floral nectaries and the 5.5—7 cm long corolla 
serve to distinguish A. panamensis from other 
species. Specimens of A. panamensis have pre- 
viously been referred to А. deppeana from which 
it may be readily distinguished. The two species 
differ in habit, leaf vestiture, corolla length, and 
fruit size and color. They are found in different 
habitats and are pollinated by two distinct groups 
of hummingbirds 


Relationships. Within Group I, A. panamen- 
sis and A. deppeana are sister species, sharing 
toothed bracts, oblique stigmas, sub-globos 
fruits, and villous pubescence ofthe lower corolla 
lip. Artificial hybridizations indicate that A. pan- 
amensis crosses readily with all other species of 
Group I. 


Additional specimens examined. PANAMA. COCLE: 
N of El Copé, near sawmill, 600-750 т, Berg & 

pti 2770 (US). COLON: ca. 7 mi. from Transisthm. 
wy., Santa Rita Ridge, Wilbur et p 15078 (DUKE), 
MeDade 283, 388 (DUKE), Smith & Smith 3433 (US). 


, US), Wilbur et al. 11316 
ait. Lewis et al. 282 (DUKE, MO, US). SAN BLAS: 
ween Rio Diablo and Rio Acuati near Nargana, 

Duke 14887 (US). 


McDADE—APHELANDRA PULCHERRIMA 


145 


7. Aphelandra deppeana Schldl. & Cham., Lin- 
naca 5: 96. 1830. TYPE: Mexico. State not 
given, Hacienda de la Laguna, Schiede & 
Deppe s.n. (holotype, B, destroyed, not seen; 
F photo 8704 in US) 


tress pectinata Nees in DC., s 117 297. 

TYPE: Colombi not given, Rio 

ú. Си иттг 1099 (lectotype, K. ed in US). 

Aphelandra h оа ees in r 11:298. 

E: Mexico. Veracruz: Co rdillera de Ve- 

pe ‘Galea 909 (lectotype, US; isolectotypes, 

Aphelandra dukei Wassh., Phytologia 25: 475. 1973. 

TYPE: Panama. Panamá: Río Bayano, 1-4 mi. 

above Aer 100 m, Duke 14397 (holotype, US; 
isotype, MO). 

Shrubs 1- : m high, pre MeV 
rately to- 
mentose, the BAR Rd Ка ы, Eg 0.75- 
1 mm long, twisted and somewhat matted, older 
stems terete, glabrate. Leaves opposite, elliptic, 

15-22 cm long, (1.5-2-)5-8 cm wide, apically 
acute to short attenuate, basally attenuate and 
decurrent on petiole, marginally entire to un- 
dulate, both surfaces moderately tomentose 
(dense on veins below), the trichomes erect, white, 
0.75-1 mm long, curling; petioles lacking or to 
1 cm long, densely pubescent, the trichomes ap- 
pressed, white, 0.5—0.75 mm long. Inflorescences 
terminal, spikes solitary or more frequently sev- 
eral (3-7), terete to sub-quadrangular, 8-12(-19) 
cm long, about 1 cm wide, sessile; the rachis 
moderately pubescent, the trichomes erect, white, 
about 0.5 mm long; bracts densely imbricate, 
broadly elliptic, apically long attenuate, margin- 
ally with 2—4 pairs of short teeth (1-2 mm long, 
0.5 mm wide) on each side, 13—16 mm long, 6– 
8 mm wide, green to dull orange, glabrous within, 
moderately pubescent without, the trichomes ap- 
pressed, white, about 0.5 mm long, margins cil- 
iate, the trichomes 0.75-1 mm long; the nectaries 
medial, composed of several (2—5) individual 
glands, each about 1.25 mm long and 0.75 mm 
wide; bracteoles lanceolate, apically long atten- 
uate and acute, 6–8.5 mm long, about m 
wide, green to pale orange, sparsely pubescent, 
the trichomes appressed, white, about 0.25 mm 
long. Sepals 8-9.5 mm long, apically acute, green 
to dull orange, glabrous except ciliate near apex, 
the trichomes white, about 1 mm long, the adax- 
ial segment narrowly ovate, about 3 mm wide, 
the abaxial pair lanceolate, about 1.5 mm wide, 
the lateral pair narrowly lanceolate, about 1 mm 
wide; corolla pink, orange, or red, 36-41 mm 


youngest stem 


146 


long, moderately pubescent, the trichomes erect, 
white, 0.25–0.5 mm long (except trichomes of 
lower lip 1 mm long), the tube 27-29 mm long, 
2 mm in diameter at base, constricted to 1-1.5 
mm wide above ovary (5 mm above base), ex- 
panding to 4-5 mm deep at throat, the upper lip 
erect, elliptic, 11– 13 mm long, 5-6 mm wide, 
bilobed, the lobes triangular, 3—4 mm long, acute, 

anther pocket poorly developed, the middle lobe 
of lower lip narrowly oblong, strongly recurved 
at anthesis, 14-15 mm long, 3-4.5 mm wide; 
filaments inserted about 5 mm above base of 
corolla, free portion of each 2.5-2.7 cm long, the 

thers 3-4 mm long, extending to within 2-4 
mm from tip ofupper lip, pollen cream or yellow; 
stigma Bot сопло У Colored, е ars hol- 
low ends 0.5- 
pi mm "beyond ‘anthers, the ovary peg 
Capsules globose, terete, green when immature, 
turning brown-black at dehiscence, 13-17 mm 
long, 5-6 mm wide, 5-6.5 mm thick; seeds brown, 
orbicular, slightly flattened, 3.5-4.5 mm in di- 
ameter, 2-3 mm wide. Seed germination semi- 
hypogeal. 


Habitat and distribution. Ranging from 
southern Mexico through Central America south 
to Bolivia and east to Surinam, Aphelandra dep- 


in the genus. It is the шой xerophytic of the 
species treated here and is found primarily in 
seasonally dry lowland euer [tropical dry to 
moist forests (Holdridge, 1967)], occasionally 
ranging to mid-elevations on leeward slopes. In 
Costa Rica and Panama, it is a common under- 
story shrub in the seasonally deciduous forest 
and shrub communities of the Pacific low 

and colonizes the disturbed secondary and edge 
habitats now common in these regions. 


Flowering vd fruiting. Flowering occurs 
primarily duri 


ability among individuals at some sites and un- 
usual individuals can be found in flower at most 
times of year. 


This species is readily distinguished from all 
other Central American Aphelandras by the 

combination of short oe (36—41 vaste and 
toothed bracts with extra nectaries. Al- 
though there is some алые, among pth 
tions from different areas of the range, especially 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


in leaf morphology, this species is remarkably 
uniform and is easily recognized. 

Wasshausen (1973a) described A. dukei as a 
distinct species on the basis of its very narrow 
(1.5-2 cm) leaves. I consider A. dukei to be a 
morphological variant of A. deppeana pes 

offi No 


for 


er morphological characters consistently sepa- 
rate the two; inflorescence characters are essen- 
tially uniform. Pollen grains of A. dukei are 
identical in size and ultrascułpturing to those of 
A. deppeana. The habitats of the two are identical 
and narrow-leaveđ plants are known only from 
within the range of A. deppeana. Narrow-leaved 
individuals have been collected from three lo- 
cations in eastern Panama. 


Relationships. Phylogenetic analysis indi- 
cates that A. deppeana and A. panamensis share 
several derived character states and are sister 
species. Aphelandra deppeana possess uniquely 
derived states of many characters, suggesting that 
it is a very divergent member of Group I. Cross- 
ing relationships corroborate this hypothesis: A. 
deppeana crossed readily only with its sister 


are perhaps related to its xerophytic habitat and 
weedy nature. Especially noteworthy are the short 
corollas that are apparently reduced from the 6- 
7 cm length considered primitive for this group. 
This change may have functional signi 


occur 


ы 
in areas with harsh dry seasons. The only avail 
able hummingbird pollinators in such areas are 
species with relatively short bills. 
Among South American species, comparative 

morphology suggests that А. /asia Leonard 15 the 

only close relative of A. deppeana (Leonard, 
1953). Plants of this Colombian species are dis- 
tinguished from A. deppeana by their longer Co 
rollas and larger and more densely pilose bracts 
with few, if any, minute teeth. 

Additional specimens examined. МЕХІСО. CAM- 
PECHE: beyond Hopalchen on Campeche e-Mérida road, 


9 km N of Tuxtla Gutierrez, 2, 500 ft., , Breedlove | 1 КА 


(US); 5.6 mi. 

Shilom Ton 2950 (DUKE, US); 13 km N of 

along Hwy. 195, 830 m, Breedlove 28299 ооа 
along road. from El Bosque to Simojovel, ! 
Shilom Ton 3076 (DUKE). GUERRERO: wy. US; 
mi. E of Acapulco, 400 ft., Carlson 3066 (DUKE, 
Valleci : 


у рат ] е 
pulco, Moore 8124 (US); between Сери» and Ju 


— „aai 


1984] 


huis. 200-600 ft., Nelson 2297 (US). ОАХАСА: Te- 
huantepec, pesco, S of Tres Cruces, 3,000 ft., 
MacDougall H56 (US); E of La Soledad, near Mitla, 


(US); 
m, Martinez-Calderón 254 (US); Cerro 
mingo, d is of Juchitan, 240 m, Conzatti 3735 (US). 
QUI : 


Co osamaloapan, 10 m, Martinez-Calderón s.n. м 
along river i e Catemaco, region 


1 
(US); Uxmal, Degener & De- 
gener 26785 (US); Coba, Crockett 150 (US); Progreso, 
Steere 3012 (US); vicinity of Chiceh, Gaumer 23798 
(US). 


GUATEMALA. ALTA VERAPAZ: near Pancajche, 900 m, 
Standley 91831 (US); Sacolal, 3,000 ft., Turckheim 
825 (US); 1 km past Tucuru on road from Tactic to 
El Estos, 1,400 ft., McDade 211 (DUKE). CHIQUIMULA: 

ween Esquipulas and Ataluapa, 800 m, Molina & 
Molina 25346 (US); 3 mi. SE of Quetzaltepeque, 1,200- 
1,500 m, Steyermark 31291 (US). ESCUINTLA: SE of 
Escuintla along Río Michatoya, 250-300 m 
89138 (US); San Antonio Jut m 
sé, sea level, Standley 64076 (US). 
GUATEMALA: Sanarate, m, Kellerman 6653 (US). 
HUEHUETENANGO: El Reposo, 900-1,000 m, Williams 
et al. 41247 (US); slopes above Río Selegua, 6,100 ft., 
Harmon 4801 (US). 1zABAL: between Сеја and Cienaga, 
Ortiz 2299 (US); vicinity of Quirigua, 75—225 m, Stan- 
Феу 23910 (US). JALAPA: between Jalapa and San Pe- 
dro Pinula, 1,400-1,800 m ЖТ 77087 (US). 
JUTIAPA: Jutiapa, 850 m, Standley 75 1 
Parque Nacional де , Tun Mh n. (DUKE, US); 
Ceibal, 150 m, Molina 15861 (US); San Clemente de 

S Arroyos, Bartlett 12827 (US). QUETZALTENANGO 
Colomba, 1,900 ft., Skutch 1370 (US). RETAL 
between Nueva Linda and Champerico, 120 m, Stan- 
dley 87650 (US); Retalhuleu, Kellerman 6584 (US). 
SANTA ROSA: i 


S 
А ul, 1,370 ft, Donnell Smith 
154 (US). SUCHITEPEQUEZ: Patulul, 330-600 m, Stan- 
Феу 62184 (US). zacAPA: above Teculutan, 250-275 
m, Steyermark 42150 (US); road between Zacapa and 
Chiquimula, 500-660 m, Standley 73849 (US). 
BELIZE. BELIZE: Gracie Rock on Western Hwy., Croa 
23905 нон um Mt. Polo group, Bartlett 71349 


TOLEDO: Monkey Ri River, Pine veas Gentle 3774 (US). 
LSALVADOR ACHAPÁN: Ahuachapán, 800-1, 
m, Standley 19893( (US). LA UNION: La Union, 150 m, 
Standley 20672 (US). MORAZAN: N of Montecristo (NE 
of San Miguel), 200 m, Tucker 450 (US). SAN SALVA- 
Pis Tonacatepeque, Standley 19440 (US). SAN vic- 
E: San Vicente, 350-500 m, Standley 21220 (US). 
мати mea San Antonio del Monte, 250 m, Standley 
22166 (US). 
ONDURAS. COMAYAGUA: Siguatepeque, 1,100 m, 


McDADE—APHELANDRA PULCHERRIMA 


147 


Williams & Williams 18475 (US). cortés: San Pedro 
5 S). EL PARAISO: road to 
ORAZAN: Cerro 


NICARAGUA. CHINANDEGA: Chinandega, Baker 2057 
pate CHONTALES: Cuapa, Marshall & Neill 6675 
KE). ESTELÍ: Pueblo Nuevo, 600-700 m, Williams 
& Prec 42405 avs ). MANAGUA, , Tipi- 
tapa, Atwood 2825 (WIS). MATAGALPA: 5-10 km W of 
Matagalpa, 600-700 m, Williams et al. 23801 (US). 
NUEVA SEGOVIA: кон Hamblett save (WIS). RIVAS: 
С) јр & Smith 146 
(US); near Tola d Rivas, White pi 54 (US). 

CosTA RICA. ALAJUELA: Grecia, Jimenez 1142 (US); 
Turrubres near San Mateo, Biolley 7075 (US); Atenas, 
Schubert & Madriz 1036 (US). GUANACASTE: 5 mi. N 

of Cañas along InterAm. Hwy., 50 m, ee кар 
377 (DUKE); ‘San ta Rosa National Park, 
of Liberia, wie 25092 (DUKE); Bahia el ssi piel 
Sardinal, 0- 


Utley 3644 (DUKE). PUNTARENAS: near Quepos an 
aranjo, 20-150 m, Burger et al. 10543 (DUKE) 

са. 10 mi. before Palmar N. on InterAm. Hwy 

Paso Real and Palmar N., McDade 290 (DUKE): 8 

km NE of Buenos Aires, 600 m, Wilbur 25266 (DUKE); 

Las Cruces Botanical Garden, ca. 8 km from San Vito 

de Java, 1,200 m, McDade 396 (DUKE). 

PANAMA. CHIRIQUÍ: 17 km NE of San Felix, new road 
to Cerro Colorado Copper Mines, 1,000 m, Nee 10680 
(US); 12.4 mi. N of David, Lewis et al. 718 (US). 
СОСТЕ: Ola, 100—350 m, Pittier 5036 (US); El Valle de 
Antón, 600 m, Lewis et al. 2595 (DU Е 
Punta Garachiné, ا‎ 
Mori & Gentry 4245 (MO). H RA: between Las Mi- 
nas and Pesé, Oliver 1 349 (U ©); О Ocú, Sens et al. 1738 


a 
munition Depot, Wilbur et al. 12893 (DUKE, US); 
near Miraflores locks, Croat 12729 (DUKE); between 
Las Sabanas and Matias Hernandez, Standley 31911 
(US); Taboguilla Island, Miller 1999 (US); Taboga Is- 
land, Standley 27864 (US); Rio Bayano, 1—4 mi. above 
Piria, Duke 14397 (MO, US); cai to B Valle de An- 
tón, ca. km 18 from Inter. ., Wilbur et al. 1558 
(DUKE); along InterAm. Es x near Jenine, Río Ca- 
fita, Duke 3840 (US). vERAGUAs: 11 km S of Santa 
Fé, 220 ei Nee 8153 (US); Soná, 500 m, Allen 1042 
bed NW of Atalaya, 100 m, Nee 8253 (US). 
= BOLÍVAR: San Martín де Loba, Curran 
99 (US); Sincelejo, ne 4057 (US); vicinity " pad 
Loi Heriberto 357 (US). BovAcÁ: San Anto 
Río Cusiari, 10 km above Maní, 250 m, Haight: 2613 
S). META: San Juan de Arama, Rio Guejar, 500 m, 
Idrobo & Schultes 1223 (US); 65 km E of Villavicencio, 


Meta, Cuatrecasas 4195 (US); 
sanare, Esmeralda, 130 m, Cuatrecasas 3816 (US). 
VAUPÉs: Cerro де Mitü, 380 m, Cuatrecasas 6878 (US). 
VICHADA: 10 km W of Las Gaviotas along road to Pto. 


148 


Gaitan, 180 m, Davidse 5344 (US); 7 km NE of San 
ih de Ocuné, 100 m, Hermann 10973 (US). 
. AMAZ ОМА. 5: Alto Orinoco, Salto Salas, 
Chae 513 (US); Alto Rio Orinoco, 30 km above 
Santa Barbara, 125 m, Maguire et al. (US); 12.5 km S 
of Pto. E 230, m, E Pen LA 
ANZOÁTEGUI: on Cara 
Boca d е Оен Peres а гу Ta ey a APURE: 
bank k of Rio М 19 WSW of Paraquito, 75 m, 
Davidse & Gonzalez 13973 (US). BOLivAR: 14 km SE 
of Caicara along Hwy. 19 to Cd Bolívar, TE m, Da- 
vidse 4338 (US). GUARICO: 14 km tagracia 
de "pies pus to s ucagera, 420 m, Davide 4160 
(US). s Mochima Hwy. between Cu- 
maná а 20 Іа rer 250 m, Davidse 5032 (US). 
GUYANA. Mee geal Falls, Atkinson 59 (US); junc- 
tion of Mazaruni and Cu т Graham 336 
(US); Ahyma, Dem erara hive: above Wismar, Hitch- 
cock 17419 (US); = of НЕ along coast, 
Hitchcock 16916 (US 
URINAM. Lower Saramacca River, Betti Creek, Jon- 
ker-Verhoef & John 539 (US). 


8. Aphelandra lingua-bovis Leonard, Contr. U.S. 
Natl. Herb. 31: 268. 1953. TYPE: Colombia. 
Chocó: La Concepción, 15 km E of Quibdó, 
75 m, Archer 2012 (holotype, US). 


Shrubs 1-2 m high, very sparsely branched or 
more frequently unbranched; younger stems 


mm long, older stems terete and glabrate. Leaves 
opposite, elliptic to obovate, 20-35(-45) cm сар 
11—17 cm wide, apically Пу acute 
to slightly attenuate, marginally entire to crenate, 


chom veins sel sce 
увере энә on veins), the trichomes зон 
white, about 0.5 mm long; petioles 0.5-6 с 
long, moderately pubescent, the inem ap- 
pressed, white, about 0.5 mm long. Inflorescence 
terminal, spikes solitary (rarely 2—3), quadran- 
gular, 20-35(-70) cm long, 1.2-1.5 cm wide; pe- 


the trichomes erect, white, about 0.5 mm long; 
bracts closely fitting but not imbricate, 2—4 pairs 
of sterile bracts subtending spikes, floral bracts 
narrowly rhombic-ovate, apically attenuate and 
acute, entire, red-orange, 12-17 mm long, 7-11 

abrous within, sparsely and minutely 
сеен. without, keel sometimes with а паг- 
row band of trichomes, margin sub-hyaline, very 
finely ciliolate, the nectaries medial, about 2.5 
mm long and 1-1.5 mm wide, composed of many 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


minute glands; bracteoles linear-lanceolate, api- 
cally acute, 11-17 mm long, 2-3.5 mm wide, 
pale orange, glabrous except keel densely pubes- 
cent, the trichomes erect, white, 0.5-0.75 mm 
long. Sepals 12—18 mm long, apically acute, pale 
orange, minutely puberulous except few longer 
trichomes near tips, these appressed, white, about 
0.5 mm long, the adaxial segment narrowly ovate, 
3.5-8 mm wide, the abaxial pair lanceolate, 2- 
3.5 mm wide, the lateral pair narrowly lanceo- 
late, 1.5-2.5 mm wide; corolla red-orange or pink- 
orange, 5.5-6 cm long, minutely papillate, with 
few scattered trichomes, coriaceous, the tube 4- 
4.4 cm long, 3.5-5 mm wide at base, scarcely 
HE x ат + hant тт 


deep at throat, the upper lip erect, broadly ovate, 
10-12 mm long, 7-9 mm wide, bilobed, the lobes 
triangular, 2.5-3.5 mm long, minutely apiculate, 
anther pocket well-developed, the middle lobe 
of lower а со reflexed at anthesis, narrow- 
ly ovate, 15-17 mm long, 6-7 mm wide, mi- 
nutely aco i ‘the lateral lobes about 1 mm 
ng, 4-5 mm wide; filaments inserted about 5 
mm above base of tube, free portion of each 
about 40 mm long, the anthers 5—6.5 mm long, 
extending to within 2-5 mm of tip of upper lip, 

pollen light yellow; stigma not distinctively col- 
ored, minutely bilobed, the style filiform, €x- 
tending 1-2 mm beyond anthers, the ovary 
glabrous. Fruits oblong, flattened, oval in cross- 


— 
о 


tened, 4-6.5 mm in diameter, 1.5-2 mm wide 
Seed germination epigeal. 


Habitat and distribution. атаа lin- 
gua-bovis is a species of lowland, premo ntane 
middle elevation 1 jurc (to 


bia. The Panamanian distribution of this species 
is difficult to establish with certainty since co! 
lections from the entire Caribbean slope of 
country are as yet very incomplete. The plants 
are understory sub-shrubs of wet forests that €x- 
perience only a very short dry season, an are 
limited to minimally disturbed sites. 
Flowering and fruiting. Aphelandra eer 
bovis flowers during the wettest months 0 
year (July through Nov.) and matures fruits P 
ing those months with least rainfall. 


ава.‏ ا 


1984] 


Individuals of this species may be identified 
by their diminutive size, narrowly rhombic-ovate 
floral bracts that are 12—17 mm long and apically 
attenuate, linear-lanceolate bracteoles, and rel- 
atively short corollas. There is considerable vari- 
ation among specimens, especially with respect 
to leaf texture and bract size. Collections are as 
yet too few, however, to discern any geographic 
patterns of variability. 

Costa Rican plants referred by Leonard (1938) 
to the Venezuelan species A. micans are properly 
placed in A. lingua-bovis. Leonard also reported 
collections of A. micans from Guatemala, but I 
have found no indication that A. micans occurs 
in Central America or that A. /ingua-bovis ranges 
north of southwestern Costa Rica. 


Relationships. The phylogenetic relation- 
и: of as lin ngua- -bovis remain incompletely re- 
solve laced it as the bas- 
al species of the Central American lineage sharing 
minute bracteal nectaries (Group II, Fig. 58). Ar- 
tificial hybridizations and distribution patterns 
of the states of many characters, however, in- 
dicate that its relationships with this group are 
more distant than the interrelationships of the 
remaining five species. More closely related 
species probably occur in South America, in- 
cluding A. garciae Leonard, A. longispica Leon- 
ard, and A. straminea Leonard (Leonard, 1953). 


Additional specimens examined. СоѕтА RICA. 
LIMON: Rio Valle Estrella drainage, Shank & Molina- 
ar pi he and Rio и 

10627 (Е); betwee 
a, 30 m, Skutch 5284 (Р, 
US); са. 10 km SE of Eu N. along InterAm. Hwy., 
ca. 20 m, Burger & Matta-U. 4650 (DUKE, US); ca. 
10 km E of Golfito, 50 m, Lent 424 (F, MO); Rincón 
de Osa, 20-300 m, Liesner 1883 (MO); vicinity of 
Tinoco station, between Río Esquinas and Palmar, 3 
m, Allen 5477 (F, US); between Palmar N. and Pto. 
Cortez, 50 m, Jimenez-M. 2245 (F); Rincón de Osa, 
SW of airstrip, 20-60 m, Utley & Utley 1060 (DUKE); 
5 km W of Rincón de Osa, 50-200 m, Burger & Liesner 


cinity of Las Cruces Botanical Garden, 1,200 m, Raven 
22017 (F, NY), McDade 442 (DUKE). SAN José: low 
hills ju Río Paquita, 5-50 m, Dodge & Goerger 
9883 (F, MO). 

PANAMA. © COLÓN: Río Guanc 1-4 km upstream 
from Portobelo road, 1-100 m, uot 8783 d 


(DUKE); near bridge over Río Buenav 
Portobelo, sea level, Foster & Kennedy 1794 (D UKE), 
McDade 383 (DUKE). DARIEN: ascent of Cerro Pirre 


McDADE—APHELANDRA PULCHERRIMA 


149 


from Rio Pirre S of El Ааа 750-1,030 m, Duke 5329 
(MO), McDade 429 (D 

COLOMBIA. да near Villa Arteaga, hwy. to 
sea, Hodge 7012 (F, US). ВОУАСА: Mt. Сћароп, NW 
of Bogota, extreme W part of Воуаса, Lawrance 18 
(GH). cHocó: Rio Atrato, Tanando, 60 m, Cuatrecasas 
& Llano 24118 (US); Rio Taparal off San Juan, 30 m, 
Robinson 229 (US); between La Oveja and Quibdó, 
Archer 1731 (US). 


9. Aphelandra leonardii McDade, Ann. Mis- 
souri Bot. Gard. 69: 408. 1982 [1983]. TYPE: 
Panama. Panama: Majé, about 5 mi. up Rio 
Nuevo, a branch of Rio Majé, Foster & Ken- 
nedy 1993 (holotype, DUKE; isotypes, F, 
MO) 


Shrubs 1—5 m high, profusely branching; youn- 
ger stems quadrangular, sparsely pubescent, the 
trichomes upwardly appressed, white, about 0.5 
mm long, older stems terete, glabrate. Leaves 
opposite, obovate to elliptic, 10—20(—30) cm long, 
4—10 cm wide, apically acuminate, basally acute 
to attenuate, marginally entire to slightly undu- 
late, upper surface glabrous, lower surface gla- 
brous to sparsely pubescent except veins sparsely 
to densely pubescent, the trichomes appressed, 
white, 0.5—0.75 mm long; petioles 0.3-1.5 cm 
long (rarely to 3 cm), sparsely pubescent, the 
trichomes appressed, white, about 0.5 mm long. 
Inflorescence terminal, spikes solitary to numer- 
ous, quadrangular, 3.5-14 cm long, 0.8-1 cm 
wide, sessile or rarely very short pedunculate; 
rachis sparsely pubescent, except frequently 
densely pubescent just below insertion point of 
each bract, the trichomes erect, white, about 0.5 
mm long; 2-3 pairs of imbricate, densely pu- 
bescent sterile bracts borne below fertile bracts, 
the trichomes appressed, white, about 0.75 mm 
long; floral bracts barely imbricate, pe. di 
ovate, apically acute, marginally entire, 7-10 m 
long, 5-7 mm wide, green to bright orange, a 
brous within, sparsely and minutely puberulous 
without, margin isset ciliolate, the trichomes 
white, the nectaries medial, 2-3 mm long and 

1-2 mm wide, рова of many minute glands 
(each ca. 0.1 mm in diameter); bracteoles lan- 
E apically attenuate, 6-9 mm long, 2-3 
mm wide, green, finely striate, glabrous except 
densely pubescent on keel, the trichomes erect, 
white, about 0.5 mm long. Sepals 10-12 mm 
long, apically acute, yellow-green, finely striate, 

margins hyaline, essentially glabrous, the adaxial 
segment narrowly ovate, 3—5 mm wide, the abax- 
ial pair lanceolate, about 3 mm wide, the lateral 
pair narrowly lanceolate, 1.5—2 mm wide; corolla 


150 


bright red, 6–7.3 cm long, essentially glabrous, 
the tube about 5 cm long, 4—5 mm in diameter 
at base, constricted to 1.5—2 mm above ovary 
(about 7 mm above base), expanding to 7-9 mm 
deep at throat, the upper lip erect, elliptic, 17- 
21 mm long, 8-10 mm wide, bilobed, the lobes 
triangular, acute, apiculate, 9-10 mm long, an- 
ther pocket well-developed, the middle lobe of 
lower lip narrowly ovate, strongly reflexed to lie 
along tube at anthesis, 21-28 mm long, 8-10 mm 
wide, acute, apiculate, the lateral lobes about 1 
mm long and 6 mm wide; filaments inserted 8— 
11 mm from base of tube, free portion of each 
4.5—5.3 cm long, the anthers 7-8 mm long, ex- 
tending to within 4—6 mm from tip of upper lip, 
pollen yellow; stigma not sm они colored 


slightly bilobed, the lobes abo ong, 
the style filiform, extends 1—6 sod an- 
thers, the ov glabrous. Fruits oblong, - 


green when immature, yellow-brown at dehis- 
cence, 17.5-19 mm long, about 5 mm wide, 3.5- 
4 mm thick; seeds brown, irregularly orbicular, 
strongly flattened, 3.5—6.5 mm in diameter, 1.5— 
2 mm thick. Seed germination epigeal. 


This species i is 
ا‎ 1967) in eastern ae” (Colón, 
Panamá, Darién, and San Blas), and from two 
localities in Costa Rica. Extensive collecting on 


Ваа and distribution. 
kno 


е ре 
to firmly establish the range of this species. Арће- 
landra leonardii is a shrub of the forest under- 
story and margins. The plants are found mostly 
in areas with little annual variation in rainfall, 
but a few collections have been made in season- 
ally dry areas. 


Flowering and fruiting. Individuals of A. 
leonardii flower during the late wet season (Sept. 
to Dec.) and fruits mature during the driest 
months of the year (Jan. to April). 


Individuals of this species may be distin- 
guished from other Central American members 
of the A. pulcherrima complex by their shrubby 
habit, sessile, terminal clusters of inflorescences 
and i 


re nu- 
merous, minute, and form a well-defined, oblong 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


patch on each side of the bract. The two species 
differ also in fruit and seed morphology, with 
terete capsules and sub-globose seeds present in 
A. a and strongly flattened capsules 
and seeds in A. leonardii. Aphelandra pulcher- 
rima is wholly South American and appears to 
include at lea 

trast, for instance, the оне of Leonard, 
1953 and Wasshausen, 1975). 

Although there is little morphological vari- 
ability among the eastern Panama populations 
of this species, plants from Costa Rica are rather 
distinct in several features of vegetative mor- 


tomentose. With respect to inflorescence and flo- 
ral characters, however, plants from the two re- 
gions are almost identical. The systematic sig- 
nificance of these differences is as yet unclear and 
will perhaps be clarified by further collections 
pn intervening areas where the species is cur- 

y unknown. Although it is possible that col- 
ids from the po countries терге di 

species, data from i Table 


10) support recognition of a single taxon 


Relationships. Aphelandra leonardii is a 
member of the lineage sharing bracteal nectaries 
of many minute glands (Group II). This dis 


Phylogenetic analysis indicates that A. me 
is the sister group of the remaining four Central 
American members of this lineage (А. laxa, 
campanensis, A. hartwegiana, and A. darienen- 
Sis). 


Additional specimens examined. COSTA RE 
José: along Río Tarrazü between Frailes and San An gà 
1, 300 m, Burger 4041 et NY). PROVIN 


F, MO, 
NKNOWN: near ulebra, Pacific coast (Puntare- 
ii Pittier 11988 Ais S). 
ANAMA. COLÓN: forest along Río Indio de Gum 
sea level, Maxon 4807 (NY, US); Río Providen 0 
km SE of tiie, 57100m, Gentry & Nee 8652 (МО), 
Río Guan 96 (MO). DARIEN: slopes 


"Аксу 9 
Cerro Pirre, 500-2, 500 f. Duke & Elias Е: 


Mie 033 (MO); summit camp adjacent Darién sea "i 
Oliver et al. 3676 (MO, US); between upper Río age 
brillo and Camp 7 on the construction road 10 


—] 


———MÁ RM M M—— JA -—— — Uo— — d— 


NEU 


1984] McDADE— 


Blas, Duke 10865 (NY); Rio Tucuti between Tucuti 
and Rio Uroganti, coe 5287 (MO); Rio Aruza, Bris- 
tan 1248 (MO). PANAMA: along Rio Chavaré above 
Chepo, 50-200 т, Pittier 4723 (US); along InterAm. 
Hwy. ata ЕІ Llan Mamoni, Duke 5631 

О). SAN BLAS: along та east of Pto. Obaldia, Croat 
16890 (US) mies around Pto. Obaldia, Pittier 4280 
(GH, NY, US); mainland opposite Ailigandí from 
mouth of Ailigandí River, Lewis et al. 172 (DUKE, 
MO, NY, US). 


10. Aphelandra laxa Durkee, Ann. Missouri Bot. 
Gard. 65: 161. 1978. TYPE: Panama. San 
Blas: 15-20 km WSW of Pto. Obaldia on 
trail to Darién, Caribbean slope of cordille- 
ra, Mori et al. 6854 (holotype, MO). 


Shrubs to 1.5 m high, sparsely branching; 
younger stems quadrangular, glabrous. Leaves 
opposite, ovate-elliptic, to about 35 cm long and 
8.5 cm wide, apically acuminate, basally atten- 
uate, marginally entire to undulate, glabrous 
above and below; petioles to about 4 cm long, 
glabrous. Inflorescences terminal, spikes solitary 
or few, sessile, to about 18 cm long and 0.5-1 
cm wide; rachis glabrous; floral bracts non-over- 
lapping, internodes 1.5-2 cm long, rhombic- 
ovate, apically acute, marginally entire, 7-10 mm 
long, 5-6 mm wide, glabrous within and without, 
margin minutely ciliolate, the nectaries sub-me- 
dial, about 2 mm long and 0.75 mm wide, com- 
posed of many minute glands; bracteoles nar- 
rowly ovate, keeled, apically acute, 7-8 mm long, 
2-2.5 mm wide, glabrous. Sepals 11—12 mm long, 
apically late, striately nerved, gla- 
brous, the adaxial narrowly ovate, abou 
3.5 mm wide, the abaxial pair lanceolate, about 
3mm wide, the lateral pair lanceolate, 2-2.5 mm 
wide; corolla to about 7 cm long, red, minutely 
puberulous, the tube 42-46 mm long, about 4 
mm in diameter at base, narrowed to 2 mm in 
diameter above ovary (3-4 mm above base), ex- 
panding to about 9 mm at throat, the upper lip 
erect, ovate, about 25 mm long and 8-10 mm 
wide, bilobed, the lobes triangular, about 11 mm 
long, acuminate, the middle lobe of lower lip 
narrowly ovate, 28-30 mm long, 9—11 mm wide, 
apically acute, the lateral lobes about 1 mm long 
and 6-7 mm wide; anthers 7-8 mm long, ex- 
tending to tip of upper lip; stigma minutely bi- 
lobed, the style filiform, extending beyond an- 
thers, the ovary glabrous. Fruits clavate, flattened, 
glabrous, about 16 mm long and 9 mm wide; 
seeds orbicular, strongly flattened, about 5 mm 
in diameter, 2.5 mm thick. 


[d 


APHELANDRA PULCHERRIMA 


151 


Habitat and distribution. This species is 
known only from the type specimen which is 
from eastern Panama in the province of San Blas. 
It is apparently found in wet forests of the Ca- 
ribbean lowlands, but its range and habitat re- 
quirements cannot yet be delimited. 


Flowering and fruiting. Aphelandra laxa ap- 
parently flowers and fruits during the wet season 
because the type specimen (collected in June) 
bore both flowers and capsules 


This species is distinguished from other Cen- 
tral American species of Aphelandra by its very 
large leaves, small bracts with minute glands, and 
elongated internodes between pairs of floral 
bracts. 


Relationships. Aphelandra laxa is a member 
of Group II (species 8-13). Its leathery bracts 
and papillate corollas indicate that, among Cen- 
tral American species, it is the sister group of A. 
campanensis, A. hartwegiana, and A. darienen- 
sis. 

Aphelandra laxa is known only from the type 
specimen. 


11. Aphelandra campanensis Durkee, Ann. 
Missouri Bot. Gard. 65: 162. 1978. TYPE: 
Panama. Panamá: Cerro Campana, 1,000 

m, Croat 12215 (holotype, MO; isotypes, 

D 


2 


Shrubs 2-4 m high, sparsely branched; youn- 
gest stems quadrangular, moderately pubescent, 
the trichomes upwardly appressed, white, about 
0.25 mm long, older stems terete, glabrate. Leaves 
opposite, elliptic to ovate, 20—30 cm long, 8-18 
cm wide, apically acute to acuminate, basally 
acute to slightly attenuate, marginally entire to 
crenulate, glabrous above, sparsely pubescent be- 
low (denser on veins), the trichomes appressed, 
white, about 0.25 mm long; petioles 3-12 cm 
long, very narrow, moderately pubescent, the tri- 
chomes appressed г and curling, white, about 0. 29 
mm long; le 
much reduced, 4—7 cm long, 2–4 cm wide, pu- 
bescence as of cauline leaves. Inflorescences ter- 
hic spikes usually 1—3 (rarely 5 or more), 

‚ 10-25 cm long, about 1.5 cm wide; 
на lacking or to 1 cm long (longer below 
lateral inflorescences), essentially glabrous; rach- 
is essentially glabrous; bracts barely imbricate, 
broadly rhombic-ovate, apically acute to slightly 
obtuse and apiculate, marginally entire, 11-14 


152 


mm long, 9-11 mm wide, deep red-orange, mi- 
nutely puberulous within and without, keel m 

erately pubescent, the trichomes appressed, white, 
about 0.25 mm long, margin sub-hyaline, gla- 
brous, the nectaries medial, 2-2.5 mm long and 
1-1.5 mm wide, composed of many minute 
glands; bracteoles keeled and slightly falcate, api- 
cally acute, 11-13 mm long, 2-3 mm wide, pale 
orange. glab td 1 1 t keel 


the trichomes erect, white, 0.5–0.75 mm long. 
Sepals 15—18 mm long, apically obtuse and fre- 
quently minutely apiculate, pale orange, striate, 
glabrous, the adaxial segment narrowly oblong, 
4–6.5 mm wide, the abaxial pair narrowly ob- 
long, 3-4 mm wide, the lateral pair linear, 2-3 
mm wide; corolla deep red-orange, 6—7 cm long, 
coriaceous, minutely puberulous and papilia: 
the tu mm long, about 3 mm in 
ameter at base, slightly constricted above ovary 
(4-5 mm above base), expanding to 7-9 mm 
deep at throat, the upper lip erect, ovate, 17—20 
mm lon 0-12 mm wide, bilobed, the lobes 
triangular, apiculate, 6-7 mm long, anther pock- 
et well-developed, the middle lobe of lower lip 
elliptic, 22-25 mm long, 8-11 mm wide, acu- 
minate and apiculate, strongly reflexed at anthe- 
sis to lie parallel to tube; filaments inserted about 
7 mm above base of corolla, free portion of each 
4.6-4.8 cm long, the anthers 8-9 mm long, ex- 
tending to within 3—5 mm from tip of upper lip, 
pollen yellow; stigma minutely bilobed, pink, the 
style filiform, extends 2-4 mm beyond anthers, 
the ovary glabrous. Fruits oblong, flattened, oval 
in cross-section, green when immature, brown- 
black at dehiscence, 20-24 mm long, 6-8 mm 

wide, 5-6 mm thick; seeds brown, orbicular, 
strongly flattened, 4—6 mm in diameter, about 2 
mm thick. Seed germination epigeal. 


Habitat and distribution. Aphelandra cam- 
panensis is foun predominantly at mid-eleva- 


del Toro) and extreme southern Costa Rica (Li- 
món). The distribution of A. campanensis is im- 
perfectly known because only a few collections 
from the Caribbean lowlands of Panama have 
been made. Plants of this species occur in cloud 
forest habitat at mid-elevations and in wet low- 
land forests (Holdridge's premontane wet and 
premontane rain forests). The species grows in 
the forest пане gaps, and disturbed, sec- 
ond-growth are 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


Flowering and fruiting. Peak flowering oc- 
curs during the mid wet season (Aug. through 
Nov.) and fruits mature late in the wet season 
and into the drier months of the year (Jan. and 
Feb.). 


Aphelandra campanensis may be distin- 
guished from most Central American species by 
its large, glabrous leaves, broadly rhombic-ovate 
poses сег — are keeled vi: ве fal- 

s. Aphe- 
landra hartwegiana i is similar in many e 
but has strongly falcate bracteoles, larger and 
more ovate bracts that diverge from the rachis, 
longer calyx segments, and extremely coriaceous 
corollas. 

There is some confusion about the identity of 
plants from the lowlands of western Bocas de 
Toro province. Collections from this region have 
preme identified as A. campanensis, A. crenata, 

A. hartwegiana. Part of the difficulty is due 
ra чн ассо condition of some of the spec- 
imens in question. There is certainly variability 
among plants iin this area, but I found that 
none of these specimens was outside of the range 
of variability encountered in A. campanensis. 
Until more collections are made and field and 
experimental studies carried out, these collec- 
tions are best referred to A. campanensis. 


коен, Phylogenetic analysis indi- 
an 


subgroup within Group II. The relationships of 
these species with other Central American mem- 
bers of the A. pulcherrima complex, and with 
South American species are discussed under A. 
hartwegiana. 


Additional specimens examined. Costa RICA. 
LIMÓN: between Cahuita and Bribri, 100 m, Mc. "o 
4 Мр ви Toro Amarillo, Canton де Pococí, Solis 

D. 


BOCAS DEL TORO: hillside above Almi Chi 
Gentry 274 2748 (MO, US); Water Valley, vicinity of 


(DUKE). aks around Dos Bocas, Río Fato valley: 
om m, е 4195 (NY, US). 
0 m, eggs et al. 4966 (MO, m 

279. (DUKE), Lewis 59 (US); 
Cerro Azul on o Pie dras, 550 m, Mi 
3284 (MO). etn valley of Río Dos Bocas 


road between Alto Piedra and Calovébora, 350-400 


ДР "а 


~ 


اس 


1984] 


m, Croat 27356 (MO); ca. 5 mi. past Santa Fé on road 
past Agricultural School, 700 m, McDade 268 (DUKE). 


12. Ма hartwegiana Nees ex Benth., Pl. 
Hartw. 236. 1846. TYPE: Colombia. Cundi- 
namarca: Hacienda de Palmar, near Gua- 
duas, Hartweg 1270 (holotype, K, not seen). 


Shrubs 1-4 m high, sparsely branched; youn- 
ger stems subquadrangular, sparsely pubescent, 
the trichomes upwardly appressed, white, about 
0.5 mm long, older stems terete, glabrate. Leaves 
opposite, broadly elliptic, 25—40 cm long, 10-15 
cm wide, apically acute to slightly acuminate, 
basally acute or attenuate, marginally entire, un- 
dulate or crenate, essentially glabrous above, 
sparsely pubescent below (moderate on veins), 
the trichomes appressed, white, 0.25—0.5 mm 
long; petioles 1-4 cm long, moderately pubes- 
cent, the trichomes appressed, white, 0.25–0.5 
mm long; leaves reduced in size towards inflo- 
rescence. Inflorescences terminal, spikes mpn 
(rarely 2-5), subquadrangular, 15—30(—40) с 
long, 1.5-2 cm wide; peduncles 0.5-1.5 cm ie 
(longer below lateral inflorescences), sparsely pu- 
bescent, the trichomes appressed, white, about 
0.25 mm long; rachis glabrous; 3—5 pairs of ster- 
ile bracts subtend spikes; floral bracts imbricate, 
broadly ovate, apically obtuse, entire, 13—16 mm 
long, 11-14 mm wide, deep orange, striate, es- 
sentially glabrous within and without, the nec- 
taries supra-medial, 3.5—4.5 mm long and 2-2.5 
mm wide, composed of many minute glands; 
bracteoles falcate, i xe apically acute, 7-10 
mm long, 3-5 mm wide, orange, glabrous or 
sparsely AL on keel, the trichomes ap- 
pressed, white, about 0.5 mm long. Sepals 17- 
22 mm long, orange, frequently fading to white 
toward base, striate, glabrous or with a few tri- 
chomes toward apex, the adaxial segment ob- 
long, apically obtuse, 6-9 mm wide, the abaxial 
pair narrowly oblong, apically acute, 4–5.5 mm 
wide, the lateral pair narrowly oblong, apically 
acute, 3-4 mm wide; corolla 6.5—7 cm long, yel- 
low (infrequently orange), glabrous, very coria- 
ceous, the tube 44—48 mm long, about 4 mm in 
diameter at base, narrowed to about 3 mm above 
ovary (about 7 mm above base), expanding to 
8-9 mm deep at throat, the upper lip erect, ovate, 
20-22 mm long, 11-13 mm wide, bilobed, the 
lobes triangular, 9-12 mm long, anther pocket 
very well-developed, the middle lobe of lower 
lip elliptic, about 25 mm long and 12 mm wide, 
apically acute, the lateral lobes about 1 mm long 


McDADE—APHELANDRA PULCHERRIMA 


153 


and 5 mm wide; filaments inserted about 7 mm 
above base of corolla tube, free portion of each 
4.2-4.6 cm long, the anthers 9-10 mm long, ex- 
tending to within 3-5 mm from tip of upper lip, 
pollen yellow; stigma not distinctively colored, 
minutely bilobed, the style filiform, extending 3– 
5 mm beyond anthers, the ovary glabrous. Fruits 
clavate, flattened, oval in cross-section, green 
when immature, turning brown-black at dehis- 
cence, 28-31 mm long, 7–8.5 mm wide, 5-7 mm 
thick; seeds brown, orbicular, strongly flattened, 
5-7 mm in diameter, about 2 mm thick. Seed 
germination epigeal. 


Habitat and distribution. Aphelandra hart- 
wegiana is found in the lowlands of eastern Pan- 
ama and northern Colombia. It is a species of 
wet forests with mild dry seasons (or essentially 
aseasonal precipitation) [Holdridge’s (1967) 
tropical wet forest]. The plants grow in gaps in 
the forest, very frequently along streams, trails 
and clearings, and in extensive secondary areas. 


Flowering and fruiting. Peak flowering oc- 
curs during the wettest months of the year (Aug. 
through Nov.), with fruits maturing during the 
drier months of Jan. through March. 


The large, broadly ovate bracts, strongly fal- 
cate bracteoles, 2 cm long calyx lobes, and ex- 
tremely coriaceous, yellow corolla readily distin- 
guish this species from all other Central American 
Aphelandras. Specimens of A. hartwegiana show 
a definite decrease in bract size from west to east. 


The sy g pp y very 
gradual, clinal variation is as yet unclear. Col- 
lections are quite few and I have not been able 
to study Colombian plants in the field. 

A single collection from the Darién (Allen 5094) 
of Panama was identified as the South American 
species A. crenata by Durkee (1978). I found this 
specimen iod be win the range of variability 

fA fr om 


this region, but recognize the need for further 
study of these two species, especially in light of 
the clinal decrease in bract size of A. hartwegiana 
that results in Panamanian specimens at least 
superficially similar to A. crenata. 


Relationships. Among the species treated 
here, A. hartwegiana is a member of Group II 
and is most closely related to A. campanensis 
and A. darienensis. Aphelandra hartwegiana and 
A. campanensis are also similar to the South 
American species A. crenata Leonard and A. 


154 


chaponensis Leonard (Leonard, 1953; Durkee, 
1978). These four species are similar in a number 
of morphological features including habit; large, 
essentially glabrous leaves that are frequently 


cate bracteoles. Elucidation of the Крис 
relationships among these species wi 
further study of the South American gs 


Additional specimens examined. PANAMA. DA 
cific coast n ear Darién-Colombia ког. 


0 т. Allen 5094 
Rio quee between Paya and Payita, Stern et al. 
177 (US): S of El Real, headwaters of Rio , са. 
100 та, чаена & Е je 7 iu сс 425 
(DUKE); Ri carcuna 
village, $80 m m, ps entry os Mori y 13383 (МО). SAN BLAS: 
mainland opposite di, Lewis et al. 191 (US). 
COLOMBIA. ANTIOQUIA: near Villa Arteaga on hwy. 
to sea, 150 m, Hodge 7053 (US); near Chigoradó, 40 
km S of Turbo, 50 m, Haught 4699 (US); Uraba, Mu- 
; eaga 


= al. 1451 (MO); mouth of Rio Truan 

669 (NY); pem coast, Cupica, пагане 354 (US); 
Bot Solano, along Quebrada Jellita, 50-100 m, ү 
& Garcia 35639 (US); Rio Chintada: "above La Nuev: 
Duke 9863 (US). 


13; gr darienensis Wassh., Phytologia 
5: 480. 1973. TYPE: Panama. Darién: Cerro 
750-1,350 m, Duke & Elias 13756 


(holotype, US; isotype, MO). 


Shrubs 1—4 m high, sparsely branching; youn- 
ger stems subquadrangular, sparsely pubescent, 
the trichomes upwardly appressed, white, about 
0.5 mm long, older stems terete, glabrate, stems 


marginally entire to crenulate, essentially gla- 
brous to very sparsely pubescent above, the tri- 
chomes appressed, white, 0.75-1 mm long, 
sparsely pubescent below (except moderate on 
veins), the trichomes appressed, white, 0.5—0.75 
mm long; petioles 3—9 cm long, moderately pu- 
bescent, the trichomes appressed, white, 0.75-1 
mm long. Infl t inal, spil litary 
(rarely 2-3), 10—18 cm long, 2.5-3 cm wide, ses- 
sile; rachis essentially glabrous; lower 1—3 pairs 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


imbricate, ovate, apically obtuse and arching 
rachis, entire, frequently notched at 
apex, 30-40 mm long, 18-26 mm wide, deep 
orange, бави leathery-coriaceous, sparsely pu- 
ous within and without, with few scattered 
pin a nei 1 mm) trichomes, the nectaries me- 
, 3-4.5 mm long and 1-2 mm 
ја of many minute glands; одем dis 
falcate, apically acute, 9.5-13 mm long, 
wide, pale orange, essentially glabrous. aun 
15-18 mm long, apically acute, dull orange, es- 
sentially glabrous or with few scattered tri- 
chomes, the a segment broadly elliptic, 8.5- 
9 mm wide, the abaxial pair elliptic, about 5 mm 
wide, the lateral pair lanceolate, 3.5-4 mm wide; 
corolla orange, minutely papillate, 6.8-7.2 cm 
long, coriaceous, the tube 48—49 mm long, about 
mm in diameter at base, narrowed to about 3 
mm above ovary (about 6 mm above base), ex- 
panding to about 7 mm deep at throat, the upper 
lip erect, oblong, 18-20 mm long, 11-13 mm 
wide, bilobed, the lobes triangular, about 8 mm 
long, 11-13 mm wide, apically emarginate and 
apiculate, anther pocket well-developed, the 
middle lobe of lower lip ovate, 27-29 mm long, 
10-12 mm wide, apically obtuse, the lateral lobes 
2-2.5 mm long and 7 mm wide; filaments in- 
serted about 8 mm above base of corolla tube, 
free portion of each 4.7—4.8 cm long, the anthers 
8-9 mm long, extending to within 5-6 mm from 
tip of upper lip, pollen yellow; stigma orange. 
bilobed, the lobes about 0.2 mm long, style fi 
liform, extending about 5 mm beyond anthers, 
the ovary glabrous. Fruits elliptic, flattened, oval 
in cross-section, green when immature, black at 
dehiscence, about 35 mm long, 8.5—9.5 mm wide, 
about 5 mm thick; seeds dark пише strongly 
arse about 9 mm i and 2-2.5 mm 
e. Seed germination Du 


Habitat and distribution. Aphelandra dari- 
enensis is apparently endemic to the mountains 
of the Darién in eastern Panama. It is restrict ted 


to i, cloud forest habitats and Jo 


ЛАРЕ КЕ 


аы. 1967) 


Flowering and fruiting. Flowering occurs 
during the early wet season (July through Sept.) 
and fruits mature during the remainder of the 
wet season (through Dec.). Data on seasonality 

of reproduction are rather tentative because col- 
lections of this species are still quite few. 


ds. 


—— 


— · a RK. Ek aaa ae 


> game 


t 


1984] 


Aphelandra darienensis is extremely distinc- 
tive and is readily identified from flowering or 
fruiting material. Most characteristic are the large 
(to 40 mm), leathery and strongly recurved floral 
bracts. The extremely large leaves and thick, al- 
most succulent stems, as well as the unique apical 
shape of the upper corolla lip lobes (emarginate 
and apiculate), and very long capsules also dis- 
tinguish the species. 


Relationships. The results of phylogenetic 
analysis indicate that this species is a member 
of the lineage including the other Central Amer- 
ican species with minute glands (Group II). 
Within this group, closest relatives are A. hartwe- 
giana and A. campanensis. Wasshausen (1973a) 
suggests a relationship based on morphological 
similarity with A. fernandezii Leonard, a Colom- 
bian species that bears at least a superficial re- 
semblance to A. darienensis. Further study of 
South American members of the A. pulcherrima 
complex will be necessary to satisfactorily re- 
solve the EE relationships of this un- 
usual spe 


Additional specimens OE PANAMA. DARIEN: 
W slope of Cerro Pirre, 2,500—4,500 ft., Duke p 
n McDade 430 Urs between Tres Bocas and 

tro Campamiento on Cuasí-Cafia trail, Kirkbride & 
Duke 1350 (МО); Cerro Campamiento, S of Cerro Pirre. 
Duke 15620 (US). 


LITERATURE CITED 


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0. 


————. 1974b. Cuticular studies in some species of 
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: 1978. Epidermal hairs of Acanthaceae. Blu- 

117 


i 1954. Hoyer's solution as a rapid 
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BEEKs, R. M . Improvements in the squa 
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BENTHAM, С. & J. Р. Ноокек. 1876. Acanthaceae. 
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1965. Delimitation and subdivision of the 

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Brown, В. 1810. Prodromus Florae Novae Hollan- 
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McDADE—APHELANDRA PULCHERRIMA 


155 


CHAUBAL, P. D. 1966. Palynological Studies on the 
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Cronquisr, A. 1968. The Evolution and Classifica- 
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1981. An Integrated System of Classification 
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DURKEE, L. Н. ceae. In R. E. Wood- 

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ENGLER, ~ 1964. Syllabus der Pflanzenfamilien. II 
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DAE Р. . Organization ofa tropical guild 

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Hossain, A. B. M. E. 1971. Studies in the Classifi- 
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18: 1-32. 
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Tobago, Volume 2. Trinidad Dept. of Agriculture, 
Trin 
1961. Acanthaceae Americanae novae vel 
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156 


1895. Acanthaceae. Jn Die Naturlichen 
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1904. 


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LLOYD, D. С. 1965. Evolution of МЕ Aty 
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s. Duke . Durham, North iri 
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t New species of Aphelar- 
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| 
| 


1984] 


McDADE—APHELANDRA PULCHERRIMA 


APPENDIX A. Members of the Aphelandra pulcherrima complex. 


albert-smithii Leonard 
aristei Leonard 
attenuata Wassh. 
barkleyi Leonard 
blandii Lindau 
campanensis Durkee 


ar 
darienensis Wassh. 
deppeana Schldl. 
& Ch 


ече 


ат. 
А. dielsii Mildbr. 


га 
А. еа. 
McD 


А. pao Leonard 

A. grandis Leonard 

A. hartwegiana Nees 
ex Benth. 

A. haughtii Leonard 

A. lasia Leonard 


leonardii McDade 


macrostachya фес 
micans Moritz ex Vatke 
mildbraediana ы 
panamensis McDade 
parvispica Leonard 
pharangophila Leonard 
pilosa Leonard 
pulcherrima (Jacq.) 
H.B.K. 


E uir 


schieferae Leonard 
scolnikae Leonard 
sericantha Leonard 


tetragona (Vahl) Nees 
trianae Leo 
xanthantha Leonard 


ethos he bis 
a 
К 
= 
8 
© 
b 
о 
E 
Qa 


A. laxa Durkee 


APPENDIX B. Sources of pollen for size analysis (LW) and scanning electron microscopy study (SEM). 


157 


Collector and Number Location Used for 
1. А. terryae 
Lewis et al. 126 (US) Achituppu, San Blas, Pan. LW 
Tyson et al. 3815 (DUKE) Cerro Piriaque, Darién, Pan. LW 
Haught 2098 (US) Santander, Col. LW 
Duke 5187 (MO) Rio Pirre, Darién, Pan. LW 
McDade 431 (DUKE) Rio Pirre, Darién, Pan. SEM/LW 
Gentry & Mori 13550 (MO) Pucuro, Darién, Pan LW 
2. A. sinclairiana 
Donnell-Smith 6694 (US) Atirro, Cartago, C.R. LW 
Wilbur et al. 13365 (DUKE) Colón, Pan Dx 
McDade 280 (DUKE) Colón, Pan. SEM/LW 
McDade 384 (DUKE) Portobelo, Colón, c SEM/LW 
Burger et al. 1977 (F) Bribri, Limón, LW 
McDaniel & Cooke 14831 (FSU) El Copé, Coclé = LW 
McDade 532 (DUKE) El Copé, Coclé, Pan SEM/LW 
Hunter & Allen 358 (MO) El Valle, Coclé, Pan LW 
McDade 528 (DUKE) El Valle, Coclé, Pan. SEM/LW 
Pittier 5572 (NY) Samba River, Darién, Pan. LW 
Von Wedel 973 (MO) Bocas del Toro, Pan. LW 
3. A. storkii 
Pto. Viejo, Heredia, C.R. SEM/LW 


McDade 350 (DUKE) 


158 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Vor. 71 
APPENDIX B. Continued. 
Collector and Number Location Used for 
4. A. gracilis 
Nee 9291 (MO) Cerro Jefe, Panama, Pan. LW 
McDade 421 (DUKE) Cerro Jefe, Panama, Pan. SEM/LW 
Lewis et al. 5392 (MO) Sta. Rita Ridge, Colón, Рап. LW 
Mori & Kallunki 1801 (MO) Sta. Rita Ridge, Colón, Pan. LW 
Allen 1671 (US) El Valle, Coclé, Pan. LW 
онаи 529 (DUKE) El Valle, Coclé, Pan. SEM/LW 
vii 5 Dressler 2954 (MO) El Llano, Panamá, Pan LW 
уле 93 (F) Cerro Campana, A Pan. LW 
64 ао, 
Skutch 3941 (US) El General, San José, С.К. LW 
McDade 378 (DUKE) Palmar, Puntarenas, C.R SEM/LW 
McDade 401 (DUKE) Corcovado, Puntarenas, C.R SEM/LW 
Croat 21884 (F) Pto. Armuelles, Chiriquí, Pan LW 
Pittier 3 Biolley 7072 (US) San Mateo, San Ў LW 
Allen 5775 (US) Esquinas, Puntarenas, C.R LW 
Liesner 389 (MO) Burica, Chiriqui LW 
McDade 251 (DUKE) San Vito, робна CR SEM/LW 
6. A. panamensis 
Foster & оя 1872 (DUKE) Cerro Jefe, Panama, Pan. LW 
McDade 4 Cerro Jefe, Panama, Pan. SEM/LW 
Foster & phate grdi (DUKE) Cerro Pirre, Panamá, Pan LW 
McDade 428 (DUKE) Cerro Pirre, Panamá, Pan. SEM/LW 
McDade 284 (DUKE) Sta. Rita Ridge, Colón, Pan. SEM/LW 
7. A. deppeana 
Ton 3076 (DUKE) Chiapo de Corzo, Chiapas, Mex. LW 
McDade 377 (DUKE) Cañas, Guanacaste, C.R. SEM/LW 
McDade 252 (DUKE) San Vito, Puntarenas, C.R. SEM/LW 
McDade 290 (DUKE) Palmar, Puntarenas, C.R SEM/LW 
Ortiz s.n. (DUKE) Tikal, El Petén, Guat LW 
McDade 533 (DUKE) El Copé, Coclé, SEM/LW 
McDade 530 (DUKE) El Valle, Coclé, Pan. SEM/LW 
A. dukei (= A. deppeana) 
Duke 14397 (US) Piria, Panamá, Pan. LW 
Mori & Gentry 4245 (MO) Pucuro, Darién, Pan. SEM/LW 
8. A. lingua-bovis 
Archer 2012 (US) Chocó, Col. SEM/LW 
Skutch 5284 (US) Golfo Dulce, Puntarenas, C.R. LW 
McDade 399 (DUKE) Corcovado, Puntarenas, C.R. SEM/LW 
Allen 924 (GH) inogana, Darién, Pan LW 
McDade 429 (DUKE) Río Pirre, Darién, Pan. SEM/LW 
McDade 442 (DUKE) San Vito, Penn, C.R. SEM/LW 
9. A. leonardii 
Duke et he 3611 (US) Cerro Diablo, San Blas, Pan. LW 
Foster 1996 (F) Majé, Panamá, Pan LW 
Lewis et al. 172 (DUKE) Ailigan Blas, P LW 
D'Arcy 9696 (MO) Portobelo, Colón, Pan. LW 
McDade 310 (DUKE) Frailes, San José, C.R. SEM/LW 
Pittier 11988 (US) Boca Culebra, San José, C.R. LW 
McDade 432 (DUKE) Cerro Pirre, Darién, Pan SEM/LW 


1984] 


APPENDIX B. Continued. 


McDADE—APHELANDRA PULCHERRIMA 


159 


Collector and Number 


Location 


Used for 


10. A. laxa 
Mori et al. 6854 (MO) 
11. A. campanensis 
Weaver 1648 (DUKE) 
McDade 271 (DUKE) 
Von Wedel 1428 (GH) 
McDade 242 (DUKE) 
McDade 531 (DUKE) 
12. A. hartwegiana 
Allen 921 (US) 
McDade 425 (DUKE) 
Cuatrecasas 26108 (US) 
Lewis et al. 191 (US) 


13. А. darienensis 


Duke & Elias 13756 (US) 


McDade 430 (DUKE) 
А. pulcherrima 
Blum 3 


523 (US) 
Killip & Smith 14516 (US) 


Pto. Obaldia, San Blas, Pan. 


El Valle, Coclé, Pan. 
El Valle, Coclé, Pan. 


Chiriqui Lagoon, Bocas del Toro, Pan. 
E 


Bribri, Limón, 
El Copé, Panamá, Pan. 


Pinogana, Darién, Pan. 
Rio Pirre, Darién, Pan. 
Antioquia, Col. 
Ailigandí, San Blas, Pan. 


Cerro Pirre, Darién, Pan. 
Cerro Pirre, Darién, Pan. 


La Popé, Bolívar, Col. 
Arjona, Bolívar, Col. 


SEM/LW 


LW 
SEM/LW 


LW 
SEM/LW 
SEM/LW 


LW 
SEM/LW 
LW 
LW 
LW 
SEM/LW 


SEM 
SEM 


160 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Vor 71 


APPENDIX С. Locations of populations of Aphelandra species used in field and greenhouse studies: (О) = 
sites of field observations for flower visitors, (IC) = sources of greenhouse grown plants used in interpopulation 
crosses. 


2. A. sinclairiana 
Colón (O)—Panama, Colón: Pipeline Rd., 5 km from Gamboa, 50 m. (Now part of Parque Nacional 
Soberania.) 


3. А. storkii 
Pto. Viejo (O)—Costa Rica, Heredia: Finca La Selva, са. 6 km from Pto. Viejo, along Rio Pto. Viejo, 
100 m. 


| 
| 
4. А. gracilis | 
El Valle (О) — Panama, Coclé: 10 km beyond El Valle de Antón, 800 m. 
5. A. golfodulcensis | 
Corcovado (O, IC)— Costa Rica, Puntarenas: Corcovado National Park, Osa Peninsula, sea level. 
San Vito (О, IC)— Costa Rica, Puntarenas: 6 km from San Vito de Java, forest below Las Cruces Botanical | 
Garden, 1,200 m. 
6. A. panamensis 
Santa Rita (IC) — Panama, Colón: 25 km from Transisthmian Hwy., Santa Rita Ridge, 300 m. 
Cerro Jefe (IC) — Panama, Panamá: 30 km above InterAmerican Hwy. on road to Cerro Jefe, 800 m. 
Cerro Pirre (О, IC) — Panama, Darién: upper slopes of Cerro Pirre, about 12 km S of El Real, 600- 
800 m. 


7. A. deppeana 
Cañas (О, IC) —Costa Rica, Guanacaste: 8 km N of Cañas along InterAmerican Hwy., 50 m 
San Vito (IC) — Costa m Puntarenas: 6 km from San Vito de Java, Las Cruces Botanical Garden, 
Palmar (IC)— Costa d Puntarenas: 10 km SE (toward Panama) of Palmar N., along InterAmerican 
Hwy., 100 m 
8. A. lingua-bovis 
Corcovado (О, IC)— Costa Rica, Puntarenas: Corcovado National Park, Osa Peninsula, sea level. 
San Vito (О, IC)— Costa Rica, Puntarenas: 6 km from San Vito de J ava, forest before Las Cruces Botanical | 
Garden, 1,200 m 
Portobelo (IC) — Panama, Colón: near bridge over Río Buenaventura near town of Portobelo, sea level. 
9. A. leonardii 
Frailes (O, IC)—Costa Rica, San José, Río Tarrazú near Frailes, 1,300 m. 
Cerro Pirre (IC)— Panama, Darién: lower slopes of Cerro Pirre, about 12 km S of El Real, 500 m. 
11. A. campanensis 
El Valle (O)— Panama, Coclé: 10 km beyond El Valle de Antón, 800 m. 
El Copé (O)— Panama, Coclé: about 10 km past El Copé, 250 m. 
12. A. hartwegiana 
Río Pirre (O)— Panama, Darién: along Río Pirre about 12 km S of El Real, 400 m. 
13. A. darienensis 


a e eee a 


Cerro Pirre (O)— Panama, Darién: upper slopes and summit of Cerro Pirre, about 12 km 5 of EI Кей 
800–1,300 m. 
EE == 


1984] 


McDADE—APHELANDRA PULCHERRIMA 


161 


APPENDIX D. Crossability indices between Central American species of the niei pulcherrima com- 
plex. NA indicates data not available. Species numbers and abbreviations as in Ta 


Pollen Parent 


Species LTE T9 NST! 4O0R'!5,GO GTA БРЕ: ВТВ > LE ILCA IHA 13204 
O LITE. ~ 0.66: 0.59. 7059 , 055: 0:24 0 0.00 0.08 МА МА 0.07 
е ASI 0.26 — 039. NA 05 ОШ 013 007 OIG NA NA 0.01 
W AST, 029 0 — 0.62 0 0.29 0.29 0 0.10 0 0 0 
i БЫК 0 NA 0 — МА 0 МА МА 0 МА МА МА 
M XOU 0856 098 0.51, 0,51 – 0.26. 5017 OARS O27 0 0 0.03 

6.PA 0.80 0.99 0.58 0.37 0.64 — 0.89 0 0.10 0 0 0 
К БОРЕ 01 „011. 014. 0,05 0.04 0 — 0017 OI 007 0 0 
a SLB 0 0 0 0.45 0 0 0.08 — 0 0 0 0 
ПО SiE ой OH 012 049. G13 2 09 003 OR — DI 025 039 
€ 11. СА NA NA 0 0 0 0 0 0 — 0 NA 
n 12. НА NA NA 0.03 NA 0 0 0 0 0 0.04 — NA 
t 13.DA NA NA NA NA NA NA NA NA NA NA NA -— 


НОРТ аа 7) سے‎ Аан А е РЧ. ا‎ на М Нан н S НИНЫ... 


(Мог. 71 


ANNALS ОЕ THE MISSOURI BOTANICAL GARDEN 


162 


APPENDIX E. Character by taxon matrix. Species numbers and abbreviations as in Table 2, characters as in 


Table 13. 


19 20 23 


$2? du 13 12 32 16 15 36 кг 18 


8 


Species 


СЭ со "<> OOO Ses ез еч 


„ТЕ 
5 


— 


о 


N 


=ч 


© 


eo 


oo 


о о 


о о 


о 


о 


о 


о 


о 


о 


— 


© 


са 


O ~ 


oo 


= | 


—— 


— 


N 


— 


— 


en 


ev c 


- © 


оо 


чо 


-O 


ea 


McDADE—APHELANDRA PULCHERRIMA 163 


1984] 


APPENDIX E. Extended. 


42 43 


32.33.34. 35 36 3171.428 39 40 41 


СО 25 26 27 28 29 30 „31 


164 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


APPENDIX F. Character state changes for phylogenetic hypothesis presented in Figure 58, by character and 
stem in which change occurs; characters and character states as in Table 13; and stem abbreviations as in Figure 
58. Letters denote apparent type of evolutionary change: P = parallelism, R = reversal, A = derived character 
state unique to species, S = derived state shared by all distal taxa. 


i Өт: 0 (Б) 18. ST: 2 (P) 
LE t 05 LB: 2 (P) 
A 1 (Р) НА: `3 (А) 
2 TE: 0 00 tud m 
LH 1 (Р) E 2 P 
DA: 1 (P) 19. DA: 0 (R) 
FF 72 avy, 6) 
H: 0 (R) 20. LE: 0 (R) 
4. GO: 2 (А) EL: m 
ы 0 9 о: 1 (Р) 
4 РА 2 0 а €T 1 D 
А i m б- Г (Р) 
с 1 0 22) 
s DA 0 00 A2 TE 1 0 
А: 1 (Р) SE 3 (A) 
Е 0 (R) DE: 0 (A) 
1 (Р А: 2 (P) 
6. АМ: 2 (5) Н: 2 (Р) 
С: 1 (R) 2n NO ® 
F: 0 (R) DE: O (A) 
7 т IM LB: 1 (P) 
С: 2 © е1 @ 
8. GR: 1 (Р) ECCO 
LA 1 (D A DA: 1 (A) 
9; AN 1 (5) HB DE 2 m 
D: 0 (R) 2 
10. Sk 3 05 La m 
GR: 0 (A) 26 B 2 0 
LB: 2 (P) Е 3 6) 
DA: 4 (А) а: 0 (8) 
€ 2 (Р) 27. НА: 1 6 
K 2 (Р) 28. GO: 2 (5 
li. 2 0 a DE: 0 (A) 
B: 1 (P) LB: | (Pp 
K 1 0 C Um 
2 A: (ШШ T : x 

13. 00: 2 P) : 
DE: 3 (A) 4. F1 m» 
A 1 0 30 A IE 
14. GR: O (P) 3. РА Те 
LA: 0 (P) LB: 1 (P) 
HA: 2 (A) 13. иі 
15. РА: 1 (А) 33. ТЕ 0 @) 
16. НА: 2 (А) ST 2 05 
“ : 1 (Р) 

7. IE 1 D 

B: 1 di of 0 (R) 
; : 4 (5 
LE 1 (P) K 20 


| 


1984] McDADE—APHELANDRA PULCHERRIMA 165 
APPENDIX F. Continued. 
34. SI: 1 (А) 39 LB: 1 ® 
% A 1 0 F: 1 (Р) 
36. DE: 0 (A) 4 E [| (5) 
R2 (5) 4L E Ре 
П АІ (5) 42. ta om 
38. LB: 0 (R) 4. EIO 
AN: 1 (S) 
Е 0 (Е) 


KLAINEDOXA (IRVINGIACEAE) AT MAKOKOU, GABON: 
THREE SYMPATRIC SPECIES IN A PUTATIVELY 
MONOTYPIC GENUS! 


ALWYN H. GENTRY? 


ABSTRACT 


This paper, in effect constituting a revision of the genus Klainedoxa, is a byproduct of ecological 


studies of tropical forest diversity с 


arried out at the CENAREST laboratory near Makokou, Gabon 


in 1981. Collections from the rain forest canopy included at least 69 taxa new to the field station, a 
number new to Gabon, and several apparently undescribed species. In the case of Klainedoxa, as well- 

wn but taxonomically difficult genus of large trees, these collections indicate a clear resolution of 
the heretofore problematical taxonomic relationships. 


Canopy trees and lianas of the tropical rain 
forest are notoriously poorly understood taxo- 
nomically, in large part because the difficulty of 
collecting them has led to a dearth of herbarium 
material. New techniques for collecting canopy 
plants, which have recently been developed in 
Amazonia but little used elsewhere, were critical 
to the study reported here. Collections of canopy 
trees and lianas at Makokou were made by using 
a tree-climbing bicycle (Forestry Suppliers cat. 
no. 27170) to reach the canopy and a lightweight 
set of aluminum tree trimming poles (available 
from the Missouri Botanical Garden) to reach 
flowering or fruiting outer branches. A similar 
technique using a movable platform to climb 
into the canopy has previously been used suc- 
cessfully to collect specimens of large trees at 
Makokou (Hladik & Hallé, 1973, pl. 3). How- 
ever, the system employing a tree bicycle (which 
can climb trees up to 65 cm in diameter) and 
telescoping tree-trimming pole (potentially 12 m 
long) is both much more flexible and less phys- 
ically demanding. Another relevant problem 
arises when taxonomic work, as has often been 
the case for tropical plants, is restricted to the 
herbarium with little communication between 
systematists and the foresters, ecologists, or na- 
tive peoples who may know plants in the field 
and be well aware of obvious differences in char- 
acters such as those of large fruits that are rarely 
preserved in the herbarium. Asa rule, and within 
a single geographic area, one who knows plant 


populations intimately in the field, no matter 
what his training, is likely to be able to evaluate 
what constitutes a species better than the most 
eminent herbarium taxonomist. The work те- 
ported here draws heavily on the field experience 
of the team of vertebrate ecologists working àt 
the Makokou laboratory. ; 
Klainedoxa, a small genus of tropical African 
canopy and emergent trees with large elephant- 
dispersed fruits, epitomizes these problems. Re- 
cent treatments (Aubréville, 1962; Gilbert, 1958) 
of the genus, variously treated as belonging 10 
Irvingiaceae or to Simaroubaceae, have recog- 
nized two species, K. gabonensis Pierre ех Engl. 
and К. busgenii Engl., the latter differentiated by 
its generally larger, more cordate leaves. The 
“Flora of West Tropical Africa” (Hutchinson & 
Dalziel, 1958) recognized, in addition to the 
widespread K. gabonensis, an unnamed Klai- 
nedoxa designated as “imperfectly known." 510% 
Kh T MS is an extreme 


form of variable K. gabonensis (Letouzey, Pe 
comm.), Klainedoxa, as currently understoor 
would seem to contain only a single highly V4? 
able species. 

The forest surrounding the field station at i 
kokou, Gabon is one of the best known areas + 
tropical Africa floristically (Hallé, 1964, 196 | 
Hallé & Le Thomas, 1967, 1970; Hladik & Hallé 
1973; Florence & Hladik, 1980). Nevertheless 
only a single species of Klainedoxa has bee? a 
ported to occur at the field station (Hallé & 


' I thank Drs. A. Hladik, К. Letouzey, P. Raven, and L. Emmons for reviewing the manuscript; Dr. E 


for originally pointing out to me the three different Klainedoxa fruit t 


г ma 
ypes; and Paul Posso and the Institut 


Recherche sur L'Écologie Tropicale (CENAREST) for making possible my field work in Gabon. This 


was supported by grants from the Explorers Club and National Geo 
? Missouri Botanical Garden, P.O. Box 299, St. Louis, M i 


ANN. Missouri Вот. GARD. 71: 166-168. 1984. 


› graphic Society. 
issouri 63166. 


1984] 


FIGURE | 
fruits). —C. К. microphylla. Line is 4 cm. 


(1980: 237) mention two sympatric “forms” of 


3-lobed, depressed-globose fruits 4—4.5 cm long 


ES Pob cm wide that remain green at maturity, 
in po» ч acute-tipped leaves that are 7-20(-30 
niles) cm long. This emergent tree is one 
le best known and most distinctive plants of 
Topical Africa. 
4 еч ая species [Gentry 33183, 33508 (МО)], 
mergent giant, has distinctly smaller fruits 
are only 2—3 cm long and 3—4 cm wide though 
д аг depressed-globose, 5-angled shape. 
рова ће 1 Hs seeds, though still hard-shelled, are 
of K. gabo cut with a plant clipper, unlike those 
аф ба This species has leaves similar 
К En ose of K. gabonensis but smaller 
ма he ) cm long]; although there is some 
P between the two species, most leaves of 


ofa 


n. ns . comm.). 

e Tu type of fruit [Gentry 33178, 33182 
5 even more distinctive. It is globose, 
› glaucous gray-green in color, and 3.5- 


4S enit ор 
In diameter, The leaves of this species 


GENTRY —KLAINEDOXA AT MAKOKOU, GABON 


Ax سر‎ 


Fruits of Klainedoxa at Makokou, Gabon.—A. K. gabonensis (large fruits).—B. K. trillesii (small 


167 


E 


are also distinctive in being obtuse apically, el- 
liptic to obovate in shape, and small (8–10.5 cm 
by 4.5-6 cm). All three of these plants occur 
along trails in the main ecological study grid at 
Makokou and no intermediates between them 
have been observed. All key out to K. gabonensis 
in the “Ноге du Gabon" (Aubréville, 1962). 

A survey ofthe literat 1 that 20 names 
have been proposed for different collections of 
what is now generally treated as K. gabonensis 
sensu lato. Van Tieghem (1905) proposed 14 spe- 
cific epithets for K/ainedoxa, basing them largely 
on vegetative characters, and several additional 
species were proposed subsequently by Engler 
(1907, 1911) and others. Pellegrin (1924) re- 
viewed the species and accepted nine of them, 
still based almost entirely on vegetative char- 
acters. Letouzey (1975 and pers. comm.) has rec- 
ognized two taxa in Cameroun, the second treat- 
ed as K. gabonensis var. microphylla but now 
considered by him to constitute a distinct species. 

Two of the extant synonyms clearly are ap- 
plicable to the two nameless Makokou species. 
Klainedoxa trillesii was characterized by exactly 
the same combination of smaller leaves and much 
smaller fruits than K. gabonensis that marks the 
small-fruited Makokou taxon. Klainedoxa ga- 

onensis var. microphylla is characterized by the 
small, blunt-tipped leaves that mark the glau- 
cous-fruited Makokou plant. Since there is no 
doubt that this represents a distinct species and 
none of the published specific epithets seems ap- 


168 


plicable to a blunt-leaved entity, elevation of var. 
microphylla to species rank is unavoidable. 


а аа (РеПергіп) А. Сепігу, 
со К. a var. mi- 
tie: e Bull. ot. France 
71: 54. 1924. TYPE: vie Maboumi 
LeTestu 1823 (P, not seen). 


This is apparently the same taxon as the “im- 
perfectly known" K/ainedoxa species from Ghana 
mentioned in the “Нога of West Tropical Af- 
rica." It is possible that the earlier name K. 
sphaerocarpa Tieghem (1905: 303) applies to this 

xon. However, that species was based entirely 
on fallen fruits, described as spherical and 3—4 
cm in diameter. Since the fruits that constitute 
the type of K. sphaerocarpa are apparently no 
longer extant (Letouzey, pers. comm. ), and since 

rrant or immature fruits of either K. trillesii 
or K. gabonensis could also fit the inadequate 
description, it seems preferable to raise the well- 
known and well-typified var. microphylla to spe- 
cific rank rather than resurrect the undocument- 
ed epithet sphaerocarpa. 

The three species of Klainedoxa at Makokou 
(and in the world) may be separated by the fol- 
lowing key. Note that the leaf dimensions refer 
only to mature leaves. The juvenile leaves of K. 
microphylla and K. trillesii are unknown. How- 
ever, since juvenile leaves of K. gabonensis are 
often much larger than mature leaves, it is likely 
that the same will prove true for the other two 
species. If so, their juvenile leaf dimensions may 
overlap with those of K. gabonensis. 


KEY TO SPECIES 


1. allintic +, T 
кина 3.5-4.5 cm in diameter, енер gray- 


microphylla 
. Leaves acute at apex, ovate to ‘ovate-lanceo- 


— 
- 


wide, turning yellow at maturity . = bud 
ves m 


(4—)5 cm wide; fruits 4-4.5 cm ots nie 
5—7 cm wide, green at maturity 


_ К, gabonensis 


Since no attempt has been made to study all 
extant material of К/аіпейоха, it may seem pre- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


mature to apply the Makokou results to the entire 
owever 


all available evidence suggests that there is no 
breakdown of the key differentiating characters 
elsewhere in Africa, despite the notorious intra- 
specific variability of K. gabonensis. Moreover, 
the three Makokou taxa clearly “pass the test of 
sympatry," mandating taxonomic recognition at 
the species level even were the species limits ob- 
scured elsewhere. By definition subspecies are 
allopatrically distributed variants. Recognition 
ofthe three Makokou taxa at varietal level would 
imply differences in only a few genes, clearly in- 
compatible with the whole suite of consistent 
differentiating characters in both fruit and leaves 
reported here. 


LITERATURE CITED 


AUBRÉVILLE, A. 1962. Irvingiaceae. Jn Flore du Ga- 
bon 3: 12-32. 

ENGLER, A. 1907. Samson africanae II. Bot. 

Jahrb. Syst. 39: 5 

. 391]. ae africanae III. Bot. Jahrb. 

Syst. 46: 285. 

FLORENCE, J. & A. HLADIK. 1980. Catalogue des pha- 
nérogames et des ptéridophytes du nord-est du 
Gabon (Sixième liste). Adansonia, Sér. 2, 20: 235- 
253. 


GILBERT, G. 1958. Vd Up ua z Flore du Congo 
Belge et du Ruanda-Urundi 7 
HALLE, N. 1964. Liste de а et de pté- 
ridophytes ue environs de Makokou, Kemboma 
et ivo : 41-46. 
1965. ав liste de phanérogames et pter- 
idophytes du N.-E. Gabon okon, Bélinga, & 
Mékambo). Biol. Gabon. 2: 337-344 P. 
& A. LE THomas. 1967. Troisiéme liste 
phanérogames du N.-E. Gabon (Makokou, Bélin- 
ga, et Мру Ар Gabon. 3: 113-120. j 
Quatrième liste de phan 
rogames et оне ди М.-Е. du Gabo 
sin du L’Ivindo). Biol. Gabon. 6: 131-138. 
HLADIK, A. & N. НАШЕ. 1973. Catalogue des pha- 
^N nquiéme liste). 


PELLEGRIN, F. 1924. 
s du genre K/ainedoxa Pierre. Bull. 
France 71: 51—56. 
TIEGHEM, P. VAN. 1905. Sur les Irvingiacées- Am 
Sci. Nat . Bot., Ser. 9, 1: 245-320. 


NOTE ADDED IN PROOr: After reading this vr 
script, John Hart and Terese Hart нече me that 
independently recognized the same three утра 
species of Klainedoxa while — ungulate 
persal in the Ituri Forest of Zaire 


o mmm 


——— и "~ 


о 


| 
| 
| 
| 
| 
| 
| 
3 
| 
3 
| 
| 


| 
| 
| 


^ 
| 
{ 


[ 


PSYCHOTRIA HEBECLADA DC. (RUBIACEAE), AN 
OVERLOOKED SPECIES FROM 
CENTRAL AMERICA! 


CHARLOTTE M. TAYLOR? 


ABSTRACT 


Two species of Psychotria, P. pubescens and P. hebeclada, occur sympatrically in Central America 
and have been erroneously combined in several recent floras. Distinctions are drawn between these 
ар 0 and inf and a descripti nee 


map, 


two species, primarily using characters of 
and illustration of each species is presented. 


The Rubiaceae are one of the largest families 
of plants, and a very conspicuous component of 
the flora of Central America. Dwyer (1980) es- 
timated that this is the largest dicotyledonous 
family in Panama. Psychotria is the largest genus 
in the family, currently estimated to include about 
800 (Dwyer, 1980) to 1,000 (Standley & Wil- 
liams, 1975) species distributed through the moist 
tropical regions of the world. This genus is well 
represented in the New World tropics, and many 
new species are being described as new areas аге 
explored. For instance, Dwyer recently (1980) 
Teported 97 species of Psychotria from Panama, 
34 of them new. 

Psychotria pubescens Sw. is a common species 

ound in lowland Central America, southern 
Mexico, and the West Indies. Psychotria hebe- 
clada DC. is also found in Central America, as 
wellas in northern South America, but itis much 
less common. These species are quite distinct 
and can be easily separated from each other, but 
копу Р. hebeclada has been treated in several 

Oras as a synonym of P. pubescens (Croat, 1978; 
Dwyer, 1980) or even overlooked altogether 
(Standley & Williams, 1975). 


: THE DIFFERENCES BETWEEN 
SYCHOTRIA PUBESCENS AND P. HEBECLADA 


inc superficially similar, these two species 
ан Ee features of the inflorescence, 
Brack ids: poene as well asin flower color, 
«ац E ; ecology, and distribution. These lat- 
Миња Uarities are less consistent, but до sup- 

Separateness of the two taxa. These dis- 


абыр. 
Of these t : 


tinctions are discussed below, and summarized 
in Table 1 and in a key. The descriptions pre- 
sented here are based on examination of ap- 
proximately 1,400 herbarium specimens from the 
collections of A, CAS, DS, DUKE, ENCB, F, 

H, MICH, MO, NY, and US. 

These species differ most strikingly in the shape 
of the inflorescence. In both species the inflores- 
cence is composed of a thyrse of similar, rather 
irregular cymes of both pedicellate and sessile 
flowers. However, as noted by de Candolle in his 
original description of Psychotria hebeclada, the 
inflorescence of P. pubescens is corymbiform in 
arrangement. The primary branches at each node 
are nearly equal in size to the central axis and 
are ascending to spreading in orientation, and 
the resulting outline of the top of the inflores- 
cence is a gentle convex curve. In contrast, the 
inflorescence of P. hebeclada has a well-devel- 
oped central axis from which smaller branches 
diverge nearly horizontally. This inflorescence is 
thyrsiform or racemiform, and its overall outline 
is conical or even somewhat trapezoidal (Fig. 1). 

The inflorescence shapes are correlated with a 
difference in the morphology of the calyx. The 
lobes ofthe calyx are cl teristically very short 
in Psychotria, and P. pubescens is typical with 
broadly triangular or somewhat ovate lobes which 
are commonly 0.3—0.8 mm long but may be as 
much as 1-1.1 mm long. The calyx lobes of P. 
hebeclada are 0.6-2.3 mm long and are lanceo- 
late or ovate. Unlike those of P. pubescens, these 
lobes are usually acuminate and are often api- 
cally reflexed as well. Further, the inner surface, 
thus exposed, often shows two well-developed 


1 
Thanks аге due to the curators of the herbaria listed above for their prompt and courteous loan of specimens 
t d 


WO species. Special thanks al Dr. К 

and peci an So go to 
К Mr. Melvin Turner for their help and suggestions 
Partment of Botany, Duke University, Durham 


ANN. MISSOURI Bor. Garp. 71: 169-175. 1984. 


L. Wilbur, curator of DUKE, and to Dr. Lucinda McDade 


` North Carolina 27706. 


170 


ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


TABLE 1. Summary of the characters which distinguish Psychotria hebeclada and P. pubescens. 


Character 


P. hebeclada 


P. pubescens 


Calyx Length 
Calyx Lobe Shape 


Inflorescence Shape 


(0.6—)0.8—2(—2.3) mm long, longer 
than gland. 


Lanceolate or ovate, apically acu- 
minate. 

Thyrsiform or racemiform, about 
(0.6—)0.8—1.3 times as long as 
broad, central axis well-devel- 


0.3-1.1 mm long, equal to or 
shorter than gland. 
Triangular, apically acute. 


Corymbiform, about 0.5-0.7 times 
as long as broad, central axis 
poorly developed, branches as- 


oped, branches horizontal. cending. 
Pubescence Pilosulous to hirsutulous, hairs Puberulous to pilosulous, hairs 
(0.1-)0.3-0.7(-0.9) mm long. (0.1-)0.15-0.4(-0.5) mm long. 
Bracts 


ers 1.5-2.5 mm long. 


Flower Color 
rose, rarely yellowish. 


Linear, those subtending the flow- 


White, usually tinged with pink or 


Triangular to lanceolate, those sub- 
tending flowers 0.5-1.5 mm 
long. 

Yellow-white or yellow, occasion- 
ally tinged with pink. 


Habitat Moist to wet forests and edges, Forests and disturbed areas, moist 
often along rivers. or seasonally dry areas, often on 
limestone. 
Habit Erect or scandent. Erect. 
Distribution Mexico, Central America, north- Mexico, Central America, West In- 
western South America. des он 


marginal veins paralleling the midvein. The ca- 
lyx lobes of P. pubescens are almost never acu- 
minate and are only rarely reflexed, and when 
reflexed the midvein is the only vein apparent 
on the inner surface. 

Plants of both species are usually covered with 
soft, spreading, pilosulous pubescence, although 

few specimens of each species were seen that 
were only sparsely pubescent or very minutely 
puberulent. The hairs of Psychotria pubescens 
are usually straight and uniform in length and 
distribution. The hairs of P. hebeclada are usu- 
ally somewhat uneven in length and distribution, 
and often wavy. This species is often more 
sparsely pubescent than P. pubescens, and the 
pubescence is sometimes rather more hirsutu- 
lous than pilosulous. 

The corollas of Psychotria pubescens are usu- 
ally yellowish white, although they may be white 
or even tinged with pink. Psychotria hebeclada 
has corollas that are usually white or pink-tinged, 
and are rarely yellowish. This species also has 
very narrow floral bracts, which may be as short 
as 0.5 mm but are generally 1.5-2.5 mm long, 
nearly as long as the flowers they subtend. These 
bracts commonly persist on the infructescences 


and are easily seen. The floral bracts of P. pl 
bescens are also narrow, but these tend to be 
more triangular than linear and are usually about 
0.5-1.5 mm long, much shorter than the flowers 
they subtend. These bracts are also usually Pê 
sistent, but are much less obvious on the infruc- 
tescence because of their small size. 
Psychotria pubescens is found from sea level 
to about 1,500 m, and is most common 1n dry 
or seasonally dry forests and edges but also 0€ 
curs in moist or wet forests and along streams 
and rivers. Psychotria hebeclada has а 5 
elevational range, but it has nearly always been 
collected in moist forests, and very often on "m 
erbanks. This species is especially well терт“ 
sented by material from the La Selva field sta” 
in lowland northeastern Costa Rica, where 
intensive program of collecting is presently 
derway (Hammel & Grayum, 1982). This ant 
has been quite extensively explored, but P. 
beclada is known only from river edge forest 
Interestingly, no P. pubescens has so far реет 
collected at the La Selva station. In Costa REM 
P. pubescens is largely found on the western 
of the continental divide, in the seasonally 
regions (Fig. 2). 


1984] TAYLOR—PSYCHOTRIA HEBECLADA 171 


RE 1, 
df d. no 
Specim 


Psychotria pubescens is found from Panama 
ссе through Central America to southern 
we nd in the West Indies (Fig. 2). It has 
Ost commonly collected in Belize, Gua- 

a 


i зе in southern Mexico, Belize, and 
No collections of this species were 


Psychotria hebeclada. а—с: a, inflorescence; b, flower, showing calyx; с, fruit. Psychotria pubescens. 
scence; e, flower, showing calyx; f, fruit. Composite drawings, based on examination of numerous 


seen from east of the former Canal Area in Pan- 
ama. Conversely, P. hebeclada increases in abun- 
dance southward and is not known to occur in 
the West Indies. This species is found from Cen- 
tral Mexico south into northern South America. 
It has been collected only sporadically in the 
northern part ofi ite range, and most of the spec- 


imens in the Cos 
Rica, Panama, and Colombia. Although some 
specimens from Colombia have smaller and more 


172 


4. Psychotria hebeclada 
© Psychotria pubescens 


SCALE 
зоо E 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


FIGURE 2. Distribution of Psychotria pubescens (circles) and P. hebeclada (triangles). 


attenuated inflorescences, the distinctive conical, 
racemiform shape of the panicle and the com- 
paratively long calyx lobes are still evident. 

At first glance, stipule morphology seems to 
be a reliable character as well. However, both of 
these species display an exceptional diversity of 
stipule shapes that precludes the use ofthis char- 
acter. In both of these species the stipules are 
fused both interpetiolarly and intrapetiolarly to 
form a sheath. This is truncate and bears two 
triangular lobes or awns on each side. However, 
the stipule sheath of Psychotria pubescens may 
be very poorly or very strongly developed, and 
the lobes may range from rounded, minute pro- 
jections t to aciculate awos 3-6 mm long. Further, 

1 br апсћ 
At: young nodes, the lobes are very close together, 
so that they often resemble one point. Alain 
(1962) in fact describes the stipules of this species 
only in this way, and since his key to Psychotria 
uses this feature many specimens of P. pubescens 
from Cuba cannot be keyed here. As the stems 
increase in girth with age, the stipules may in- 
crease in diameter in several ways. Sometimes 
there is intercalary growth between the lobes, so 
that these are moved further apart, and the sheath 
remains in a continuous ring. Often, the sheath 
expands to a limited extent between the lobes, 


then tears partially or completely as the stem 
continues to grow. Occasionally, the sheath pc 
simply tear as the stem expands, leaving 
separate stipule lobes with no evidence of po 
petiolar fusion. The variation in stipule тог 
phology encountered in this species alone, cr 
on one branch of one individua of this spec! 

d me of the confusion 
which oin the identity of many species 0 
Psychotr, 


KEY To PSYCHOTRIA гон AND 
P. HEBECLA 


1. Inflorescence thyrsiform or racemiform " er 
ally (0.6-)0.8-1.3 times as long as W е 
a well-developed central ax 
branches (especially the middle and үа 
bran ranches) more — than the axis an ^ 
s lanceolate to ec 


acuminate and reflexed apically; pubescence 
of the inflorescence hirsutulous ог co of inet ^ 
e hairs often what crinkled or о 
ular lengths, 0.1-0.9 mm long, the longest База јаја 


usually about 0.3-0.7 mm long — 1. o7 
1. Inflorescence жы usually ©. 


times as long as , with a central pee 
which is usually little stouter 2 more em al branch- 
sized than the branches ix sadly 


es spreading or — à 


нь 


1984] 


triangular or slightly ovate, 0.3-1.1 mm long, 
as long as or usua 


rul 
ofuniform lengths, 0.1—0.5 mm long, the long- 
est hairs usually about 0.15—0.4 mm long ..... 
2. P. pubescens 


l. Psychotria hebeclada DC., Prodr. 4: 513. 
1830. ТҮРЕ: Mexico, not seen. 


Psychotria justicioides Schldl., Linnaea 9: 596. 1834. 
TYPE: Mexico. Barranca de Tioselo, not seen. Ura- 
goga justicioides Kuntze, Rev. Gen. 1: 300. 1891. 

Psychotri lli Scl & Krause, Bot. Jahrb 
Syst. 40: 331. 1908. туРЕ: Colombia. Prope las 
Juntas ad Rio d'Agua, Cauca, 200-500 m, Leh- 
mann 4667 (holotype, B, not seen; photograph 
МҮ!; isotype, К, not seen; photograph NY!). Psy- 
chotria molliramus Steyerm., Mem. New York 
Bot. Gard. 23: 529. 1972. 


Herbs or more often shrubs 1—4(-8) m tall, 
erect or sometimes lax or scandent. Stems round- 
ed, sparsely to somewhat densely puberulent or 
pilosulous with spreading hairs, generally gla- 
brescent with age, with a fleshy section about 
0.5-0.8 cm long usually present immediately be- 
low each node and generally constricted with 
drying. Stipules persistent, puberulent or pilo- 
sulous with spreading hairs, composed of a short 
sheath bearing two triangular lobes; sheath about 
ман mm long, continuous around the stem ог 
metimes splitting int tiolarly instead of ex- 


“ 


е 0.5 cm long, basally acute to attenuate, 
:3-)7.5-17 cm long, (1-)2.5-8 cm wide, about 


ан with the costa and sometimes the lateral 
about ee ne Dilosulous, with the lateral veins 
ly archi 15 on each side of the midrib and broad- 
aii њи with petioles (0.2-)0.5—1(-2.5) cm long 
ris rulent or pilosulous with spreading hairs. 

i oo terminal, erect, usually peduncu- 
45 ky Lo subsessile, the peduncle (0.5—)1– 

: ong, the panicle thyrsiform or racemi- 


Or com 


t trapezoidal 


kie : well-developed central axis and horizon- 
Té Сч lateral branches, 1.7-4.5 cm long, 
иш Ст wide, (0.6-)0.8-1.3 times as long as 
бы зе the base, the peduncle, axis, branches, 


nda 


TAYLOR—PSYCHOTRIA HEBECLADA 


173 


sparsely or usually rather densely spreading-pi- 
losulous or spreading-hirsutulous, the hairs 0.1– 
0.9 mm long, the longest usually about 0.3-0.7 
mm long; bracts linear, often with ciliolate mar- 

ins, 1.5-6 mm long, those immediately sub- 
tending flowers about 1.5-2.5 mm long. Flowers 
sessile or borne on pedicels to 5 mm long; calyx 
spreading-pilosulous or spreading-hirsutulous, 
the free portion cut into five lobes, these narrowly 
lanceolate or ovate or sometimes widely so, 
somewhat foliaceous, acuminate and usually re- 
curved at the apex, (0.6—)0.8—2(-2.3) mm long, 
with the costa and two marginal veins prominent 
on the inner surface and the margin generally 
somewhat ciliate; corolla tubular, puberulous or 
very shortly pilosulous outside with spreading 
hairs, glabrous within except for a short-pilose 
ring at the level of the attachment of the fila- 
ments, white or sometimes tinged with green or 
rose, the tube about 3—4 mm long, the five lobes 
triangular, (1.2-)1.5-2 mm long and about half 
as wide as long at the base; anthers narrowly 
oblong, about 1.2-2 mm long, in the long-styled 
form included in the tube, in the short-styled 
form partially exserted; styles dimorphic, the short 
form extending to the level of the stamen at- 
tachment, the long form conspicuously exserted, 
both forms with a bilobed stigma and surround- 
ed at the base by a gland or nectary about 0.5 
mm long, this gland composed of two cycles, the 
outer one somewhat lobed and foliaceous, the 
inner bilobed or rather toroid and smooth and 
glandular; fruit elliptic, compressed-globose, 
didymous, angled when dry with five smooth, 
nearly plane faces on each half, about 3-5 mm 
ong and wide, sparsely puberulent, maturing to 
blue-black; seed angled, with about 5 smooth 
planar faces and a longitudinal invagination on 
the inner face. 


— 


+ A anaac Aa) 


Moist or wet fe ges, g rivers; 
sea level to about 1,500 m, most often collected 
between 100 and 400 m. Flowering and fruiting 
throughout the year, and often concurrently on 
the same plant. Figure 1a-c. 


Steyermark (1972) maintained Psychotria 
molliramus (Schumann & Krause) Steyerm. as a 
species separate from P. hebeclada primarily be- 
cause of a unique, five-lobed foliaceous gland 
found at the base of the style. He placed this 
species in a monotypic series, Mollirami Stey- 
erm., but suggested that because of this special- 
ized structure P. molliramus may deserve rec- 
ognition as a separate genus. He reported the 


174 


geographic range of P. molliramus as including 
Costa Rica, Panama, Venezuela, Colombia, and 
Ecuador. According to Steyermark, P. hebeclada 
is found in Guatemala and southern Mexico, and 
has a solid, bilobed gland. However, examina- 
tion of specimens from all of these areas, in- 
cluding specimens cited as P. molliramus by 
Steyermark (1972), suggests that there are diff- 
culties with this distinction. The form of the gland 
is similar on all specimens examined, and con- 
sists of both an outer, rather foliaceous ring, which 
is usually lobed, and an inner, solid portion, which 
is often bilobed. Thus, Steyermark’s description 
of the disk of P. molliramus as an “elevated, 
conical form ending in five, [sic] loose, erose or 
dentate lobules” was accurate, but incomplete, 
as was his description of the gland of P. hebe- 
clada as a “‘bilobed disk." The other differences 
between these species that he lists, in inflores- 
cence shape and size, morphology of the inflo- 
rescence bracts, and presence or absence of the 
constricted zone below the nodes, are not dis- 
tinctive. The differences in inflorescence char- 
acters are not consistently correlated with each 
other or with any geographic distribution and 
represent the normal variation of these charac- 
ters within the species. The presence of the con- 
stricted zone beneath each node on dried spec- 
imens is characteristic of the subgenus 
Heteropsychotria Steyerm.; these zones were seen 
on all sheets examined. Thus, P. molliramus can- 
not be maintained as a — Apes 

Standley (1926) i ti 
of Psychotria aureola sse ex DC. and Р, 
bracteolata Martius & Galeotti suggest that these 
species are “closely related" to P. hebeclada. Since 
no material has been seen, it is unclear whether 
these species are in fact synonymous with either 
P. hebeclada ox P. pubescens. Judging from the 
description, P. aureola is certainly not synony- 
mous with P. hebeclada; however, it may be a 
form of P. pubescens. 

Dimorphic heterostyly has been noted often 
in species of Psychotria. Herbarium material sug- 
gests that this condition occurs in P. hebeclada 
but examination ofliving plants will be necessary 
for confirmation 


2. Psychotria pubescens Sw., Prodr. Veg. Ind. 
Occ. 44. 1788. TYPE: Jamaica. Brown 161, 
not seen. Uragoga pubescens Kuntze, Rev 
Gen. 2: 962. 1891. пета е 
A. Hitchc., Annual Rep. Missouri Bot. Gar 
4: 95, 1893. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


ipie Mie e Swartz var. cuspidata DC., 
been а de 1830. TYPE: Santo Domingo. Ber- 


Кос scabriuscula Bartling ex DC., Prodr. 4: 513. 
830. E: Mexico. Acapulco, not seen. Uragoga 
cabr cate Kuntze, Rev. Gen. 2: 962. 1891. 
Psychotria о де Linnaea 41: 569. 1877. 
s: Costa Rica. San José, Polakowsky 377 
& 3 78, g% FA - Санте glauca Kuntze, Rev. 
Gen. 2: 960. 


Shrubs 1.5-2.5(—6) m tall, erect. Stems round- 
ed, sparsely or more often moderately to densely 
spreading-puberulent or spreading-pilosulous, 
occasionally glabrescent, with a fleshy section 
about 0.5-1 cm long usually present immediately 
below each node and generally constricted on 
dried specimens. Stipules persistent, often be- 
coming indurate with age, puberulent or pilo- 
sulous with spreading hairs or sometimes gla- 
brescent, variable in shape but usually composed 
of a short sheath bearing two triangular lobes, 
sheath to 1.2 mm long, continuous around 
the stem or ti splitting partially or com- 
pletely to the base instead of expanding, lobes 
(1.1—)1.5—2.5(—4) mm long, acute or aciculate at 

the apex, sometimes fused into one entire or раг- 
tially bifid lobe. Leaves with membranous blades, 
these narrowly to widely elliptic or somewhat 
oblong, apically acute or more commonly atten- 
uate, (5-)8-13(-17) cm long, (1.223-4.5 (C65) 
cm wide, usually about (1.5—)2-3.3 times as long 
as wide, spreading-puberulous or spreading-pi- 
losulous throughout or sometimes glabrescent, 
with lateral veins about (7-)8-13(-16) on each 
side of the midrib and arching, with petioles 0.2- 
2 cm long, puberulous or short-pilosulous with 
spreading hairs or sometimes glabrescent. Inflo- 
rescences terminal, erect, the peduncle 15236 
4) ст long, the panicle corymbiform, rather open 
and lax, the main axis not strongly develo 
and the lateral branches usually spreading 10 Ф 
cending or occasionally widely spreading, l- T: 
cm long, 3-9.5 cm wide, usually about t 0.50. 
times as long as wide (1.5-2 times as wide 45 
long) at the base; peduncle, axis, branches, P 
and pedicels often flushed with purple, spre4 
ing-puberulent or spreading pilosulous, | — 
densely so but rarely glabrescent, the hairs | 
0.5 mm long, the longest usually about 0. 7 
mm long; bracts triangular to lanceolate, W 
entire margins, 0.5-5 mm long, those imm 
se subtending the flowers about 0.5-1.5 mm 


- 


glabrescent or usually puberulous or pilosul 


- 


— 


1984] 


with spreading hairs, the free portion cut into 
five triangular or shortly ovate lobes, these api- 
cally acute or rarely shortly acuminate, 0.3-1.1 
mm long, with the midvein sometimes visible 
but usually without apparent nerves; corolla tu- 
bular, puberulous or sometimes glabrous out- 
side, glabrous within or often bearing a pilose 
ring at the level of the stamen attachment, white 
or more often yellowish white or yellow and 
sometimes tinged with green or rarely with pink, 
the tube about 3-4 mm long, the lobes 5, tri- 
angular, 1.6–2.1 mm long and about half as broad 
as long at the base; anthers narrowly oblong, 1.1- 
1.6 mm long, in the long-styled form included 
in the tube, in the short-styled form partially 
exserted; styles dimorphic, the short form ex- 
tending to the level of the stamen attachment, 
the long form conspicuously exserted, with the 
stigma bilobed on both forms and both forms 
surrounded at the base by a gland or nectary 
about 0.5-1 mm long and composed of two cycles, 
the outer one somewhat lobed and foliaceous, 
the inner bilobed or rather toroid and glandular; 
fruit elliptic, compressed-globose, didymous, an- 
gled when dry with 5 smooth, somewhat plane 
faces on че half, about 3—5 mm long and wide, 
sparsely puberulent or glabrescent, maturing to 
blue-black or black; seed angled, with about 5 
smooth planar faces and a longtudinal invagi- 
Nation on the inner face. 


Moist or wet forests and d seasonally dry 
forests and edges, disturbed ground, and often 
9n limestone slopes or Ји E sea level to 
about 1,500 m. Flowering and fruiting through- 


TAYLOR—PSYCHOTRIA HEBECLADA 


175 
out the year, often concurrently on a single plant. 
Figure 1d-f. 


This species also appears to be heterostylous, 
but again this must be confirmed with living ma- 


ct 
e 


rial. 

Psychotria pubescens is very common 
throughout most of its range, and it often grows 
in very accessible areas. Because of this a very 
large number of specimens of this species are 
available in most collections. This species is also 
rather nondescript, and it is often misidentified. 
It is commonly mistaken for other species of 
Psychotria and it is often found among uniden- 
tified specimens of Rubiaceae. 


LITERATURE CITED 


ron H. 1962. Flora de Cuba 5. Editorial Univ- 
ewig Universidad de Puerto Rico, Río Pie- 


ds 

CROAT, T. B. 1978. Flora of Barro Colorado Island. 
Stanford University A Stanford. 

DwYER, J. 1980. Fam e Rubiaceae. Jn R. 
E. Woodson, Jr. & W ora A Panama, 
Part IX. Ann. Missouri Би. Cad 67: 1-522. 

HAMMEL, B. E. & М.Н. UM. 1982. Preliminary 
report on the flora project of La Selva field station, 
Costa Rica. Ann. Missouri Bot. Gard. 69: 420- 


STANDLEY, P. C. 1926. Trees and shrubs of Mexico. 
Contr. U.S. Natl. Herb. 23: 1313-1721. 
. О. WILLIAMS. 1975. Rubiaceae. Jn Flora 
of Gua ria ^ Part XI. Fieldiana, Bot. 24: 1-274. 
SOME J. A. 1972. Rubiaceae. /n B. Maguire 
& Colla borators, The Botany of the Guayana 
Highland, Part IX. Mem. New York Bot. Gard. 
23: 227- 


ESTIMATION OF GENOME SIZE (C-VALUE) IN 
IRIDACEAE BY CYTOPHOTOMETRY' 


PETER GOLDBLATT,? VIRGINIA WALBOT,? AND ELIZABETH A. ZIMMER* 


ABSTRACT 


Nuclear genome sizes have been calculated for 19 genera and 30 species of Iridaceae using cyto- 
spectrophotometry. Mean extinction values for nuclei in squashes of actively growing root tips stained 
in Schiff's reagent were compared with a standard, maize, of known genome size, treated in the same 
way. Values range from lows of 1.1 to 4.9 pg DNA per nucleus in diploid species of subfamily Ixioideae 
to a high of 65.1 pg in Iris histrio, subfamily Iridoideae. Genome size in diploid Iridoideae ranges 


species or genera have very similar genome sizes. 


Iridaceae are a plant family of nearly world- 
wide distribution, comprising some 1,500 species 
in about 85 genera usually assigned to two or 
three subfamilies, Iridoideae, from which Sisy- 
rinchioideae may not be separable, and Ixioi- 

eae. Species are concentrated in Africa where 
more than half the genera and species occur, and 
in South and Central America including Mexico. 
The systematics of the family is comparatively 
well known, particularly in the Old World. Chro- 
mosome cytology is also well known, and un- 
usually varied for a family of this size. Chro- 
mosome size ranges from very small in some 
Australasian and South American genera to very 
large in Old World genera such as 1715, Moraea, 
and their allies, while base numbers for genera 
range from x — 16 to 6. Chromosome numbers 
and karyotypes are known for most genera and 
for many species in most of these but there have 
not been until now any satisfactory measure- 
ments of absolute size of the genome of various 
genera and species, i.e., the amount of DNA per 
cell or C-value. In this paper we present mea- 
rem f nuclear g ize for a wide range 
of species and genera of Iridaceae following a 
standar i t hot i thod 


antc 


ytosp | d for es- 
timating DNA content. Genome sizes for the 30 
species in 19 genera studied here have been cal- 


culated by comparison against a standard, Zea 
mays, of known genome size, 6.3 pg (Hake & 
Walbot, 1980). 


MATERIALS AND METHODS 


Plants studied were all of wild origin, the col- 
lection data and voucher information for which 
is presented in Table 1. Measurements were made 
on nuclei in root tip apices fixed in Carnoy’s 3: 
1 absolute etl EN pode à : 1 and stained 


in Schiff's reagent. Root tips of the maize stan- 
dard were fixed and stained at the same time and 
in the same way as the species of Iridaceae. Cy 
tophotometric determinations were made using 
a Zeiss Universal microscope equipped with 2 
Zeiss Type 03 Microphotometer with an auto- 
matic scanning stage. A planapochromat oil 1m- 
mersion objective NA 1.32 x 100 was used for 
all measurements. 

Approximately 20 measurements were made 
for each species. Mean relative values of the 
amount of DNA per cell were calculated for each 
species by obtaining the average of the lower 
readings (2C-values) and half the high reading 
(4C-values). Low readings represent cells 1n a 

Күн qup E «^£ Aunnlication 


DOS e 
of the genome and the high readings ho 
cells that have completed the duplication 9 


' Supported by grants DEB 81-15322 to У. №. and DEB 81-19292 to P. С. from the U.S. National Scient? 


Foundation. We thank Dr. O. R. Collins, Department of Botany, 
making available to us his microphotometry equipment. We 


Department of Biology, Washington University, 
? B. A. Krukoff Curator of African Botany, 
63166. 


* Department of Biology, Washington University, 


ANN. Missouri Bor. GARD. 71: 176-180. 1984. 


University of California, Berkeley, for Le "ei 
also extend our thanks to Dr. Alan TemP 


St. Louis, for his advice on how to analyze the data statisti у. 
Missouri Botanical Garden, Р.О. Box 299, St. Louis, Miss 


3 Department of Biological Sciences, Stanford University, 


Stanford, California 94305. 


St. Louis, Missouri 6313 


a 


—— 


1984] 


TABLE 1. 
Botanical Garden (МО). 


GOLDBLATT ET AL.—GENOME SIZE IN IRIDACEAE 


177 


Voucher information for the species used in this study. All specimens are housed at Missouri 


Species 


Collection Data 


SUBFAMILY a (Including SisvRINCHIOIDEAE) 


Tris histrio L. 
Dietes grandiflora N. E. Br. 
Galaxia fugacissima (L. f.) Druce 


M. ciliata (L. f.) Ker 
M. fugax (de | Roche) Jacq. 
population 
populati f 
M. meme Goldbl. 
M. calcicola Goldbl. 
M. tulbaghensis L. Bol. 
M. villosa (Ker) Ker 
M. unguiculata Ker 
M. bipartita L. Bol. 
Hexaglottis namaquana Goldbl. ined. 
Homeria bifida L. Bol 
H. pendula Goldbl. 
. flaccida Sweet 
Sessilistigma radians Goldbl. ined. 
Gynandriris setifolia (L. f.) Foster 
Roggeveldia fistulosa Goldbl. 


Cipura paludosa Aubl. 
isyrinchium convolutum Nocca 


тири 


wt л л {л (л (л (л (л үл л {л (л (л и 


р WORLD 


Israel, Golan Heights, Goldblatt s.n., no voucher 
‚А 4 


Я , Riebeek East, Bayliss 
Africa, Cape, Middleton, dade Goldblatt 2631 
Africa, Cape, Elim, Goldblatt 2 
Africa, Cape, алате се. 3300 
са, Cape, Wolseley, Goldblatt s.n., no voucher 


Africa, Cape, Klawer, Goldblatt 5778 
Africa, Cape, Koeberg, Goldblatt 4080 
Africa, Cape, Caledon distr., Goldblatt 5635 
Africa, Cape, Saldanha hills, Goldblatt 4118 

ca, Cape, Gouda, Goldblatt s.n., no voucher 
лека Саре, below Суйо Pass, Goldblatt 2594 
Africa, Cape, Pub. Goldblatt 2777 
Africa, Cape, near Hankey, Goldblatt 2076 
Africa, Cape, Spektakelberg, direc dd 3059 
Africa, Cape, Rebunie, Calvinia, Goldblatt 
Africa, Cape, Kamiesberg, Goldblatt 4306 
Africa, Cape, Twenty Four Rivers, Goldblatt 3924 
Africa, Cape, near Macgregor, Goldblatt 5903 
Africa, Cape, near Matjesfontein, Goldblatt 3215 
Africa, Cape, Roggeveld Escarpment, Goldblatt 4163 


New WORLD TAXA 


Nicaragua, Henrich 143 
Nicaragua, Henrich 152 


SUBFAMILY IXIOIDEAE 


шю л л лл лл л 


Africa, Cape, Olifantskop, Langebaan, Goldblatt 2335 
Africa, Cape, Sandbaai, anus, Goldblatt 5293 
ca, Cape, near Albertinia, Goldblatt 4855 
, Cape, eskraal, Caledon dist., Powrie s.n. 
Africa, Cape, Spektakelberg, Namaqualand, Goldblatt 2789 
ca, Cape, near Botrivier, Goldblatt 5641 
Айок Cape, Wildepaardehoek, Namaqualand, Goldblatt 5754 
Africa, Cape, Roggeveld, Goldblatt s.n. 


this group is very high, but the results are, never- 


мате but have not begun to divide. The high 
in ape were consistently approximately twice 
in ings in the low range. Intermediate read- 
ES Were disregarded. In all samples studied, 
e 


ge. 
Muf ly was experienced in obtaining mea- 
; zi in Ixioideae. The nuclei were weakly 
and contrasted poorly with the back- 


theless, of value for comparison with other Iri- 
ceae 


RESULTS AND DISCUSSION 


The results of our measurements of genome 
size relative to the maize standard are reported 
in Table 2, along with the standard deviation of 
the measurement. The haploid and basic chro- 
moomo number of each species, also included 
in n from previously published 
cats оти 1971, 1976, 1979, 1980) ог 


ч. 


178 


from papers in preparation. This represents the 
only extensive set of measurements in Iridaceae 
of nuclear genome size, which, in non green cells, 
can be regarded as essentially equivalent to the 
total cellular DNA content. The only previous 
determinations of genome size in Iridaceae, ac- 
cording to Bennett’s (1972) review of amounts 
of nuclear DNA in angiosperms, are two reports 
for Gladiolus. One, by Sparrow et al. (1965), for 
a cultivar, Gladiolus ‘Friendship,’ is an estimated 
value of 13.5 pg. In the other, Baetke et al. (1967) 
obtained 6 pg for Gladiolus ‘Mansoor.’ In both 
cases the material studied was reported to be 
tetraploid. This second report is in fairly close 
agreement with our own estimation of 3.2 pg for 
a diploid species of this genus. The much higher 
figure reported by Sparrow et al. must apparently 
be disregarded. The relatively low genome sizes 
established for Gladiolus seem characteristic for 
subfamily Ixioideae, in which a range of values 
from 1.1 to 4.9 pg have been determined for 
seven diploid species, each a different genus. The 
genome size in the tetraploid Pillansia, 5.4 pg, 
is also consistent with the range for Ixioideae. 
These results are consistent with karyotypic ob- 
servations for Ixioideae (Goldblatt, 1971), in 
which small cl 1 teristi d 
there seems no substantial variation in the total 
amount of chromosome material, as estimated 
by linear chromosome measurement, in diploid 
members of a range of genera of this subfamily, 
from Babiana with a low x = 7 to Gladiolus with 
x= 15. 

Subfamily Iridoideae provides a sharp con- 
trast. Genome sizes range from 6.4 pg in Galaxia 
fugacissima to a high of 36.4 pg in Moraea cal- 
cicola, g diploid species in Southern Africa. 
A 65.1 pg genome was found in the Middle East- 
ern Iris histrio, a species possibly of tetraploid 
origin although it is not polyploid compared with 
closely related species. The figures reflect the large 
difference in total chromosome size of Old World 
Iridoideae vs. Ixioideae, pointed out by Gold- 
blatt (1971). The results also seem to confirm 
Goldblatt’s (1976) contention that cytological 
evolution in Moraea, diploid species of which 
have haploid numbers of n = 10, 9, 8, 7, 6, and 
5, proceeded from a basic chromosome number 
of x = 10 to a derived x = 5 by aneuploid de- 
crease. Representatives of the three primitive 
subgenera of Moraea, M. ciliata (subgenus Mo- 
raea), M. inconspicua (subgenus Visciramosa), 
and M. anomala (subgenus Monocephalae), all 
x = 10, have genome sizes of 22 to 23 pg. Species 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


of the derived subgenus Vieusseuxia, all x = 6, 
have genomes ranging from 23.4 pg in M. bi- 
partita to 33.1 in M. atropunctata and 36.4 pg 
in M. calcicola. Two tetraploid species of Mo- 
raea, M. villosa, and M. tulbaghensis, have ge- 
nomes of 72.4 pg of DNA, a value remarkably 
close to twice the 36.4 pg value obtained for the 
nearly allied M. calcicola. 

There is some evidence in Moraea subgenus 
Vieusseuxia of the C-value paradox (Walbot & 
Goldberg, 1979). Related species of the same 
subgenus and section, and with similar karyo- 


L + 


Des 
(Table 2). The difference between the genome 
size of M. unguiculata and either M. atropunc- 
tata or M. calcicola is of the order of 5096. In 
genera allied to Moraea such as Homeria this 
paradox is also evident. In Homeria, most species 
of which have a basic x — 6 and very similar 
karyotype, H. pendula has a genome size of 22.5 
pg, while H. bifida has 29.2 pg and the tetraploid 
Н. flaccida, 41.2 pg. Sessilistigma, an unde- 
scribed monotypic genus closely related to Ho- 
тета, has a genome size of 31.6 pg, а figure 
consistent with the range found here in Нотепа. 

Hexaglottis, a genus also probably allied to 
Homeria has a genome size of 20.6 pg. This 15 
low in comparison with Homeria but consistent 
with cytological observations which indicate 4 
chromosome complement very similar, but 
slightly smaller than in Homeria. In examples of 
two other genera of Iridoideae, Gynandriris has 
a genome size of 24.1 pg, and Roggeveldia has 
16.5 pg. Of the species studied here, these two 
genera are probably most closely related to Mo- 
raea bipartita, the genome size of which is 23.4 
pg. The genome size data tend to support the 
hypothesis that there is a reasonably close те e 
tionship between M. bipartita and Gynandriris 
their genomes being very similar in size. Rf 
geveldia, which seems related to this ЁГОШР 
(Goldblatt, 1979), presumably has lost a sub- 
stantial amount of DNA in the course of its 690" 
lution if its relationships are, in fact, with thes? 
species. ; 

Of the two New World taxa examined, $15" 
rinchium convolutum (an octoploid with ? ^ 36) 
has a genome size of 10.9 pg and Cipura paludosa 
(a tetraploid form with п = 14) has 19.5 pg. Basi 
genome size in Sisyrinchium would accorers y 
be of the order of 2.7 pg. This is comparable with 
Ixioideae rather than with Iridoideae, tO which 
Sisyrinchium is usually allied. Cipura on the oth- 
er hand has a basic genome size of the order 9 


жайын — жы 


== 


— 


1984] GOLDBLATT ET AL.—GENOME SIZE IN IRIDACEAE 179 


ТАВІЕ 2. Mean genome size (C-value) for 30 species of Iridaceae with standard deviation (s.d.), haploid 
chromosome number (n) and basic chromosome number (x), arranged by subfamily. 


Species C-value s.d. n X 


SUBFAMILY I[RIDOIDEAE (Including SiSYRINCHIOIDEAE) 
OLD WORLD TAXA 


Tris histrio L. 65.1 +1.6 10 10 
Dietes grandiflora N. E. Br. 13.5 0.2 10 10 
Galaxia fugacissima (L. f.) Druce 6.4 0.8 9 9 
Moraea anomala Lewis 22.0 L3 10 10 
nconspicua Goldbl 23.0 3 10 10 
M. ciliata (L. f.) К 247 0.9 10 10 
M. fugax (de la Roche) Jacq. 
population 1 19.9 12 6 10 
population 2 19.9 07 6 10 
M. atropunctata Goldbl. 33.1 1.9 6 6 
M. calcicola Goldbl. 36.4 2.5 6 6 
M. tulbaghensis L. Bol. 72.4 3.4 12 6 
M. villosa (Ker) Ker 72.4 3 12 6 
М. unguiculata Ker 26.2 3.4 6 6 
M. bipartita L. Bol. 23.4 0.6 6 6 
Gynandriris setifolia (L. f.) Foster 24.1 L? 6 6 
Roggeveldia fistulosa Goldbl. 16.5 0.3 6 6 
Hexaglottis namaquana Goldbl. ined. 20.6 0.7 6 6 
Homeria bifida L. Bo 29.2 7 6 6 
Н. pendula Goldbl 22.5 1.6 6 6 
H. flaccida Sweet 41.2 2.5 12 6 
Sessilistigma radians Goldbl. ined. 31.6 1.9 6 6 
New WoRLD TAXA 
Cipura paludosa Aubl. 19.5 1.4 14 7 
Sisyrinchium convolutum Nocca 10.9 0.6 36 9 
SUBFAMILY IXIOIDEAE 
Anomatheca viridis (Ait.) Goldbl. 1.9 0.9 11 11 
Freesia alba (G. L. Meyer) Gumbleton 13 0.3 11 11 
Watsonia brevifolia Ker 1.6 0.5 9 9 
Pillansia templemanii L. Bol. 5.4 23 20 10 
Lapeirousia verecunda Goldbl. 4.9 0.5 8 10 
Gladiolus virescens Thunb. 3.2 0.3 15 15 
Hesperantha bachmannii Baker 1.1 0.3 13 13 
Babiana virginea Goldbl. _ = - 


are, with minor exceptions, long lived, geophytic 
perennials so that differences in life cycle (Ben- 
nett, 1972) cannot be used to explain genome 
size differences. In particular, the Old World taxa 


= much larger than Sisyrinchium, and a 
Sis псе clearly reflected in the karyology 
u blatt, 1981). The genome size accords well 

the Old World Iridoideae, although it is 


Oo the small side for the subfamily, 
there 15 no doubt that Cipura is a member 

of Iridoideae. 
Tad Teasons for the often large differences in 
* size among genera and species of Iri- 
are obscure. All members of the family 


studied here all have a similar life cycle and sim- 
ilar environmental and edaphic requirements. 
The reasons for the primary difference in the 
genome size between Iridoideae and Ixioideae 
thus appear rooted in the evolutionary history 
of these subfamilies. The secondary differences 


180 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


within Iridoideae, between closely allied genera 
and within genera, apart from polyploidy, are 
qually difficult to explain and we can offer no 
reasonable explanation for the genomic differ- 
ences in the taxa studied here. It is clear that if 
the primitive genus Dietes (Goldblatt, 1981) is 
regarded as having close to the basic genome for 
Iridoideae, then trends for both a decrease (in 
Galaxia) or an increase (in Moraea, Homeria, 
etc.) in genome size have taken place during the 
evolution of the subfamily. 


LITERATURE CITED 


ВАЕТКЕ, K. P., А. H. SPARROW, С. H. NAUMANN « S. 
5. SCHWEMMER. 1967. The а чз of DNA 
content to nuclear and chromosome volumes and 
to radiosensitivity (LD;,). Proc. Natl. Acad. U.S.A. 
58: 533-540. 

BENNETT, M. D. 1972. Nuclear DNA content and 
minimum generation time in herbaceous plants. 
Proc. Roy. Soc. London, Ser. n 181: 109-135. 

& J. B. SurrH. 1976. Nuclear DNA amounts 

in Angiosperms. Philos. S ns Ser. B, 274: 227- 

74. 


bassi si 1971. Cytological and ерин an 
tudies in the Southern African Iridaceae 
pense вы 37: 317-460. 


1976. Evolution, Марси, + and subgeneric 
classification in Mora “inti Ann. Mis- 
ouri Bot. Gard. 63: 1-2 


——.. 1979. A e is a new genus of southern 
African Iridaceae. Ann. Missouri Bot. Gard. 66: 
839-844 

. Redefinition of Homeria and Moraea 

(Iridaceae) i in the light of biosystematic data, with 

heome gen. nov. Bot. Not. 133: 85-95. 

981. Systematics, phylogeny and evolution 

of Dietes (Iridaceae). Ann. Missouri Bot. Gard. 

68: 132-153. 

1982. Chromosome cytology in relation to 

suprageneric systematics of Neotropical Iridaceae. 

Syst. Bot. 7: 186-198. 

„5; 


ALBOT. 1980. The genome of Zea 

mays, its ‘organization and homology to related 
sses. Chromosoma (Berlin) 79: 251-270. 

шде ме A. H., В. C. SPARROW, К. Н. THOMPSON & 

A. ScHAIRER. 1965. The use of nuclear and 

ap BOE variables in determining and pre- 

dicting radiosensitivities. In The Use of Induced 

Mutations in Plant Breeding. Radiat. Bot. Suppl. 


5: 101-132. 

WaLBOT, V. & R. GOLDBERG. 1979. Plant genome 
organization and its relationship to classical ир 
genetics. Рр. 3-40 їп Т. С. Hall & J. W. Da 
ae اا‎ bres Acids in Plants. CRC Press Hes т 


= _ 


—— ===> — —— 
—M y © ч 


A SURVEY OF SEED SURFACE MORPHOLOGY IN 
HESPERANTHA (IRIDACEAE)! 


WARREN L. WAGNER? AND PETER GOLDBLATT? 


LI L 


ABSTRACT 


4 К, uM DOME уз 4 2 1 


Seeds ofa range of i 


= 


(SEM) and compared with three species of the most closely related genus, Geissorhiza. A turbinate to 
globose shape with a persistent funicle and a testa of uncontorted epidermal cells with smooth surfaces 
is apparently the basic seed type. Modifications of the basic type include increasing compression and 
а triangular or more or less irregular shape, sometimes accompanied by wrinkling and crumpling of 
the epidermal cells, and the development of dual tails and wings. This is most marked within Hes- 


perantha sect. Radiata (but not H. marlothii of the section), wh р 
b ing-like structures are also developed within sections Hesperantha (H. 


reduction in seed siz 


8 k 
Spicata and H. cedarmontana) and Concentrica (H. fib 


+h 


| 
rosa) but in both of these groups without 


accompanying crumpling of the epidermal cells, which coincidentally have developed rough surfaces. 


Hesperantha Ker is a genus of some 55 species 
of corm bearing perennials of Iridaceae subfam- 
ily Ixioideae. It is centered in Southern Africa, 
but а few species occur in the montane areas of 
tropical Africa, extending as far north as Cam- 
eroon and Ethiopia. The genus has recently been 
revised for the winter rainfall area of South Af- 
пса by Goldblatt (1982, 1984) and is being stud- 
led in eastern Southern Africa by Hilliard and 
Burtt (1979, 1982). This study of seed mor- 
phology in Hesperantha was made in conjunc- 
tion with the revisionary work, now completed 
Or In progress. 

Seed morphology of Iridaceae is in general 
poorly known and thus seldom has been of taxo- 
попис value below the generic level. Differences 
он between genera are, however, sometimes 
dm g and may provide important generic 
ü Cteristics. Good examples are the circum- 

rentially winged seeds of Gladiolus and its close 
н "es the two winged seeds of Watsonia, and the 
dd S^ seeds with spongy testa of Tritoniopsis 
i al This study was thus undertaken 
поли оре that some characteristics of taxo- 

.- use would be found in Hesperantha at 

H d generic level. Seventeen species of 
€sperantha, including examples from all four 
sections (Goldblatt, 1982), as well as three species 


А. 


of the related genus Geissorhiza Ker were assem- 
bled for light and scanning electron microscope 
examination. This represents a large sample for 
a monocot genus such as Hesperantha, in which 
seeds are typically produced after flowering and 
are seldom collected and consequently poorly 
kn 


Seeds of Hesperantha have not previously been 
studied in detail, but SEM studies of seed mor- 
phology have been made in a few other genera 
of subfamily Ixioideae, in conjunction with the 
systematics notably in Syringodea (de Vos, 1974) 

i ocus (Baytop et al., 1975; Mathew, 
1976). In Crocus some interesting seed surface 
features including trichomes and papillae have 
been found to be of taxonomic significance. In 
systematic studies of other genera of Ixioideae, 
seed morphology is occasionally of limited taxo- 
nomic use, as in Tritonia (de Vos, 1982: 113) 
where one or two species stand out from their 
allies in having unusual seed modifications. 

The extensive study of Huber (1969) on the 
seed morphology of the monocotyledons deals 
largely with internal seed structure, and not at 
all with detailed surface microstructure such as 
is observed with the SEM. His observations on 
Hesperantha are very general and relate primar- 
ily to tribal and familial classification. 


1 в 
çj, iS research was supported by Grant DEB 78-10655 and DEB 81-19292 from the United States National 
es +“ Foundation. We thank Mike Veith, Washington University, St. Louis, for his assistance in the SEM 


1n: 
s в дор Museum, P.O. Box 19000-A, Honolulu, Hawai'i 96817. hie 
‚ A. Krukoff Curator of African Botany, Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 


63166. 


ANN. Missouri Bor. Garp. 71: 181-190. 1984. 


182 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


MATERIALS AND METHODS 


The seeds of 16 species of Hesperantha (about 
a third of the genus) were examined by scanning 
electron microscopy (SEM). Sufficient viable 
seeds were studied to document the variation 
present within each population. Four to ten seeds 
were generally adequate. Three additional species 
of the closely related genus Geissorhiza were also 
examined as out-groups in the hope that this 
would aid in the establishment of character po- 
larity (Table 1). One population only of all species 
except H. marlothii was examined with the SEM. 
The variation in seed size in H. marlothii was 
such that two populati tudied, covering 
the extremes encountered in the species. Samples 
of several populations of H. falcata and H. ra- 
diata were also examined under the light micro- 
scope to determine whether material studied was 
typical of the species. In all cases they matched 
closely the samples studied. One more species, 
H. pauciflora (sect. Hesperantha) was also ex- 
amined under the light microscope and since it 
had seeds exactly like those of H. falcata (also 
sect. Hesperantha), it was not examined further. 


Гы 1 


The number of pop may ap- 
pear to be too small to gauge the variation within 
species but as indicated in the introduction, seed 
samples are difficult to obtain in Hesperantha in 
which plants are seldom collected in fruit. The 
material studied here therefore represents an un- 
usually large assemblage. Where more than one 
population was available, as in H. falcata and 
H. radiata, the seed was examined with the light 
microscope and found to match the seed of the 
population studied with the SEM. Thus as far as 
it is possible to estimate, the single populations 

tudied apr tot p tati the species. 
Several of the species examined (H. elsiae, H. 
purpurea, H. brevifolia, H. cedarmontana) are 
known from one or very few populations and are 
so restricted in their distributions that the ma- 
terial studied here represents a good sampling of 
the species. Among the widespread species, sev- 
eral populations were checked in H. falcata and 
H. radiata while only single samples were avail- 
able in H. bachmannii and H. pilosa. 

Viable seeds were attached with water soluble 
white glue to aluminum stubs, coated with 500— 
700 À of gold in a sputter coater, and examined 
in a Hitachi S-450 SEM at 15 kV and 60-80 pA. 
Photomicrographs were made with Type 55 P/N 
Polaroid film. Contact prints were made on Ill- 
ford No. 2 paper. Surface features are presented 


at two magnitudes of magnification: 35x-90x 
to show overall seed shape and surface topog- 
raphy, and 1,000 x to resolve the microsculpture 
of the epidermal cell surface. 


DESCRIPTION OF SEED FEATURES 


The variation in the seeds of Hesperantha 
species is often limited to relatively minor mod- 
ifications that produce large differences in seed 
shape, sometimes even within one capsule. There 
are, however, certain patterns of variation that 
appear, at least from the small ples available, 
to be characteristic of particular species. The 
variation within Hesperantha as well as that found 
in a sample of three species of the closely related 
genus Geissorhiza is presented in Figures 1-29. 
Only 13 of the 16 species of Hesperantha ex- 
amined are illustrated. The additional species 
studied add no significant inf tion to the ob- 
served pattern of variation. The variation is de- 
scribed in the following pages in sections dealing 
with shape, size, color, surface morphology, and 
microsculpturing. 


Shape. The basic shape of Hesperantha seeds 
is turbinate to turbinate-globose. The embryo 
containing portion is globose to ovoid and this 
is modified to a turbinate shape by the persistent 
funiculus present on the seeds of many of the 
species (e.g., Figs. 1, 3, 5, 8). The same basic 
shape is evident in Geissorhiza (Figs. 16. 17). 
The more regular globose shape, illustrated here 
by H. erecta (sect. Concentrica) and H. falcata 
and Н. luticola (both sect. Hesperantha) (Figs 
1, 5, 8), occurs in species of all sections of Hes- 
perantha except sect. Radiata, as well as in Gels 


sorhiza (G. humilis). The seed is more abruptly | 


constricted to the persistent funiculus in thes | 


species. і 
The basic turbinate to globose shape 15 тоў 
ified in a number of the species. The т 


tions can be grouped into three different YP | 


| 


An irregularly wrinkled surface occurs in several | 


species of Hesperantha distributed in several sec 
tions (e.g., H. bachmannii, Fig. 4; Н. muiri, PE 
13) and in Geissorhiza burchellii (Fig. 18). 
In contrast, seeds with irregular shaP® 
strongly wrinkled or crumpled surface COUE 
with the presence of two tails (one is the e 
lus), and/or longitudinal wings characterize 07 
of the five species of sect. Radiata; Н. ТШ > 
elsiae (Fig. 14), H. radiata (Fig. 11), and H. ње 
folia (Fig. 12). The latter species appears " 
the most specialized in this respect. These " 


| 


a 


1984] WAGNER & GOLDBLATT —НЕЗРЕКАМТНА 183 


TABLE 1. 
Hesperantha are 


Voucher information for the species of Hesperantha and Geissorhiza studied here. Species of 
arranged taxonomically according to the sectional classification proposed by Goldblatt (1982). 


All collections are from the Cape Province, South Africa. 


Species 


Collection Data 


H. erecta (Bak.) Benth. ex Bak. 
H. fibrosa Bak. 


H. flexuosa Klatt 
H. montigena Goldbl. 
Н. pilosa (L. f.) Ker 


H. bachmannii Bak. 
H. purpurea Goldbl. 


H. brevifolia Goldbl. 
H. elsiae Goldbl. 
H. marlothii Foster 


H. тити (L. Bol.) Lewis 
H. radiata (Jacq.) Ker 


Н. falcata (L. f.) Ker 

H. cedarmontana Goldbl. 
H. pauciflora Lewis 

Н. luticola Goldbl. 


Н. spicata subsp. inifoli 

die р. graminifolia (Sweet) 
G. burchellii Foster 
G. humilis (Thunb.) Ker 


G. heterostyla L. Bol. 


Hesperant 

ect. Concentrica 
Saldanha distr., Donkergat, Posberg, Goldblatt 4095 (MO). 
Commonage 8 of Caledon, Goldblatt 5899 (MO). 
Wildepaardehoek Pass, Goldblatt 5755 (MO). 
Worcester distr., Mt. Brodie, Esterhuysen 35307 (MO). 

Caledon Zwartberg, Goldblatt s.n., no voucher. 


Sect. Imbricata 
N of Hankey, Goldblatt 4937 (MO). 
Perdekraal, Calvinia distr., Goldblatt 6246 (MO). 


Sect. Radiata 

Piketberg, Zebrakop, Esterhuysen 35320 (MO). 

Cedarberg, top of Krom River Kloof, Goldblatt 5331 (MO). 

Culvinis -Middelpos Rd. near Blomfontein, Goldblatt 5813 
(MO)-— population 1; Nieuwoudtville escarpment, 
Goldblatt 58354 (MO)— population 2. 

Hills W of Riversdale, Goldblatt 5437 (MO). 

N end of Cold Bokkeveld, Goldblatt 5343 (MO). 


Sect. Hesperantha 
Bulshoek, Olifants R. Valley, Goldblatt s.n., no voucher. 
Cedarberg, Middelberg Plateau, Goldblatt 51 5 "ан 
Kamiesberg, Welkom, Goldblatt s.n., no vou 
Calvinia—Middelpos Rd. near Blomfontein, саб 8 5814 
(МО). 
Саре Peninsula, near Саре Pt. Reserve, Goldblatt 5263 


Geissorhiza 
Langeberg near Swellendam, Esterhuysen 35604 (MO). 
Cape Peninsula, near Cape Pt. Reserve, Goldblatt 5263 


(MO). 
Near Humansdorp, Goldblatt 6211 (MO). 


tures are nant 


di the genus. They 
not, however, characterize all species of sect. 
pulation 2 of Hesperantha marlothii 


Radiata. Po 


Finally, Hesperantha fibrosa (sect. Concentri- 
ca) (Fig. 2) and two species of sect. Hesperantha, 
H. spicata (Fig. 6) and H. cedarmontana diee 


(Fig. 5) has the generalized turbinate shaped seed 7), have ds witk 


that is ch 


abl 


lation and is 
of 


aracteristic of the genus while the other 
ноо of Н. marlothii studied has seed of a 
У Pyramidal shape (Fig. 10). This is Е 
ly linked to the large seed size in this 
presumably caused by the on е 
Seed packing in the capsules. Dual tails and 


narrow longitudinal and apical wings and little 
or no contortion of the epidermal cells. 

At the distal end of the raphe of many species 
of Hesperantha there is a porelike depression of 
the testa (Figs. 1, 3, 5). This is sometimes less 
conspicuous as in Н. marlothii (Fig. 9) or very 


e not always present on all seeds ex- 
micas (e.g., Н. elsiae, Figs. 14, 15), but at least 
Ani seeds in each sample have these features. 
n, this lack of n is presumably due 

t0 the effects of seed packin 


prominent as in H. luticola (Fig. 8). Several 
species have a broader depression at the distal 
end (Figs. 2, 4, 11, 13, 14) or the seeds are merely 
truncate (Figs. 6, 7, 10) 

The raphe is often conspicuous and appears as 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


к. » 
~ 


> 
~ 
A 


T 
-— 
e 
> 


" vn Da 
поља ДИУ 


, 4, sect. Imbricata; 5, 
manr 


FIGURES 1-6. Scanning electron micrographs of seeds of Hes 


ntrica, 
perantha species (Figs. 1, 2, sect. С ae pen 
sect. Hesperantha).—1. H. erecta.—2. H. fibrosa. —3. Н. purpurea. —^- 
1ї.— 5. Н. falcata.—6. Н. spicata. White bar = 100 um. 


h 


WAGNER & GOLDBLATT—HESPERANTHA 


А 


Z 
= 4 
— n n 
E : 


* 


Чу Ф, 


(= 


erigi. 


9 PIGURES 7-12. Scanningelectron micrographs of seeds of species of Hesperantha (Figs. 7, 8, sect. Hesperantha; 
-12, sect, Radiata).—7. Н. cedarmontana. —8. Н. luticola.—9. Н. marlothii (population 1).— 10. H. marlothii 


Population 2). — 11. Н. radiata.—12. H. brevifolia. White bar = 100 um. 


Radiata and 
100 pm 


.— 17,18. С. burchellii. White bar = 


=> 


4 p ^ ~ 


Де ~ У Tay 


of Hesperantha sections 


pecies 


5 


7 | @: i 


Зе: 


NSS 
ANS 


Q 
Û 


tron micrographs of seeds of 
,15. H. elsiae.—16. G. humilis 


Z 
ры 
а 
са 
< 
Q 
- 
< 
= 
2. 
< 
= 
О 
22 
z 
- 
o 
un 
2 
= 
E 
т 
E 
Еа 
о 
uv 
d 
< 
Z 
Z 
< 


Scanning elec 


а.— 13. Н. muirii.—14 


FIGURES 13-18. 


Geissorhi 


WAGNER & GOLDBLATT—HESPERANTHA 


E. IGURES 19—24. Sca 
Whig Geissorhiza. — n H. erecta.—20. H. purpurea.—21,22. H. radiata.—23. G. heterostyla.—24. G. humilis. 
te bar = 10 um. Scale ‘ane рч all Figures. 


usd сетов micrographs of epidermal cell surfaces of seeds of species of Hesperantha 


188 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


| ' | ran- 
D 25-29. Scanning electron micrographs of epidermal cell surfaces of seeds of species of He M | 
— 25. H. cedarmontana.—26. H. spicata.—27. H. luticola.—28. H. brevifolia. —29. Н. elsiae. 


10 um. 


a flat or raised area of the testa where the epi- 
dermal cells are elongated along the longitudinal 
axis of the seed (e.g., Figs. 1, 3, 6, 7). The species 
of Geissorhiza sampled have seeds with similar 
raphe and distal depressions (Figs. 16, 18). 


Size. Most species of Hesperantha have rel- 
atively small seeds typically from 0.8 to 1.5 mm 
long. The seeds of Geissorhiza species examined 
also have a similar size range. Four species, H. 
montigena (sect. Concentrica), H. bachmannii 
(sect. Imbricata), H. marlothii (sect. Radiata) (Fig. 
10), and Н. luticola (sect. Hesperantha) (Fig. 8), 
have larger seeds, ranging from 1.3 to 2 mm long 


or to 2.5 mm long in one of the two popula 
of H. marlothii studied (population 1). 18 m 
trast, three species of sect. Radiata, H. We 
(Fig. 12), H. muirii (Fig. 13), and H. eda iT 
14, 15), guid particularly small seeds, 0 

0.8) mm I 


Color. 


The seeds of both Hesperantha 3 | | 
are light to dark brown except each 
of Н. flexuosa, Н. radiata, and Н. luticola, ) 
in а different section, which are reddish Wi | 

The seeds of most species аге moderately Н. 
trous but some are much more so, such i | 
bachmannii (sect. Imbricata) and Н. таг 


нь == 2“ 


1984] 


(population 1) (sect. Radiata). Seeds of G. het- 
erostyla are similarly lustrous. Only H. fibrosa 
of sect. Concentrica and H. luticola of sect. Hes- 
perantha have an unusually dull seed coat sur- 
face. The whitish color with a brown background 
of the seeds of H. spicata is a unique feature 
among the species sampled. 


Surface morphology. The seed surfaces of 
both Hesperantha seeds and of those species of 
Geissorhiza sampled are composed of variable 
shaped epidermal cells (Figs. 19-29). Most cells 
are more or less isodiametric, but on ridges, wings, 
or contorted areas, the cell shape is usually al- 
tered (e.g., Fig. 20). The exposed periclinal cell 
wall is typically flat (Fig. 19) to slightly convex 
(Fig. 23). They are also often modified over parts 
of the seed surface to undulate (Fig. 21), convex 
(Fig. 22), irregular (Figs. 28, 29), or more spher- 
ical (Fig. 27). These modifications are either 
unıque to one species such as the more spherical 
cells of H. luticola or are distributed sporadically 
In several sections, such as the three other types 
mentioned. The epidermal cell boundaries are 

stinct and fairly uniform among species of Hes- 
ретатћа (Figs. 19, 21, 22, 25, 26) and appear 
similar to those of Geissorhiza (Figs. 23, 24). The 
boun ries are occasionally obscured by por- 
tions of the exposed periclinal walls that overlap 
(Fig. 20). Sometimes the boundaries are in full 
view but are not conspicuous (Figs. 28, 29). All 
three of these modifications appear to be minor 
and may be linked to the wrinkling or contortion 
of the testa surface as a result of packaging or 
desiccation, 


Micr osculpturing. The surface of the epider- 
mal cells is generally smooth in both the Hes- 
Perantha 3 гл sy FEM js 

5 SP Vey 

inei Geissorhiza humilis, has an irregularly 
Pis ened surface. Within Hesperantha there are 
( Species with roughened surfaces, Н. fibrosa 
dios Concentrica), H. cedarmontana, and H. 
These. (both sect. Hesperantha) (Figs. 25, 26). 
EL vend surfaces in Hesperantha are 
i one another but different from that of 
"gus iza humilis (Fig. 24). The similarity of 
ae pened surfaces of these three Hesper- 
a Suggests the possibility of a close 
pirani re а among them. Other species of Hes- 
(Fig. 29) hg irregularly wrinkled cell surfaces 
oa. his type of surface is closely linked 
"AL intortion of the surface or portions of the 
Speciali In many species (e.g., Fig. 4). The very 

ized seeds of Н. brevifolia have a wrinkled 


о 


A 
UNE. 


WAGNER & GOLDBLATT—HESPERANTHA 


189 


cell surface unique among the species examined 
(Fig. 28). 


DISCUSSION 


The basic seed shape in Hesperantha seems to 
be turbinate to more or less globose with a per- 
sistent funiculus and an epidermis of isodiamet- 
ric cells with unwrinkled surfaces. A more glo- 
bose shape may be due to either looser packing 
of the seeds in the capsule or a relatively simple 
modification that has occured several times in- 
dependently. In any case this variation appar- 
ently has nothing to contribute to our under- 
standing of species relationships. 

There appear to be no seed characters restrict- 
ed to Hesperantha and none have been identifed 
that differentiate Hesperantha from Geissorhiza. 
Seeds of certain species such as H. marlothii 
(population 2) are virtually indistinguishable fi 
those of some species of Geissorhiza. Moreover, 
there is limited variation among species of Hes- 
perantha. The most conspicuous variations, like 
contorted and wrinkled seed coats, appear to be 
relatively minor changes and may be a conse- 
quence of the density of seed packing in the cap- 
sules or to desiccation or a combination of the 


two. 

Wrinkled seed coats and globose seed shape 
have a sporadic distribution in the various sec- 
tions of Hesperantha as well as in Geissorhiza, 
in the case of wrinkled seed coats, and they pre- 
sumably have no taxonomic utility. Modifica- 

1 d 


e 41 


tions that pp y y reproduced 
(as far as it is possible to judge from the sam- 
pling), such as triangular seeds in H. marlothii 
(population 1), oddly wrinkled surfaces of the 
epidermal cells of H. brevifolia, or the more 
spherical epidermal cells and large seeds of H. 
luticola, appear restricted to only one species or 
form, and thus are also not useful in determining 
species relationships. The only exception to this 
is in sect. Radiata, where seeds with irregular 
shapes, strongly wrinkled or crumpled surfaces, 
a tendency for small size, and dual tails and/or 
wings support the belief in the close relationship 
of H. radiata, H. muirii, H. brevifolia, and H. 
elsiae based on gross morphology. Hesperantha 
juncifolia and H. longicollis, the other species of 
the section, were not available for study, while 
H. marlothii, evidently closely allied to H. ra- 
diata (Goldblatt, 1984), does not have this dis- 
tinctive seed type. 

The similarity between the seeds of H. fibrosa 
(sect. Concentrica) and H. cedarmontana and H. 


190 


spicata (sect. Hesperantha), all of which have 
seeds with narrow wings, little or no contortion 
of the epidermal cells, and roughened cell sur- 
faces, in contrast seems fortuitous as there seems 
to be no support from gross morphology to sug- 
gest that H. fibrosa may be allied to the species 
of sect. Hesperantha with these same character- 
istics. 

From the relatively small sample of 17 species 
examined here, it appears that the main pattern 
of evolution in seed structure in Hesperantha has 
been one of change from a basic turbinate shape 
with uncontorted, smooth surfaced epidermal 
cells to increasing compression anda triangular 


у angular | 
a result of dense “packing within the сарае 
sometimes асана! ty ИЕ and crum- 
pling of the ep 
of dual tails and wings. ae is most EE 
within sect. Radiata (but not in H. marlothii of 
this section), where these modifications are ac- 
companied by reduction in seed size. However, 
narrow wings are also developed within sections 
Hesperantha (H. spicata and H. cedarmontana) 
and Concentrica (only in H. fibrosa of the species 
examined) but in both of these groups without 
accompanying crumpling of the epidermal cells, 
hich have distinctive rough surfaces, appar- 
ently developed coincidentally. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


LITERATURE CITED 
BAYTOP, T., B. MATHEW & C. BRIGHTON. 1975. Four 
new taxa in Turkish Crocus. Kew Bull. 30: 241- 
De Vos, M. Р. 1974. Die Suid Afrikaanse genus Sy- 
ringodea. J. S. African Bot. 40: 201-254. 


—— ——. 1982. The African genus Tritonia Ker-Gaw- 


"d | reor Part 1. J. S. African Bot. 48: 105- 


ES Е. С. 1948. Studies in Iridaceae У. Some 

new or noteworthy species of Hesperantha. Contr. 
y Herb. 166: 3-27. 

К кыы Р ДОТ Cytological and morphological 
studies in the Southern ican Iridaceae. J. S. 
African Bot. 37: 317—460 

82. _Corm morphology in Hesperantha (Iri 

daceae, I 

onomy. Ann. Missouri Bot. Gard. 69: - 370-378. 

4. A revision of Hesperantha (Iridaceae) 

er rainfall area of Southern Africa. J. 


HILLIARD, O. BURTT. 1979. Notes on 
some DUE of southern Africa chiefly from Natal: 
VIII. Notes Roy. Bot. Gard. Edinburgh 37: 284- 
325. 


ws 
Г 


1982. Notes on some plants of 
southern Africa chiefly from Natal: IX. Notes Roy. 


Samenmerkmale und Ver- 

ne оао dE der Liliifloren. Mitt. Bot. 
Munchen 8: 219—538. 

MATHEW, B. 1976. Crocus olivieri and its allies (Iri- 
daceae). Kew Bull. 31: 201-208. 


| 
| 


A FLORISTIC STUDY OF VOLCAN МОМВАСНО 
DEPARTMENT OF GRANADA, NICARAGUA! 


JOHN T. ATWOOD? 


ABSTRACT 


Volcan Mombacho is a moderate sized (1,345 m elev.), quiescent volcano with one of two cloud 
forests in southwestern Nicaragua. Of 457 species listed, 80 are pteridophytes and 87 are orchids. The 
species richness of these groups may be accounted for by their high fecundity e e Dh This 
study has revealed only one endemic species. Since Mombacho is the apparent rn range limit 
of several orchid species, it is suggested that the flora of the cloud forest has most its affinities with 
Costa Rica. The lack of several wide ranging species on Mombacho which are known only as far south 
as northern Nicaragua further supports this contention. As with most of tropical America, the cloud 


forests of Mombacho are threatened by exploitation of their natural resources 


Volcán Mombacho (Fig. 1) is a quiescent, much 
eroded, and well vegetated volcano located near 
the city of Granada, Nicaragua. *Mombacho" is 
a modification of the Nahuatl Se 
meaning “inclined mountain” (Mantica, 1973). 
It is located at 11°50'N latitude, rae "W lon- 
gitude (see map, Fig. 2), and is the fifth largest 
ofthe quaternary volcanos in western Nicaragua 
forming a chain from El Salvador to Costa Rica 
(Mooser et al., 1958). With a maximum eleva- 
tion of 1,345 m, Mombacho is somewhat lower 
than several other Nicaraguan volcanos, the 
highest of which is 1,745 m. It i is, however, per- 
haps the most massive with a basal diameter of 
about 7 km. Its U-shaped crater rim is 1.5 
М diameter and the crater floor is about 750 т 
Ower than the highest peak. The lowest point on 

€ crater rim is 1,080 m 
E ona the highest NR ofthe southeast crater 
di еге is a second peak on the northwest rim 

an elevation of 1,222 m. Adjacent to this 
one ad ge flat area appropriately called “Plan 
Ke Ж: Within this area are two small 
О we each of unknown depth and 
ái m in diameter. Eastward from Plan 
as Flores lies a trough-shaped valley over 1.5 
di =“ extending xls from the crater 
га distance of 3.5 k 


Em. PM 


Aerial photographs reveal a number of lava 
flows extending down the sides of Mombacho, 
but these features have been obscured in the 
northeast valley and the open south side of the 
crater rim by later seismic events. The lava flows 
are for the most part fully vegetated, and their 
basal limits are sharply defined where they meet 
pastured savannas. 

Certain areas, notably the flanks of the crater 
rim and the sides of the valley extending north- 
eastward, are precipitous. These areas, often with 
a slope well over 100 percent, are mostly vege- 
tated, but frequent landslides have left conspic- 
uous scars and a jagged crater rim 

Very few permanent streams can ihe found on 
Mombacho, although stream beds occur in var- 
ious ravines filled only during times of heavy 
precipitation. Most of the precipitation seeps 
down through the loose volcanic substrate, leav- 
ing little runoff. Because of the porous substrate, 
the two craters at Plan de las Flores do not con- 
tain lakes. 

Viewed from Granada, Mombacho appears as 
arich green, broadly truncated, and much eroded 
volcanic cone. It is most impressive in cloudless 
late afternoons, when the various physical fea- 
tures cast shadows pointing up the rough topog- 
raphy. A number of cut-over areas mar the slopes 


"1 wish to thank J. Incer B., C. Gutierrez H., and Universidad Centroamericana for laboratory and field 
F. С. Seym 


S . 
late н in 1976 under 


5 
па - Thanks are also extended to D. A. Neill for assistance in field work, 
and use of his herbarium. For various determinations gratitude is extended to the Ало J. H. 


and to our for his 


an. 
у Botanical Gardens, 811 South Palm Avenue, Sarasota, Florida 33577. 
ANN. 
Missouri Bot. GARD. 71: 191-209. 1984. 


192 


FiGURE 1. 


and much of the lower areas have been defor- 
ested or severely disturbed. 

Everywhere in the tropics the mountain forests 
are disappearing at alarming rates. It is hoped 
that interest in the flora of this mountain will 
help bring an awareness by government officials 
that the development of the Nicaraguan cloud 
forests is not in their best interests. 

Volcan Mombacho was selected partly be- 
Cause it contains a substantial amount of extant 
virgin forest and, because being close to urban 
areas, it has educational, recreational, and eco- 
nomic potential. For these reasons it seemed that 
a survey of the flora of this volcano would be a 
greater contribution than a similar work on a 
more remote mountain. Collections made spe- 
cifically for this work were made during the 
months of May through July 1975 and February 
and March 1977. The most complete set of 
voucher specimens has been deposited in the 
Beal-Darlington Herbarium of Michigan State 
University. 


GEOLOGICAL History 


Mombacho’s violent past is reflected in the 
size of the crater and the general topography. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


Profile view of Mombacho from the north. 


Little is known of its geological history, but û 
few seismic events have been documented since 
the time of the Spanish conquest. ; 
As a member of the west Nicaraguan volcanic 
chain Mombacho is probably not older than two 
million years and may be considerably younger. 
Mooser et al. (1958) reported that the most г 
cent authenticated eruption occurred in 1560, 
but this report is not supported by Incer (pts 
comm.). Incer (1973) indicated that during the 
same century the south crater rim avalanch | 
away, causing the destruction of the south flan 
and an Indian village of 400 inhabitants. Craw- 
ford (1902) reported that an eruption oS ed 
in 1850, but Mooser et al. (1958) also шас 
that a small parasitic cone called “Pilas” form i 
on the north flank of Mombacho in 1850, bu 
this reportis probably confused with the g 
the same name. However, a small cone no 
of Mombacho may have been active in h 
times. ests 
The uniform texture of the crater walls d 
that in its early development Mombacho ps 
built up primarily from ash rather than lava pr af 
The ash probably formed a volcanic cone si™ 


istoric 


(Мог. 71 


~ — 


— 


- 


1984] 


ATWOOD— VOLCÁN MOMBACHO 


193 


в La Asuncion 005 


в 
La Trinidad 
Santa Teresa 


» 
of El Cacao 
o 


Las • 
Delicios 


Nisus: lava flows, which seem 
arty cover the surface of the mountain. 
A ^ not clear exactly how the crater was formed, 
ki. € Very steep sides suggest that an internal 
ы ти gecurred, caused by subsiding lava not 
a Xplosion similar to that which took place 
he toa. The two craters at Plan de las Flo- 

apparently were formed by collapse (Incer, 

Pers. comm.). 
Exactly which events took place in the six- 
= У Causing the destruction of the south 
tly lis not clear, but it is known that a 
Ad зм eme: within the crater (Incer, 1973). 
inate y the loose substrate collapsed under 
bii E and pressure from the crater lake, 
ere mate avalanche was probably precip- 
ably y an earthquake. A similar event prob- 
leaving д much earlier on the northeast flank, 
trough shaped valley. Since the six- 


P 2. MapofVolcán Mombacho (after Hoja 3051 III and Hoja 3051 IV published by Instituto Geografica 
000) 


cional and Servicio Geodesico Interamericano, 1972 edition, scale 1 : 50, : 


teenth century, Mombacho has remained rela- 
tively quiet, but the rough topography and fu- 
maroles of the crater rim attest to its violent past. 


CLIMATE 


The climate oflowland Pacific slope Nicaragua 
and the lower slopes of Volcán Mombacho may 
be described as “tropical dry." No single mean 
monthly temperature below 17.1°C has been de- 
termined at stations reported by Incer (1973). 
The widest range of variation of monthly means 
for any station is less than 4°C. However, Incer 
(1973) indicated that the daily temperature at 
Managua (with an annual mean of 26.3*C) may 
deviate at least 7.3?, because a temperature of 
19°C in January has been recorded. The tem- 
perature therefore fluctuates little throughout the 
year. After the rains cease in December a dry 
season ensues with essentially no rainfall in the 
lowlands until May. This period of drought 
roughly corresponds to the winter season of the 
north. Because rainfall is much more abundant, 
the climate of the summit is moister and cooler, 
with swift gusty winds as attested by frequent 
blow-downs. 


194 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


~ 
со 
T 


Temperature (C°) 


~ 
= 
т 


Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec 
Month 


FicuRE 3. Mean monthly temperatures at Nan- 
daime (data from Incer, 1973). 


No temperature data were available for Volcán 
Mombacho, but data were taken from the nearby 
village of Nandaime (Incer, 1973), which lies 12 
km southwest of the volcano at 150 m elevation 
(Fig. 3). To estimate the mean annual tempera- 
ture of Mombacho's summit (ca. 1,200 m elev.) 
the mean dry and wet adiabatic rates were ap- 
plied to the data from Nandaime. If the dry adi- 
abatic rate of 1°C per 100 m (Strahler, 1973) is 
applied to the mean annual temperature at Nan- 
daime (27.5°C), the mean annual temperature at 
the level of 1,200 m could be depressed 10.5? to 
a minimum 17°C. The wet adiabatic rate of 0.6°C 
per 100 m would depress the mean annual tem- 
perature 6.3°C to 21.2°C. Thus the calculated 
range of mean annual temperature falls between 
17°C and 21.2°C. To estimate the minimum tem- 
perature at 1,200 m the dry adiabatic rate can 
be applied to the minimum temperature at 
Managua (19°C at 50 m elev.). The estimated 
temperature difference between the two eleva- 
tions is 11.5°C, therefore the temperatures at 
Mombacho’s summit could drop to 7.5°C. Clear- 
ly, if frost ever occurs at the summit, it must be 
a rare event. 

The forests become increasingly wet with el- 
evation. Not only is there more convectional and 
orographic rainfall, but also the dense vegetation 
behaves as a screen, filtering moisture from pass- 
ing fog, as has been noted on other mountains 


(Oberlander, 1956; Twomey, 1957; Vogelmann 
et al., 1968; Vogelmann, 1973). Oberlander 

1956) noted that significant d ti 
only where trees are tall and fog-laden winds are 
strong. Baynton (1969) indicated that precipi- 
tation from fog in elfin forest vegetation at Pico 
del Oeste, Puerto Rico, comprised only ten per- 
cent of the total rainfall. This low percentage may 
reflect the shorter height of the vegetation and 
the subsequent lesser screening effect. Observa- 
tions o S weather ist with 
Baynton's more detailed considerations. Owing 
to the effects of nearby Lake Nicaragua, Volcán 
Mombacho probably receives more precipita- 
tion than do the volcanos to the north. 

Figure 4 is a graph ofthe monthly precipitation 
at La Asunción (580 m elev.), on the north flank 
of Mombacho. Clearly the dry season is evident 
from December to April. The rainy season from 
April to December includes two peak months, 
June and September, with а “mini” dry season 
in July. Although the mean monthly rainfall at 

ombacho's summit is undoubtedly higher, the 
shape of the rainfall curve is expected to have 
the same shape as the rainfall curve at La Asun- 


fM ү е 1 


ción. 

Rainfall undoubtedly varies locally with the 
slope. Clouds on the windward side move par- 
allel with the slope, but move vertically when 
approaching essentially vertical cliffs. With ver- 
tical air movement a corresponding higher local 
precipitation is expected. 

Figure 5 includes histograms of monthly evap- 
oration at La Asunción. It shows that the реп 
from March to May is the driest, corresponding 
to the period of maximal temperature at Nan- 
daime. 

The rapid changes of climatic factors at the 
summit are striking. Rapidly moving fog can dis- 
appear, revealing the full force of the sun only 
for the pattern to be repeated with a sudden blan- 
ket of fog. Such changes in the weather may hav? 
a considerable effect on the vegetation. 


A BRIEF ACCOUNT OF THE VEGETATION 


H r t- 

For purposes of this study it seems most e 

ural and convenient to divide Mombacho ИЦ 
three altitudinal vegetation zones. For the l0 


Nicaragua the term “deciduous seasonal for 
of Beard (1942, 1944) seems most appropri? 
reflecting the deciduous nature of the vegetati 
as affected by seasonal rainfall. The second 200 


——"áÀ р ННЦ É—a— н | ۸۹ 


А. ә — 


н н 


1984] 


Precipitation (mm/month) 


нар 


Dec Jan Feb Mar Арг May Jun Jul Aug Sep Oct Nov 
Month 


FIGURE 4. Monthly precipitation at La Asunción 
on Volcán Mombacho (elev. 580 m 
four year period from 
1976. The vertical bars, horizontal bars, and rectangles 
represent the range, mean, and one standard deviation 

ly (d ided by Empresa 


E 


Nacional de Luz y Fuerza). 


15 here termed the “cloud forest." The cloud for- 
ests of Momhach d distinct from 
the deciduous forest. The third and highest vege- 
едеу zone, also often beclouded, is the “elfin 
bee characterized by stunted trees to about 8 


The deci d seasonal forest during the rainy 
icis n similar in appearance to the trop- 
ees » Orest. Even the stately emergent Ceiba 
nage m to both forests in Nicaragua, although 
Pues Y does not gain its greatest stature in the 
wu forest. When the rains cease in De- 
Enid пе forest becomes leafless, and several 
ou flowering (Plumeria, Byrsonima, 

permum), lending color to the otherwise 
pe. 


1 The bby layer includes Casearia, Karwin- 
Biota several vines of the families Convol- 
a Bignoniaceae, Solanaceae, Aristolo- 
is та Cucurbitaceae, and Vitaceae. This layer 
ly torched by landowners to rid grazing 
ae е ics weeds and ticks. Because of 
wae mands made upon the deciduous sea- 
ees Test by man, very little can be found in 

ural state, and essentially none on Volcán 


ATWOOD—VOLCAN MOMBACHO 


195 


+= 


94489 pas 


Evaporation (mm/month) 
Ed 
+ 
а == 


Dec Jan Feb Mar Арг May Jun Jul Aug Sep Oct Nov 
Month 


FIGURE 5. Monthly evaporation at La Asunción on 
Volcán Mombacho (elev. 580 m). The data span a four 
year period from December 1972 to November 1976. 
The vertical bars, horizontal bars, and rectangles rep- 
resent the range, mean, and one standard deviation 

om th tively (dat ded by Empresa 


= 


fr I y( 
Nacional de Luz y Fuerza). 


Mombacho. Most of the forests surrounding 
Mombacho were probably converted to agricul- 
ture by native Americans long before the Spanish 
conquest. 

ombacho contains one of two cloud forests 
other occurrin 


extends from approximately 400 m elevation on 
the east-northeast flank nearly to the summit. It 
begins considerably higher on the south-south- 
west flank, owing to the rain shadow. The cloud 
forest is characterized by evergreens and gener- 
ally lush vegetation, a manifestation of the abun- 
dant precipitation. The many shades of green of 
the cloud forest indicate a complex aggregation 
of species, but this diversity diminishes with in- 
creasing elevation. 

The tallest trees are to be found in the lower 
cloud forest, and the forest becomes shorter with 
elevation until the dwarfing effect culminates at 
the elfin forest. 

Characteristic of the cloud forest is the pres- 


angiosperm families Bromeliaceae, Gesneri- 
aceae, Piperaceae, Araceae, Lentibulariaceae, and 
Ericaceae, but by far the most species rich family 
is the Orchidaceae, although it is low in biomass. 

The herbaceous flora of the cloud forest is 


erate shade in the upper cloud forest, but never 


196 


in deep shade. Several composites occur, mostly 
in disturbed habitats. Two species of Dieffen- 
bachia are found; one in the lower, the other in 
the upper cloud forest. Terrestrial orchids are 
found locally. Tropidia polystachya, supposedly 
abundant and widespread in much of the New 
World tropics, was found on two occasions. 
Goodyera cf. bradeorum is more often found in 
the upper cloud and elfin forests, two species 
of Malaxis. 

In the lower 
non-vascular epiphy t ly uncommon 
on the lower portions of trees but occur in large 
numbers in the canopy. Most epiphytes were col- 
lected from trees that had fallen or were felled, 
but undoubtedly many more species remain un- 
collected. Several bromeliads and orchids in this 
area, such as Guzmania lingulata, Tillandsia 
schiediana, Trigonidium egertonianum, Nidema 
boothii, and Encyclia fragrans, are also common 
to lowland rain forests of the Zelaya Department. 
Two common epiphytic aroid species, Anthu- 
rium scandens and A. cubense are most abundant 
in this zone, the latter occurring in the marginal 
areas with the deciduous forest. 

The shrub layer of the lower cloud forest in- 
cludes the urticaceous Urera, but probably the 
Piperaceae is best represented here. Potho- 

llected with vari peci Pip- 
er in disturbed areas, but other species of Piper 
were found in the darkest understory. In the low- 
er cloud forest of the east slope, Carica papaya 
was observed to assume a dominant position in 
the understory. 
number of pioneer and adventive species 
llected in disturhe eas, and many were 
undoubtedly dispersed by man. Among the more 
attractive is Mirabilis jalapa, a common weed 
of coffee plantations. 

The lower cloud forest is the most disturbed 
zone of evergreen vegetation, and the little re- 
maining primary forest is threatened. The best 
examples of extant lower cloud forest seem to be 
in the northeast facing valley above Finca Las 
Delicias. However, agriculture here is showing 
its effects because most of the primary lower cloud 
forest has either been removed or severely dis- 
turbed. 

The upper cloud forest is characterized by a 
low, few-layered canopy lacking distinct crowns. 
The trees are often conspicuously covered with 
vascular and non-vascular epiphytes even to the 
base of their trunks, and the light intensity at the 
ground level is much higher than that of the lower 
cloud forest. Three commonly observed tree 


cloud forest both vascular and 


L 
тотрпе 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


species of the upper cloud forest were Hedyos- 
mum montanum, Clusia salvinii, and Senecio 
arborescens, but the latter never the stat 
ure of the higher surrounding trees. The herba- 
ceous flora is rich and includes several terrestrial 
orchids, two locally abundant species of Carex, 
and occasional composites as well as numerous 
rns. 

The upper cloud forest seems to be less threat- 
ened by agriculture than the lower cloud forest. 
However, its restricted size renders it vulnerable 
to complete and rapid destruction. The tell-tale 
tracks of wandering cattle were noted above Fin- 
ca Las Delicias near the crater rim. Expansion 
of a coffee plantation was once tried but failed 
at Plan de las Flores, but further attempts in the 
remaining forest seem inevitable. 

In the elfin forest precipitation is abundant, 
wind velocities are high and gusty, and the forest 
is usually beclouded. Elfin forest I tudied 
Brown (1919) in- 
g ( y forest) on Mount 
Maquiling on the island of Luzon, Philippines. 
Beard (1942, 1944) studied elfin forests in the 
Antilles, and Steenis (1972) noted the elfin for- 
ests of Java. Detailed investigations have been 
conducted at Pico del Oeste, Puerto Rico by 
Howard (1968, 1969) and Gill (1969). Alvarez 
del Castillo (1976) contributed an ecological and 
floristic work on an elfin forest on Volcán San 
Martin Tuxtla, Veracruz, Mexico. 

Beard (1944) characterized the elfin forest of 
the Caribbean area as an “open woodland about 
8 m high of stunted, gnarled trees, often stilt- 
rooted and with thick fleshy leaves, with long 
rambling branches pointing away from the wind. 
There may be an understory of dwarf palms and 
tree ferns. The whole is loaded with moss, li- 
chens, and epiphytes, and forms a completely 
impenetrable thicket." 

Viewed from the air, the elfin forest of Volcán 
Mombacho appears as an even, dense canopy 
pruned by the elements. The upper cloud forest 
lacks the pruned appearance, and the line delim- 
iting the two forests is often distinct. The сап 
consists of one stratum beneath which WU 
casional shrubs (especially Psychotria spp. 
numerous herbs. Nearly every branch 1s 
ited by bryophytes, and epiphytic vascular planis 
are common everywhere. The leaves of arbor? 
cent elfin forest species with few exceptions ' 
to be leathery, entire, and small to medium- 

Aerial photographs show that the elfin 
of Mombacho extend along all exposed a 
and pinnacles down to an elevation of about 


су 


by а number of investigators. 
+ PIRE жад. (~ ac. 


forests - 


1984] 


m. It blankets even the roughest topography, in- 
cluding nearly vertical cliffs. 

The arborescent stratum of the more protected 
elfin forest contains numerous species including 
Clusia salvinii, Rapanea ferruginea, Freziera 
friedrichstaliana, Myrcianthes fragrans, Oreo- 
panax xalapense, Viburnum hartwegii, a number 
of Rubiaceae, and tree ferns of the genera Cyan- 
thea and Nephelea. Concerning the elfin forest 
Beard (1944) noted that “риге stands of Clusia 
spp. Constitute this formation in some of the less- 
er Antilles between 1,000 and 1,100 m ...." 
Pure stands of Clusia occur on Mombacho, but 
only along the most exposed ridges and pinnacles 
(Fig. 6). Ferns, bromeliads, and orchid g 
the most numerous and diverse epiphytes en- 
countered in the elfin forest. Among the genera 
of epiphytic ferns represented are Elaphoglos- 
sum, Grammitis, Polypodium, Hymenophyllum, 
and Trichomanes. Bromeliad genera include 
Aechmea, Guzmania, Pitcairnia, Tillandsia, and 
Vriesia. 


The terrestrial herbaceous stratum is expect- 
edly rich. In the shaded area of the mature elfin 
forest the terrestrial herbaceous flora consists 
largely of ferns. An absence of grasses was noted, 
but Oplismenus hirtellus forms mats in open 
areas. Three species of Cyperaceae, Carex don- 
nell-smithii, C. polystachya, and Uncinnia ha- 
mata, occur frequently in the elfin forest, often 
along damp and exposed banks. The terrestrial 
orchid inhabitants include Malaxis maxonii, M. 
tipuloides, Erythrodes spp., Goodyera bradeo- 
биље and Psilochilus cf. macrophyllus. One ter- 
61а! gesneriad, Kohleria spicata, is commonly 

g Plan de las Flores 

The herbaceous flora of disturbed areas varies 
psy. The herbs of the disturbed crater 
Pte almost exclusively of Isachne arun- 
: 4 With a scattering of weedy composites. 

rundinella deppeana is the most characteristic 
ee id disturbed Plan de las Flores. Other herbs 
dst ng Castileja arvense, several composites, 

the ferns Phlebodium aureum and Ophio- 


mA more diverse elfin forest are shrubby 
mia (2) па spp. and a bristly melastome, Clide- 
“= E Sp. The diversity of shrubs of disturbed 
whens аа higher, except along the crater rim 
= E us is most abundant. At Plan de las 
coffee © open disturbed area once cleared for 
and i rowing consists of a large number of shrubs 
erbs. Among the shrubby species are Con- 


ATWOOD—VOLCAN МОМВАСНО 


197 


FIGURE 6. View of the highest peak of Mombacho 
with Clusia thicket in the foreground. 


ostegia spp., Monochaetum deppeanum, Ardisia 
sp., Parathesis sp., Viburnum hartwegii, and 
Cestrum aurantiacum. 

At least four alien floristic elements were ob- 
served at Plan de las Flores. Hippeastrum sp. 
was observed and collected once. A row of Hi- 
biscus rosa-sinensis was observed in the aban- 
doned clearing as were Coffea arabica and oc- 
casional clumps of Musa paradisiaca. Among a 
large number of pioneer species and weeds found 
in the disturbed area of the cloud forest above 
Finca Las Delicias was a cultivated Coccoloba 
uvifera. None of the once cultivated elements 
found seemed to be reproducing and no juvenile 
individuals were observed. Occasional waifs from 
lower elevations, such as Mormodes sp. and Jac- 
quiniella globosa, were found in the elfin forest. 


HisTORICAL SKETCH OF BOTANICAL 
EXPLORATION ON VOLCÁN MOMBACHO 


The first pioneer traveler and naturalist known 
to make collections on Volcán Mombacho was 
Emanuel Ritter Friedrichstal. His travels includ- 
ed the Antilles, Nicaragua, Guatemala, and the 
Yucatan, from 1837 to 1841 (Allgemeine 
Deutsche Biographie, 1878). It is probable that 
several Friedrichstal specimens attributed to 
Guatemala actually took their origin in Nicara- 
gua, as may be the case with Freziera friedrichs- 
taliana known only from Mombacho (Kobuski 
1941), and Honduras (Melina, 1975), and not 
from Guatemala (Standley & Williams, 1961). 

Anders Sandge Oersted visited Mombacho in 
December of 1847 (fide F. Seymour, pers. 
comm.). He also collected Heliocarpus nodiflo- 
rus (Lay, 1949) and it is probable that he col- 
ected many more specimens. 

Kobuski (1941) noted that G. Wright collected 


> 


— 


198 


Freziera friedrichstaliana on Volcan Momba- 
cho. 

Paul Levy, a French engineer, resided in Gra- 
nada and collected Nicaraguan plants between 
1869 and 1885 (Hemsley, 1887; Chaudhri et al., 
1972), but if he made collections from Mom- 
bacho none of his specimens have surfaced. 

Charles Fuller Baker, graduate of Michigan 
Agricultural College in 1891 (Cattell, 1906) made 
collections on Mombacho in February of 1903 
= herbarium sheet, Baker 2488, MSC). 

1909 the first of two volumes of “Flora 
ie by Miguel Ramirez Goyena was 
published, and to this day it remains the sole 
flora of the area. Goyena doubtless botanized 
Mombacho, but nothing is known of his col- 
lecting there. Unfortunately his work cites no 
specimens, and only a few localities, so its utility 
is limited. 

W. R. Maxon, A. D. Harvey, and A. T. Val- 
entine visited Mombacho in July 1923. They 
collected a new species of Malaxis that Oakes 
Ames named M. maxonii (Ames, 1923). 

Verne Grant collected on Mombacho in 1940 
and 1941 (fide F. Seymour & F. Almeda, pers. 
comm.). 

In January 1967 L. O. Williams, Antonio Mel- 
ina R., and A. H. Heller collected there during 
a three-day period (Heller, pers. comm.). A. D. 
Moore, D. A. Dudey, and Charles Nichols col- 
lected on the southeastern slope on January 9, 
1969. Much of the material for this work comes 
from their collections. 

On January 27 of the following year Edwardo 
Narvaez S. and I collected in the disturbed area 
around the vacation house above Finca Las De- 
licias. 

On April 9, 1971, I collected about 30 numbers 
from the elfin forest on the northwest crater rim. 

In May 1972 R. L. Wilbur, D. E. Stone, and 
F. Almeda made collections near the crater (F. 
Almeda, pers. comm.). 

Frank C. Seymour made collections on July 
25, 1972 and also on August 1 of the same year 
with Stuart B. Robbins. 

David A. Neill, Stephan A. Marshall, and I 
collected around the north and northwest crater 
rim in December 1973 and January 1974. 


THE FLORA 
Many of the collections in the following check- 
list were difficult to determine owing to lack of 


revisionary work. As monographic treatments are 
produced for various genera, many names in- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


cluded here will be found to be incorrect. The 
checklist is complete to 1980, but additional 
species have since been collected by W. D. Ste- 
vens. 

A set of specimens collected in 1975 and 1977 
was left at Universidad Centroamericana (UCA) 
at Managua, but the principal set of 1975 col- 
lections is contained in the Beal-Darlington Her- 
barium (MSC) of Michigan State University. 
These latter collections are preceded by A (At- 
wood), N (Neill), or AN (Atwood & Neill). Most 
of the specimens collected before 1975 by F. Sey- 
mour, D. Dudey, D. Moore, С. Nichols, 5. Rob- 
bins, E. Narvaez S., D. Neill, A. Marshall, and 
me were owned by Mr. Frank Seymour, who 
kindly provided me access to his herbarium. This 
collection is now incorporated at the Missouri 
earn Garden (MO). 

classification of the fern families и 
siete is authored by Crabbe et al. (1975). Th 
classification of the angiosperm families is w 
sically that of Cronquist (1968). 

A total of 457 species are represented in the 
checklist, including 80 species of pteriodophytes 
distributed among 15 families and 33 ) genera, - 
377 species of 
ilies and 256 genera. No gymnosperms are known 
from Mombacho. The largest fern families аге 
the Aspleniaceae and Polypodiaceae with 24 and 
16 species respectively. The largest angiosperm 
ompositae with 


87 and 29 врео respectively. 

It is unwise to speculate on the phytogeograph- 
ic significance of most floristic elements of Mom- 
bacho because the species and their ranges are 
poorly known. Nevertheless several observa 
tions concerning phytogeography seem justified. 

The large numbers of pteridophyte and orchid 
species are probably in part accounted for by 


their high fecundity and dispersibility. However, | 


it is curious that the Gesneriaceae, also 
fecund and supposedly pri dispersed, is ње 
resented by only three spe 

Five epiphytic orchids fnd aah northernmost 
limits on Mombacho or central Nicaragua 
include: Epidendrum lacustre, E. selaginell 
Mesospinidium warscewiczii, and Pleurothallis 
convallaria. The northerly range limits of thes? 
orchids and the absence of Carpinus, Liquid- 


ambar, and Pinus suggest that the flora is Costa 


ican. 


are noted for Volcan Mombacho. The first 


is Maxillaria mombachoensis (Orchidaceae ^ an : 


One endemic and one near endemic species 


1984] ATWOOD—VOLCAN MOMBACHO 199 


attractive orange orchid of the Maxillaria cu- 
cullata complex and the second, Freziera fried- 
E (Theaceae), known otherwise only 
from Honduras 


LIST OF SPECIES 
FERNS AND FERN ALLIES 


ADIANTACEAE 
Adiantum concinnum Willd. M 6254, 1 Au- 
gust 1972 (MO). Lower cloud for 
A. lunulatum (Roxb.) Burm. f. pre 77120a, 8 
February 1977 (MSC). Very local in lower cloud 


A. macrophyllum Sw. Atwood A48, ds Ары) 1975 
MSC). Common in lower cloud for 

А. trapeziforme L. Atwood 77105, 8 сд е 1977 
(FSU, MO, MSC). Local in lower oy forest. 

еи calomelanos L. Seymour 6099, 25 
July 1972 (MO). Locally abundant in oud forest. 

Р. шне (Kunze) Maxon. Atwood 3899, 27 Jan- 
ад "ah 970 (MO). Apparently uncommon in cloud 


Pteris е Poir. Atwood 3909, 27 January 1970 
wer cloud forest. 
к т remota Fee. Atwood 7742, 3 Feb 
7 (FSU, MSC). Common elfin forest epi чё 
ASPLENIACEAE , M уе 
Asplenium abscissum Willd. Neill N40, 29 April 1975 
(MSC); Atwood A170, 15 May 1975 (so. Local 
On crater js and at Plan de las Flor 
A. cristatum Lam. Atwood & Neill AN1 197, 16 July 
1975 (MSC). Lower and upper cloud forests. 
A. cm Willd. Dudey & Moore 1966, 9 January 
69 (MO); Atwood & Neill AN93, 2 July 1975 
бс. Rare lithophyte on border of deciduous 
forest and cloud forest at Finca Las Delicias. 
A. A "he tri Sw. Dudey & Moore 1966a, 9 January 
A. hoffmanni Hieron. Atwood & Nal АМ57, 1 July 
1975 (MSC). Lower cloud fore 
A. pteropus Kaulf. Atwood A13, 29 “April 1975 (MSC). 
Near northeast crater rim in elfin forest. Growing 


epiphyte. 
A. cf. pulchellum Raddi. нозі: hid 1, 27 January 

1970 (MSC). Lower cloud fore 
ag var. partitum Споља Hieron. Atwood 
77 ы 6 Ее NN 1977 (MSC). Rare epiphyte of 


lou 
Bobs а elad тел (Sprengel) Ching. Dudey & 
ооте 1968, 9 January 1969 (MO). Lower cloud 


Ctenitis hemsleyana (Baker ex Hems.) Copel. At- 
77157, 15 February 1977 (FSU). Locally 


iplazium cristatum (Desr.) Alson. Atwood А dd 5 
nm 197 1975 (MSC). Common in elfin fores 
moet (Sprengel) Link. Atwood 3907, 37 Jan- 
D. „= wer cloud forest 
oo astrum Lellinger. Atwood, Marshall & Neill 
Dre 6 December 1973 (MO). Cloud forest. 
bei karwinskyana (Mett.) Kuntze. Atwood 


77156, 10 February 1977 (FSU, MSC). Locally 

common in elfin forest. 

Elaphoglossum рә њена Christ. Atwood 5451, 9 
April 1971 (VT). Elfin forest 

E. palmense Christ. Neill N41, 29 April 1975 (MSC); 
Atwood A308, 5 June 1975 (MSC); Atwood & Neill 
AN196, 16 July 1975 кс Local epiphyte of 
upper cloud and c for 

E. tectum (H. B. e Willd.) M ооге? Atwood, Mar- 
shall & Neill 6724, 16 December 1973 (MO). Ap- 
parently uncommon epiphyte of upper cloud and 
elfin forests. 

E. sp. Atwood A30, 29 April 1975 (MSC); Atwood 
A302, 5 June 1975 (MSC). Elfin forest epiphyte at 
Plan de las Flores. Other species of Elaphoglossum 

undoubtedly occur on ыам порите 

RT Tod (Sw.) Morton. Atwood 3913, 27 

0 (MO); pronis: Marshall & Neill 

06707 15 ван 1973 (М 
Polybotrya cervina (L.) Kaulf. Atwood & Neill AN200, 
16 July 1975 (MSC). Upper cloud forest on east 


flank. 
ко prep (L.) Morton. Atwood 3908, 
7 Jan 197 


MO). 
B heracleifolia сулы. ) Underw. Atwood 
09, за Uncommon ter- 
restrial of маод ey Mb 
T. mexicana (Fee) Morton. PAD 7144, 10 Feb- 
ruary 1977 (MSC, SEL). Lower cloud forest. 
BLECHNACEAE 
Blechnum cf. divergens (Kunze) Mett. Atwood A42, 
30 April 1975 (MSC). Upper cloud and elfin forest 
terrestrial. This may be the same as B. ensiforme. 
B. ensiforme (Liebm.) C. Chr. Atwood, Marshall & 
Neill 6731, 16 December 1973 (MO); Neill N39, 
29 April а diues Upper cloud and elfin forest. 
B. fragile m.) Morton & Lellinger. Atwood, 
Ma n je 6730, а _ 1973 (МО). 
Upper cloud and elfin for 
B. lehmannii Hieron. Atwood A292, 2 June 1975 
(MSC). C 
B. occidentale L. Dudey & Moore 1965, 9 January 
1969 (MO). Frequent in cloud and elfin forest. 
B. pyramidatum (Lam.) Urb. Nichols 2005, 9 Jan- 
uary 1969 (MO). 
B. unilaterale Sw. Atwood 77168, 15 February 1977 
d Local on eroded banks of upper cloud for- 


CYATHEAC 
Cyathea sp. tod 298a ее 1975 (MSC). Tree 
fern common at Plan de las Flores. 
— mexicana seat oy & Cham.) Tryon. At- 
10 July 1975 (MSC). Tree of elfin 
forest. Posted 
DAVALLIACEAE 
Ni peg pectinata (Willd.) Schott. Atwood A14, 
29 April 1975 (MSC). Locally common in upper 
cloud forest about 
I 


CEAE 
Gleichenia bifida Дафи Sprengel. Atwood. A1 7,29 
April 1975 (М 


of crater rim and si forest. =" produces пеаг- 
ly impenetrable — 
NOPHYLLACEA 
H ood 7770, 
6 February 1977 (US). Elfin forest Pe 


200 


H. a arco (Sw.) Sw. Atwood, Marshall & Neill 
6708, 6723, 15 December 1973 (MO). 

beans capillaceum L. 4190 3902, 27 Јап- 
џагу 1970 (MO). Cloud for 

T. ae Hook. & Grev. dd 5468b, 9 April 
1971 (MO). Elfin forest. 


T. pyxidiferum L. Atwood 7769, 6 February 1977 
(US). Elfin eredi epiphyte. 
. radicans Sw. Atwood 3900, 27 January 1970 (MO); 


Pis N45, 29 April 1975 (MSC). Common in elfin 


4: н Sw. Atwood, Marshall & Neill 6722, 16 
January 1972 (MO). Cloud and elfin forests. 
LOPHOSORIACEAE 
Lophosoria quadripinnata (Gmel.) C. Chr. Atwood 
A297, 5 June 1975 (MSC). Plan de las Flores. 
LYCOPODIACEAE 
Lycopodium oe Mett. Atwood 7774, 6 
February 1977 (US). Very rare epiphyte in elfin 


L. dichotomum Jacq. Atwood & Neill AN65, 1 July 
1975 (MSC). Epiphyte of lower cloud forest. 
L. linifolium L. Atwood 7741, 3 LE 1977 
MSC). Occasional epiphyte of elfin 
L. taxifolium Sw. Atwood 5454, 9 Rae 1972 (MO). 
Epiphyte. 
L: но var. parvifolium d e id 
Lellinger. Atwood February 7:008), 
Very "us epiphyte in elfin forest. 
MARATTIACEAE 
Marattia interposita Christ. Atwood & Neill AN188, 
16 July 1975 (MSC). Upper cloud and elfin forest. 
OPHIOGLOSSACEAE 
Ophioglossum reticulatum L. Atwood A353, 10 July 


1975 (MSC). Very abundant at disturbed area of 


Grammitis blepharodes (Maxon) Seymour. Atwood 
53, 9 April 1971 (MO); Atwood, Marshall & 
Neill 6728, 16 December 1973 (MO). Upper cloud 
and elfin forest epiphyte. 
G. serrulata (Sw.) Sw. Atwood eid = April 1975 
(MSC). Upper cloud апа elfin 
G. к с Lellinger. canoes 7773, 6 
7 (US). Apparently a very rare epi- 
ace Ea pris forest 
Microgramma lycopodioides (L.) Copel. Neill N27, 
26 rt 1975 (MSC). Common at Plan de las 


Phlebodium aureum (L.) J. Smith. Atwood A163, 15 
May 1975 (MSC). Common at Plan de p Flores. 

Pleopeltis percussa (Cav.) Hook. & Grev. Atwood & 
Neill узыны 1 July 1975 (MSC). Epiphytic i in lower 
cloud fore: 

P. revoluta سڪ‎ ex Willd.) A. R. Smith (syn. 
Polypodium astrolepis Liebm.). Atwood 7733, 3 
February 1977 (US). 

Polypodium angustifolium Sw. Atwood 7 738, 3 Feb- 
ruary 1977 (MSC). Very common epiphyte of elfin 
forest. 

P. dissimile L. Atwood 3906, 27 January 1970 (MO); 
Neill N43, 29 ain 1975 ue Lower cloud for- 
est on east flan 

P. cf. fructuosum haa & Wonk Robbins 6251, 1 
August 1972 (MO). Probably also аяр 6098, 
25 July 1972 (MO). Lower cloud fores 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


P. loriceum L. Atwood, Marshall & Neill 6725, 16 
December 1973 (MO). Northwest crater rim. At- 
MO d 0f. 15 May 1975 (MSC). Plan de las Flo- 


Р. pr PON Schlecht. & Cham. Atwood 3905, 27 
January 1970 (M » Cloud forest inhabitant. 
P. plesiosorum Kunze. Seymour 6097, 25 July 1972 
09), Lower Saat forest. 
plumula Humb. & Bonpl. ex Willd. Atwood & 
ken АМ91, 2 July 1975 (MSC). Growing on boul- 
Ts in margin of Mus s deciduous forest. 
P. polypodioides (L.) W ar. pip At- 
wood & Neill AN92, 2 July 197 5 (MSC). In margin 
of deciduous and lower cloud forest 
P. wiesbaueri Sod. Atwood 5452, 9 April 1971 (VT). 
Upper cloud forest. 
SCHIZEACEAE 
Lygodium venustum Sw. Seymour 6096, 25 July 1972 
(MO); Atwood & Neill AN86, 2 July 1975 (МО). 
In lower cloud and deciduous forests. 
SELAGINELLACEAE 
Selaginella sp. Atwood 7730, 3 February 1977 (MSC). 
Prostrate species common in elfin forest. 
THELYPTERIDACEAE 
на balbisii (Sprengel) Ching. Baker 2449 


T. columbiana (C. Chr.) Morton. Atwood A26, 29 
975 Ne uni cloud and elfin forests. 
T veru (Forsk.) E. St. John. Atwood A444, 30 


w 
T. mombachensis Gomez. Atwood A304a, 5 June 6 
1975 (MSC); Atwood, Marshall & pent 6726, 1 
December 1973 (МО). Elfin forest at Plan de las 

Flores. 


FLOWERING PLANTS 


ACANTHACEAE n 
Aphelandra deppeana Schlecht. & o Dudey 
Moore 1959, 9 January 1969 (M 
A. танын ома) пи Eu 7T 
ebruary 1977 (FSU, MO, M SC). Locally co 
wa in си са at Finca Las Delicias. 
wers canary 
ан к Juss. peut A156, 15 May 
MSC). Weed of disturbed sind forest. 
the ^ bn may not be disti 
B. pyramidatum (Lam.) Urb. idiot 2005, 9 Jan 


Dyschoriste skutchii Leonard. Narvaez 3888, 27 Jan- 


9 

Ruellia inundata H.B.K. & Moore 1960, 
January 1969 (MO). Lower cloud forest. 

Achyranthes азр L. Atwood А55, 30 April 1975 

urbed area by f house 5881, n 

Alternanthera сит јади Standl. М 


О). Moore 
Chamissoa altissima (Jacq.) H.B.K. Dudey i: 
uary 1969 E Disturbed dr for 


1977, 9 Jan 
est above Flick Las Delici Dude) 
vem achyranthoides (H. B. X) Мо te 
Moore 1979, 9 Jan 19 
Gomphrena decumbens NN Path & 4 Neill ANM 
2 July 1975 (MSO. In pastures and roadsides # 
Finca Las Delicias 


1984] ATWOOD— VOLCÁN MOMBACHO 201 


ИМ celosia L. Dudey & Moore 1977, 9 January 
MO). Lower cloud forest. Locally abundant 
ir Ayr sold in markets for decoration. 
ANACARDIACEA 
Mangifera indica L. Atwood 3921, 27 January 1970 
escape in deciduous forest areas. 
E 


Echites cf. turrigera Woodson. don. di Neill AN7 1, 
2 July 1975 (MSC). Deciduous for 

Plumeria rubra L. Not collected but ons obse 
asa conspicuous element of the deciduous vei 
This is the national flower of Nicaragua. The 


e flowers. 
Rauvolfia littoralis Rusby. Atwood & Neill AN84, 2 
July 1975 (MSC). Common herb in deciduous for- 
est area near Finca Las Delicias. 
Stemmodenia donnell-smithii (Rose) Woodson. At- 
wood & Neill AN69, 1 July 1975 (MSC). In decid- 
ous forest. 
AQUIFOLIACEAE 
Пех aff. carpenterae Standl. Atwood A192, 15 May 
pee (MSC). Collected at Plan de las Flores. 


Anthurium cubense Engl. Atwood & Neill AN82, 2 
July 1975 (MSC). Common epiphyte in trees of 
d Finca Las 


cloud forest ay sot common in coffee planta- 
tions at Finca Сишт 

Dieffenbachia pig ы Engl. Atwood & Neill 
AN206, 16 July 1975 (MSC). Upper cloud forest 
ravine above Finca Las Delicias about 900 m. 

D. seguine L. Atwood A212, 18 May 1975 (MSC). 
"im terrestrial in deep shade at about 600 


M. мол! Schott. А d AA2, 27 April 1975 
MSC); Atwood A172, 15 May 1975 (MSC); Neill 
N28,27 леве 1975 (MSC); Atwood A363, 10 July 
1975 (MSC). Common liana of cloud forests. 


fores 


ues 
Oreopanax xalapense (H.B.K.) Dcne. & Planch. d 
wood A299, 4361, 10 July SEDIS SC). Freque 
in upper cloud and elfin forests 
ACEAE 


Chamaedorea sp. Atwood A17 1, 15 May 1975 (MSC). 

Cloud and elfin forests, mostly in disturbed areas. 

ndetermined. Atwood & Neill AN50, 1 July 1975 

(MSC). Lower cloud forest near Finca Cutirre 
LOCHIACEAE 


рена anguicida Jacq. Atwood & Neill АМ81, 
uly 1975 (MSC). In deciduous forest near Finca 
s Delicias, growing near the following species. 
Pann! iin fruit only. 
. €f. max. Jacq. A + e AN77, 2 July 
1975 (M (MSC), DM 
"IADAC 
opment ч. Robbins 6260, 1 desea 1972 
(MO) Lower yii and deciduous fores 


Gonolobus sp. Neill 1363, 3 February 1977 (UCA). 
Vine of cloud forest. 
BEGONIACEAE 
Begonia filipes Benth. Dudey & Moore 2004, 9 Jan- 
MO). Cloud forest. 
B. КА Liebm. Dudey & Moore 1985, 9 January 
1969 (MO). Lower cloud forest 
BIGNONIACEAE 
Arrabidaea mollissima Bur. & K. Schum. Dudey & 
Moore 1957, 9 January 1969 (MO). Probably col- 
lected in deciduous forest. 
Cydista diversifolia (H.B.K.) Miers. Atwood & Neill 
N207, 16 July 1975 (MSC). In deciduous forests 
below Finca Las Delicias 
BIXACEAE 
Bixa orellana L. Atwood & Neill AN67, 1 July 1975 
sae ae a mmon in lower cloud forest above Fin- 


a Cutirr 
BOMBACACEA 
Ceiba sp. No на made. Forms ек 
р ough- 


out deciduous forest 
Quararibea funebris (Llave) Vischer. Neill 1008, 3 
October 1976 (FSU). Tree about 25 m tall. Lower 
cloud forest. 
BORAGINACEAE 
ier dentata Poir. Atwood & Neill AN75, 2 July 
75 (MSC). Finca Las Delicias in deciduous for- 


нт indicum 1. Atwood & Neill AN74, 2 
July 1975 (MSC). Deciduous forest near Finca Las 
Delicias 

BROMELIACEAE 

Catopsis sp. оо, Neill AN205, 16 July 1975 
(MSC). d 

Eco cen angustifolia (Baker) Wittm. Neill 7582, 
8 August 1976 

G. о. Mez. Neill 7583, 8 August 1976 (MO). 
G. lingulata var. minor (Mez) L. B. Smith. Atwood 
] 8 mm 


epiphyte of cloud forest. Very attractive species 
with brilliant red bracts. 

G. monostachia (L.) Rusby ex Mez. Atwood & Neill 
AN204, 16 July 1975 (MSC). Common epiphyte 
ied cloud forests. Тһе contrasting black veined low- 


ater species a Guzmania on Mombach 
С. nicaraguensis Mez & С. Е. Baker. edd. & Neill 
AN306, 30 July gr (MSC). Uncommon at crater 
rim. Elfin forest epiphyte. 
наш Seyi oe Beer. Atwood 7796, 8 Feb- 
7 (MSC). Epiphyte of deciduous forest. 
Р sardi (Brongn.) Regel. Neill 7580, 8 August 
1976 (UCA). Common in elfin forest at Plan de 


las Flores. 

Tillandsia bulbosa Hook. Atwood & Neill AN58, 1 
July 1975 (MSC). Lower cloud forest. 
T. fasciculata Sw. Atwood 5459, 9 April 1971 (VT). 
Cloud and elfin forest epiphyte. 


x At 
4 July 1975 (MSC). Lower cloud forest. 
T. leiboldiana Schlecht. Neill 7529, 7 August 1976 


1. monadel Ipha (E. Morr.) Baker. Atwood & Neill 
AN352, 1 July 1975 (MSC). Lower cloud forest. 
T. schiediana Steud. Atwood & Neill AN80, 2 July 


202 


Pe а t abundant in dry decid f 


J 


T. аи Atwood 3916, 27 January 1970 (МО). 
Соттоп cloud forest epiphyte. 
Vriesea Į ez & Werckle) Sm. & Pitt. At- 
wood Al 6, 29 April 1975 (MSC). Elfin forest epi- 
ph 


yte. 
V. sp. Atwood A15, 29 April 1975 (MSC). Upper 


Bursera simaruba (L.) Sarg. Atwood & Neill AN214, 
16 July 1975 (MSC). Common tree of deciduous 


orest. 
CAMPANULACEAE 
Lobelia laxiflora H.B.K. Atwood 5477, 9 April 1971 
(VT). wa 2 
CAPPARACE 
Forhan mnia matudai Lundell. Atwood 77116, 8 
February 1977 (MSC). Lower cloud forest tree. 
CAPRIFOLIACEAE 
Viburnum hartwegii Benth. Atwood 4200, 14 May 
1975 (MSC). ш. gyno sites of elfin forest at 
Plan de es Flor 
CARICACEA 
Carica peated L. Not collected but observed in low- 
er cloud forest in deep shade 
CARYOPHYLLACEAE 
Drymaria cordata (L.) Willd. ex Roem & Schult. 
Neill 1003, 3 October 1976 (UCA). Coffee plan- 


tion weed. 
ааа ee 
Недуогтит тотапит М. Вигрег. Меш 408, 28 
Мау 19 MSC). Cae elfin forest tree. 
CHRYSOBALANAC 
Chrysobalanus icaco L. Robbins Ро eam 1972 
(MO). Probably lower cloud for 
COCHLOSPERMACEAE 


Cochlospermum vitifolium Willd. Atwood & Neill 
AN78, 2 July 1975 (MSC). Common deciduous 
forest component, but found as high as 800 m 

COMBRETACEAE 

Combretum fruticosum (Loeff.) Stuntz. Dudey & 
Moore 1951, 9 January 1969 (MO). Probably low- 
er cloud forest. 

COMMELINACEAE 

Campelia hirsuta Standl. Dudey & Moore 1974a, 9 
January 1969 (MO). 

C. zanonia (L.) H.B.K. Neill N50, 29 April 1975 
(MSC). Common in cloud forest. 

Commelina erecta L. Narvaez dod 27 January 1970 
(MO). Cloud and elfin for 

Dichorisandra hexandra (Aubl. Standl. Atwood & 

Neill AN186, 15 May 1975 (MSC); эы кые 29 
_ April 1975 (MSC). Local i in cloud Mens 


8 Clarke. 
wood A1 68, 15 frog 1975 (MSC). Ad disturbed 
s Flo 


anensis (К unth) Woodson. At- 
wood A 444, 30 April I (MSC). In disturbed sites 
at Plan de las Flore 
COMPOSITAE 
Baccharis trinervis (Lam.) Pers. Atwood A7, 29 A 
D (M 2 ч А43, 30 April 1975 Sc 
urbed near vacation house. 
Bidens prt L Ripa d by F. C. Seymour (pers. 
m.). 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


B. riparia H.B.K. Narvaez 3891, 27 January 1970 
B. squarrosa H.B.K. Atwood 3924, 27 January 1970 
(MO 


Chaptalia nutans (L.) Hemsl. Seymour 6105, 25 July 
). Common in disturbed areas of cloud 


Chromolaena odorata (L.) King & Robinson. Át- 
ood A54, 29 April 1975 (MO). Disturbed site at 
нее house. 

Cirsium mexicanum DC. Atwood 5479, 9 April 1971 
(MO); Atwood A46, 30 April 1975 (MSC); Neill 
N60, 30 April 1975 (MSC). Disturbed cloud forest. 

Clibadium 1. Atwood А161 y 
1975 (MSC). Small tree in elfin fore 


E pieta (L.) Kuntze. Atwood 3923, 27 January 
0 (MO). Disturbed cloud forest 

Eu hieracifolia (L.) R. Nichols 201 4, 9 January 
1969 (MO). Disturbed cloud forest. 

Erigeron bonariensis L. Narvaez 3895, 27 January 
1970 (MO). aang area in cloud АИ above 
Finca Las Delic 

Eupatorium нагна Less. Atwood 77142, 20 
September 1977 (MSC). Small tree of disturbed 
cloud forest on таа flank. 

E. sinclairii (Benth.) King & Robinson. Narvaez 38%, 

27 January 1970 (MO). ы disturbed area of cloud 
forest at vacation hous 

Fleischmannia pratensis (Klatt) King & Robinson. 
Atwood A155, 15 May 1975 (MO). Disturbed site 
at Plan de las Flores. 

Galinsoga x ыа» Man ) Blake. ма pie 27 


m cf. discolor (Hook. & Arn.) Benth. & Hook. 
x Hemsl. Atwood A188a, 15 Gn 1975 (MSO) 
Rare i in disturbed ua orest. 

Melampodium divaricatum (L. Rich. ex Pers.) DC 
Atwood & Neill 4485, 2 July 1975 (MSO). Decid- 
uous forest. 

Melanthera nivea (L.) Small. Dudey & Moore 1961, 
9 January 1969 (MO). Cloud forest 

Neurolaena lobata R. Br. Atwood 77 107, 8 February 
1978 сы, hes of disturbed cloud forest. 

raguense Blake. Dude 

1991, 9 Б 1969 (М h- 

Pseudelephantopus spicatus (Juss.)C C. F. Baker. e 
ols 2011, 9 January 1969 (MO). Weed of dist 
cloud forest. 30 

Senecio ос Steetz in Seem. Neill №38, Я 
April 1975 (MSC): Atwood А21, 29 April 19 
(MSC). AA mmon tree in upper cloud forest. v 

Spilanthes americana (L. f.) Hieron. ex 175 
wood A19, 29 April 1975 (MSC); Atwood АПУ 
15 May 1975 (MSC). On crater rim and at V 

ouse. 

S. ocymifolia (Lam.) A. H. Moore. Narvaez 
27 January 1970 (MO 


3892, 


). | 
Verbesina fraseri Hemsl. Dudey & Moore 1 963, 9 
А 81, 15 May 


Јапџагу 1969 (МО 
ernonia canescens H.B.K. Atwood Al 

1975 (MO). Common in disturbed е elfin fore 
. patens H.B.K. Atwood & Neill 1567, 14 


vacation | 


DELL LL Lll RN 
P soo lll ortus. hGh!ÓTDRREOQQ-LC-L-LO- | pes ћи 


=== 


1984] ATWOOD—VOLCAN MOMBACHO 203 


1977 (FSU). Lower cloud forest weed at Finca 


NVOLVULACEAE 
Ipomoea alba L. Atwood 77112, 8 Pe y 1970 
(MSC). Roadside vine at Finca Cutirr 
Merremia tuberosa (L.) Rendle. Neill 1565. 14 March 
1977 (MSC). Collected by a local resident for dec- 


oration. 

M. umbellata (L.) Hallier f. Atwood 77146, 10 Feb- 
m 1977 7 (MSC). Locally common lower cloud 
ore 

Рау. hederifolia (L.) G. Don. Dudey & Moore 

1956, 9 January 1969 (MO); Atwood 77145, 10 

February 1977 7 (MSC). 

TACEAE 

Costus cf. sanguineus Donn.-Sm. Nichols 1998, 9 

January 1969 (MO). 

CRUCIFERAE 

е ae (L.) Hieron. Narvaez 3886, 27 Jan- 
70 (MO). In disturbed cloud forest. 
По ен и АЕ 
Melothria pendula L. Atwood A180, 15 May 1975 
C). Common vine of disturbed cloud forest. 
Momordica charantia L. Atwood 77117, 8 February 
1977 (MSC). Weed of coffee plantations. 
Rytidostylis ciliata (Oerst.) Monachino. Atwood & 
Ne p N304, 30 July 1975 (MSC). Disturbed for- 
reas. 


CYPERACEAE 
Carex cf. donnell-smithii L. H. Bailey. Atwood A162, 
15 May 1975 (MSC). Common herb of elfin and 
= и Spikes seem a bit short for the above 


С. po Sw. ex Wahl. Atwood, Marshall & 
Neill 6733, 16 January 1973 (MO); Atwood A197, 
Ši Y 1975 (MSC). Not uncommon in elfin for- 


peri mutisii (H.B.K.) Griseb. Robbins 6256, 1 
August 1972 (MO 

C. te оң uis Sw. Dude ey & Moore 1973, 9 January 1969 
(MO). Common i in disturbed areas at low and high 
elevations 
· Sp. ied A182, 15 аы 1975 (MSC). In open 
areas at Plan de las Flor : : d 

Mon; polyphylla Vahl Atwood A179, 15 May 
so. Common in disturbed areas of elfin 


rc hamata (Sw.) Urban. Atwood 5457, 9 April 
LÀ 1 (MO). Common in elfin and cloud forests. 
LAEOCARPACEAE 
C calabrura L. Seymour 6103, 25 July 1972 
om 
ERICACEA e mon tree of deciduous forest area. 


oe crassifolia (Benth.) Hemsl. Atwood A35, 
M B 975 (MSC); Neill N24, 26 April 1975 
Satyria undant in upper cloud and elfin forests. 
Warszewiczii Klotzsch. Neill 1101, 25 Oc- 

Sphyros U). Elfin forest tree. 
Pan ma majus Griseb. Atwood A11, 29 April 
MSC). = epiphyte of upper cloud 


p. Урћа ча, ~ Jacq. complex. Atwood 7744, 
omy 7. Locally common tree of elfin 


A. setosa A. Rich. Atwood & Neill AN48, 1 July 1975 
(MSC). Common weed of coffee plantation. 

Croton cf. pungens Jacq. Neill 1407, 8 February 1977 
(MSC). Tree of deciduous forest below Finca Las 


Delicias. 
E ер: cf. graminea Jacq. Narvaez 3883, 27 Јап- 
uary 1970 (MO). Common in disturbed cloud for- 


est area. 
Ricinus communis L. Dudey & Moore 1952, 9 Jan- 
uary 1969 (MO). Below upper cloud forest level. 
Sapium macrocarpum Muell. Arg. Atwood 77147 
: Va tree of cloud forest. 
FLACOURTIACEA 
Casearia corymbo. с. Atwood & Neill AN213, 
16 July 1975 (MSO). ponies shrub in deciduous 
forest near Finca Las Delic 
GESNERIACEAE 
Achimenes misera Lindl. Atwood, Marshall & Neill 
6736, 16 сеа 1973. Аррагепіу гаге їеггеѕ- 
trial on crater 
Columnea а Standl. ех Yuncker. Atwood 
D 9 April 1971 l1 Common epiphyte of 
oud and elfin fores 
Kohleria spicata (H.B. К) Oersted. Atwood 7737, 3 
ebruary 197 EF (MSC). Common € herb 
on dist orth 


flank. 
GRAMINEAE 
Arundinella deppeana Nees. Atwood A40, 30 April 
aes (MO). Common in disturbed areas at Plan 


res. 
Eleusine indica (L.) Gaertner. Dudey & Moore 1970, 
9 January 1969 (MO). Common herb of lower 

cloud forest 
Isachne arundinacea (Sw.) Griseb. Atwood A10, 29 
pril 1975 (MO, мес. Vine forming impenetra- 

ble mats in elfin fo 

Lasiacis ruscifolia (H. B. K ) Hitchc. Dudey & Moore 
948, 9 January 1969 (MO). Common in dis- 


ts. 
Oplismenus burmannii (Retz.) Beauv. Dud 
9 


15 May 1975 (MSC). Locally common in upper 
cloud and elfin forests. 
О. hirtellus (L.) Beauv. Atwood A10a, 29 April 1975 
_ (MSC). Common in elfin forest. 
Ell. Neill 868, 26 September 


76 (UCA). 

È: anus Sw. Dudey & Moore 1971, 9 January 
1969 (VT). Probably from lower cloud forest or 
pine s fo 

oo ew Berg. Robbins 6255a, 1 Au- 

972 (MO). 


P. ае m L. Seymour 7521, 6 August 1976 
(MO). depo > dominant grass in upper 
cloud and elfin 

Setaria panicula ‘Gieade!) Fourn. Atwood A360, 
10 edie 5 (MSC). Common in disturbed elfin 
forest wi 

Sporobolus ruins (L.) R. Br. Atwood A1 99, 14 May 

75 (MO). Common in disturbed elfin forest. 
Ауе 


Clusia salvinii Donn.-Sm. Atwood A311, 5 June 1975 
(MSC); Neill N222, 7 June 1975 (MSC). Very com- 
mon especially in forest where nearly solid stands 
are to be found along the most windswept ridges. 


AEMODORACEAE 
Xiphidium caeruleum Aubl. Neill 2922. Common 
herb of disturbed embankments. 
HELICONIACEAE 
Heliconia cf. collinsiana Griggs. Observed near Fin- 
ca Cut 2 le sized plant with pendulous in- 
floresc 
H. laispatha Benth. Williams & Molina 200027 (F). 
LABIA 
Н se E mociniana Benth. Atwood A185, 15 May 
1975 (MSC). Weed in open disturbed area of elfin 


orest. 
Н. verticillata Jacq. Nelson 7596, 8 August 1976 
MO). 


Salvia он Sw. Nichols 2006, 9 панн 1969 
(MO disturbed areas of cloud fore 
АНЕКС 
Ocotea veraguensis (Meisnn.) Мех. Baker 2493, 20 
February see ê (MSC). “Small tree, 20-30 ft. high 
with strong and pleasant odor . 
веле in high forests” (from Baker herbarium 
shee 
LEGUMINOSAE 
Cassia ркы f. Neill 1561, 14 March 1977. De- 
ciduous fore 
C. spectabilis DC. Neill 2723, 12 October 1977 (MO, 
ПОСА). 


паре affine 8 
1969 (УТ 
D. aff. costaricense (Schindl.) Standl. Atwood 7734, 
3 February 1977 ы SC). Occasional in disturbed 
areas of elfin fo 
D. cf. incanum DC. Neill N227, 6 June 1975 (MSC). 
Cloud 
D. sp. Neil 1005, 30 October 1976 (MSC). Lower 
cloud fo 
Gliricidia sepium (Jacq.) Steud. Neill 1565, 14 March 
1977 Мир SC). Tree cultivated for shade in coffee 
plan 
Inga Fame Willd. Neill 1406, 8 February 1977 
( . Deciduous forest tree, perhaps planted. 
Mimosa pudica L . Not collected. Common in open 
disturbed areas of cloud forest. 
Mucuna argyrophylla а ope : И 7, 19 Ѕеріет- 
ber 1976 (MSC). Cloud 
Schizolobium parahybum Pm Bl ake. Neill s.n. 
MSC). Tree of lower cloud and deciduous forest. 
LENTIBULARIACEAE 
Utricularia cf. praetermissa P. Taylor. Possibly a new 
species. Atwood A351 


hlecht. Nichols 2001, 9 January 


abundant epiphyte in cloud and elfin forest. 
LILIACEAE 
Hippeastrum cf. solandriflorum Herb. At twood A364, 
10 July 1975 "cea Probably once cultivated. 
Plan de las Flore 
Hypoxis ns L. Neill N226, 5 June 1975 
(MSC). Disturbed areas of cloud forest. Probably 
common. 
MALPIGHIACEAE 
Byrsonima crassifolia (L.) H.B.K. Neill 2640. Small 
tree of deciduous forest. 
MALVACEAE 
Hibiscus rosa-sinensis L. Atwood A191, 15 May 1975 
(MSC). Once ием at Plan de las Flores but 
now abandon 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL 71 


Pavonia rosea Schlecht. Neill 875, 26 September 1976 
(FSU). 


Sida acuta Burm. Robbins 6273, 1 August 1972 
MO). Common weed of deciduous forest. 
MARANTACEAE 
Calathea macrosepala var. macrosepala K. Schum. 
Atwood & Neill AN192, 16 July 1975 (MSC). 
риса! in | forest Чам 9f lower cloud forest. 
Maranta a ооа A357, 10 July 1975 
(MSC). Common i in pron plantations on north 
коны >. g "E 1 1 А 


9 улу 


t 


NU. 
Marcgravia brownei (Tr. & Planch.) Krug & Urban. 
Atwood A22, 29 April 1975 (MSC); Neill N223, 7 
. Common vine of elfin forest. 
E 


Arthrostema ciliata R. & P. Atwood A188, 15 May 
E E ME SC). Uncommon vine of disturbed elfin 


Cond cf. fh ысы Co & Cham.) 
G. Don. Narvaez ry 1970 (MO). 
Disturbed area of аа ps к Finca Las 

li 


De 

Clidemia o or Henriettea? Perhaps a new species. Al- 
wood A350, 10 July 1975 (MSC). Common under- 
story shrub of elfin forest. Very distinctive for its 


29 April 1975 (MSC); Atwood ATTE 15 May 1975 
(MSC). Small tree occasional at vacation house 
CUN Plan de las Flores. 
С prendo (Beurl.) Triana. Atwood & Neill 
fet hie 29 July 1975 (MSC). In deciduous forest 
w Finca Las Delicias. 

мота laevigata (L.) DC. Atwood & - ANS3, | 
July 1975 (MSC). Near Finca Cutirre in lower cloud 
orest. 

M. minutiflora DC. Atwood 3922, 27 January 1970 


M. cf. theazans (Bonpl.) Cogn. ped s 29 Де > 
1975 (MSC). Above Finca Las 
turbed areas of cloud fores 

Monochaetum deppeanum РЕТИ & Cham.) 
Naud. Atwood A173, 15 May 1975 (MSC). Com- 
mon in open areas of elfin forest. This species 
ranges north to Mexico and southward to the is 
land of Omotepe in Lake Nicaragua. 

Ossaea ee (Sw.) кте экы 783, 19 Septem 


ber 19 76 (MSC). Cloud 7, 6 
ud ee vant ) Baill. Atwood 776 adi 
Februa 7 (FSU). Common in dist 
fiet 
MELIACEAE 


Trichilia glabra L. Atwood 7745, 8 February 1977 
(MSC). Common at smaller crater rims at 
las Flores and deciduous forest. 

MENISPERMAC 


Cissampelos pareira L. Neill Меш 3 October 1976 


(MSC). Deciduous forest vi 
MOLLUGINACEAE uly 
Mollugo ites L. Atwood & Neill AN88, ee 

(MSC). Weed in open areas at Finca 
Delicias. 
MORACE 


Cecropia peltata L. Atwood & Neill AN70, 1 July 


a р aaa, Tis sone нне на 


"нт 


1984] ATWOOD—VOLCAN МОМВАСНО 205 


1975 ваја one tree nearly everywhere in 
disturbed аг 
Ficus sp. Baal i in lower cloud forest. 
MUSACEAE 
Musa paradisiaca L. Not collected but observed at 
Plan de las Flores. Undoubtedly planted 


MYRSIN 
Ardisia minor Standl. Atwood 5475, 9 April 1971 
(MO orest. 
А. nigropunctata Oerst. Neill 1331, 21 November 
1976 (FSU). 
A. oblanceolata Standl. Atwood 7749, 3 February 
1977 (MSC). 
A. revoluta H.B.K. Neill зың, 8 February 1977 
FSU). Lower cloud fores 
Rapanea cf. sn nea P "Atwood А159, 15 May 
1975 (MSC). Common elfin forest component. 
MYRTACEAE 
Eugenia oerstedeana Berg. Neill 1403, 8 February 
1977 (UCA). 


Myrcianthes fragrans (Sw.) McVaugh. Neill N225, 7 
June 1975 (MSC). Common in elfin forest. 

Psidium x hypoglaucum Standl. Atwood A160, 15 
May 1975 (MSC). In disturbed area of elfin forest 
and probably cultivated. 

Syzygium jambos (L.) Alston. Neill N21, 26 April 
1975 (MSC); Atwood AA43, 30 April 1975 (MSC). 
Near Finca Las Delicias. Probably cultivated. 

NYCTAGINACEAE 

Cryptocarpus globosus H.B.K. Dudey & Moore 1978, 
9 January 1969 (MO). 

Mirabalis ja jalapa L. Robbins 6528, 1 August 1972 
(MO); Atwood A358, 10 July 1975 (MSC). In shad- 

bout coffee plantations. 

M. violacea Heimerl. Atwood & Neill AN87, 2 July 
1975 (MSC). In deciduous forests at Finca Las 
Delicias. 

ORCHIDACEA 
Bletia florida Salish) Б. Вг. eo 77300, March 
1977 (Live collecti h B. purpurea, 
but no Постаје + were esti rve 

B. Purpurea (Тат) DC. Atwood 77160, 15 February 

hom Common i in open dry areas at Plan 


hi 
вртне подова (L.) Lindl. Not collected but not 


5 
5 
EE 
xs ax 
E 
214 
© 


st. 
Я mL. С. Rich. Atwood ie 30 
T 1975 (MSC). In dry deciduous fore 
aularthron bilamellatum (Rchb. f. ) мати ‘Neill 
1566, 14 March 1977 (SEL). Cleistogamous pop- 
ulation in deciduous forests. 
Clowesia russelliana (Hook.) D 
77135a, 10 February 1977 (Live жас iiid», 
s fores 


. Occasional in elfin forest. 
s muricata (Sw.) Lindl. Atwood A28, 29 April 
bw (MSC). Upper cloud and elfin forest. 
ms Gleason. Atwood A347, 10 July 1975 
ry similar to D. panamensis, but ovary 
8? ее Elfin forest. 
cf. tuerckheimii Schltr. Atwood A207, 14 May 


1975 (MSC). пива is sterile, but the small 
size suggests this species. Elfin forest. 

Elleanthus cf. маанаи Rchb. f. Neill N42, 29 
April eh (MSC); Atwood A184, 15 May 1975 
(MSC). Very common epiphyte of elfin forest. 

E. cynarocephals (Rchb. f.) Rchb. f. Atwood A301, 
SJ 5 (MSC); Atwood, Marshall & Neill 
6742, E Ls aires 1973 (MO). Abundant epi- 
phyte in elfin forest. 

E. graminifolius (Barb. Rodr.) Lojtnant. Atwood, 
Marshall & Neill 6743, 17 December 1973 (MO); 
Atwood e 15 May 1975 (MSC). Common in 
elfin for 

E. пала EN Rchb. f. Neill N32, 30 April 1975 
(MSC); Atwood A186, 15 May 1975 (MSC). Com- 

on in upper cloud and elfin forest. 

Encyclia chacaoensis (Rchb. f.) Dressl. & Pollard. 
Atwood A2, 27 April 1975 dosing Common in 
lower cloud and deciduous fores 

E. cochleata (L.) Dressl. Neill 1002, 3 October 1976. 
Common epiphyte in lower cloud and deciduous 
orests. 


E. fragrans (Sw.) Dress]. Atwood АЗ, 27 April 1975 
(MSC). In deciduous and lower cloud forests, but 
to be expected in elfin forest. 

E. gravida (Lindl.) Schltr. Atwood A1, 27 April 1975 

ои in deciduous forest on south- 


Е. p (val Dressl. Atwood 7756, 3 February 
1977 (SEL). Uncommon in elfin forest 


E. lacustre Lindl. Atwood, Marshall & Neill 6738, 
16 December 1973 (MO). Scattered throughout 
the elfin forest. 

E. laucheanum Rolfe. SN 5470, 9 April 1971 
(MO). Elfin forest inhabita 

E. pansamalae Schltr. Neill 885. 26 September 1977 

E 


(SEL). 
E. physodes Rchb. f. According to files of the late E 
H. Heller (now at SEL) this occurs on Mombac 
E. polyanthus Lindl. Atwood g-62. Collected Мау 
197 


E. рзеийотатозит Schltr. Atwood & Neill 7058, 20 
January 1974 (MO). Common in elfin forest. 


E. selaginella Schltr. Atwood A206, 14 May 1975 
Et Rather common locally at Plan de las Flo- 


E. turialvae Rchb. f. еб 7589, 8 August 1976 (SEL). 
u 


oodyera bradeorum tic Atwood, Neill & Mar- 

shall 6741, 16 December 1973 (MO). Local ter- 
restrial of upper cloud and elfin forests. 

ен нч lindeniana . Atwood 5462, 9 

April 1971 (MSC). Occasional i in lower cloud for- 


est. 

Н. micrantha (Lindl.) Ames & Correll. Atwood A4, 
27 April - (MSC). Common in lowland de- 
ciduous fores 

Isochilus cf. эел” Schlecht. & Cham. Atwood & 


206 


ia 7045, 15 January 1974 (MO). Common in 


Jacquiniella globosa (Jacq.) Schltr. Atwood 77166, 
rate ry 1977 (SEL). Occasional inside drier 


+. TO (Sw.) Britt. & Wils. Atwood 5460, 9 
pril 1971 (MO). Common epiphyte on lower 
flanks of mountain in deciduous кы», but found 
also in protected areas of elfin for 
Kegeliella sp. Atwoo se і : May 1975 (SEL). Rare 


iie 77161, 15 February 
1977 (SEL). Local i in elfin forest. Close to L. tur- 
ialvae, but lip lacks midlobe. 

L. sp. No. 2. Atwood 77 143, 10 February 1977 (SEL). 
Upper cloud forest. Leaves are orbicular, as with 
species No. 3, but petals are differently shaped. 

L. sp. No. 5 ee 77165, 15 February 1975 (SEL). 
“Cloud fo 

га Rchb. f. ex Krzl. Atwood 5468, 
: 2 1971 AO. Locally in cloud for 


Pre aromatica Lindl. Live collection made (SEL). 
Local in cloud forest on north flan 
L. токторду (Роерр. & Endl.) Lindl. At wood g-65, 
6 December 1973 (SEL). Upper cloud tacta Un- 
common. 
Malaxis maxonii Ames. Atwood A6, 29 April 1975 
(M 30). Common i in cloud and elfin forests е 


bacho is the type locality of the specie 

М. tipuloides (Lindl.) Kuntze. Atwood 4345, 10 July 
1975 (MSC). Upper cloud forest саре This 

may be the northernmost limit of the s 

Masdevallia chontalensis Rchb. f. Atwood P Neill 
AN305, 30 vas 1975 (MSC). Common in cloud 
and elfin fores 

M. simula Rchb. T Atwood & Neill 7042, 15 January 
1974 (MO). Apparently rare in upper cloud and 
elfin forests. 

Maxillaria brunnea Linden & Rchb. f. Atwood 7781, 
5 February 1977 (SEL). Uncommon in cloud for- 


M. crassifolia күү тв f. Atwood 7798, 8 Feb- 
on EL). Epiphyte of lower cloud forest. 

M.m Ai eos Heller ex Atwood. Atwood 7757, 
: February 1977 (SEL). Common epiphyte in elfin 

endemic to Volcán Mombacho. 

P giai Schltr.) L. O. Wms. Atwood 7782a, 5 
February 1977 (SEL). 

M. aff. reichenheimiana Rchb. f. Atwood 77159, 15 
February 1977 (SEL). 

M. tenuifolia Lindl. Atwood & ANS9, 1 July 
1975 (MSC). Lower cloud fore 

M. uncata Lindl. Atwood & Neill 7038, 15 January 
1974 (MO). Localized in areas of cloud forests. 

M. variabilis Batem. ex Lindl. Plants observed in 
cloud forest in December 1973. 

Mesospinidium warscewiczii Rchb. f. Atwood 7778, 

February 1977 (SEL). NN epiphyte in 

shade of upper cloud fores 

Mormodes sp. No collection pus. RN in decid- 
uous forest, living on rotting bran 

Nidema boothii Schltr. се, poem occasional 
epiphyte of lower cloud fores 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


Oncidium ascendens Lindl. Atwood 3917, 27 Janu- 
ary 1970 (MO). In deciduous forest around Finca 


O. stenotis Rchb. f. Atwood pee Me 1977. 
Uncommon in aad маа for 

Platystele ais cta Анан á Neill 7043, 15 
Jan s 974 mise Not uncommon in cloud 


for 
пагана blaisdelii $. Wats. Atwood & Neill 7040, 
О). Uncommon in upper cloud 
and yes forest. 
P. convallaria Schltr. Atwood, Marshall & Neill 6745, 
7 December 1973 (MO). Flowers white and 
red-purple. Found only in elfin forest on northwest 


P. cf. erinacea Rchb. f. Atwood & Neill 7063, 20 
January 1974 (SEL). Rare epiphyte in cloud forest. 
P. foliata Griseb. Atwood A12, 29 2 ril 1975 (MSC); 
Atwood A300, 5 June 1975 (MSC). Locally abun- 
dant, but = inconspicuous epiphyte of cloud and 
elfin fores 
Ames & Schweinf. Atwood & Neill 
7044, 15 January 1974 (SEL). In elfin forest. This 
is an apparent range extension from Costa Ricca. 
P. pruinosa Lindl. Atwood 77100, 8 February 1977 
| Lower cloud forest on trees above Finca 


Cu 
P. racemiflora Lindl. ex Hook. Atwood 8-63 ( (MSC). 


masses. Misi in b dei слове 
Р. ruscifolia Ta R. Br. Atwood 712 10 Feb- 
ruary 1 EL). 


р. me туы (Sw.) Sprengel. Atwood & Neill 
AN54, 1 July 1975 (MSC). Collection made north 
of Finca Cutirre at about 550 m 
P. tribuloides (Sw.) Lindl. Atwood, Marshall & Neill 
7046, 15 January 1974 (MO). Local cloud forest 
inhabitant. This species is башын for its bright 
and echinate ovari 
Polystachya masayensis Rchb. " "Atwood & Neill 
ANO, 1 Ju 1975 (MSC). In deciduous forests at 
Finca rre. 
Ponera cf. po Lindl. AQUAM 5463, 9 April 1971 
). Upper cloud fores T 
Prescottia dde (Sw.) Lindl. Atwood 77155, 
9 (SEL). Uncommon in elfin forest 
Psilochilus А, ео (Lindl.) Ames. А 
& Neill AN308, 30 n н bii 
crater rim above vacati 
Scaphyglottis behrii (Rchb, t) Benth & Hos 
Нет]. Atwood 8 February 1977 (MSC, SEL). 


Local rest. 

Sobralia hawkesii A. H. Heller. Atwood & Neill 7059. 
20 January 1974 (MO). Common epiphyte of 
and vertical cliffs. 

Spiranthes acaulis (J. E. Sm 
8 February 1977 (MSC, SEL) In lower cloud 
of Pace С Cu 

S. elata (Sw.) L. C. Rich. Atwood 77148, enin 
4ш (SEL). Rare in cloud forest. Only 


Suanhopéa wardii Lodd. ex Lindl. Atwood 77122. Xs 
рох 1977 (MSC). Uncommon in cloud 


Stell cucullata Ames. Atwood A194, 14 May 1975 


wood 77115, _ 
.) Cogn. At о. _ 


1984] 


(MSC). Common in upper cloud and elfin forests. 
Other species of Stelis undoubtedly occur on 
Mombacho. 
Т нр glumacea Garay ? Atwood A209, 18 May 
75 (MSC). One budded plant found on та 
et flank near top of a t peak. Known fro 


Cos ica and Omo tepe. 
Trichopilia sp. eec in cloud forest, but not 
wering or frui 


Trigonidium Ја зе Batem. Atwood & Neill 
AN61, D July 1975 (MSC). Common epiphyte in 


e above 
collection is sterile, but undoubtedly teste 


8 species 
D polystachya 0 Ames. Atwood & Neill 
7041, 15 January 1974 (MO). Cloud forest on 
southeast slo а УЉЕ а terrestrial. 
Xylobium elongatum (Lindl.) Hemsl. Atwood & Neill 
anuary 1974 (MO). Not uncommon in 
upper cloud forest. 


OXALIDA 


Oxalis neaei DC. Atwood A34, 30 April 1975 (MSC). 
Weed of disturbed area around bey house. 
This may be the same as the follo 

O. yucatensis Kunth. Nichols 2002, 9) iecit 1969 


PAPAVERACEAE 


Bocconia arborea S. Watson. Atwood 7743, 3 Feb- 


unam 1977 MSO. Upper cloud forest tree. 


поље име biflora Lz Lam. Atwood A33, 30 April 1975 
“ы 2 disturbed area at vacation house 

is E Neill 7506, 6 August 1976 (MO 

Probably Be | 5 


P. sexifiora а Neill 1095, 25 October 1976 (FSU). 
PEDALIA CEAE 


m indicum L. Atwood & Neill AN208, 16 


Sesamu 
July 1 jid ee zh MNA forest escape 


LAC 
Petiveria ice] За ei & Moore 1980,9 J — 
1969 (MO). Disturbed areas of cloud fore 


Phytolacca rivinoides К, unth & Bouché. Neill. N48, 
of 


29 April 1975 (MSC). Weed in disturbed area 
vacation house. 
Rr humilis L. Dudey & Moore 1981, 9 January 
969 m Cloud forest. 


Peperomia E lophylla Miq. Atwood & Neill AN94, 
2 т E (MSC). Epiphyte of 6 cloud forest 
Р deciduous fores 
ud. — & С. Nichols 2207, 9 Jan- 
р чу 1969 (M 
Ee o Neill N26, April 1975 (MSC); 
Mosen ao 30 a 1975 (MSC). Rather common 


Р. b odere (L.) A. Dietrich. Atwood 7746, 3 
bruary 1977 7 (MSC). Epiphyte of elfin n Mood 


P. serpens (Sw.) Loud. Neill N36, 29 April 1975 
(MSC). Cloud forest ep 
и адипсит L, Neill N N22, 26 April 1975 (MSC). 
PPer deciduous or lower cloud forest on south- 
^ east flank. 
amalago L. Atwood ана v Die 1975 (MSC). 
Small tree at Plan de las : 


ATWOOD—VOLCAN MOMBACHO 207 


P. auritum H.B.K. Atwood & Neill AN301, 30 July 
1975 (MSC). In ravine of lower cloud forest above 
Finca Las Delicias. 

P. pseudofuligineum C. DC. Atwood A41, 30 April 
1975 (MSC); оа & Neill AN211, 16 July 1975 
(MSC). Disturbed areas of lower cloud forest. 

P. cf. umbricola C. DC. Atwood A8, 29 April 1975 
(MSC); Neill N33, 29 April 1975 (MSC). Dis- 

area of cloud forest above 900 m 

fe pons umbellata (L.) Miq. Atwood & Neill 

с 1 July 1975 (MSC). Weedy and common 
n disturbed areas of cloud forest. 
PLUMBAGINA ACEAE 

Plumbago scandens L. Atwood & Neill AN83, 2 ч ET 

1975 ge I deciduous forest her 
POLYGALACEA 

Monnina s amat H.B.K. Atwood 5472, 9 April 
1971 (MO); Atwood A352, 10 July 1975 (MSC). 
In disturbed areas at Plan de las Flores. 

POLYGONACEAE 
Coccoloba uvifera (L.) Jacq. Atwood A45, 1 July 1975 
MSC). Cultivated plant at vacation house. 
PORTULACEAE 

Talinum cf. paniculatum (Jacq.) Gaertn. Not col- 

lected, but observed in deciduous forest areas. 
RHAMNACEAE 

Karwinskia cf. humboldtiana (R. & S.) Zucc. Atwood 
& Neill AN212, 16 July 1975 (MSC). Common 
shrub in deciduous forest below Finca Las Deli- 


cia 
ROSAC 
Rub adrocarpus Standl. & Steyerm. Atwo 
A9, 29 April 1975 (MSC); Atwood A36, 30 April 
19 Common shrub of disturbed areas 
of crater rim, orest, and cloud forest. The 


— is —l« because of the gla- 
brous drupe 
CEAE 


Borreria laevis (Lam.) Griseb. Robbins 6266, 1 Au- 
gust 1972 (MO). Common weed of disturbed area 
of vacation house. 

Coccosypselum hirsutum Bartling ex DC. Atwood 
A256, 10 July 1975 (MSC). Elfin forest па жендин 

1 Plan Flores 


Coffea arabica L. Robbins 6267, 1 August 1972 (MO). 
T. 4 A A anitivatan hist rimi t љеља 


Guettarda crispifolia Vahl. Neill 407, 28 May 1976 


Hamelia patens Jacq. Atwood A53, 30 April 1975 
(MSC). Common and perhaps dominant shrub of 
disturbed area above Finca Las Delicias 

Н. rovirosae Wernh. Robbins 6268, 1 August 1972 


(MO 

ш ocymifolia Миу ) К. Schum. Seymour 
7516, 6 August 1976 (M 

Hoffmannia oreophila L va Wms Neill N53, 29 
April 1975 (MSC). Upper d forest. 

Manettia reclinata » Neill 1 102 e October 1976 
(M. 


— angustifolia H.B.K. Hall & Bockus 7541, 
7 August 1976 (MO). Cloud forest. 
P. galeottiana Mart. Atwood A346, 10 July 1975 
a ig pui Plan de las Flores. Rather 
sii Other species of Palicourea undoubt- 
edly occur on Mombacho. 


208 


Psychotria graciflora Benth. ex Oerst. Atwood A293, 
5 June 1975 (MSC). Elfin forest component at Plan 
de las Flores. 

P. cf. minarum St. & St. Atwood, Marshall & Neill 
6735, 16 December 1973 (MO). Shrub in shade 
of upper cloud forest 

P. molinae ec Hall & Bockus 7542, 7 August 
1976. Cloud for 

P. oerstediana Standl. H Hall & weis 7572, 8 August 
1976 (MO). Upper cloud for: 

P. aff. trichotoma Mart. осм A57, 29 April 
1975 (MSC); Atwood = 18 May 1975 (MSC). 
Shrub or small tree of cloud forest. 

P. uliginosa Sw. Atwood A23, 29 April 1975 (MSC); 
Atwood A291, 5 June 1975 (MSC); Atwood & Neill 
АМ189, 16 July 1975 (MSC). Upper cloud and 
elfin forest. Purple flowered shrub of elfin forest. 

P. sp. Atwood & Neill AN216, 16 July 1975 (MSC). 
Rnadcdaind iA £ helo Finc 


Delicias. 
Richardia scabra L. Seymour 7517, 6 August 1976 
(MO). Deciduous forest wee 
SAPINDACE 
Paullinia clavigera Schlecht. Atwood & Neill AN210, 
16 July 1975 (MSC). Deciduous forest inhabitant. 
Serjania sp. Neill 1401, 6 February 1977 (FSU). De- 
ciduous forest vine. 
SAPOTACEAE 
Manilkara sp. Neill 1563a, 8 ачыры 1977 (ОСА). 
Shade tree of coffee plantat 
SCROPHULARIACEAE 
Castilleja arvensis Schlecht. & Cham. Atwood A154, 
15 pels Я (MSC). Local in disturbed area of 
elfin for 
Schlegelia pem (Oerst.) Monachino. Atwood 
47, 3 February 1977 (FSU, MSC). Common 


E 
Picramnia teapensis Tulasne. Neill 1399, 8 February 
1977 (MO). Lower cloud forest. 
SOLANACEAE 
Cestrum aurantiacum Lindl. Atwood ЕАМ 10 July 
1975 (MSC). Shrub at Plan de las Flor 
С. cf. racemosum R. & P. Atwood 77110, 5 па 
1977 (MSC). Tree of lower cloud fore 
Jaltomata procumbens (Cav.) J. L. a Neil 988, 
3 October 1976 (UCA). Lower cloud for 
Physalis cordata Mill. Neill 998, 3 Oe 1976 
). Weed of lower cone fore st. 
m Mil 


LAL? 


, | August 
1972 (MO). 
S. canense Rydb. Neill 1567, 14 March 1977 (MSC). 
Deciduous forest 
‚ & О. Narvaez 3927, 27 тн) 
1970 (MO). Disturbed areas in cloud fore 
S. torvum Sw. Atwood A38, 29 ipm 1975 (MSO. 
Disturbed area near vacation 
Witheringia cf. meiantha (Do pu 
ziker. Atwood A58, 30 ћете 1975 (мз С ува 
turbed cloud forest. 
W. solanacea L’Herit. Atwood A59, 30 April 1975 
(MSC). ppe areas near vacation house. 
STERCULIACEA 
Byttneria OR Jacq. Neill 774, 19 September 
1977 (UCA). 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


Melochia nodiflora Sw. Dudey & Moore 1953, 9 Jan- 
1969 (VT). 


Sterculia apetala (Jacq.) Karst. Atwood & Neill AN76, 
2 July 1975 (MSC). Deciduous forest tree. 
THEACEAE 
Freziera friedrichstaliana iu Kobuski. Atwood 
5 May 1975 (MSC). Elfin forest compo- 
nent. “Known only from Honduras and Volcan 
Mombacho. 
TILIACEAE 
Apeiba tibourou Aubl. Atwood & Neill AN215, 16 
July 1975 (MSC). Deciduous forest inhabitant. 
Heliocarpus donnell-smithii Rose. Baker 2490 (MSC). 
Reported by Lay (1949). 
H: — Donn.-Sm. & Rose. Oersted 14829. 
Cited by Lay (1949). Tree of secondary growth. 
Е m Baker 2311 (MSC). Probably i in decid- 
uou 
Prieta SUE РАК Schlecht. Dudey & Moore 
5,9 m 1969 (MO). Cloud forest. 
UMS 254 
Trema n (L.) Blume. Neill 1300 3 Еергџагу 
1977 (FSU). Deciduous forest tr 
UMBELLIFERAE 
Eryngium о mL. Robbins 6259, 1 August 1972 
Da mmon in disturbed areas of lower cloud 


for 
Spananthe paniculata Jacq. Atwood. 5474, 9 An 
1971 (MO). Lower cloud forest in disturbed ar 

URTICACEAE 
F M aestuans (L.) Gaud. Dudey & Moore 1975, 
са (MO). Common herb in cofee 


скала 
си зр. pow collected but common in coffee plan- 


ns. 
VAL RIA ANACEAE 
Valeriana scandens var. candolleana (Gard.) Muell. 
Atwood A47, 30 April 1975 (MSC). Weed of coffee 
i and disturbed cloud forest on п north 


VERBENACEAE 
Cornutia grandiflora (Schlecht. & Cham. 
wood & Neill AN79, 2 drag 1975 ap 
uous forest areas at Finca Las Delici 
Lantana унет tp pes uS. & Moore 
1958, 9 Jan 19 


) Schau. At- 
In decid- 


у 

ma H m ue Seymour 6104, 25 July 1972 
(MO). Lower cloud fore 
Б. — hirsuta Moldenke Atwood A355, 10 July 
5 (MSC). Roadside in lower cloud forest. 
Lippia cardiostegia Benth. Nels ч 7510, 8 August 
1976 (MO). Lower cloud fore » 

L. controversa var. bre podia Moldenke. 
wood A202, 14 May 1975 — Cole o": 


Priva ipei (L.) Pers Dudey & 
January 1969 (MO). Cloud forest weed. 
VIOLACEAE — K 
Hybanthus attenuatus (Humb. & Bonpl.) G. 
Schulze. Atwood & Neill AN73, 2 July 1 1975 (MSC) 
£s : к t 


кк 


forest. 
observed 


Vitis Pe Humb. & Bonpl. Sterile vines c Mol 


wer cloud forest areas, south side О 
cho. 


= 


1984] 


ZINGIBERACEAE 
Renealmia атотапса (Aubl.) Griseb. Atwood, Mar- 
shall & Neill 6711, 15 December 1973 (MO). Only 
one plant found in elfin forest. 


LITERATURE CITED 


ALVAREZ DEL CASTILLO, C. 1976. Estudio ecologico 
y floristico del crater del Volcan San Martin Tuxla. 
Thesis. Universidad Nacional Autonoma de Mex- 
ico, Mexico. 

Ames, O. 1923. New or noteworthy orchids. Sche- 
dulae Orchidianae 6: 36. 

Additions to the ана flora of tropical 
America. Schedulae Orchidian i 

соор Deutsche Biographie. ћи Duncker and 
Humblot, Leipzig. Volume 8: 68. 

BAYNTON, Н. W. 1969. The ecology of an elfin forest 

erto Rico. Part 3. J. Arnold Arbor. 50: 80- 


— m 


BEARD, J. S. 1942 


. Montane vegetation in the An- 
tilles. an 1- —74. 


Forest. 3: 


19. The vegetation of Philippine 
monn untains. The relation between en پو ا‎ ment an 
i. Publ., 


Man 13. 


бы А M. 1906. American Men of Science— A 


Biographical > Edition 1. The Science 
ss, New ч 
CHAUDHRI, М. N., VEGTER & C. M. DE WAL. 


"p 
ns Index I eu Part II(3). керий Veg. 


СКАВВЕ, J. А. A. C. JERMY & J. T. MICKEL. 1975. A 
new are sequence for the pteridophyte her- 

az. 11: 141-162. 
CRAWFORD, E "1902. List of the most important vol- 
ic eruptions and earthquakes in western Nic- 
aragua within historic times. Amer. Geol. 30: 111- 


Cronauisr A. 1968. The Evolution and Classifica- 
З | бат Plants. Houghton Mifflin Com- 


dii А А. М. 1969. The ecology of an elfin forest in 


ATWOOD- VOLCÁN MOMBACHO 


209 


Puerto Rico. Part 6. J. Arnold Arbor. 50: 197- 
09 


209. 
GOYENA, M. R. 1909, 1911. Flora Nicaraguense, Vol- 
: Biologia Centrali-Americana. 
Appe ndix: : a sketch of the history of the botanical 
ipd of Mexico and Central America. Bot- 
7-137. 


HOWARD, R. A. 1968. The ecology of an elfin forest 
in Puerto Rico. Part 1. J. Arnold Arbor. 49: 381- 
8 


Я шеше The — of an elfin forest in Puerto 
art 8. J. Arnold Arbor. 50: 225-267. 

eee 1. dens Geografia agen de od tipa Li- 
breria y Editorial Reca A. Managua 

Konuski, C. E. 1941. pek on the <p 8. А 
synopsis of the genus Freziera. J. Arnold Arbor. 
22: 471-472. 

Lay, K.K. 1949. Arevision ofthe genus Heliocarpus. 
Ann. Missouri Bot. Gard. 36: 507-541. 

3. El Habla Nicaraguense. Educa, 


MANTICA, C. 
Salvador. 

MELINA, A. 1975. Enumeracion de las plantas de 

Honduras. Ceiba 19: 1– 

Mooser, F., Н. MEUER-ABICH & А. R. MCBIRNEY. 
1958. ане of the eed Hopon of the world 
including solfatara fie с International 
Vulcanological рй yp d 

OBERLANDER, G. T Summer i precipitation 
on the San Francisco Peninsula. Ecology 37: 851— 


852. 

STANDLEY, P. C. & L. О. WILLIAMS. 1961. 
Guatemala. Part 7. Fieldiana, Bot. 24: 3 

SrEENIS, С. С. С. J. VAN. 1972. The mountain flora 
of Java. E. J. Brill, Leiden 

PRAES, A. N, 1973; Introduction to гоні. Ge- 
ography. John Wiley & Sons, Inc., New 

TWoMEY, S 1957. Precipitation by direct Liha 
tion of cloud water. Weather 12: 120-122. 

VOGELMANN, H. 1973. Fog precipitation in the 
cloud forests of eastern Mexico. BioScience 23: 
96-100. 


Flora of 
0. 


—, Т. 51ССАМА, D. Leepy & D. C. Оупт. 1968. 
Precipitation from fog moisture in the Green 
Mountains of Vermont. Ecology 49: 1205-1207. 


AN INDEX TO THE FAMILIES IN ENGLER AND PRANTL’S 
“DIE NATURLICHEN PFLANZENFAMILIEN”! 


THOMAS MORLEY? 


While teaching a course in the families of flow- 
ering plants over a period of many years much 
use was made of Engler and Prantl’s publication, 
“Die Natürlichen Pflanzenfamilien.”’ Ultimately 
it was found useful to compile an index to both 
editions ofthis great work. Families of non-flow- 
ering plants were added with the thought of mak- 
ing the index of general utility. The index is com- 
plete for the first edition and includes all presently 


The following abbreviations are used in the first edition: T — Teil €: PENE Ab = Abteilung (division, 
nd N = Nachträge (supplement). N PN 2; 4 are the four 


sometimes also further subdivided); a 


published numbers of the second, namely: Band 
Ib, 2, 3, Sal, SbVIII, 6, 7a, 8, 10, 11, 13, 14a, 
14d, 14e, 15a, 16b, 16c, 17aH, 17b, 18a, 19a, 
1951, 19c, 20b, 20d, and 21. According to Dr. 
F. A. Stafleu (pers. comm.), further progress with 
edition two is very slow and it is not at all certain 
if any other treatments will ever appear. There- 
fore it seems worthwhile to bring out this index 
at the present time. 


supplements to Т 2—4. The following abbreviation is used in the second PUR Bd = Band (volume). 


Taxon Ist edition 2nd edition 
ЛИ е 
АСПИ Е T 4, ae oe Pie N 1:304; N 2:71: N 3: 
321; N 4:2 
Acarosporaceae I T 1, Ab in Ар иу M Ва 8:213. 
ӨЛГӨН ...... | - : E 5 5:203 N AIDEN 3:202: 
Achariaceae a. N a я Bd 21:507. 
ACNWIDONDAGÉÁO н и Ва 16c:174. 
Achnanthaceae:.... c 2 е УУ м n ИЕ Bd 2:269. 
стоврептасеае,... css геру и, T1-^AbI 
Астордасеаё:........, o = ТІ, Ab 2. is N to T 1, Ab 2:216. 
Actinidiaceae... <.. oon „секу ал „= UEM = ни Bd 21:36 
Або 1 sS T 4, Ab 4:170, 190; N 1:316; N 3:332; N 
Agaricaceae о Е T L Ab PO  " и Bd 6:210; 
see Bd 5al. 
Aizoacbée т Т 3, Ab 1b:33; N 1:156; М 2:20; М 3:106; Bd 16c:179. 
784 
Akaniachié 1... у с TS £192. yS Bd 19bI:173. 
dee 1. n = Ea Ab ТЕТ 
Alangiaceae: o 1, N 4:213. 
Albuginacelé ... се с .. T 1, Ab 1:110. 
рс. see Alismataceae. 
Alismataceae н T 2, Ab 1:227; N 1:38; N 2:2; N 3:9; N 4: 
Amaranthacese 65.4 Т 3, Ab 1a:91; N 1:151; N 2:20; N 3:103; Ва 1627. 
AmaMBNEM . . — 91 Т 2, Ab 5:97; N 1:77; N 2:11; N 3:48; М Ва 152:391. 
4:37. 
Amauochasaebée .............ф....ф..ф.. d ou i i 2:321 
Amblystegiaceae... esso у пе o Са ee Bd 11:332 
Ampelidaceae — see Vitaceae 
hiotaome s. se ee ооо Bd 2:68 
Amphilothales .............. s кесе. a у oen Bd 2:68 
трМшопайасеае ,.. 1... T 1, Ab 1a:137 


; Veiis costs have been supported in part by the Hayden Fund of the Botany Department, Universit? 


of Minneso 


? Botany D 220 Bioscience Center, University of Minnesota, St. Paul, Minnesota 55108. 


ANN. Missouri Bor. GARD. 71: 210-228. 1984. 


ie el 4 


1984] MORLEY —INDEX TO ENGLER AND PRANTL 
RE ea as i ed ул Л ee er ee ee Bd 2:77 
amusbbaeriaceae . ... eck а Pe 1-1; Ab 1413: 
ПН. ата. Т 3, Ab 5: 138, 458; N 1:213; N 2:38; N 
3:196; N 4:185. 

NN Se и T 3, Ab 6: 274; ы 1258. N $236 ........ Ва 21:589. 
200 OMünp ___ лл - = E TIL AD UGG К Т НЕ ин see Bd Sal. 
EM ли T 1, Ab 1:88 

20 0 МОК у. му ызуу... V Ab3253 о E Bd 10:129 
o сољу ва TGhoAD.E252 6. 0 ox le res TE Bd 10:126 
Andreaeales, pow. PEE И хс о аксе. Bd 11:523 
Angiospermae, Sencral o 3 И THAU PDS 1... .v V A Luv Bd 14a. 
РОИ Ta Ab 2:23; М 1:159; N 3:112; N 4:89.. Ва 17аП:1. 
EE са IJ, АБ 3:135. 


Aphanochaeta ede ye ee me A МАО РУКА ЊУ ОЗ Genes ee у... Bd 3:235. 


mae о тИ Т 2, Ab 1:218; N 4:7. 
Ате NE C S UB VA T 3, Ab 5:183; N 1:217; N 3:197 ........ Bd 20b:36. 
0 oe EE | <= | T 2, Ab 3:102; N 1:58; N 2:8; N 3:29: N 
4:27. 
EE o. уу... OA ee у... Bd 7a:55; 
à see Bd Sal. 
EE o o uuu ss svn T 3, Ab 8:1; N 1:268; N 3:253; N 4:217 
BEENDEN uo to МЕ EU Ме Iu. Bd 13:249. 
И >. > ов к е и ДАНЕ e essen Bd 10:155 
aaa ТОНИ S S s vessel 2:334. 
а ИО ОЕ Т 3, Ab 1:264; N 1:150; М 2:19; N 3:100; Ва 16b:204. 
N 4:78. 
А оиа ОРИ о а о ek Ва 16:3. 
е TIS. с Ваве. 
Акира, INED OS D ава ко T 4, Ab 2:189; N 1:285; N 2:60; N 3:300. 
о ОТНЕ НЕ ОВИ АВИИ S ес es ss зее Ва 5а1. 
EE i iV V Von T 1, Ab 1:161 
ЭМА S S Ln T 1, Ab 1:145. 
Ascolichenes нажа сен ур г Erud "aio c s. оа Bd 8:61 
ene... CES Л л ср АО у... .... у... see Bd Sal 
Asperlfoliaccae — see Boraginaceae. 
EN ЈЕ ИЕ Т 1, Ab 1a:177 
Astothliaeae e ee e КОЛЛ у у; eee 8:85 
00 у | пл УУ о. E di vents ва 2:36 
oo: ee oe т о о . . o ess Bd 10:440 
МИ ы МИНИ НИНА ee Ва 6:105 
PS у — T 1, Ab 1**:82. 
И у: T 1, Ab 1**:24. 
a 1: ae T 1, Ab 1b:31. 
AMEN. s. SUUS T 1, Ab 1b:31. 
IG ae S ........... Bd 2:105. 
ОЕ —— —  — É T 1, Ab 1a:20. 
боа e T 3. Ab 1:243; N 1:149; N 2:19; N 3:99; Bd 16b:296. 
4:76. 
Жы .... Ce н. Bd 16b:4. 
Balanopsidaceae qc c TE M E N 1:114; N 4:63. 
BEEN. o 5 T 1, Ab 1:288; T 3, Ab 5:383; N 3:210; N 
i T1 T 1, Ab 2:191. 
NT у iu T 1, Ab 2:307; N to 
partramíaceae Р Ое. ИЕ аа Ва 10:447. 
оон осоки МР КЛЕ КМ 3:105................ Ва 16с:263. 
ШИ. 0 |. ...... see Bd Sal. 
pisidiomycetes (aa PR TCI Ti- 1, 
ENEMME.. ee T 3, Ab 16118; N 3:105 
Beggiatoaceae ОО tou cU p ан а ТЕ а:41. 
Bego Bd 21:548. 


E. SS SE SITE T 3, Ab 6a:121; EM |... 
Bennettitaceae N 1:14; N Bd 13:87. 


"UC? АВИИ ROO WR PR REOS ek кои a DIESEL T НОСИ a a a ge ee 8 
e et ве a a a ee Жө da ЖЧ Ана сео си и 


212 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


Berberidaces@ic2 35. oy. ay eee deut T 3, Ab 2:70; N 1:170; N 3:122; N 4:92. 
Betulaceae |... с а ак = Т 3, Ab 1:38; N 1:117; N 2:17; М 3:95. 
Вісоесаседе сат, е TRAD 13:121: 
Biddulphiastéé.... rv oa rion QUEDA PM EBEN ее еен оет Еи 
Bignoniaceae 250... i... ee a T 4, Ab 3b:189; N 1:301; N 3:320; N 4: 
E es NOR ML ы CE а ЗАВЕО ВЕНЕ ЗА и 
Biastocladiaceac EOE UA E E MEG E eee TE 
Blasigainincene ee ИИА er 
Bl DOM B os чыке UN CEL AD2Z/3. ы dc 
BlattiacéaB. io ee em а T3, Ab 7: ui A 1:261 
Водопасеве (Зове RULES ТІ, Ab 1 
Војењсеве у 1 005 у па Vices Е EUM а а а qu E 
Bombacetes@. а r A A. 6:53; N 1:240; N 2:42; N 3:214; 
заи аен и د‎ 2: 417; N to T 1, Ab 2:239. 
Boraginaceae паса cere rtr vp Vt T4, Ab 3a:71, 377; N 1:289; N 2:63; N 3: 
306; N 4:265. 
Borzinematacene: o uo lov mo UT I ow II Ре Рат OU I D uU ee ee а 
Bothrodendraceae и с 55 T 1, Ab 4:739. 
Botrydiacedé а она на THADEI i as is dur оно As 
Вотуососсаседе. creat NOTLA 2:05 $1. 385. X LS 
Brachyonsidiacese а ee DUOC dci dei lupi E teu d c EE 
Brachytheciaceae... се с ae ба Tq At E а ен се те 
Breteldinceae АИ ЕРЕ TI Ab 1:28: 
Bretschneidetracese е SS 
Bromeliaceae — |... ss T 2, Ab 4:32; ir 1:61; № 3:41; N 4:31. 
Bruneliacess: a А DEE TR МАТЕ ce Aas es 
Bruniacene Е РА улу а Pese e N 3:142; N 4: 
Breen aii ir 3. 

COR o E iu e uod. ЧАЮ 32532) A о ти 
Bryales oo ses ee Se TI АБ IOR . . . 2 12 
ЕЕ Е КАВНЈЕ N to ТУ АВ 2:124 у... 
ВгуохйрМмасеас............у...у...1...5 о 000 25 у 
Вие асеве i o хм T IAD „злс Фр 0 АНЕ 
BIHARAN | о T 2, Ab 6:44; N 1:96; N 3:72; М 4:41. 
Burseracgene c ks re LEM ES. vro N 1:208; N 2:36; N 3:188; 
Butomacéab |... |... S o ee T + ies 1:232; NOD38:N ZEN SIEN 
Buxacede - -. |... = ууу a Т 3, Ab 5:130; N 1:213; N 2:38; N 3:195; 

N 4:185. 
Вухраштјасеве с... e oS TRAD S664 o 
Вихбашпшез..........;............... ee uos 
Вуһдасеас........................... ооо =. _ 
Вумојотасеве.....:.. оси густини ооо и 
Cactaceae ............‚.... ee Т 3, Ab 6a:156; N 1:258; N 2:47; N 3: 
237; N 4:208. 
Calamariacesé ............. у 0 T 1, Ab 4:551. 
Calamopityaceae ...... suco d. Dos ae a ae о у ET 

заседе cl TN cL ЧОТО ON у... 
Callitrichaceae -...... 2 КЕ АБУ МЕЛ у. 

alomniaceae 2 X TRAD IOG 0. o o ooo 
Caloplacaceae ...... и л = a. T huh 1 TT 
Calostomataceae а. TL ABT, ll у. 
Calycanthaccáe о. T3, Ab 2:02; N 1:172 
CalymperaceBé |... o ev = TEA ZII HAM ар 
Calyceracese’ о. T 4, Ab 5:84; N 

panulacesé® ...;.................... Hh Ab 5: 40, 394: N 1: 319 N 2:78 NX 
Camptotrichaceae ........... E xi T 1, Ab 1а:90. 


Candolléactae |... o so oss = T 4, Ab 5:79. 


(Мог. 71 


Ва 2:233. 


Bd 21:313; 
see Bd Sal. 
Bd 2:54. 
Bd 3:178. 


see Bd Sal. 


see Bd Sal. 


Bd 19a:405. 


Bd 11:487. 
Bd 11:487. 


Bd 18a:286. 
Bd 8:133. 


Bd 21:594. 


E C — o — — P КП 


ae mme 


~ 


a. ow 


ње 


Lo. - 


——— HOÀ 


1984] MORLEY —INDEX TO ENGLER AND PRANTL 
оТ ОТИУИ T olde prt M Ри Ое 
Coon E аса REEL T2 ARGO Dd sss eer 
don: CIT due cM EUN T 3, Ab 2:209; N 1:177; N 2:28; N 3:134; 
N 4:105. 
ESSE URINE SUEDE ИАР T 4, Ab 4:156; N 1:316; N 3:330; N 4: 
301. 
000 oer c d aut UE M M ME 
Bra Lbs Ж а THAT. s T3, Ab OE М 1:297; М 3233 ........ 
RR насенная E ННВ КО АЕ ee Sao eters 
po eee til EE рз D DU T 3, Ab 1b:61; N 1:156; N 2:21; N 3:106; 
N 4: 
СРИВ v reno rena T3: Ab 1: | М 1113: N 3:92. 
Пе os ghia yn dad БОА ууу rro 
Oe ee ee T 1, Ab 2: а NGILADZUS.—.. 
о ОТОО erg о л, Па REMO. ee aser ie are sole eese 
СЕКИ ТО PERO Т 3, Ab 5:189, 459; N 1:221; N 2:39; N 
3:198; М 4:186. 
ОИЕ MMC + As ee 
EE л у е nda ELE 
ИИА. Ta М 2 LI; me CONCISE eae ke cs 
EE eee ud c I РОУ РИО 
ME у у у. лм ТЗ Ab 283 МУНО... 
NT а а DN NEST E cere c T 
ПА з, а А АРА е c cr Face re e 
ПИПИНА се о ге а T 1, Ab 2:481; N to T 1, Ab 2:246 
ООРОО л ye are are oak РА ee 
END... he REGE ЕМА КЕ erg ne ym 
ПА ae ey з CEOs та РИСА 
ПИПИН сл ух T 1, Ab 1:405. 
MEN 7 уу. T 3, Ab 2:10; N 3:107. 
ore T 1, Ab 2:335; N to T 1, Ab 2:211. 
E a И т И oo sm 
Ас Т 1, Ab 1:131 
США гае... ш, ул... МАУ ЛЫ | ess 
н irn ne T 1, Ab 2:86, 160; N to T 1, Ab 2:75 . 
А —— — . — ree emt 
EN. е TI ДЫ л terms 
MET S lun T 1 Ab 2:161; N to T 1, Ab 2:135 B 
ZEN ш о о ПН vsus ORAE EMILE teme 
ИИК з 1; T3, Ab 12:36; N 1:151; N 3: 102, N 4:81. 
соо ......‚. у тл О. o v nnn 
quM “Wee oT se c E ae T 3, Ab 6: de 
ydobacteria: 
mm ел... 
mon Але aD M MA UE UE T.3, Ab E12 
Не LO еи 
eG С а ee a D SUE уйд ОО 
Chloromonadineae ..................... T 1, Ab 1a:170. 
So, о. T 1, Ab 2:24, 159; N to T 1, Ab 2:1. 
Chlorosphaeraceae ..................... en Oe a 
sS ll ee emen 
ЭО кен... oto Xo T 1, Ab 1:131. 
RE One re Pe ST T 1, Ab 2:221; N to T 1, Ab 2:163. 
Choristocarpacege ....................-- T 1 Ab 2:190; N to T 1, Ab 2:145. 
qu c m HU TE T И о се. Or eee a 
Crroolepidaceae Atte Giri N to T 1, Ab 2:92 
Шлем о T 1, Ab 1a:153 
Chrysomonadineae ...................-- T 1, Ab la:151. 
Qurysothricacea Be i ie Шушы pe OS. 
е Т 1, Ab 1:64. 
DENN E л лил T 3, Ab 6:299; № 1:251; N 3:228 ........ 
Cladochytriaceae uc су .. El oov 
ope у, сос TIME у... 


Bd 21:323; 
17а1'221. 

Ва 15а:640. 
Ва 175:146. 


Bd 1b:118. 
Bd 21:510. 

Bd 16c:275, 365. 
Bd 10:445. 

Bd 3:301. 


Bd 13:98. 
Bd 20b:87. 


Bd 1b:38. 


Bd 8:134. 
Bd 21:289. 


214 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


Cladophoraceae: л олуш ERIS T Abe Мо ВБ АВ ог са: 
(e hus. -. ......... uu MN виа реј титана пуке таи 
СТОПУ ees sus TDI TO ee Беине ин 
Clathracsae 0. НО PIS ОТАРИ О cl o oe v rec E 
icc tenga AT dart E Rs T 1, Ab 1:18 
CIBVADHOOHÉ oe ee a ae a os T At FIO S о a Sa oe res 
CISNE UM r ата ABTI, 
CUE АКП N ТТАР 37A os Ba es a a д 
Слурориринстиеве. cee ces eee T 1, Ab 1:451 
Спескабене и и ak T 3, Ab x M N DAN 3:186 V ee 
СООО у. у ки tei T 1, Ab 14:14. 
СООЛ АЕ ТО, у а E T 1, Ab ni 50. 
COChIOSDETHRCERB oe SR ee UE EA TP MR A: 
pede o а оа а T 1:Ab2:138;: 010 T КАРЕН Те 
Cosingiatese oo oV ес ,. N to T 1, О 
CO OOD OEE LAT TA es зу ee eas 
СООО у таа NW to TL Abo 105-255. 
(е гв уяту е 08 Co a ey T 1, Ab 1**:548. 
(galline. ep у у NE ee ТРАСТ 168 И 
COIGQEITDBEORMT oL essor iir veo можу a ууш о л з у 
COMMGIIACERO О... iis ЕР А мш, T 4, Ab 3b:186; М 3:320. 
СОО so ee ee T 3, Ab 7:106; N 1:262; N 3:240; N 4: 
Commelinaceae е ee T 2. Ab 4:60; N 1:69; N 2:9; N 3:42; N 4: 
Composit >... па eee ЈЕ 4, Ab 5:87, 387; М 1:320; М 3:337; М 
4:315. 
n: MM, noc cuu T 1, Ab 2:318; N to T 1, Ab 2:197. 
Cone i.e a c T 2; па ве + То уруу ро er 
Coniferae, Fossil ........... и ee ee DL ма. не со e e 
Coniocarpinae@e sS Чч ы OO oc. са о усу с у 
Coniisatas s eese oe а | s АВНЕ А АБ: 
Connaraceae Ио. T 3, Ab 3:61; N 1:189; N 2:30; N 4:117. 
Convolvalactae ..;..... Ser o T 4, Ab 3a:1, 375; N 1:288; N 2:63; N 3: 
304; N 4 4:260. 
MICE ooo Оре а ETIN AM EM M NI Ne ET 
Corallinaceae - = oe е T 1, Ab 2: owl N to 1 1, АБ 7257. 
огданасево л у ee ТАЮ И .: C ONT тулу UNIS 
Cordierttidacese. ll Ж, AD 19 
Coriaria TRI T 3, Ab 5: 128: N 1:213, 
Comaceab lo T 3, Ab 8:250; N 2:52; N 3:265; N 4:231. 
Co АСА ее eoe eee asesino) сое = <= ee 
Согупенареве о TEL 1:411 
КУПОСИТРАБЕЋЕ иеа МЕЛЕ МУИ 1 у. 
Crespedomondadiaceae ..::::...:.......:: T 1, Ab 1a:123. 
СТЕМИ ос осе , Ab 2a:23; N 1:180; N 2:28; N 3:138; 
:108. 
CIDA ...........;..... г], PU. uci INA у у у. NS 
Cbr Eoo oe ooo eeu eee SS 
СТОЛДОР o Soo л. TLNEPTEME V esas 
CINE ..........................., T 2 Ab ae jas N 1:175; N 2:27; N 3:130; 
Стомовопинасеве ......... a 
СҮТҮМ... ду у. о... T Ab Таб; РА LN c T С 
СтуюшШеласеве........................ ONU у 
ск re T L AD la: 
СОИ, ТАБ У. М 2:75; N 3: 
; 333; № 4: 307. 
CUOI EUN ....................... T 1, Ab 1:408. 
СИМОИ Sasi T 3, Ab 2a: 96 N CISA; МА. 
Cupretéace e ..................@........ DUET iu Du 
СИНИМ ое т 5. Ab 2:262; N to T 1, Ab 2:177. 
Cyanastraceae 


тестов вове вооа 46 web 5 À Ab 


пе теже тежини еони сетат a Ж 


(Мог. 71 


Ва 6:151; 
see Ва Sal. 


Bd 11:64. 


Bd 19a:184. 


Bd 21:316. 


Bd 15a:159. 


Bd 13:121. 


see Bd Sal. 
Bd 13:112. 


see Bd Sal. 
Bd 20b:22. 


Bd 18a:352. 


see Bd Sal. 
Bd 17b:227. 


Bd 11:75. 
Bd 1b:223. 


ва 18а:229. 
Ва 13:361. 


Bd 15а:188. 


алаан. 


pee mo 


м 


bens 


1984] MORLEY —INDEX TO ENGLER AND PRANTL 


ESET a Te eee QD РОТ Bd 1b:102. 
CE rer ee T 1, Ab 4:113, 138. 

EE S сус е T ee EP WT с... Bd 13:44. 
EE M Verres ОРИ У Иек" Ва 13:5. 
— — Cil eb E M Tr ы О ска Bd 13:19. 
EM S he T 2, Ab 3:93; N 1:58; N 3:28. 

ENE IN REEL M MEE TL ABIDE. л Лр чууру... ва 8:128. 
КИ оснидаселе......... os VO uel T 1, Ab 2:106; N to T 1, Ab 2:106 ...... Bd 3:242. 
ocrambaceae — see Thelygonaceae 
ОРОСООР КИЕ N 1:268; N 3:253. 
ННН Т 2, Ab 2:98; N 1:47; N 2:7; N 3:22; N 4: 
An 
ПИ ace, UA od TIL уйна Ше Up I IT i Cher see Bd 5al. 
EE o ever TRADI A ir eee Bd 8:98. 
Па ја ЗРЕЛЕ ee ва 205:1. 
EE pie e TIENES ss Bd 11:99. 
EEUU — . .. ...— ... (CUu ON V A а Doa EE S Eh see Bd 5aI 
Поа Т 1, АЂ 1:241. 
o ар М е н ОА Ва 19¢:233. 
Décryomycetaceae. e sees bie, s. x з у... Bd 6:119; 
see Bd 5al. 
nune ол ee oe Т T 1, Ab 1**:96. 
eee T 1, Ab 2:152; N to T 1, Ab 2:119 ...... Bd 3:282. 
ue г. EM o 221 iu TRAVE М 1288... sese Bd 21:543. 
ES  . . TUI MEE T Qoo с. Bd 11:520. 
ПИПИН V V V Vue Т. А672: 406; N to T 1, Ab 2:229. 
ШИ и... ie се нестане ena тые енене. see Bd Sal. 
mus pee Кү у ee T 1, Ab 2: 129: N to T 1, Ab 2:126 ...... Bd 3:323. 
ool eme dq uM quc c pU QU see Bd Sal 
RS —. .  .... Tip dB м а Ero 8:70. 
~ COR CAE ORE SR РИМА ПРЕ a ee ee PLUME Bd 1b:104. 
ИО ао Ва 1:101. 
EE uu s sss T 1, Ab 2:209; N to T 1, Ab 2:160. 
| ERE s S SS Ss T 1, Ab 2:1, 159: N to T 1, Ар 256 ...... Bd 3:340. 
eae жоо, AI UI T 4, Ab 1:80; N 1:270; N 4:235. 
Di ОТОС ве и TLAbLA o ee see Bd Sal 
bee ы ыу M de А T 1, Ab 1:270 
eee... о оо Т 3, Ab 4:345; М 1:210; М 3:190; N 4 Ва 19с:1 
164 
ЛА ы. >и + ет ү ee ва 10:214. 
рустапассае equ cc ru c T mU Ti ABT ae ae -.............. Bd 10:172. 
bia a emp сы uU T 1, Ab 2:212; N to Т 1, Ab 2:161. 
re ee T 1, Ab 1:4. 
бы Ts Т 1, Ab 2:291; N to T 1, Ab 2:185. 
ee, Ss. ce со о. С. Ва 2:331. 
о О ОН T 3, Ab 6:100; М 1:245; М 2:43; № 3:218; Ва 21:7. 
N 4:203. 
ОА Ва 2:73. 
ZEE" O Bd 2:72. 
inosphaeracea, у du s v uu c ME E а на mene hare ek y enn Bd 2:84. 
"EMEND. _______ _ Т 2, Ab 5:130; N 1:80; N 2:11; № 3:49; N Ва 15a:438. 
Diphysciacese |... P Ed oue у '" Bd 11:489. 
"MN. o crore НД сео :140. 
~ ыо pg О аен see Bd Sal. 
а ОО. Т 4, Ab 4:182; N 1:317; N 3:332; N 4 
oo ee cn 13. Ab 6:243; N 1:250; N 2:45; N 3227 .. Ва 21:237. 
ae... — — TEMPI eere 8:122. 
Caren lu, CCC ом LM 
TU osx ce e Ta eS 10:316. 
ИН |. — . . T 1, Ab 1a:147. 


Lo —.— — 3 — T 1, Ab 1a:147. 
Ditrichaceae Bd 10:157. 


о. apse poe as ca a. lla ecu eee oe үзүн. ee Под и we eee Oe ШЕ ЭШ ЖШ Ж ШАР Щ А А МАШ 
аот ele ee ae а ee ве же ват ет" 


216 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


ројтонни нове. sk ушу ee ac T2 Ab 1:27. 
Dothidesatese ‚ууз ne CE nes АИТ со 
Doi. A eese rcc Ead T HABITA 
Dothioracéab 29 1... ос Ана Е ee ce ences 
DE ug D E Tq AB РА o o ee e 
E с ке Б cem Т 3, Ab 2:261; N 1:179; N 3:134; N 4: 
DumonBWacBae Уо T 1: Ab 2:515; N to T 1, Ab 2:252. 
Dyspheniacede ee ERES oe. a aes cows s ocio dad CER. 4 
Ebenacéab оа T 4, Ab 1:153; N 1:280; N 3:289. 
Echinodiacene <<) O Уа не РАДНА S у о eee 
Echiniostelincese у. зуу, лгу р лы а ае 
Кабсапио а у уз у оса го. TE ke Ap 22182 N to Т 1; Ab 2:139. 
Fctolechinvsse o. oso do hoses TEAD OT o eo nr eee 
Elachistacen@ |... СИ ree IIT T 1, Ab 2:216; N to T 1, Ab 2:162. 
puc Uo И T 3, Ab 6a:246; N 1:260; М 4:212. 
Elaeccarpacese:. с с. расе и сите Т 3, Ab 6:1; М 1:230. 
Blanbomvyoswncene з... eoe ries T КАШИ АРА РАВНЕ РОА АКО СОЉУ 
Elatinacese: S ес vo dde ies T 34 AGUET N B250 ти а vus 
ЕОНИ еее, ‘PE SAD 5:173; 
ЕСТУ аена СЕ О рис и 
КСО esee эу ES T 1, Ab 2:197; N to T 1, Ab 2:154 
Епдопопбба ooo a ELLEN с OILS LI UOI. о гл санке TACNA 
ЕСОН. ОРОО, Iesu a шы. 
БОДоР Ин ее е Т1 А5123. 
Брена Јев ee едо 
Рпїйдо ове... -- с ас ТИИТ ШЗ о. се okt ace 
tomophithioráeceae ...... ss e АЮ ОКО TECLAS es 
Eton. kos снесе T 1, Ab 1:134. 
Entophysali ален НАВОИ eles 
МИИ е Т 4, Ab 1:66; N 2:53; N 3:267. 
Eba E eae Aye NM UEM Ж Ah SOA ас Se ed 
Ephedraceae: ...-.:. os a eo ee ees 
Брћетеставсав icici И und TIE nel uu ва oe cu 
Брцдоввсеве cori erro е ИЕГИ E Rane LOS eee 
Epithelial O E е ee 
Bauissteciub. а easi Md т T t Ab 4:520, 548. 
Ericaceaé uca er T 4, Ab 1:15; N 1:269; N 2:52; N 3:266; 
122342. 
ЕПОСАШВОВАВ о сш уст. Ti pede N KOLN 3:37: № 4:31: 
Erpodiaceae |o. eee o eo LE c. + БОЈНИ у... у 
Erys bacite.. ..,.. оста TT БАВЕ 328. 
ЕГУ рПаСеВе . (осе стенске Ru ee са > БА ee ee 
rythropalacege с... Боки Se Se на за IM у у о о 
Lade. s; o еее аа ее T 3, Ab 4:37; N 1:204; N 3:182; N 4:153 .. 
Buseck o 2. ELO CA TI, Ab 1:150: 
БИМУШАШЕ....  ..........-.;+. ie. a  S 
Eucommiaceae... oseiro U ee ee 
КОСУ ео TZ АРЕ |. o у, ; 
Bes ere стао. T 1, Ab 1:174 
Eula T 1, Ab 1a:173 
усб, ОБИМ .................... DT . 
unoti СТРУИ ке о о Mid == 
Bush O T 3, Ab 5:1, 456; N 1:210; N 2:37; N 3: 
191; N 4:166. 
a ee Ce ee DL a 
Бомијиесеве ......................@... er ee 
Rue у ................. E о 
Биро -._......:...:.. 2. Tt Ab PE n 
x o са секс. ce T 1, Ab 1:158. 
ا‎ ................‚‚. ВИ ТРИЈУ... o и 
Касе mE T I T 1, Ab 1**:103 


ORO COCO CR CE RECORD 4086954 


А ЕС ИРИНУ 


(Мог. 71 


Bd 10:418. 
Bd 17b:766. 


Bd 16с:272. 


ва 11:213. 
Bd 2:324. 


see Bd 5al. 
Bd 21:270. 


Bd 10:241. 


see Bd 5al. 


see Bd 5al. 
Bd 20b:401. 
Bd 192:130. 
Bd 10:143. 
Bd 182:348. 
Bd 21:47. 

Bd 5al:1; 6:V. 
Bd 2:268. 

Bd 19c:11. 
Bd 172 1:173. 


Bd 10:420. 
Bd SbVIII:20. 


Spesso cc Fm 1 


—— "^" 


РРА — —_ илән 


— 


C 


1984 MORLEY —INDEX TO ENGLER AND PRANTL 

] 

кее ШИ E ш а зз ык TEAD Sok Е Сулу а 
К O Г Ab 147: N 1:118; N 2:17; N 3:96; N 

EE ЗОВСОН = 1, Ab 4:13. 

по о M oe Fe pe ee se ПАЗИ Pa as 

EE и T 3, Ab ба:1: N 1:252; М 2:46; N 3:232; 

N 4:205. 

20 луге лу I e T2 ATP NL ВУ ee ie IL 
ERES o ое с. T 1, Ab 1a:93. 

ПН... рык IE UPDODUEUDE S uo uus 

EE  — SL USC. T 3, Ab 6:298; N 1:251; N 3:228. 

о E asa А РАВЕНА ЧИН ра е b И О нана aa T 
BEEN  —. . ' . ee tt £2 t SG Er. o ore) ques ds DEN 
ооо Т 1, Ab 2:268; N to T 1, Ab 2:178. 
EE 54 АЕ TI AR ои. 
Fungi аә ee o CREME eds T 1, Àb.1**:347) 

BEEN vvv N 4:62 
Gaseromyeciea Ие eee IE 
кок Riiie via T 3, Ab 6a:205. 
ПНЕ... И T 1, Ab 2:340; N to T 1, Ab 2:215. 
ao пр UC Па а dc is км нек 
ОИЕ" Т 4, Ab 2:50; N 1:282; N 3:292; № 4:244. 
ВИИ ОИ ouo eer e 
ИШАН \.................;..... лл о. 
ЭА С ......................: T3 Ab 4:1; N 1204; N 3:177, N 4:151. 
ПИ сс ш о a as > 
SENE л соксо бшсш ee T 4, Ab 3b:133; N 1:299; N 3:317; N 4: 
ок, 280, 328. 
SS T 1, Ab 2:352; N to T 1, Ab 2:217. 
Gigaspermaceae ESOS aie aa 
ШШ | о е. ИИМИ eer 
Ginkgoales ERA tos is a in ME DU Dr d br c 
Gleicheniaceae ПАР a з па КЕ T 1, Ab 4:350, 355 
Н TG ee 
Glischrode pe Mu pl ЕШ I ad mugs ie (uic аео Sek a sae + 
BD... |. В T 4, Ab 3b:270; N 1:304. 
Gleiosibhonaceae _______- ~ Т 1, Ab 2:505; М to T 1, Ab 2:251. 
00 КА з. а Т 2, Ab 1:116; N 1:26; N 3:6; № 4:6 ..... 
Gn vel ж у Lou ПА eU equ ur M 
Gnomoniaceae зл о. T 1, Ab 1:447. 
ON ee T 1, Ab 2:119. 
МИНИ семе... REE ЕН LENS er Rm 8 
Сото б. А И он N 1:172; N 2:25 
dene... РЕЗЕРВЕ н АЕ eee ee 
а о ёле ee ee 
Пе... ст М 1:231. 
уче АЕ о у. T 4, Ab 5:70; N 1:320; № 4:311. 
ЛЫ АОК T 2, Ab 2:1; М 1:39; N 2:3; N 3:12; N 4: 
о А иим а... 
Ши ЕА ТИС cote 
Graphidaceae vii c E s BEN. eme 
оса сме d c E sso bi tsetse ТОО аи е. 
Grarioupiaceae о. GT ES T 1, Ab 2:508; N to T 1, Ab 2:251. 
Ge EE ns Т1 DE ....................- 
Шы... ~ | ~ T 3, Ab 6:194; М 1:247; N 2:44; N 3:227; 
: :204. 
о 0 , Ab E 
edic c c p d ИИ 666. 


ааа ао ком ааа еа ачи 


217 


Ва 11:282. 


Ва 10:143. 
Ва 21:377. 


Ва 15a:6. 
Ва 11:54. 


Ва 2:251. 
Bd 21:276. 


Ва 10:320. 


Bd зру 15; 
see Bd Sal. 


see Bd Sal. 
Bd 10:345. 
Bd 19a:43 
Bd 19a:4. 


Bd 10:314. 
Bd 13:98. 
Bd 13:98. 


Bd 2:81. 
Bd 7a:46. 


Bd 13:429. 
Bd 13:407. 


Bd 1b:222. 


Bd 16b:46. 
Bd 21:154. 


218 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


Gunn С БИН з шр а ТВОР T SL ВЕРЕ о a АЕ 
Gymnodiniaceae: . TT (eo fey 0h02 AE De ea ОТ UN 
СТУПИО eo ушж O шо у гыш е Bi у E ce ње EAE 
Goran o aa АУ ВООЧАТ Е 2700525505 0 ted 
Gyrostermona ae o ОИУ А расе на ir ez EI ERES 
Настодотасеве аА О PO фы жыйыш кен со hs теста oe кит 
Halorrhagdceae а а а ет N 
Halor a ORAN... es ee, T 3, Ab 7:226 
НАШЕВО ense Lee Cen T3, Ab 2a:115; N 2:29; N 3:142; N 4 
Hanlnbioniacese e: о еони 
PRTC И. esser eoo LS Mi келеш у еш x aes idea L Mane 
Harpocr ШИИ... oso не неке NC пон RE Mri eI etre en TERRE 
WIENER beens л. HIT ADU A кз ee РАВАН ин 
Heltcon NÉ еее еее ПО EEE IINE не о ужа а А 
Helminthocladiaceae ..-...-... cs 1. ol, AB ZG ato, 11 Ар 2-203 
Helotiacede соусу. уу ae ae ПАЮ ie ушл oo 
Нејусђасеве. ITE LS TI SD I у ш. 
Нејусшпено о T 1, Ab 1:163 
Orns et A ee ONE T 1, Ab 1:142 
Heminscineae 2.2... 2 , TL AD:1:143 
Hemibagdi о IIIA AEQ еа ees 
НЕМЮ ueris C EIE T 1, Ab 
HeppiacéBe и SI ABISIA уу. ВЕРНА а 
ernandiaceBe |... э он лл лыш T 3, Ab 2:126; М 4:96 
Небетостопивсене у. eee ie КСО М Шы NL Tu ен ы ORA 
Heterocontüe Куз os EH о ооо era 
НОЮ i. дә. ОТИ ТОНИ К. к ce Os ce снесе 
росананасеве ol in ои TS AD.9:273..459: N 4:227. 
Hippocrateaceae oil уы T 3, Ab 5:222; N 1:225; N 2:40; N 3:202; 
Holomastgacege У T 1, Ab la:112. 
НООКЕЙПАСЕВЁ co) Fs ca со ccc ERE pde concur мз зуу у неком 
Ноокенајва нае оки oe ee ae ee ee У 
НОПО: ance cs oed see ee ee 
НОД. о л з ELE T 1, Ab 1a:61. 
Humina 5. о АО T 3, Ab 4: 35; N 3:182. 
нудјопасеве. ical T 1, Ab 1**:95. 
Нузјовсурнасеве... оре RI a iU 
Нуајоуојуосассас.....:.. | ed. NETLA uo et 
НУСАА Sl ул з Wo ovo lo. а са соја се 
НУбПАОШАСЕМ Leere eei cese пена а а = 
FIDE, D ес а ен сена +, Ар Sides, AIS: М 3301 2: 
Hyd Ce Rev cu ne, TI Ab 72223. 
Hydrocha RD... oos euam eo T 2, Ab 1:238; N 1:38; N 3:12; N 4:9. 
Hydrodt КАМЕ. з... T1, Ab ZION OTL AD263 
НУСКОО ......................: N to T 1, Ab 2:51. 
Нубготукане ,............ ЈАР КОНА РА КА 
нон ООБА Т 4, Ab 3a:54, 377; N 1:289; N 3:305; N 
Hydrostachyaceae ...................... T 3, Ab 2а:1; № 1:179. 
НуЮСо QR -s ne n9 у о о о ооо 
Нуево анан TOO у. 
Hymenogastrineae.......... UA LEY. TEA IND o | s 
Hymen ee CHER ТРАВИ ou у о 
Hymencmioentaceee 266. ThA ~ 
Hymenomyceteae .......... ыо о у ee 
Hymenomycetne .................. T 1, Ab Тее 105 ee eee 
Hymenophyllaceae ..................... TEAR ORI TT 
Fiyonocnviiscese S .....] TE : 
Нурро, транш 
Нерпесеве“. оа Т 1, Ab 3:1020 


"oA $ 9 2 виа € M 4 o» v.) Rn" Pe 


[Vor. 71 


Bd 182:303. 


see Bd Sal. 


Bd 6:1. 

Bd 8:173. 
Bd 3:378. 
Bd 3:375. 


Bd 20b:198. 


о 


1984] MORLEY —INDEX TO ENGLER AND PRANTL 
- crm ti gd aa aia E утисне ЗОШ ВИ og Md у у у, Bd 10:433. 
ИШЛЕ DE ES ILLI. eL TAD ISA ues Bd 6:133; 
see Bd Sal. 
Ee nar TOTO T 1, Ab 1:540. 
I ee a a T 1, Ab 1:343 
= sm ataceae NAE TRAIO 1T л. шу уллу... see Bd Sal. 
ypopterygiaceae B екы IS TULAD у. Ives eese Bd 11:270 
ИЮ ELLA TEUNEGITRNMT oe сое сс... Bd 7a:20; 
ПИ... iR PLOE T1, ÀAb1:272; Ж чы ы 
ПИ. e eos res T 1 AbT:265; 
ОИ СООРОН а а Т 3, Ab 5:233, 459; N 1:225; N 2:40; N Ва 20b:322. 
: лш л з. у з лу у T 2, Ab 5:137; N 1:88; N 3:51; N 4:39 Bd 15a:463. 
и: i а а. а И ОМ ПРВА Le NARNIA Ba TI 
ПИ | о и: T 1, Ab 4:756, 779 
Manic: ОВИ Т 3, Ab 1:19; № 1:114; N 2:17; N 3:92 
= ен а rt 
а I e ceo Не ro E ERE RE T 2, Ab 5:1; N 1:70; N 2:9; N 3:43; N 4 Bd 15a:192. 
-—— E incon T2; Ab 1222: N 1:38. 
niaceae 
ОЗО Иер tM Т 1, Ab 3:38. 
Па ари Таа ee ee T-1; Ab 3:61. 
iis le ei ОЕ T 3, Ab 6:319; N 3:231; М 4:205 
Е САО ИИ en Ва 2:71 
ШО ооо  .. 11 О Ва 2:70 
MEC |... T 4, Ab 3a:183, 379; N 1:290; N 2:67; N 
Laboulbeniaceae эш И Epor ra 
осле qe dr T a T 1, Ab 1:491 
ае ИТИ oe os tek ИА Te SU. cop у у... Bd 21:321. 
ҺЕ eer hy eee a Sieg ape Ee. c Fi RE EIER see Bd Sal. 
i о ee eee T 3, Ab 2:19. 
ses ER EET ae ее ,Ab 
VEN |. — — T 1' Ab 2:242; N to T 1, Ab 2:166. 
rardizabalaceae ei ee DM DA Т 3, Ab 2:67; N 1:1 
uraceae IESE GE DEC ДЕБ у: T 3, Ab 2:106; N 1:174; М 3:128. N 4:95. 
Lecanactidaceae tee te а AN ОО АРКА о... mnn ва 8:131 
ors АОИ qn ee TI Е, БОИ ОТОТ Ва 8:220 
ОЕ ОИ Qoo ern Bd 8:191 
= —— — —  — T 3, Ab 7:26; N 1:261; N 3:239. 
Leeaceae a 1... е ee a ae Bd 20d:372 
E — — T 3, Ab 3:70; N 1:190; N 2:30; N 3:145; 
POR N 4:119. 
E E T 3, Ab 1:28; N 1:117. 
Lemaneaceae Eee T 1, Ab 2:324; N to T 1, Ab 2:203. 
Pie) ERN... — СИИИ. Ва 11:202 
ЕИ ee. Т 2, Ab 3:154; № 1:61 
Lennoacea c у, л. у d А 112. 
Ce x иу Кане CD TuS T 4, Ab 3b:108; N 3:316. 
Leidodendaccc HM IM NN T 1, Ab 4:717 
qoc ата ERU M T1, Ab 1:101. 
о ИСС  — 3 TLAS OP ....................... Bd 10:404 
wees ОИЕ РТ [7366 _....;у............ see Bd 5 
Lepyrodontaceae sind end ON V E ceed ee a TL ss baw ee Bd 11:109 
Leskeaceae е л a TT TT 6. TS ва а 
у ТЕ ЛЕХ 1166.................... Bad 10220 
Гер О!асезе ОООО TJ ЛЮТА 1214.................... Ва 11:91 
Ио ОЛО nnnm Ва 11:267 
Liceaceae rer E Ti Ab G lcar Bd 2:318 
е и Ва 2:318 
Lichenes Bd 8:1. 


... 
..... 
МЕ и Ө ӨЛӨ б ee we ee аса 


219 


220 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


Bichinacede e cas DADE IGA a 

E E GT T2, ee PEA Nea 
4:34. 

ТИ ОВЕ РАЧИ НА ПА А eoo Sas ык те, л LAE, аана аат 

розе НАВОДЕ о Т 3, Ab 5:136. 

АСЕЕВ ИЕ е: Т 3, Ab 4:27; N 1:204; N 3:180; N 4:153 . 
DASOQTSlACEBE е. арка асн ОЕЕО I 6 асалар тагон 
EROS ORONO CLAD а оаа а T 1; Ab 2:260; N to T. 1, Ab 2:173. 

LBS не NIME Lo a C RE T 3, Ab 6a:100; М 3:236; М4:208 OT 
ТООЦОО о с тга шшш уот. ка T 4, Ab 2:19; N 1:282; N 3:291. 
Tobhiostonistucedé . а, TUA 
Lora MDA E e а у T3: Ah 1: 156: N 1:124; N 2:18; N 3:98; 
ТОПОМ аа Ss ee ee и er ee 
УСОВ АТАС С уу... losers O ee OEE PLR DERI REPL re 
D ee soto s уу... ees ITANE. МАНИ НИМ N 
Lvcoperdiéae .... Ул. eee E ANI IB ate cs rr SEM 
Русррошасеве ла T 1, АБ 4563, 715 
Lyginodondracedé .... 01 л А ee a 
Lyt RHO ууу уу ул овие T 3, Ab 7:1; N 1:260; N 2:48; N 3:239; N 
4:212 
MagnolacBae TTT 13 AbB22: N 1:197 2:22: N 3:108. 
Malesherbiaceae: aee sees ore ERES ИН И NIS. v СЕ 
Malpighiaceae iS T 3, Ab 4: T SST 1:205- N 234: N3: 
182; N 4 
Máalvactae Ns T Ab 630; N 1:235; N 2:42: N 3:211; 
N4 
Магапіасеае yS т2, Dr N 1:94; N 2:12; N 3:65; N 
Магашасеве.....: oa у + P Ab 4:422, 473. 
Marcaraviacent cll, TO OO UR ee ae 
Marchantiatese: us eo us T 1, Ab 3:16. 
argaritacede ИНЕ ea ee 
a ОНООС ук ee 
MESE о г, T 1, Ab 4:403, 421. 
Martyniaceae с... с ас з. T 4, Ар 3b:265 
Massaridceae n a T 1, Ab 1:444. 
Мавзпросыйасбае........;...;. ИС А ЕА ИИ eor lvi. ee 
AStOGIACCRE MG BR IAEA A I у. 
Matoniaceat т ee нео T 1, Ab 4:343, 347 
Мауна: cs ee es T 2, Ab 4:16; N 1:61; REM. тенка 
Меш овассаёЁ Lees ease noel ит АБИ у а о 
ейшшдупасезс ............. о ои 
Meeseacéae ео. TL AB OG уу: 
MMoOXVIBON ivr a a у о. 
Melampsoractas ....................... БАВЕ S 2 e (ders 
MelanconiiceBe ..... ...-.. о... T 1, Ab 1**:398 
МОЛИИ o... ll T1, Ab 1**:398 
Melancomdtacese ._..._ . 3. T 1, Ab 1:468 

їапорайассае-...................... Ca ey a о у о 
МЕашошашошые.;................. T j Ab 7:130; N 1:263; N 2:49; N 3:247; 
Molane пе d do a T 3, Ab 4: 258; N 1:208; N 2:36; N 3:188; 

N 4:161. 
МЕНЕП =... es 5 T3, Ab 5: :374. 
SOBRE оаа T 1, Ab 1 
Mene. ek e на. X34 Ab 2:78; N 1:170; N 2:23; N 3:125; 
:92: 

MONDE а А Gere T 1, Ab 2:21; N to T 1, Ab 2:12 
Meteoriótab. ......................... ооо o 
МЕСТОСВАЊСОМ................ even ens о S сера 
ie 7 070 о 
МООИ ое 


T 1, Ab 3:532 


+... осе» «ње 979829589949 


[VoL. 71 


Bd 8:160. 


Bd 15а:227. 


Bd 15a:1. 


Bd 19a:82. 
Bd 2:319. 


Bd 21:522. 


Bd 16b:98. 


Bd 1b:115, 


Bd 1b:136. 
Bd 8:92. 


Bd 19611. 


Bd 11:154. 
Bd 1:159. 


прави БЛ soccer а ысы 


í 1984] MORLEY —INDEX TO ENGLER AND PRANTL 221 
| 
| 
| Па... л. usu T АБ 3: a Поре 055 у ро Ва 10:406. 
| а з VV ууу... РА Ab 1:2 
| EE A о T 1, Ab 1: Aber 
EB — ЕЖ ТТ,АБ] 
| НИНИ T 3, Ab 2: с М EIN DIS М 3:127: 
| Monoblepharidaceae.................... Tiki S es v von. Bd 3:252; 
| see Ва Sal. 
| ШЕ йл эру ыс к ed шү Т 1, Ab 1:106 
| ПН MN ыл о с у ва 3:407. 
7 ТОО АИА I: Ab 1:66; N 1:119; N 2:17; N 3:96; N 
00 00 bv .................... + T P OMIT LI I Bd 17b:693. 
[| NEM GS .. . . .. . TIAE ВИ И о у... ,.уу..,. Ва 8:63. 
Mortierellaceae Кол уху. у... T 1. Abo 
рее qua КЕ V s Sois а у АН А у о: see Bd Sal. 
ОТАН i ELI (па Bh TO ба АИ S uniri see Bd Sal. 
| Ie i у: Т 1, Ab 1:119. 
| ou аде О Бае: MISE N 2:12: N 3:51 ..... Ва 15a:505. 
olco o ....................... T 1-Ab З 142. 
EAAS . T Е Ab 2:101, 160. 
) Hy ENDS А Бои БК ЛИ ЕТ с eise. Bd 8:92. 
| оси озу TS ВИР ИВЕ APR uU ees я see Bd Sal. 
| о А se T 4, Ab 3b:354; N 1:309. 
| М et Sc bE ONES I T 1, Ab 1:319. 
| ШО о... T3 AD 1:26; М 393 
Myriotrichiaceae б шуу E T 1, Ab 2:214; N to T 1, Ab 2:161. 
| MS NE o а у tee et T3 Ab 240 N EIGEN IIT —...... Bd 17а1:177. 
| us BEES а oerte AX re з у... 18a:262. 
| eee а Se QI MEQUE Oe T 4, Ab 1:84; N 1:270; N 3:269; N 4:235. 
єє ooo ss T 3, Ab 7:57; N 1:262; N 2:49; N 3:247; 
N 4:214. 
Myuriaceae 
Bras) ПЕРА vxor cro d UU M А E EIU IAS P Bd 11:123 
М аселе „ооо ee NtoT 1, АБ oe... 3:80. 
Rees а тв а а X h Abd б^ худ oy Sd уу... ва 2:304. 
EE. Ss vv. ара Яо 
ПИ ——— ——  — T : Ab 1198; EM a Bd 16b:92 
Najadaceae ..... ; 
О o — Bd 2:272 
ескегаседе ...... 1:17 
Мена н РУ ТІ, АБ x El M I S. Bd 11:178. 
Nu ОЕ T 1, Ab 17382. 
Ne Oe ае T deser N to T 1, Ab 2:254. 
eee ае ас ка TAS YO Sei cra ws Bd 11:215. 
Nig thaceae Ure ce ere E INE E T3 A52: d N IBN 4106 o. Bd 17b:728. 
У ЕРА о КОЕН Ва 7а:56. 
ОООО: core... Bd 7a:52. 
Nilssoniaceae ПА ee eee eee Bd 13:97 
a, quo a eg kia Ve MM Bd 2:293 
Whee” ОЕ еее cb ew eee orn Bd 2:47 
“Meas ia у. MS T 4, Ab 3b:1. 
мао dui о a түш шо nemen Bd 15:177. 
Мусин о А ue in ic О pu M Bd 1b:131. 
ee si ЖАЛ ООМО ete oe E T3, Ab 15:14; N 1:154; N 3:105; N 4:83 .. Ва 16:86. 
N E O TA Apel М LISTEN 2:22: М 3:107. 
тиш о yS N4 4:21 13. 
wol 0 NS | T 3, Ab 6:131; N 1:245; N 3:219; N 4: Bd 21:53. 
03. 
eu onadaceae НА | I E T 1, Ab 1а:163. 
Ee M dept a MM TEE N 4: ИСОИ А Ва 16:42. 
QE mataceae — see Octoknemaceae. 
Oedosonig a n e n e ОН ене Bd 10:332. 
aceae.. o T 1, Ab 2:108; N to T 1, Ab 2:107 ...... Bd 3:244. 
Oen oeraccac оо, 3:249. 
Око peace OO T 1, Ab la:118 


222 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


Olacacede РА es eS налу T 3, Ab 1:231; N 1:144; N 2:18; N 3:98, 
Oleaceae v. ee ee T4 Ab 2:1; N 1:281; N 3:290; N 4:243. 
OMICS оке ie eae F 3; Ab vy $. 

Olpidiaceap оро а Ч УЛ E Io papa rec dn 
ООВ o- уму ка тему T3 4 N 1:268; N 2:50; N 4:216 
CARINE, 5, тутора РВИ ле ресе ти ои 
а да ET ess МО РА SAD 292s) TA 

СЛОВНО с odori ере лима TI ADSI. 
OOOO а а при TES TL Ab 1:63; 
Ophiocyiiscese ~ SOM Сена E ME МОКА Ab 749 UE aA 
OSEE. 1:0 ra riy ce Rus T 1, Ab 4: 449, 472. 
Ophigstomiatacese: ssa О ee а и 
OPINION EAN N RIZ DEAT TO o 
ODORS Se аса ТИ es s si ee eee 
OHNE soe ba о а vee ae ву ава ek екипи 
CT oe i oS T 2, Ab 6:52; N 1:97; N 2:12; N 3:75; N 
Orobanchaceae SE тениске T 4, Ab 3b:123; N 1:299; N 3:316. 
ООО I ee evi уу у у уу у. ПН TE ЕРЕ онн 
GCS OAC TJ ABIESOL | с Пра пр кея 
о C MERE EE I уу. T 1, Ab 4:372, 380 
ОМОРИ с, и HD REDE LI. uii qi S cx o а 
Ostropncese сз: ee Tt, Ab E271. 
Qxalidaeae 2с. Kaya RM T 3, Ab 4:15, 351; N 1:204; N 2:34; N 3: 
180, N 4:152. 
Охубокасеве.......:.... ос но d CC abe пење 
Рајта oao ж... ee E T 2, Ab 3:1; N 1:49; N 2:8, N 3:22; N 4: 
23. 
Рапдасеае........... у. и D N4 
Рапйапасесаё............; у T2 ey нЕ NISL N 2:2 N36, N 
4:6. 
Pan Mt. E и а T 1, Ab E. ERES Su л ул и 
Pantostomatncae uS i Е TL Ab ETT, 
арауегасене rusos РО о, TX Ab 2:130; N 1:174; N 2:27. N 3:129; 
:96. 
Parethelacéle 21112, у. сд T1 “Ab Fen Uu E 
PaflelaleS l1 E NEN pr cx pua qos c NI NEU CAR MD у. 
Parkeriacedé аА T 1, Ab 4:339. 
Parmeliaceae о Eo Мег у T ee 
Pascherinėmataceae ....,............... РЕН А SS 
РазаШогисеве -......:.. о и. GR: Т 3, Ар ба: GN КОЕН 3243. се: 
Pateliatiatene је см un T БАБ 1:221. 
беде e UC не En T 4; Ab 3b:253; N 1:304; N 3:320; N 4: 
283. 
PEU CI TA Ab ОВ, у, у... 
РАША О лл у. у уу. T 3, Ab 6a:208. 
Ре С... санке os Ui eee л о ee 
РЕПЕР. „2... onn s N 1:214; à р РРА oir e n 
PEO os her UNE M з сен T 1, Ab 1 
POTN ioco eee | c d | > su i 
Pern e . ОНИ 
Peridiniging IR с. КАРИ 1533. a 
Регцистушасеве...... uS Baits REE a о. у E 
Репаронасее Coil N es ТІ, AD Ва. И НЕ as 
РЕГИО а T 1, Ab 1:325. 
Ретоловрогасбаб ......... 0,1; н ss 
РОСОЮ s а T 1, Ab 1:108. 
NONE C ea TI ADIPIS а 
Ре ШОМ о о TEADIS о прси a 
PONE с... d qu IEAI. 
РЫМ o. ee ea Т, АОБ у a 
РБАСМИННОВЕ окос Л м АН T 1, Ab 1:243. 
Fhacopbyctse o. TS T 1, Ab 2:176. 


[Vor. 71 


Bd 16b:5. 


Bd 3:399. 


Bd 11:10. 
Bd 1:193. 
Bd 2:96. 
Bd 19a:11. 


Bd 2:97. 


Bd 8:175. 
Bd 17b:5. 


mess RR 


1984] MORLEY —INDEX TO ENGLER AND PRANTL 
Be лаке сата voten БЕБЕ T 1, Ab 1a:129. 
Se eee ee eae Т ЖАКАН ИИИ O 
ОЕ ИОС етене TJ AD TEIG ee 
EE S cibi T. 2: AB 4735 170 S oe cus 
а а UI A T 4, Ab 3b:361; N 1:309. 
АЕ T L AGED: 

ПН 00си oy Лр УМ ee ORE ce Ga ve A UTE 
о a TRE ERR ECRERETSETE T LAUP II Ор Оту uA Ie 
ae a ЕУ ER ELE TL AGEGE S. V Sees 
ОСА ИО REO T E-Ab 2125. 160: Nto T 1; Ab 2:133. 
Phymatosphaeriaceae ................... Tt Ab: 5242: 

a Поета UND з DIL. Io pop M a 

y os LAUDE ee OS ee са UE e uL ee ee ere 
0 0. бо TH WP PNE I C s ers 
o Lg СИС Uere Re 
cene En corned T 3, Ab Ib:1; N 1:154; N 4:82 .......... 

o SS ТІ, ADI 
Pilacracea BA се sy i vi аксе CS T4, Ab 1 86 
ZEN eene T 1, Ab 1*:116 
HEN ОИЯИ TE АОИ оз л 

а ТА с a У T2, Ab 1:28; N'E21; N 22; №3:4; N 
Pone Bei ст rice T 3, Ab 1:3: N 2:16; N 3:92; N 4:62. 
Ip тераа ера Ser ae T 1, Ab 1:132. 
ч Ет СООРО Те T 4, Ab 1:3; N 1:269. 
ЗИСТА Онон ee ne 
ое О САВТИ у л. 
Plagiotheciaceae SS а асва э во жор 47V жеө ee wee ж © NUM E ae a ee 4 459 ив сево r жа. өз ена оёт во 676 RO 
Plato EN —— ——— — — nma 4 — 
Plan ПИ UE CT C C HORREA UE 
EC i e е Ч 29 
ы Ei o 
Pi latanacea EU. nl v M T 3, Ab 2a:137. 
Pecasoess <. ш ы ET T1, Ab 1:290. 
ВВ а... PAD Coe 

С0ѕрогасеае..... Т 1, Ab 1:428 
Prurocapsaceae | po E : :428. 

EN тен 
Pl EE зу ш о ан ene eee ht tes eris 
ee V ed PODER I P T 1, Ab 4:754. 

Piste EL. I i IULII T 1; Ab 254 160: N 10 T..1, Ab 2:35 .... 
sen EE. У НЕ БАРЕ erent cess 

TRU o уу еу te T 4, ar :116; N 1:271; N 3:286; N 4: 
239. 

Podaxacea 

Podaxineae 22. ОКЕ ТЕ Ab 19332 1d (guis disp ате сө OR AR Ate е 

к С 

ПН"... sns oL dius CELER LBS UD еен рањена. 

Podostemonaceae 414 3 V alee ө M RR VE Уа Ае ји аков MR Y e Ln 1 s... N4 107 аә 

PEL t ин e T 3, Ab 2a:1; N 1:179; N 3:135 

Po eee о se See E ње ee ee E оз 5 Qi о очи и MERE ua вов аси P E өлкә Фе hé Kot ro 

| I erie T 4, Ab 3a:40, 377; N 1:289; N 3:305; N 

Pol 4: ^ 
НИ... __-__ =. - Т 3, Ар 4:323; М 1:209; М 2:19; М 3:190; 
Рој N 4:163. 
ПИ. | T 3, Ab 1а:1; N 1:151; № 2:19; N 3:101; 
Polykri N 4:80. 
Ро krikacea СОУСЕ denuo ты т т са ITE 
ро pottiaceae p. E a T 1, Ab 4:139, 473. 
СОН она уне а о 
Polysto 
Po oly аса" ОИТ ИНУ ТУО Е 
TR Ce e ПЕЛЕ КО a cen nk 


пев аа жаана аиа иер еа ee ee eS a RA OR NO eee eR ae eee о о 


Bd 7a:96; 
see Bd Sal. 
Bd 7a:76. 


Bd 15a:190. 


Bd 11:174. 
Bd 8:200. 
Bd 8:81. 
Bd 3:334. 


Bd 
Bd 16c: 135. 


Bd 11:216. 
Bd 13:271. 


see Bd 5al. 


Bd 1b:80. 
Bd 1b:79. 


Bd 3:99. 
Bd 10:219. 


Bd 7a:116. 


223 


224 ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL. 71 


Pontederiacese ss ae es ee TA ee CTO TT УЛ BS ATA. Bd 15а:181. | 
Portulacacese +. io so E T 3, Ab 19:51 N 1:156; N 2:20; N 4:85 .. Bd 162: 234: | 
Potamogetonaceae : о та ке T 2, Ab 1:194; N 1:36; N 3:8; N 4:7. | 
Pothactat и ул а Н 10.9 34 8 9 о sss Bd 10:243. | 
Pottüales- 030. А А РО ИМА ee UN. Же ушл cece a EE ва 10:228. | 
PiiimulsDeBEr c а ee кн ст. Ер T 4, Ab 1:98; N 1:270; М 3:278; М 4:236. 
Pronodonteceae |... S See ИТЕ FIA seii rit Bd 11:112. | 
Pronrocilucaceae os sn уу уш НО i ы дул ва 2:39. ) 
РТОГОСЕНЉНИОНИМ iri co DRE ee TENE NND ва у, Bd 2:37. | 
ProteaGeae еее eA MORES T3, Ab 1:119; N 1:123; N 3:98; N 4:70. | 
Protoascinene =s... уг 024. гу и TIE AG 1:150. 
و‎ БАЗАНЫ Mos San о ен (dE TI Ab 18824 
тоосаайапассае cosa oer err nn s T 1, Ab 4:558. | 
Рони Be а E T M tu our Mm MEE nt ер Bd 2:83. 
особрисене а o o o a EE па а TA ЛОО МОТ, AD 2:41 2... Bd 2:81. | 
Prot Erg cuu АЕ SU MONI Ri orn M M MAL Bd 3:27. 
Protodiseineae ^... | али T 1, Ab 1:156. 
Ргоїошакцпшпеас Tl ш T L Ab Tact 19: 
Ртојотусешседе:. a T 1, Ab 1:147. 
Protopitvaceae ona a e a om ee 13:22; 
Protosiphonacene: с ос и л. o coo ULT DOM LM VL qu а Bd 3:151 | 
Prototheca сс... и.к а P LE Rs n I. Doo. o 131 / 
a rcc p HE ы cm ey ry ee ode ое see Bd Sal. 
Pale. os cc ee о: T 1, Ab 4:606, 620. 
er E ei T 1, Ab 1a:61. | 
Р ГӘР. 2:1... естонски си T 1, Ab 4:1. | 
Pico у... л. ee Шш у a л л у Bd 11:125 
Pterospermataceae ll Р E Bd 3:94 
Ptychodiscateaes .4 22... г a ле ух ва 2:70 
РУСО АЕ. У,у, a TT ва 11:6. 
Ptychommiaceas ...... о... TAUI NA I л ва 11:102. 
Pucciniaceae уы... ууун. зоо оо и АО ТРД Tl Ва 6:48. 
Pulvinulanacese <.. oaran ее Bd 1b:118. 
Риписасене оо с TI AD 722 
Pyrenidiacese а у tae, mk adir cnr a Bd 8:89 
епосагрсаё зз: о р; о Be oi ECT Bd 8:61 
Pyrenomycetineae | a o T L Ар 1:321. | 
Pyrenopsidaceae ...... oos. сем TLA IR. e S и Bd 8:153. | 
Pyrenothamoisceao...... Sn. TLADI DI Уу з a Bd 8:73. | 
Ругепо RO по ва 8:91. | 
Pyrenulaceae, > <-> or r TLADI OL М... ш... Bd 8:74. 
Ругопетасеве: о... прса а лесе не Li AB 1176. 
Pyronemataceae... о eee un ____- | see Bd Sal | 
о УА он P на не ла ок EI Bd 2:96 | 
РУШИОМНЕ...... с. л, T 1, Ab 1:104. | 
ОВО м ууу. TIRADE О ва 21:106. 
Rafflesiaceae ..... ло. uU. T3, Ab 1:274; N 1:151; № 2:19, N 3:100; Ва 16b:243. ) 
N 4:78. | 
Raiti o T 1, Ab 2:240; N to T 1, Ab 2:166. | 
Ranunciwiscese:.............,... ud I 3 Ab 2:43; N 1:167; N 2:22: М 312 | 
4:91. 
Ларки o у; T2, Ab 4:28; N 1:61; 'N IAT. Bd 15a:59. | 
BINE -o о 1. E ТА ВЕЛИК Ыз | Bd 17b:659. | 
Restionaceae. n Sn T 2, Ab 4:3; N 1:61; N 2:9; N 3:35 ...... Bd 15a:8. | | 
КОЊЕ... а у у ee TLALE Si ЮИ EA Bd 2:316. { 
Rhacopilaceae ........ soo TPHABIUM у Ss Bd 11:50 
WE so о. ul 3 3, Ab 5393; N 1:229; № 2:41; № 3:210; Bd 2047 | 
Rhamngles .............ф....‚ӊ ос с. "леш (ле = е Bd 204:1. | 
ИһеюпаїобойЫсеае............ = X... T 1, Ab 3:1125 | 
Кһеппайдассаё.................... 04 199 о ооо ооо 0 5 0 Bd 13:20. 
Rhizidiacese о "БАРАМА | 5 0 5 5 о see Bd Sel. | 
Rhiinaeéé lT TARY oe о. sce BÀ Sk | 
Rhizogoniaceeé’.... 63. TT Т1,АЫЗ сии Bd 10:424. | 


1984] MORLEY —INDEX TO ENGLER AND PRANTL 
eee T 1, Ab 1а:113 

ПИК. PG Wot И ИСА ДО ЕЁ Боосу. ss es 
MMO КЫ te, RET EE T3 Ab 7:42; N 1:261; N 2:48; N 4:213. 
ПН. T1, Ab2 

СНОС a ИЕ T 1, Ab 2:317. 

BEEN E VIR МОРАВЕ ДА 10 11 1i 
РИД ШЫ T 1, Ab 2:421; N to T 1, Ab 2:240. 
ОТТОО РЕ T. | Ab 2:298. 
Se re ree TL AS25662 N to Т1, Ab 2:221. 
ee EM e gee, uU. ТАЛАБЫ 2396: N to TIE Ab 2:224. 
Ивана BEER ме N н XR MI E c cT. 

BEEN VV Vo LEGS TI Ab:3:8. 
ОСИ Ti 2. N 
BEEN ...................... pu ee N неко See 
КОШЧУ узду ут eR. 

Co edu rhe у... ee UD T 3, Ab 3:1; N 1:186; N 2:29; N 3:143; N 


a ea on aks 
a iv ке Stemonaceae. 
u 


ENS SV SV V V V VV КИ 
Ru EU ml “ie Oe qux MI у. 
ПН | 


а - 
Salviniaceae 


Saprolegniaceae 
Saprolegniineae 
ceniaceae 
iales 


Scheuchzeria, riaceae 
: <histophyllaceae 
Ostegaceae 


* 59 5:4 epee A Ye OY ek Pe ки ee UR So Ve 
"Os We do $7 CR P Фата ожа ^ ELA 
ACPU e p ваа Oe а шж er агаа 


est ah ote, Ok All Se ө и еее A A ж 


Scytone 
Зоре 


Re. Ait кора и ле 
wo" *-W a ато К» 


ен 9» » 9 фотке p dine M iN 
зове Po» оаа ве ок alan a S 


Sematophyllace KS 5 P AOR BOR ACE те во UR A RR UE aie ak al К 


4 ее ево жир TG теў ө» а ж 


T 4, Ab 4:1; N 1:309; N 2:72; N 3:326; N 
4:290, 330. 

T 3, Ab 4:95, 357; N 1:208; N 2:34; N 3: 
187; N 4:156. 


Т N 3:210. 
Тт AGLI 
1220199 N1117: М 217; М 3:93; М 
4:62. 


ТАРАР СЛ М ЕВ. NC E 
T 1, Ab 4:383, 4 
T 3, Ab 1:202; N 1:141; N 3:98; N 4:74. 


T 3, Ab 5:277, 460; N 1:227; N 3:202; N 
T 4, Ab 1:126; М 1:271; М 2:53; М 3:287; 


rig Tr e xs " Di ECT 
ur Ab 22:41; N 1:180; N 2:29; N 3:141; 
:108. 


N 22, N 3:9. 

тї те; B v 

T 1, Ab 4:356, 371. 
a:2. 


Коа ае C6 442342922 вета њи ка 


T 4, Ab 35:39; М 1:293; М 2:70; N 3:310; 
N 4:273. 


LL “Ab 1a:76 
N 1:242; N 2:43; N 3:217; N 4:202. 
T1, Ab 1**:299 


аиа еа N a ee he а е 


C. RON RAIN R9 RO ee те важи и 


жол Өр Ө ИЕ ае ө» кей ә» еа а ра өө ва тетт ә өө 


WEG ae ek oe eee ee mn 


see Bd Sal. 


Bd 3:94. 


Bd 17b:1. 
Bd 11:475. 


Bd 1b:162. 


Bd 8:123. 
Ва 18a:346. 


Bd 18a:69. 


Bd 19a:187. 


Bd 11:115. 
Bd 2:249. 


see Bd Sal. 


Bd 20b:232. 


Bd 16b:52. 
Bd 16b:1. 


see Bd Sal. 


Bd 17b:704. 
Bd 17b:701. 


Bd 18a:74. 


Bd 10:143. 
Bd 10:344. 


Bd 1b:1, 223. 


Bd 1b:145. 


Ва 7а:110; 
see Bd 5al 


Bd 10:167. 
Bd 11:404. 


226 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


Sigillo oss са a ТІ, Ab4 
Simarubacede 9»... 1: STE T3, Ab 4: ss N 2:36; N 3:187; N 4:158 .. 
Sinbondla.... ua... IVELIT belt Hm AN. sn GEI EE 
Siphonocladales.. ooe ss истини ee S не косаи ло: 
Siphoanonematacese -css ыз. ы ea EE лл л a язча оинае, 
нас о pi усы T1, Ab1 
Solanaceae. Li E T 4, Ab за; N 1:292; N 2:69 N 3:309; 
Solentübcedes es PINE И О Е oe COUPER EE S PASS 
Sonneratiaceae аА N 1:261; N 3:239. 
Ti uu hv eae ea id CUP LIS T 1, Ab 1:390 
Sorapillaceae......... PR а ry pe iae OT n R 
ИИ Е LL ш Vr RIRs T2, Ab E1922 N 1:35; N 2:2; М 3:8. 

е iio Т 1, Ab 2:233. 
Spermophihoraceae, ира еру ООО АИИ Ао IN 
орпасејанисеае е... чаа T 1, Ab 2: = М to Т 1, Ab 2:146. 
SHREDS cL T1, Ab la 
Spha Hec ОИ T LAbI ced О cu e E eee 
Sob NE IL Lease у кина T 1, Ab 1:384. 
Sphasrobolaéeme оиа 1, АРИ ЗАб osc... нан 

пветососсасеве._ Lc от T We HA N to T 1, Ab 2:223. 
Sphaerophoraceae сеи ENE o наиве а Co a 
SphasropleBceae. оон T 1, Ab » RE ete РБ Ab23123 |; 
Sphaeropddalek- ие ELADI 
Sphagnaceae o vos уз шыу T 1, АБЗ {ун A т лы C ты; 
Sphagnales |. у уг р, р л не SIR ul шу г у г 
Sphenophyliacese |... V = . T ТАБ А4913 
Spiridentaceae cE ПА АН TIUS у о ee 
оршшасеве 7... 1... | | р ЕТ, Аб Ја: 
Splachnacede CL T 1, Ab 3:498, SRI нк E ч. 
Sporochnatesie о, с а a T 1, Ab 2:236: N to T 1, Ab 2:166. 
Зорштанасеће._ |... = з ~ T 1, Ab 1:29. 

апага... 2.1. у 2, s T 1, Ab 2:532; ч 1, Ab 2:54. 
Stachyuracese > а Т 3, Ab 6:192; УЗ а ск MR сое 
Stackhousiaceae.. e ee T3, Ab S.231; 3 " 13898 O 
Staphyleacese | Ра раса us JERRY Dore: Не 
Steloxylacége у... Vor ол ш о ee eee 
Stemonaceae ll EL AOSS NINA V ULIS 
Stemonitaceae ..... St ee TEAL р о ee eee 
Stemonitales 2... а И ен а пе се MK 
Stenomvelschle Le не е и а и а 
Sterculiactaes са о ee E Т 3, Ab 6:69; N 1:240; М 2:43; N 3:214; 

М 4:201, 328. 
SUCCES ........ з. зш... Т AD Bee so hs у eres 
опснавсеве о T 1, Ab 1:245. 
Stigmateactne. .....................,. alas a 
Маа. ie tins слан скока T AD И у у. у. rrr 
Sulbaceae |. as ee Ж І АВ Age ll x у 
ООСОР u Т 1, Ab 2:230; N to T 1, Ab 2:165 
бйтиейасеае...:................... Oo ee ЕС 
САГИ ER SR E em TIAE AM N to T 1, Ab 2:159. 

BENE ue oe а Ex LAD КОЛЛ S. ........... о... 
Svid о. скока се... М 3:336; 

ПНЕ S ERNEUT UNUS C it Ab 1:173; N 1:281; N 3:90 М 4: 
5ушрһуойовшсеае..................... о тен с нос = 
Symplocaceae (озул ON а SI САБА ае М 1:281; М 3:289. 
SYNCHVITINCERE Е а TLASIH AE. “а 
T E M a cS THAAD SIZICN BON S49 у... 
Таас и. T 3, Ab 6:289; N 1:251; N x E 
T ND Iu II Si T 2, Ab 1:107; N 1:20; N 3: gae pues 
ТАО sS 
Taxodiactee о 


SES TN A 9 лено Жоке ewe ме ) FAX S 4 ee ич 


[VoL. 71 


Bd 19а:359. 


Bd 7a:51; 


Bd 10:105. 
Bd 10:101. 


Bd 10:474. 
Bd 10:333. 


1984] MORLEY —INDEX TO ENGLER AND PRANTL 227 


BEEN | CU а uus TERADI e as и Bd 5bVIII:35; 
see Bd Sal. 
Ternstroemiaceae—see Theaceae. 
ooo ۹ esse me ne es T Ab 12:143. 
Do OO о а а CUTE RD OD TUE X 1' Ab 2:43, МО Т 1, Ab 225 .... 84365: 
ПИТИ... ME HR T3; AB 6:175: N 1:245; N 3:226; N 4: Bd 21:109. 
204. 
Пе ee os КЕ AE ЊЕ ВА Fan А ee M rima Kin e d 237. 
EE — ....——————— TIE ABIT V у río ten Bd 6:135; 
see Bd Sal 
cea 
EM Test АЛА Р ы рана RG пи ne ek пч пы S Bd 11:278 
EE 0 0 . T 1, Ab 1*:229 Bd 8:251 
не EE иы ерун RO TE CAM ЕЕЕ ара реси на 8:13 
Ко. КОО з. 13 AD Re НУ узш ул од уу Ва 16с:368 
AU. E une Bee 3:267 
IDEM RN Ua US NM ITIN T 1, Ab 2:321; N to T 1, Ab 2:199 
00 ase QN CE D нв ___"______-_ Bd 11:309. 
Thurniaceae 
s he e c ЕСО ОС IM M Pet н Bd 15a:58. 
EN ||| T 3, Ab 6a:216; N 1:260; N 3:237; N 4: 
5 12. 
ШОШ а сз. Таб МЕЗЕ N 2:42: N 7211; N 
Tilletiaceae СОС EUM e T 5 1**:15 Bd 6:16 
illetiinea МЕ у СА 
l ПИ... УЧА на T ASIS Она re te етно Ва 6:16 
T 
a ee ee T 1, Ab 2:265; N to T 1, Ab 2:177. 
int D ovo end кке UE TRAN BO ОЕ Bd 10:476. 
ШО Е errr eM T 3, AG OOO ан iE Bd 17b:224. 
Trachypodaceae а ond ne Та i c c IQ UN a ees Bd 1:117. 
Tenn DNI e M KU T E » jd 3 ыр 
Т eo hes eee CF uris > О, уу. шуу. 
ты к о E ТОЛОТ хз у м. Ва 6:103. 
еке. ала Zi 
EE ^ о 
Tri гыбы еј кил eee EE D Bd 3:403 
Tai eme eme ee A A еен 2:3 
TED Ou e emm Оо ane ата И ОРЕ Bd 2:334 
ee mea Pea ee ee T 1, Ab 1:310. 
Trichothysiace ET S T T 1, Ab 1а:84. 
fo He c c CPS Ce Oe А MM ОАЗА САО see Bd Sal 
ج‎ i AT P3; — 4: а N 1:209; N 4:163. 
Tanda ee Т 1, Ab 1 
па: Mrs ge оние T2 АБЕ oe N 1:38; N 2:3; N 4: 
Теш Бене. у... em T3, Ab 2:21; М 1:158; N 2:22; N 3:110. 
Ta О GT T 3, Ab 4:23, 352; N 1:204; N 3:180..... Bd 19a:67. 
Tyblidiaceae 
Tr ee Иља ВАРНАВА 
Tu DP D Er TE a. Pc E Bd 8:81. 
MEM see Bd 5al 
i E01 ul lu Il xu uar i ir in ipe esr ri. 
Tu ace Que aan и СУЎ see Bd Sal. 
rri conc dE о LL у м oe) as ap e eese Bd 5bVIII. 
о тетиве ПЕН a LOL eee К Bd 2:317. 
T NEN EE o1 utut nsus eu eee) E E E see Bd Sal 
"SF ABER LUE куу TLADI? не Ва 7а:46; 
Tum Bd Sal. 
Thien ER... ы R TET Т 3, Ab 6:575 М 1:253................. Bd 21:459. 
Уо... у IL о T 2, Ab 1:183; N 1:35; N 2:2; М 3:6. 
в ea Ec aes T 3, Ab 1:59; N 1:118; N 2:17; N 3:96; N 
Ulothri 4:66. 
Ulv Lo em Ен ee T 1, Ab 2:79; о agree оа Bd 3:157. 
Umbellifery; a sacs Cece a T 1, Ab 2:74; N to T 1, Ab 2:69......... Bd 3:172. 
Uredinales Bressa a А ens T 3, Ab 8:63; E. 5 5256 N 4:221. 
© a eer TA Ab 124: 
Une See а as з ка ode N 1:122; М 3:97; М 4:69. 
U ma ооло Ce у ТОТА —.........,........... Bd 8:238. 
a + паж у з eer Tf die So oe ERE Bd 6:7. 
tilaginales Bd 6:24 


Џ кайыбы ele а Ed NER ow dw» err un "RE CAM Sa. E M MN ANM ee Ga МР ИРЦ TAS E енер А ШШ ЩЩ ее 
= © лз а... Ва 6:6. 


воље E и RE Cee биво о 


228 ANNALS OF THE MISSOURI BOTANICAL GARDEN 
Valerianaceat 07а TE Ae 4172: N 1:316: N 2:74: N3332 
N 4:302. 
Valonraceae Е TI AÀAb2145 NOT Ab 2309 11.55 
peat- па Ee I а ЧОО РАНТА УУ S ан DOES 
biis oe ЗА c DR RURAL RET DE UN OL doe usa АН рна 
ucheéridéeae |... лл еы DELIS ТРАВИ МОГ Ab ZISE | 
менее ЕС ЧЕ ЧСА ОВА IO ee к И. 
Verbenarenei ое Т 4, Ab 3a:132, 377; № 1:290; N 2:64; М 
3: 307: N " 266. 
Метгисанасвав не | се Шул UA Авро | 1. 045220 6h 
Violaceae а а ee ese T3 AbG6:22:N.|[:252:N 245: М 3:232: 
N 4:205. 
MijtRcede o Ul oes ea Ha ed AE T3 Ab $427: N E230: N 241: N3211: 
N 4:1 
bio. ol AMENS у... T3, Ab 4: 312::.N 2:37, 
уојудбаграе |... ЕИ T-I-Ab 229 NOT IAB DII a 
VUE AGEL Se OT 
Мјатпомласеве ii OO 
WEDE LR ee a T 1, Ab 3:662, 1210 
Welwitschisicese os i не EE 
Winteranacesé:. o oso ул T 3, Ab 6:314; N 3:231. 
Wittrockiellaceae о NIOIDLONb255:58 4: 52x ту. 
WoronhlnaceBBe v а o аг Р RI A E E 
хае a О E Id uc cem rca ООО EC ae 
Aylandcenm uode T 1, Ab 1:480. 
Xvridacise Beh bs e и TT Ir Ab 4:182.N 1:61: N.2:9: N SIT 
ZADgIDeFaceae пр пи PV T2, Ab 6:10; N 1:90; N 2:12; N 3:53; N 
4:39 
LIGIER у, oa у. TA 2:16: 
ТУЙДА оао MOFI PURE I I I С Ва 
AYO Sl + LAG ЕНУ. 
Zysophyllacede | = = с; T 3, Ab 4:74, 353; N 1:207; N 3:187; N 


[Vor. 71 


see Bd Sal 


Bd 8:65. 
Bd 21:329. 


Bd 20d:174. 


Bd 3:28. 
see Bd Sal. 
Bd 2:51. 
Bd 13:419. 


Ва 3:225. 
see Bd Sal. 


Bd 8:91. 


Bd 15a:35. 


Bd 15a:541. 


Bd 3:362. 


Bd 19a:144. 


MM M — > ль 


= rere паа | 


TECHNIQUES FOR COLLECTING AQUATIC 
AND MARSH PLANTS! 


ROBERT В. HAYNES? 


Aquatic and marsh plants are those species 
occurring in substrates saturated with water most 
or all of the year. These substrates may be in- 
undated permanently or may have the water ta- 
ble at the substrate surface. This habitat often 
poses a barrier to the collector and special prob- 
lems in specimen preparation. As a result, aquat- 
ic and marsh plants are often inadequately col- 
lected and, therefore, poorly represented in 
herbaria. l 

When collecting for aquatic or marsh species, 
I examine almost every wet spot, pool, lake, or 
stream I encounter and wade to the plants, if 
necessary. The substrate is often quite muddy 
and I may sink to the knees or deeper. When the 
water is too deep to wade, I prefer using a small 
boat and then dragging the substrate with a rake 
or grappling hook (one constructed from pipe ca. 
20 cm long by 2 cm wide, coat-hanger, and rope 
ca. 10 m long is adequate). One can, of course, 
stand on shore and toss the grappling hook into 
the bed of plants, if the plants are fairly close. 
It is important to make complete specimens, 
including stems, leaves, roots, and reproductive 
structures — preferably mature flowers and 
fruits—of aquatic and marsh plants. Both sta- 
minate and carpellate fl ld be collected 
for taxa with imperfect flowers, e.g., Hydrochar- 

e Steril 4 ti А OPON ee ee wi 


пасеа p 
for those taxa, e.g., Lemnaceae, that are so rarely 
seen in flower that the taxonomy is based upon 
vegetative features. Some persons believe that 
aquatic habitats are visited so rarely that it is 
better to collect a sterile specimen than none at 
all. However, if the specimen cannot be deter- 
mined, it might as well be left in nature. 
Lahel data А 


1 . 


pecially important with aquatic 
Or marsh plants. Information other than normal 
locality data that should be included are depth 
of water; flow rate of water: range of leaf size; 
Whether leaves are submersed, floating, or emer- 
gent; color of flower; odor of flower; time of day 


а 


of flowering; whether flowers аге submersed, 
floating, or emergent; and whether fruits are sub- 
mersed, floating, or emergent. 

Care must be taken to prepare quality speci- 
mens of aquatic vascular plants. They normally 
do not need to be pressed immediately following 
collection. I usually wrap each collection in dry 
newspaper and store these wrapped collections 
in plastic bags or styrofoam chests. These bags 
or chests are kept in the shade to prevent over- 
heating the plants. The moisture from the spec- 
imens is adequate to moisten the newspaper and 
to keep the specimens fresh and pliable for sev- 
eral hours. The plants can be pressed later that 
day when one has ample time to do the task 
carefully. 

Several taxa, e.g., Heteranthera and Utricu- 
laria, have delicate flowers that are destroyed or 
from which the corolla falls offin the bag or press. 
Two or three flowers of these taxa should be 
preserved in 50% aqueous methyl or ethyl al- 
cohol solution. Plastic 20 ml vials are excellent 
for this. Also, the “duckweed press," which is 
discussed later, works well for pressing these 


г 


Мапу р і а t d marsh plants have 
fairly large bulky stems, leaves, and subterranean 
parts. These large organs pose special problems 
when pressing. First, all parts of a specimen, oth- 
er than the bulky structures, will have inadequate 
pressure in the press; as a result, they shrink 
during the drying process. This shrinking can be 
corrected by placing layers of newspaper on the 
flatter parts while the plant is in the press. Sec- 
ond, these bulky organs tend to have large 
amounts of water and, therefore, dry slowly—so 
slowly, in fact, they may completely decay while 
in the press. This decaying can be eliminated by 
splitting the large structures before pressing and 
by changing the corrugates and blotters of the 
press each day. 

Delicate aquatic plants, especially those that 


_ I wish to thank Lawrence J. Davenport, Charles N. Horn, Donald Les, Marvin L. Roberts, Ronald L. Stuckey, 


Critical comments are grea 


John W, Thieret, Edward G. Voss, and John H. Wiersema for reviewing the manuscript. Their suggestions and 


2 De tly appreciated. 
partment of Biology, University of Alabama, University, Alabama 35486. 


ANN. Missouri Bor. GARD. 71: 229-231. 1984. 


230 


grow submersed, need to be floated (see expla- 
nation below) onto a sheet of paper prior to press- 
ing. I prefer to float the specimens onto half sheets 
of newspaper. These sheets are then placed be- 
tween folded newspaper—the “pressing pa- 
per” —for pressing. I float and field press these 
delicate specimens at the time of collecting, rath- 
er than in the evening, so that I may use the body 
of water in which they were growing for floating. 
This procedure eliminates the need to take a pan 
for specimen floating on collecting trips. 

The specimens are floated by placing the plant 
in water with the half sheet of newspaper below. 
After the plant is positioned properly on the pa- 
per, it is held in place to the top of the paper by 
the thumb as the newspaper is slowly lifted from 
the water. The paper is lifted in a manner so that 
water flowing from the paper separates the leaves, 
and the specimen adheres to the wet paper. 

Some plants often have mucilages, either pro- 
duced by the plant itself or by epiphytic algae, 
and, as a result, will stick to the half sheet and 
pressing paper upon complete drying. To prevent 
this sticking, I place the folded pressing paper 
between two sheets of blotting paper with min- 
imal pressure and leave them for four to six hours 
at ambient temperature. This time period allows 
excess water to be absorbed by the blotting paper 
but does not allow adequate time for complete 
drying of the specimen. The specimens are then 
carefully removed from the pressing paper (in- 
cluding the half sheet), placed between unused, 
dry, folded paper, and p d ual. Thi 
transfer is done at the end of the collecting day 
when all other pressing is accomplished. Speci- 
mens rarely stick to the paper following this treat- 
ment. This procedure works quite well with such 
delicate species as those of Utricularia. Taxa that 
are extremely mucilaginous, e.g., Brasenia, may 
still stick to the paper even after this procedure. 
My students and I have found that these speci- 
mens are less likely to stick if they are pressed 
in folded nylon screen (available at local hard- 
ware stores) rather than paper. The screen is then 
placed between two blotters of the press. This 
screen should be used only with rather coarse 
taxa because it will damage delicate tissue. 

If there is no time to change the paper, then 
one may wish to place waxed paper on one side 
only of the specimen to prevent it from sticking 
to the top sheet of the pressing paper. I do not 
use this technique, since the specimen will stick 
to the sheet used for floating. If the waxed paper 
technique is utilized, then the collector must float 


nan 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 
the specimen onto some good quality paper, such 
as bond typing paper or herbarium paper. Waxed 
paper works quite well with vegetative parts, but 
it will stick to delicate corolla lobes, such as thos 
of Utricularia. These corolla lobes, however, do 
not stick to newsprint. Thus, a small section of 
the waxed paper should be torn off so that the 
waxed paper will not cover the corolla. 

When pressing plants with whorled, dissected 
leaves, e.g., Myriophyllum, it is useful to section 
one node and float that node onto a small portion 
of paper. The number of leaves per whorl, as well 
as the number and arrangement of segments per 
leaf, are often important in these dissected-leaved 
plants. A single node floated onto a small section 
of paper makes observing these characteristics 
much less difficult. 

The shape of stems or petioles may be im- 

ortant for identification of aquatic or marsh 
plants. These structures have large lacunae and, 
as a result, may collapse during pressing. There- 
fore, cross sections of stems and petioles should 
also be pressed to indicate the shape. 

Specimens o eae are often very poorly 
prepared. Wads of these plants—as well as snails, 
insects, small sticks, and other debris—are often 
smashed between folded newspaper during usual 
pressing. One obtains, from such a preparation, 
a mass of individuals seemingly welded together. 
Duckweeds are much better prepared by storing 
them in 50% methyl or ethyl alcohol in the field 
and by pressing them later in the laboratory. 1 
take into the field 25—30 plastic bottles, each with 
a capacity of ca. 250 ml. At least one-third of 
these bottles is filled with absolute methyl ог 
ethyl alcohol. When a population of Lemnaceae 
is located, the plants are collected by skimming 
a tea strainer or dip net (available at aquarium 
stores) along the surface of the water. I fill à bottle 
about half full with the plants. Then an aqueous 
solution of ca. 5096 (v/v) methyl or ethyl alcohol 
is prepared and the bottle is filled with this 50" 
lution. I use the water in which the plants Were 
growing to prepare the solution. The plants 
remain without deterioration for several weeks 
The chlorophyll, of course, will be bleached ov 


ain 


cnch ac 


back in the laboratory, and following ident 
cation, the specimens are sorted by taxon ОП 
standard index cards and are pressed. S 


tes 
can be made from pressing сог Aex cards 


cut into 


I do not use blotters or newspaper, but if they d 


e c 


ы————=—„ —— 0 


ћ 4 


1984] 


are used, they would be cut to sizes equal to the 
index cards. Neither frames nor straps are used 
with the press. Instead, one rubber band (ca. 7 
mm wide and 75 mm in diameter) is placed 
around the press in the short direction for pres- 
sure. This rubber band gives enough pressure to 
keep the plants flat but not so much that the 
plants are welded to the paper. When the spec- 
imens are dried, two or three cards of each taxon 
prepared by this technique are placed inside a 
packet constructed from 100% rag typing paper 
and the packet is glued onto an herbarium sheet. 

Members of the Nymphaeaceae and Nelum- 
bonaceae are mostly large and difficult to press. 
Since flowers and fruits are important in the tax- 
onomy of these taxa, these structures should be 
pressed open or split lengthwise so that the in- 
ternal structure can be observed. One or two 


HAYNES—COLLECTING AQUATIC PLANTS 231 


leaves are all that need be pressed for each spec- 


B 


en. 
Michaelis (1981) has proposed using 5096 glyc- 
erol (v/v aqueous) as a storage medium for all 
aquatics prior to pressing. I can see no value to 
such an approach because it would necessitate, 
for prolonged trips, transporting large amounts 
of glycerol. Also, specimens carefully processed 
by usual pressing techniques are equal to or bet- 
ter in quality than those prepared with the glyc- 
erol technique. This technique might be of value 
when one wishes to save some of the material in 
the three-dimensional form for teaching purpos- 
es, however. 


LITERATURE CITED 


MICHAELIS, F. B. Preservation of freshwater 
macrophytes ede лдан Aquatic Bot. 11: 389. 


WOOD AND STEM ANATOMY OF BERGIA SUFFRUTICOSA: 
RELATIONSHIPS OF ELATINACEAE AND BROADER 
SIGNIFICANCE OF VASCULAR TRACHEIDS, 
VASICENTRIC TRACHEIDS, AND FIBRIFORM 
VESSEL ELEMENTS 


SHERWIN CARLQUIST! 


ABSTRACT 


Bergia suffruticosa Fenzl provided sufficient lower stem and upper stem material to compare wood 


and stem anatomy to those 


of putatively related families: Clusiaceae (including Hypericaceae), Fran- 


keniaceae, haa and Haloragaceae. ож only Clusiaceae proves close; resemblances to 
2 1 LA | +1 e £e + + fa 


ates, presence of t 

eleme nt type, presence of vasicentric "ове and fibri 

iseriates, vertical orientation of scala 

e of brownish compounds in par 

. Other features such as seed anatomy ва the HD of eee ж 
siaceae 


iform vessel elements, predominance of uni- 
riform vessel- -ray pitting, absence of 


де 


Clusiaceae. The presence and nature of vasicentric tracheids in Bergia suffruticosa and С 
prompts an examination of this cell type. Vascular tracheids are defined here as: (1) present in Wwe 


only (except for so 


species are frequent or preponde 


ome genera in which all wood is like latewood); (2) not always present near vessels; 


ments in 


m 
4) may be associated a foe (with various types of pitting) or 


tend to be unlike the shrubs (predominantly from families in which herbaceous 
rant) in which vascular tracheids occur. Vascular tracheids as defined 


here do not have vest y 1 perforations; cells with such perforations are regarded as vessel elements 


by definition. Fibrifor 


and wide vessel Meine) have been reported i in other groups, notably vines, where fibriform d 
of 


elements may result from vessel dimorphism (lateral enlargement 


narrow vessels preempted by the 


great widening of a few vessels). Fibriform vessel elements may also occur in some nonvining families, 


such as Hydrophyllaceae, however. 


Mrs e mee Bes are available on stem 
atomy (m mary stem) of Bergia suf- 
puse Ace A Chalk, 1950), the nature of 
secondary xylem has not been described for this 
species, the only species of Elatinaceae that could 
be considered at all woody. The material kindly 
provided me by Dr. Peter H. Raven included 
stems and ll roots. Roots were not large 
enough to make study of root wood feasible. No 
material of leaves or flowers was provided, and 
those structures are therefore not included in the 
present study. 
Although wood anatomy is often not decisive 
in delineating relationships of dicotyledon fam- 
ilies, wood anatomy of Bergia suffruticosa proves 


unusually valuable in indicating the probable re- 
lationships of Elatinaceae. The affinities of Ela- 
tinaceae have been claimed by various authors 
to include such families as Clusiaceae (including 

the allied 


tales), Myrtales, and Cornales—according to 
system of Thorne (1976). Opinions. are not eq 
ly divided on which of these groups is most closely 
related to Elatinaceae. A few nd have fa- 
vored placement near Frankeniaceae and Tam- 


aricaceae (e.g, Wettstein, 1935). Hutchinson 


ov Santa Ana Botanic Garden and Department of Biology, Pomona College, Claremont, California 


ANN. Missouri Bor. GARD. 71: 232-242. 1984. 


„ы — 


—, 


6 


1984] 


(1959) claimed affinity of Elati with Cary 
ophyllaceae. However, more recent phylogeniss 
opt unanimously for placement of E 
Theales near Clusiaceae (Cronquist, 1981; жег 
gren, 1980; Takhtajan, 1980; Thorne, 1976). The 
families Clusiaceae and Hypericaceae are very 
close and are treated as a single family by most 
authors, such as the four just cited. I will follow 
that treatment in my discussion, and I will use 
the name Clusiaceae for the combined family. 
The wood of Bergia suffruticosa demonstrates 
an unusual near-continuum in morphology be- 
tween wide vessel elements, fibriform vessel ele- 
ments, and tracheids. This phenomenon proves 
referable to concepts variously designated by 
particular terms. The concepts of vascular tra- 
cheids, канш  tracheids, оюп уен! ЄР 
ments, and v nd 
contrasted. The functional nature of these de 
nomena is also explored. Further work to refine 
definitions of these cell types is needed. 


MATERIALS AND METHODS 


Of the liquid-preserved specimens of Bergia 
suffruticosa placed at my disposal, one series, 
vouchered by the specimen B. C. Daramo 6 
MO), was selected because xylem accumulation 
was maximal and straight stem portions suitable 
for sectioning were present. This material was 
collected from a shrub 90 cm tall growing near 
the uam Bridge on the Benu River near Nu- 

man, Gong ngola, Nigeria. The liquid-preserve 
material was provided as bottles labeled “stems” 
and "roots" respectively. However, sections of 
the latter revealed presence of pith and endarch 
xylem. Therefore these segments have been des- 
ignated “lower stems,” and those labeled as stems 
have been designated as “upper stems" in the 
descriptions that follow. Bergia suffruticosa is 
M from near the base; the “lower stem" 

Ow most of this branching whereas the up- 
Per stems, much smaller in diameter, are taken 
from above most of this branchin 


sd iid of vessel walls and of sec- 
ER ordinary rotary microtome or sliding 
Fs ome techniques. Such small stems are, 
огеоуег, difficult to handle with a sliding mi- 
e Therefore a new method in which in- 
tration and embed paraffin are preceded 


CARLQUIST —STEM ANATOMY OF BERGIA 


233 


by treatment of the material in ethylene diamine 
(Carlquist, 1982) was used. The softening action 

of the ethylene diamine was hastened mide placing 
the materia a paraffin oven (60°C) 
for four hours. Sections were , stained cat a saf- 
ranin-fíast green combination. 

Macerations were prepared from pickled ma- 
terial with Jeffrey's Fluid. Macerations were 
stained with safranin. 

For comparison with Bergia suffruticosa, wood 
of side species of Vise git was sectioned. 
These w of the Rancho San- 
ta Ana с Garden bog sample collection, 
but are designated by serial numbers of the U.S. 
National Museum, which contributed them to 
that godes This material did not require spe- 
cial softening techniques and was sectioned on a 
sliding microtome and stained with safranin. 
Macerations were prepared with Jeffrey's Fluid 
and stained with safranin. 


ANATOMICAL DESCRIPTIONS 


Lower stem (Figs. 1-9). Growth rings absent; 
larger vessel elements tend to be progressively 
wider in diameter (Fig. 1). Vessel elements range 
up to 230 um in diameter. Perforation plates are 
simple. Cells that appear to be imperforate tra- 
cheary elements as seen in transection include 
both fibriform vessel elements (Fig. 3) and tra- 
cheids. Fibriform vessel elements are more nu- 
merous than the tracheids but grade into them, 
as well as into the wider vessel elements. Because 
there is a complete intergradation among classes 
of tracheary elements, none of these classes can 
be isolated for the purposes of measurement, and 
only extremes can be quantified. Wider vessel 
elements are about 320 um long, tracheids are 
about 600 um long. Wall thickness of wider ves- 
sels is 7 um, wall thickness of tracheids, 3 um. 
Intervascular pitting of vessels is composed of 
alternate pits that can be polygonal in outline 
where crowded (Fig. 7), otherwise circular in out- 
line or somewhat laterally widened (Fig. 6); pits 
average about 6 um in diameter. Vessel-ray pit- 
ting is composed of circular or elongate pits, the 
latter often elongate parallel to the long axis of 
the stem (Fig. 6), a kind of scalariform pattern. 
Vessel-ray pitting is bordered on the vessel side, 
simple on the ray cell side. Axial parenchyma is 
in strands of two cells. Axial parenchyma is often 
beside larger vessels (Fig. 4), but can also be scat- 
tered among other tracheary elements (Fig. 5). 
Because the fibriform vessel elements are so 


234 


abundant, virtually all axial parenchyma may be 
adjacent to vessel elements and is therefore para- 
tracheal. Rays are uniseriate to multiseriate (Fig. 
2), wide multiseriate rays are infrequent. Rays 
mostly have lignified walls, a few have thin non- 
lignified walls (Fig. 2). Ray cells are mostly erect 
or square; a few procumbent cells are present, 
but these are only a little longer radially than tall 
axially. Some ray cells are idioblastic and bear 
tanninlike compounds (Figs. 2, 4). Secretory ca- 
nals are absent from rays. Wood is nonstoried. 
Druse-bearing cells and tannin-bearing cells oc- 
cur idioblastically in both cortex and pith (Figs. 
8, 9). Starch grains are frequent in parenchyma 
cells in both cortex and pith. Protophloem fibers 
are present (Fig. 8) and tend to be scattered in 
groups rather than as a continuous cylinder 
around the stem 


Upper stem (Figs. 10-12). Widest vessels 
about 70 um in diameter (Fig. 10). Perforation 
plates simple. Vessels are quadrangular in tran- 
sectional outline near pith, as claimed by Met- 
calfe and Chalk (1950), but rounded in outline 
otherwise, suggesting that very little secondary 
xylem was present in the material studied by 
Metcalfe and Chalk. Length of wider vessel ele- 
ments is about 400 um; length of tracheids is 
about 530 um. Fibriform vessel elements are 
present, somewhat less abundant in comparison 
to wider vessel elements and tracheids than they 
are in the lower stem. Pits on vessel elements are 
alternate, about 5 um in diameter. Fully bor- 
dered pits are present on tracheids (Fig. 12). Ax- 
ial parenchyma is sparse. Rays are mostly uni- 
seriate (Fig. 11), but some biseriate rays are 
present. Very few rays are more than two cells 
wide (a maximum of four cells wide was seen). 
Ray cells are erect only, no square or procumbent 
cells were seen. Secretory canals are absent in 
rays. Wood is nonstoried. Druses are present in 
pith and cortex; solitary crystals are present as 
chambered crystals in strands of phloem paren- 
chyma. Tanninlike compounds are present in 
idioblastic cells in both cortex and pith, also in 
xylem parenchyma. Protophloem fibers are pres- 
ent, forming a nearly complete cylinder inside 
the cortex. 


RELATIONSHIPS OF ELATINACEAE 


One can consider Clusiaceae, Tamaricaceae— 
Frankeniaceae, Lythraceae, and Haloragaceae as 
comprising the four groups to which Elatinaceae 
is compared in the present paper. All of these 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


families except Clusiaceae have libriform fibers 
with simple pits, in contrast to Elatinaceae, in 
which tracheids bearing fully bordered pits are 
present (Fig. 12). While this discrepancy does not 
absolutely rule out a relationship, most families 
of dicotyledons do not have a wide range of pit- 
ting in imperforate tracheary elements. 
Myrtalean affinity of Elatinaceae seems ruled 
ig additionally because Elatinaceae lacks in- 
raxylary phloem and vestured pits, features 
бит in Lythraceae (Baas & Zweypfenning, 
1979). 


An undetermined Australian species of Fran- 
kenia represented in my wood slide collection 
has rayless wood, a feature not present in Bergia 
suffruticosa. Tamarix has unusually wide rays 
(10-25 cells wide), but has few or no uniseriate 
rays according to Metcalfe and Chalk (1950). 
Tamaricaceae has storied wood. Thus Franken- 
iaceae and Tamaricaceae contrast with Elatina- 
ceae. 

Although wood of Haloragaceae does not differ 
sharply from that of E except in having 
simple pits in imperforate tracheary elements, 
other differences in stem anatomy may be found. 
For example, Haloragaceae have crystals in tri- 
chomelike cells in the cortex; such cells are ab- 
sent in Elatinaceae. The distribution of proto- 


phloem fibers in Haloragaceae (where such fibers 


are rare) is unlike that of Elatinaceae. 


Affinity of Elatinaceae with Clusiaceae, the re- _ 


lationship claimed for Elatinaceae by recent phy- 
logenists, can be supported by numerous wood 


features, in contrast with the above comparisons. - 
Imperforate tracheary elements with fully bor- | 
16, right; 19, right) - 
exactly like those on vessel elements (and thus - 
tracheids) occur in both families. The occurrence - 
ofa tracheary element type intermediate in mor + 
phology between tracheids and wide vessel ele- | 
ments, termed fibriform vessel elements above | 
can be seen in Hypericum (Fig. 19, left) as well $ 
as in Bergia suffruticosa (Fig. 3). The occurrence i 
of vasicentric tracheids in Calophyllum and oth- I 


dered pits (Figs. 15, right; 


er Clusiaceae is an allied phenomenon discu 


below. Rays in Clusiaceae are most often uni- 1 
seriate or biseriate (Figs. 14, 15), although some" 


what wider rays have definitely been repo 
The presence ofa few wide rays in the lower stem 
of Bergia suffruticosa (as compared to the ШРре 
stem) may be an interpolation related to stare 
and water storage, and probably does not rep- 
resent any remnant of any hypothetical bor 
rayed condition. The predominant erectness 


КУ | 


== 


-— 


—— 


— 


m Map €—Á—— 


4 


1984] CARLQUIST—STEM ANATOMY OF BERGIA 


= - ~ 


ү my m 
— "a 


TP aros. 


9! 


E 
Li 
А; 


FIGURES 1-5. Sect ons of lower stem of Bergia suffruticosa, Daramo 6 (MO).—1. Transection; note wide 

· Ta ови section. Wide multiseriate ray, center; other rays are mostly ae or biseriate. — 3. 

f radial каш ‚ Showing two tracheids (left) and three fibriform a жилы with small perforation 

right), — section; ray cells filled with tanninlike deposit.—5. T ection. Axial parenchyma cells 

Sn ter and аш, vessel, lower left. Figures 1, 2, magnification scale roni Figure 1 (finest divisions — 
Figures 3-5, magnification scale above Figure 3 (divisions = 10 um). 


near cen 
10 


ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


2 


arch, he: лор fibers, ri 
‘ena 7 2. Sections of upper s giri Transection of second. ylem, pith s; P ripe 
Ta наа ан гауѕ уегу аат Portions of tracheids from radial section; pits fully order [ 
6—9, 12, magnification scale above Figure 3. Figures 10, 11, magnification scale above Figure 


1984] 


ray cells in Bergia suffruticosa is doubtless re- 
lated to its stature as an herb, judging from char- 
acteristics of herbs and herblike plants discussed 
earlier (Carlquist, 1962). Diffuse parenchyma, as 
in Elatinaceae, can be found in a few Clusiaceae, 
such as Mammea (Metcalfe & Chalk, 1950), but 
a wide range in parenchyma types exists in Clu- 
siaceae, ranging from apotracheal bands, as in 
Calophyllum (Figs. 13, 18) to absent, as in Hy- 
pericum (Fig. 20), or paratracheal (as can be 
claimed for Bergia) in Tovomitopsis (Metcalfe & 
Chalk, 1950). Vessel-ray pitting in Bergia suf- 
Јтипсоза may be scalariform, the pits elongate 
vertically (Fig. 6); this can be found in Clusiaceae 
also (Fig. 17). Presence of brown-colored com- 
pounds, presumptively regarded as tanninlike 
above, is widespread in dicotyledons, but these 
are very abundant in Bergia suffruticosa and in 
Clusiaceae. Secretory canals are absent in rays of 
Bergia, but they are absent in many Clusiaceae 
also. Druses and solitary crystals are widespread 
in dicotyledons; both types occur both in Elatina- 
ceae and in Clusiaceae, however. The major rea- 
sons for allying Elatinaceae with Clusiaceae lie 
in gross morphology, the more important wood 
features outlined above, and in seed anatomy 
(Corner, 1976). Because of parallel aneuploidy 
in Clusiaceae and in Elatinaceae, chromosome 
number . °1 +: а 1 . 1 . 1D 
1975), 


LÁ X , 


VASCULAR TRACHEIDS, VASICENTRIC 
TRACHEIDS, FIBRIFORM VESSELS, AND 
VESSEL DIMORPHISM: DEFINITIONS 
AND SIGNIFICANCE 


‚ Among the anatomical features for which list- 
ings of families are given by Metcalfe and Chalk 
(1950, 1983) is presence of vasicentric tracheids. 
This feature, however, seems not to have re- 
ceived extensive comment in any paper. Vasi- 
centric tracheids may be closely allied to other 
hei of tracheary elements. Consequently, def- 
nitions and discussion are offered here. This dis- 
cussion may be regarded as preliminary, and re- 

€nts and modifications are to be expected. 


Vascular tracheids. Vascular tracheids are 
vessel elements so narrow that they lack perfo- 
= plates. Criteria for their recognition in- 
~ the following. (1) They occur in woods that 

ve sharply demarcated growth rings, and the 
Marien tracheids always occur in latewood only. 

ceptions to this may be found in woods that 
"Present such a high degree of xeromorphy that 


CARLQUIST—STEM ANATOMY OF BERGIA 


237 


all wood in those species is comparable to late- 
wood, as in Loricaria thuyoides (Carlquist, 1961) 
or globular cereoid cacti (Gibson, 1973). (2) Vas- 
cular tracheids are known only in highly spe- 
cialized wood in which imperforate tracheary 
elements have simple pits only and therefore are 
libriform fibers. A minor exception is formed by 
Calycanthaceae, in which fiber-tracheids (with 
quite vestigial borders, however) are present and 
in which vascular tracheid ily distinguishabl 
from the fiber-tracheids occur (Carlquist, 1983). 
(3) Vascular tracheids tend to be the same length 
as the vessel elements in any given sample, but 
are appreciably shorter than the libriform fibers 
with which they are associated. When comparing 
vascular tracheids to vasicentric tracheids (be- 
low), distribution within the wood is the most 
important of the above criteria. Thus, although 
Calycanthaceae are listed by Metcalfe and Chalk 
(1950, 1983) as having vasicentric tracheids, the 
family actually has vascular tracheids, formed 
only in the latewood of growth rings. The draw- 
ing of a transection of Chimonanthus fragrans 
wood by Metcalfe and Chalk does not include 
any indication of vasicentric tracheids (which are 
denoted by a special pattern in drawings of the 
woods that do have vasicentric tracheids else- 
where in their book). Vascular tracheids are found 
in such families as Asteraceae (Carlquist, 1960), 
Cactaceae (Gibson, 1973), and Scrophulariaceae 
(Michener, 1981). Functionally, vascular tra- 
cheids offer the safety of true tracheids under 
drought conditions in that air embolisms cannot 
spread from one vascular tracheid into another, 
whereas air bubbles can spread from one vessel 
element into numerous vessel elements subad- 
jacent or superadjacent. Tracheary elements like 
vascular tracheids but with vestigial or pitlike 
perforations are not admitted as vascular tra- 
cheids here, but are considered vessel elements 
if any perforation occurs. Vascular tracheids 
probably occur most commonly in drought-de- 
ciduous shrubs; their occurrence is not familiar 
to those who study wood of trees exclusively. 


Vasicentric tracheids. Judging from system- 
atic occurrence (Metcalfe & Chalk, 1950: 1351; 
1983: 205), vasicentric tracheids must have aris- 
en more than о licotyledons, and therefore 
How- 


+ 
nee in 


+ My 


may p І 
ever, the following criteria тау be used to iden- 
tify and define vasicentric tracheids. (1) Vasi- 
centric tracheids are imperforate cells that bear 
fully bordered pits like the pits of vessel elements 
in the woods in which they occur. (2) Vasicentric 


re solitary 


17. Porti 
Figures 13. 


their bordered pits.— 


center, pits vertically elongate forming a scalariform pattern. 


l. Figures 15-17, magnification scale above Figure 3. 


16369, wood sections.— 13. Transectional vessels à 


2. 
ul 
а 
га 
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Z 
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E 
Q 
m 
z 
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О 
N 
2 
2 
E 
T 
E 
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О 
2 
2 
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‚ Showing character of these two cell types and 


Calophyllum vitiense, USw- 
; vessel-ray pitting at 


umre 


ТТА 


nw? 


FiGures 13-17. 
14, magnification scale above Figure 


of radial section 


1984] CARLQUIST—STEM ANATOMY OF BERGIA 


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FIGURES 18-21. 
centric tracheids are 
upper vessel. 19 


narrow, n 
Figure 18 


mon 21. Tangential section; rays are mostly uniseriate. Figure 18, | scale above 
IVIS 
above Fig 


5. — 
ions = 10 um). Figure 19, magnification scale above Figure 3. Figures 20, 21, magnification scale 
ure 1. 


240 


tracheids are distributed around vessels and ves- 
sel groups. (3) Vasicentric tracheids tend to be 
at least somewhat longer than vessel elements in 
any given wood. (4) Vasicentric tracheids are not 
distributed with relation to growth rings and are 
present in earlywood as well as in latewood. Vasi- 
centric tracheids may occur in woods without 
growth rings (e.g., Calophyllum, Fig. 13). The 
diffuse porous woods in which they occur are not 
so highly xeromorphic that the entirety of the 
wood may be regarded as a kind of latewood, a 
phenomenon true of the wood of cacti, cited 
above, in which vascular tracheids occur. (5) 
Vasicentric tracheids tend to be wider than the 
remaining imperforate tracheary elements in 
woods in which they occur (Figs. 15, left; 16, left; 
18). (6) Vasicentric tracheids tend to be more 
densely pitted than the remaining imperforate 
tracheary elements in woods in which they occur 
(Figs. 15, left; 16, left; 19). 

Vasicentric tracheids may grade from cells very 
similar to the imperforate tracheary elements in 
the woods in which they occur to very unlike the 


Ifa wood has true tracheids, vasicentric tracheids 
would be indistinguishable from true tracheids, 
and by definition we can say that vasicentric tra- 
cheids are absent in woods with true tracheids. 
Calophyllum (Figs. 13-18) has what may 
termed fiber-tracheids that are more slender, 
longer, and more sparsely pitted than the vasi- 
centric tracheids in that wood. This situation may 
also be found in Asclepias albicans Watson. On 
the other hand, Connarus has vasicentric tra- 
cheids markedly different from the libriform fi- 
bers which form the ground tissue of wood in 
that genus (Dickison, 1972). I have observed as- 
sociation of vasicentric tracheids with libriform 
fibers in Oceanopapaver neocaledonicum Guil- 
laumin, a member of Capparaceae. 

Hypericum galioides (Figs. 19-21) has fiber- 
tracheids with bordered pits in addition to vasi- 
centric tracheids. However, there are also elon- 
gate vessel elements that resemble tracheids but 
that have small perforation plates (Fig. 19). These 
may be termed fibriform vessel elements because 
they are narrow, long, and with pointed ends as 
compared with ordinary vessel elements. Pres- 
ence of fibriform vessel elements is characteristic 
of Bergia suffruticosa, but in that species all im- 
perforate tracheary elements must be termed tra- 
cheids, andt 


be sai 


to occur. 
The functional significance of vasicentric tra- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


| 


[Vou 71 | 


cheids seems potentially much like that of vas- | 
cular tracheids. Vasicentric tracheids form ап ex- | 
cellent subsidiary conductive system in case of 
occlusion of vessels by air embolisms, theoreti- 
cally. Indeed, in many of the species with vasi- 
centric tracheids, vessels are notably large and 
therefore vulnerable (Calophyllum, Connarus, | 
Quercus). Other species with vasicentric tra- 
cheids occur in notably dry habitats (Asclepias 
albicans, О 
a subsidiary conducting system composed oft tra- 
cheids and thus safer than a system composed 
only of vessel elements i presumptively ni non- 
conductive libriform ve 
selective value. ноа vasicentric tracheids 
would be of high value, theoretically, precisely 
because of their distribution in wood: they sur- 
round vessels so that if the vessels are disabled, 
the three-dimensional conduction patterns are 
minimally rerouted. The potential significance of 
maintaining this network intact can be realized 
if one notes that libriform fibers (which presum- 
ably function little if at all in conduction) or гау 
cells frequently separate one vessel from another 
in a particular wood, so that a three-dimensional 
rerouting across such relatively nonconductive 
cells is not possible. This would seem an advan- 
tage of vasicentric tracheids over vascular tra- 
cheids until one takes into account that vascular | 
tracheids are formed in large numbers and are | 
often in association with very narrow vessels. | 
which are relatively safer than wider vessels, 50 | 
that rerouting of conduction in case of embo- 
lisms in narrow vessels is also likely to be min- 
imal. Vascular tracheids and vasicentric tra- 
cheids may be successful for many of the pss | 
reasons, but probably occur in different kinds о 
plants 


Fibriform vessel elements. This term pe 
originated by Woodworth (1935) to descr 
slender vessel elements, fusiform in shape " 
often longer than the ordinary vessel elemen 
they accompany in any given wood in which 
occur. Because the tips of these cells are poin 
the perforations are subterminal and о т? 
pear lateral thereby. Some fibriform vesse 
ments can be considered under the м 
vessel dimorphism below. Others, es c 
peart 
dimorphism. In Eriodictyon (Carlquist ©! - 
1983) and other Hydrophyllaceae ( o: и 
Eckhart, 1984), fibriform vessel elements 
present but vessel dimorphism we be 


— 


1984] 


occur: vessel elements intermediate in diameter 
are frequent. In the Hydrophyllaceae in which 
fibriform vessel elements occur, there is a con- 
tinuum not merely in diameter of vessel ele- 
ments, but between fibriform vessel elements and 
tracheids (or fiber-tracheids) in the genera Er- 
iodictyon, Turricula, and Wigandia. There may 
be an adaptive value for production of the nar- 
row fibriform vessel elements, for narrow vessels 
ought to be adaptive in plants of dry areas such 
as those occupied by Eriodictyon (Carlquist, 1966, 
1975). 


Vessel dimorphism. The term vessel dimor- 
phism was used earlier (Carlquist, 1981) to de- 
note the tendency in a vining family (Nepentha- 
ceae) for vessels to be either very wide or else 
very narrow and fibriform with a small perfo- 
ration plate (often only a little larger than a bor- 
dered pit). The latter class of vessel elements was, 
in that family, only slightly longer than the for- 
mer. This tendency can be found in other vining 
families of dicotyledons, such as Convolvula- 
ceae, in which Mennega (1969) termed the slen- 
der vessel elements “fibres” with “apertures” (= 
perforations) on their radial walls. These ele- 
ments also have bordered pits and thus do not 
differ from the wide vessel elements except in 
their shape and size. 

Probably the phenomenon of vessel dimor- 
phism applies to virtually all vining families and 
genera. It can be regarded as a byproduct of the 
production of very wide vessels, which are adap- 
tive in vining plants for reasons suggested else- 
Where (Carlquist, 1975). In this hypothesis, the 
Production of few but very wide vessels would 
preempt the widening of many vessel elements, 
Which thereby are destined to become fibriform 
Vessel elements. A slightly greater length for fi- 
briform vessel elements as compared with the 
wide vessel elements they accompany in a par- 

icular wood m may be expected simply because 
Slender cells tend to retain greater intrusive ca- 
Pacities than wide ones. Fibriform vessel ele- 
ments in a species with vessel dimorphism would 
делу form an effective part of the соп- 
чепуе system, albeit small in capacity when 
Compared to the very great hydraulic capacities 
9f the wide vessel elements. 

Obviously the characteristics of vessel ele- 
—X vascular tracheids, and vasicentric tra- 
к=, тау vary somewhat from any particular 

me, and thus generalizations are premature 
uently, the listing of vasicentric tracheids 


CARLQUIST—STEM ANATOMY OF BERGIA 


241 


given by Metcalfe and Chalk (1950, 1983) should 
be regarded as a starting-point for research, not 
as a summation. 


LITERATURE CITED 


Baas, P. & R. C. V. J. ZWEYPFENNING. 1979. Wood 
anatomy of the Lythraceae. Acta Bot. Neerl. 28: 
117-155. 

— 2 S. 1960. Wood с of Astereae 

mpositae). Trop. Woods 113: 

961. Wood anatomy of Inuleae (Compos- 

itae). Aliso 5: 21-37. 

. A theory of paedomorphosis in dicot- 

yledonous з» Phytomorphology 12: 30-45. 
1966. Wood anatomy of Compositae: a sum- 

ary, wi with comments on factors controlling wood 

evolution. Aliso 6(2): 25—44 

Ecological Strategies of Xylem Evo- 
lution. Univ. of California Press, Berkeley and 

London. 

1981. Wood anatomy of Nepenthaceae. Bull. 
Torrey Bot. Club 108: 324-330. 

. The use of ethylenediamine in soft- 
ening hard plant structures for paraffin sectioning. 
Stain Technol. 1-317 

1983. 


ood anatomy of Calycanthaceae: 
ecological and systematic implications. Aliso 10: 
427-441. 
. M. ЕСКНАКТ. 1984. Wood anatomy of 
Hydrophyllaceae. II. Genera other than Eriodic- 
tyon, with comments on parenchyma bands con- 
taining vessels with large pits. Aliso 10: (in press). 
& D.C. MICHENER. 1983. Wood anat- 
omy of Hydrophyllaceae. I. Eriodictyon. Aliso 10: 
397-412. 
Corner, E. J. H. 


1976. The Seeds of Dicotyledons. 
bridge 


CRONQUIST, A. An Integrated Syste em of Clas- 
sification of Flowering Plants. Columbia Univ. 


Press, New York. 
DAHLGREN, R. 1980. A revised system of classifica- 
giosp inn. Soc., Bot. 80: 91— 


1972. Anatomical studies in the 
e. II. Wood anatomy. J. Elisha Mitch- 
ell Sci. Soc. 88: 120-136. 
GIBSON, А. С. 1973. Comparative anatomy of sec 
ndary xylem in Cactoideae (Cactaceae). Biotro- 


124. 
DickisoN, W. С. 
nnara 


pica 5: 
HEYWOOD, V. H. 1978. Flowering Plants of the World. 
Mayflower Books, New York. 


HuTCHINSON, J. 1959. The Families of Flowering 
Plants. Volume 1. Dicotyledons. Oxford Univ. 
Press, Oxford 

MENNEGA, À. M. W. 1969. The wood structure of 
ae (Convolvulaceae). Acta Bot. Мееп. 
18: 1 

ен C. E & L. CHALK. 1950. Anatomy of the 

i ledons. Clarendon Press, Oxford. 

——— 1983. Anatomy of the Dicotyle- 
dons. Edition 2. Volume II. Wood Structure and 
Conclusion of the General Introduction. Claren- 
don , Oxford. 

MiICHENER, D. C. 1981. 


Wood and leaf anatomy of 


242 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 | 


Keckiella (Scrophulariaceae): ecological consid- THORNE, К. Е. 1976. A phylogenetic classification of 
i : 39-57. Angiospermae. Evol. Biol. 9: 35-106. 
RAVEN, P. Н. 1975. The bases of angiosperm phy- WETTSTEIN, R. 1935. Handbuch der Systematischen 
2 ik nd Wien 


— рана Ann. Missouri Bot. Gard. 6 Botanik. Franz Deuticke, Leipzig 
724-76 WOODWORTH, R.H. 1935. Fibriform vessel members 
ا‎ L. 1980. Outline of the classification in the Passifloraceae. Trop. Woods 41: 8-16. 
flowering plants Mc p phyta). Bot. Rev. 


ние 46: 225-3 | 


THE EVOLUTION OF DIOECY—INTRODUCTION!” 


GREGORY J. 


That flowers can be unisexual, and that pis- 
tillate and staminate flowers may be borne on 
separate plants of the same species (i.e., dioecy) 
has been recognized for some time. For example, 
dioecy was one of the 24 classes in Linnaeus’s 
sexual system of classification (1737, Genera 
Plantarum), and Darwin discussed dioecy at 
length in his 1877 book, The Different Forms of 
Flowers on Plants of the Same Species. Almost 
45 years later, C. and H. Yampolsky’s broad sur- 
vey of the angiosperms (1922, Biblioth. Genet. 
3: 1-62) confirmed that dioecy is not an aber- 
ration among angiosperms but is indeed wide- 
spread. They reported that 37 of 51 angiosperm 
orders have at least one dioecious species. In 
Spite of this, there was relatively little interest in 
dioecy through much of the following four de- 
cages, Ho However, in recent years the study of pol- 
inat biology in gen- 
eral—neo- natural history — have once again 
become popular scientific pursuits. With this re- 
awakening, there have been many new studies, 
and controversy has arisen regarding the impor- 
tance of dioecy and the evolutionary mecha- 
nisms promoting it. Some of these studies, and 
Some of the controversy, are presented in the 
Papers that follow. 

One result of this renewed interest has been 
the recognition that dioecy is more extensive than 
Yampolsky and Yampolsky’s original estimate 
of 3-496 of the angiosperm species. Estimates 
now range up to 28% for some regions (e.g., the 

оаа flora, see paper by Baker & Cox, be- 

low), but overall, David Lloyd estimates that 
about 10% of the angiosperm species are dioe- 


* The лач 


ANDERSON? 


cious (1982, Amer. Naturalist 120: 571—585). In 
fact, some of the species recently described as 
dioecious are not obviously so. For instance, my 
studies of Solanum (1979, Nature 282: 836-838; 
Anderson & Symon, **Dioecious species of Sola- 
num from Australia,” manuscript in prep.), and 
the short report included below by Bill Haber 
and Kamal Bawa, illustrate that there are a num- 
ber of taxa that are functionally, if not morpho- 
logically, dioecious, and that this seemingly ob- 
vious breeding system can be overlooked. 

In a similar fashion, renewed interest has led 
to reconsideration of the stability of sexual 
expression, a topic that is reviewed below by Carl 
Freeman, E. D. MacArthur, and K. T. Harper. 
Herbert Baker and Paul Cox consider another 
facet of the distribution of dioecy issue in a new 
analysis of the frequency of occurrence of dioecy 
in island floras. The study of islands has been of 
particular interest because some have been 
thought to have a very high percentage of dioecy 
(as indicated above). 

There has also been an increase in interest in 
experimental analyses of the evolutionary and 
ecological consequences of dioecy. This ap- 
proach is represented here by two papers. Spen- 
cer Barrett summarizes work from his lab on the 
influence of sex expression, population structure, 
and population distribution on mating success 
in two Aralia species. Tom Meagher uses Cha- 
maelirium luteum as a case study to discuss the 
impact of the different resource allocation re- 
quirements of androecious and gynoecious plants 
on the evolution of life eod characteristics of 


whole. 


Ly 


A : < 


ван. 


meeting (with the Sonic Society of America and the Am 
Ft 


1а State University i in August o 


of Plant Taxonomy annual 
erican Institute of Biological Sciences) held at The 
Bawa was not presented at the 


at the 


ts: K. Bawa, R. Bertin, J. Estes, C. 


‚ Т. Lee, and Т. Philbrick. I thank James Estes for helping set up thes = and Nancy Morin for 


encouraging this publication and for the final editing of the papers. rk in reproductive sys 
part by the National Science бије 1 (INT-7910959, BSR- зар ата 
Group UAS TI The University of Connecticut, Storrs, t 062 


ms symposiu was supported in 


ANN. MISSOURI Bot. GARD. 71: 243. 1984. 


tems and 


Connecticu 


FURTHER THOUGHTS ON DIOECISM AND ISLANDS! 
HERBERT G. BAKER? AND PAUL ALAN Cox? 


ABSTRACT 


Non-dioecious taxa are the floral majority, both in island floras and in those of the mainlands. This 
is true at all latitudes. Temperate zone islands have very low percentages of dioecious species. The 
percentages are somewhat higher in subtropical islands. Relatively high percentages of dioecism are 
found only in moist tropical islands or in floras that have had a moist tropical influence on their 
composition. Low islands in the tropics and rather arid islands in the sub-tropics and tropics have 
only small numbers of dioecious species in their floras. A multiple regression analysis shows that 
latitude and maximum height of islands together account for 82% of the variation in percentage of 


dioecism in our samples. Although autochthonous development of dioecism 
ge of dioe 


immigrant cannot be ruled out yet, the percenta 


in an hermaphrodite 


to the percentage in a probable source flora in a comparable climatic zone. This equivalence could 
result from parallel evolution but probably depends more upon the long-distance dispersal, establish- 
ment, and radiation of taxa, including dioecious ones. This may be facilitated for the dioecious taxa 


by “leakage” in the dioecious breeding system, by di 


spersal of multiple-seed units, by longevity and 


1.217. + as Be 4 


> 4" г (= r P я > a i ali1 ачыу bt Ahi сүтүм VI d 9 È 
In tropical regions, bird-dispersal of seeds particularly may have been involved in the stocking of 


forests on islands. 


Lately, there has been increased interest in the 
breeding systems of seed plants and, more re- 
cently, this has been concerned with the role of 
dioecism in the origin and maintenance of ad- 
aptation to various environmental conditions 
(Ornduff, 1966; H. G. Baker, 1976; Freeman et 
al., 1976, 1980; Lloyd & Webb, 1977; Webb, 
1979; Willson, 1979, 1982; Bawa, 1980, 1982; 
Bawa & Beach, 1981; Beach, 1981; Givnish, 
1980, 1982; Lloyd, 1980, 1982; Cox, 1981, 1982, 
1983; Thomson & Barrett, 1981; Ross, 1982). 

Among these considerations has been the sig- 
nificance of dioecism in those flowering plants 
that make up the floras of islands (Bawa, 1980, 
1982). Traditionally, it was temperate floras 
whose reproductive biology was studied, but as 
more attention is being given to islands in warm- 
er climes, it is important that we do not go too 


aM +1 A; 


that tropical 
islands are typical of islands in general. 

There is no difficulty in spotting dioecism or 
monoecism in wind-pollinated temperate zone 
trees and herbs, for the morphological differences 
between staminate and pistillate inflorescences 
are striking, being related to the very different 
functions of casting pollen into the wind and 
sieving pollen out from an aerial suspension, re- 


spectively. But making a quick diagnosis of the 
breeding system is not so easy with insect-pol- 
linated species, particularly in the tropics. Be- 
cause both staminate and pistillate flowers must 
attract the same visitors, they tend to be similar 
in appearance, sometimes even to the extent of 
having pistillate flowers that produce non-func- 
tional pollen grains (e.g., Actinidia chinensis, 
Schmid, 1978; Solanum spp., Anderson, 1979). 

Some of the difficulty that this has produced 
in attempts to quantify the occurrence of dioe- 
cism in tropical floras is shown by estimates of | 
dioecism in the Hawaiian flora. Carlquist (1965) 
judged it to be 27.7% while Gilmartin (1968), 
basing her analysis on the flora written by Hil- 
lebrand (1888), reported it to be only 5%74 
striking discrepancy. Both authors claimed not 
to include gynodioecious and other deviant 
species in the percentage. Possibly the truth lies 
somewhere between these extremes, but we ust 
the Carlquist figure because Gilmartin, herself, 
suggested that Hillebrand (1888) may have had 
difficulty in identifying dioecism from impe" 
fectly preserved specimens or rarely collecte 
species. Also, Carlquist (1965) made studies 0 
many species and did not rely solely on the 
erature. 


_ 


1 We thank Irene Baker for help and assistance and Paul Groff for drawing to our attention the олив 
dispersal characteristics of Cotula. During this study Cox has been supported by a Miller Fellowship from 


Miller Institute for Basic Research in Science 
2 


partment of Botany, University of California, Berkeley, California 94720. 
3 Current address: Department of Botany, Brigham Young University, Provo, Utah 84602. 


ANN. MISSOURI Вот. GARD. 71: 244—253. 1984. 


~~ 


— 


1984] BAKER & COX—DIOECISM AND ISLANDS 245 
TABLE 1. Percentages of Dioecism in Islands and Corresponding Mainlands. 
Number % Number % 
of ioe- Comparable of Dioe- 
Category Island Species cism Mainland Species cism 
Cool temperate Iceland 472 3 British Isles 1,489 3 
Warm temperate Azores 391 2 Portugal 2,183 2 
Bermuda 136 4 Carolinas 3,274 4 
Ава аи ме "i : ) California 3,727 3 
Subtropical Guadalupe 116 3 Baja California 2,564 3 
Juan Fernandez 141 11 
Norfolk Island 153 12 
New Zealand 1,800 13 
Subtropical Dry Easter 30 0 
Tropical Dry Galapagos 439 3 
Tropical Low Bikini Atoll i 2 
Leeward Islands 40 0 
ra 171 4 
Chagos Arch. 71 1 
Tropical High 
i Réunion 838 4 
| Mauritius 682 11 
Seychelles 237 8 
Pacific Ocean Tonga 404 16 
Guam 279 13 
Samoa 539 17 
Auri 5o s. A Hawan 1,467 28 


DIOECISM AND ISLAND COLONIZATION 


In a thoughtful and thought-provoking paper, 
Bawa (1982) suggested that “dioecious taxa may 
have been disproportionately more successful in 
colonizing the (Hawaiian) islands." This would 

m to be out of accord with what Stebbins 
(1957) called “Baker’s Law" —that taxa that suc- 
cessfully establish seed-reproducing populations 
after long-distance dispersal will usually be self- 
compatible (or apomictic) and, by implication, 
show relatively low levels of inbreeding depres- 
his following self-pollination (H. G. Baker, 1955, 

967). A convenient assumption in the past has 
been that the original colonists of isolated islands 
b have been hermaphrodites or monoecious 
2M heir dioecious descendants developed out- 
i T. oe y (tnat 
^^ after arrival on the island) (Н. G. Baker, 1967; 
Гапашы, 1965, 1966, 1974; Gilmartin, 1968). 
a Bawa (1982) and others have pruned 
с = of genera in which dioecism is most likely 
been „еп after the Hawaiian islands had 
рой colonized by hermaphroditic plants, by 
ting to the existence of dioecious species in 


some of these genera outside of Hawaii. The sub- 
ject is also discussed by Godley (1979) for the 
New Zealand flora. 

Clearly, though, selection for outcrossing on 
islands could favor the evolution of dioecism 
since di m is more easily evolved than a 
functional self-incompatibility system. Mere al- 
teration of the hormone system in a plant can 
produce separate staminate or pistillate flowers 


+h h + 


even on ( р ) 
without genetical difference. Consequently in the 

. 1 >" po 7S DESEE, niiti 12.8 14 +h. ac: 0 
>“ “ 


a few genetic changes. 

We believe that there is merit in considering 
the floras of a wider selection of islands than just 
the favorit nd New Zealand. We have 
made use of floras written by specialists on the 
islands in question and have analyzed their 
species lists, with a special emphasis on **ocean- 
ic" islands that probably had no connection with 
a mainland since the origin of angiosperms. 

We have been up against some difficulties be- 
cause some published floras are little more than 
check-lists and, to some extent, it has been nec- 


.. 
214/211 2 


246 


h аи. ofa ] h 


essary to take t 
as indicative of its sexual condition in the flora 
in question. Even less satisfactory is the need to 
judge, in other cases, simply on the known char- 
acteristics of the genus. We have taken care to 
consider only species that are native to each par- 
ticular island, thereby excluding human intro- 
ductions that are especially numerous on such 
islands as Bermuda and other relatively densely 
populated places. 

Monocots and dicots were treated separately 
in our analyses but their subtotals are combined 
here for an overall representation of the propor- 
tions of hermaphrodite and monoecious versus 
dioecious species in each flora. Hermaphrodite 
and monoecious species are lumped because the 
point at issue is the potentiality, or lack of it, for 
` self-pollination—and monoecious plants have 
this to almost the same extent as do hermaph- 
rodites. Hermaphroditic species, in these calcu- 
lations, mean not only those species that have 
so-called “perfect?” flowers, but also those in 
which hermaphroditic flowers are accompanied 
by staminate flowers (andromonoecism), by pis- 
tillate flowers (gynomonoecism) or a mixture of 
all three (polygamy). Even gynodioecious and 
androdioecious species are counted in with the 
hermaphrodites, the criterion being that the pop- 
ulations include at least some plants that can 
function both as pollen-donors and ovule-pro- 
ducers. This is in contrast to the species that are 
regularly dioecious. Needless to say, the uncer- 
tainties are greater for little-studied tropical is- 
lands than for those that are extra-tropical and 


х 


statistics that have emerged are probably accu- 
rate enough for the genesis of some conclusions. 
There exists an estimate of the proportion of 
dioecious species in the world, published in 1922 
by Yampolsky and Yampolsky. This is very use- 
ful as a standard for comparison with local floras 
even though, as Bawa (1980) has pointed out, it 
is probably an underestimate because of the un- 
derrepresentation of tropical species in this ven- 
erable compilation. But it is most unlikely that 
anyone else will undertake the Sisyphean labor 
of producing an updated version, so, with our 
fingers crossed, we can use the 3—4% that the 
ү upon lecti t 


of the proportion of dioecious flowering plants 
in the world. All investigators are agreed that 
there is a positive partial correlation of dioecism 
with a woody habit (e.g., Bawa, 1980; Givnish, 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


1982), and this means that floras rich in trees 
and shrubs will tend to have a higher percentage 
of dioecious species. 


ISLAND FLORAS 
TEMPERATE ZONES 


The temperate zone islands whose published 
floras we have analyzed (Table 1) are those of 
cool temperate Iceland (Lóve, 1970) and the 
warm temperate Azores (Watson, 1870), Ber- 
muda (Britton, 1918), San Clemente (Raven, 
1963), and San Nicolas (Foreman, 1967). The 
last two islands are situated in the Pacific Ocean 
off the coast of California. Available lists of 
mainland floras that can be compared with these 
oceanic areas are, respectively, those of Great 
Britain (Clapham et al., 1962), Portugal (Pires 
de Lima, 1947), the Carolinas (Conn et al., 1980), 
and California (Jepson, 1928; Munz, 1963). We 
quote the number of species for California from 
Jepson (1928) but found the same percentage of 
dioecism by analyzing the flora by Munz (1963). 

We find that the proportions of dioecious 
species (Table 1) are no greater on the islands 
than they are on the mainlands and they are as 
low as Yampolsky and Yampolsky's (1922) world 
standard. 


SUBTROPICS 


Although the tropics are delimited by the 
Tropic of Cancer in the northern hemisphere and 
the Tropic of Capricorn in the southern hemi- 
sphere, there is no convenient boundary for the 
subtropics. Consequently, our categorization of 
Guadalupe Island (Eastwood, 1929), off the coast 
of Baja California, as subtropical and the exclu- 
sion of San Clemente and San Nicolas Islands 2$ 
warm-temperate is somewhat arbitrary. this 
connection, it is notable that the percentage of 
dioecious species in the flora of Guadalupe does 
not show any difference from those of the tem- 
perate zones and Guadalupe has the same рег 
centage of dioecious species as the Baja Califor- 
nia mainland (Wiggins, 1980). The Juan 
Fernandez islands, off the coast of Chile, Am also 
sub-tropical, although with tropical floristic af- 
finities (Skottsberg, 1922a, 19225, 19285). Нето 
with 11%, there is a definite suggestion of in- 
crease in the percentage of dioecism. 

New Zealand is difficult to categorize рош 
of its wide latitudinal range, and, even though! 
is largely temperate in climate, many of its fio- 
ristic affinities are with the more tropical ! 


| 


1984) 


to the north. This may have some responsibility 
for the rather 

in its flora (Godley, 1979) for, as we shall see, 
tropical islands that are large and mountainous 
are clearly richer in dioecious species than those 
of temperate regions. 

Norfolk Island is interesting because it repre- 
sents a sub-tropical island whose flora is prob- 
ably derived from the same sources as the trop- 
ical or subtropical elements of the New Zealand 
flora, and, although the flora of Norfolk Island 
(Maiden, 1904) is smaller in number of species 
than that of New Zealand, its үне of dioe- 
cious species is comparable— 12%. 


TROPICAL HIGH ISLANDS 


In the tropics, floras of the islands that have 
mountains bearing moist forests have relatively 
high percentages of dioecious species (Table 1). 
This is shown by the floras of Samoa (Setchell, 
1924; Christophersen, 1935, 1938), Hawaii (Hil- 
lebrand, 1888; Carlquist, 1965), Tonga (Yunck- 
er, 1959), and Guam (Stone, 1970) in the Pacific 
Ocean and the Seychelles (Summerhayes, 1926), 
and Mauritius (J. G. Baker, 1877) in the Indian 
Ocean. Only the flora of Réunion (Cordemoy, 
1895) in the Indian Ocean gives a surprisingly 
low percentage (4%). 

owever, this result for Réunion only accen- 
tuates an apparent slight difference between the 
percentages for the sampled islands of the Pacific 
and Indian Oceans, respectively. n may be that 


Oinae n 


y higher in Pa- 
Cific Islands than i in those of the Indian Ocean. 

This should be examined further and an attempt 
should be made to see if an explanation is to be 
found in the composition of the source floras or 
in the flyways of migratory birds. It has been 
Suggested that other islands in the Indian Ocean 
саз! of Madagascar serve not as destinations but 
rather as “safety nets" for vagrant birds (Ren- 
voise, 1971; Penny, 1971). Another possible ex- 
Planation for the low proportion of dioecism in 
Réunion may be a relative overabundance of 


groups зан as sri ee and grasses which are 
rarely dioec 


TROPICAL LOW ISLANDS 


Unlike the high, forested islands, there are 
many small islands in the Pacific and Indian 
bats that are topographically low, and, in these 
& such as Aldabra (Hemsley et al., 1919), 

os archipelago (Willis & Gardiner, 1931), 


BAKER & COX—DIOECISM AND ISLANDS 


247 


Bikini atoll (Taylor, 1950), and the Leeward Is- 
lands of the Hawaiian archipelago (Christopher- 
sen & Caum, 1931), the largest proportion of the 
flowering plant species occupy the littoral and 
strand zones. There is a striking lack of dioecious 
species on these islands (Table 1) and the same 
is dii: true for the strand and littoral floras 

hig forests (Long 


in zr 1968). 

The flora of the Aldabra islands, in the Indian 
Ocean, has been studied more completely than 
most low islands (Fosberg, 1971; Renvoise, 1971, 
1975; Woodell, 1979; Wickens, 1979) and its 
relationships to the bird fauna have been com- 
mented upon by Renvoise (1971, 1975) and 
Woodell (1979). These authors agree that the 
littoral flora of Aldabra had probably arrived by 
rafting whereas the inland flora had been intro- 
duced by stray birds or fruit bats. Penny (1971) 
has noted that Aldabra is not a wintering ground 
for any migrant waders (which, anyway, would 
not be likely to be important agents of inland 
fruit and seed distribution). 


TROPICAL AND SUBTROPICAL DRY ISLANDS 


The Galápagos are discussed separately here 
becau I dry for tropical “high” 
islands. Their fon (Wig iggins & Porter, 1971) 
shows a very low percentage of dioecism. It is 
notable that Rick (1966) performed a series of 

t 18 species 
with th hermaphrodite flowers i in the Galápagos and 
found no evidence of self-incompatibility, sug- 
gesting that outbreeding mechanisms are not 
strongly represented in the Galápagos flora. 

Easter Island, being extremely isolated at a dis- 
tance of 2, 300 miles from the coast of Chile, has 
avery (Skottsberg g, 1928a), 
even though it reaches a height of 1 969: feet (600 
meters). The climate is subtropical, and, because 
of its volcanic rocks and steep slopes, the land- 
scape of Easter Island is arid (Skottsberg, 1928a), 
so it qualifies as a subtropical counterpart to the 
tropical Galapagos islands. The flora is predom- 
inantly herbaceous. Of the 30 angiosperm species 
present, none is dioecious; this is in agreement 
with our results for the Galapagos. 


TROPICAL WOODY FLORAS 

The only Еси of a complete tropical main- 

1 Wi th those 

of the islands is ! that by Croat (1978, 1979) for 
Barro Colorado Island, which, prior to the flood- 


< 
RE 


; 4n 


FIGURE 1. Graphical representation of percentage 
ff AS i 2 ч 22 A 8 1 44 E | 4 + 


island height in meters and distance from the equator 
easured in degrees latitude for 22 different archipel- 
i i ) San 


us rm 
waii), (12) Bikini, (13) Aldabra, (14) Ch 
ago, (15) Azores, (16) Seychelles, (17) Galapagos, (18) 
Tonga, ( ek е , (20) Réunion, (21) New Zealand, 
and (22) H 


ing of the Panama Canal from 1911 to 1914, was 
part of the mainland. Croat’s (1979) calculation 
is that there are 9% of dioecious species in the 
Barro Colorado flora. Other calculations have 
been made for forest floras (in most cases just 
the trees) in mainland areas and they are sum- 
marized in Bawa (1980). Sobrevila and Arroyo 
(1982) have recently contributed a Venezuelan 
example. Percentages vary from 20 to 37%. This 
suggests that the tropical island forest floras have 
been derived from mainland sources that show 
a high percentage of dioecious species as Bawa 
(1982) and Givnish (1982) have already pointed 
out. 


CORRELATIONS WITH ISLAND HEIGHT 
AND LATITUDE 


The relationship between maximum island 
height and distance from the equator with the 
proportion of dioecious species can be seen in 
Figure 1. Through the use of multiple linear 
regression, we find that 82% of the variation in 
levels of dioecism between islands can be ex- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


plained solely on the basis of maximum height 
of the island and its distance from the equator 
(as expressed in degrees of latitude) (Table 2). 
For the regression, percentage data were first 
transformed with an angular transformation (Û = 
1 р, where р is the percentage expressed 
in decimal form). An analysis of variance of the 
regression indicates the regression to be very 
highly significant (P is very much less than 0.001), 
and F statistics computed for both partial coef- 
ficients of the regression show them to differ sig- 
nificantly from 0 (Table 2 
It is our belief that part of the remaining vari- 
ation (18%) can be explained by the differing 
amounts of precipitation in the islands, but since 
this variable is not clearly independent of island 
height or latitude, nor is it uniform from year to 
year, we have not used it in our multiple regres- 
sion. 


DISCUSSION 


In the 22 island floras we have studied, two 
important features are apparent: (1) the per- 
centages of dioecious species in these islands do 
not generally differ from those in latitudinally 
comparable mainland floras, and (2) there isa 
very strong correlation between the level of dioe- 
cism and both the maximum island height and 
proximity to the equator. 

Thus the contrast in the tropics between the 
low islands (and the dry islands), on the one hand, 
and the high forested islands, on the other, 1$ 
clearly shown in statistics in Table 1 and in 
graphical form in Figure 1. This is very likely 
related to differences in the derivation of their 
floras from tropical mainland sources; that is, 
forests for high islands versus littoral vegetation 
for low islands. Island height may be thought t of 
as a simple index of the potential habitat diver 
sity of islands, particularly in the tropics. 

erefore, it is worth examining possible re" 
sons why dioecism appears not to be such an 
impediment to the colonization of islands 35 
might have been thought. mu 

First, there may be the evolution of dioecis™ 
іп a taxon that arrived at the island in the form 
of a self-compatible hermaphrodite. 

(1974) listed 14 genera of flowering plants that 


(1982) has pointed out that subsequent a 
has demonstrated эм ten of these 14 узев 
actually dioecious in certain non-Hawaiian 10" 


w | 
cations as well. Tho in itself, does not Pre ) 


1984] 


BAKER & COX—DIOECISM AND ISLANDS 


249 


TaBLE2. Analysis of Variance of Multiple Regression. Regression equation is: 0 = 12.6 + 0.0036(height) — 
0.123(latitude) (0 = arcsin Ур where р = 96 dioecism in decimal form). Percentage of variation in transformed 
data explained by multiple regression = 1 — (50.3/274.8) = 82%. Both partial regression coefficients are signif- 


icant at the 0.01 level. 


Degrees of 
Source of Variation Freedom Sum of Squares Mean Square F 
Regression 2 Ez = 4,815.5 2,407.5 47.8% 
Deviations 19 d= 956.27 50.3 
Total 21 5,771.8 274.8 


that they have not evolved dioecism autochtho- 
nously in Hawaii, for they have demonstrated 
the genetic capability of becoming dioecious and 
could do so more than once. And there are still 
four genera (Hedyotis and Canthium in the Ru- 
biaceae, Santalum in the Santalaceae, and Wik- 
stroemia in the Thymelaeaceae) that may have 
developed dioecism only in the Hawaiian is- 
lands. There are also five endemic genera that 
are dioecious (Carlquist, 1974) and these could 
have developed dioecism in Hawaii (Bobea and 
Straussia in the Rubiaceae, Broussaisia in the 

fragaceae, Labordia in the Loganiaceae, and 
Touchardia in the Urticaceae). So autochtho- 
nous evolution of dioecism cannot be ruled out 
entirely yet. 

But it does seem that we should also be willing 
to allow that dioecious species can colonize is- 
lands in something like the same proportion that 
they show in mainland situations. And we need 
to explain why this is possible if they seem to 
need to be cross-pollinated to start the devel- 
opment of a seed-reproducing population. One 
possibility is that dioecism is not perfect in these 
species, Clearly, gynodioecious taxa should not 
be с as dioecious, but it is also true that 
many taxa considered to be truly dioecious have 
Occasional flowers of the opposite sex or of a 
te structure. Thus, there is the pos- 

ty of occasional seed setting, probably by 
self-pollination, in these taxa—especially as we 
know that in those cases that have been exam- 
pes experimentally, hermaphroditic flowers in 
lOenWioni:c . 1c АТУ с 
р are se patible ( , UN- 
oum data). This phenomenon, which we term 
саку dioecism," 15 the condition that prevails 
loi hermaphroditism or bisexuality occurs at 
'*vels in populations of otherwise dioecious 
Species, 


An “ample of leaky dioecism is found in Sa- 
heo populations of Freycinetia reineckei, a liana 
Pandanaceae. Traditionally, the Pandana- 


ceae have been believed to be a classic case of a 
dioecious family (Hutchinson, 1973). However, 
a recent examination (Cox, 1981) of populations 
of F. reineckei in Western Samoa has revealed a 
consistent low level of bisexual plants (at levels 
ranging from 4 to 996). The bisexual inflores- 
cences borne by these plants produce viable pol- 
len and also set fruit. 

Working in the Philippines, B. Stone has also 
found a similar condition in Freycinetia negro- 
sensis (see Cox, 1981), and Cammerloher (1923) 
noted it also in F. strobilacea in Indonesia. An 
F. scandens individual grown in the Royal Bo- 
tanical Gardens in Sydney, Australia, from a sin- 
gle seedling from northern Queensland has been 
observed to produce staminate and pistillate 
spikes at the same time (Cox & B. Webster, un- 
publ. data). Although these levels of bisexuality 
may be low enough to be missed in herbarium 
studies, they may have been an important factor 
in the colonization of numerous isolated islands 
by the 190 species of this genus. 

Other striking examples of leaky dioecism oc- 
cur in the rubiaceous genus Coprosma. In the 
Juan F islands, Skott 2 ( ) d 
a number of bisexual flowers on a branch of pis- 
tillate Coprosma triflora. In New Zealand, God- 
ley (1979) reported hermaphrodite flowers on 
staminate plants of C. robusta. Fosberg (1937) 
reported pistillate inflorescences on a staminate 
bush of C. cookei, endemic to Rapa Island. A C. 
pumila bush growing in the University of Cali- 
fornia Botanical Garden in Berkeley produced 
some hermaphrodite flowers (Baker, unpubl. 
data). 

Also in Charpentiera (Amaranthaceae) there 

is leaky dioecism (Sohmer, 1972). Sanctambro- 

sia (Caryophyll )i ded as h y 

dioecism in the Desventuras Islands (Skottsberg, 
p 


r 


al. -—— ste crane. 1 
4 Ld 


the Pacific Coast and the offshore islands of N 


+ 


rth 


250 


and South America. Also, F. chiloensis is a her- 
maphrodite in Hawaii (Staudt, 1962). 

Other examples of leaky dioecism occurring in 
New Zealand that have been noted by Godley 
(1979) include species in the genera Cotula 
(Compositae), Clematis (Ranunculaceae), Pit- 
tosporum (Pittosporaceae), Dodonaea (Sapin- 
daceae), Alectryon (Sapindaceae), Anisotome 
(Umbelliferae), and Astelia (Liliaceae). Fuchsia 
procumbens has been made to produce seeds on 
staminate plants by hormonal treatments (God- 
ley, 1979) and drought stress can result in the 
develop tofst inate fl g the pis- 
tillate flowers in monoecious Zea mays (Moss & 
Downey, 1971). This listing could be greatly ex- 
tended. 

The late George Gillett, who knew the Hawai- 
ian flora intimately, once said that he doubted 


Г. +1 Ж | 


whether there were any pCTICCLU Y D 
in Hawaii —that there was always the possibility 
of an occasional seed being set by an abnorma 
flower on a staminate or pistillate plant. 


Although it is not an island species, Carica 
H . РЧ oo 1 г : *4l 


leaky dioecism (H. G. Baker, 1976). Staminate 
trees of this species are heterogametic as far as 
sex-determination is concerned (Storey, 1958, 
1967). Consequently, when a staminate tree forms 
an occasional hermaphroditic flower that can be 
self-pollinated, the seeds produce plants of both 
sexes in the next generation. Thus, by leaky dioe- 
cism the dioecious condition is rederived from 
a single plant. 

Another possible factor in the establishment 
of dioecious taxa after long-range dispersal is en- 
vironmentally induced sex-lability, which has 
been demonstrated in several flowering plant 
genera (Freeman et al., 1976, 1980). It may be 
that on islands as well as mainlands, variations 
in environmental factors may trigger a change in 
sexual expression, resulting in the production of 
both pollen and eggs within an individual or a 
clone. 

Another mechanism that might overcome the 
apparent disadvantage faced by a dioecious tax- 
on upon arriving on an island by a single act of 
dispersal is the dispersal of multi-propagule units 
rather than single seeds (also mentioned by 
Wickens, 1979). Thus, more than one plant can 
be produced from a single immigration event. 
This is particularly likely to be the case with 
endozootic dispersal by birds of the seeds in ber- 
ry fruits (which by definition are many-seeded). 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


It is notable that both Bawa (1980, 1982) and 
Givnish (1982) h d ttention to the prev- 
alence of endozootic dispersal of tropical forest 
tree seeds and have linked endozootic bird-dis- 
persal of seeds with dioecism. They have sug- 
gested that potential dispersers will be more at- 
tracted to the greater fruit display that a pistillate 
tree can provide compared with the more re- 
source-limited display of trees with hermaph- 
rodite flowers and have proposed that the pri- 
mary vectors of tree seed-dispersal to high tropical 
islands are such frugivores. 

We simply bring these ideas together with the 
suggestion that endozootic dispersal, which pro- 
motes the defecation of several seeds as a group, 
could occasionally be effective in bringing sta- 
minate trees and pistillate trees onto islands in 
close proximity both in time and space. Thus, à 
seed-reproductive colony could develop. Al- 
though we believe that there is an abundance 0 
multi-seed fruits in the tropics, it is notable that 
Flores and Schemske (1983) have shown an ех- 
ceptional abundance of drupes in Puerto Rico. 
However, although drupes by definition are de- 
rived from a single, simple or compound pistil, 
they are not always one-seeded. A good example 
of a multi-seeded drupe is provided by the fruits 
of species of Spondias (Anacardiaceae). 


Incidentally, endozootic dispersal is not the | 


only mechanism by which multi-propagule units 
of dioecious taxa can be dispersed. For example, 
Lloyd (1972) has found in the genus Cotula in 
New Zealand that the achenes of these compos 
ites are dispersed individually in the monecious 
species, but in the dioecious species the entire 
head may be dispersed as a unit. ; 

In this regard, evolution may have gone either 
way in any particular taxon. Thus, either oe- 
cious species may have been selected for fleshy 
fruitedness or fleshy-fruited taxa may have беса 
selected for dioecism. In any event, the corre 
lation is the same. HR 

As a side-light, it may be noted that dioecis™ 
has been linked with multi-propagule units ® 
plants other than angiosperms. Thus, Schuste? 
(1966) noted that the four spores resulting ай 
meiosis remain united as a tetrad in almost 
of the dioeci bryophy . and this tetrad, rath- 
er than the individual spore, becomes the ! 
of dispersal. B each tetrad in the dioecious 
taxa contains two “male” and two pe 
spores, male and female gametophytes Сап 
velop in proximity to each other. 


——P ra — eee * tu ——. 


1984] 


Another factor that mitigates the potentially 
deleterious effects of dioecism is a woody, pe- 
rennial, iteroparous habit, often associated with 
strong powers of vegetative propagation (Bawa, 
1980). Thus, a single plant of a dioecious species 
on an island may simply *^wait" for the advent 
of a propagule of the opposite sex to grow to 
maturity nearby. 

One has only to think of the Canadian pond- 
weed, Elodea canadensis, which invaded Europe 
during the nineteenth century and succeeded in 
blocking waterways by purely vegetative pro- 
duction of ramets even though probably only a 
female plant was introduced (Clapham et al., 
1962). An island example of this phenomenon 
can be seen on San Clemente Island, in the Pacific 
Ocean off the California coast. A single pistillate 
bush of Baccharis viminea was noted in 1900 by 
Trask (1904) and was still there when Raven 
(1963) saw it, although it had grown considerably 
during the interval. To the best of our knowledge 
it still remains there, although we hope that its 
lonely vigil has since been rewarded by the ar- 
rival of a staminate plant. Certainly it can con- 
tinue to wait for a long time, in our human scale, 
but such a delay in the advent of a reproductive 
s ag may not be long on the evolutionary time 

е. 


The picture of pollination biology on moist, 
high tropical islands appears to be in accord with 
another idea proposed by Bawa, who suggested 
(Bawa, 1980, 1982; Bawa & Opler, 1975) that 
Many dioecious species in the tropics have flow- 
ers that are adapted to visitation by small gen- 
eralist insects, particularly small bees and flies. 

ause potential insect pollinator faunas on 
Oceanic islands are frequently depauperate in 
number of species (Carlquist, 1974), and the in- 
«си are believed to be unspecialized in their 
choice of flowers to visit, dioecious plant species 
that do not require specialized pollinators may 
havea greater ct festablishment than those 
Plants that require a specialized kind of visitor. 
Linsley et al. (1966) have shown that a high pro- 
Portion of Galapagos plants are pollinated by a 
um carpenter bee (Xylocopa darwinii). Simi- 
Y, Woodell (1979) has demonstrated that a 
corresponding role is played on Aldabra by a 

beetle (Maucoleopsis aldabrensis). 
advantage of unspecialized pollination 
Systems is not limited to entomophilous taxa, 
“a also in dioecious taxa with vertebrate 
Поп. Thus, the genus Freycinetia, which 


BAKER & COX—DIOECISM AND ISLANDS 


251 


is widespread throughout the islands of the Pa- 
cific, is pollinated by a variety of opportunistic, 
non-coevolved vertebrates that range from large 
flying foxes and starlings to small white-eyes and 
endemic honeycreepers in Hawaii (Cox, 1982, 
1983). A variety of bats, birds, and rodents has 
been recorded as visitors to the genus Freycinetia 
in various other places in the South Pacific (Cox, 
982) 


— 


Another case of unspecialized vertebrate pol- 
lination in dioecious taxa might be seen in the 
epiphyte genus Collospermum (Liliaceae), which 
may be pollinated by the endemic sheath-tailed 
bat in New Zealand (Daniel, 1976), but which is 
probably pollinated by a variety of other bats, 
birds, and possibly insects in other islands in the 
South Pacific. 

All of these considerations that we have made 
have been directed to the demonstration that 
island floras usually bear a close resernblance in 
the percentage of dioecism to the mainland flo- 
ras, from which they have been derived more or 
less by long-distance dispersal. And, if the main- 
land flora is a forest flora with a high proportion 
of dioecious taxa, it can be reproduced on the 
island without serious violation of Baker’s Law. 
But we should be less than circumspect if we did 
not draw attention to another area in which in- 
vestigation is needed. This is related to studies 
of the breeding systems of trees in dry and wet 
forests in Costa Rica (Bawa, 1974; Bawa & Opler, 
1975) that have shown that a high proportion of 
the hermaphrodite-flowered tree species are self- 
incompatible. A similar result is reported from 
Venezuela (Sobrevila & Arroyo, 1982). 

Is this picture of high levels of self-incompat- 
ibility also reproduced in the forests of large, 
high, moist tropical islands? Until the necessary 
experimental work is done, we cannot know. But, 
Godley (1979) and Pandey (1979a, 1979b) agree 
that while dioecism is strongly represented in the 
New Zealand flora, self-incompatibility appears 
to be rather rare, and we note the negative results 
of tests for self-incompatibility in the drier Ga- 
lápagos flora conducted by Rick (1966). 

However, there have been a few indications of 
self-incompatibility in the Hawaiian flora, e.g., 
Plantago grayana (Tessene as quoted in Carl- 
quist, 1970), and we must wait for further ex- 
periments to show if we need to invoke “leaky 
self-incompatibility" as well as “leaky dioecism" 
to account for plant breeding systems in the is- 
lands! 


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ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


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————— 


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SEXUAL DIMORPHISM AND ECOLOGICAL DIFFERENTIATION 
OF MALE AND FEMALE PLANTS! 


THOMAS R. MEAGHER? 


ABSTRACT 


vine evolution of dioecy within a plant population e pei a situation in which there is divergent 
selection for Male and female individuals play different roles 
in the reproductive biology of a dioecious species and тайгу have very different ге 

imposed upo m. The selection pressures presented by these different resource deman 
turn lead to ње oma of sexual dimorphism. Empirical studies of several dioecious plant species 
have shown that male and female plants differ in their resource allocation patterns. These differences 
between the sexes have also been shown to lead to sexual dimorphism in a wide range of life history 
characteristics i in the dioecious perennial Chamaelirium luteum, including age at first reproduction, 


resource demands 
ds could in 


allocation patterns for C. luteum suggest that the observed se 
den о sexes separately rather tibi itis result of selection specifically 


of independent selection on the two 
favoring vane dimorphism. 


The establishment of a stable genetic poly- 
morphism that results in separate male and fe- 
male individuals is just the first step in the evo- 
lution of sexual dimorphism. The two sexes, by 
virtue of attaining reproductive success in dif- 
ferent ways, play distinct roles in the biology of 
a species. Thus, a genetic polymorphism for sex 
expression is likely to have a wide range of eco- 
logical consequences, which in turn could result 
in selection pressures that may eventually lead 


Sa 


the sexes. Secondary differences that have been 
observed between male and female individuals 
within dioecious species have included morpho- 
logical, ecological, and behavioral attributes and 
are often referred to collectively by the phrase 
e сори 


that SCX- 
ual dimorphism is evident i in almost every aspect 
of their ecology and evolution (for reviews, see 
Selander, 1972; Maynard Smith, 1978; O'Don- 
ald, 1980). Traditional studies on sexual dimor- 
phism in plants have been limited largely to floral 
characteristics (for review, see Lloyd & Webb, 
1977); but, over the past few years, there has 


"pues e genetic studies of reso 
morphism is probably the result 


been a growing interest in broader manifestations 
of sexual dimorphism in plants (e.g.. Lloyd 

Webb, 1977; Grant & Mitton, 1979; Onyekwelu 
& Harper, 1979; Wallace & Rundel, 1979; Han- 
cock & Bringhurst, 1980; Bullock & Bawa, 1981; 
Bullock et al., 1982; Meagher & Antonovics, 
1982a, 1982b). This has included extensive dis- 
cussion of various factors involved in the evo- 
lution of dioecy (e.g., Bawa & Opler, 1975; Lloyd, 
1976, 1979; Charlesworth & Charlesworth, 1979), 
but there i is still relatively little koh about the 
plants beyond 


differentiation of sex function. 


Charlesworth & Charlesworth, 


1981; 
1982: Meagher & Antonovics, 1982a, 19826) 208 | 


in turn, to divergent selection pressures, 
will act to enhance the evolution of sex 
morphism. In fact, observed cases of sex 
morphism in traits related to life history 
resource allocation (Lawrence, 1963, ! 


which 
ual di- 


and 
964; 


1 The author was supported during this research by a National Institute of Health. Graduate Trainees ip 


through NIH grant No. GM02007-08 rores by the University Program 


versity Phytotron, and DEB-7904737 to T. Meagher. Travel to field sites was supported by the 
Department of Duke University. I thank the following people for helpful commen 


and the Botan 


an е draft of this paper: С. J. Anderson, L. К. Meagher, М. В. Ме eagher, M. D. Rausher, and an an 


review 


= Deve; iit of Botany, Duke University, Durham, North Carolina 27706. 


ANN. MissouRi Bor. GARD. 71: 254—264. 1984. 


ual di- | 


uke Univa | 


ee ИИИ a 


1984] 


Bouwkamp & McCully, 1972; Putwain & Harp- 
er, 1972; Brockman & Bocquet, 1978; Lovett 
Doust & Harper, 1980; Gross & Soule, 1981; 
Meagher & Antonovics, 1982b) are presumably 
related to differential selection pressures that are 
imposed on male and female plants. 

However, th tent of 1 di phi 
the rate at which it is likely to evolve are subject 
to a variety of ecological and genetical con- 
straints. For example, in order to remain a sex- 
ually reproducing species, male and female plants 
must maintain sufficient overlap in their ecolog- 
ical tolerances and life history characteristics to 
be able to interbreed effectively. This ecological 
limitation may be overcome by species with apo- 
mictic female plants (cf. Gustafsson, 1946-1947, 
cited in Grant, 1971). Genetical constraints arise 
because male and female individuals are mem- 
bers of the same species, and hence are limited 
in the extent that they can undergo genetically 
based divergence due to the overlap in genes in 
their respective genomes and the resultant ge- 
netic correlations (Lande, 1980). Thus the evo- 
ution of sexual dimorphism embodies the bal- 
ance between factors acting to promote change 
and constraints tending to restrict change within 
populations. 

The present paper addresses the processes and 
constraints involved in the evolution of sexual 
dimorphism in plants through an analysis of the 
“loeclous perennial Chamaelirium luteum (Lil- 
laceae). The population biology of this species 
has been well studied (Meagher, 1980, 1981, 
1982; Meagher & Antonovics, 1982a, 1982b) and 
C. luteum has been shown to have extensive sex- 
ual dimorphism both in its overall morphology 
Ee in Various life history characteristics. The 
F ussion below will draw on investigations of 

ur naturally occurring populations in the pied- 
mont of North Carolina designated as Natural 
Area, Seawell, Silver Hill, and Botanical Garden; 
нр locations and site descriptions аге given 
EM. (1980). Experimental analyses dis- 
fron ae Ow are based upon use of seed collected 
E. oe these sites. Seed collected by com- 
oma! sate parent (halfsibship) were planted 
A raised in the Duke University Phytotron. 
A » 30 seedlings representing 30 halfsib- 
Mtas total individuals) were planted. These 
oni ere taken through a series of induction 
Bis (low temperature, short photoperiod) to 

Mote flowering. The specific growth condi- 


Hh anda 


MEAGHER— MALE AND FEMALE PLANTS 


255 


tions and results of studies on the sex ratio are 
described in Meagher (1981). 

The discussion that follows will focus on the 
following questions. How does sexual dimor- 
phism influence the breeding structure of a pop- 
ulation? What are the ecological consequences of 
sex differentiation? What are the genetic bases of 
sexual dimorphism and the probable selective 
forces that lead to the evolution of sexual di- 
morphism? Finally, what is the nature of eco- 
logical and genetic constraints imposed on the 
evolution of sexual dimorphism? 


SEx RATIO AND SPATIAL DISTRIBUTION OF 
MALE AND FEMALE S 


Aside from separation ofthe sexes into distinct 
individuals, there are other ways in which sex 
differentiation affects breeding relationships and 
the reproductive behavior of male and female 
plants. For example, the relative numbers of male 
and female plants, the sex ratio, has an influence 
on the effective population size (e.g., Ewens, 1969: 
32-36). Also, if there is a strong numerical excess 
of one sex, the genetic contribution per individ- 
ual of that sex will be correspondingly lower than 
that for individuals of the other sex. Finally, if 
differences between the sexes are sufficient to lead 
to noticeable differences in ecological tolerances, 
there may result a tendency for male and female 
plants to occur in different microhabitats, leading 
to increased spatial separation of the sexes. 

A particularly striking feature of populations 
of Ci ul iiber ihe ewerina 
ratios are extremely male biased (Meagher, 1981). 
If one observes the sex ratio among flowering 
plants during the breeding season in any given 
year, there is a large excess of male plants (Table 
1). However, because only a relatively small per- 
centage of the plants in a population flower in a 
given year, estimates of sex ratios based on a 
single flowering season could be biased by dif- 
ferences between male and female plants in their 
flowering schedules. There is a great deal of year 
to year variation in flowering sex ratios within 
any one site, showing that differential flowering 
behavior between male and female plants can 
have a dramatic effect on sex ratio estimates for 
any one season. In the present study, individual 
plants were monitored over a series of flowering 
seasons, so that for each successive year it was 
possible to obtain a cumulative estimate of the 
population sex ratio based not only on the plants 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


TABLE 1. Sex ratios in four populations of Chamaelirium luteum (from Meagher, 1981). Flowering sex ratios 
(male/female) are given for 1974—1979; С? (1 degree of ps test results for departure from a one to one 
sex ratio were statistically significant for all flowering sex ratio 


Percent of Cumulative 
Population Flowering Sex Ratio 
Site Year in Flower Sex Ratio Estimate 
Natural Area 1974 9.7 4.51 
(N = 2,200) 1975 10.6 3.07 
1976 1353 3.30 
1977 19.9 3.41 2.47 
1978 6.7 4.52 
1979 3.6 10.57 
1980 11.0 3.90 
Seawell 1975 16.2 7.11 
(N = 949) 1976 14.0 6.00 
1977 14.6 4.79 3.37 
1978 9.5 6.50 
1979 1.6 14.00 
1980 25.0 4.39 
Botanical Garden 1975 25.1 2.80 
(N 50) 1976 19.1 3.47 
1977 27.8 3.47 1.76 
1978 15.8 2.89 
1979 15.6 3.38 
1980 38.9 2:37 
Silver Hill 1975 125 3.18 
(N = 1,103) 1976 9.0 3.71 1.74 
1977 19.1 252 
1978 5.9 2.82 NES S | 


in flower in a given year, but also on plants that 
had flowered previously. Inspection of such cu- 
mulative estimates showed a monotonic decline 
as the number of successive flowering seasons 
considered increased (Meagher, 1981). These cu- 
mulative estimates leveled off after the first sev- 
eral years and showed that the sex ratios for these 
four populations do show an overall excess of 
male plants (Table 1), even though this excess is 
generally not as dramatic as that observed within 
a single flowering season. 

One can also look at the Ситон of sex 
ratios over different nits o 
a population as a means of враня the relative 
spatial distributions of male and female plants 
within a population. Tests of within population 
heterogeneity in sex ratio (Fig. 1) indicate that 
the sex ratio is not uniform within natural pop- 
ulations but rather varies from subunit to sub- 
unit, reflecting an underlying differential spatial 
distribution of male and female plants. Differ- 
ences between male and female individuals of C. 


~ 


within a population have been confirmed in 
number of statistical analyses (Meagher, 1980; | 
Meagher & Burdick, 1981). | 
The above discussion outlines a range of eco 
logical consequences of dioecy. The dieen | 
between flowering sex ratios and cumulative #5 6 
timates of the overall population sex ratios P 
Chamaelirium luteum suggest that male and | 
male plants show different types of flowering 
havior. The tendency toward differential disti. 
bution of male and female plants over er | 
microsites, presumably the consequence of 
ferential survivorship of the two sexes Over these 
different microsites, provides evidence of we 
logical differentiation between the sexes. 
phenomena are both related to the life history | 
characteristics of the two sexes in terms offe , 
productive activity and survivorship. The 
a comparative examination of the na 
of male and f 
for obtaining insight into such ecological 
effects of sex differentiation. 


| 
luteum in their relative spatial distributions | 
! 
| 


= 


sam 


= 


| 


| 


1984] 


NATURAL AREA 


MEAGHER— MALE AND FEMALE PLANTS 


BOTANICAL GARDEN 


$£ {3 1 16 5 1 о 
АА hA ET | | л 
1, |28, [18, [19 в, |53, loo, [14 2 + "Ра 
“i нај 31. 712] 72 | Геј ^il ^ | р| Лл| 7 
з, les, |20, [22, |16, isz. |28 6 E |1 
^ | al 714|- "s | ml ^s] ^n | | 1 @ 
з, [21 3 o, |28, |28 9 6 13 
ПК | У |. | У] % r^ LIAT 
1 0 Та 4 о 
© отат ^41 ^4 
о з, |17 
yy | 17, 
SILVER HILL SEAWELL 2 : Ё 
2 6 1 2 
пи == —— ^ 2 ^9 ^ 
а, |21, |n о зв, |36, Fi 
Ep Á / ! 6, 
2 21 ^ 1 | + | в | 6-1 ^ 1 & [2 3 1 1 
4, 121, |зв 
у, |21, |38, 45, 167, | 
2 5| 717 | | ^o | ^| ^o ох Бяз 8 0 
т ye б; ЈА А 
27 27 1 
х ^o | ^o о | 7 
38 5 | 
7 | ^u| 4 20 | % 4 1 


FIGURE 1. Within site heterogeneity in sex ratio (male/female) in C. /uteum (from Meagher, 1980). G? test 


results indicated 
Garden (P < 0.005) sites (Meagher, 1980) 


LIFE History DIFFERENCES BETWEEN 
MALE AND FEMALE PLANTS 


a effect of sexuality on life history charac- 
ing аи can be conveniently illustrated by mov- 
== зу through the lifespans of the two 
ы he first aspect of life history considered 
сте 15 the age at first reproduction (Fig. 2). These 
= at first reproduction are based on the num- 
a ve induction cycles to which a plant 
Ба нерн before it flowered for the first time 
“чам Ч е cohorts of plants raised in the Duke 
ini Tsity Phytotron. Clearly, male plants were 
Ded to begin flowering at an earlier age than 
male plants, 
Роне features of the sex ratio of C. luteum 
Mitre! above suggest that, among sexually 
че ED. ue male and female plants differ 
ама Owering schedules. The flowering 
ules of male and female plants are com- 
ted here by considering the number of times 


Pla ; 
nts of a given sex flowered over a span of years 


significant heterogeneity for the Natural Area (P < 0.05), Seawell (P < 0.005), and Botanical 


(Table 2). Male plants flowered more frequently 
than did female plants. An alternative way of 
stating these results is that female plants tend to 
have longer inter ring episod 
than do male plants. 

Once an individual of C. /uteum becomes es- 
tablished, its size, measured as the number of 
rosette leaves, plays an important role in deter- 
mining its subsequent life history behavior 
(Meagher, 1982). The number of rosette leaves 
on female plants tends to be greater than the 
number of rosette leaves on male plants (Table 
3), indicating that female plants are, on average, 
larger than male plants. Furthermore, the impact 
of flowering on the resource status of an indi- 
vidual is reflected in the year to year change in 
rosette leaf number. Percentage changes in the 
number of rosette leaves from the year before to 
the year after flowering were estimated for male 
and female plants (Table 4), and there was a 
significant reduction in size among plants that 
had flowered, suggesting that flowering imposed 


DO Yr 


258 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Уол 71 


70g- d А Pg с 
oof ћ - 
$ B à 
5 p In | Pi { { 
= fai іх А А 
Е fiu Ha 
zt «| А] | РА are ЧИШ 
2t Mi | j 
Е ` : t 
Е ра 4 i | у PX РАНИ 
ег = PX A Ё [ у Ӯ 4 i X 
| a : H Y Н LE 4 јр. Ре. У A 
Жш о T] fries MERC 
Р 5 | / ү ii rj МА 
E E. Ls -i i МАЗ 
3 10 ПР а 1,“ E ^T 3 E: E ~ 
EX. / j 
р 1 H H 
Га еа i EEE tea ae 
1 2 а 4 5 6 1 2 3 4 БИ 


їс Uy ee eee ae ра 
number of consecutive induction cycles 


FiGURE 2. Age at first reproduction for male (dashed line) and female (dotted line) seedlings in the Duke 
божай Phytotron; sites of origin for the seed are Natural Area (a), Silver Hill (b), and Botanical Garden (c). 


a substantial drain on the resources of an indi- 
vidual. This effect was much more pronounced 
for female than it was for male plants. 

The final stage in the life history to consider 
is death. Cumulative estimates of annual mor- 
tality rates for the two sexes (Table 5) show that 
female plants had a higher mortality rate than 
did male plants in two of three sites. For one of 
these two sites, the female mortality rate was 
significantly higher than the male mortality rate. 

When these various life history characteristics 
of male and female plants are considered collec- 
tively, an overall pattern emerges that indicates 
a higher resource cost of flowering for female 
plants. With a later age at first reproduction and 
longer intervals between flowering episodes, fe- 

1 il they 


flower successfully. The tendency of female plants 
to be larger than male plants is also suggestive 
of a higher resource "threshold" that may be 
necessary for flowering to occur. In other words, 
female plants may delay flowering until they have 
achieved a greater size and are hence better buff- 
ered against the proportionately greater resource 
depletion that flowering represents for them. Fi- 
nally, the extra costs and consequent resource 
depletion brought on by flowering for female 
plants could expose them periodically to a higher 
risk of mortality, resulting in a relatively higher 
mortality rate for female plants 

It seems quite reasonable that many of the 
observed life history differences between the sexes 
are causally related to the specific male and fe- 


male resource demands and resource allocation 
patterns. From an evolutionary standpoint, 
therefore, one would expect that male and female 
plants would have very different types of selec- 
tion pressures imposed on their resource allo- 
cation patterns. There may be divergent selection 
that favors male plants that put a relatively low 
proportion of their resources into flowering an 
that flower more frequently and that favors Ё- 
male plants that put a relatively high proportion 
of their resources per flowering episode into less 
frequent flowering. 


RESOURCE ALLOCATION AND THE EVOLUTION 
OF SEXUAL DIMORPHISM 


di- 
Traits or characters associated with en 
morphism, such as differences in resource 


инини н‏ س 


ме | 
cation, are quantitative rather than qualitativ 


aracters is 
odels in 
ult from 
allelic picti pe en a lenit number yere н: - 
of which makes a small additive contribution 
the overall expression of the trait under $ 


in nature. The genetic basis of such ch 
ben defined - — seo m 


(Falconer, 1981; Mather & Jinks, 1982). The © | 


netic and evolutionary behavior of such quan 


titative variation can thus be studied by 


the ар“ | 
| 


plication of appropriate statistical methods. i | 


е phytotron studies described above 


tion 
еде оп halfsibships of seedlings; from se d 


| 
unir | 
3 


| 


= 


| 


1984] 


TABLE 2. The percentage of plants in flower in a 
given season that last flowered X years ago. These per- 
centages represent averages over all consecutive years 
for which flowering data had been obtained through 
1980 (see Meagher, 1981). 


MEAGHER—MALE AND FEMALE PLANTS 


259 


TABLE 4. Percentage in rosette leaf number from 
the year before to the year after flowering (year 3-year 
1); sample sizes are given in parentheses. Significance 
tests of departures from 0 were made using a / test 
(Sokal & Rohlf, 1969). Results from / tests comparing 
male transitions and female transitions were all statis- 


Male Female tically significant (P « 0.001). 
Site X Plants Plants 

Natural Area 1 37.4 1.6 , Male Female 
2 22.9 17.8 Site Plants Plants 
3 12.0 19.0 Natural Area ~17 (247) —39 (133) 
4 2.1 14.2 Seawell —16 (118) —29 (34) 
5 2-2 6.0 Silver Hill +2 (28) 234 (12) 
6 L5 0.0 * Not significant. 

Seawell 1 30.1 0.0 ùb P < 0.05. 
2 33.0 7.8 e P < 0.001 
3 18.3 8.3 
4 au 8.0 
5 7.3 11.4 

Silver Hill 1 344 7.7 tical analysis because in both cases transformed 
2 34.1 17.2 values showed a better fit to a normal distribu- 
3 4.2 17.7 ur 


duction cycle in the phytotron, male and female 
plants within 22 of the 30 halfsibships were in 
flower for the first time and plants were harvested 
for dry weight measurements of three vegetative 
and three reproductive structures (Table 6). It is 
interesting to note that although male plants had 
a Proportionately greater dry weight in their veg- 
@айуе parts than did female plants, all of the 
Structures on female plants had a higher absolute 
weight. Even though all plants were the same 
age, the femal pl 1 Шап 
the male plants. 
Dry weight values were log-transformed and 
Percent dry weight values were subjected to arc- 
SiN square root transformations prior to statis- 


ais 


BP Rosette leaf number for male and female 
ra e lames luteum. Values presented are 
nc -1979 pooled; cumulative numbers of ob- 
and Rs for each sex are given in parentheses. Male 
= jm means within each site were compared us- 
pairs of, ОУА (Sokal & Rohlf, 1969), and all three 

means are significantly different (P < 0.0001). 
———... 


In order to evaluate genetic components of 
variation from these data, a partially hierarchical 
analysis of variance involving population of or- 
igin and sex as main effects and halfsibships as 
a nested effect within populations was employe 
(Brownlee, 1960). The interactions of sex by pop- 
ulation and of sex by halfsibship nested within 
population were also analyzed for each mea- 
surement. The effect of population of origin was 
taken into account because the halfsibships used 
were collected from three different populations, 
and differences among the populations made a 
significant contribution to the overall variation 
in eight of the 12 measurements analyzed. 

In this analysis, there are two genetic com- 
ponents of variation that are relevant to the pres- 
ent discussion. The component of variation 
among halfsibships nested within populations is 
equal to one-fourth of the additive genetic vari- 


TABLE 5. Annual mortality rates for male and fe- 
dcc ^ 21 1 £L øC liri. latorria Values pre- 
sented аге from 1975—1979 data pooled. Comparisons 
between male and female mortality rates are based on 
the log-likelihood ratio (Bishop et al., 1975). n.s. = not 
significant. 


н Male Female Male Female 
Site Plants Plants Site Plants Plants Contrast 
N 
есче Агеа 4.1 (2,492) 4.4 (1,014) Natural Area 3.0 2.6 n.s. 
Silver ~ 4.4 (1,025) 4.9 (260) Seawell 17 4.0 n.s. 
ill 4.9 (628) 5.3 (298) Silver Hill 1.3 5.1 P<0.01 


260 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


TABLE 6. Mean dry weight and percentage of total dry weight for vegetative and reproductive plant parts | 
nt 


for plants harvested in the phytotron experiment. 


Male (N = 57) Female (N = 59) | 
% of % of | 
Character Mean Total Mean Total 
Vegetative 
Rosette Leaves 2.64 46.9 2.98 39.5 
Rhizome 1:53 29.3 1:73 24.4 
Roots 0.72 14.3 0.99 142 
Vegetative Total 4.89 90.5 5.72 78.1 | 
Reproductive | 
Inflorescence Leaves 0.06 1.3 0.30 44 | 
Inflorescence 0.11 24 0.25 3.2 
0.31 6.1 1.01 14.3 
Reproductive Total 0.48 9.5 1.56 21.9 


ance, which is the portion of the overall variation 
that is most directly involved with response to 
selection (Falconer, 1981). In analyses of this 
type based on field collected progenies, one as- 
sumes that maternal effects on the characters 
measured are negligible and that the female plants 
have mated at random with male plants in the 
population. Because the characters assessed in 
the present study were measured on fully grown 
individuals, th pti ing 1 
effects is probably reasonable. Violation of the 
second assumption would confound attempts to 
measure the actual level of additive genetic vari- 
ance; but in the present study we are only con- 
cerned with whether or not such genetic variance 
exists, not with its actual magnitude. 

he component of variation attributable to the 
interaction between sex by halfsibship nested 
within populations provides a means of evalu- 
ating genetic variation in the relative character- 
istics of male and female plants. In essence the 

x by Бапа је на з о: 


genetic variation for sexual dimorphism. 

Analysis of variance (Table 7) showed a strong 
indication of sexual dimorphism in that differ- 
ences between the sexes were significant for four 
of the six dry weight measurements and also for 
four of the six percentage dry weight measure- 
ments. Significant sex by population interactions 
for rhizome weight and for percent dry weight 
Ни Жыр до i 


the extent 


of sexual dimorphism found, at least for vege- 
tative characteristics, is not uniform over the 
different populations. The observed differentia- 


tion among populations suggests further that the 
extent of sexual dimorphism in resource allo- 
cation patterns may be subject to evolutionary 
modification within particular ecological com | 
texts. However, the characters that showed e 
dence of additive genetic variation for sexual di- 
morphism, inflorescence weight, and percenta | 
dry weight of rhizome and inflorescence, are not ) 
the same characters that showed a significant P 
by population interaction. There were, however 
significant levels of additive genetic variation 
found for rhizome weight, and percentage o 
weight of rosette leaves, roots, and {йог 
stalk. The first three of these characters were 
characters that did show a significant sex by pe 
ulation interaction. It therefore is reasonable | 
conclude that the among-population difera 
tion in the extent of sexual dimorphism 15 
outcome of the independent responses of 

and female plants to site-specific selection pe 
sures - 

The manner in which response to selection € 
a trait in one sex will influence the express! ai 
that trait, and hence the fitness, in the other "m | 
depends on the nature of the genetic correla н | 
that exists between the sexes for that trait. heil | 
that show a strong genetic correlation, ы nol 
positive or negative, between the sexes se | 
likely to show an independent response e genet | 
tion on male and female plants because а ‚эй 
change that influences the fitness in one € обе 
also have an influence on the fitness of the 
sex. Such genetic correlations have e d 
posed as a major factor limiting the evol 


| 


w 


ee * 


1984] 


MEAGHER— MALE AND FEMALE PLANTS 


261 


TABLE 7. F-ratio test results* from the partial hierarchical analyses of variance for plants harvested in the 


phytotron study. 
Reproductive 
A. Log Dry Weight Vegetative 
Inflores- 
Rosette cence  Inflores- 
Effect df Leaves‘ Rhizome? Roots a cence’ Stalk 
Population I ipe 3.14 5.18 3.38 2.54 9.1 
Sex 1 27 3.99 17.5 PTM 122 146.3 
Sex * Population 2 2.78 4.9» 0.1 0.2 1.4 2.54 
Halfsibs within Populations 19 1.2 1.8* 1.64 0.9 0.4 1.5 
Sex * Halfsibs within Populations 19 1.6% 7 КД 1.0 1.8 1:2 
Error 72 
AN o C НИ 
Reproductive 
B. Arcsin % Dry Wei : 
ry Weight Vegetative йг 
Rosette cence  Inflores- 
Effect df Leaves Rhizome’ Roots Leaves!  cencef Stalks 
Population а 3 7.2% 3,08 2.0 1.0 0.4 
e [© адво — ОБН а 736 9.9 122 
Sex * Population 2 3.3 1.5 6.6: 0.3 0.0 0.6 
ANM within Populations 19 2.5b 12 2.18 1.1 0.3 1.84 
Sex * Halfsibs within Populations 19 1.5 1.8 0.9 1.8 1.7% 1.0 
Error 72 
*P<0.05 
* P < 0.005 
*P < 0.001 
"eni 


* Previously published F-ratios on these data (Meagher & Antonovics, 1982a) were based on non-transformed 
al 


values of a subset of the data included 


se : А 
р dimorphism (Lande, 1980). A small ge- 
Correlation between the sexes for a given 


Bicis however, would allow independent re- 
== to selection in males and females. 
МА cg Correlations between the sexes (?,) can 
A from the analysis of variance dis- 
For th above using the method of Yamada (1962). 
€ present analysis, 
У A-B 
Ns RR 
"АВЕС (1) 
ге A, B, and C are the mean squares for half- 


m Within populations, sex by halfsibships 
~ tions, and error, respectively. Be- 
anced E data set being analyzed was unbal- 
be Mr Эйр, f, for the total data set will 
чы Козер П order to reduce this bias and also 

à standard error of f, for significance 


tests, the genetic correlations presented below 
actimat 1 1 LL st; 4. 2 3 fF 


TAV 


& Schucany, 1972; see also Rausher, 1984). For 
this method, estimates of fj, i = 1,..., 22, were 
obtained by omitting the і" halfsibship and es- 
timating f, from analysis of the resultant subset 
of the overall dataset. The reduced bias estimate 
of f, is then given by 


r = N.f- N- 1).2,, (2) 
with a standard error of 
s.e. = [2,(f, — £)"/N(N — 1)]” (3) 


where N is the number of halfsibships. 

Genetic correlations between the sexes were 
estimated for all of the measured traits that had 
significant levels of additive genetic variance 
(Table 8). Significance tests for rosette leaf and 


262 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(VoL. 71 


ABLE 8. Genetic correlations (r,) between the sexes for log dry weight and arcsin % dry weight in vegetative 


and reproductive structure 


s. The estimates of the correlations and their standard errors were obtained using the 


jackknife method (Gray & ө та 1972); t test results for differences between the estimates and +1, 0, ne 


— ] are also shown. 


Reproductive 


Vegetative 
Rosette Inflores- 
Leaves Rhizome Roots cence 
k 0.16 + 0.65 0.57 + 0.68 >0.32 + 1.18 —4.19 + 5.25 
to (r, = +1) 13 0.6 1.1 1.0 
too (T, = 0) 0.3 0.8 0.3 0.8 
b t N 1.8* 23 0.6 0.6 
Vegetative Tate 
Rosette cence Inflores- 
Leaves Rhizome Roots Leaves cnc И 
h 0.50 + 0.40 0.12 + 0.33 0.97 + 0.62 0.07 + 0.58 —32.24 + 29.43 0.45 ± 1.05 
оо (t * +1) : 1.6 1.1 1 
tao (t, = 0) 17 1.5 0.1 1.1 e 
too (r, = — 1) 3.79 29 1.9» 1l ^ 7" И 
‘F< 01 
* P < 0.05 
*P«DOI 
rhizome weight and for percent dry weight in form of partial spatial segregation between male 


rosette leaves, roots, and inflorescence leaves, 
indicated positive genetic correlations. The ge- 
netic correlation between the sexes for percent 


dry weight i in rhizomes 


41 


differ ои t 


from both +1 and —1 but not from zero, indi- 
cating a low genetic correlation for this trait. The 
other estimated correlations had such a high 
variance that no conclusions can be made as to 


their magnitude or direction. 


The presence of positive genetic correlation 
between the sexes for some traits is hardly sur- 
prising; such results imply that the same genes 
are influencing these traits in both sexes. How- 
ever, a small genetic correlation, as in the case 


of percent dry weight in rhizomes, indicates that 


there is relatively little overlap in the genes reg- 
ulating that trait in male versus female plants. 
Therefore the two sexes are capable of indepen- 
dent responses to selection on this trait. The level 
of resources contained in the rhizome, which 
probably serves as a storage organ, may well have 
a direct physiological relationship to the life his- 
tory differences observed within natural popu- 


lations, particularly flowering schedules. 


CONCLUSION 


The ecological consequences of sexual dimor- 
phism in plants are sometimes manifested in the 


and female plants along environmenla! ¢ 
man et al., 1976) or altitudinal (Grant & Mitton, 
1979) gradients or over different microhabitats 
(Meagher, 1980). If such spatial зерге ШЕ 
taken to extremes, ultimately male and fe 4 
plants might occur too far apart to effect sex dí 
reproduction. Other ecological cons 
REN dimorphism that have been 0 served 
ome plant species are differences ber 
sexes in life history characteristics an 
allocation patterns as cited above. Indeed spatial 


rential 
the result of diffe 
segregation is most likely Mer" dif 


view). Other life history dimorphism idi 
differences in flowering schedules (Bullock я 
1982; Меарћег, 1981; Уегпеї, 1971; Val e 
& сене 1979) ог more specifically in the ! 
sponse conditions that promot 
(Meagher, 1981, 1984), might үи a mee 


bar 1 iert 


plants. For example, such differencesin flowering | 


might reduce the probability of simul uH 
flowering of male and female plants. с 
result in greater spatial separation of 81 
neously flowering plants of opposite sex. 
order for a species or population to p 
course, male and female plants must display 


yet, i0 
of 


> 
1 


1984] 


че. чишү. 


enatial di 
к 


flowering 
Géhevior to allow reproduction to occur. This is 
particularly true for plants, which are nonmotile 
and incapable of the migration during breeding 
season that occurs in some sexually dimorphic 
animal species (e.g., Bartholomew, 1970). The 
limit to the extent of ecological differentiation a 
species can undergo and still persist thus consti- 
tutes an effective limitation on the evolution of 
sexual dimorphism 
The observed examples of sexual dimorphism 
in Chamaelirium luteum emphasize differences 
ш spatial distribution, life history, and resource 
allocation, and provide a firm empirical basis for 
evaluation of the ecological consequences of sex- 
ual dimorphism. At the same time, these studies 
also represent a good start toward understanding 
ecological constraints on the evolution of sexual 
dimorphism 
Studies on the genetic basis for resource allo- 
cation patterns in the two sexes also provide in- 
sight into the evolution of sexual dimorphism. 
Significant differentiation between the sexes sug- 
gests that there has been in the past strong di- 
Vergent selection on resource allocation patterns 
inthe two sexes. However. male and fi 
in a dioecious population share a common ge- 
his heritage; autosomal genes that are present 
exposed to selection in one sex will ulti- 
Ber occur in progeny of the opposite sex. Be- 
Cause genetic changes, or responses to selection, 
which act to enhance fitness in one sex may con- 
сетуабју prove to be deleterious to the other sex 
(Fisher, 1958: Lande, 1980; Yamada & Schein- 
& ыш) this genetic correlation between male 
€ plants could act to retard divergence 
аена е cue Over evolutionary time, strong 
کا‎ Selectıon on a particular trait could re- 
а ап accumulation of sex-limited gene 
Pression for the genetic loci influencing that 
a tering the constraints imposed on 
dE топ of sexual dimorphism by genetic 
ns between the sexes 
Interpretation of the evolution of a set of char- 
B. "ci an understanding of both the ge- 
Меча or those characters and of the eco- 
к ntext within which those characters are 
ea Sexual dimorphism in dioecious pop- 
wal. st an unusually clearcut situation 
кәнә ich to consider ecological and genetic 
MIS €s of a set of characters simultaneously. 
ine consideration, we obtain an understand- 
d ба only of the type of selective forces acting 
mote change in dioecious populations, but 


MEAGHER— MALE AND FEMALE PLANTS 


263 


also of the nature of ecological and genetic con- 
straints that act to regulate evolutionary change. 


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) 


| 
| 


| 


| 


THE ADAPTIVE SIGNIFICANCE OF SEXUAL LABILITY 
IN PLANTS USING ATRIPLEX CANESCENS 
AS A PRINCIPAL EXAMPLE! 


D. C. FREEMAN E. D. MCARTHUR,? AND К. T. HARPER‘ 


ABSTRACT 


Experimental studies demonstrate that up to 2096 of the individuals of Atriplex canescens and other 
species of the genus can alter their sexual state from one season to the next. Approximately 5% of the 


A. canescens individuals changed from an exclusively pistillate phenotype t to an 
5% w the in ndividuals c hanged their primary sexual emphasis, e.g., 


phenotype or vice versa. Another 


y staminate 


addition, 


ntly stami inate, 


10% of the population changed from a unisexual state to a monoecious state in which siis and 
equal in number (or vice versa). In Atriplex oat pis sex change 


occurred in response to three stresses: an unusually cold winter, drought, and p 
ced under stress, pistillate individuals are significantly more likely to change sex than sta- 
minate individuals. The ability to change sex appears to 


When pla 


or heavy seed set. 


o confer a survival advantage to the individual. 


Plants which change sex also — to begin reproducing earlier than pistillate MEN while producing 


as many seeds as pistillate plants do. T 
advantages in the population studied. 


Recent ecological studies indicate that an- 
droecious (male) and gynoecious (female) indi- 
viduals of several dioecious plant species exhibit 
partial niche separation; J. L. Harper has termed 
this pattern the Jack Sprat effect (Onyekwelu & 

arper, 1979). The most commonly reported 
manifestation of the Jack Sprat effect is the seg- 


iduals along strong environmental 
gradients. For example, Freeman et al. (1976) 
Showed that the sexes of five dioecious plant 
Species of the intermountain region of the west- 
етп United States segregated along gradients of 
Water availability or salinity. Androecious plants 
T ge tony more abundant at the 
ка end of the gradient and gynoecious plants 
on og A more prevalent in favor- 
: vironments. In another study, Fox and 
kia (1981) demonstrated that slope expo- 
z ected the sex ratio of Hesperochloa kingii. 
Y typically found that androecious individ- 

à E the species were more common in areas 
W soil moisture whereas gynoecious in- 


о ке 


dividuals were usually more common in moister 
areas. Similar results have been observed by oth- 
ers (Davey & Gibson, 1917; Richards, 1975; 
Waser, pers. comm.). Cox (1981) showed that 
the sexes of Trophis involucrata and Mercurialis 
perennis segregate along gradients of phosphorus 
availability and pH, respectively, and Onyek- 

welu and Harper (1979) ! found differences i in x 
ratios of spinach in 
ferent intensities of "intraspecific competition. In 
all of these cases, androecious plants were pro- 
portionately more abundant in the most stressful 
environments. Further evidence for partial niche 
separation between the sexes of dioecious ein 
comes from the studies of Putwain and Ha 
(1972), who showed that competition ‘aces 
members of the same sex was considerably more 
intense than competition between androecious 
and gynoecious plants of Rumex acetosa and R. 
acetosella. 

A growing number of researchers have found 
physiological and morphological differences be- 
tween the sexes of dioecious species (Heslop- 
Harrison, 1972; Adams & Powell, 1976; Lloyd 


ure Forest Service, Intermountain 


*deral funds for wildlife restoration were provided through Pittman-Robertson Project W-82R. The Snow 
th 


on is соран уну maintained by the U.S. 
ge Experiment Station, the 


Utah Division of f Wildlife 


ment of Agriculture 


Resources, Utah State University, and 


mrt College Funds were also provided by NSF grant «DEB 81-11010. S. C. Sanderson provided technical 


; Departmen of Biological Sciences, Wayne State University, Detroit, Michigan 48202. 
Scien 


84601 


S. Department of Agriculture Forest Service, Shrub 


nces Laboratory, 735 N. 500 E., Provo, Utah 


* Department of Botany and Range Science, Brigham Young University, Provo, Utah 84602. 


ANN. MISSOURI Bor. GARD. 71: 265-277. 1984. 


266 


& Webb, 1977; Valdeyron & Lloyd, 1979; Han- 
cock & Bringhurst, 1979; Gross & Soule, 1981; 
Meagher & Antonovics, 1982). Such differences 
apparently arise as a result of natural selection 
operating differently on individuals of each sex. 
Selection appears to operate on differences in 
requirements for staminate and pistillate func- 
tions. For example, androecious and gynoecious 
plants growing on common sites experience dif- 
ferent levels of water stress. Gynoecious plants 
of several species [Atriplex hymenelytra (Stark, 
1970), A. canescens, A. confertifolia, A. cuneata, 
n& 


perochloa kingii (Fox & Harrison, 1981), Sim- 
mondsia chinensis (Hikmat et al., 1972), and 
Spinacea oleracea (Freeman, unpubl. data)] tend 
to be under greater water stress than androecious 
plants, particularly during midday in the fruiting 
season (Freeman & McArthur, 1982). Freeman 
and Vitale (unpubl. data) show that under severe 
water stress, the pistillate function in spinach was 
impaired to a greater degree than was the sta- 
minate function. In her studies of tropical or- 
chids, Gregg (1973) has shown that shading more 
adversely influenced the pistillate than the sta- 
minate reproductive potential. 

Whereas numerous studies indicate partial 
niche separation between the sexes of dioecious 
plants, little or no attention has been given to 
the evolutionary consequences of the Jack Sprat 
effect. Furthermore, few studies examine the se- 
lective forces that create staminate biased sex 
ratios in one environment and pistillate biased 
ratios in another. 

If two species in physiological competition 
show partial niche separation, conventional the- 
ory would predict that the reproductive potential 
of those species would be unequal at some sites 
of coexistence, and that the physiological re- 
sponses of the two species would differ signifi- 
cantly for at least some widespread and recurrent 
environmental stresses (Birch, 1953a, 1953b). In 
a similar fashion, if the sexes of dioecious plants 
do indeed display partial niche separation along 
a resource gradient, we would then expect an- 
droecious and gynoecious plants to respond dif- 
ferently to at least some environmental vari- 
ables. In such cases, if patch size is small relative 
to the distance androecious plants can disperse 
pollen, androecious and gynoecious plants may 
not be equally fit in all environments. 

Using sex allocation theory, Charnov and oth- 
ers (Charnov & Bull, 1977; Freeman et al., 1980; 
Charnov, 1982) have shown that if the sexes are 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


not equally fit in all environments and the en- 
i ~ 1:72. 1.3 1 + 3 : e 


time an 

or space, and if an individual has little control 
over which environment it will experience, then 
genes allowing environmental control of sex will 
be favored over genes imparting strict genetic 
control of sexual expression. Given these as- 
sumptions, in some environments or at some 
times individuals of a dioecious plant species 
that can alter sexual expression in response to 
environmental cues can increase their genetic 
contribution to future generations. That over 50 
dioecious plant species are known in which in- 
dividuals have been observed to change sex or 
to produce hermaphrodite or monoecious off- 
spring supports the hypothesis that labile sexual 
expression imparts some selective advantage to 
individuals in at least some situations (Freeman 
et al., 1980). 

Mathematical models developed by Charnov 
and Bull (1977) predict that if monoecious Ш- 

ividuals were placed in a environment 
where staminate and pistillate functions had un- 
equal fitness, floral sex ratios would be locally 
altered to favor the more successful sex. That 
kind of a response appears to have occurred i 
Acer grandidentatum (Barker et al., 1982), Ji- 
niperus osteosperma, Quercus gambelii, and Sar- 
cobatus vermiculatus (Freeman et al., 1981). 


VARIABLE FITNESS OF ANDROECIOUS AND 
GYNOECIOUS INDIVIDUALS IN 
COMMON ENVIRONMENTS 


Sex allocation theory predicts that labile " 
expression may evolve where patch quality E 
ferentially affects staminate and pistillate fitness 


To test that theory, the first question Mer 


uals of dioecious plant species. We are aware 
only four studies that document differences 
the environment and associated fitness of "i 
droecious and gynoecious plants (Gregg. 19724 
Fox & Harrison, 1981; Freeman & Vitale, 02° 
publ. data; Freeman et al., unpubl. data). с 
droecious and gynoecious individuals аге 

equally fit in all environments, a plant may €- 
hance its fitness by changing sex; thus, Sex change 
may be viewed as an adaptation to patchy - 


in 


— a — 


~ 


— 


чш» 


2 


1984] 


+ Ни 


FREEMAN ЕТ AL.—SEXUAL LABILITY IN ATRIPLEX 


d a E ЈЕ | 
f four 


TABLE 1. The effect of environment on 


Plants were grown in 


full or 50% of full Мела The fitness values w were computed by dividing number of 


inflorescences in partial shade by the number produced in full sun (data from Gregg, 1973) 


Relative Fitness 


Species Growing Condition Androecious Gynoecious 
Cycnoches warscewiczii Full su 1.00 1.00 
Bright Pipes 17.50 1.00 
Catasetum expansum Full sun 1.00 1.00 
Bright shade 4.71 0.18 
Cycnoches densiflorum Full sun 1.00 1.00 
Bright shade 0.63 0.11 
Cycnoches stenodactylon Full sun 1.00 1.00 
Bright shade 0.42 0.06 


vironments. If androecious and gynoecious in- 
dividuals have equal fitness in all environments, 
nothing would be gained by changing sex. We 
will now examine the four studies that have not- 
ed differences in the environment and that report 
measures of staminate and pistillate fitness. We 
will consider whether fitness differences exist be- 
tween the two sexes and whether those differ- 
ences are correlated with environmental differ- 
ences, 
== (1973) conducted manipulative exper- 
poe with four species of polygamous orchids. 
Pre plants in full sun and then in “bright 
е” (50% full sun) and noted the sex ex- 


ha 


with androecious plants. For two species, an- 
ng та Performance was enhanced by shad- 
of v of her studies coupled with those 
> н 962), which demonstrated that ап- 
аны Plants of some orchid species are pro- 
hon. more abundant in shady areas and 
mE plants more common in light gaps, 


Mein plants to shading (partial niche sep- 
hei. rerom (1981) compared the sex 
би puiations of Hesperochloa kingii, a 
Sie ^ ein in mesic versus xeric 
uo: 5. They found six to seven bar dif- 

In Soil water potential between xeric and 


mesic sites. As previously noted, they observed 
proportionately more androecious plants in the 
xeric environment. Fox and Harrison (1981) also 
used the number of inflorescences per individual 
as a measure of fitness. Because both sexes usu- 
ally produced the greatest number of inflores- 
cences in mesic environments, we report fitness 
of both sexes as 1.0 on those sites. To allow easy 
comparison, the inflorescences/plant ratios on 
xeric sites are given as a fraction of the number 
produced on the more moist paired site (Table 
2). In three of the four cases considered, an- 
droecious plants were appreciably more fit than 
were gynoecious plants on xeric sites. The fourth 
case was puzzling to Fox and Harrison and is to 


"TABLE 2. e effect of environment on the fitness 

plants of Hesperochloa 

kingii (Fox & эзи 1981). See text for ап expla- 
nation of fitness values. 


An- Gy- 
droe- noe- 
cious cious 

Fit- it- 

Site Description ness ness 
A Moist alluvial bench 1.00 1.00 
Dry sandy slope 1.00 0.57 

B Moist north-facing slope 1.00 1.00 
Dry south-facing slope 0.50 0.24 

C Moist grassy bottom land 1.00 1.00 
Dry south-facing slope 0.61 0.11 

р Moist sagebrush bench 1.00 1.00 
Dry west-facing slope 0.89 1.42 

Overall | Moist 1.00 1.00 
Average} Dry 0.75 0.59 


268 


us as well, because the fourth site shows the great- 
est difference in sex ratio between moist and dry 
microhabitats in the study, i.e., a slight pistillate 
biased sex ratio was observed in the wet envi- 
ronment (S/P = 0.69) whereas a significantly sta- 
minate biased sex ratio occurred in the dry en- 
vironment (S/P = 3.76 and x? = 24.39, P< 
0.01). Thus, data for sex ratios are in agreement 
with our E but the relative fitness val- 
ues ob sly do not agree with our thesis. When 
we include E data from this aberrant site (D), 
the overall averages show that dry environments 
depressed pistillate fitness more than staminate 
fitness (Table 2) although the difference is not 
significant (t = 0.69, P < 0.53). When site D is 
excluded the difference is highly significant (t = 
36: Р< 005) 

Freeman and Vitale (unpubl. data) germinated 
spinach seeds in a common environment an 
then randomly assigned seedlings to well watered, 
‘wet’ treatment and a water stressed, ‘dry’ treat- 
ment. Plants in the ‘wet’ treatment received five 
times more water than stressed plants. The av- 

rage number of viable pollen grains per anther 
multiplied by the average number of anthers per 
plant was used as the measure of staminate fit- 
ness. Pistillate fitness was taken as the average 
number of germinable seeds produced/gynoe- 
cious plant. Using Freeman and Vitale’s data, we 


conditions as a fraction of that in the ‘wet’ treat- 
ment. Androecious plants in the ‘dry’ environ- 
ment had a relative fitness of 0.77 while the rel- 
ative fitness of gynoecious plants in the ‘dry 
environment was only 0.16 

Freeman et al. (unpubl. data) have compared 
the reproductive biomass of androecious and 
gynoecious individuals of Atriplex canescens 
growing on steep slopes versus alluvium at slope 
bases. Androecious reproductive biomass was 


productive biomass was taken as the weight of 
fruits just before fruit abscission. Because gynoe- 
cious plants on alluvial soils produced more fruits 
than gynoecious plants on slopes, we calculated 
relative fitness of the latter by dividing their re- 
productive biomass by the comparable variable 
for gynoecious plants on alluvium. Relative fit- 
ness of slope and alluvium androecious plants 
was similarly computed. Relative fitness of ‘slope’ 
androecious plants was 0.82, but relative fitness 
of ‘slope’ gynoecious plants was only 0.33 (t = 
4.82, P < 0.001 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


In each of the foregoing cases, the relative per- 
formance of gynoecious plants on stressed sites 
was less than the relative fitness of androecious 
plants. Such a response would be predicted if the 
sexes actually showed partial niche separation as 
suggested by Freeman et al. (1976) and Onyek- 
welu and Harper (1979). However, we note that 
it is not necessary for gynoecious individuals to 
respond less well than androecious individuals 
under stress to validate the assumption of sex 
allocation theory. It is only necessary that fitness 

and g be unequal 
under some conditi tions. Some physiological, 
morphological, and anatomical studies of dioe- 
cious plants have shown differences between an- 
droecious and gynoecious plants, but in most 
cases there is little indication that the differences 
have ecological or evolutionary significance 
(Lloyd & Webb, 1977; Freeman et al., 1980). In 
contrast, the foregoing case studies suggest per 


in common environments. Such results have 0b- 
vious practical consequences, but they also sug 
gest possible avenues for the evolution of at least 
some dioecious plant taxa and/or taxa capable 
of reversing sexual expression. Linking unequal 
fitness of male and female gametes at common 
sites to evolution of a dioecious species will re- 
quire evidence that androecious plants in stress- 
ful environments sire more descendants by & 
porting pollen to more mesic sites than could be 
produced by nearby stressed gynoecious plants. 
If such a condition existed, plants with pistillate 
flowers in dry environments could increase their 
genetic contribution to future generations by pro- 
ducing staminate flowers instead. In the only €x- 
perimental study 
uate the fitness of stressed and unst 
androecious and gynoecious plants, Freeman 
Vitale (unpubl. data) show that androecious plants 
from a dry environment that sired three gyn 
cious plants there and one in a wetter environ- 
ment would leave more offspring in the ибт 
generation, оп average, іп the moist than in 
dry environment (54 in the moist versus 21 є 
the dry), because gynoecious plants were sixfo 
more fit in the moist than dry environments- 
SEX CHANGES AND TERMINOLOGY 
droe- 
ast some 
2 in all 
mecha” 
птеп! 


re foregoing evidence indicates чи ап 


dioecious plant species are not ди 
уобичајен Because we know of no 
m by «аыл Блада ла 


— 
anvirO 


| 


| 


| 


1984] 


in which they fall, some plant species satisfy the 
assumptions of sex allocation theory and would 
be predicted to be capable of switching sex by 
that theory. The question we now address is, “Do 
individuals of dioecious plant species change sex 
(or, in the case of annuals, show environmental 
sex determination)?” Also, do individuals of 
monoecious plant species alter their floral sex 
ratios in response to changes in environmental 
quality? 

Dioecious species, by definition, contain only 
unisexual individuals. Obviously a plant that 
changes sex must be genetically bisexual and is 
not strictly speaking dioecious. The ecological 
and evolutionary significance of altered sex 
expression is equivalent to dioecy, however. We 
will refer to species that display environmental 
sex determination or change sex as subdioecious. 

Typically, Atriplex canescens individuals are 
either unisexual (Gynoecious = G, or Androe- 
cious = A) or monoecious (Mo = having both 
staminate and pistillate flowers on the same in- 
dividual). A plant that is exclusively gynoecious 


Oecious individual one year that displayed a sin- 
pe staminate flower among a myriad of pistillate 
Owers the next has not changed its primary sex- 
val expression. Nevertheless, the plant has dem- 
ie. apacity to p staminate 
ad а : ~, will consider any gynoecious plant 
mine obtains an appreciable fraction of its 
= say 20%) through pollen has changed its 
Pi State. For convenience, changes of less 
20% will be described as sexual inconstancy 
= hange of the primary sexual state. 
леч exceeding 20% sex change. 
rei % of the flowers are of the sex not 
as ni displayed, we will describe the plant 
чы 1005. If changes exceed 80%, we will 
udin * situation as a change in primary sex- 
Pression, ` 


A 
add "nin of researchers, most notably Lloyd 


е 
urthermore, they argue that if plants 


tion of th rimary sexual expression, the frac- 
We will © Population so affected is trivially small. 
Present evidence suggesting that in the 


x 
change p 


FREEMAN ET AL.—SEXUAL LABILITY IN ATRIPLEX 


269 


case of Atriplex canescens, the Lloyd and Bawa 
position is inconsistent with the data. If plants 
do track the environment as hypothesized in sex 
allocation theory, then small changes in ratios of 
staminate to pistillate flowers from year to year 
on monoecious plants would also be predicted 
and should be more frequent than large changes. 
Thus, plants that respond to modest environ- 
mental changes may appear to be only sexually 
inconstant. Absence of large changes in floral sex 
ratios of individuals would constitute strong evi- 
dence against sex allocation theory. If large 
changes can be documented, sex allocation the- 
ory would be strengthened. 


SEXUAL STATES IN ATRIPLEX CANESCENS 


In 1977, McArthur reported that some indi- 
viduals of a half sib family of Atriplex canescens 
changed sexual expression. Work has continued 
with this population to the present. Several kinds 
of data on the sexual state of individuals now 
exist. Annually, all individuals have been clas- 

arl E 1 (A), gy i (G)or mon- 
oecious (Mo). In Table 3, the kinds of changes 
observed are listed. As expected, the bulk of the 
changes were between gynoecious and monoe- 
cious or i nd i states; only 
33 of 665 individuals changed from androecious 
to gynoecious or vice versa. additional six 

lants were monoecious at one time in their life, 
exclusively androecious another year, and exclu- 
sively gynoecious in yet another year. Changes 


support sex allocation theory. However, gynoe- 
cious ^ monoecious and androecious ^ mon- 
oecious changes could represent either sexual in- 
constancies or major changes of sexual expres- 
sion, depending on ratios of staminate and 
pistillate flowers of individual plants. These data 
by themselves are not sufficient to allow discrim- 
ination between sexual inconstancy and sex 
change without the addition of floral sex ratio 
da 


ta. 

Fruits were collected from 14 of 35 plants that 
had been and 1 d i but never 
gynoecious. Fruit production of these monoe- 
cious plants was compared with average fruit set 


gle episode of sexual change. In cases in which 
plants had multiple episodes, the year of largest 
fruit set was used. Plants producing less than 20% 
as much fruit by weight as th ge gy i 

re classified lly inconstant. Plants 


1 + 
piani We 


270 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Мог. 71 


TABLE 3. Summary of floral phenotypes in the U103p family of Atriplex canescens over the period 1972- 
1978. The population is maintained at the Snow Field Station, Ephraim, Utah (McArthur & Freeman, 1982). 


Number of Plants 


Constant Changed Phenotypes 


Without Phenot 4 Probability 
Floral Changing = ans E OR SEE YE of Constant 
Phenotype? 1972 Phenotype 1973" G A Мог“ Phenotypes 
G 372 40 149 и 22 161 0.51 
А 228 39 155 11 nt 23 0.85 
Mo 34 2 1 12 13 6 0.09 
0 ж 8 1 3 6 B 0.29 


Totals 665 894 306 26 41 203 


a G = Gynoecious; A = Androecious; Mo = Monoecious; 0 = No flow 
°С, А, and Mo, phenotypes considered constant if only departure was one 0 phenotype. 
* Includes plants that were С or A some years in addition to being Mo for at least one year 
ё Actually 101 plants died and seven were sacrificed for pathological study by 1978. The other 19, however, 
are accounted for under “changed phenotypes.’ 


producing 20-80% as much fruit as an average — androecious phenotype. If such plants were sim- 
gynoecious plant were considered to have changed ply sexually inconstant, only a slight reduction 
from unisexual to a monoecious state, and those іп fruit set would be expected when the plant was 
producing greater than 80% of the average fruit monoecious. We now compare fruit crop of gy- 
crop were considered to have changed their pri- поесіоџѕ ~ monoecious plants against average 
mary sexual expression. These data show that fruit crop of the same plants while they were 
3696 of the 14 test plants were sexually incon- functioning as exclusive gynoecious plants. If re- 
stant, 43% were monoecious and 21% changed duction in fruit crop was less than 20%, plants 
their primary sexual expression. Thus by our cri- жеге classified as sexually inconstant. When fruit 
teria, over 64% of the androecious ^ monoe- set reduction exceeded 80%, plants were consid- 
cious plants made significant changes in sexual егей to have had a change in primary sex н 
expression during the period of record. Had we expression. Changes between 20 and 80% in frui 
counted multiple episodes of sex changes rather production were considered as possible changes 
than only the year of largest fruit set, percentages to the monoecious condition. Again, we consid- 
for the sexual states would be: sexually incon- егей all changes and the largest change exhibited. 
stant, 42; functionally monoecious, 46; and Data exist for only 48 of the 173 plants. 
piri n in primary SM expression, 12. all changes are considered, 46% were less Pe 
t that seven (21% x 20%, and 38% exceeded 80% reduction in fru! 
ie of the androecious > monoecious plants set. The remaining 17% of changes fell be у 
changed their major sexual expression, whereas 20 and 80% reduction in fruit set. When У we con 
an additional 15 plants were monoecious for at sider only the largest changes, 33% of the ве | 
least one year. Thus the total number of plants were less than 20%, 52% exceeded 80%, and 1 а 
changing sexual emphasis should be increased exceeded 20% but were less than 80%. These 
by the seven plants that were staminate and be- documenta drastic reduction in fruit set as plan 
came pistillate biased monoecious individuals. ^ changed from strictly gynoecious tO a mo for 
n order to provide a complete inventory of  cious condition. Two possible explanations ^ 
individuals capable of sex change in the popu-  theresults exist: (1) plants changed to a prim 


lation, we must add plants that changed from — staminate biased monoecious state, OF (2) „= | 


pistillate to predominantly staminate biased меге only sexually inconstant but had low 
monoecious individuals (80% or more staminate production. 

flowers) to the 46 plants noted above. We also In addition to recording fruit produ m 
collected fruit from plants displaying gynoecious plant, we have also subjectively rated overall 
and monoecious states but not the exclusively productive potential (staminate plus ~ 


ction bY ! 
istillate 


—— 


1984] 


functions) of monoecious plants. The rating scale 
ranged from 0 to 9 and was based upon the num- 
bers of flowers of each sex. Although the subjec- 
tive rating data are crude, they do give some 
indication of the importance of the male sexual 
functions on plants that have never displayed the 
exclusively androecious phenotype. Such data 
exist for 84 plants that displayed the gynoecious 
and monoecious phenotypes, but were never ex- 
clusively androecious. If these gynoecious mon- 
oecious plants were only slightly sexually incon- 
stant while in the monoecious state, one would 
predict that their overall reproductive potential 
as androecious individuals would be slight. How- 
ever, if primary sexual expression changed, one 
would expect high subjective ratings and a low 
fruit production. It is important to note that pol- 
len was not limiting in this population (Mc- 
Arthur et al., 1978). 

Plants were assigned to one of the ten cate- 
&ories of ‘reproductive potential, and the mean 
number of grams of fruit produced (and standard 
deviations) were computed for each category. For 
*xample, plants that displayed the gynoecious 
Phenotype in 1975 and were given the rating of 
l, Produced, on the average, 1 g of fruit; plants 
B ven a rating of 9 in 1975 produced an average 
of325 8 of fruit. In 1974, gynoecious plants with 
po pdt rating of 9 produced an average of 

99 8 of fruit. Given the standards for plants 
= exclusively pistillate flowers, we can ex- 
== с set of monoecious individuals and 
у vs individual to a reproductive poten- 
di Ss solely on the basis of fruit set. For ex- 
ds „а plant that was phenotypically monoe- 
me ae m and produced 60 g of fruit would 
diis gned to &ynoecious reproductive class 4 

€ basis of fruit production. If the plant had 

a Md 2 4, we would conclude that the bulk 
ша 7 uction was through the gynoecious 
: 1, on the other hand, a monoecious 


= Produced 60 g of fruit and received а rating 


-— flowers. Thus, the important parameter 
айыы Co! in a plant's rating as a mon- 
solely у LÍ" and its expected rating based 
ing P rip Tuit production. Individuals show- 
nces 
айыы pe or four classes, we considered 
МИ ланца ave changed to a functionally mon- 
€, and if the difference was greater 


FREEMAN ET AL.—SEXUAL LABILITY IN ATRIPLEX 


271 


than five, the plant was considered to have 
changed its primary sexual expression. The data 
show that 48 ofthe 84 plants (5796) were sexually 
inconstant, 25 plants (30%) changed from the 
gynoecious to functionally hermaphroditic state, 
and 11 plants (13%) changed sexual expression. 
These data are consistent with conclusions 
drawn from Table 3, and suggest that both ex- 
planations for the reductions in fruit sets may be 
valid (i.e., some plants become predominantly 
staminate, whereas others become monoecious 
but produce little fruit). They also provide a con- 
servative estimate of the number of plants that 
were gynoecious and changed to prevailingly sta- 
minate biased monoecious individuals. Multi- 
plying 13% by the number of plants that were 
gynoecious or monoecious but never androe- 
cious (173), we obtain an estimate of 23 gynoe- 
cious plants that became prevailingly staminate 
biased bisexual plants. Adding this to the пшт- 
ber of plants observed to change from androe- 
cious to gynoecious (33) plus the number of an- 
droecious plants that changed to pistillate biased 
monoecious individuals (7) plus the six plants 
that displayed all three phenotypes, gives a total 
of 69 plants that changed sex completely or 
changed their pr imar y 1 р 1 ( gh ly 
10% of the total of 665 individuals studied). This 
is still only part of the story, for we have not 
considered plants that changed from the unisex- 
ual to the monoecious state, for which 20 but 
less than 80% of their flowers were of the sex 
opposite to that previously produced. For the 
androecious to monoecious class, 26 plants are 
tallied (35 plants x 0.4615). For gynoecious to 
monoecious, the number would be 52 plants 
(173 x 0.2979). Thus, by our criteria 69 + 78 or 
147 plants of 665 (21%) changed their sexual 
state. We consider this a conservative estimate 
for two reasons: (1) many sex changes were re- 
corded during the drought of 1976-1978, but 
those data were not usable, because correspond- 
ing fruit set data were not taken, and (2) at least 
some plants considered sexually inconstant on 
the basis of available data have the potential to 
change sex under other conditions. The latter 
consideration is dramatized by plant $7—40, 
which, by the criteria employed here, was a sex- 
ually inconstant gynoecious individual. That 
plant was cloned into 24 ramets, seven of which 
have flowered. Five of the seven ramets pro- 
duced only staminate flowers and produced as 
many flowers as the average ramet from pure 


272 


TABLE 4. The number of individuals changing sex 
in natural populations of five species of Atriplex. All 
populations consist of a sample of 200 individuals 

at random, except for A. lentiformis. The A. 
lentiformis population included all 70 individuals. The 
observations cover the five years from 1978 to 1983. 


Type of Change 
in Sexual Morph 


G^ AorG “+ Мо А 9 
+ Mo 8 


Species 


А. canescens 


А е Mo 17 

А. confertifolia а  Аогао Мо • А 17 
(Desert Experi- а ^ Mo 8 
mental Range A ^ Mo 8 
Population) 

A. confertifolia G^AorG^Mo^A 6 
(Purgatory а ^ Mo 0 
Basin A ^ Mo 2 
Population) 

A. corrugata G^AorG^Mo^A 12 

^ Mo 9 

A ^ Mo 54 

A. cuneata G^AorG^Mo-^A 6 
а > Mo 26 

А > Мо 11 

А. lentiformis GeAorGeMorA 9 
а ^ Mo 9 

А ^ Mo 5 

A. tridentata G^AorG^Mo-^A 11 
G ^ Mo 39 

A ^ Mo 9 


androecious plants. Clearly, this “sexually in- 


"right" circumstances. 
The above data suggest that individuals of 
Ане | + с کو‎ s +1 


results because they are derived from a popu- 
lation of half sibs descended from a single gynoe- 
cious plant. Data from Freeman and McArthur 
(unpubl. data), however, demonstrate sex change 
in natural populations of A. canescens, A. con- 
fertifolia, A. corrugata, A. cuneata, A. lentifor- 
mis, and A. tridentata (Table 4). In the majority 
of cases, individuals changed from a unisexual 
to a monoecious state, but complete changes were 
also observed in all species. Furthermore, exten- 
sive studies on natural populations and clones 
of A. canescens derived from natural populations 
are in agreement with these results. The half sib 
family of A. canescens, then, is not atypical for 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


the genus; sex change seems deeply entrenched 
in species of Atriplex of the intermountain west 
of North America. 


RELATED STUDIES IN SEX CHANGE 


In addition to our own studies, well docu- 
mented records of individuals that change sex 
under natural conditions have been reported for: 
Juniperus australis and J. osteosperma (Vasek, 
1966), Acer pensylvanicum (Hibbs & Fischer, 
1979), Acer saccharinum (Sakai, unpubl. data), 
and Elaeis guineensis (Williams & Thomas, 
1970). In addition, there are voluminous data on 
Arisaema triphyllum and A. dracontium, Se 
quential hermaphrodites (typically individuals 
begin by prod g staminate fl d change 
to production of pistillate flowers) that are widely 
acknowledged to change sex (see Gow, 1915; 
Pickett, 1915; Schaffner, 1922; Maekawa, 1924; 
Camp, 1932; Sokamoto, 1961; Policansky, 1981; 
Bierzychudek, 1982; Lovett-Doust & Cavers, 
1982). In all of these species, some individuals 
are reported to change from the unisexual t0 à 
monoecious state. Unfortunately, however, there 


is а paucity of information concerning the ре" | 


centage of staminate and pistillate flowers pro- 
duced by monoecious plants of these species. 


MECHANISMS AND CONSEQUENCES OF SEX 
CHANGE IN ATRIPLEX CANESCENS 


The foregoing data suggest that the assump 
tions of sex allocation theory are valid for many 
plant species in a variety of distantly related "€ 
ilies. The magnitude of change in seve di is 
ent populations demonstrates that sex change i 
not numerically trivial. At this point we e 
with a number of d questions: (1) 
conditions induce plants to change ?0) 
changing sex enhance an individual's per 
By what mechanisms do plants change 5€*' x 
Is sex change compatible with the cun 
derstanding of the genetics of sex determina 
in plants? 

In regard to the question of the con 
induce plants to change sex, we have 
the sexual expression of each indi 


the 
half sib family of Atriplex canescens ae 


i ei seve 
period 1968-1978. This includes à (1976 I 


period (1972-1973) and a major drought 
1978). In both stressful periods, significantly a 
plants shifted away from femaleness (1€ 
Mo or A, and Mo — A) than towards fe 


sex? (2) DOS | 


ditions that | 
recorded 


vidual in the 


Ea — — 


шшк уыт чн сероз 


1984] 


TABLE 5. Direction of change in sexual state fol- 
lowing severe external stress. The winters of 1973- 
1974 and 1974-1975, were normal for temperatures 
and precipitation. The winter of 1972—1973 was un- 
usually cold, and the winter of 1975—1976 was much 
drier than normal. Magnitudes of difference in popu- 
lation changes in sexual expression in normal and 
stressful years are tested for significance by Chi-square 
analyses. G = Gynoecious; A = Androecious; Mo = 
Monoecious. The expected values are shown in paren- 


Type of Sex Change 


G to Mo A to Mo 
Year ОСА MotoA MotoG orG 
1972-1973 85 10 
(48.8 (10.6) (28.5) (26.1) 
1973-1974 16 12 52 42 
(52.2) (її) O05 Or 
х? = 98.2 P- Uu] 
G to Mo A to Mo 
o A MotoA MotoG orG 
1974-1975 13 6 10 
(25.5) (1.5) (4.8) (5.2) 
1975-1976 104 16 
(91.5) (5.5. одар (18.8) 
ALLE OD ee 34.1 P « 0.01 


dn G or Mo and Mo — G) (Table 5). In ad- 
Е n to such obvious external stresses, we have 
ron the influence of prior year fruit pro- 
(Ta ed On sexual expression in the next year 
X € 6). Plants that produced heavy fruit crops 
> 125% of the plant's annual longterm av- 
Yin teh changed sex more readily than plants 
ali light (X = 75% of the plant’s average 
D) ог normal fruit crops (0.75% < X < 1.25%). 
^ also observed that mortality was signifi- 

4 "id d among plants on the edge (4390) 
edt sib family plantation than among in- 
ulation ч in the center (11%) of the pop- 
í - : е consider that edge plants are more 
e Mie =“ water because of their greater ex- 
софи ight and wind. When the incidence of 
for E changes (С ~ A) are compared 
the interi occupying the edges versus those in 
c E. the patch, significantly more 
(Table 7). in plants growing around the edges 
be Ме emphasized temperature and water 
of n the foregoing analyses, but the work 
(1973), Cox (1981), Schaffner (1922, 


FREEMAN ET AL.—SEXUAL LABILITY IN ATRIPLEX 


273 


TABLE 6. In this table we examine the hypothesis 
that a heavy seed set in year X may influence the sex 
of individuals in year X + 1. Because not all individ- 
uals appear to be capable of changing sex, we selected 
those which could change sex and then classified them 
into two groups, i.e., those that changed in year X + 
1 and those that did not. We then ranked the seed set 
of the individuals in year X into three categories, i.e., 
х < 0775-850. 15% = © 099 12531 <x. 


75% < 
z< 75% х= 125%: 12596 — x 


Did Not Switch 8 13 6 
02) 616 41.34 
Switched 23 21 41 
(23.53) (23.51) (35.66) 
У x? = 6.67; P < 0.05. 
1925, 1927) and others suggests that Ё such 


as light intensity and mineral nutrient availabil- 
ity may also affect sexual expression of plants. 
Gregg (1973) showed that when gynoecious or 
large monoecious individuals of the tropical or- 
chids she studied were placed in the shade, they 
produced staminate flowers. Androecious plants 
placed in full sunlight often produced pistillate 
flowers. Such effects of light on sexual expression 
suggest that studies of sexual expression of co- 
horts of dioecious tropical forest trees are needed 
during the period when individuals move from 
shaded forest floor and subdominant positions 
into the canopy. Are the mortality rates of an- 
droecious and gynoecious plants equal? Are an- 
droecious and gynoecious plants equally fit at all 
ages and in all positions within and below the 
canopy? Do individuals change sex? Studies on 
Castilloa elastica (summarized in Dzhaparidze, 
1967) show that sequential I phroditi oc 
curs in at least one tropical tree species. 
Unfortunately, we currently have only indirect 
measures to predict whether sex change will en- 
hance fitness. Cole (1954) was the first to em- 
phasize the contribution of early reproduction to 
fitness. In this connection, we find that Atriplex 
canescens plants of variable sexual expression 
reproduce significantly earlier in life than con- 
stant gynoecious individuals but later than con- 
stant androecious individuals (Table 8). Results 
are based on 70 ramets from sexually labile in- 
dividuals, 70 ramets of constant androecious 
plants and 61 ramets from constant gynoecious 
plants. Of the 70 androecious ramets, 69 flow- 
ered in the second year after cloning; 34 sexually 


274 


TABLE 7. Comparison of the distribution (edge ver- 
sus the interior of the patch) of plants that have com- 
pletely changed sex (A ~ С) versus those that have 
never changed sex. Expected values are shown in ра- 
rentheses. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


TABLE 8. Incidence of flowering among two-year 
old ramets of Atriplex canescens. The analysis is of the 
number of plants in each category. Expected values in 
parentheses. 


Plantation 1 Androe- ynoe Sexually 
ALG Constant (irrigated) cious cious Labile 
Edge 28 108 Flowering 69 6 34 
(18.0) (118.0) (36.86) (35.28) (36.86) 
Interior 31 278 Nonflowering 1 1 
(41.0) (268.0) (33.14) (31.72) (33.14) 
x? = 9.22 P « 0.01 x? — 110.99 P « 0.001 
Plantation 2 Gynoe- Sexually 
Classes (non-irrigated) cious Labile 
of : 
Flowering 6 34 
A а Sex Change (19.56) (20.44) 
Edge 28 68 Nonflowering 61 36 
(19.7) (76.3) (47.44) (49.56) 
Interior 31 160 ×2 25.99 P « 0.01 
(39.3) (151.7) 
x? 6.6 Р < 0.01 


labile ramets also flowered, but only six gynoe- 
cious plants had flowered by the end of the sec- 
ond growing season (Table 8). Of the ramets from 
sexually labile individuals that flowered, 11 were 
staminate, 21 were monoecious but prevailingly 
staminate, and two were exclusively pistillate. 
In addition to the time of onset of reproduc- 
tion, parental longevity and the number of off- 
spring per reproductive event have an effect on 
the fitness of an individual (Cole, 1954). We have 
obtained two measures of longevity: the first is 
based on the average age at death of individuals 
in the half sib family; the second considers mor- 
tality through time in ramets of common age 
from constant staminate, constant pistillate, or 
sexually labile individuals. In the half sib pop- 
ulation, the average gynoecious plant died at an 
earlier age than either androecious or sexually 
labile plants. Plants that changed sex lived sig- 
nificantly longer than either androecious or gy- 
noecious plants (Table 9). In our second set of 
data, no mortality was observed among ramets 


y after seven years. 
Androecious plants exhibited 99% survivorship, 
but gynoecious survivorship was only 87% after 
seven years. The ability to change sex thus ap- 
pears adaptive, at least as far as age at first re- 
production and survivorship are concerned. 

Finally, we examine fruit production of con- 
stant gynoecious plants and plants that vacillate 


between the gynoecious and monoecious states: 
We have no valid way of comparing reproductive 
output of androecious plants and sexually labile 
individuals, but we can compare fruit production 
of sexually labile plants and gynoecious plants. 
For the four years for which fruit production data 


are available, plants that changed sexual expres- _ 


sion at some time in their life averaged 327 
fruit per year, whereas constant gynoecious plants 
averaged 330 g per year. We point ош, however, 
that the very highest fruit producers are con 
gynoecious plants (McArthur et al., 1978). d 
addition, of course, the sexually labile indivi" 
uals also reproduced via pollen in at least one 
year. For the period of record, it would appear 
that plants that change sex are not disadvan- 
taged, but indeed may enjoy a fitness advantage 
in terms of offspring produced per year. о is 
complete demographic analysis is needed 
under way. the 
The third question posed earlier concerns Ab 
mechanism(s) by which plants change wo 
though we lack experimental data on how р = 
change sex, it is important at this stage pe 


go 


sible models be formulated. Two fairly ме sion | 


ied models could account for our ova О | 
on Atriplex canescens. The first is derived 978). 
the work of Chailakhyan and Khryanin (1 like 
They have shown that in spinach (which 


Atriplex, is a member of the Спепороди pie | 


and hemp, the ratio of cytokinin to gi 


or 


1984] 


TABLE 9a. Age at death of Atriplex canescens in- 
dividuals of different sexual morphs. All individuals 
are from the half sib population of McArthur (1977). 
All plants originated from seed germinated in 1968. 
Th 1 2 e 1435 tad + éh с Fi 


pop ield Station, 
Ephraim, Utah. 
Initial 
Number % Average Age 
Sexual of Indi- Mortality at Death 
Morph viduals 1972-78 (years)? 
A 190 21.6 4.85 + 1.56 
G 203 20.2 зе T LED 
Mo 261 8.0 LL IS 


* All means differ significantly from each other. 


acid controls sexual expression. With cytokinin 
In excess, plants g ally produce pistillate fl 

ers. Itai and Vaadia (1 970) have shown that un- 
der conditions of water stress, cytokinin is not 
transported to above ground parts from sites of 
synthesis in the root. Chailakhyan and Khryanin 
(1978) have shown that gibberillic acid continues 
to be synthesized in leaves when plants are 
Stressed for water. Thus, should a plant experi- 
ence severe water stress, cytokinin flow to stem 
tips appears to diminish, whereas gibberillic acid 
continues to be produced. Under such condi- 
tions, even а plant genetically predisposed to 
Produce cytokinin in abundance, and thus pro- 
duce pistillate flowers, might instead produce 

ers 


Staminate flowers. 
Pharis (1975) has shown that the ratio of polar 


Converted to non 
polar forms, and again, plants 
Produce pred wis 


à ominantly micr i - 
ductive E y osporangiate repro 
Stly, we return to the question of genetic 
чао f sexual expression, a theme that two 
е previously discussed (McArthur, 1977; 
1982). It et al., 1980; McArthur & Freeman, 
subdioeci seems likely that not all dioecious or 
ual ex "ns plants are capable of changing sex- 
"*Pression. In some species, sex appears to 
маа controlled by genetics. Perhaps the most 
сазе of such control occurs among the 
inherit a | (Viscum) in which gynoecious plants 
androeci агре translocation ring, a feature that 
us plants lack (Wiens & Barlow, 1979). 


FREEMAN ET AL.—SEXUAL LABILITY IN ATRIPLEX 


275 


TABLE 9b. Mortality among Atriplex canescens in- 
dividuals of different 1 morphs. Ramets were tak- 
en from plants taken from a population native to the 
Book Cliff area of east central Utah. 


Morph % Survival After 7 Years 
Mo 100 
A 99 
G 87 


Other rigid genetic systems are also known to 
occur (Westergaard, 1958; Lloyd & Bawa, in 
press). It is not clear how common such systems 
are. The problem is complicated because even 
in species such as Atriplex canescens, which are 
known to contain individuals with labile sexual 
expression, an appreciable fraction of the pop- 
ulation does not seem capable of sex change and 
shows no form of sexual inconstancy. Sexual 
expression in such individuals is constant and 
indifferent to environmental fluctuations. We 
have observed thousands of plants over nearly a 
decade. Many have maintained a constant uni- 
sexual state throughout the entire period. When 


are cloned and placed in a variety of environ- 
ments, sexual expression of ramets is always that 
of the parent plant. There is thus little doubt of 
a strong genetic component to sexual expression 
in Atriplex, particularly in A. canescens. Never- 
theless, we also find many individuals of A. ca- 
nescens and many other species with subdioe- 
cious individuals that express more than one 
sexual state in their life. The work already pre- 
sented in this paper indicates that at least three 
sexual morphs occur: androecious, gynoecious, 
and labile. We recognize that the third sexual 
morph may ire furtl bdivision when de- 
tailed genetic studies are made. We believe that 
all of the observed facts can be accommodated 
by known genetic mechanisms since sexual 
expression depends on both the quantities of and 
ratios among hormones, and hormone produc- 
tion is affected by both genetic and environmen- 
tal factors. Given differential effects of environ- 
mental stress on hormones controlling sexual 
expression, tissue differentiation and flower 
morphs could be dramatically altered in kind or 
degree from year to year on the same individual. 
We thus fail to see any compelling reasons to 
interpret A. t ph or diphasic 
model as do Lloyd and Bawa (in press). A variety 


276 


of data for A. canescens argues for at least three 
sexual morphs with igs нижа morph capable of 

/ers only, pistillate flow- 
ers only, o or 1 individuals having a уа- 
riety of staminate to pistillate flower ratios. Our 
clonal studies, which will be summarized else- 
where, show that all of these phenotypes can be 
derived from a single sexual labile individual in 
a single year under common garden conditions. 


CONCLUSIONS 


The picture now emerging of sex expression 
in A. canescens is far more dynamic than most 
have previously believed. Some individuals ap- 
pear capable of widely divergent floral sex 
expression in response to variable local environ- 
mental conditions and the individual’s own 
physiological state. Modifications range from 
modest adjustments to complete changes of sex- 
ual expression. Such modifications appear to be 
adaptive. How such modifications are achieved, 
through interactions of environment, physiol- 

and genetics are subjects requiring further 

ње Орн у Likewise, mechanisms by which 

androecious, gynoecious, and sexually labile in- 

dividuals persist in common populations remain 
to be identified. 


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VARIATION IN FLORAL SEXUALITY OF DICLINOUS 
ARALIA (ARALIACEAE)! 


SPENCER C. H. BARRETT? 


ABSTRACT 


Spatial and temporal variation in floral sexuality of di 


system and reproductive success of individuals. Observations of the phenology of the sex condition 


bution. In forest habitats flowering staminate ramets occur a 
particularly in shaded locations. This pattern is due to differences between ramets of th 


and dioecious Aralia nudicaulis indicate non-random patterns of 
а fema 


in the frequency of flowering, p 
data on the flowering phenology 
fi 


info 
ize 


several othe 


r plant communities and may result from the absence of functional 


Previously published 


of staminate and pistillate ramets are re-interpreted in light of 
rmation showing differences in the microdistribution of flowering ramets of the sexes. Large genet 
"eg : 


in pistillate plants of dioecious species and their importance to total fitness in hermaphrodite plants. 


The mating success of individuals in diclinous 
plant populations is strongly influenced by spa- 
tial and temporal variation in the sexual con- 
dition of flowers. The variation is manifested at 
various levels including individual flowers, in- 
florescences, ramets, and genets during a single 


r 
of diclinous populations have usually revealed 
non-random patterns of flowering in space and 
time of the sexual morphs or among staminate- 
and pistillate-functioning flowers (Lloyd, 1973, 
1974, 1981; Jong, 1976; Webb, 1976; Cruden & 
Hermann-Parker, 1977; Lloyd & Webb, 1977; 
Bawa, 1980a; Lovett-Doust, 1980; Primack & 
Lloyd, 1980; Bullock & Bawa, 1981; Lovett- 
Doust & Cavers, 1982; Lindsey, 1982; Schless- 
man, 1982). This has led to the formulation of 
a variety of hypotheses that attempt to explain 

e adaptive significance of variations in floral 
sexuality. The hypotheses involve several inter- 
related concepts including outbreeding advan- 


tage (Charlesworth & Charlesworth, 1978, 1979; 
Maynard Smith, 1978; Thomson & Barrett, 
1981a; Lloyd, 1982), sexual selection (Gilbert. 
1975; Janzen, 1977; Willson, 1979; Bawa, 1980: 
Givnish, 1980), optimal allocation of resources 
to maternal and paternal function (Charno". 
1979, 1982), and strategies for coping with €n- 
vironmental uncertainty (Thomson & Barrett. 
1981b; Lloyd, 1982). Whereas the relative 1m- 
portance and degree of interdependence of thes? 
concepts for particular taxonomic and ecological 
groups are still under active debate, there 15 
eral agreement on the need for more de 
information on the factors influencing the sexual 
performance of individuals in natural popula- 
tions. 

Until recently the description and nan 
ment of plant sexuality has lacked a quantitati 


gen- 


alone can be particularly misleadin 
mous species. Numerical indices О 


' I thank James Thomson, Kaius Helenurm, and Kamal Bawa for stimulating discussions on Aralia 010108 


and the Natural Sciences and Engineering 


Research Council of Canada for research fun 


2 Department of Botany, University of Toronto, Toronto, Ontario M5S 1A1, Canada. 


ANN. MISSOURI Bor. GARD. 71: 278-288. 1984. 


MM = 


-—À 


~ 


1984] 


BARRETT—DICLINOUS ARALIA 


279 


TABLE 1. Reproductive characteristics of Aralia hispida and Aralia nudicaulis populations from central New 
Brunswick. From Barrett and Helenurm (1981) and Thomson and Barrett (1981). 


Aralia nudicaulis 


Characteristic Aralia hispida 
Major Habitat forest clearings and open, dis- forest understory 
turbed sites 
Clone Size small very large 
Flowering Period July June 


Major Pollinators 


Breeding System 


bumble bees especially Bombus 
vagans and B. terricola vag 
andromonoecism with synchro- 


bumble bees especially Bombus 
ans and B. ternarius 


dioecism 


nized protandry and self-com- 


patibility 
Average Number Flowers per 324 
Ramet 
23.2 


Average Flowering Time per 
Ramet (days) 
Fruit 


fleshy fruit with 5 seeds 


9 75.2, 8 120.0 
9 4.9, 8 7.4 


fleshy fruit with 5 seeds 


gender (Lloyd, 1979, 1980a; Thomson & Barrett, 
1981b) emphasize the quantitative and dynamic 
nature of sexual performance, particularly in 
plants with hermaphroditic flowers. Although the 
Indices make certain unrealistic biological as- 
k umptions, e.g., panmixia, they are useful in il- 
ustrating the great variation in which individ- 
uals can succeed as pollen or seed parents and 
B drawing attention to the basic dichotomy in 
- Sexuality between populations that are 
ies oe in gender and those that are di- 
" т 12 (Lloyd, 1979). These theoretical de- 
a in combination with the use of elec- 
е techniques for estimating mating 
ош. Parameters such as оуше and pollen out- 
&H vits rates (Brown & Allard, 1970; Horovitz 
ме ва 1972; Ross, 1977; Clegg, 1980; Rit- 

_ ) are likely to provide new opportu- 


frequency dependent phenomena 
T E. 1982; Ross & Gregorius, 1983). 
dta eh reproductive success of an individual 
би К will depend on the frequency, 
han ition, and fertility of the remaining 
d лы in the Population. Studies of mating 
only at LE be investigated accurately, therefore, 
acer) Population level, taking into account 
"es and temporal aspects of variation in 

active behavior. 

led observations of flowering patterns and 


sexual performance of individuals in natural 
populations are available for relatively few di- 
clinous taxa. Lloyd and Webb (1977) reviewed 
much of the data prior to the mid 1970s for 
sexually dimorphic taxa. More recent studies in- 
clude Meagher (1980, 1981), Bullock and Bawa 
(1981), Lloyd (1981), Cox (1981, 1982), Poli- 
cansky (1981), Bierzychudek (1982), Lovett- 
Doust and Cavers (1982). Our own studies of 
Aralia (Araliaceae) have involved an examina- 
tion of flowering patterns in the sexually mono- 
morphic A. hispida Vent. (Thomson & Barrett, 
1981b; Thomson et al., 1982) and the sexually 
dimorphic A. nudicaulis L. (Barrett & Helenurm, 
1981; Barrett & Thomson, 1982). Here I review 
some of these studies and make some attempt 
to explain the functional significance of variation 
in sex expression in light of various models of 
selection. 


NATURAL HISTORY OF ARALIA 


The four Aralia species of eastern North 
America are diclinous, perennial herbs or shrubs 
of wooded habitats. Aralia nudicaulis is dioe- 
cious, the remaining species (A. hispida, A. ra- 
cemosa, and A. spinosa) are andromonoecious. 
Our work was undertaken in spruce-fir forests 
and associated habitats in central New Bruns- 
wick during the summers of 1978-1981. In this 
region A. nudicaulis is abundant in the under- 
story of forests, whereas A. hispida is more com- 


280 


BLE 2. Floral sexuality and fruit set (percentage 
of hermaphrodite flowers with mature fruit) in three 
andromonoecious populations of Aralia hispida from 
central New Brunswick. After Thomson and Barrett 
(1981). 


Population 
mple- Percentage 
size, Total Fruit 
ramets) Flowers ó Set 
A (N = 51) 7,407 30.0 70.0 95.8 
B (N = 49) 11,893 26.6 73.4 92.2 
C (N = 50) 8,926 35.0 65.0 97:2 


monly encountered as a weed of disturbed sites 
such as forest clearings, roadsides, and burned 
areas. Where logging roads traverse the forest, 
the two species can be found growing together. 
Although these species share similar pollinators, 


interspecific pollination (Table 1). 

Many aspects of floral biology in Aralia species 
resemble those described for the related Um- 
belliferae (Miiller, 1883; Ponomarev, 1960; Bell, 
1971; Cruden & Hermann-Parker, 1977; Webb, 
1979, 1981; Lovett-Doust, 1980; Lindsey, 1982; 
Schlessman, 1982). Flowers are small, whitish 
green, and aggregated into umbellate inflores- 
cences. Hermaphroditic species are self-compat- 
ible and frequently exhibit complex patterns of 
synchronized protandry or protogyny (see be- 
low). Inflorescences of dioecious taxa occasion- 
ally contain hermaphrodite as well as staminate 
and pistillate flowers. However, our observations 
of A. nudicaulis in Canada and those of Bawa et 
al. (1982) in Massachusetts, indicate that vari- 
able sex expression of individuals is a rare con- 
dition in this species. 

One of the most important ecological differ- 
ences between A. hispida and A. nudicaulis is 
clone size. Clones (genets) of A. hispida are rarely 
larger than a few meters in diameter, with the 
majority being smaller. Genets are composed of 
one to ten ramets, most of which are reproduc- 
tive. In contrast, clones of A. nudicaulis are very 
large and probably of considerable age. Field ob- 
servations of isolated clones, excavation work, 
and mapping studies (reviewed below) suggest 
that in the forests studied by us genets may cover 
several hundred square meters, although un- 
equivocal evidence for this is difficult to obtain. 
Large genets of A. nudicaulis are composed of 
hundreds of ramets, many of which are vegeta- 
tive. The relative proportion of vegetative to re- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


productive ramets varies with local site condi- 
tions, ec dd the light regime (see below). 
Characters such as size, inflorescence produc- 
tion, wail flower number per ramet in A. nudi- 
caulis do not display the high degree of pheno- 
typic plasticity exhibited by A. hispida. 

mble bees are major pollinators of both 
Aralia species. Because flowers are open, small, 
and with anthers and stigmas borne in similar 
positions, wy visitor is * potential pollinator. 
Minor halictid bees, 
and syrphid flies. Foraging bees preferentially visit 
umbels that contain a large number of flowers, 
and there is some evidence that staminate-phase 
inflorescences are preferred over pistillate in A. 
hispida (Thomson et al., 1982). Observations of 
marked bumble bees indicate that indivi 
restrict their foraging to a limited number of plants 
that they visit in regular sequences or *traplines." 


Following pollination кой fertilization fruits of 
both ack, ver- 


tebrate dispersed, мае that usually con- 
tain five seeds. 


GENDER ALTERNATION IN ARALIA HISPIDA 


Aralia hispida exhibits synchronized ges 
i ivi 


ual ra : 

and pistillate phases during their blooming ре 
riod as each umbel order flowers. Controlled po 
linations demonstrate that the period of stig- 
matic receptivity of hermaphrodite flowers 80 
not overlap significantly with the staminate flow- 
ering period and the probability of geitonogamy 
is accordingly reduced. On average a rame 
tions as a male for approximately three weeks 
and as a female for one week. Pollen release by 
hermaphrodite flowers within an umbel lasts for 
four to five days, whereas the pistillate pm 
compressed into one to two days. The © 
proportion of hermaphrodite flowers in à e 
ulation is approximately one-third of the 10 


in 
flowers (Table 2) and their pep ecline 
successive umbel orders or as th son 
gresses. A detailed account of the Ает" bio 


and phenology of flowering of A. hispida is #! ae 
in Thomson and Barrett (1981b). 
Alternation between staminate and pistillat 
function in ramets of A. hispida re 
plex patterns of gender expression within 
ulations. A wave form pattern of flo 
was evident in a population of ramets 


throughout the flowering season (Fig. !)- ти 


sults in com | 
рор 


un. I n 


1984] BARRETT—DICLINOUS ARALIA 281 
3- 
2-4 
9/0 
| ~ 
< 
етага г со да а р а pag er ттт 
0 10 20 30 40 
DAYS 


FIGURE 1. Wavef 


lati T | lin hi 


E 2 P 
Staminate-functioning flowers is plotted daily throu 


and Barrett (19815). 


ud In comparison with the number of days 
jenen cite peaks of different umbel or- 
dii a dition, there is a marked tendency for 
ets of a single genet to be developmentally 
oa with respect to umbel order and 
condition. Intense competition for ovules 
а а а“ A fdifferent 


emm occurs at regular intervals during the 
Pees Period corresponding to the troughs in 
ol a ; Using estimates of functional gender 
duin nine the reproductive success of in- 
tow emiten and pistillate-functioning 
ме. а population with this flowering be- 
VIOr. male c : ES. 

M degree of synchrony between a given ramet’s 

pattern and that of the population. Ra- 


"ld 4 LA а 
SAVAGE YY Lee 


Mets thar ~ 4 


Sita - yi oi 8 
-a time when most other individuals are in their 
te phase will encounter little competition 


for . i 
mates. Figure 2 gives estimates of male re- 


da. The ratio of pistillate-functioning 
r Thomson 


ghout the flowering period of 48 ramets. Айе 


productive success for a ramet which was closely 
synchronized with the remainder of the popu- 
ation. 

Selection on the male component of fitness as 
well as the avoidance of inbreeding may explain 
the complex flowering behavior in A. hispida. 
Intrasexual competition among pollen donors 
may account for the extended staminate phase, 
in comparison with the pistillate phase, of in- 
dividual ramets. The gradual release of pollen 
over a three week period is likely to maximize 
the number of insect visitors and hence the po- 
tential number of mates. Within the life span of 
an individual flower, pollen is released gradually 
by sequential anther dehiscence, and nectar se- 
cretion occurs throughout the day (Thomson et 
al., 1982). The extended staminate phase could 
also have been selected to reduce the likelihood 
of reproductive failure owing to environmental 
unpredictability (Thomson & Barrett, 1981b). 
Unfortunately, models that invoke sexual selec- 
tion or *bet-hedging' often make qualitatively 


— 


282 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог, 71 


OFFSPRING PER MALE FLOWER 


35 


DAYS 


+ throughout 


FIGURE 2. Estimate of mating success of stuminate 
its flowering period. The flowers which 
Breaks between ће curves are days when th 


п 28. i 
are n.ost successful are the n and latest within ea eac 


bel order. 
e. After Thomson and abes Бе 9810) 


similar predictions about the evolutionary re- 
sponse of reproductive traits. Devising experi- 
ments to distinguish the relative importance and 
independence of these processes is a major chal- 
lenge and reminiscent of the difficulties associ- 
ated with various models of selection of self- 
fertilization (see Jain, 1976; Lloyd, 1980b). 
Despite the protracted staminate phase of um- 
bels, mating success via pollen tends to be con- 
centrated at the beginning and/or end of the sta- 
minate flowering period of umbels, resulting in 
characteristic Ms or J-shaped reproductive suc- 


uniformly high 
(Table 2) and therefore there may be no selective 
advantage to a protracted pistillate phase. Tight 
flowering synchrony may be advantageous for 
pistillate-functioning flowers to compensate for 
their apparently reduced attractiveness to polli- 
nators (Thomson et al., 1982). 


Lloyd and Yates (1982) have developed ESS 
models to find the proportions of time that out- 
crossing, dichogamous, hermaphrodite flowers 
should spend in their staminate and pistillate 
phases a optimize total fitness. The models can 
be usefully applied to observations of flowering 
behavior in A. hispida. If paternal and mat 
fitness are pollinator limited, fitness 15 oa 
mized if flowers spend equal amounts of tim 
functioning as males and females. However 
where an increase in male fitness is limited by 
access to ovules and female fitness is limited 9 
resources (Bateman, 1948), natural sé select! 
should favor prolongation of the «алии рч 
The latter conditions fit well with the 
data from A. hispida, in which es 
are consistently high throughout the bloo 
period and fecundity is near maximum. 

The developmental synchronization. 
tandry within and among umbels of 


levels 


и 


1984] 


reduces the likelihood of self- and geitonoga- 

pollinati inbreeding. Thus the 
complex systems of dichogamy exhibited by the 
Araliaceae and Umbelliferae may be viewed as 
outbreeding mechanisms. They may have 
evolved as alternatives to physiological self- 
incompatibility which appears to be rare or per- 
haps absent from these families. In the absence 
of dichogamy or self-incompatibility, the aggre- 
gation of many, small unspecialized flowers in a 
single inflorescence would be particularly likely 
to result in high levels of selfing. 

A different explanation for the synchronized 
patterns of sexual expression was proposed by 
Lovett-Doust (1980) based on his studies of Um- 
belliferae. He suggested that the separation of 
anther dehiscence and stigma receptivity repre- 
sents a pattern of resource allocation that mini- 
mizes competition between male and female ga- 
mete production. This view has been questioned 
by Webb (1981) who suggested that intrasexual 
selection among plants in their staminate phase 
and outbreeding advantage may explain the oc- 
currence of protandry and tight developmental 
synchronization, respectively, in the famil 
Clearly there is a need for experimental tests to 
distinguish between these competing hypotheses. 
а rhe effectiveness of synchronized protandry 


VINILO 


ments could select for increased clone size. Ra- 
mets in а large clone are likely to experience 
bons different environmental conditions, and 
Manius unlikely that mechanisms could exist to 
€ ме sexual phase synchrony with the result 
thes Eu amy would increase. It is possible 
du ert ese circumstances the outbreeding 
eic "d gained by a unisexual mutant could 
veces ۲ with dioecism ultimately being 
кан uch an explanation could account for 
plant Кг between patterns of sexuality and 
terest ы, о served in Aralia. It would be of in- 
bellifergs xamine these relationships in the Um- 
Y onion Which dioecy and various forms of 
tion of Heed “йр. In addition, ап examina- 
Чы. Ме ative effects of self- and cross-fer- 
чоо т ооа vigor and fertility in ап- 
cious taxa would be useful for 


BARRETT—DICLINOUS ARALIA 


283 


evaluating the plausibility of the outbreeding ad- 
vantage model. 


FLOWERING IN ARALIA NUDICAULIS 


Populations of Aralia hispida are frequently 
composed of scattered colonies of flowering ra- 
mets, which on excavation proved to be genets. 
Expansion of clone size is often limited by dis- 
turbance or successional processes and hence the 
limits of individual genets can usually be esti- 
mated. In A. nudicaulis the size and complexity 
of the rhizome system makes identification of 
genets, as well as determining the sex of vege- 
tative ramets, a difficult task. This problem is 
particularly acute in locally disturbed areas or 
where high flowering density occurs. As a result 
of these difficulties the unit of investigation in 
our studies has exclusively been the flowering 
ramet, composed of a single inflorescence and 
subtending leaf. The extent to which the behav- 
ior of ramets reflects that of the genet is un- 
known. In large clones it is possible that ramets 
separated by a considerable distance are physi- 
ologically independent (see Bawa et al., 1982). 


TEMPORAL PATTERNS 


the summers of 1979 and 1980. To avoid over- 
representation of individual genets, transects 1— 

km in length were adopted for sampling phe- 
nological patterns. Four transects were censused 
at one or two day intervals along a roadside and 
in forest habitats. Further details are given in 
Barrett and Helenurm (1981). In three of the four 
transects, pistillate ramets began flowering and 
reached peak flowering before staminate ramets. 
This difference was particularly evident in the 
two forest transects. In virtually all other studies 
of the flowering phenology of the sexes in dioe- 
cious species, the reverse pattern is evident (see 
Lloyd & Webb, 1977) and several adaptive ex- 
planations have been proposed. For example, 
Bawa (1980a) and Bullock and Bawa (1981) have 
suggested that early staminate flowering and late 
pistillate flowering in the small tree Jacaratia 
dolichaula (Caricaceae) may be attributed to in- 
trasexual competition among staminate plants 


and mate Бур р 5, respec у. 
Other explanations mainly associated with dif- 


detailed in Lloyd and Webb (1977). 


284 ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL. 71 
100 жш; gogo m i б SD Ф 
ње AS а E нај 8 ro SU 
GAP о ден ce CMM ts Fae GO 45 ^ ay Ab 
90 о Q 
aog A A, Ak OO Q оО д А А RS 
^ O o о ^ a о о o? oO: H ^ a a 
A 0 MN поља неон А aA % 
во 48 од оо Ф®а A^ 2} 
О 4 0 оо, о о oo [e] » A of 
ог фр GP Фор. 9 Ch ee O ШШ 
[e] оо С) O o оф А a* о 
= е SIKO о o9 
70 QUAE 4ھ‎ 
um 9 de 


h 
a, 4 Чо А ар 
104 МАО А 4 А a о 
O 
^, ل‎ ia apat асо o © 
А I. ~ 57 осу Q5 
T I e © ^ 
0 IO 20 30 40 50 60 70 80 90 19 
meters 


FIGURE 3. Distribution of staminate and pi 
New B 


block of spruce-fir forest in cent ew Brun 


tillate flowering ramets of Aralia nudicaulis within ао 
swick during t f 1979. Open circles 


he summer о are stam 


ramets (N = 1,244), solid triangles are pistillate ramets (N = 449). After Barrett and Thomson (1982). 


The flowering patterns in A. nudicaulis may 
not reflect genetic differences between the sexes 
in flowering time. The observed differences may 
result from the non-random distribution of flow- 
ering ramets of the sexes in the habitats sampled. 
Flowering in shaded areas tended to be delayed 
by several days relative to exposed sites. Ex- 
amination of the spatial distribution of flowering 
ramets indicated that females were less likely to 
flower in shaded sites in comparison with males 
(Barrett & Thomson, 1982 and see below). In 
our forest transects it seems likely that the de- 
layed flowering of staminate ramets may have 


ative propo 


resulted from differences in the rel 
ramets 


tions of staminate and pistillate flowerIn 7. " 
in shaded areas. It is also possible that eo 
our efforts to avoid over-representation of iod 
clones in our samples through the use of is 
transects, genetic differences between до 
flowering time, unrelated to sex, тау have = 
involved. These problems in the inte 
of field data on flowering behavior 1n ^ onam 
caulis highlight the difficulties of evolu" 
interpretation of variation patterns in large + 
al plants where single genets may оссирУ е5 
saic of environments. They also draw 


attentio® | 


| 


1984] 


to the likelihood of interaction between spatial 
and temporal influences on reproductive behav- 
ior. 


SPATIAL PATTERNS 


The spatial relationships of flowering ramets 
were examined in a one hectare square block of 
spruce-fir forest during the summer of 1979 (for 
details see Barrett & Thomson, 1982). The dis- 
tribution of all 1,743 flowering ramets is illus- 
trated in Figure 3. It is tempting to suggest, based 
on visual inspection of the map, that several large 
clones of A. nudicaulis occupy most of the space 
within the forest block. A greater diversity of 
genetic markers than sex alone would, however, 
be required to distinguish individual clones. 
Electrophoretic studies, of the kind undertaken 
by Silander (1979) on Spartina patens would be 
valuable for examining the clonal structure of A. 
nudicaulis populations. Notwithstanding the dif- 
ficulties of establishing the genetic aspects of 
Population structure in the forest block, several 
valuable insights into the flowering behavior of 
A. nudicaulis were obtained. 

By dividing the forest block into 100 10 m? 
by 10 m? plots, it was possible to examine as- 
Sociations between flowering ramets of the sexes 
at Various spatial scales as well as with various 
environmental conditions. Throughout the block, 
as well as in other forest sites in New Brunswick 
(Barrett & Helenurm, 1981) and Massachusetts 
(Bawa et al., 1982), staminate flowering ramets 
outnumber pistillate. Flowering ramets of both 
sexes occurred more frequently in plots under an 
Me лору. However, there was a reduced like- 

ihood of pistillate flowering in heavy shade in 
comparison with staminate ramets (Fig. 4). This 
тау be associated with differences in the cost of 
aa in the sexes. Studies of resource 
= on in A. nudicaulis indicate that repro- 
uctive effort in pistillate ramets is considerably 


higher than in androecious ramets, and that the 


ан pensity, particularly in forest sites (Bar- 
we 1 98 1). Evidence to support this 
бош 1S was obtained by Bawa et al. (1982) 

ап examination of the flowering histories 


= еи bear а series of scars left by the 
Nee oliage leaf as well as by the inflorescence 
sible te where flowering occurs. Hence it is pos- 

reconstruct the past history of flowering 


BARRETT—DICLINOUS ARALIA 


285 


OBSERVED DENSITY 
EXPECTED DENSITY 
о 
а 

40" 


nue 


Ss t | | 1 1 


І 2 3 
CANOPY CLOSURE INDEX 
FIGURE 4. Density response of staminate and pis- 


tillate flowering ramets of Aralia nudicaulis to canopy 
closure. Closure index: 0 = most open canopy, 4 = most 


stronger than the male respon 18.61, 
df = 4, P < 0.001). After Barrett and Thomson (1982). 


of a ramet by careful dissection of individual 
shoots. Bawa et al. (1982) found that staminate 
ramets were more likely to flower in consecutive 
years in comparison with pistillate ramets. In 
addition they also found no differences between 
the sexes in the recruitment or mortality patterns 
of ramets from field observations over a three 
year period. Thus it seems likely that the male- 
biased sex ratio of flowering ramets in A. nudi- 
caulis is largely the result of sex specific differ- 
ences in reproductive costs. 


FECUNDITY IN ARALIA NUDICAULIS 


Inspection of Figure 3 indicates that consid- 
erable variation exists in the distance separating 
flowering ramets of the sexes of A. nudicaulis. 
Intersexual distance could be a potentially im- 
portant influence on reproductive success. Bar- 
rett and Thomson (1982) investigated the rela- 
tionships between the spatial pattern of ramets 
and fecundity within the forest block. Since the 
position of all flowering ramets in the block was 
known, it was possible to examine the relation- 
ships between the fruit set of pistillate ramets 
and the sexual composition of neighboring ra- 
mets at a range of spatial scales. No systematic 
variation in fecundity in relation to position was 
detected. At most of the biologically meaningful 
spatial scales, fecundity was uncorrelated with 
either staminate flowering density, pistillate 


ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 
100 г 
1978 
bio m 1979 
جح‎ 
5 50 i- 1978 
1978 
* 1978 
~ 
TE 
25 F 1979 
1979 
я 1978 | | 1979 1979 
SS eas 
Aralia Cornus Maianthemum Medeola Trientalis 
nudicaulis canadensis canadense virginiana borealis 
FIGURE 5. Natural levels of percentage fruit set in five entomophilous, clonal herbs from spruce-fir fores о 
in central New Brunswick during summer 1978 and 1979. Sample sizes (flowers) for 1978 and 1979 are: Ara 


_— - 827, 20,078; Cornus canadensis 965, 
a 6 


5,069; Maianthemum canadense 101, 4,040; Medeola virgin 
bl. data). 


3, 320; Trientalis borealis 69, 16. Barrett and Helenurm (unpub 


flowering density or the local sex ratio of ramets. 
Barrett and Thomson (1982) suggested that the 
relatively long flight distance of bumble bees vis- 
iting the population, pollen carry over, and the 
predominance of staminate flowers at the site, 
all interact to reduce spatial effects on fecundity. 
Presumably at very low flowering densities iso- 
lation distances would be a more important in- 
fluence on fecundity. 

The fruit set of A. nudicaulis at the forest site 
averaged 68%, with the modal fecundity class 
90-100%. This level was considerably higher than 
several other insect pollinated self-incompatible 
herbaceous species co-occuring with A. nudicau- 
lis in this area. These species (Cornus canadensis, 
Medeola virginiana, Maianthemum canadense, 
and Trientalis borealis) share several common 
features with A. nudicaulis. All species are long- 
lived clonal perennials, three of the four (C. can- 
adensis, M. canadense, and T. borealis) flower at 
the same fime as A. nudicaulis, have юасы 


1 


SHMA ollinator 
Fi (Barrett & Helenurm, unpubl. pee Of 
the five species only T. borealis does not possess 
fleshy fruits. The levels of fruit and seed set in 
А. nudicaulis were higher than the remaining 
species in км two years in which data were ге- 
corded (Fig. 
These ари although based on a small num- 


ber of species, are in accord with predictions p 
by Bawa and Opler (1975) in their consideratio 
of the pollination biology of zoophilous dioe- 


cious and self-incompatible plants. They argue 


ble 
success than would occur in a self-incompati 
breeding system. Their arguments involve : 
likelihood of increased pollination efficiency 


Шеп _ 
dioecious taxa as a result of the absence of ‘ponch | 


clogging’ of incompatible stigmas (Shore & Bar- 


rett, 1984) as well as the increased 
movement of pollinators visiting 
species owing to greater variation in 


port inae suggestions is limited, Bawa an а 
(1975) did report that the fruit set of bees 
species was generally higher than in ii 
patible taxa in a tropical deciduous forest? 2 
ta Rica. A similar pattern was obse he n 4 
pata and Kalin Arroyo (1978) in а SU" i 
breeding systems and reproductive опао f 
secondary deciduous forest in Venezu zuela. ^ 
comparisons of fecundity in co-occuring € 
cious and self-incompatible species are req f 
before generalizations can be made. Howev * | 
a clear pattern emerges. it may result A ee 


unre О 
acting on inflorescences of plants with the 


the пак у 


— чеш = LLL 


inter-plamt | 
dioecious 
floral f | 


Sn OP | 


| 
| 
| 
| 
| 


| 


| 


| 


1984] 


breeding systems. High flower/fruit ratios in out- 
crossing hermaphrodites may result from selec- 
tion for increased inflorescence size to enhance 
pollen donation and male success (Willson 
Rathcke, 1974; Willson & Price, 1977). Clearly 
these selective forces cannot occur in seed bear- 
ing individuals of a dioecious species. Accord- 
ingly low fruit set levels in self-incompatible 
plants, in comparison with есіте Species, may 
result from tnum- 
ber of hermaphrodite flowers which function 
solely as males in self-incompatible plants (see 
Sutherland & Delph, 1984) 


CONCLUSIONS 


Ош Studies of the reproductive behavior of 
diclinous Aralia species document spatial and 
temporal variation in sexual function and enable 
some evaluation of the ecological consequences 
of sexual dimorphism. They give only limited 
clues, however, to the potential selective forces 
that maintain flowering patterns. The longevity 
and size of many d 
examination of the genetic dimension so vital to 
evolutionary interpretations. As a result we are 
огсед to assume that the phenotypic variation 
in fitness components related to sexual perfor- 
mance that we measure in the field has a genetic 
basis. Most of the literature documenting genetic 
effects on sexuality in higher plants involves ag- 
ricultural and horticultural crops. Many exam- 
ples ofgenes with large effects (e.g., male sterility) 
are reported, but there is less information on the 
MEX of sex expression and allocation patterns 
idi € and female reproductive function. The 

ailable data (reviewed in Charnov, 1982) sug- 
а. genetic variance for sex differential fer- 
= a within plant populations does oc- 
нове Oss, 1982; Ross & Gregorius, 1983). 
many pla аң Suspects that the high plasticity of 
ing ga ма Exc , particularly those involv- 
mé я ower number, as well as environ- 
i ©; сн will complicate attempts 
"es LÀ major fitness components. How much 
"E Tved variance in reproductive perfor- 
in diclinous plant populations can be as- 


si 
ned to genetic causes is a major unresolved 
Question. 


LITERATURE CITED 


BAR 
ratios a C. H. & K. HELENURM. 1981. Floral sex 
and life history in Aralia nudicaulis (Ara- 
laceae), b v ation 35: 752-762. 
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230. 


EVOLUTION OF DIOECY IN SAURAUIA 
(DILLENIACEA E)! 


W. A. HABER? AND K. S. BAWA? 


ABSTRACT 


Saurauia veraguensis in Costa Rica is morphologically tecla pud band functionally dioecious. 


e flowers i is tricolporate, 


probably plays a role in pollination by serving as a reward, but it does not germinate on the stigmas 


and is therefore non-functional in fertilization. Dioecy in 


although other evolutionary pathways such as via gynodioecy cannot be ruled out. 


Saurauia Willd. (Dilleniaceae) is a large genus 
of small- to medium-sized trees with approxi- 
mately 300 species distributed in tropical Asia 
and America (Willis, 1973). Approximately 65 
species occur in the Western Hemisphere from 
central Mexico to Chile (Hunter, 1966). Taxo- 
nomic treatments of the genus imply that the 
species have perfect flowers (Hunter, 1966). 
However, Soejarto (1969), in a detailed study of 
herbarium specimens, found that several species 
in South America are sexually dimorphic. On 
the basis of pollen fertility and the size of pistils, 
he concluded that at least seven species are dioe- 
cious and one androdioecious. During the course 


of our ongoing studies of the reproductive biol- | 


ogy of tropical forest plants in Costa Rica, we 
Observed two distinct sexual phenotypes in Sau- 
таша veraguensis, a species not studied by Soe- 
jarto. One Phenotype appeared to bear only : sta- 


mina 


a other only 1 
Owers, indicating the occurrence of sndrodioe- 
су. use androdioecy is presumed to 


tremely rare among angiosperms CR tenon 
аи, 1978; Bawa, 1980) we inves- 
ко € reproductive biology of S. veraguen- 

еге we describe the sexual system of S. 


ve 
и and discuss the evolution of dioecy 


STUDY SITE AND PLANTS 


Sa 
up lan veraguensis is a small tree, reaching 
restri m in height. Our field observations were 
cted to two populations; one was on the 


Pacific face of the Cordillera de Tilarán in the 
Monteverde cloud forest and the other on the 
Atlantic slopes ofthe Volcan Poás, both in north- 
west Costa Rica at an elevation of 1,500 to 1,600 
m. Holdridge et al. (1971) characterized the 
vegetation of these areas as Lower Montane Moist 
Forest-Wet Forest Transition. Voucher speci- 
mens of the species investigated (Bawa 3001 and 
3002) have been deposited in the herbarium of 
the California Academy of Sciences (CAS), San 
Francisco. 


FLOWER MORPHOLOGY AND 
POLLINATION BIOLOGY 


4 +1 


The infl illary and thyrsiform. 
The average number of flowers in staminate in- 
florescences (34) is significantly greater than in 
‘hermaphrodite’ inflorescences (18) ( = 4.1, P < 
0.01; five inflorescences from each of five trees 
of each sex). Flowers in both flower morphs are 
up to 30 mm across. In both types of flowers, 
the petals are white, there are numerous (38—47) 
stamens, and a 5-locular ovary with five styles. 
In ‘hermaphroditic’ flowers, the styles (7 mm) 
extend well above the stamens, in contrast to 
staminate flowers in which styles are short (0.9— 
1.1 mm) and always obscured by the stamens 
(Fig. la—b). 

The flowers are pollinated by medium-sized 
bees (especially Melipona, Meliponinae) that col- 
lect pollen from the stamens. Neither flower 
morph secretes nectar. 


1 
_ Supported in part by NSF grants DEB 75-21018 and DEB 77-25558. We thank Mary Smith for the SEM 


T ment of Entomological Scie 


. Anderson, C. T. Philbrick, and David Lloyd for many valuable suggestions for im- 


script, and ас Keller for confirming the identification of species. 
ces, University of California, Berkeley, California 94720. 


ent of Biology, арыну! of Massachusetts, Boston, Massachusetts 02125. 


ANN, 
Missouri Вот. Garp. 71: 289-293. 1984. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


1984] 


DIMORPHIC POLLEN AND SEED SET 


We found significant differences between the 
pollen of staminate and the apparently ‘her- 
maphroditic’ flowers (Fig. 1с—е). First, the pollen 
of staminate flowers is about two to three times 
smaller than that of the ‘hermaphroditic’ flowers. 
Second, the pollen of the staminate flowers is 
tricolporate, whereas pollen from ‘hermaphro- 
dite’ flowers is inaperturate. Both types of pollen 
from fresh flowers stained well with lactophenol, 
but an SEM examination of pollen from herbar- 
ium specimens showed that of ‘hermaphroditic’ 
flowers to be collapsed (Fig. 1d). Furthermore, 
crossing experiments using the pollen of ‘her- 
maphroditic" flowers, and an examination of 
stigmas of open-pollinated *hermaphroditic' 
flowers [utilizing Martin's (1959) technique] 
showed that this inaperturate pollen generally 
does not germinate (Fig. 1e); out of the several 
hundred pollen grains examined on the stigmas 
of more than 20 flowers, tubes were observed 
from only five pollen grains and these tubes were 
very sh 

Observations of more than 40 trees each of 
androecious and apparently ‘hermaphroditic’ 


trees revealed that staminate flowers do not pro- 
duce fruits. 


DISCUSSION 


Clearly plants with staminate flowers transmit 

i мј p via pollen and those with morpho- 
cd hermaphrodite’ flowers function only 
4 Parents. Thus, Saurauia veraguensis is 
ao. This is not the first dioecious species 
i -fy the genus. Recall, Soejarto (1969) de- 
seven dioecious and one androdioecious 


tility on stylar dimorphism and pollen fer- 
as determined by stainability. Soejarto re- 
d differences in the size of pollen grains 
um by the androecious (or hermaphrodit- 
Nai D plants. In the dioecious species, 
аи t long style flowers have empty pol- 
Brains, but in the androdioecious species such 
contained up to 8096 stainable pollen. It 


HABER & BAWA —DIOECY IN SAURAUIA 


291 


is possible that in the androdioecious species he 
studied the pollen grains borne by the hermaph- 
roditic plants do not germinate. We also found 
that pollen grains of gynoecious 5. veraguensis 
plants stain well; only their failure to germinate 
in crossability studies established their sterility. 
Nevertheless, reports of putative androdioecy in 
the genus are interesting and of considerable val- 
ue in ultimately determining the evolutionary 
pathway to dioecy. 

Hooker (1841), in his *Icones Plantarum," first 
suggested the possibility of dioecy in the genus. 
In reference to Sauruja pedunculata (= Saurauia 
pedunculata) Hooker commented: “The flowers 
which I examined appeared to be all male, having 
small abortive pistil, and very short, erect styles." 
Soejarto (1969) also referred to several earlier 
suggestions of dioecy in the genus. However, in 
the most recent revision of the genus, Hunter 
(1966) dismissed the possiblity of unisexuality 
despite the fact that he noted both pollen and 
stylar dimorphism. For example, Hunter stated: 
“Fifteen of the specimens examined had tricol- 
porate pollen with no discernible surface orna- 
mentation. Five ofthe specimens had much larg- 
er grains which were irregularly roughened. The 
irregularly roughened tt ically 
significant, however, since two of the species in 
which they occur are also among the 15 speci- 
mens with tricolporate pollen .... These irreg- 
ularly roughened cells may represent a devel- 
opmental phase of the pollen, possibly the pollen 
mother cells, or they may be the final phase of 
an abortive pollen. Some species frequently have 
flowers in which the pistils are aborted. Such 
flowers have been interpreted as unisexual, but 
this condition may be merely a matter of mat- 

ration. 

Elsewhere in the family, 7etracera has been 
described as androdioecious (Kubitzki & Ba- 
retta, 1969), but there is no empirical evidence 
for the transmission of genes via pollen by plants 
with hermaphrodite flowers. In fact, the andro- 
dioecy pathway to dioecy has not been fully doc- 
umented for any species. Definite evidence for 
the existence of androdioecy has been presented 


flowers. a-c. Saurauia veraguensis.—a. ‘Hermaphrodite’ or functionally pistillate flowers.—b. Staminate 
both х %. с. Pollen from а staminate flower.—d. Pollen from a pistillate flower; both х 1,100.—e. Part 


“з and the pollen tubes from the smaller pollen of staminate flowers, х 500. 


292 


so far for only one species: Xerospermum inter- 
medium (Appanah, 1982). Even in this case, 
plants essentially function either as pollen donors 
or pollen recipients. 

The sexual system of Saurauia is very similar 
to that of a dioecious Solanum species (Ander- 
son, 1979) in which the pistillate flowers also 
produce non-germinating inaperturate pollen; 
however the pollen from the two sexes in Sola- 
num does not differ in size, as it does in Saurauia. 
Interestingly, an earlier report based on mor- 
phological criteria alone also referred to the nine 
Australian dioecious species of Solanum as an- 
drodioecious (Symon, 1979). These have sub- 
sequently been determined to be functionally 
dioecious as well (G. J. Anderson & D. E. Symon, 
pers. comm.). The production and dispersal of 
inviable pollen by pistillate flowers has also been 

reported in the dioecious Actinidia chinensis of 
the Actinidiaceae (Schmid, 1978). 

The evolutionary pathway to dioecy in Sau- 
rauia is uncertain. The vast majority of species 
in the Dilleniaceae are described as having per- 
fect (bisexual) flowers, and dioecy is not partic- 
ularly common in the order. Five evolutionary 
pathways to dioecy have been proposed (Bawa, 
1980; Ross, 1982). Of these, evolution via gy- 
nodioecy or androdioecy is plausible in Sau- 
rauia. The morphological similarity to andro- 
dioecy does not, however, preclude the possiblity 
of evolution to dioecy via gynodioecy, that is, 
the establishment of a male-sterile mutant in the 
population was followed by replacement of her- 
maphrodites by female-sterile mutants. 

The difficulty of androdioecy evolving in a 
population as a result of selective pressure for 
outcrossing is outlined by Lloyd (1975) and 
Charlesworth and Charlesworth (1978). It has 
been argued that in plants that can self-fertilize, 
the pollen of androecious plants is at a disad- 

vantage compared to the pollen of hermaphro- 
dites. This disadvantage disappears in outcross- 
ing populations, but only if the androecious plants 
have a two-fold advantage in fitness via pollen 
over hermaphrodites (Charlesworth & Charles- 
worth, 1978). 

Saurauia veraguensis is pollinated by bees. 
Pollen appears to be the only food reward offered 
to the pollinators, and this is probably one of the 
reasons why gynoecious individuals have re- 
tained the capacity to bear pollen, which of course 
does not germinate but is important in pollinator 
reward, as in Solanum (Anderson, 1979) and 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


Actinidia (Schmid, 1978). The pollen produced 
by машине flowers is much smaller than that 
, and staminate i 
also bear more flowers than the pistillate inflo- 
rescences. Although we have no data on 
quantity of pollen produced by staminate and 
pistillate flowers in Saurauia veraguensis, in 
dioecious Solanum the amount of pollen pro- 
uced by androecious plants is twice that of 
gynoecious plants (Anderson, 1979). It is con- 
ceivable that in the putative androdioecious 
ancestors of dioecious species, the androecious 
phenotypes might have become established be- 
cause of their greater pollen production resulting 
from pollinat tor 
1980; Bawa & Beach, 1981; Beach, 1981; see also 
Ross, 1982). Thus in such cases it may be un- 
necessary to invoke outcrossing as a selective 
force in the evolution of androdioecy. 
Ultimately, the more than 300 species of Sau- 

rauia may hold the key to understanding the evo- 
lution of dioecy via androdioecy. A comparative 
study of the sexual systems should help in eval- 
uating the importance of androdioecy and gy- 
nodioecy in the evolution of dioecy. The possible 
evolutionary pathway of androdioecy to o 
in Saurauia and Solanum offers a more ге 
ing avenue of study than many other sexual 
dimorphic genera. 


о 
ж 


LITERATURE CITED 

ANDERSON, G. J 
of herm 
converg 
md S. 
rospermum intermedium 

rain err t. Biol. 


CH. 


and the eve 

no aturalist т“ 572-97. 
CHARLESWORTH, В. & D. PR : 
model for the evolution of wes and gyn 


HOLDRIDGE, LR. WG. GREN 
. LIANG & J. A. Точ, ЈЕ. 
ronments of Tropical Life Zones. Pergam 
New York. 1-34. 
HOOKER, J. D. 1841. Icones Plantarum 4: aa cent 
Hunter, G. 1966. Revision of Mexican 
American Saurauia (Dilleniaceae). Ann. Mi 
Bot. Gard. 53: 47-89. 
Kusirzki, K. & Р. BARETTA. 1969. гое dinar 
und Androdiozie bei Tetracera (ОШепіасеае 
паара 56: 219-220. 


9. e зоа species 


e of broad _ 


1980. a. Linn of eT ne | 


anette 


, 


1984] 


LLovp, D. G. 1975. The maintenance of gynodioecy 
androdioecy in angiosperms. Genetica 45: 325- 


MARTIN, F. W. 1959. Staining and observing pollen 
tubes in the style by means of fluorescence. Stain 
Technol. 34: 125-128. 
OSS, M. D. 1982. Five evolutionary pathways to 
318. 


ive anatomy of Actinidia 
chinensis ge or Bot. Jahrb. Syst. 100: 
149-195. 


HABER & BAWA —DIOECY IN SAURAUIA 


293 


SoEjARTO, D. D. 1969. Aspects e reproduction in 
Saurauia. A hi cea Arbor. 50: 193. 

Symon, D. E. 1979. Sex forms in ш. (Solana- 
ceae) and d role of pollen collecting insects. Pp. 
385-397 in J. G. Hawker, . Lester & A. 
Skelding (editors), The Biology and Taxonomy of 
the Solanaceae. Academic Press, New York. 

WILLIs; J. C. Ў 
Plants and Ferns. (Revised by Н. К 
Edition 8. Cambridge Univ. Press, Cambridge. 


THE EVOLUTION OF DIOECY —CONCLUDING REMARKS 


K. S. BAwa! 


Since the pioneer work of Darwin on the evo- 
lution of sexual systems in plants (Darwin, 1877a, 
1877b) no sexual strategy in recent years has at- 
tracted h attention as dioecy. First, а пшт- 
ber of population genetic models were developed 
in the 1970s to trace the evolution of dioecy via 
different pathways (Lloyd, 1975, 1976, 1979; 
Ross, 1970, 1978, 1980, 1982; Charlesworth & 
Charlesworth, 1978a, 1978b). Almost concur- 
rently, field studies highlighted the ecological 
consequences of dioecy (Bawa & Opler, 1975; 
Lloyd & Webb, 1977; Wallace & Rundel, 1979; 
Meagher, 1980, 1981; Bullock & Bawa, 1981). 
Then a resurgence of interest in the sexual selec- 
tion theory led to a search for new selective pres- 
sures driving the evolution of dioecy (e.g., Will- 
son, 1979). The finding that dioecy is associated 
with certain pollination and seed-dispersal syn- 
dromes further eroded the traditional view that 
outcrossing is the main selective force in the evo- 
lution of dioecy (Bawa & Opler, 1975; Bawa, 
1980a; Givnish, 1980; Beach, 1981; but see 
Thomson & Barrett, 1981; Lloyd, 1982; for a 
balanced review, see Charnov, 1982). Here, I 
briefly consider the major unresolved problems 
in the evolution of dioecy, including some al- 
ready discussed at length by the contributors to 
this symposium. 

First, a fundamental problem concerns the ex- 
tent to which sex expression in dioecious species 
is constant. Freeman et al. (this symposium) doc- 
ument in detail substantial sex reversals in Atri- 
plex canescens. On the other extreme the dioe- 
cious lily, Chamaelirium luteum, studied by 

| 2 Vawhrhite n 


ymp ) exhibits no change in 
sex expression. Furthermore, the two sexes in C. 
luteum show remarkable ecological divergence. 
Sexual dimorphism in many other dioecious 
pecies is also р d (Lloyd & Webb, 1977; 
Bawa, 1980b; Bawa etal., 1982; Bullock & Bawa, 
1981; Bullock, 1982; Bullock et al., 1983). If in- 
deed there i constancy in sex expression, then 
we need models to explain how sex-linked di- 
vergence in morphological, behavioral, physio- 
logical, and biochemical traits might have 
evolved. Freeman et al. (1980, this symposium) 


mention many other species that presumably 
change sex, but as pointed out by Lloyd and 
Bawa (1984), patterns of gender modification in 
plants are varied and complex. In order to un- 
derstand the origin of these complex patterns and 
their adaptive significance, it is necessary to dis- 
tinguish, for example, extremes such as “sex 
choosers” (e.g., Arisaema triphyllum) and “sex 
adjustors” (e.g., many dioecious species, see Lloyd 
& Bawa, 1984). Only a precise quantitative de- 
scription of gender may allow the resolution of 
various patterns of gender modification. For 
many species that are assumed to change Sex, 
such information is simply not available (Lloyd 
& Bawa, 1984). 

Second, the study of evolutionary pathways to 
dioecism remains an area of major importance. 
Dioecism has been presumed to have evolved 
via five distinct routes directly from hermaph- 
roditism and via androdioecy, gynodioecy, MOn- 
oecy, and heterostyly (Bawa, 1980a; Ross, 1982). 
It is not known if the ecological pressures favor- 
ing the evolution of dioecy are the same in €4€ 
pathway. However, the population genetic models 
for almost all pathway lective pressure 
against inbreeding as the major driving force 
(Lloyd, 1982; Ross, 1982 and references therein). 
Field studies for specific taxa are badly needed 
to test the models. Another major problem m 
the understanding of evolutionary pathways 5 
the uncertainty about the frequency with whic 
dioecy has evolved directly from hermaphrodit- 
ism or via androdioecy. In fact, the evolution 
and occurrence of androdioecy itself has been 
questioned (Charlesworth & Charlesworth. 
1978a, 1978b, pers. comm.; and see Haber 
Bawa, this symposium). Systems such as those 
in Actinidia chinensis (Schmid, 1978), $ашаша 
spp. (Haber & Bawa, this symposium) and Sola- 
num spp. (Anderson, 1979) may prove to be use 
ful in the search for general models for the evo 
lution of dioecism via androdioecy. E 

Third, the importance of selection agains! = 
breeding depression (see e.g., Willson, pK 
Bawa, 1980a, 1982a; Givnish, 1980, 198^ 
Thomson & Barrett, 1981; Beach, 1981; Char 


' Department of Biology, University of Massachusetts, Boston, Massachusetts 02125. 


ANN. MISSOURI Вот. GARD. 71: 294-296. 1984. 


eat сш» 


—— 


a 


1984] 


nov, 1982; Lloyd, 1982) is, perhaps, the most 
outstanding of the unresolved issues in the evo- 
lution of dioecy because its resolution has the 
potential to fundamentally alter our overall view 
of the evoluti у in plants (Will- 
son, 1979; Bawa & Beach, 1981). 

Fourth, explanations for the recently discov- 
ered “ecological correlates” of dioecy (Bawa & 
Opler, 1975; Bawa, 1980a; Givnish, 1980) need 
to be empirically examined. Divergent opinions 
have been expressed to account for the associa- 
поп between dioecy and pollination by small 
bees or generalist insects and that between dioecy 
and fleshy fruits (Bawa & Opler, 1975; Bawa, 
1980a; Beach, 1981; Givnish, 1980, 1982; Char- 
nov, 1982; Lloyd, 1982; see also Bawa, 1982b; 
Herrera, 1982). In particular, for species polli- 
nated by small bees or generalist insects, we need 
to know a) if an increase in male reproductive 


fruit crops results in a disproportionate gain in 
npe 1 і disp ( , 1980a, 
1982; Givnish, 1980; Charnov, 1982; Herrera, 
1982; Lloyd, 1982). 
a ба the origin and evolution of sexual di- 
bi 1 m ene morphological, physiological, 
Ochemical, genetical, and ecological differences 
Modes sexes—is virtually an unexplored area 
8,04 & Webb, 1977; Wallace & Rundel, 1979; 
a Ub; Meagher, 1980, 1981, 1982, this 
1982b. Bay Meagher & Antonovics, 1982a, 
Bullock ullock, 1982; Bullock & Bawa, 1981; 
us et al., 1983). As Meagher points out in 
is Stir above, the study of sexual dimorphism 
telectio in providing insights into the type of 
оси п Lan results in divergence as well as the 
The d петоро of such divergence. 
iod fis erences їп resource allocation for var- 
mains Ctions in different sexual morphs re- 
: à particularly interesting problem, espe- 


that thes mutants and the hermaphrodites 
obvious Im eventually replace. Although it is 
M hat the mutants, by the “ау of com- 
Mt (Darwin, 18772), should allocate more 
herman to male or female functions than the 

Phrodites, we do not know the extent to 


BAWA —DIOECY —CONCLUDING REMARKS 


295 


which these differences are present when the mu- 
tant arises versus the extent to which the differ- 
ences develop during the evolution of dioecy. 
Note that if, as argued by Lloyd (1982), the initia 

differences are not large, sudden gains in male 
and female reproductive success of the mutants 
may not be possible. Such gains would be es- 
pecially difficult to make in the absence of in- 
breeding depression in the original population of 
hermaphrodites, a phenomenon required in Ba- 
wa's (1980a) and Givnish's (1980) hypotheses. 
In this context, comparative data on the repro- 
ductive ecology of various types of male- and 
female-sterile mutants that arise in a population 
are also needed. It is possible, and likely, that of 
the many types of mutants that arise, only a small 
fraction with appropriate reproductive traits be- 
come established to convert a monomorphic 
population into a sexually dimorphic popula- 
tion. 

Ornduff (1983) has recently questioned the 
preoccupation of biologists with rare sexual sys- 
tems such as dioecy. After all, approximately 9096 
of the angiosperms are estimated to be cosexual 
(Lloyd, 1982). But in asking why plants are dioe- 
cious, in many ways we are trying to determine 
why the vast majority of flowering plants are 
cosexual (see e.g., Charnov, 1982; Lloyd, 1982). 


LITERATURE CITED 


ANDERSON, G. J. 1979. Dioecious Solanum species 
of hermaphroditic origin is an example of broad 
convergence. Nature 282: 836-838. 

Bawa, K. S. 1980a. Evolution of dioecy in flowering 
plants. Annual Rev. Ecol. Syst. 11: 15-39. 

. 1980b. Mimicry of male by female flowers 
an petition for pollinators in Ja- 
caratia dolichaula (D. Smith) Woodson (Carica- 

ae). Evolution 34: 467-474. 
1982a. Outcrossing and incidence of dioe- 
cism in island floras. Amer. Naturalist 119: 866— 
871 


fracevwvnia 


— —. 1982b. Seed dispersal and the evolution of 
dioecism in flowering plants— a response to Her- 
rera. Evolution 36: 1322-1325. 

& J. H. BEACH. 1981. Evolution of sexual 
systems in flowering plants. Ann. Missouri Bot. 

Gard. 62: 254-274 

P. A. Opler. 1975. Dioecism in tropical 

forest trees. Evolution 29: 167-179. 

‚ C. R. KEEGAN & К. Н. Voss. 1982. Sexual 

dimorphism in Aralia nudicaulis. L. (Araliaceae). 
Evolution 36: 371-378. 

ВЕАСН, J. H. . Pollinator foraging and the evo- 
lution of dioecy. Amer. Naturalist 118: 572-577. 

BULLOCK, S. Н. 


296 


the annual flowering pattern in Jacaratia doli- 

chaula (D. Smith) Woodson (Caricaceae) in Costa 

Rican rain forest. Ecology 62: 1494-1504. 

, J. Н. BEACH & К. S. ВАМА. 1983. Episodic 
flowering pattern and sexual dimorphism in 
Guarea rhopalocarpa in a Costa Rican rain forest. 
Ecology 64: 851-861. 

CHARLESWORTH, B. & D. CHARLESWORTH. 1978a. A 

model for the evolution of dioecy and gynodioecy. 

Amer. Naturalist 112: 975—997. 

& 8b. Population genetics of par- 
tial male-sterility and the evolution of monoecy 
and dioecy. Heredity 41: 137-153. 

CHARNOV, Е. L Theory of Sex Allocation. 
Princeton Univ. Press, Princeton. 

Darwin, С. Е. 1877a. The Different Forms of Flow- 
ers on Plants of the Same Species. Murray, Lon- 


1877b. The Effects of Cross- and Self-Fertil- 
ization in the Vegetable Kingdom. Murray, Lon- 


FREEMAN, D. C., К. T. HARPER & E. 1. CHARNOV. 

980. Sex change in plants: old and new obser- 

vations and new hypotheses. Oecologia 47: 222- 
232. 


GIvnisH, T. J. 1980. _ Ecological constraints on the 
tion ofb 
cy and dispersal in gymnosperms. Evolution 34: 
959—972 


1982. Outcrossing versus ecological con- 
straints in the evolution of dioecy. Amer. Natu- 
ralist 119: 849-865. 

HERRERA, C. M. 1982. wies systems and dis- 
n related maternal uctive effort o 

outhern рер паса plants. Evolution 
36: 1 
LLOYD, D. G. 


1975. The maintenance of gynodioecy 
giosp Genetica 45: 325— 


1976. The oe of genes via pollen 
and ovules in gynodioecious angiosperms. Theor. 
Populat. Biol. 9: 299- 316. 

1979. Evolution toward dioecy in hetero- 

stylous populations. Pl. Syst. sca 131: 71-80. 
——— 1982. Sele i versus separate 


sexes in seed plants. Amer. Mesa 120: 571- 


585. 
& K. s. ВАМА. 1984. Modification an "- ке 


Biol 


> 


17: 255-338. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


& C. J. WEBB. 1977. Secondary sex characters 
in seed plants. Bot. Rev. (Lancaster) 43: 177-216. 

MEAGHER, T. R. Bu population biology of 
Chamaelirium luteum, a dioecious lily. I. Spatial 
distribution of ا‎ and females. Evolution 34: 
1127-1137. 


981. The population biology of Chamae- 
lirium luteum, a dioeciou 


ily. IV. Two-sex population projections and stable 

population structure. Ecology 63: 1701-1711. 

& J. Амтомом1с5. 1982a. Life history vari- 
ation in dioecious omi sear eet a case study 
of Chamaelirum luteu . 139-154 in Н. Din- 
gle & J. Р. Hegmann cua Evolution and Ge- 
netics of Life Histories. Springer-Verlag, New York. 

1982b. The population biology | of 
CH liy; Vestavia 
family: life history studies. Ecology 63: 1690-1 708 

OnNpurr, R. 1983. Interpretations of sex in higher 
plants. Pp. 21—33 in W. J. Meudt (editor), Strat- 
egies of Plant Reproduction, Beltsville Symposia 
in Agricultural Research (6). Allenheld, Osmun 
Publishers, Granada and London 

Ross, M. D. 1970. Evolution of dioecy from gyno- 

ioecy. Evolution 24: 8 
The evolution of gynodioecy and sub- 
ioecy. Evolution 32: 174- 

. 1980. The evolution and decay of overdom- 
inance during the evolution of gynodioecy, SU ub- 
dioecy and dioecy. Amer. Naturalist 116: 607- 
620. 

————. 1982. Five evolutionary pathways to sub- 
di . Amer. Naturalist 119: 297-318. 

SCHMID, R. 1978. Reproductive anatomy of equ 
chinensis (Actinidiaceae). Bot. Jahrb. Syst. 00: 
149-195. 

Тномѕом, J. D. & S. C. Н. BARRETT. 1981. Selection 
КЕ P inside sexual selection, and the evolution 

lants. Amer. Машан st 118: 443- 


449. 
WALLACE, С. 8. 


& P Did RUNDEL. 1929, Sexual di- 

morphism and resource allocation in male and 

female shrubs af. poni graded Оесо- 
ава 44: 34–39. 


LLSON, М.Е. 1979. Sexual selection in plants. Amer. 
atat 113: 777-790. 


FLORA OF THE VENEZUELAN ОЈАХАМА—1 


JULIAN А. STEYERMARK! 


XYRIDACEAE 
Aratitiyopea Steyerm. & Berry, gen. nov. TYPE: 
Aratitiyopea lopezii (L. B. Smith) Steyerm. 
& Berry. 


Inf 


multiflora doc бакын Flores 


E rimeri pur- 
rpurea fere actinomor- 
phica | gamopetala trilobata, tubo anguste cylindrico, 
] Stamina 3, filamentis 
ш parte suprema tubi corollae insertis. Ovarium 
3-loculare superum. Stylus simplex basi appendicibus 


ti. Herbae perennes, acai valde elongatis sub- 
horizontalibus vel serpent 


Aratitiyopea from Cerro Aratitiyope, Territo- 
rio Federal Amazonas, Venezuela. 


Aratitiyopea lopezii (L. B. Smith) Steyerm. & 
тгу, comb. nov. Navia lopezii L. B. Smith, 
Bot. Mus. Геаћ. 15: 40. 1915; 16: 195. pl. 
28. 1954. Fl. Neotrop. Monogr. 14: 465. fig. 
163: L-M. 1974. type: Brazil. Amazonas: 
Cerro Dimití, upper Rio Negro basin, on 
rocks, 800 m, May 12-19, 1948, Schultes & 
López 9956 (holotype, US-1985318; iso- 
lype, US- 1985319). Figure 1. 


Stem trailing, subhorizontal to ascending at 
the apex, elongated to 2 m, rooting near the base, 
сч foliose, to 2.5 cm thick. Leaves rich green 
aa Sides, densely crowded towards the apex, 

duous lower down, many ranked, spreading- 
ic those immediately subtending the in- 
py та ligulate-lanceolate, 10-14 cm by 2.5- 
x woe lower down more elongated, 21-23 
ries Y 3.5-4 cm, firmly membranous, abruptly 

minate, entire; leaf sheaths lustrous, brown 
Inflorescence sessile, epe- 
dunculate, broadly hemispheric, capitate, ter- 
ney multiflorous, 10-12 cm diam., T cm 
ple, chartace ddish 

i ous- -scarious, wine-red or reddish 
Purple, lanceolate, acute, 3.2-3.3 cm by 0.6-1.1 


cm, the outermost ones ovate-lanceolate, sub- 
acute, 2.2 cm by 1.1-1.2 cm. Bracts subtending 
flower similar in size to those subtending inflo- 
rescence. Sepals pale lilac, chartaceous-scarious, 
free to the base, linear-lanceolate, attenuate to 
an acute apex, 4.5-5. cm long, 5-12 mm 
wide at base, 5 mm wide upward, two of them 
strongly keeled, the third not keeled. Corolla pur- 
ple, straight or nearly so, actinomorphic or nearly 
so, 7-8.3 cm long, tube narrowly cylindric, 5— 
6.2 cm long, 4-4.5 mm wide; lobes 3, equal, 
straight, linear-ligulate, rounded or broadly ob- 
tuse at apex, 1.5-2.2 cm long, 3-4 mm wide. 
Stamens 3, epipetalous; filaments 8—12 mm long, 
attached 2-7 mm below base of sinus of corolla 
lobes in upper fourth of corolla; anthers golden, 
linear, 5-10 mm long, 1.5-2. m wide, basi- 
fixed, slightly bilobate at base. Stigmas 3, purple, 
suborbicular-ovate, spreading, 3 mm long, 2 mm 
wide, fimbriate-penicillate. Style exserted, lav- 
ender, filiform, 8 cm long, 0.8-1 mm wide, 3- 
angled, provided at the base with 3 fleshy, ligu- 
late-oblong glands 3-4.5 mm by 1.5-2 mm, the 
glands strongly reflexed, touching the apex of the 
ovary, obscurely crenulate at the truncate apex, 
and raised on 3 clavate stipes 3.5 mm by 1 mm 
closely appressed to the stylar base. Ovary pale 


liptic, rounded at each end, or slightly apiculate 
at one end, 1.1 mm long, 0.9-1 mm wide, lon- 
gitudinally 12-14-ridged, alveolate with ca. 15 
transverse ribs. 

Distribution: Territorio Federal Amazonas of 
southwestern Venezuela, northwestern Brazil and 
southeastern Colombia (Vaupés). 


Specimens Сера. VENEZUELA. AMAZONAS: 
and sphagnum-covered crevasse in wet 


Brocchinia thickets at 


mo, 990 
mark, Berry & Delascio 130088 (MO, NY, US, VEN); 


i . ^ 
Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166-0299. 


ANN. MISSOURI Вот. GARD. 71: 297-340. 1984. 


298 ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL. 71 


| 


FIGURE 1. Атаппуореа lopezii. —A. Habit. —B, С. Corolla with ‘Sepals, showing length Mp ie sepals.— 
—E.I —F.Pi 


.On 1С of til, shows 


style, stigmas, stylar appendages at base, and ovary.—G. Cross-section of ovary. —H. Natural nci po to 
of stylar appendages at apex of ovary and detail of stigmas.—I. S ppendages elevated, showing relatio 
base of style and ovary.— J. Seed, lateral view. — К. Seed, end ы 


мкл Ol CO 


"m a ————— 


1984] 


locally frequent in scrub forest on granitic dome on 
right bank of river, Río Siapa, just below Raudal Gal- 
lineta (about 110 river km from mouth), 600-700 m, 
21 July 1959, Wurdack & Adderley 43564 (NY, US, 
VEN); lower N escarpment, hanging on wet cliffs, Cerro 
Sipapo, 1,300 m, 27 Nov. 1948, Maguire & Politi 29497 
(NY, US, VEN); Cerro Sipapo, 1,500 m, 17 Dec. 1948, 
Maguire & Politi 27742 (NY, US); 10 Jan. 1949, Ma- 


pa, Río Siapa, 10*30'N, 65°51’W, 1,510 m, 5 Dec. 
А Dunsterville & Dunsterville s.n. (US, VEN, photo 
S). 


Aratitiyopea lopezii var. colombiana (L. B. Smith) 
Steyerm. & Berry, comb. nov. Navia lopezii 
var. colombiana L. B. Smith, Bot. Mus. Leafl. 
e 195. 1954. Fl. Neotrop. Monogr. 14: 465. 

74. 


Distribution: Vaupés of southeastern Colom- 


Specimens examined. COLOMBIA. УАОРЁЅ: Cerro 
Isibukuri, Río Kananari, 4 Aug. 1951, Schultes & Ca- 
бега 1 3342 (holotype, US; isotype, COL, GH); Cerro 
p ukuri, Río Kananari, 4 Aug. 1951, Schultes & Ca- 

rera 13393 (US); 23-25 June 1952, Schultes & Ca- 
brera 15078 (COL, US). 


When Dr. Lyman B. Smith (in Schultes, 1951: 
40) originally published the description of this 
outstandingly beautiful plant, he wrote Dr. 
Schultes that “This species has flowers more than 
twice the size of any previously known Navia, 
and the rose-purplish color of the petals appears 
to be unique in the genus.” 

Unfortunately, when the species was de- 
eae the stamen number was apparently over- 
RU ed, since only three, rather than six, stamens 

Present in the flowers of Navia lopezii. A 
Navn Comparison of herbarium specimens of 
4 ореги with the newly collected material 

'atitiyopea leaves no doubt but that they are 


Congeneric and conspecific. The sessile large heads 
with rose- 


* Presence of three prominent, reflexed, fleshy 
Niele. a at the base of the style, 
nation us three stamens, the same combi- 
tiis: c aracters duplicated in Orectanthe, a 

Th T of the Xyridaceae. 
кы омыр of the genus Aratitiyopea is 
озеју shown with the genus Orectanthe, 


STEYERMARK — VENEZUELAN GUAYANA 


299 


in habit approaching the elongated caudex of O. 
ptaritepui 1ratitiyopea radically departs from 
Orectanthe in the completely different seeds, 
which are exalate, alveolate, prominently ridged, 
and symmetrically ovoid-elliptic in Aratitiyopea 
rather than broadly winged, non-alveolate, an 
non-ridged as in Orectanthe, in the equal, linear- 
ligulate lobes of the purple nearly actinomorphic 
corolla, and in the sessile, epedunculate inflo- 
rescence. 

The stylar appendages in both Aratitiyopea and 
Orectanthe are strictly basal, the reflexed apex 
of the glandular appendages touching the apex 
of the ovary, whereas in Abolboda they are ele- 
vated above the ovary. Moreover, the glandular 
portion of the appendage in Aratitiyopea and 
Orectanthe is flattened, plate-like, oblong-ligu- 
late, and much broader than the slender sup- 
porting stipe, whereas in Abolboda the glandular 
portion is very slender, scarcely or not at all 
broader than the filiform, supporting portion and 
does not touch the apex of the ovary. Addition- 
ally, the apex of the ovary in Abolboda is slightly 
split into three triangular or ovate-lanceolate, 
acute, usually indurate lobes, whereas in Arati- 
tiyopea the ovary is entire and ofthe same texture 
throughout. The seeds of Aratitiyopea are sym- 
metrical, whereas those of Abolboda are asym- 
metrical and suboblique, although the two are 
similar in having alveolate, striate surfaces. Al- 
though Maguire (in Maguire et al., 1958: 2-3. 
fig. 1: g, К, 1) described and figured the style of 
Orectanthe as “‘crateriform, . . . undivided” and 

a : ок. А 


РЧР 


ium material provides evidence that the stigma 
is trifid as in Aratitiyopea, which in freshly pre- 
served material definitely shows a trifid or deeply 
three-lobed fimbriate-penicillate stigma. 

Dr. Joan Nowicke, palynologist of the De- 
partment of Botany, National Museum of Nat- 
ural History, Smithsonian Institution, Washing- 
ton, D.C., has studied the pollen of Aratitiyopea 
lopezii, and has kindly supplied the following 
description based upon herbarium specimens 
preserved in 70 percent ethanol, with a double 
stain according to Alexander (1969). “Pollen 
spheroidal, 175—195 ит diam. (exclusive of pro- 
jections), inaperturate, intectate, the wall 9-10 
ит thick, the surface with a very thin layer of 
sparsely distributed granules (pila?) and with 
prominent knob-like projections 6–7 um long. 

Pollen of Aratitiyopea lacks the typically strat- 
ified angiosperm exine that consists of endexine, 


300 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


footlayer, columellae, and tectum. Only two parts 
of the wall absorbed the stain, the knob-like pro- 
jections and a very thin surface layer of sparsely 
distributed granules. This suggests that they have 
similar composition, and being the outermost 
components suggests that both are ektexine. The 
remainder and vast majority of the wall was 
translucent. The most likely interpretation of the 
pollen wall in Aratitiyopea is that reduction of 
the exine has occurred. Judging from the staining 
pattern, the granules and knob-like projections 
are the only remaining components of exine; the 
thick, clear portion of the wall is probably intine. 
Since the exine is so thin, preformed openings 
(apertures) are not necessa 

The staining pattern of Aratitiyopea is similar 
to that reported by Carlquist (1960) for three 
xyridaceous genera, Abolboda, Orectanthe, and 
Achlyphila: an outer portion, the spines and or- 
namentation, which absorbed safranin red, and 
an inner portion which absorbed fast green. The 
pollen of Aratitiyopea is very similar to that of 
theab all large i i 


with an outermost thin granular layer and spines 


validity of the transfer of Navia lopezii from Bro- 
meliaceae to Xyridaceae.” 

Among the characters Maguire used in differ- 
entiating Orectanthe (in Maguire et al., 1958: 2), 
the caulescent habit was given in his table of 
contrasts and comparisons between the known 
genera of Xyridaceae. However, when the two 
known species of Orectanthe are keyed out on 
the following page (in Maguire et al., 1958: 3), 
it is stated that O. sceptrum includes “plants es- 
sentially acaulescent,” as contrasted with 
ptaritepuiana having “plants caulescent.” This 
same inconsistency is repeated in Maguire’s later 
key to the genera of Xyridaceae (in Maguire et 
al., 1960: 12). 

Although Maguire at first believed that taxo- 
nomic evidence supported Erdtmann’s sugges- 
tion that Abolboda and Xyris were not compat- 
ible familially (in Maguire et al., 1958: 1-2, 1960: 
11) and that Abolboda should be referred to a 


e m 
familial, tribus (etc.) in praelectionibus anni 
1937), Maguire later conceded (in Maguire et al., 
1960: 15) that all four genera known at that time 
pertain to a single family, Xyridaceae, and “ти- 
tually exclude them from any other monocoty- 
ledonous family or families.” 

The following key is provided to account for 


the additional genus, Aratitiyopea, of the Хуп- 


daceae 


[Vor. 71 


KEY TO THE GENERA OF XYRIDACEAE 
1. Corolla gamopetalous; stylar appendages usu- 


ally present 


2. Sepals 3; stylar appendages basal, at apex 
of ovary, the reflexed portion ligular-ob- 
long, broader than the supporting stipe, and 
touching the apex of the ovary; apex of the 


broadly winged, not al 


veolate nor ridged 
Orectanthe 


о 


. Corolla lobes equal in size and shape; 
corolla purple; inflorescence sessile; 


seeds exalate, alveolate, ridged .................. 


.. Aratitiyopea 


e the a 


2. и» pad 2 dara: appendages rai 
the style 


apex of the ovary 


Ет not coding ма apex, the reflexed por- 
tion filiform and about equalling width of 
the filiform-supporting ада арех во e 


ovary 3-toothed, undura 


Bede polypetalous; stylar "appena ab- 


xo Rhizomatous caulescent herb; inflores- 
cence open, the flowers pedicellate; se- 
pals not keeled; staminodia lacking ... 


л _. Achlyphila 


~ 


Non-rhizomatous, us 


ually acaulescent 


herb, inflorescence capitate, the flowers 
sessile; 2 lat tare ral sepals keeled; sai 


nodia present |... 


RAPATEACEAE 


Stegolepis maguireana Steyerm., sp. n y 
Venezuela. Bolivar: Chímantá: Mass Ac 


pan-tepui, 


savanna area, NW portion, 1, 25 m, m 
1984, Steyermark, Luteyn & Huber 12 
(holotype, VEN; isotype, NY). 


Herbae perennes, 2-metralis 


plicatis 17 cm by 6 cm enervatis m 


membranaceis; laminis utrinqu 


altae; vaginis condi" 
ibus scarioso- 
ue och friabilibus 


valde 1-nervatis 1.5-2 m longis 2-3 cm latis; pedun- 


- axillari cin non dilatato foliis pus 
re 2-2.5 cm longo 5-6 mm diam.; 
eminere 3.2 n longo 3.5-3.8 cm di 


flora; spiculis ovoideis occultis 
pali 


ifeste “ 


эм lt 


9 mm x 4 mm; 5€ 


8- 
s induratis non reflexis; petalis luteis parvis 


This species differs from 
vipetala Steyerm. and subsp. 


the related S. Pa” 
chimantensis Ma- 


guire in the peduncles prominently longer = 
the leaves, the very brittle narrower leaves ' 
2-3 cm wide, the leaves glaucous on both 


not silvery below with 
vipetala, and in the yellow in 
als. 


stripes as in 5. par 
stead of orange pe 


| 


ДУ vB 


1984] 


Stegolepis t is Stey , SP. NOV. TYPE: 

Venezuela. Amazonas: Cerro Marahuaca, 
cumbre, extremo noreste, 3°50'N, 65?28'W, 
2,580-2,600 m, 30 Mar.-1 Apr. 1983, Stey- 
ermark & Delascio 129197 (holotype, VEN). 
PARATYPE: same locality and date, Fernan- 
dez 66 (VEN). 


Herbae perennes 0.5-1-metralis; vaginis valde con- 
duplicatis 14-15 cm longis apice 2.5-3 cm latis, au- 
riculis prominentibus ligulatis suborbicularibus apice 
rotundatis 1.5-1.8 cm longis 2.5-3.5 cm latis margi- 
nibus scariosis; laminis coriaceis lineari-ligulatis 
apice falcate rotundatis vel obtusis 47-54 cm x 3-3.5 
cm, costa media nervis secundariisque tantum leviter 
manifestis haud ү i ibus; pedunculis 6-7, valde 
costatis 25—55 cm longis 2—3 cm crassis infra spiculam 


petalis 1.5-2 cm longis; antheris linearibus transverse 
rugosis 9-10 mm longis. 


This species is related to S. hitchcockii Ma- 


cately obtuse leaf blades with more strongly 
developed ligulate auricles and obtuse broader 
bracteoles. In its 3-7(rarely 1—)-flowered inflo- 
rescences, it is more closely allied to S. hitch- 
cockii but the latter has shorter anthers and 
broader leaf blades. From S. membranacea it 
may additionally be distinguished by the indu- 
rated, enervate, coriaceous leaf blades which are 
inconspicuously nerved, and in the broader apex 
Pisa peduncle, while from S. pulchella it further 
b TS in the usually greater number of spikelets 
the less conspicuously, coriaceous leaf blades. 

d азаа Maguire (1982: 139) states that the 
ks d es in S. pulchella and S. membranacea 
к Obtusas" or “obtusiusculis,” an ex- 
dii ы of these taxa, as well as S. hitchcockii 
all lance р morichensis, indicates that they are 
ae. E ate or deltoid-lanceolate and narrowed 
ты за = apex, whereas those of S. terra- 
ei ong-lanceolate and much broad- 

Owards an obtuse apex. 

Has focis is named to commemorate the 
on Terramar, under whose auspices the 


Guns 
Pedition to Cerro Marahuaca was adminis- 


NOTE ON SAXOFRIDERICIA SPONGIOSA 
MAGUIRE AND S. DUIDAE MAGUIRE 
In 2 А " 
M his description of the leaf width of S. duidae 
aguire (1982: 94) states “2-3.5 cm de ancho" 


STEYERMARK— VENEZUELAN GUAYANA 


301 


and that of S. spongiosa (Maguire, 1982: 97) as 
“7-10 ст de ancho." Measurements of material 
of S. spongi theless indicate a more lim- 
ited range of variation from 4–8 cm, with some 
specimens only 4–6 cm wide 

The peduncles of S. spongiosa are stated to be 
*abruptamente ensanchados y bulbosos debajo 
de la inflorescencia." Some specimens, such as 
Wurdack & Adderley 4366 are not. The sponge- 
like texture of the sheath is characteristic. 


On the other hand, 5. duidae may exhibit a 
pronounced enlargement below the heads, as in 
S. spongiosa, although in his key Maguire (1982: 
90) states that the peduncles are **ensanchados" 
only “gradualmente debajo de Іа inflorescencia.” 

Although 5. duidae is included under the por- 
tion of the key (Maguire, 1982: 89) which states 
that the heads are “4 cm mas o menos ancho," 
nevertheless the text under P. duidae (Maguire, 
1982: 94) gives greater dimensions of “‘inflores- 
cencia 4.5—5.5 cm de diametro." There is inter- 
gradation in head size between these two taxa. 
Huber 6182, identified as 5. duidae, is S. spon- 
giosa. 


IRIDACEAE 


Trimezia chimantensis Steyerm., sp. ПОУ. TYPE: 
Venezuela. Bolivar: Piar, Macizo de Chi- 
manta, sector centro-noreste del Chimanta 
tepui, cabeceras orientales del Cano Chi- 
manta, 5°18’N, 62°09’W, 2,000 m, 26—29 
Jan. 1983, Steyermark, Huber & Carreño 
12807 1 (holotype, VEN). PARATYPE: Macizo 
de Chimantá: sector SSE, altiplanicie sur- 
oriente del Acopán-tepui, cabeceras del Río 


5*11'N, 62*00'W, 1,920 т, 14-16 Feb. 1984, 
Steyermark, Luteyn & Huber 129864 (VEN). 


T. fosteriana foliis angustioribus 3 mm latis 
utrinque viridibus haud glaucis, petalis minoribus 2 
cm longis, spathae valvis 2.5-3.5 cm longis, antheris 
minoribus 3-3.5 mm longis recedit. 


Cormous herb 0.8-1.2 m tall; leaves rich green 
both sides, narrowly linear, 0.7—0.8 m long, 3 
mm wide; scape 0.7-1.2 m tall, equalling or ex- 
ceeding the leaves, 3 mm wide, 2-3-bracteate; 
bracts linear, the lower ones 16—45 cm long, those 
in the upper third 4—8.5 cm long; spathes lan- 
ceolate, acuminate 2.5-3.5 cm long; perianth 
completely yellow, unspotted, the segments 2cm 


302 


long; anthers 3–3.5 mm long; style 6 mm long, 
branches 4 mm long. 


This species differs from the related T. fosteri- 
ana Steyerm. in the generally narrower, com- 
pletely green, non-glaucous leaves, shorter spathes 
and perianth segments, and smaller anthers. 
Originally described from specimens collected in 
the Gran Sabana of Estado Bolivar, T. fosteriana 
is also now known to occur on the summit of 
Chimantá Massif (Steyermark, Huber & Car- 
rerio 128440 and 128798). 


SARRACENIACEAE 
REALIGNMENT OF THE GENUS HELIAMPHORA 


Introduction. One of the outstanding endem- 
ic genera of the Guayana Highland of Venezuela 
is Heliamphora. Thus far, it is known to be re- 
stricted to the summits of some of the sandstone 
table mountains of the Roraima formation of 
Estado Bolivar and Territorio Federal Amazonas 
of the Venezuelan Guayana and adjacent Sierra 
de Neblina and Pirapicu of northwestern Brazil. 
The genus also descends to the Gran Sabana of 
southeastern Estado Bolivar in Venezuela. 

The original species, H. nutans, was collected 
by Robert Schomburgk from Roraima and de- 
scribed by Bentham in 1841. Asa result of Tate’s 
collections from the summit of Cerro Duida, 
Gleason described three additional species, H. 
macdonaldae, H. tatei, and H. tyleri in 1931. A 
fifth species was added by Gleason (in Gleason 
& Killip, 1939: 164) as a result of collections 
made by Tate and Cardona from the summit of 
Auyan-tepui. Subsequent to his expedition to 
Ptari-tepui in 1944, Steyermark (in Steyermark 
et al., 1951: 239) described a sixth species, H. 
heterodoxa, and presented a key to the known 
species, at that time commenting on the varia- 
tion as demonstrated by H. heterodoxa as well 
as by the H. tatei-tyleri-macdonaldae group. 

A review of the comparative morphology, fo- 
liar trichomes, and glands present on the species 
of Heliamphora known up to 1942 was published 
by F. E. Lloyd (1942: 9-16). His account was 
based partly on previous literature, as well as 
herbarium material and living plants of H. nu- 
tans. A popular article on the mechanism of the 
trap in the species of Heliamphora on Cerro de 
la Neblina appeared in 1973 by Charles Brewer- 
Carías. In 1978, Dr. Bassett Maguire published 
a review of the genus Sarraceniaceae (in Maguire 
et al., 1978: 36-62). In that treatment two new 
species, H. ionasii and H. neblinae, and four new 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


varieties (two in H. heterodoxa and two in H. 
neblinae) were described, while H. tyleri was syn- 
onymized with H. tatei, and H. macdonaldae 
was reduced to a variety of H. tatei. 

Present work. In an attempt to identify nu- 
merous specimens of Heliamphora collected by 
the writer on various expeditions to the Vene- 
zuelan Guayana during the past five years, Ma- 
guire's treatment of the genus was used. Unfor- 
tunately, due to the tremendous variation 
exhibited throughout the genus, it became evi- 
dent that several characters employed in his key 
were inapplicable to distinguish various taxa. | 
has resulted in the present realignment in which 
a re-examination and evaluation has been made 
of various gross morphological characters avail- 
able in differentiating the taxa. а 

Previous observations by Steyermark (in Stey- 
ermark et al., 1951: 240—242) stressed the w 
phological variations which occurred In. Hs 
heterodoxa and within the H. tatei-tyleri- 
macdonaldae group. Attention at that time was 
also called to the variation in pitcher size к 
shape induced by changes in wetter habia 
servations on living plants as well as or 
collections from expeditions made in 1953, 1955, 
and since 1960 to the present have further v 
the writer in his realignment of the p 
examination of the extensive collections 5 8 
liamphora in the Herbario Nacional of Ri 
zuela (VEN), supplemented by duplicate pol 
rial from NY, has been a basis for the follo 
observations and a new key to the taxa. ps. 

Variation within the genus. It should E 
phasized that all the taxa іп Heliamphora an 
a great amount of plasticity, varying 10 gp: a 
extent that scarcely a single character у 2 
foolproof for their differentiation. Size an hs 
of pitchers, their appendages, height of flower 


cauline 
plant, contraction or elongation of the E 
of 


axis, glabrity and length of pedicels, ко 
apex of the lowest floral bract, shape ап relative 
tepals, number of flowers on the E 2 with 
length of the lowest floral bract as compa oie 
length of the lowest pedicel, and eae 
sence of a foliar bract on the scape be hibits 
inflorescence—each of these characters ks сой 
a certain degree of instability and intergra 


generally recognized differences betw 


cod e 
such characters may change under уап 


"па 


1984] 


ronmental conditions. Certain characters, how- 
ever, have been found to be more or less constant 
and applicable, even though exhibiting some 
variation. I refer here to the relative number and 
length of the anthers, the relative total length of 
the upper pubescent zone of the interior surface 
of the pitcher in proportion to the length of the 
pitcher itself, and the density and relative length 
of the hairs of this upper pubescent zone. Each 
of the characters examined will be discussed in 
the following section of this study (see Table 1 
for summary of these characters). 
Androecium. The number of anthers within 
а flower has been found to be generally reliable 
їп Separating the main taxa of the Territorio Fe- 
deral Amazonas from those of the Estado Boli- 
var, the latter varying from usually (4—)8-14(— 
15 or rarely 16), the former from 15-20. The 
taxa of Estado Bolivar include H. minor with 
stamens varying from 10-14, H. heterodoxa var. 
heterodoxa from 8-14 (rarely to 16 in Steyer- 
mark & Wurdack 374 from Chimanta Massif) 
0), Н. het i odoxa var. exappendiculata from 
0 rarely 4 in Cardona 1523 from Chimantá 
Massif (VEN), 10-14 in H. nutans, and 15 (ac- 
cording to Maguire in Maguire et al., 1978: 54) 
in H. ionasii. The taxa of Territorio Federal 
Amazonas, H. tatei and H. neblinae, and their 
variations, possess 15-20 stamens. 
E ength of the anthers varies from 3-8.5 
" a anthers of 3-3.5 mm are found in 
AS à Med ionasii, while larger anthers 
of ei созе ы found in Н. heterodoxa 
с с" : js the H. tatei-H. neblinae 
eu AL ederal Amazonas. How- 
eterodoxa sometimes has anthers only 
while anthers of only 5 mm long 


а 

ог fr 

Len : 

& kou of the upper pubescent interior zone of 
er. In H. nutans and Н. minor the up- 

bescence on the interior surface of 


ermark 103775 [VEN : 
d i. 
ie ]) and may vary in H. mi 


ха, : 
wipes Ming from %43% the entire length, 
5 H. heterodoxa and the taxa of the 


Tricho 
mes of the upper pubescent zone. An 


STEYERMARK — VENEZUELAN GUAYANA 


303 


Em p 
YT 
FEM K у 

UE Mt d 

ТИЛШИ ЛД 


viniviri МА 


У) 
К 


La! tara 
irit 
E43 
13 
UN 


I 


| 
j 
| 
1 
Bits 


| ВАВА 
ОТЕ. 
EARS po Ку МЕГЕ Па (Би | 


ТЕ ОУ ti 
АТИ 


Ficure 2. Interior leaf surface of species of He- 
liamphora, semi-diagrammatic.—A. Heliamphora nu- 
ns.—B. H. heterodoxa—C. H. minor.—D. H. iona 
sii.—E. H. tatei var. tatei.—F. H. tatei var. neblinae. 


examination of the trichomes of the upper pu- 
bescent zone of the pitcher reveals some differ- 
ences which are mainly constant within a given 
taxon (Fig. 2). In H. nutans, H. heterodoxa, and 
in the taxa from Territorio Federal Amazonas, 
the upper pubescent zone consists of a velvety 
mat of minute, densely crowded, retrorse tri- 
chomes mainly 0.2-2 mm long. These minute 
hairs are shortest in the upper half of the zone, 
becoming longer toward the basal part, eventu- 
ally merging with a basal zone of more elongated 
retrorse trichomes. A longer type of trichome 2- 
5 mm long, with the hairs more widely separated 
from one another, prevails in H. ionasii and Н. 
minor, the former having the elongated hairs 
scattered over most of the surface, whereas in 
the latter, the longer hairs are dispersed more 
prominently in the lower portion of the zone, 
with a mixture of longer scattered hairs over a 
dense covering of minute trichomes 0.5 mm or 
shorter in the upper interior sector. Glabrous 


TABLE 1. Summary of characters in the realignment of the genus Heliamphora. 
tatei var. 
minor nutans heterodoxa tatei neblinae ionasii 

Pitcher length (cm) 5-22(-30) 15-29 12-32(-42) 25-50 (12-)1 5-30 40-50 
Pitcher length hairiness 2-8 6-8.5 7-18 9-14 10-15 14.5-19 

(cm) 
Pitcher hairiness ratio 13—38 13—38 № or less to 38 % to nearly У % to nearly У % or more 
Pedicel pubescent densely pubescent sparsely densely more or less 
Pedicel glabr - rarely pubescent rarely pubescent — 
Tepals in anthesis (mm) 21-50 by 7-19 35-45 by 11-16 30-60 by (10-)12— 3 by 7-30 35-60 by 13-35 30-35 

2 

Tepals in fructification 40-53 by 12-20 45-47 by 20 45-80 by 18-37 45-72 by 20-40 70 by 30 55-60 by 15 

(mm) 
Anther length (mm) 3-5 3-3.5 4.5—6(—8.5) -7.5 5-8 2.5 
Lowest bract emer. variable rarely only equal- sometimes only 

lowest ling slightly exceeds 
Lowest Muri oss than — E — — 

lowest pedicel 

Pedicel length (cm) 1.5-10 2-7 2-11(-16) 2-10 1-7.5 8-12 

Height of plant (m) 0.1-0.85 0.3-0.5 0.3-0.9 0.3-2 0.4-1.2 0.85 

Number of flowers to (12-5 4 2-7 2-3 2-3(-4) 8-10 

scape 

Floral bract rounded — – 

Floral bract cuspidate rarely mainly == — Е 

Length of lowest floral 2-6 3–3.5 2-10 6-17 (4.5-)9-21 4-5 

bract (cm) 

Pitcher appendage (mm) 3–15(–20) by 2- 2-7 by 5-12 6-35 by 5-30 10-40 by 5-20 25-40 by 20-42 16-20 by 10-30 
15(-20) as broader than often longer longer than (also 11 by 11 about as broad 
broad as long or long than broad to as broad as broad as long 
broader than broad as long long, also longer 
long (var. exappen- th roa 

E 0.2 by (neblinae f. par- 
va 6-28 by 6- 
20) 
Lowest floral bract bearing x - 
appendage 
Lowest floral bract lacking — — — sometimes sometimes — 
appendage 
Number of anthers 10-14 10-14 (7-)8-14(-16) 15—20 15—20 15 


РО 


N3QG3IVO TVOINV.LOS PHOOSSIN JHL 30 5ТУММУ 


IL лод] 


а Er rub КК eT eee ee 27А РЕГ ху лет, ee 


ИРОД Se ee IEEE MU али rur vmm tc ee ee Г ал ара Le NER авва а ыйын ЫСЫ М АЫ a a me am S eee e 


1984] 


forms are known in H. heterodoxa, H. minor, 
and H. tatei f. macdona 

Pitcher shape and nues The ventricose 
shape of the pitcher has been employed by Ma- 
guire (in Maguire et al., 1978: 50—51) to distin- 
guish the species occurring in the Estado Bolivar 
from those having an “essentially tubular” shape 
found among the taxa of the Territorio Federal 
Amazonas. Unfortunately, the character of the 
shape, while more or less uniform among the 
taxa from the Territorio Federal Amazonas, var- 
ies considerably in Н. heterodoxa, Н. minor, and 
Н. nutans, Changing from | a ventricose to a tu- 
bular type } 1951: 
240) noted previously. that under conditions of 
more abundant moisture and shade, H. hetero- 
doxa had larger and more elongated pitchers 
(Steyermark 59934), and in subsequent collec- 
tions (Steyermark et al. 115698, 115742, Stey- 
ermark & Wurdack 374, 375, Steyermark 
121104) this was noted on collection labels. 

In H. minorthe pitchers, although usually ven- 
tricose, are more elongated and subtubular in 
Steyermark, Huber & Carrefio 128666. Heliam- 


gated tubular pitchers, as shown by Delascio & 
Brewer 4733 from llu-tepui and Delascio & 
Brewer 4967 from Kukenan-tepui. In the Ter- 
ritorio Federal Amazonas the taxa usually have 
the pitchers elongated to as much as 50 cm in 
length, but may be smaller and reduced to 12 cm 
long when they are growing in more desiccated 
or more exposed situations, as exemplified by 
Steyermark 103775 and 103844 from Neblina, 
by Farinas, Velasquez & Medina 279 and 549 
from Duida, and by the type collection (Maguire, 
Wurdack & Bunting 37171) of H. neblinae var. 
Parva Maguire. In his key, Maguire (in Maguire 
et al., 1978: 51) partly differentiated H. ionasii 
from H. heterodoxa on the basis of pitcher length, 
indicating 40-50 cm long for H. ionasii, based 
upon the type collection only, and “30 cm or less 
long" for H. heterodoxa. However, the abundant 
material of H. heterodoxa represented in VEN 
shows a variation of pitcher length from 12 to 
42 cm. 

Elongation of the cauline axis. Some em- 
phasis has been placed by Maguire (in Maguire 
et al., 1978: 50-53) upon the differentiation of 
the taxa from Estado Bolívar having rosette- 
forming pitchers on shortened axes from those 
with pitchers cauline on more elongated axes 2— 
3 dm long. In this manner, H. nutans and H. 
minor are separated from H. heterodoxa and H. 


STEYERMARK — VENEZUELAN GUAYANA 


305 


ionasii. However, no reliability can be placed 
upon this character. Observations ofliving plants 
of H. minor on Chimantá Massif and Auyan- 
tepui furnish evidence of the effect of the envi- 
ronment on habit of growth with reference to the 
elongation of the caudex. Field observations and 
voucher herbarium material indicate that the 
plants growing in desiccated areas exposed to full 
sun, especially during the months of the dry 
season, form rosettes with a shortened axis, 
whereas those plants inhabiting the moister cliff 
faces, where water is dripping or where more 
shade occurs, develop more elongated axes with 
cauline ae as exemplified by the specimen 

of Н. minor (Steyermark, Huber & Carrefio 
128666) bum Chimantá Massif. Some speci- 
mens of H. nutans (Delascio & Brewer 4733) 
from Kukenan-tepui have a pitcher attached 5 
cm above the rosette clump, and in Maguire 
33379 (VEN) the caudex is elongated at least 5 
cm below the leafy rosette. 

Although the cauline axis is more commonly 
elongated in H. heterodoxa, the degree of elon- 
gation varies with the habitat. One can find ro- 
sette-forming plants with a shortened axis in H. 
___- уаг. Aetenadaxa, especially 1 in н open 


E Pe 33890 [VEN], Steyermark & Dun- 
sterville 104240 [VEN]), and in var. exappendic- 
ulata (Steyermark 74888 [VEN] and Steyermark 
& Wurdack 441 [VEN]). 

Height of plant. The height of the plants in 
Heliamphora varies, of course, according to the 
elongation of the cauline axis. There is consid- 
erable variation in this respect among the several 
taxa. Dwarfed plants of H. minor may attain only 
1 dm in height (including the inflorescence), 3 
dm in H. nutans, and 3 dm in H. heterodoxa, 
but H. nutans may reach a height of 5 dm, 
minor may attain 8.5 dm, and H. heterodoxa as 
much as 9 dm 

The taxa (H. tatei and H. neblinae) in Terri- 
torio Federal Amazonas generally attain a rela- 
tively taller height, reaching an average of be- 
tween 1-2 m in Н. tatei, and, on occasion 
(according to Maguire in Maguire et al., 1978: 
56-57) to 4 m. However, in the same colonies of 


Marahuaca (Steyermark et al. 126356). In Stey- 
ermark, Liesner & Brewer-Carías 124564 from 
Cerro Duida, plants of H. tatei are noted to vary 


306 


from 0.5 to 1.5 m in height, and plants of H. 
neblinae from Cerro de la Neblina may vary from 
0.5 to 1.5 m, smaller individuals (Steyermark 
103745) having been referred by Maguire (in 
Maguire et al., 1978: 56-57) to H. neblinae var. 
parva. 

So far as height and elongation of the caudex 
are concerned, there is intergradation between 
populations of plants of H. tatei from Cerro Dui- 
da, Cerro Huachamacari, and Cerro Marahuaca, 
and of H. neblinae from Cerro de la Neblina. 
These two taxa do not reveal any real differences 
in anther length, as stated by Maguire, but do 
exhibit a distinct character in their type of pu- 
bescence occurring on the upper interior surface 
of the pitcher. 

Branching of axis. In his key to Heliamphora 
Maguire (in Maguire et al., 1978: 51) alludes to 
the stems of H. tatei as being *dendroid, much 
branched," as contrasted with “stems not den- 
droid, simple or little branched" in H. neblinae. 
The terminology **dendroid, much branched," 
as employed by Maguire, is in need of clarifi- 
cation and modification. If a "dendroid, much- 
branched" stem leads one to expect a much- 
branched, tree-like habit, certainly there is 
nothing evident from herbarium material or 
photographs to justify this description. There- 
fore, in order to verify, clarify, and re-examine 


RERUM J © + T 

to the summits of Cerro Duida and Cerro Hu- 
achamacari in 1981, 1982, and 1983, where 
thousands of individual plants of H. tatei occur, 
to observe, record, collect, and make detailed 
photographs of the growth habit of this species.” 
As a result of an examination of numerous in- 
dividuals, the following conclusions have been 
drawn: 

The ramification noted by Maguire is subject 
to various interpretations. In many individuals 
there is no indication of branching (Fig. 3) and 
only a simple, solitary stem is seen, as exempli- 
fied by Steyermark 129428-C and D (VEN). In 
other individuals a shortened lateral axis is de- 
veloped which bears an abbreviated rosette or 
leaf cluster. This lateral leaf cluster on a short- 
ened axis may occur along the side of the stem 


. : icopter tri 
2 I am deeply grateful to the Terramar Foundation for their generous support in supplying helicop are het 


the summit of Cerro H 
acknowledged to Walter Smitter who pho 
am also greatly thankful to Dr. Charles B 
Duida. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


(Steyermark 129428-A and E [VEN], ог near or 
at its apex (Steyermark 129428-B [VEN], in the 
latter case producing a bifurcate aspect (Fig. 4). 
This short attachment, usually either one or 
sometimes two, developed part way up the main 
stem or producing a bifurcation when developed 
at or near the apex, provides the basis for Ma- 
guire's use of the term “branched.” However, по 
individuals were found, among the numerous 
ones examined, which could be described as 
*much branched." Many specimens were seen 
with several leafy plants growing from the base 
of the stem, and these basal growths attained 
different lengths of leafy tufts (Fig. 5). Such in- 
dividuals, however, cannot be considered as hav- 
ing a branched stem, but merely as having leafy 
offshoots arising from their base. Moreover, of 
the numerous individual specimens observed, à 
larger proportion exhibited only simple, un- 
branched stems which lack any attached leafy 
rosettes or leafy clusters. 

Thus, the usual growth habit which was ob- 
served on the Heliamphora tatei plants from the 
summits of Cerro Duida and Cerro Huacha- 
macariis that ofa simple, monopodial stem which 
continues to elongate upward, the older dead 
pitchers, which occur along the longitudinal v 
tical axis of the stem, persisting and remaining 
attached to the axis for many years, while the 
new pitchers, which form the green leafy grow" 
appear in the uppermost and apical ado 
the same axis. In some plants a shortened е : 
rosette may be produced, but no elongated lig 
neous **dendroid" branches are present. у 

Ebracteate and bracteate scape. А мн 
used by Maguire in his key (in Maguire et "d 
1978: 50-51) to distinguish the taxa of Territo 


commonly found below the middle 
rescence in the taxa from Territorio ай 
Amazonas, while it is absent among the v 
from Estado Bolívar. Actually, each a 
the inflorescence in H. neblinae and H. ee 
subtended by a leafy bract, but the d i 
is more elongated and more foliose than 

ers. However, in the majority of s 
amined, no other bract occurs below t 


he lowest 


ps 10 


uachamacari, particularly to Armando and Fabian Michelangeli. Speci th il 
tographed the plants of Heliamphora tatei on Cerro 
rewer-Carías, who supplied helicopter support to the sum 


c 
enar of Сето 


pecimens с“ | 


Í 
| 


1984] 


STEYERMARK— VENEZUELAN GUAYANA 


Ficu 
RE 3. Completely unbranched axis of Heliamphora tatei. 


one : 
nis the lowest pedicel. In the ma- 
+ OF Specimens examined, the lowest bract 


Present 
Оп the scape below the inflorescence on 


Some 
“a. laxa from Estado Bolivar, as ex- 
*d in Н. minor by Steyermark et al. 


116001 from Auyan-tepui, Steyermark, Huber 
& Carreño 128269 and 128666 from Chimantá 
Massif, H. heterodoxa var. heterodoxa (Steyer- 
mark & Nilsson 338 and Steyermark 121104) 
and H. nutans (Delascio & Brewer 4967) from 
Ilu-tepui, and may be absent, on the other hand, 
on many specimens from the Territorio Federal 
Amazonas. 

Floral bract. The applicability of the relative 


308 


FIGURE 4. Lateral leaf cluster on stem of Heliam- 
Phora tatei. 


length of the floral bracts as compared with the 
length of the pedicel, as used by Maguire (in 
Maguire et al., 1978: 50-51) is generally useful 
with reference to the lowest floral bract only, but 
an unreliable character for separating the taxa of 
Estado Bolivar from those of Territorio Federal 
Amazonas when applied to the bracts other than 
the lowest one. While the lowest floral bract is 
shorter than the lowest pedicel in H. ionasii, H. 
heterodoxa, and H. nutans, all originating from 
Estado Bolivar, it varies greatly in H. minor, also 
from Estado Bolivar. Thus, in Н. minor the low- 
est bract is found to either exceed the lowest 
pedicel or it may be shorter. This variation may 
depend on the relative age of the plant, since 
longer pedicels are often correlated with the low- 
est flowers which are the first to appear in an- 
thesis, whereas the flowers on the shorter upper 
pedicels come into anthesis at a later Stage of 
flower succession. Moreover, in the taxa from 
the Territorio Federal Amazonas the floral bract, 
on some specimens, may only equal or slightly 
exceed the pedicel. 

This floral bract varies in length from 2-6 cm 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


in H. nutans, H. minor, and H. ionasii, and from 
2-10 cm in H. heterodoxa, whereas in the taxa 
from Territorio Federal Amazonas, variation ex- 
tends in length from (4.5—)6 to 21 cm. In the taxa 
originating from Territorio Federal Amazonas 
the floral bract is usually provided with an ap- 
pendage similar to that of the pitcher, whereas 
this appendage is lacking in the taxa from the 
Estado Bolívar. However, some specimens ofthe 
taxa from Territorio Federal Amazonas may have 
only a cuspidate apex instead of a definite ap- 
pendage. In Н. minor, Н. ionasii, and Н. het- 
erodoxa the apex of the floral bract is rounded 
or cuspidate, although mainly cuspidate in H. 
heterodoxa but rarely so in H. minor. So far as 
specimens examined are examined, it is Cuspl- 
date in Н. nutans. 

Pedicel length and indument. The presence 
or absence of pubescen ce on the pedicel was used 
by Maguire in his key (in Maguire et al., 1978: 
50-51) to differentiate some of the taxa. Within 
certain limits this character appears to have val- 
ue. It is found to be useful in the majority of 
specimens examined, although showing var 
ability. The pedicels are glabrous in H. ionas, 
H. heterodoxa, and H. nutans, but rarely pubes- 
cent in H. heterodoxa (Steyermark & de 
374, 375 [VEN] and Steyermark 74888 M 
and in H. nutans (Delascio & Brewer e 
[VEN]). They are nearly always pubescent ү Д 
minor, and usually so in the taxa from the > 
ritorio Federal Amazonas referred to H. fate! an 
Н. neblinae, but in H. tatei may vary from 3 
bescent to glabrate. In Maguire’s key (in pu 
et al., 1978: 50) the difference in pedicel gla s 
has been inadvertently transposed, and Ec 
actually read “pedicels glabrous" for H. ла d 
and “pedicels pubescent” for Н. minor, 115 
Of vice-versa as given in the key. PE 

The length of the pedicel varies accor iy 
the maturity of the inflorescence, the ness 
maturing earlier than the others, WIS = њи 
in the lowest fruiting pedicel 8 
length. This length varies with the ن‎ 
the maximum of 16 cm recorded for Н. 
doxa, 12 cm for H. ionasii, 10 cm for 


for H. nutans, but minimum leng 
are known in the flowering pedicels of si 
taxa, except for H. ionasii, where 8 cm 
corded 

Number of flowers in an ое сы 7" 
greatest number of flowers on one scape 
recorded for Н. ionasii, in which 8-10 осе 


H. mino 


as beî | 
т. If 


aa‏ ——— ا 


1984] 


STEYERMARK — VENEZUELAN GUAYANA 


WU 


м? 


"M d 22 


«Pic o 


Ficu و‎ 
RE 5. Several leafy shoots growing in clump at base of plant of Heliamphora tatei. 


heterodoxa, 22 
the : 
tos from Territorio Federal diras re- 
Д to Н. tatei апі Н. пеЫіпае, 2-4 flow 

Pear; in Н. nutans we find 4, and in H. minor 


the 
“йы ranges from generally 2 to 5, rarely 


7 flowers may be present, in 


Appe ndage of the pitcher. 


of the боља The shape and size 


г appendage is extremely variable, 


and, except for H. heterodoxa var. exappendic- 
ulata, in which it 15 scarcely developed, is an 
unreliable taxonomic character to serve for the 
differentiation of taxa, although it was used orig- 
inally by Gleason (1931: 367) in his key to sep- 
arate the various taxa in size and shape. Heliam- 
phora nutans and H. minor may have the 
appendages as short as 2-3 mm long, but vary 


309 


310 


in Н. nutans from a minimum length of 3—7 mm 
to a maximum length of 10 mm and in H. minor 
to 20 mm. On the other hand, the taxa from the 
Territorio Federal Amazonas show relatively 
longer or broader appendages, varying from 10— 
40 mm by 5—20 mm in the taxon referred to Н. 
tatei var. macdonaldae, and from 10-40 mm by 
10-42 mm in the taxon referred to Н. neblinae 
var. neblinae. However, in H. neblinae var. par- 
va the appendage is much smaller, 6—28 mm by 
6-20 mm, thus breaking down the difference be- 
tween the taxa from the Territorio Federal Ama- 
zonas and H. heterodoxa var. heterodoxa with 
appendages 9-40 mm by 7—30 mm and H. ion- 
asii with appendages 16–20 mm by 10-30 mm. 

Perianth. While the usual number of peri- 
anth segments (tepals) is 4, specimens occur with 
5 or 6. In H. minor and H. heterodoxa the tepals 
vary from 4 to 5, and ina glabrous variety of H. 
heterodoxa (Cardona 2661 [VEN]) 6 tepals аге 
present. In his key to H. neblinae, Maguire (in 
Maguire et al., 1978: 57) states that the perianth 
segments are “commonly 5-6” in H. neblinae 
var. neblinae and “commonly 4” in var. viridis. 
However, although the isotype of var. neblinae 
(Maguire, Wurdack & Bunting 37151) at VEN 
has 6 tepals, most of the other specimens ex- 
amined (Maguire, Wurdack & Bunting 37035 
and Steyermark 103956) and cited by Maguire 
as var. neblinae, have only 4 segments, whereas 
Steyermark 103775 and Maguire, Wurdack & 
Maguire 42465 show both 4 and 5 segments. 
Since the number of tepals is a variable character 
within these varieties, and no other taxonomic 
differences are indicated, they may be considered 
only as variations of tepal number within the 
same taxonomic variety. 

The inner perianth segments, usually 2, are 
shorter and narrower than the generally 2 outer 
ones. They are always smaller in anthesis than 
in fructification. The tepals of H. minor and H. 
nutans, when in flower, are generally smaller than 
any of the other taxa, with an average length of 
25-35 mm, but attain 45-50 mm in fruit. The 
largest perianth segments are encountered in H. 
heterodoxa of Estado Bolivar, attaining a max- 
imum length of 60 mm, and in the taxa from 
Territorio Federal Amazonas, attaining a max- 
imum length varying from 55-60 mm. In fruc- 
tification these same taxa (H. heterodoxa, H. ta- 
tei, and Н. neblinae) attain greater lengths of 80, 
72, and 70 respectively. Since the minimum and 
maximum lengths show a wide range and inter- 
grade between the various taxa, this character 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


has not been found applicable for purposes of 
differentiation. 

е perianth segments in H. minor are lan- 
ceolate, broadest at the base, and acuminate to 
cuspidate in anthesis. Those of H. nutans are 
similar in shape but less acuminate or cuspidate, 
while in H. heterodoxa the segments have a 
slightly broader oblong-lanceolate or ovate-ob- 
long shape, varying from broadest at or near the 
base to broadest toward the middle, and from 
an acute to cuspidate apex. The taxa from Ter- 
ritorio Federal Amazonas, because of their gen- 
erally broader outer tepals, have an oblong-el- 
liptic or lance-oblong form, obviously broadest 
around the middle and vary at the apex from 
acute to obtuse. 

Other variations. Within the genus Heliam- 
phora, the interior upper surface of the pitcher 
is generally covered by a zone of numerous, 
closely packed, minute trichomes or with longer 
trichomes placed more distantly between one 
another. In H. heterodoxa var. glabra, H. het- 
erodoxa var. exappendiculata f. glabella, H. mi- 
nor f. laevis, and H. tatei var. macdonaldae this 
ordinarily pubescent zone is replaced by one 
nearly or completely glabrous, excluding the bas- 
al aggregation of elongate, retrorse hairs located 
at the summit of the glabrous lower interior por- 
tion of the pitcher. : 

Observations of large colonies of H. tate! and 
var. macdonaldae on Cerro Duida in 1981 and 


thor's opinion, the internally glabrous P 
should be considered at most a form, гаће! f 
a variety, of H. tatei. The glabrous verse’ " 
H. heterodoxa, described as a variety 
guire, likewise may be considered as т‹ Ju 
glabrous state of the species and recognize 
only a form. 2 
Results. А re-examination of herbarium ~ 
living material of Heliamphora collected = a 
cent expeditions by the author have shown à di 
degree of variability and plasticity among E 
several taxa within the genus. The characters i ке 
ployed by Maguire (in Maguire et al., 1978: 2i 
51) in the most recent treatment of the genus hus 
to provide for this degree of variation. It ist 
necessary to modify and realign the taxa 


1 n on the same p 
colony, but eve fants 
T 


m, ___ енен 


"Hh. 


4 


1984] 


on less variable characters. As а result, the fol- 
lowing key and changes in nomenclature are giv- 
en: 


Heliamphora tatei Gleason, Bull. Torrey Bot. 
Club 58: 368. 1931. 


Heliamphora tatei Gleason var. tatei f. tatei. 


Heliamphora tyleri Gleason, Bull. Torrey Bot. Club 
58: 368. 1931. 


Heliamphora tatei Gleason var. tatei f. macdon- 
aldae (Gleason) Steyerm., stat. nov. He- 
liamphora macdonaldae Gleason, Bull. Tor- 
rey Bot. Club 58: 367. 1931. 

Tee tatei var. macdonaldae (Gleason) Ma- 
guire, Mem. New York Bot. Gard. 29: 57. 1978. 

Heliamphora tatei Gleason var. neblinae (Ma- 

: : indie 
neblinae Maguire, Mem. New York Bot 
Gard. 29: 57. fig. 54. 1978. 

Heliamphora neblinae Maguire var. pe Maguire, 
m. New York Bot. Gard. 29: 59. 1978. 
Heliamphora tatei Gleason var. neblinae f. parva 
(Maguire) Steyerm., stat. nov. Heliamphora 
neblinae var. parva Maguire, Mem. New 
York Bot. Gard. 29: 59. fig. 49: G-H, 50: 

A-C, 1978. 


Heliamphora heterodoxa Steyerm. var. hetero- 
doxa f. glabra (Maguire) Steyerm., stat. nov. 
Heliamphora heterodoxa var. glabra Ma- 
tos Mem. New York Bot. Gard. 29: 54. 


Heliamphora minor Gleason f. laevis Steyerm., 
f. nov. ТҮРЕ: Venezuela. Bolívar: crece en 
Zonas pantanosas, Cerro Auyan, 2,100 m, 
Jan. 1949, Е. Cardona 2661 (holotype, 
VEN). PARATYPES: Venezuela. Bolívar: Piar, 
T eam margin at edge of wet savanna, Ma- 
cizo del Chimantá, cumbre del altiplanicie 
en la base meridional de los farallones supe- 
roms del Apacará-tepui, sector N del ma- 
cizo, 5?20'N, 62°12’ W, 2,200 m, Steyer- 
mark, Huber & Carreño 128416 (VEN); 
lugares muy húmedos, sabana y bosque, Sal- 
to Angel, alrededores caida de agua, Auyan- 
tepui, 13 Aug. 1968, Foldats 7008 (VEN); 
summit, Auyan-tepui, 2,100 m, 18 Feb. 
1984, Luteyn & Steyermark 9590 (NY, 
VEN). 


STEYERMARK— VENEZUELAN GUAYANA 


311 


A H. minor amphoris intus zona media barbata ex- 
epta glabris, tertia vel quarta supera ventricosa oc- 
cupatis recedit. 


This form differs from typical H. minor in the 
completely glabrous inner face of the upper ex- 
anded portion ofthe pitcher, except for the zone 
of elongate hairs at the constriction at the base 
of the upper expanded portion. In Steyermark et 
al. 128416 this glabrous upper expanded portion 
occupies about a fourth of the length of the pitch- 
er. In typical H. minor, the interior upper ven- 
tricose face of the pitcher is usually pubescent 
with a zone of scattered elongate hairs. In the 
newly described form these hairs are completely 
absent except for the zone of hairs at the base of 
the ventricose portion at its constriction. The 
Steyermark, Huber & Carreño 128416 collec- 
tion occurred in a shaded zone of shrubbery by 
the border ofa savanna where another collection 


hibits a diminished number of hairs, tending to- 
ward the f. laevis. 

I have referred the Cardona, Foldats, Luteyn 
& Steyermark, and Steyermark et al. collections 
to H. minor rather than to H. heterodoxa, since 
the upper ventricose zone is limited to '4—!^ of 
the total length of the pitcher instead of having 
this upper portion %-/ of the total length as a 
characteristic of H. heterodoxa. 


Heliamphora heterodoxa var. exappendiculata f. 
glabella Steyerm., f. nov. TyPE: Venezuela. 
Bolívar: Auyan-tepui, cumbre de la parte 
norte de la sección sur (division occidental), 


1964, Steyermark 937 12 бе: VEN). 


A var. exappendiculata a interiis in dimidio 
superiore glaberrimis rece 


This form differs from var. exappendiculata in 
having the interior of the pitcher glabrous, except 
for some hairs at the basal zone of the expanded 

rtion, whereas in var. exappendiculata the ex- 
panded interior of the upper portion of the pitch- 
er is densely covered with trichomes. 


Concluding remarks. As an auctoctonous ge- 
nus, isolated on the ancient Roraima formation 
of the Guayana Shield of South America, and 
evidently separated since remote geological time 
from its nearest North American relatives, He- 
liamphora would appear to be a genus of ancient 


312 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


KEY TO THE SPECIES, VARIETIES, AND FORMS OF HELIAMPHORA 


[Уог. 71 


1. Anthers mainly 16-20; lowest floral bract usually equalling or much exceeding the lowest pedicel; plants 
a 


of Territorio Federal Amazon 


2. Upper interior portion of pitcher glabrous above the pubescent ring . H. tatei var. tatei f. macdonaldae 
i 3 


2. Upper interior portion of pitcher densely pubescent above the pubescent ring 


3. Upper pubescent zone of hairs with a mainly uniform length of 0.8-2 mm 


erior surface of pitcher glabro H. tatei var. neblinae f. parva 


4. Ex ucl ees 
1. Anthers (4–)7—15(—16); lowest floral bract usually shorter than the lowest pedicel; plants of Estado 
Bolív 


6. Appendages of the pitchers obviously developed, 3-40 mm 1 


g e 
7. Anthers 3-5 mm long; upper ventricose portion of pitcher occupying %4—' of the total length : 
H. minor f. laevis 


7. Anthers (4.5-)5-8 mm long; upper ventricose portion of pitcher occupying %—У» of the total 
length 


сол а iet А Д ано e Н. heterodoxa var. heterodoxa f. glabri ч 


nasil 


© 
d 
а. 
3 
v 
3| 
5, 
о | 
б | 
а | 
б 
A; 
а | 
= | 
S 
5 | 
б 
T 
| 
t 
Ni 
Ма: 
=! 
$i 
а 
O 
а 
Y. 
[e] 
l= 3 
e 
a 
y 
N 
N 
+ 
دي‎ 
<> 
— 
о 
8 
5 
de 
Е 
AT 


the pitcher 


oo 
б 
[4] 
3 
e 
[=] 
E 
”“ 
D 
[e] 
e 
o 
им | 
Lad 
= 39 
[4] 
— 
i4 
oO 
5. 
о 
~ 
o 
= 
e 
Er 
O 
Y, 
ec 
[e] 
I" 
[4] 
Las | 
T 
5 | 
=f 
а. 
e 
B 
go 
= 
[4] 
g 
s 
z 
7с 
о 
| 
i= ж 
e 
m 
2 
# | 
5. 
cg 
ә H 
8 
в 
| a 


mınute, more or less uniform velvety indument of hairs 0.5-1 mm lon 


zone consisting of more or less uniform hairs 0.7-1 mm lon; 


У long; upper pubescent zone of the interior of the pitcher occupying %- 
% the length of the pitcher, 6-8.5 cm long; most of the indument of the upper гор 


nt 
‚ nutans 


10. Anthers (4.5-)5-8 mm long; upper pubescent zone of the interior of the pitcher occupying 
Ys—V^ the length of the pitcher, 7-18 cm long; most of the upper indument of the upper 


bescent zone consisting of hairs 0.5-0.7 mm long, the lower portion with longer wind 
BÉ e eS - 


1 mm lon 


rodoxa 


geological origin. However, judging by the high quinima, sector suroeste central, bosque Е 
degree of variation and plasticity shown by the galeria y bosque alto, a lo largo del aon 
known taxa of the genus, it would indicate that suroccidental del Rio Carapo, 5°45 је 
these taxa have become separated from one 63°35'W, 950 m, 26 May 1978, common In 
another in only relatively recent times, and that the tall forest of trees 20-25 m tall, e 
they are still in the process of evolutionary in- ermark, Berry, Dunsterville & Dunster! 
stability as shown by the similarity of their floral 117468 (holotype, VEN; isotype, US). 


characters and high degree of vegetative varia- 


tion. The degree to which the taxa have diverged Arbor 20-metralis; ramis, petiolis, rhachibus €t p 


during their evolutionary history has been rela-  liolisglabris; foliis 1—3-foliolatis; petiolis 
m longi 5 


tively insufficient to have resulted in their sharp _ 215; foliolis 7-9.5 cm lo 
differentiation from one another. terminalibus racemosis &-11-floris 


2.5-6 cm lon- 
wd 


усе 1.2-1.5 cm longo dense o-t en 

LEGUMINOSAE thesi inaequaliter 4—5-lobato, petalis 5-7 oblan oye 
vel obovatis apice rotundatis 25 mm longis 12- L5- 

CAESALPINOIDEAE latis glabris; ovario lineari-elliptico 4-5 mm longo ~ 


Aldina berryi Cowan & Steyerm., sp. nov. TYPE: 
Venezuela. Bolívar: cumbre, Cerro Guai- 3mm longo glabro. 


ad 


2 mm lato glabro vel basi pilis paucis minutis bulato 2 
munito, stipite 5 mm longo glabro; stylo Su 


— 


ne 


— mt 


а. 


= „—__ 


—— 1 


STEYERMARK —VENF7ZIIFI AN GUAYANA 3 1 3 


1984] 


Tree 20 m tall; branches, petioles, rachis of 
leaves and leaflets glabrous; leaves 1—3-foliolate 
or the uppermost sometimes simple, mainly al- 
ternate; petioles 2.5—6 cm long; lateral petiolules 
7-11 mm long, terminal 22—30 mm long, thick- 
ened portion 11-13 mm long; leaflets charta- 
ceous, gray green beneath, ovate or oblong-ovate, 
obtusely acuminate at apex, acumen 4—5 mm by 
2-3 mm, 7-9.5 cm by 3—5 cm; lateral nerves 
inconspicuous to obsolete, 10-14 on each side, 
tertiary venation absent; inflorescence terminal, 
simply racemose, 8—1 1-flowered, 7-11 cm long; 
peduncle 1.5-2 cm long, densely brown-tomen- 
tose; flowers pedicellate, pedicels 3-7 mm long, 
articulate at apex, densely brown-tomentose; ca- 
lyx (in bud) obovoid to ellipsoid, densely dark 
brown tomentose; unequally 4—5-lobed in an- 
thesis with reflexed lobes, 1.2-1.5 cm long (tube 
olive green, 7-9 mm long, 10-11 mm wide at 
summit; 3 lobes broadly lanceolate, subacute, 9— 
10 mm by 4-5 mm, fourth lobe ovate to broadly 
Ovate, subobtuse, 10 mm by 9 mm, all lobes 
glabrous and white within except for pilosulous 
margins above middle); petals white, 5—7, ob- 
lanceolate or obovate, rounded at apex, 25 mm 

y 12-13 mm, glabrous; stamens numerous, uni- 
form, filaments white, fasciculate, 15-18 mm 
long, glabrous; anthers yellow, linear, rounded 
at upper end, asymmetrically bilobed at base, 
dorsifixed, 4.5-6 mm by 1 mm; ovary linear- 
elliptic, 4-5 mm by 1.5-2 mm, glabrous or with 
à few, minute appressed hairs basally, stipe gla- 
brous, 5 mm long; stigma terminal; fruit not seen. 


This taxon is named for Paul Berry, who ac- 
companied the author on the present expedition, 
and who rendered great collecting assistance. Al- 
din © ber ryi is very conspicuous when flowering 
with Its masses of fragrant, white flowers at the 
summits of the tall forest on Cerro Guaiquinima. 
115 distinguished by the complete glabrity of the 
Ovary and vegetative parts. 


PAPILIONOIDEAE 


Dipteryx РћаеорћуПа Steyerm., sp. nov. TYPE: 
Venezuela. Bolivar: Cerro Guaiguinima, 
cumbre, Salto de Río Szczerbanari, parte 
central del cerro, 5?44'4"N, 63?41'8"W, 750 
m, 20-25 Jan. 1977, Steyermark, Dunster- 
ville & Dunsterville 113200 (holotype, VEN). 
PARATYPE: same locality and date, Steyer- 
mark, Dunsterville & Dunsterville 113248 
(VEN). 


Arbor 4-20-metralis; foliis petiolatis 5-foliolatis pa- 
ribus lateralibus oppositis, foliolis oblongo-vel lanceo- 
lato-ellipticis api dati i i 1-2 cm lon- 
go basi obtusis 7-10.5 cm x 2-3.5 cm subtus minute 
adpresso-puberulis; petiolis rhachidique minute ad- 
presso-puberulis; infructescentia pedunculata 12–21 cm 
longa minute denseque adpresso-puberulis; fructu fu- 
siformi-elliptico extremitatibus subacutis 4-6 cm x 
1.2-1.8 cm minute adpresso-puberulis. 


Tree 4—20 т tall; leaves petiolate, 5-foliose, 
the two lateral pairs opposite; leaflets dark green 
above, brown below, oblong- to lance-elliptic; 
caudate at the apex with a slender acumen 1-2 
cm long, obtuse at base, 7–10.5 cm by 2-3.5 ст, 
glabrous above, minutely appressed-puberulent 
‘below on surface and midrib; lateral nerves 8— 
10 each side, obsolete below, slightly evident 
above; midrib elevated below, depressed above; 
tertiary venation minutely and obsoletely retic- 
ulate below; petiole and leaf-rachis 3.5—5 cm long, 
minutely appressed-puberulent; petiolule 5-10 
mm long, minutely appressed-puberulent; in- 
fructescence paniculate, 12—21 cm long, the fer- 
tile portion 7-15 cm long, densely appressed- 
puberulent, pedunculate; peduncle 4.5—8 cm long, 
densely and minutely appressed-puberulent; le- 
gume mustard brown, fusiform-elliptic, subacute 
at both ends, finely reticulate, 4—6 cm by 1.2- 
1.8 cm, minutely appressed-puberulent; flowers 
not seen. 


This taxon is characterized by the minutely 
dense puberulence which occurs on the infruc- 
tescence, lower leaf surface, rachis and petioles 
of the leaves, and the caudate-tipped leaflets. 


LINACEAE 


Ochthocosmus berryi Steyerm., sp. nov. ТҮРЕ: 
Venezuela. Amazonas: tall forest along 
stream, NE shoulder at base of bluff, Cerro 
Aratitiyope, 90 km SW of Ocamo, 1,000 m, 
26 Feb. 1984, Steyermark, Berry & Delascio 
130228 (holotype, VEN). 


1:: 1 + T 


Arbor 8 lis; ) is api e 
tusis basi cuneatim angustatis 3.5-6.5 cm x 2-4 ст, 
marginibus utroque latere obsolete 6—7-crenulatis; in- 


vel pedunculatis usque 5 mm longis; sepalis inaequa- 
libus quattuor 0.8-1 mm x 0.5 mm glanduliferis, se- 
palo quinto longiore 1.2-2.5 x 0.5-0.6 mm eglandu- 
lifero; petalis late obovatis 3.5 mm x 1.8 mm; 
filamentis 2-3.5 mm longis. 


Tree 8 m tall. Leaves obovate, subcoriaceous, 
pale green below, rounded at the retuse apex, 


314 


cuneately narrowed at base, 3.5—6.5 cm by 2-4 
cm, dull green above with inconspicuous ner- 
vation, faintly nerved below, obscurely 6-7- 
crenately toothed along each margin; petioles 3– 
5 mm long. Inflorescence paniculate, many-flow- 
ered, the flowering portion 2.5-3 cm long, 2-3 
cm broad, shorter than the leaves, epedunculate 
or the peduncle to 5 mm long, flowers white. 
Pedicels 1.2-2.5 cm long. Sepals unequal, 4 of 
them ligulate-oblong, rounded at apex, 0.8-1 mm 
by 0.5 mm, prominently glandular on the thick- 
ened margins; fifth sepal longer, ligulate-oblong, 
1.2-2.5 mm by 0.5-0.6 mm, eglandular. Petals 
broadly obovate, rounded at apex, 3.5 mm by 
1.8 mm. Filaments 2-3.5 mm long. Style 1.4— 
1.8 mm long, usually longer than the ovary. Ovary 
1.1 mm lon 


This species is related to O. floribundus Glea- 
son, from which it differs in the shorter inflores- 
cence, shorter than the leaves, inflorescence epe- 
dunculate or at most to 5 mm in length, the 
eglandular, elongated fifth sepal contrasting with 
the other four shorter glandular sepals, which are 
more prominently thickened and more abun- 
dantly glandular than in O. floribundus, and the 
relatively smaller and more broadly obovate pet- 
als. 

The other species known from Territorio Fed- 
eral Amazonas of Venezuela, О. multiflorus 
Ducke, together with its variations, is a small 
ligneous plant of the savannas with entire or 
nearly entire leaf margins. Ochthocosmus berryi 
is a tree in a woodland habitat. 


RUTACEAE 


Rutaneblina Steyerm. & Hane ien nov. TYPE: 
R. pusilla Steyerm. & Lute 


Inflorescentia terminalis multiflora subsessilis sub- 
о 


tam 

mentis basi intus glanduliferis. Discus Obsoletus. Pis- 
tillum sessile, st e 5-lobato, =e 
simplici. Ovarium subglobosum, -carpellis 5 basi con 
natis supra medium liberis unilocularibus - Ovulum 
quoque locule solitarium. Folliculi 4-5 divaricati ~ 
bri, dir мора 3- аши Fruticulus. Folia ter- 
nata, integerri vel obscure crenulata, nervis late- 
ralibus nullis. 


Rutaneblina pusilla Steyerm. & Luteyn, sp. nov. 
TYPE: Venezuela. Amazonas: altiplanicie en 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


la cumbre del brazo noroccidental, Cerro де 
la Neblina, al norte del campamento base a 
lo largo del Rio Mawarinuma, afluente del 
Río Baria, 0*52-53'N, 66?05'W, 1,880 т, 8 
Feb. 1984, Steyermark 129798 (holotype, 
VEN). PARATYPE: same locality and date, 
Luteyn 9451 (NY, VEN). Figure 6. 


Frutex pusillus 0.7-1 metralis; foliis 3-verticillatis 
breviter petiolatis, obovatis apice truncatis vel sub- 
ncatis mucronulatis basi acutis vel subacutis 1-2.5 
cm longis 1-1.5 cm x oxi petiolis 1-2 mm lon- 
gis; inflorescentia term 
diam. 


d 


laribus subobtuse acutis 2.1 mm x 1-1.5 mm, sib 
rioribus lanceolatis 2 mm x 1 mm, marginibus p 


mm longis 1.1-1.5 mm latis intus utroque latere A 
nervis чейре. staminibus 4 mm m lo ongis, filamenti 
5 т 


арісе iilis apiculatis 0.7 mm ui pistillo T 5 Ps 
longo, stylo 0. 3 mm longo, ovario rm m longo 1.2 mn 
lato; f blongis 7 mm ong 
5 mm latis. 


Low shrub 0.7-1 m tall with irregularly сшу- 
ing branches. Leaves 3-verticillate, with fra- 
grance of bitter orange, coriaceous, rich green 
both sides with pale yellow-green midrib above, 
obovate, truncate or subtruncate at apex with 
mucro 0.5 mm long, narrowed to an acute ог 
subacute base, 1-2.5 cm by 1-1.5 ст, glabrous, 
entire or obscurely crenulate, midrib sulcate 

above, elevated below, lateral nerves absent, ter- 
tiary venation minutely reticulate on both sur- 
faces; petiole 1-2 mm long; inflorescence 1.1 cm 
long, 1.3-1.5 cm diam., subtended at base by 4 
few bracts; bracts coriaceous, lanceolate, acute, 
carinate, 4-5 mm long, 1.2-1.5 mm wide; flowers 
subtended by bracteoles ovate-deltoid, acute, 1 
mm long; pedicels 2 mm long, 1.5 mm wide; 
sepals dull lavender, unequal, the outer ovate- 
triangular, 2.1 mm by 1.4-1.5 mm, the innt 
lanceolate, 2 mm by 1 mm, subobtusely acute. 
dorsally carinate, margins slightly paler ECC 
rious, persistent and not enlarged in fruit; petal 
creamy white, elliptic-oblanceolate, subacute. 
dorsally carinate, 3-3.5 mm long, 1.1-1.5 ™™ 
wide, the inner surface with a broad median j 
tion and 4—6 lateral branches; stamens 2 me 
long, anthers deltoid-ovoid, bluntly apiculate 
apex, bilobed basally, filaments 1.4-1. 5 mm long, 


at 
0.4 mm wide, glabrous with glandular patches 


— 


a—— у 


ай 


1984] STEYERMARK— VENEZUELAN GUAYANA 31 5 


Eoo. aT th 


© 


> oum ے‎ „Уз > 


K 


FIGURE 6, n pusilla. —A. Habit. – В. Flower, natural position. —C. Outer sepal, dorsal view.— 

ппег sepal, do ie iew.—E. Petal, ventral view. — Е. Petal, dorsal view. – С. Portion of flower, showing relation 
of parts, — s and pistil, with petals and sepals removed.—I. Portion of androecium, with glandular 
kei patches at p т filaments within.—J. Vertical section through gynoecium.—K. Gynoecium, natural 


base within; gynoecium sessile, 1.5 mm long; This low shrub is common on the drier rocky 

stigma capitate, obscurely 5-lobulate, rounded, elevation near the periphery of the summit, but 
0.3 mm long; style simple, 0.3 mm long; ovary also occurs in the slightly depressed and wetter 
Subglo se, 1 mm high, 1.2 mm wide; fruit valley portion. The inner portion of the cortex 
brown, the 4—5 divaricate follicles 7 mm long, 5 is orange and the leaves have a fragrance remi- 
тт wide, glabrous, rugulose within. niscent of bitter orange. 


316 


The new genus cannot be placed generically in 
the treatment by Cowan (1967) of the Rutaceae 
of the Guayana Highland. Nor does it fit into 
any of the genera treated by Bentham and Hook- 
er (1862) and by Engler (in Engler & Prantl, 1896). 
The genus is characterized by its combination of 
simple 3-verticillate leaves, 5 stamens equal in 
number to the imbricate sepals and petals, the 
free sepals and petals, the slightly unequal 
obliquely carinate sepals, the uniovulate 4—5 car- 
pels connate below and free above, the follicular 
dehiscent spreading fruits, and the apparent ab- 
sence of a disk which is represented apparently 
by only gland-like dark areas at the base of the 
filaments. The relationship of the genus is ob- 
scure and at this time not apparent. 


Raveniopsis cowaniana Steyerm. & Luteyn, sp. 
nov. TYPE: Venezuela. Rio Negro: Cerro de 
la Neblina, altiplanicie en la cumbre del bra- 
zo noroccidental, al norte del campamento 
base a lo largo del Rio Mawarinuma, af- 
luente del Río Baria, 0*52-53'N, 66?5'W, 
1,880 m, 7-8 Feb. 1984, Luteyn 9413 (ho- 
lotype, VEN; isoty Y). PARATYPE: same 
locality and date, Steyermark 129814 (VEN). 

Planta sublignea, caule simplici 0.3 m alto apicem 


versus dense pubescenti; foliis „ар trifoliatis, fo- 
liolis oblanceolatis L 5-3. 8c x Q. 5-1. 1 ст supra 


= жакы munitis; inflorescentia coarctata subses- 
sili 1-2 cm longa, pedunculo 1-5 mm longo dense 
= corolla rubra 15 mm longa (tubo 7 mm 


ЊЕ lobis duobus anguste lanceolatis 4 ш х 

mm; lobis tribus oblongo-vel obovato-ellipticis 5 mm 
х 3-3.5 mm extus sparse pubescentibus “ү simpli- 

cibus reflexis munitis). 


Subligneous, simple-stemmed plant, 0.3 m tall; 
leaves revolute, dark green above with sulcate 
nerves, buff-woolly below, digitately trifoliate, 
shortly petiolate to subsessile; leaflets oblanceo- 
late, subacute to obtusely acute or mucronate at 
apex, sensibly narrowed to the base, 1.5—3.8 cm 
by 0.5-1.1 cm, glabrous, strongly sulcate-nerved 
and strongly punctate above, densely buff woolly 
below; petiole well-developed; inflorescence ter- 
minal, subterminal, or axillary, subsessile or 
shortly pedunculate, congested, cincinnate, uni- 
laterally racemose, 1-2 cm long; peduncle 1—5 
mm long, densely woolly pubescent; flowers ses- 
sile or pedicellate to 2 mm long; calyx lobes 5 
unequal, imbricate, densely buff-olive pubes- 
cent, the outer two lobes broadly lanceolate, 9— 
11 mm by 3-4 mm, the interior 3 lobes narrowly 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


lanceolate, subacute, 5 mm by 1.5-2 mm; calyx 
tube 1-2 m long; corolla red, 15 mm long, zy- 
gomorphic with 2 narrower and 3 broader lobes, 
tube cylindric, 7 mm a 3 mm aei 2 e wide 
at base, sparsely p itl 

the 2 narrower ibet vara lanceolate, 4 mm 
by 1-1.5 mm, the 3 broader lobes oblong- or 
obovate-elliptic, subacute, 5 mm by 3-3.5 mm, 
pubescent without, exterior pubescent with sim- 
ple, sparse, reflexed hairs, interior of corolla tube 
5-ridged with thickened pubescent ridges; fertile 
anthers lanceolate, narrowed to apex, 2 mm by 
0.6 mm, filaments 0.6 m long; ovary depressed- 
subglobose, 1.5 mm long; style 10 mm long; stig- 
ma capitate. 


The only other known trifoliate species of Ra- 
veniopsis are R. trifoliolata Cowan of Cerro de 
la Neblina and R. stelligera Cowan of Cerro Yu- 
taje. The new taxon here described from Cerro 
de la Neblina differs from R. stelligera in the 
simple pubescence with much longer corollas and 
petioles, and from R. trifoliolata in the congest- 
ed, short, densely pubescent inflorescence, small- 
er, narrower leaves with very short or even sub- 
sessile petioles, deeply sulcate upper leaf surface, 
and densely pubescent lower leaf surfaces ап 
upper portion of the stems. 

The species commemorates the name of Dr. 
Richard S. Cowan, for his excellent work on the 
genus Raveniopsis and other genera of Rutaceae 
of the Guayana Highland. 


NOTE ON RAVENIOPSIS FRATERNA 
AND R. SERICEA 


Raveniopsis fraterna Cowan is distinguished 
from R. sericea Cowan on the ie и we 
corolla tube (9 mm), larger calyx ( adl 
lower leaf surface, as contrasted with the smal 
corolla tube (5.5 mm), smaller calyx (3-3. a 

y 2-3 mm), together with the sericeous pu M 
cence of stems and lower leaf surface of R. ~ 
ricea. Cowan (in Maguire et al., 1960: 32) (t 
that paratypes of R. sericea (Steyermark & ie 
dack 811 and Steyermark 75905) do not 
form to the uniform t 
by the type collection (Steyermark & Wur “ 
646) from Chimanta. The collections of St а 
mark et al. 128764 and 128902 from Chim = 
Massif have the smaller measurements wc 
icea, but it is doubtful if the two taxa сап e 
maintained separately as species. 
that only one taxon can be recognized W 


= ~ _ 


— 


=" 


= 


1984] 


ies in size of calyx and corolla and type of to- 
mentum. 


EUPHORBIACEAE 


Phyllanthus jablonskianus Steyerm. & Luteyn, 
Sp. nov. TYPE: Venezuela. Amazonas: Río 
Negro, Cerro de la Neblina, altiplanicie en 
la cumbre del brazo noroccidental, al N del 
campamento base a lo largo del Río Ma- 
warinuma, afluente del Río Baria, 0°52- 
53'N, 66°5’W, 1,880 m, 8 Feb. 1984, Stey- 
ermark 129816 (holotype, VEN; isotype, 
NY). PARATYPE: same locality and data, Lu- 
teyn (VEN, NY). Figure 7А-Е. 

Suffrutex 0.2-0.4-metralis; ramificatione phyllan- 
thoidea; foliolis ellipticis, obovati-ellipticis vel anguste 
oblanceolatis apice rotundatis basi acutis vel obtusis 


1 1 us masculinis: laciniis calycinis 
ligulato-oblongis 1.5 mm x 0.8 mm, disco 6 glandu- 
oso, glandulis distinctis, quadrato-oblongis; stamini- 
bus „antheris 0 "arl вои сасу ота : | 

liberis laciniis calycinis brevioribus; floribus foemineis: 
disco annulari undulato i 
: suborbicularibus apice rotundatis 1.8-2 mm x 1.2- 

5 mm; stylis 3 ad basin profunde bifidis 1.2 m 


long; staminate flowers: solitary or 2—3-fascicu- 
о mm diam., 6 segments spreading, 
ан €-oblong, 1.5 mm by 0.8 mm; disk with 6 
ct quadrate-oblong glands rounded-trun- 

os, at distal end, 0.4 mm by 0.3 mm; 3 anthers 
tiie, long with globose anther sacs 0.4 mm 
fied ја aments free, stout, 0.8 mm long, shorter 
ndi i саша segments; pedicels filiform, 2— 
ow "qe pistillate flowers: 3 mm high, 4 mm 
ui > 9 perianth segments ascending, suborbic- 
T, rounded at apex, 1.8-2 mm by 1.2-1.5 mm; 
Pedicel 8-10 mm long in anthesis, 10-15 mm 


long in fruit: 3 ' 
; 3 styl 
each styles yles deeply bifid to the base, 


STEYERMARK— VENEZUELAN GUAYANA 


317 


From P. maguirei Jabl. of Neblina the new 
taxon differs in the broader leaflets mainly 2–3.5 
times longer than broad which are mainly ob- 
ovate-elliptic to elliptic, and in the well-devel- 
oped pistillate disk. From P. neblinae Jabl., also 
of Neblina, this new taxon differs in the much 
narrower, non-emarginate leaflets which are usu- 
ally elliptic to obovate-elliptic and lustrous above. 
In leaflet shape, conspicuous nervation and lus- 
trosity above, it resembles P. /ongistylus Jabl., 
but lacks the long style and sublaminal gland of 
that species. Additionally, it differs from P. stro- 
bilaceus Jabl. in the short anthers with globular 
anther sacs and free styles bifid to the base. 

The species commemorates the name of the 
dedicated worker on the Euphorbiaceae of the 
Guayana Highland, Dr. Eugene Jablonski. 


Venezuela. Amazonas: 
nilla, N of Cerro Aratitiyope, on sandstone 
scrub-covered slopes, 440 m, 1 Mar. 1984, 
Steyermark, Berry & Delascio 130328 (ho- 
lotype, VEN). Figure 7F-I. 


A P. vacciniifolius ramulis deciduis usque 13 cm 
longis, foliolis 15—30 gerentibus recedit. 


Shrub or treelet 2—2.5 m tall, branchlets with 
15-30 leaflets, to 13 cm long; leaves broadly ob- 
ovate, rounded at apex, acutely narrowed to base, 
7-12 mm by 5-9 mm, laminal gland on lower 
side 1.5 mm below apex, lateral nerves 7-10 each 
side; petiole 1.5 mm long; staminate flower: ped- 
icel 1.5 mm long, outer perianth segments 2.1 
mm by 1.8 mm, inner ones 2.1 mm by 1 mm; 
3 anthers narrowly oblong, long-apiculate, nearly 
3 times longer than wide, filaments scarcely de- 


pistillate flower: pedicel 4.5-5 mm long; outer 
perianth segments 2.2 mm by 0.8 mm, inner ones 
2.5-1.1 mm; ovary continuing into a conic style, 
1.5 mm long, style 1 mm long, 6 disk glands 0.4 
mm long, separated, shallowly crenulate on sum- 
mit; capsule subglobose, 3 mm high, 4 mm diam. 


This new subspecies is disjunct in its distri- 
bution, where it is isolated in the Territorio Fe- 
deral Amazonas. Typical P. vacciniifolius is oth- 
erwise known only from the sandstone table 
mountains and the Gran Sabana of Estado Bo- 
lívar in eastern Venezuelan Guayana. The sub- 
species vinillaensis has the same elongate exten- 
sion of the anthers, the erect short conical style, 


318 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 | 
? 


B 
E 
E 
ч 
о 
Е 
E 
" 
o 
і 
f 
$ 
| 
FIGURE 7. Phyllanthus. A-E. P. Jablonskianus. — А. Staminate flower.—B. Stamen.—C. Fui flower. = | 
D. Seed, ventral ме“. —Е. Seed, dorsal view. F-I. Р. vacciniifolius subsp. viniliaéniis —F. Stamen disk 


gland indicated by dashed lines. С. Pistillate flowe с ds in үркө” 
I. Опе of disk glands. er with pedicel.—H. Pistil, showing disk glan 


А 


1984] 


and the same size and shape of the leaflets of 
typical P. vacciniifolius. It differs in the number 
of leaflets on the deciduous branchlets, these 
varying from 15-30, whereas in typical P. vac- 
ciniifolius the leaflets vary from 5—15(–20), al- 
though Jablonski (in Maguire et al., 1967: 89) 
placed that species in the part of the key having 
“deciduous branchlets with 5—12 leaflets.” Phyl- 
lanthus strobilaceus Jabl. has 20-30 leaflets on 
the deciduous branchlets, thus simulating subsp 

vinillaensis, but the anthers are rounded at the 
summit and the style is depressed and 3-lobed 
instead of erect and conical. 


OCHNACEAE 


Dario с 


І у & Maguire, gen. nov. ТҮРЕ: 
P. steyermarkii (Maguire) Steyerm. & Ма- 
guire. 


Flores sessiles vel fere sessiles. Sepala 3 plus minusve 
persistentia. Petala 5 valde imbricata alba. Stamina 5. 
: у 5. Fructus in- 
dehiscens lignescens non lobatus 2-3-locularis. Arbor 
vel frutex. 


The name is derived from perissos = odd, in 
the sense of different or extraordinary, and kar- 
DOS = fruit. 

The new genus is related to Elvasia, but that 
genus has the flowers distinctly pedicellate, se- 
pals quickly deciduous in anthesis, yellow petals, 
more numerous stamens (7—25), an elongated fi- 
fee or subulate style, and a distinctly 5-lobed 


i Elvasia steyermarkii Maguire (1968: 297, fig. 
Aid described from flowering material col- 
$ тот the Peninsula of Paria, Estado Sucre, 
*nezuela, by Steyermark and Rabe in 1966. 
( ause of its reduced number of stamens, Sastre 
Bu comm.) doubted its placement in the genus 
the us Subsequently, fruiting specimens from 
"i = rie of Cerro Sarisarinama and Jaua in 
Tách; ezuelan Guayana and from the state of 
ira, Venezuela, were collected between 1974 

and 1981, but re nor ene ин 


paki genus until 1982 and 1983, when newly 
tie | flowering material provided evidence 
fatis nspecificity between the flowering and 
8 Specimens. 
Ciis I the specimens known at the present 
= "ge s the existence of at least two species 
с Subspecies. Опе of the undescribed 
з on the summits of some of the 
= 2 le mountains of the Guayana while 
рестез, related to the taxon of the 


STEYERMARK — VENEZUELAN GUAYANA 


319 


northeastern portion of Venezuela, occurs in the 
sandstone hills of the state of Táchira in the west- 
ern Venezuelan Andes. 


KEY TO THE SPECIES OF PERISSOCARPA 


. Inflorescence umbellately or subumbellately 
unculate; apex of the petals 


— 
5 
= 
© 
O 
un 
e 
[47 
a 
e 
5 
£e 
3 
5. 
С) 
E 
£5 
e 
e, 
< 
= 
£e 
5 
O 
= 
=, 
ё. 
c 
5 


culate; apex of petals deeply emarginate; pet- 
iole 5-25 mm long 2 
Petals with a narrow sinus at apex, 2 mm 
wide above the middle, 3.5-4 mm long; 
plants of northeastern Venezuela _______ 
ИЕ P. steyermarkii subsp. steyermarkii 
2. Petals with a broad sinus at apex, 4-5 mm 
wide above the middle, 3 mm long; plants 
of the western portion of the Andes of Ven- 
ezuela _____ P. steyermarkii subsp. tachirensis 


N 


Li: (MM 


t ) Steyerm. & 
E J X o / J 
Maguire, comb. nov. Elvasia steyermarkii 
Maguire, Acta Bot. Venez. 3: 297. fig. 6. 
1968 


Tree 8-15 m. Leaf-blades oblong-obovate to 
broadly elliptic, rounded to acuminate at apex, 
cuneately narrowed at base, 9—18 cm long, 4—10 
cm wide; petioles 1–2.5 cm long. Inflorescence 
paniculate, in anthesis to 15 cm long, in fructi- 
fication 15—23 cm long with 6-12 ascending axes 
3-8 cm long; peduncle stout in fructification, 3.5— 
10 cm long, 3-6 mm diam. Flowering axes sub- 
spicate, densely flowered, pedicels very short, ca. 
] mm long. Sepals ovate-oblong, suborbicular, 
or oblong-subpandurate, apex incurved with a 
bilobate scarious appendage, 3—4 mm long, 1.5— 
2 mm wide, at first erect, at length reflexed. Petals 
white, suborbicular- to rhomboid-obovate, 
broadest above the middle, narrowed to base, 
emarginate or bilobate at apex with a narrow to 
broad sinus, strongly incurved-imbricate, con- 
volutely adherent, 3-4 mm long, 2-5 mm wide 
above the middle. Stamens with filaments 0.3— 
0.5 mm long, anthers 1.2-2 mm long. Style 0.5— 
0.8 mm long. Fruit ferruginous-brown, subglo- 
bose-pyriform, when mature 1.5—1.6 cm long 
(high), 1.5-2 cm broad. Seeds 3, trigonous, 1.5 
cm long, 1.5 cm broad. 


O THE SUBSPECIES OF 
PERISSOCARPA STEYERMARKII 


Petals narrowly emarginate at apex, 2 mm wide 
above the middle, 3.5-4 mm long, plants of 
northeastern Venezuela __-_-______ = 

P. steyermarkii subsp. steyermarkii 


320 


Petals broadly emarginate at apex, 4—5 mm wide 
above the middle, 3 mm long; piani of the 
western portion of Pus Andes of Venezue 

. steyermarkii Sube. tachirensis 


Perissocarpa steyermarkii (Maguire) Steyerm. & 
aguire subsp. steyermarkii, E/vasia stey- 
ermarkii Maguire, Acta Bot. Venez. 3: 297. 
fig. 6. 1968. TYPE: Venezuela. Sucre: Cerro 
de Humo between Los Pocitos and La Roma, 
Peninsula de Paria, 700-800 m, 11 Aug. 
1966, Steyermark & Rabe 96342 (holotype, 

NY; isotype, VEN) 


Distribution: evergreen forests of the Penin- 
sula de Paria, Estado Sucre, and Cerro Turu- 
miquire, Estado Monagas, northeastern Vene- 
zuela 


Specimens examined. VENEZUELA. lees Cerro de 
La Roma, Peninsula 
a, 1 fa 1966, porkon & 
Rabe 96342 (holotype, аш. isotype, VEN). MONAGAS: 
Acosta, Serrania del Turumiquire, altiplanicie en la 
Fila de а, ced del Río Negro (afluente del 
Río с en el borde sur de Іа meseta, 10°02' 
63*52'W, 1,600 m, 12 May 1982, Huber, Canales & 
Vasquez 6317 (VEN). 


Perissocarpa steyermarkii subsp. tachirensis 

rm. & Maguire, subsp. nov. TYPE: Ven- 

ezuela. Tachira: between dam site and nar- 

row ridge, along Rio San Buena, wooded 

sandstone hills, area of Presa Las Cuevas 

De orados Camburito у Compli- 

mentario Agua Linda), ca. 10 km E of La 

Fundación, 7°47—48'N, 71°46-47'W, 550- 

600 m, 21 June 1981, Steyermark & Ma- 
nara 125174 (holgtpe. VEN). Figure 8. 


ми“ прања bilobato sinu ‘lato recedit. 


Distribution: sandstone slopes in evergreen 
forest, foothills of the southwestern-facing slopes 

f the Andes, 450-1,000 m, Estado Tachira, 
western Venezuela. 


Specimens examined. VENEZUELA. TACHIRA: Uri- 
bante, forest along road from La Siberia to entrance to 
s Cuevas Represa, 10 July 1983, van der Werff & 
боп zalez 5282 (MO, VEN); on Rio San Buena, 10 km 
of La Fundación around Represa Dorada, 700-1 ‚000 

m, "T41-ASN. 71°46—47'W, 13-15 Mar. 1980, Lies- 
ner, Gonzalez & Smith 9655 (MO, VEN); 10 (airline) 
km жө of La Fundación, 23 km by road, around 
Represa Dorada, 0-3 km below dam, 459-650 m, 
T4T N. 71*46-47'W, 29 Арг. 1981, Liesner & Gua- 
riglia 11577 (MO, VEN), 600-900 m, 30 Apr. 1981, 
Liesner & bige e 11593 (MO , VEN), 600—1,000 m, 
10-13 Mar. 1981, Liesner & Gonzalez 10249 (MO, 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


VEN); between dam site and narrow ridge, Ye Río 
ly 


San Buena, a Las Cueva 
La d 


550-600 
21 June 1981, Steyermark & Manara 125174 (holo. 
type, VEN). 


Perissocarpa umbellifera Steyerm. & Maguire, 
sp. nov. TYPE: Venezuela. Amazonas: Cerro 
Duida, between rim and camp, occasional 
along ridge trail from Culebra, Rio Cunu- 
cunuma, 1,400 m, 18 Nov. 1950, Maguire, 
Cowan & Wurdack 29529 (holotype, VEN; 
isotype, N 

x 1.5—3-metralis; foliis obovato-ellipticis, de 
tico- дети vel late oblongis apice rotundati de 

с 


vel 
is vel obtusis basi vel 


obtusis 2.5-11 cm longis 1.8-6 cm latis; du n 

ngis; inflorescentia sessili subumbellatim га- 

culata 2—6.5 cm longa, axibus 3-9 — 

dsc m longis; floribus brevipedicel 

ин, pedicellis 0.5 mm longis; sepalis su borbicular 

tis 2 mm Jongis pas flabellatis M nihil ve 

m loneis apice 2 Doe mm atis; 

fructu ipee e D 6-11 mm longo 8-11 mm 
lato (immaturo). 


Shrub 1.5—3 m tall. Leaves alternate, opposite, 
or pseudo-verticillate, elliptic-oblong, bro adly 
elliptic to LAO roune truncate, 
or obtuse р uneately acute 
to cud at base, 2.5-11 cm rd ¥ cm wi 
midrib subelevated below, finely impressed 
above; petioles 1-8 mm long. Inflorescen Т 
minal, sessile, epedunculate, M 
branched with 3—9 strongly ascending, candela- 
bra-like axes 2-6 cm long, 2-5 mm thick, the 
rachis 1-2 mm thick, dic flowered from base 


to apex. Floral bracts triangular-lanceolate Vm 


all ссе аї си 2 21 mm long, fe 
wide at apex. Fruit brown, rugulose, immat 2 
subglobose-pyriform, 6-11 mm long, 6-118 
broad 

Distribution: dwarf forest and rocky o: 
on sandstone mesetas of the Venezuelan е 
yana іп Territorio Federal Amazonas aes al- 
Duida) and Estado Bolivar (Sarisarinama) а 
titudes of 1,250-1,400 m. 

BOLIVA ar: Cerro 

Specimens examined. porción noreste, 4°41 ‘ae 

64?13'20"W, 1.41 Om “10 Feb. 1974, 5 


С, 
refio & Brewer-Carías 108902 (УЕМ); 14 “14 Feb. 


——— s 


К 


~ 


—ÁA 


~ 


a 


a= amma 


— —— _ — 


1984] STEYERMARK— VENEZUELAN GUAYANA 321 


Ficure 8. Perissocarpa steyermarkii subsp. tachirensis.—A. Habit of branch with inflorescence and infruc- 


ce.—B. Flower in late bud.—C. Flower, late anthesis, natural position.—D, = Stamen.—F. Pistil.—G. 
Cross-section of ovary.—H. Calyx dorsal view.—I. Seed, dorsal vi ew.—J. пега, * ntral ме“. – К. Corolla in 
vud. —L. Cal lobe, i interior view howi te appendage. — M. Calyx lobe, a bêar view.—N. Petal, lateral 


view.—Q, Petal, ventral vi 


322 


Steyermark, Liesner & Brewer-Carias 124300 (VEN). 
AMAZONAS: Cerro Sipapo (Paraque), lower Caño Negro, 
1,400 m, 11 Jan. 1949, Maguire & Politi 28091-A (NY, 
VEN); Cerro Duida, between rim and camp, occasional 
along ridge trail from Culebra, Río Cunucunuma, 1,400 
m, 18 Nov. 1950, Maguire, ae & Wurdack 29529 
Neer see VEN: isotype, rriba de la Culebra, 
1,250 m, Oct. 1983, Colonnello 738 (VEN). 


Tyleria breweriana Steyerm., sp. nov. TYPE: 
enezuela. Bolívar: Sucre, Meseta de Jaua, 
cumbre, sección oriental-central, aflora- 
mientos de piedra arenisca en sitios ex- 
puestos con vegetación herbacea y arbustos 
achaparrados, 4?35'N, 64%15 У, 2,020 m, 

14 Feb. 1981, Steyermark, Brewer-Carías & 
Liesner 124326 (holotype, VEN). Figure 9. 


Frutex 1-1.5 m altus glaberrimus, ramis ics 3- 
3.5mm diam.; ; foliis petiolatis, petiolis 1.5—2 cm 


volutis caducis; laminis чле eee icis longiaris statis, 
arista 4-8 mm longa, bas eatim dec ntibus 4— 
5 ст longis 1.7-2.2 ст ж ane PU wis con- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


fertimque adpresso-serrulatis glabris; inflorescentia 
erecta, 5-flora 3 cm longa; calyce quincunciali, sepalis 
5, ovato- arido apice obtusis vel rotundatis 7 mm 
longis 3-4 mm latis; petalis albis ad centrum flavis 5 
obovato-oblongis 15 mm longis 10 mm latis. 


Tyleria breweriana belongs to the aristate- 
leaved group of species represented by 7. aris- 
tata, T. pendula, and T. tremuloidea of Cerro de 
la Neblina of Venezuela and T. silvana of adja- 
cent Brazilian Serra Pirapucü. It appears most 
closely related to 7. pendula Maguire & Wurd., 
from which it differs in its erect, few-flowered, 

shorter "or shorter, broadly elliptic leaf 
blades, and shorter petioles. 

This is the Rer species of Tyleria to be re- 
corded from the Meseta de Jaua, the first being 
T. phelpsiana Maguire & Steyerm. (in Steyer- 
mark et al., 1972: 868. fig. 9), a species of quite 
different leaf morphology of the group related to 
T. floribunda and T. spathulata of Cerro Duida. 

The following key is presented to indicate the 
position of T. breweriana with respect to the oth- 
er known members of the aristate-leaved group. 


KEY TO THE SPECIES OF TYLERIA 


1. Leaves sessile; petals 15—20 cm long, rose or pin 


T зрела 


1. Leaves petiolate; 
2. Sepals acute to subacute at apex 


nk 
petals 4 cm or less long, white or white with yellow at base „uum ‚= 


3. Sepals glandular-scarious at apex; arista of leaf blade 16-22 mm long Õu- 
3. Sepals non-glandular at apex; arista of leaf-blade 5-8 mm long NM AD 
4. Flowers solitary; petals 1.6-1.8 cm long, 0.8-1 cm wide; petiole 3—5 mm long; TE «i 

g 


mm ion 


= 


12-15 mm lon 


T петина 


м 


Sepals obtuse to rounded а 


Flowers 2—4, racemose; petals 2.5-4 cm long, 1.8-3 cm wide; petiole 1.2-1.8 cm long; pedicel 
long 


petiole 2—4 


apex 
5. Inflorescence pendulous, many-flowered, 10—15 cm long; leaf blades 7—11 cm long, oblanceolate: | ja 


. T. breweriana 


5. рен a 5-flowered, 3 cm long; leaf blades 4–5 cm long, broadly elliptic; petiole 1. fa 
4c 


NOTES ON ADENANTHE BICARPELLATA 


This monotypic genus, endemic to the summit 
of the Chimantá Massif, Estado Bolívar, of the 
Venezuelan Guayana, shows quantitative vari- 
ation in both vegetative and floral characters. A 
recent collection from the summit of the Macizo 
de Chimantá (Steyermark, Huber & Carreño 
128637) manifests maximum extremes of mea- 
surements. The plants noted here grew in dense 
thickets of moist forest along a small stream on 
Amuri-tepui, one of the sectors of Chimantá 
Massif. In such forested habitats plants of Ad- 


: : ith 
enanthe attain a height of 5 m as contre 
a usual height of 1-2 m. Correlated wit 
greater size of the plants are larger ee 

ules, and fruits, as well as an increase 1 
= degree 
the 
of branching of the inflorescence an 
lateral axes branched from the base; 
the inflorescence is unbranched. 


These quantitative differences may be apP в 
uremen 


quie val 
taken from collections originating from the u$ 


: on 
open or savanna-like habitats of the эрес 
Chimantá Massif with those from the wet ® 


m --"— may 


1984] 


STEYERMARK— VENEZUELAN GUAYANA 323 


Open or savanna-like habitats 


Petals 1.5 cm by 0.8-1 cm 

Sepals 5-8 mm long 

Anthers 3.5-4 mm long 

Stipules 8-10 mm by 7 mm 

Leaves 2.5-4.5 cm by 1-2 cm 
Inflorescence 5-15 cm by 5—6 cm 
Inflorescence bears 7-10 lateral axes 
Lateral axes usually unbranched 
Inflorescence 17-22-flowered 
Capsule 8-14 mm 


Collection of Steyermark, Huber & Carreño 
128637 from wet forest 

2.3 cm by 1.3 cm 

8-12 mm long 

4—6 mm long 

20-27 mm by 8-15 mm 

10-13 cm by 3-4 cm 

15–22.5 cm by 7 cm 

Inflorescence bears 10-12 lateral axes 

Lateral axes branche 

Inflorescence up to 50-flowered 

Capsule 16-18 mm long 


Such differences, at first glance, might indicate 
that the collection of Steyermark, Huber & Car- 
reno 128637 merits some taxonomic recogni- 
tion. However, most of these apparent differ- 
ences break down when other specimens 
originally included in the type description of this 
taxon (Maguire et al., 1961, fig. 27: А; B) are 
examined. In only two characters, i.e., the much 
larger stipules and the larger capsules. does the 
Steyermark et al. 128637 collection manifest any 
noteworthy contrast. Such contrasts may be the 
result of development in the more shaded and 
moister forest habitat instead of the more ex- 

sed, often drier ambience under which A. bi- 
carpellata usually occurs. Pending future obser- 
vations and a more intensive study ofthe different 
habitats in which this species occurs, no separate 


епатће. 


THEACEAE (BONNETIACEAE) 


Acopanea Steyerm., gen. nov. TYPE: A. ahogadoi. 
Steyerm. 


a а, demissus. Folia basalia rosulata ut videtur 
ls а n Sicco multi parallelo-pinnato-nervia. Cau- 
. orter simplex reptans radicans horizontalis vel 
€cumbens bracteatus. Bracteae foliosae sub- 


um 3-loculare, placentatione ax 
mi 
~ чуо 3 3-partito. Capsula крш Semina li- 
oblonga 1-3 anguste alata 
R А i i a 
Maceo €d to Acopán-tepui of the Chimanta 
Si! of southeastern Venezuelan Guayana. 


+ ahogadoi Steyerm., sp. nov. ТҮРЕ: 
*nezuela. Bolívar: Piar, Macizo del Chi- 


mantá, sector SEE, altiplanicie suroriental 


г 
62°00'W, 1,920 т, 14—16 Feb. 1984, Stey- 
ermark, Luteyn & Huber 129924 (holotype, 
VEN; isotype, NY). PARATYPE: same locality 
and date, Huber, Steyermark & Luteyn 9023 
(VEN, NY). Figure 10. 

Planta pusilla, ares brevi ligneo 2-11 cm longo l- 
2 cm crass 


apice subobtusis vel obtuse acutis basi paullo angus- 
tatis, 4.5-8.5 cm longi latis, subtiliter pa- 
ralleloneuris infra medium аесуз, рга 


1pue 

superioribus minute ciliolato-serrulatis‏ و 

glanduliferi vel infra 

rosulam ahora exorienti, = cries reptanti 

radicanti simplici vel semel ramoso 55-70 cm lo 
iu 


bracteis foliosis instru 

latis vel lanceolatis acutis vel subacutis coriaceis 1 

7 cm distantibus 1-2(-3) cm longis ме 2 mm tis 
mm lon 

Г. 52 mm latis; bracteolis 3 naviculatis ad и 
obtuse carinatis ligulatis vel lineari-lanceolatis apice 
abrupte пева cuspidatis 4.5-5 mm longis 1.2-1.3 
mm latis dentibus 1—2-setulosis adscendentibus in- 
structis; еген» vinaceo-rubris vel pegy exte- 
rioribus duobus ovatis acuminatis 7 mm mm, ce- 
teris late ети 7.5 mm х 3. 5-4 mm, 
fructiferis 20-25 m و‎ mm; petalis albidis го- 


subtrun catis - versus angustatis 10-13 mm kasis 
supra mediu –16 mm latis basi 2 mm latis; sta- 
minibus numerosis filamentis albidis 1.5-2.5 mm lon- 
gis basalite ranam 1.5 mm longam affixis; 
antheris aureis is suborbicularibus 0. 7-0.8 mm longis 0.8 
ideo 3-3.5 mm x 


breviter fimbrillatis; capsula са 


ovidea 2–2.2 cm x 1–1.2 ст 
2-3 mm m crasso; seminibus nigusie oblongis una ex- 
1:5 


324 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


FIGURE 9. Tyleria breweriana.— A. Нађи of flowering branch.—B. Petal.—C. Outer i: _—D. Inner sepal. 
U т half sl 1 1 is fut 1 half a1 : p е АД: Учу | 


. Uppe 8 | 
with 5 зтаПег. — Е. Stamen.—G. Pistil. 


mm x 0.5 mm 1-3 anguste porcatis vel alatis, pagina 
minute punctata. 


This unusual species is dedicated to Antonio 
Ahogado, who is chief of the planning program 
for the Electrification of the Caroni river basin 
of the state of Bolívar in Venezuela, the admin- 


arger ones alternating 


o 


istration known as EDELCA. Through the e 
of Mr. Ahogado, the expedition to Acopan- 
was made possible. 

This genus is characterized by th 
rooting, unbranched inflorescence on 
gated axis and the 1-ѕегіаіе monadelphous 


e trailing and 
an elon- 
fila- 


1984] 


ZM 


FIGURE 10. Acopanea ahogadoi.—A. 
dorsal —F. Androecium 
of onte I. Septi 
With persistent columella and adherent seeds.— 


ments attached to a basal membrane. The trail- 
ing, rooting, unbranched inflorescence is 
unknown elsewhere in the family and immedi- 
ately distinguishes the genus from any of its con- 


15 congeners are noted as follows: 

Mane bracteoles. These are found in Neb- 
йин some species of Воппепа. ! 

Кр peduncle or pedicel. Present in both 

pes ЕС and Neotatea, and some species of 


lags Wenation. Neogleasonia and Neblinaria 


Ciliolate upper margins of the wane These 


cidal capsule at ар А of свака —J. 
K. Seeds, various positions. 


STEYERMARK — VENEZUELAN GUAYANA 325 


Habit. — B. Leaf showing parallel and pinnate venation. —C. Flower in 
natural ioci with single bract subtending 3 bracteoles. — D. Inner sepal, dorsally cuspida 
F and gyn i 


Showing two valves of the dehiscent capsule 


are to be noted in some specimens of Neoglea- 
sonia. 

Leaf scars. Located on the thickened stem 
below the leaf rosette of the new genus, they like- 


flowers in each bract is not duplicated elsewhere 
in the family. The attachment of the 1-seriate 
monadelphous filaments to a basal membrane 
may be considered as approaching the penta- 
delphous stamens of Archytaea and sets it apart 
from Bonnetia, Neblinaria, Neotatea, and Neo- 
gleasonia. On the other hand, the 3-celled ovary 
with axile geminate placentation, septicidal cap- 
sule with persistent columella, the narrowly 
winged seeds, numerous stamens and sessile or 
subsessile, alternate, densely crowded, rosulate 


326 


leaves are common to its closest congeners of 
Neblinaria, Neogleasonia, Neotatea, and Archy- 
taea. 


NOTES ON BONNETIA 


In his treatment of Bonnetia for the flora of 
the Guayana Highland Maguire (in Maguire et 
al., 1972: 139-154) has identified certain collec- 
pei with B. wurdackii Maguire and B. tepuien- 
upon further 
study, supplemented by newly made field obser- 
vations and collections, reveal the existence of 
three new species and one variety. They are de- 
scribed below. 


Bonnetia chimantensis Steyerm., sp. nov. TYPE: 
Venezuela. Bolivar: Chimanta Massif, To- 
rono-tepui, savanna below summit of W es- 
carpment, 2,090 m, 9 Feb. 1955, Steyer- 
mark & Wurdack 680 (holotype, VEN; 
isotypes, F, NY). 

rutex 1-metralis; foliis d 
lipticis vel oblongo-ellipticis apice aea basi obtusis 
mm x 5-8 mm; stylis 3-partiti 


lati shih 1 


Leaves rigidly coriaceous, elliptic ог oblong- 
elliptic, acute at apex, slightly narrowed to an 
obtuse base, sessile, 12—27 mm by 5-8 mm, pin- 
nately nerved below, enervate above; flowers 3 
at the apex, pedicellate; pedicels 4 mm by 1.5 


oblong-obovate, rounded at apex, narrowed to 
the base, 9—9.5 mm by 4-6 mm; stamens nu- 
merous, filaments fascicled, free, 1.5-2 mm long; 
pistil 5.5 mm long, ovary 3.5 mm by 2.5 mm, 
styles 3, distinct, 2 mm long. 


This species differs from B. tepuiensis Kobuski 
& Steyerm., with which it was identified by Ma- 
guire in having the style 3-parted, leaves nar- 
rowed to an acute, non-retuse apex, obtuse and 
not rounded base, leaves smaller, elliptic or ob- 
long-elliptic instead of broadly ovate or oblong, 


1 


and shorter filaments. 


Bonnetia huberiana Steyerm., sp. nov. ТҮРЕ: 
Venezuela. Bolívar: Chimantá Massif, To- 
rono-tepui, summit at edge of escarpment 
in and among zanjones, 2,165-2,180 m, 9 
Feb. 1955, Steyermark & Wurdack 633 (ho- 
lotype, VEN; isotypes, F, NY; US 
PARATYPES: Venezuela. Bolívar: Chimantá 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


Massif, E section of Chimantá-tepui, 5°18'N, 
62°03'W, 2,450-2,500 m, 9 Feb. 1983, Stey- 
ermark, Huber & Carrefio 128973 (VEN); 
Amurí-tepui, 5?10'N, 62?07'W, 3 Feb. 1983, 
Steyermark, Huber & Carreño 128559 
(VEN); Acopán-tepui, NW portion, highly 
eroded sandstone strata around zanjones, 
1,960 m, 16 Feb. 1984, Steyermark, Luteyn 
& Huber 129991 (VEN). 


Frutex 1.5-2.5-metralis; foliis ener, pe 
lanceolatis apice subacutis 10—2 5-7 m 
Marginibus superioribus emao ИЦ am 
tibus duobus minutis adpressis in quoque 1 mm mun- 
itis; floribus solitariis; petalis luteis flabelliformibus 8 
mm longis supra medium 7 mm latis basi 2 mm; stylis 
tribus 1.8-2.5 mm longis usque ad basem divisis. 


Leaves sessile to subpetiolate 1 mm long, as- 
cending to spreading, coriaceous Or subcoria- 
ceous with the margins thinner, concolorous or 
slightly paler green below, linear-oblanceolate, 
subacute at apex, gradually narrowed to the base, 

10-26 mm long, 2.5-7 mm wide, upper margins 
subspinulose- Lenis with 2 minute appressed 
teeth to every 1 mm; flowers solitary, fruiting 
pedicels terete, 8-16 mm long; bracts sepaloid, 
closely subtending calyx, oblanceolate; petals 
yellow, flabelliform, rounded at apex, 7 mm wide 
above middle, 2 mm wide at base; stamens nu- 
merous, multiseriate, filaments free, 0.5-1.5 m 
long, anthers subreniform 0.6 mm by 0. 2-0.3 
mm; styles 3, subulate 1.8-2.5 mm long, divided 
to the base; capsule 8.5 mm long. 


This species was originally identified |: Ma- 
guire (in Maguire et al., 1972: 148) as В. wur 
dackii. п differs from that species in the smaller 
petals, narrowly linear-oblanceolate, subacute 
leaves with subspinulose appressed teeth on the 
leaf margins. It is related to B. roraimae Oliver 
from which it is distinguished by the yellow pet 
als and concolorous yellow-green leaves. ar 
guire employed the character of the leaf-margin 
as one of his criteria in differentiating 8. тога 
. roraimae 
being described as “ѕсагіо-ѕріпшоѕе Ae 
wurdackii as “narrowly scarious, feebly ог 10 
all spinulose." The leaf margins of B. теа 
those of В. а pas new taxon resembling 
more those of B. wurdackii. 


: bsp- 
Bonnetia tepuiensis Kobuski & Steyerm. и 
minor Steyerm., subsp. nov. ТҮРЕ: we 

la. Bolívar: Chimantá Massif, Bo 


oP ZUR QUIS Е а 


~~ 


~ > 


mm 


—— ү 


— 
4 


—— 


1984] 


thicket along upper part of branch tributary 
to Cano Mojado, E of N escarpment of To- 
rono-tepui, 1,975 m, 20 Feb. 1955, Stey- 
ermark & Wurdack 990 (holotype, VEN; is- 
otypes, F, NY, US). PARATYPES: Venezuela. 
Bolívar: Chimantá Massif, Río Tirica above 
middle falls below summit camp, central 
section, summit, 1,863 m, 5 Feb. 1955, 
Steyermark & Wurdack 481 (F, NY, VEN). 


A B. tepuiensis foliis minoribus 1-2 cm longis 0.8- 
1.4 cm latis nervis subtus desunt supra inconspicuis 
vel desunt; sepalis dorsaliter carinatis recedit. 


Shrub to small tree 1—4 m; leaves spreading, 
ovate, obtuse, obtusish or retuse at apex, nar- 
rowed to a rounded or obtuse base, 1-2 cm long, 
0.8-1.4 cm wide, nerves below not evident, faint- 
ly impressed above, margins thin-scarious with 
deciduous dark cilia, the bases of which often 
persist; flowers solitary, sessile; flowers sessile, 
Solitary; sepals dorsally keeled, the outer broadly 
Ovate, acute, or cucullately incurved, subobtuse 
ventrally (when viewed dorsally), 8-10 mm by 

mm, the inner sepals suborbicular, abruptly 
acute, 6 mm by 5 mm; petals white with pink 
Margins, obovate, abruptly mucronate at apex, 
10 mm by 4.5-5 mm; stamens fasciculate in sep- 
arate phalanges, filaments 2-2.5 mm long; pistil 
5 mm long, style undivided, 2 mm long. 


Bonnetia tepuiensis was described (Kobuski, 
1948: 399) from specimens collected by Steyer- 
mark from the slopes of Carrao-tepui of Estado 
Bolivar. The leaves on the type (Steyermark 
2 and paratype (60902) are 2-2.8 cm by 
jian cm and the sepals are dorsally convex 
nei keeled. Subsequent collections show 
ps a to 6.5 cm by 3 cm. The lateral nerves 
boni iud of subsp. tepuiensis are impressed on 
diis aces being inconspicuous to scarcely 

anilest on the lower surface and more con- 
SPICuous on the upper surface. 

E i subsp. minor the leaves are smaller, and 
фи 9 With nerves scarcely evident on the 
ат к and absent or essentially so on the 
dip ТЕ ES while the sepals are dorsally car- 
ds hss own specimens of the subsp. minor 
Mar ue to the summit of the Chimantá 
uq А €reas subsp. tepuiensis occurs farther 
Ven St in the Venezuelan Guayana in Cerro 
ато, Iu-tepui and Ptari-tepui. 


v toronoensis Steyerm., sp. nov. TYPE: 
: enezuela. Bolívar: Chimantá Massif, To- 
9no-tepui: dryish open savanna, N-facing 


STEYERMARK — VENEZUELAN GUAYANA 


327 


slopes, summit above valley of Cano Mo- 
jado, 2,030-2,150 m, 21 Feb. 1955, Stey- 
ermark & Wurdack 1047 (holotype, VEN; 
isotypes, F, NY, US). 
rutex 1.5-2-metralis; foliis conferte imbricatis ob- 
longo-lanceolatis apice subacutis vel acutis basi leviter 
angustatis obtuse 1.7-3.1 cm by 0.7-1.3 cm subtus 
valde pinnatinervatis nervis elevatis supra impressi- 
dA : nen api и. 


palis ovato-oblongis obtusis vel rotundatis 8-9 mm x 

; petalis rosaceis subdeltoideo-obovatis 11—12 
longis apicem versus 9-10 mm latis; stylo partim 
3-partilo. 

Leaves deep green above, pale yellow-green 
below with wine-red margins, sessile, closely im- 
bricate, spreading to ascending, coriaceous, ob- 
ong-lanceolate, subacute to acute at apex, slight- 
ly narrowed to an obtuse base, 1.7–3.1 cm by 
0.7-1.3 cm, strongly nerved below with fine el- 
evated nerves, less 1 inently impressed nerved 
above, lateral nerves 9—12 each side, anasto- 
mosing with less prominent tertiary veins, mar- 
gins finely and closely denticulate with slender 
setulose teeth ca. 10 to each 5 mm of margin; 
sepals unequal, ovate-oblong, obtuse or rounded 
at apex, minutely denticulate around apex, con- 
vex dorsally, 8-9 mm by 4—5 mm; petals pink, 
subdeltoid-obovate, subtruncate at apex, nar- 
rowed to base, 11—12 mm long, 9-10 mm wide 
near apex, 2.5 mm wide at base; style 3-parted 
one-third distance from the top. 


— 


In the size and close imbrication of the leaves, 
this species resembles B. tepuiensis subsp. minor 
but is distinguished from that subspecies by the 
3-parted instead of entire style. The prominently 
nerved lower leaf surface is also in marked con- 
trast to the enervate lower surface of the leaves 
of B. tepuiensis subsp. minor. Additionally, the 
sepals of B. toronoensis are obtuse to rounded at 
the apex and the leaf apex is subacute to acute. 


NOTES ON SOME GENERA OF THE 
THEACEAE (BONNETIACEAE) 


In his key to the genera of the Bonnetiaceae, 
a family which Maguire (in Maguire et al., 1 : 
131-165) recognized as distinct from the Thea- 
ceae, the distinction is drawn between Bonnetia 
on the one hand, and Neblinaria, Neogleasonia, 
and Neotatea on the other, primarily on the basis 
of the leaf venation and secondarily on whether 
the flowers are solitary and axillary or “solitary 
or the inflorescence variously compound." As 
regards the character of the venation, the leaves 
are stated to be “pinnately veined” in the case 


328 


of Bonnetia and “closely parallel-nerved 
(veined)" for Neblinaria, Neogleasonia, and 
Neotatea 

In an attempt to apply this distinction to the 
various taxa within the genera above treated, one 
encounters difficulties in separating one group 
from another. For example, Neotatea obviously 
has closely parallel nerves but at the same time 
they are pinnately arranged. Bonnetia lanceifolia 
has leaves scarcely or inconspicuously nerved, 
difficult to classify. Neogleasonia duidae has fine- 
ly nerved leaves both pinnately nerved as well 
as closely parallel and strongly simulate those of 
Neotatea longifolia, the major difference in ve- 
nation being that the angle of the nerves with 
respect to the midnerve is greater in Neoglea- 
sonia duidae. In their original diagnosis Kobuski 
and Steyermark (in Kobuski, 1948: 411) de- 
scribed the leaves of Bonnetia duidae (basionym 
of Neogleasonia duidae) as having the “veins la- 
teralibus numerosis, proximis (ca. 20 per cm), 
parallelibus, subangulo acutissimo adscendenti- 
bus." This character influenced Maguire to trans- 
fer this species to the genus Neogleasonia, al- 
though its placement in that genus he considered 
at the time to be tentative (Fig. 11) 

With respect to the genera Neblinaria and Neo- 
gleasonia having "closely parallel-nerved 
(veined)" leaves, it should be stressed that al- 
though the nerves are closely parallel, yet they 
emerge at various higher levels from the central 
zone of the leaf in Neogleasonia than in Nebli- 
naria, those of the latter genus having nearly all 
of the parallel nerves arising at or close to the 
leaf base, whereas in Neogleasonia the upper- 
most nerves, although parallel to the others, arise 
pinnately and ascend strongly from 1.5-3 cm 
above the base of the leaf. In Neogleasonia a 
midnerve is more evident on the lower leaf sur- 
face, whereas in Meno scarcely any mid- 
nerve is developed (Fig. 1 

So far as the parallel mes venation is con- 
cerned, there is little to separate Neblinaria from 
Neogleasonia. So far as characters used to sep- 
arate Neblinaria from Neogleasonia and Neo- 
tatea, we are informed (Maguire et al. , 1972) that 
in Neblinaria the “peduncles” аге "strongly an- 
cipitous and oe ше leaves; bracts gom 
spicuous, whorled, s 
subtending a ш, pedicel; ا ا‎ 
let,” w 


ing; nonpachycaulous shrubs or small trees." 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


The importance attached to the character of 
the peduncle as terete or ancipital in differen- 
tiating the above three genera would appear to 
be weak and inconsistent in view of the fact that 
in his key to the species of Bonnetia Maguire (in 
Maguire et al., 1972: 139) divides the various 
taxa into those with ancipital peduncles as con- 
trasted with ones having terete peduncles. Also, 
among the species of Bonnetia, are some, such 
as B. stricta and B. cubensis, with whorled con- 
spicuous bracts as in Neblinaria, and others, such 
as B. paniculata, B. celiae, and B. kathleenae, 
with inconspicuous bracts as in Neogleasonia and 
Neotatea. 

Finally, the importance of the pachycaulous 
character of Neblinaria versus the nonpachycau- 
lous Neogleasonia and Neotatea may be judg 
as relatively very weak in distinguishing these 
са bias НЕР соу de present in à 

n Neblinaria, may 
be viewed : as having evo as a response 10 
particular environmental conditions. Instances 
of corky pachycaulous stems are found in many 
species of plants, such as in the cork oak, Quercus 
suber, Gnetum schwackeanum, species of Cissus, 
and many others, but such species are not Con- 
sidered generically distinct because of such a de- 
velopment. In Neogleasonia wurdackii a rela- 
tively thick or pachycaulous stem is develo 
but does not possess the corky nature seen " 
Neblinaria. Actually, the pachycaulous stems 0 
Neblinaria do not possess a woody resistance as 
in a true shrub or tree, but quickly snap off or 
break when knocked or brushed against. More 
over, those who have collected Neogleasonia 
wurdackii and Neotatea testify that their stems 
may be termed pachycaulous as in Neblinaria. 

In view of the fact that the various Me 
by Maguire to differentiate Bonnetia from 
linaria, Neogleasonia, and Neotatea писте 
in such characters as leaf venation, ancipital 
sus terete peduncles, whorled peo ке the 
contrasted with inconspicuous bra val 
degree of pachycauly, it is айай t p 0 
criteria cannot be maintained. Могеоуег, Ee 
above genera share the same basic floral је“ 
phology, such as а 3- rarely 4-celled оу и 
placentation with numerous caf 
ovules, geminate placentae, mainly 4-cell 


r, vegetatively they 
exstipulate leaves. Only the lactiferou 
Neotatea may be considered as a strong 


OO a 


1984] STEYERMARK— VENEZUELAN GUAYANA 


A 


329 


о 
ص‎ 


FIGURE 11, Leaf nervation.—A. Neblinaria celiae.—B. Neogleasonia wurdackii.—C. Neotatea longifolia.— 


. Neogleasonia duidae 


330 


character of sufficient significance to warrant its 
separation from Neblinaria, Neogleasonia, and 
Bonnetia. Historically, we may note that many 
specimens earlier determined by Maguire as per- 
taining to the genus Bonnetia were later trans- 
ferred by him to Neogleasonia and Neotatea. 
The following nomenclatural changes are nec- 
essary as a result of the above conclusions: 


Bonnetia maguireorum Steyerm., nom. nov. 
Neblinaria celiae Maguire, Mem. New York 
Bot. Gard. 23: 157. 1972 non Bonnetia ce- 
liae Maguire, Mem. New York Bot. Gard. 
23: 143. 1972. 


Bonnetia multinervia (Maguire) Steyerm., comb. 
nov. Neogleasonia multinervia Maguire, 
Mem. New York Bot. Gard. 23: 158. 1972. 
Neogleasonia wurdackii Maguire, Mem. New 
York Bot. Gard. 23: 160. 1972 non Bonnetia 
wurdackii Maguire, Mem. New York Bot. 
Gard. 23: 147. 1972 


It is not possible to retain Neogleasonia mul- 
tinervia and Neogleasonia wurdackii as distinct 
taxa. Both species show ciliation of the leaves, 
one of the characters used in the separation of 
the two taxa, the youngest upper ones of a rosette 
often having ciliation in the upper half or near 
the apex, whereas the lower margins or older 
leaves are eciliate. Maguire’s description of the 
leaves of Neogleasonia multinervia as “‘lanceo- 
late” was based on a single collection, as opposed 
to “ovate, sublanceolate, oblanceolate” for N. 
wurdackii based on many collections. However, 
comparison of many collections of N. wurdackii 
with the isotype of N. multinervia (Maguire 
33329) show little, if any, difference in leaf shape; 
those of N. wurdackii have leaves on the older 
lower portion of the rosette becoming sublan- 
ceolate, while the young new leaves ofthe rosette 
tend to be more ovate. Another character em- 
ployed by Maguire for differentiating the two taxa 
was that of petal length “petals 3 cm long, showy” 
in N. wurdackii. This character is found to in- 
t d dditional collecti fi Chimantá 


Massif have become available. 


Bonnetia neblinensis Steyerm., nom. nov. Neo- 
tatea neblinae Maguire, Mem. New York 
Bot. Gard. 23: 163. 1972 non Bonnetia neb- 
linae Maguire, Mem. New York Bot. Gard. 
23: 148. fig. 23. 1972. 

Bonnetia colombiana (Maguire) Steyerm., comb. 
nov. Neotatea colombiana Maguire, Mem. 
New York Bot. Gard. 23: 164. 1972. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


| MYRTACEAE 

Calycolpus calophyllus (H.B.K.) Berg var. an- 
gustifolius Steyerm., var. nov. TYPE: Vene- 
zuela. Amazonas: Atabapo, Salto Matushi, 


de Culebra, 3?43'N, 65?40'W, 220 m, 5 Apr. 
1983, Steyermark & Delascio 129391 (ho- 
lotype, VEN). 


A C. calophyllus foliis anguste lanceolato-ellipticis 
e tt + z rei! 2 fic 5.0 em longis 


i21 cm latis 4—5-plo longioribus quam latioribus re- 
cedit. 


Calycolpus calophyllus is a shrub or small tree 
ofthe Territorio Federal Amazonas of Venezuela 
with leaves ovate to elliptic-ovate, abruptly short- 
acuminate or obtusely acute at apex, 2-4 cm 
wide, and generally 1.5-2.5 times longer than 
broad. 


Myrcia bonnetiasylvestris (Steyerm.) Steyerm., 
comb. nov. Gomidesia bonnetiasylvestris 
Steyerm., Fieldiana, Bot. 28(3): 1016. 1957. 


Recent collections from Chimantá Massif in- 
dicate that this taxon should be placed more log- 
ically in the genus Myrcia. A more detailed ex- 
amination of the anthers indicates a 2-locular 
instead of 4-locular condition. The calyx lobes 
were described in the original publication as sub- 
orbicular and rounded but a re-examination of 
the type collection as well as newly collected, 
more mature specimens, reveals that the calyx 
lobes are ovate-lanceolate and acute. I am 1 
debted to Dr. Landrum for his observations and 
kind suggestions. 


Specimens examined. | VENEZU 
mantá Massif, Chimantá-tepui, sec 


Carrefio 128756; Chimantá-tepui, E secto Huber 
62°03’W, 2,450 m, 7 Feb. 1983, Steyermark, 
Carrefio 128885. 


RUBIACEAE 


erm. 
Aphanocarpus steyermarkii (Standley) Stey 
phan = у ese un 


hr rew- 
Steyermark, Carreño, McDiarmid & B 


er-Carías 115968 (holotype, VEN). 


1984] 


A A. steyermarkii foliis subtus glabris vel glabre- 
scentibus recedit. 

Aphanocarpus steyermarkii, known from the 
Gran Sabana and sandstone slopes and summits 
of a few of the eastern tepuis (Auyan-tepui, Chi- 
manta-tepui, Ptari-tepui) of Estado Bolivar, has 
leaves densely gray-silvery sericeous pubescent 
on both upper and lower surfaces. The present 
collection of the species, newly recorded for 
Aprada-tepui, has the lower leaf surface glabrous 
or nearly so. Some of the youngest leaves may 
exhibit traces of pubescence on the midrib or 
surface, but are generally glabrescent or glabrous. 
A collection from Auyan-tepui (Steyermark et 
al. 116000) has the lower leaf surface only sparse- 
ly to moderately sericeous-pubescent, but not 
glabrous throughout as in the case of A. glabrior. 


Aphanocarpus steyermarkii f. elongatus Stey- 
rm., f. nov. ТҮРЕ: Venezuela. Bolivar: Piar, 


del Chimantá-tepui, cabeceras orientales del 
Cano Chimantá, 5*1 8'N, 62?09'N, 2,000 m, 
26-29 Jan. 1983, Huber & Steyermark 6945 
(holotype, VEN). PARATYPE: same locality 
and date, Steyermark, Huber & Carrefio 
128188 (VEN). 
и Ал. steyermarkii pedunculis 9-13 cm longis pro- 
© 1n- 


volucri bracteis foliosis usque 10-17 mm longis. 


Collections of this endemic species of the Ven- 
&zuelan Guayana generally have simple mono- 
cephalous peduncles 1.3-5(-7) ст long. On a 


= €xpedition to the summit of the Chimantá 


t 3 
un one head of flowers with an elongated pro- 
ne Ог axis which terminates in an addi- 


NOTES ON PSYCHOTRIA CRASSA BENTH. 


et е crassa Benth. is a characteristic 
ойл ~ to subscandent shrub of wet forests 
ho ummits and upper slope forests of the 

Stone table mountains throughout the Ven- 


STEYERMARK — VENEZUELAN GUAYANA 


331 


ezuelan Guayana and adjacent northern Brazil. 
Throughout this range it exhibits some variation 
in leaf size and shape. Generally the leaf blades 
vary from ovate or elliptic-obovate to broadly 
oblong-elliptic and from 1.5-5 cm wide. More- 
over, the peduncle, axes of the inflorescence, and 
pedicels are red, the calyx and hypanthium often 
roseate or reddish, and the fruit dark red. 

Among the extensive collections of this species 
in the Herbario Nacional de Venezuela (VEN) 
are two variations of noteworthy comment. One 
is a narrow-leaved variation with leaf blades nar- 
rowly lanceolate or elliptic-lanceolate and 0.5- 
1.2 cm wide. The other variation departs from 
the usual coloration in having the peduncle, axes 
of the inflorescence, pedicels, calyx and hypan- 
thium, and fruit completely white. The varia- 
tions may be considered merely as taxonomic 
forms as follows: 


Psychotria crassa Benth. f. angustior Steyerm., 
. NOV. TYPE: Venezuela. Bolívar: Piar, Ma- 
cizo de Chimantá, sección oriental del Chi- 
mantá-tepui, cabeceras del afluente derecho 
superior del Río Tirica (“Cano del Grillo"), 
5°18’N, 62?03'W, 2,450 m, 7-9 Feb. 1983. 
Steyermark, Huber & Carrefio 128992 (ho- 


Feb. 1978, Steyer- 
mark, Carreño, McDiarmid & Brewer-Car- 
ias 115867 (VEN); altiplanicie en la base 
meridional de los farallones superiores del 
Apacara-tepui, sector norte del macizo, 
5920"М, 62°12'’W, 2,200 m, 30 Jan.-1 Feb. 
1983, Huber & Steyermark 7006 (VEN). 


A P. crassa foliorum laminis anguste lanceolatis vel 
elliptico-lanceolatis 0.5-1.2 cm latis recedit. 


Other collections which approach this form are 
i tá Massif (Steyermark, Huber & 
Carreño 127983, Huber & Steyermark 7128, 
Steyermark et al. 115768), from Ilá-tepui (De- 
lascio & Brewer-Carías 4954), from Kukenan- 
tepui (Delascio & Brewer-Carías 4910), from 
Roraima (Delascio & Brewer-Carías 4853, Stey- 
ermark, Brewer-Carías & Dunsterville 112450), 
and Ptari-tepui (Steyermark et al. 115704). 


Psychotria crassa f. alba Steyerm., f. nov. TYPE: 
Venezuela. Bolívar: Piar, Macizo de Chi- 
mantá, sector centro-noreste del Chimantá- 


tepui, cabeceras orientales del Caño Chi- 
manta, 5°18'N, 62?09"W, 2,000 m, 26-29 
Jan. 1983, Sept uber & Carreño 
128062 (holotype, VEN). 


P. crassa inflorescentiae pedunculis axibusque, 
pedicellis XE hypanthioque frutos albidis recedit. 


Remijia berryi Steyerm., sp. nov. TYPE: Vene- 
zuela. Amazonas: Estación Experimental de 
Santa Barbara del Orinoco, a 1-2 km al sur 
de Trapichote, 130 m, 26 Feb.-2 Mar. 1976, 
Berry & Chesney 2116 (holotype, VEN). 


Arbor 10-metralis, ramulis junioribus adpresso-pu- 
bescentibus; foliis ovatis, elliptico-ovatis vel lanceo- 


inferioram axillasque foliorum utrinque Tis; 
lateralibus utroque latere 11- 12; infructescentia tri- 
9-10cm 


longo sparsim pilosulo; ИН 1011: : mm x 5-7 mm 
tenuiter pubescentibus 


Tree 10 m, younger branches appressed-pu- 
bescent; leaves broadly ovate or elliptic-ovate to 
lanceolate or lance-elliptic, subacute at apex, cu- 
neately narrowed at base, 8-14 cm long, (2.5-) 
6.5-8.5 cm wide, glabrous on both sides except 
sparsely pilose along midrib and leaf axils below, 
lateral nerves 11-12 each side, divaricately as- 
cending at an angle of 30*; infructescence axil- 
lary, trichotomously branched, long peduncu- 
late, to 12 cm long (including peduncle), broader 
than long, 3.5-4 cm high, 4—7 cm broad, the 3 
main axes slender, 1.5-2.5 cm long, sparsely pi- 
lose; peduncle slender, 9—10 cm long, 2 mm wide, 
sparsely pilosulous; bract subtending base of in- 
fructescence lance-triangular, 1.5 mm long, pi- 
losulous; fruiting pedicels appressed-pilosulous; 
fruiting calyx and hypanthium 1.5-3 mm long, 
appressed-pilosulous without; fruiting calyx lobes 
ovate-lanceolate, subacute, 1.2-1.7 mm long, 0.5 
mm wide, appressed pilosulous without, gla- 
brous within; capsule oblong-elliptic, 10-15 mm 
by 5-7 mm, finely pubescent, dehiscent down- 
ward from apex; seeds fusiform, 6—8 mm by 1.5- 


This taxon is characterized by the relatively 
small leaves acute or subacute at both ends, their 
glabrity except for the sparsely pilose lower mid- 
rib and leaf-axils, the sparsely and finely pubes- 
cent upper branches, peduncles, and capsules, 
the slender elongated peduncles, and the rela- 
tively short infructescence. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


Remijia delascioi Steyerm., sp. nov. TYPE: Меп- 
cruel. Amazonas: Cerro Vin a 


N of Cerro Aratitiyope and SW of Осай | 
440 m, 1 Mar. 1984, Steyermark, Berry & 
Delascio 130339 (holotype, VEN). 


Planta lignea 1—1.5-metralis, caule simplici; folio- 
rum laminis lineari-ellipticis vel anguste lanceolato- 
ellipticis apice subobtusis basi acutis. 11-21 cm x Fs 

5 


supra glabris subtus praeter costam medium in 

em strigosam glabris, nervis lateralibus utroque latere 

n 15, petiolis 6-15 mm longis, pedunculo dense stri- 

о 6.5-9. x cm; calyce hypanthioque dense sericeo 6 

m, calycis tubo cylindrico spathaceo ob- 

scure sae ii dentato 4 mm longo; capsulis oblongo- 
cylindricis 12 mm x 5 mm strigillosis. 


Single-stemmed ligneous plant 1—1.5 mm tall; 
leaves petiolate, petioles tawny, 6-15 mm by ! 
mm, tomentose to glabrous above; leaf blades 
erect, pale yellow-green below with buff midrib, 
linear-elliptic to narrowly lance-elliptic, паг- 
rowed to a subobtuse apex, narrowed to an acute 
base, 11-21 cm by 1–2.5 cm, averaging 10 times 
longer than broad, glabrous above at maturity, 
glabrous below except for the subelevated stri- 
gose midrib, the youngest leaves sparsely strigose 
above on surface, densely strigose on midrib, 
moderately to densely strigose below on surface 
and midrib; lateral nerves 11-15 each side, a 
cending at an angle of 60*; tertiary venation finely 
reticulate beneath; inflorescence axillary, im- 
mature; peduncle densely strigose 6.5-9.5 cm long 
in fruiting stage; bracts brown-maroon, in Pre 
anthesis broadly lanceolate, obtusish, 6 mm у 
2 mm, sericeous without; 2 bracteoles a 
ing flowers lanceolate, ee 3.5 m it 
mm, densely sericeous without; calyx = y 
panthium brown-maroon, densely sericeous. : 
mm by 1.5 mm; calyx tube cylindrical, "e 
ceous, unequally and shallowly obscurely dé 
tate, glabrous within, 4 mm long, with scatter 


in fruit 4.5–9 cm long; ped oblong-cylindrie 


2 mm by 5 mm, strigillose 


This taxon differs from other known spe 
of the genus in the extremely narrow, poe је: 
liptic to narrowly Јапсе-е рис leaves which 
narrowed at both ends and only 1-2.5 cm e 
averaging 10 times longer than broad. em 
ture leaves are glabrous on both surfaces 
only the midrib beneath strigose. The SP? 


als — V——Q ^ umen :! —— 


1984] 


ceous calyx-tube is well developed with shallow, 
scarcely evident teeth at the summit. 


Sipanea carrenoi Steyerm., sp. nov. TYPE: Ven- 
ezuela. Bolívar: Gran Sabana, open densely 
covered slopes, al pie del Salto del Apon- 
guao, 42.5 km al NE de la Misión de Santa 
Teresita de Kavanayén, 1,130 m, 22 Feb. 
1978, Steyermark, Carrefo, Dunsterville & 
Dunsterville 115598 (holotype, VEN). 


Planta herbacea, caulibus prostratis vel decumben- 


о i. НЕ. = ы z а ht H 
vel subacutis 1-2 cm x 0.6–0.9 cm omnino glabris; 
nervis lateralibus utroque latere 2-3; inflorescentia ple- 
rumque 3—7-flora, raro l-flora; corolla 15-21 mm lon- 


Herbaceous 0.2 m; stems sprawling or trailing, 
densely or moderately pilose with subspreading- 
ascending hairs; stipules triangular-lanceolate, 2— 
3mm by 0.5 mm, densely strigose without; leaves 
short-petiolate, petioles 0.5-1.5 mm long, mar- 
gins pilose-ciliate; leaf blade elliptic-oblong, ob- 
tuse to subacute at apex, acutely narrowed to the 
base, 1-2 mm by 0.6-0.9 mm, glabrous both 
Sides, revolute on margins; lateral nerves 2-3 
cach side, lightly impressed on lower surface, not 
evident on upper surface; inflorescence terminal, 
rarely axillary, cymosely 3—7-flowered, rarely 
l-flowered, sessile or with short lateral branches; 
bract subtending inflorescence narrowly elliptic- 
oblanceolate, acute, 0.4 mm by 0.9 mm, ciliate; 
calyx 7-7.5 mm long, lobes 4.5 mm by 0.7-0.8 
mm, linear-lanceolate, acuminate, glabrous ex- 
cept for ciliate Margins; corolla hypocrateriform- 
infundibuliform, 15-21 mm long, tube 10-13 
hc long, зрагзеју pilose without in upper por- 
ee glabrous within except at orifice; orifice 

she had brush of hairs which 


pie: 6-6.5 mm by 5—7 mm, glabrous without; 
ers linear, 3-3.5 mm; style 10 mm long, gla- 


tary 

lobe, lan 
M mm, densely hirsutulous with ascending 
s This taxon is related to the common S. pra- 
Кану Aubl., from which it differs in the creeping 
di Ung habit ofthe stems and the densely crowd- 
ы glabrous, obtuse to subacute, fewer- 

€d leaves. The species is named in com- 


STEYERMARK— VENEZUELAN GUAYANA 


333 


memoration of my valued field assistant, Victor 
Carreno Espinosa. 


COMPOSITAE 


A re-examination of Achnopogon quelchioides 
Aristeg., based on Steyermark 93497 from Au- 
yan-tepui, shows that it cannot be separated from 
А. steyermarkii Aristeg., also from Auyan-tepui. 
Steyermark noted in his collection of A. quel- 
chioides that the flowers are “clustered as in 93496 
(Quelchia bracteata) but with larger size of flow- 
ers and leaf pubescence as in 93512 (A. steyer- 
markii)," leading to the supposition that it was 
a putative hybrid between these two collections. 

However, there appears to be no differences in 
separating A. quelchioides from A. steyermarkii, 
both having sessile, 2—3-flowered heads, white 
corollas, glabrate bracts in several series, sub- 
sessile to shortly petiolate, broadly oblong to ob- 
long-obovate leaf blades, rounded at the apex 
with a minute mucro, and densely lanulose, brown 
stems and leaf bases. 

Some collections of Achnopogon steyermarkii 
(Steyermark et al. 116088, 116139, and Foldats 
7117), all from the summit of Auyan-tepui, have 
been misidentified as Quelchia x grandifolia 
Maguire, Steyerm. & Wurd., considered by their 
authors to be a putative hybrid between Quelchia 
bracteata and Q. eriocaulis. The latter species has 


ha 
white corollas, closely or densely sericeous stems 
with malpighioid hairs, and the lower surface of 
the leaves pubescent to glabrous, but not densely 
lanate. 

In habit, Achnopogon steyermarkii, A. quel- 
chioides, Quelchia eriocaulis, and Q. bracteata 
simulate one another in their simple, ligneous 
stems enveloped in their upper portion by dense- 
ly crowded, ascending, subsessile to shortly pet- 
iolate leaves, which conceal the inflorescences 
present at their base. However, the corollas im- 
mediately distinguish these four taxa, Quelchia 
having the inflorescence 1-flowered with regular 
5-lobed corollas, whereas Achnopogon has 2-5- 
flowered inflorescences with bilabiate corollas. 

The synonymy of Achnopogon steyermarkii 
follows: 


Achnopogon steyermarkii Aristeg., Acta Bot. 


Venez. 2(5—8): 350. fig. 30. 1967. 


> Ó 


ЖИ ی‎ 


LA m 
27 


m 


4164 
Ay) 


ANNALS OF THE MISSOURI BOTANICAL GARDEN [Vor. 71 


"m 


1G 


FiGURE 12. Chimantaea huberi.—A. Habit.—B. Upper half, mature achene; lower half with crown ofa 


and stylar base.—C. Upper part of achene in late bud stage, showing corona and stylar base.—D. Cap! 


tulum of | 


ge 


~ 


+ 


| 


њи 


1984] 


Achnopogon quelchioides Aristeg., Acta Bot. Venez. 
2(5-8): 348. fig. 29. 1967. 


Chimantaea acopanensis Steyerm., sp. nov. TYPE: 
Venezuela. Bolivar: Piar, Macizo de Chi- 
manta, sector SSE, altiplanicie, sur-oriental 
del Acopan-tepui, cabeceras del Rio Arauac, 
praderas humedas y arbustales enanos sobre 
turberas, bosquecillos riberefios y vegeta- 
ción sobre rocas abiertas, 5°1 I'N, 62°00'W, 
1,920 m, 14-16 Feb. 1984, Steyermark, Lu- 
teyn & Huber 129932 (holotype, VEN). 


Planta pusilla rosulata caespitosa usque ad 10 cm 
alta; foliis linearibus apice rotundatis vel obtusis 35— 
40 mm x 3.5-6 mm valde revolutis supra non-sulcatis 


latis; involucro 5-seriato, bracteis lineari-lanceolatis 
acuminatis intimis 14 mm x 2.5 mm exti 

mm х 2 mm tertia parte superiore dense lanulosis; 
receptacul 

exteriores subulatis 19 mm x 0.5-1.5 mm in dimidio 
| | ini mnino ciliolatis; cor- 
olis 14 mm longis, lobis lineari-ligulatis subobtusis 10 
mm x ] mm; antheris 5 i i bi i 


subsessile densely lanate base, 35-40 mm by 3.5- 
6 mm; heads sessile, solitary, terminating the leaf 
rosette, campanulate, 28-flowered, 2 cm hi 

5 cm wide; involucre 5-seriate, bracts linear- 
lanceolate, attenuate to an acuminate dark ma- 
вета apex, densely buff tomentose in the upper 
third, glabrous in lower third, innermost 14 mm 
by 2.5 mm, outermost 10 mm by 2 mm; recep- 
tacle flat, shallowly alveolate; heads homoga- 
mous; paleae 3, inserted between the outer fo- 
rets, subulate, 19 mm by 0.5-1.5 mm, pubescent 
In upper half: corollas 14 mm long, the tube 4 
mm long, 1.8 mm wide at summit, 1.2 mm wide 
2 base, lobes equal, linear-ligulate, subobtuse, 

Ü mm by | mm; anthers dark magenta-wine 
bes 3 mm long; style lavender, 16 mm long, 

'&mas ligulate-oblong, obtuse; achene slenderly 


"LC Ре 


STEYERMARK — VENEZUELAN GUAYANA 


335 


fusiform-cylindric, 4-4.5 mm by 1 mm, loosely 
pilose; pappus tawny, the numerous bristles 12— 
14 mm long, minutely serrulate. 


This taxon may possibly prove to be a putative 
hybrid between C. huberi Steyerm. and C. Au- 
milis Maguire, Steyerm. & Wurd., both species 
occurring in the immediate area. The non-sulcate 
upper leaf surface and densely buff tomentose 
involucral bracts together with the deep brown 
lanulose pubescence are shared with C. humilis, 
whereas the dwarf caespitose, rosulate habit and 
non-sulcate upper leaf surface are shared with C. 
huberi. 


Chimantaea huberi Steyerm., sp. nov. ТҮРЕ: 
Venezuela. Bolívar: Piar, Macizo del Chi- 
mantá; peq Itiplanici la base sep- 
tentrional de los farillones superiores del 
Amuri-tepui (sector occidental del Acopán- 
tepui), 5?10'N, 62?07'W, rocky exposed out- 
crops of savanna on heliport just W of camp- 
site, 1,850 m, 2-5 Feb. 1983, Steyermark, 
Huber & Carrefio 128815 (holotype, VEN; 
isotypes, K, MO, NY, U, US). PARATYPES: 
same locality, 2-5 Feb. 1983, Huber & Stey- 
ermark 7118 (K, MO, NY, U, US, VEN); 
altiplanicie suroriental del Acopán-tepui, 
cabeceras del Río Arauac, praderas hüme- 
das sobre turberas, 5°11’N, 62?00'W, 1,920 
m, 14-16 Feb. 1984, Steyermark, Luteyn & 
Huber 129924 (VEN); Apacará-tepui, 
5°20'N, 6212 W, 2,300 m, 1 Feb. 1983, 
Steyermark, Huber & Carrefio 128419 
(VEN). 


Planta pusilla rosulata caespitosa 1—3 cm alta; foliis 
apiculo diminuto obtusiusculo acuto 10-20 mm x 2— 
4 mm supra glabris subtus albo-pannosis valde revo- 
lutis; capitulis sessilibus 2 cm x 0.7–0.8 cm; involucro 
campanulato 6-7-seriato in base tomentosa albida 
insidenti; phyllariis ca. 30 praeter margenes ciliatos 
glabris, exterioribus late triangulari-lanceolatis acu- 

i 4 mm intimis anguste ligulato-sub- 
spathulatis 14 mm x 2 mm; receptaculo plano al 
lato glabro; paleis non visi; floribus 7-15 
actinomorphicis, corolla albida 10 mm longa trans me- 
dium fissa 5-nervata, tu mm x 2 mm, limbo 1 
mm х 2 mm, lobis erectis ligulato-lanceolatis subob- 
tusis 6.5 mm х 0.9-1 mm, tubo lobisque extus glabris, 

“+ г. 1 1 2 harhat 1 

gla 


e 


1 


„пса; 


veo- 


~ 


flowers with involucre. —Е. Floret, exterior view.—F. Interior of floret. —G. Stamen. —H. Stigmas.—I. Middle 


Involucra] bracts 


— 
. . 


po 


: Stylar base surrounded by coronal disk. —K. : 
Portion of receptacle.—M. Corolla in bud with lanulose tomentum of involucral base.—N. Pappus seta and 
rion enlarged 


Outermost involucral bract.— L. Alveolate 


336 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


bro; achaeniis 6 mm x 2 mm densissime albo-sericeis; 
pappo ochroleuco pluriseriato, setis 8—10 mm longis. 


Dwarf perennial, caespitose rosulate plant 1— 
3 cm tall, forming large mats; stems greatly re- 
duced, subligneous, or not evident, simple or 
branched, 0.5-1.5 cm diam.; leaves numerous, 
stiff-coriaceous, erect, strongly revolute, crowd- 
ed, sessile, linear, linear-sublanceolate or linear- 
oblanceolate, subobtuse at apex with a minute 
obtusely acute thick apiculum, slightly narrower 
and subunguiculate toward the base, 10-20 mm 
y 2-4 mm, shining and rich green above, white 
pannose tomentose below for 7-16 mm but the 
narrower, sulcate, basal 2—5 mm portion below 
glabrous; flower heads homogamous, sessile, ter- 
minal, 2 cm by 0.7–0.8 cm; mature involucre 
shortly campanulate, 6—7-seriate, on a white to- 
mentose base; involucral bracts maroon-purple, 
rigidly chartaceous, ca. 30, glabrous except for 
the ciliate margins, the outer broadly triangular- 
lanceolate, acuminate, convex, 7 mm by 4 mm 
intermediate ligulate-lanceolate, acute or obtuse, 
12 mm by 2.5 mm, interior narrowly ligulate- 
subspathulate, 14 mm by 2 mm; receptacle flat, 
alveolate, glabrous; pales not seen; flowers 7—15; 
corolla white, 10 mm long, cleft more than half- 
way down, 5-nerved, tube salverform, 3 mm by 
1.5-2 mm, throat 1 mm by 2 mm, lobes erect, 
ligulate-lanceolate, subobtuse, the apex and mar- 
gins somewhat thickened, 2-пегуед, 6–6.5 mm 
by 0.9-1 mm, tube and lobes glabrous without, 
lobes glabrous within, tube densely barbate-lanu- 
ginose within at the throat, elsewhere glabrous; 
anthers lavender-brown, linear, 4mm by 0.6 mm, 
acute at apex, sagittate at base, basal appendages 
free, somewhat incurved at the apex, 1 mm long, 
glabrous; pollen grains tricolpate, not spinose; 
style pale green at apex, surrounded by an entire 
fleshy collar 0.7 mm high and 1 mm wide at 
base; achenes cylindric 6 mm by 2 mm at apex 
with a short slightly undulate to entire crown 1 
mm high, densely white-sericeous; pappus buff, 
multiseriate, the awns subequal, 8-10 mm long, 
barbellate, slightly coherent at base. 


~ 


Itisa great р | thi ltaxon 
for Dr. Otto Huber, dedicated student of the 
Guayana flora, under whose successful manage- 
ment the expeditions to Chimanta were com- 
pleted. 

This taxon may be considered a very reduced 
member of the genus Chimantaea and derived 
from a still further reduction of an evolutionary 


branch of Chimantaea rupicola Maguire, Stey- 
erm. & Wurd. From the other known species 0 
the genus, all of whose taxa but one (C. cinerea 
(Gl. & Blake) Maguire, Steyerm. & Wurd. of Au- 
yan-tepui) are known from the Chimanta Massif, 
C. huberi differs in the very dwarfed, rosulate, 
caespitose plants growing in dense mats less than 
3 cm high, the short corolla and corolla lobes, 
the absence of paleae, and the much shorter, nar- 
rower leaves. Anatomical studies of the leaves 
and palynological examination agree with the 
placement of this species in Chimantaea. 

In their original description of the genus Chi- 
mantaea, Maguire, Steyermark & Wurdack (in 
Maguire et al., 1957: 428) described the recep- 
tacle as pubescent with few (2—5) marginal pales, 
tips of the corolla lobes more or less barbellate, 
and pollen grains spinulose. Later, Aristeguieta 
(1964: 831, 879) correctly described the generic 
characters in broader terms and allowed for an 
absence or presence of pales on the pubescent or 
non-pubescent receptacle, as well as for a gla- 
brous or pilose apex of the corolla-lobes. More- 
over, the pollen, stated in the original description 
of the genus to be spinose (in Maguire et al., 
1957b: 428), may be nearly psilate in some 
species, such as C. similis, as shown by Car lquist 
(1957: 446—447. fig. 93c). Senora Maria Léa La- 
bouriau of IVIC (Instituto Venezolano de In- 
vestigaciones Cientificas) of Caracas, Venezuela, 
an authority on pollen, has kindly supplied -- 
with a description of the pollen of C. huberi as 
follows: subprolate, non-spinose lobate grains 
with salient poles. Fossa perturate. Grains УГУ 
dark colored. Apertures: 3 colporate. Com yes 


Exine non-espinose with vestigial spinules, va 
thick at the polar region. Sexine very thick М 
two layers: tegilum and infrategillar bacula layer, 
bacula visible from x 400 up. She concludes the 
the grains are very similar to those of Carlquist $ 
description of C. similis. 

The anatomical study of the leaves Was made 
by Senorita Luisa Lopez of the Direccion de E 
vestigaciones Biólógicas of the Jardin Botánic? 
in Caracas, Venezuela, whose description is a8 
follows: 


Epidermis adaxial sclerified with опе layer ч 
cells, with prominent cuticular membrane. hy 
podermis adaxial with 3-4 cells in thickness 
thickened walls, constituting à band along 


length of the leaves: mesophyll undifferen 


—— — 


1984] 


with a spongy parenchyma and palisade cells of 


idermis abaxial monostratified with 
the stomata sunk below a tomentum of simple 
hairs with slender walls. Toward the leaf margin 
an exceptional development of sclerenchyma oc- 
curs which facilitates the revolute portion of the 
leaf to function. She notes that the marked scle- 
rophyll type of leaf enables the plant to adapt to 
loss of water, high evaporation, and unfavorable 
edaphic conditions. The scleromorphic leaves of 
the species are small and coriaceous and are pro- 
vided with cutinized cell walls. She notes that 
there is evidence to show that a lack of nitrogen 
is responsible for the appearance of scleromor- 
phous characters, and that nitrogen deficiency is 
associated with sclerophylly. 

Chimantaea huberi possesses characters com- 
mon to both of the genera Chimantaea and Sto- 
matochaeta. In common with Stomatochaeta it 


cence, and densely pubescent achenes. While 
sharing with Chimantaea а 5-nerved corolla tube, 
free anther tails, and similar tomentum on the 
lower side of the strongly revolute leaves, it dif- 
fers from the other species of Chimantaea in the 
smaller, fewer-flowered heads and an entire, in- 


C. similis. The epaleaceous ос of С. hu- 
beri manifests its still further reduction from its 
most closely derived taxon, i.e., C. rupicola which 
помене: 1-2 deciduous marginal paleae. Chi- 


nt. 


in a series from a tall arborescent “‘espeletioid” 
type to 3 m tall, as shown by C. mirabilis and 
С. lanocaulis, to a nearly herbaceous rosulate 
chabit, a tendency suggested by Maguire, Sn. 
NR. and Wurdack (in Maguire et al., 1957a 


Chimn»: Z2 


— On bare open, exsiccated, flat sandstone 
== (as noted in Steyermark et al. 128419 
: 128815) or in open swampy ground of sa- 

anna-like habitats where the soil is more sat- 


rated (n; y t 1 
1 29924) т. ater (as in = оин, et a 


posed eit 


STEYERMARK — VENEZUELAN GUAYANA 


337 


which it resembles strikingly in such characters 
as erect, olive green, stiff-coriaceous leaves, and 
white tufts of tomentum at the base of the leaf 
tone Mte, de such instances, the convergence of 
close that one must 
observe the two with especial perception in order 
not to confuse the two families. Where Chiman- 
taea huberi grew on the dry sandstone ledges, it 
was also associated with Brocchinia reducta, 
Stegolepis ligulata, Ledothamnus decumbens, 
Achnopogon virgatus, and other xeromorphic 
species. On the wet swampy savanna-like habitat 
it was associated with such species as Epiden- 
drum alsum, Tepuia venusta, Myrtus alternifol- 
ia, Stegolepis ligulata, Tillandsia stenoglossa, 
Stomatochaeta cymbifolia, and others. 


Chimantaea cinerea (Gl. & Blake) зелена ssi 
erm. urd. f. glabra Steye 
TYPE: Venezuela. Bolivar: аа paran nde 
derecho del Salto Angel, 15 Aug. 1968, Er- 
nesto Foldats 7100 (holotype, VEN). 


C. cinerea corollae lobis secus margines pilosulis; 
achaeniis glabris recedit. Folia obovata apice Missis 
basi angustata petiolata, 5—7 cm x 2.5-3.5 cm supra 
glabra subtus dense cinerea, nervis lateralibus oblikurie 
utroque latere 8-10; petiolis 5-7 mm x 3-3.5 mm ci- 

nereo-tomentosis; corollis 19-20 mm longis, tubo 5 

mm longo intus basi loborum dense piloso aliter gla- 
bro; achaeniis 6—7 mm longis glabris; pappi setis 18— 
20 mm longis. 

This form has the glabrous achenes of C. sim- 
ilis Maguire, Steyerm. & Wurd. but the margins 
of the corolla lobes are pilosulous, as in C. ci- 
nerea. The differences separating C. cinerea and 
C. similis are perhaps not sufficient for specific 
recognition. The achenes of C. cinerea vary from 
densely or moderately sericeous to only sparsely 
so, while the corolla lobes may vary from usually 
pilose to glabrous, as in the collection of Pannier 
& Schwabe 1927-A from Auyan-tepui. The co- 
rolla lobes of C. similis, on the other hand, while 
ordinarily glabrous, may also show some pilos- 
ity. The two taxa are isolated on separate tepuis, 
C. cinerea occurring on Auyan-tepui and C. sim- 
ilis on the Chimantá Massif. 


NOTES ON HYBRIDIZATION IN 
CHIMANTAEA AND QUELCHIA 


On the extensive series of plateaus which com- 
prise the Chimantá Massif (Macizo de Chiman- 
tá) there have evolved many genera and species 
known nowhere else in the Venezuelan Guayana. 
Of these, one of the most remarkable genera is 


338 


the mutisioid composite, Chimantaea. Except 
for the occurrence of two species, one found on 
the nearby (but distant) Auyan-tepui, the other 
on Aprada-tepui, both in the state of Bolivar, the 
remainder of the taxa are known only from Chi- 
manta Massif of Bolivar state. It is on the Chi- 
manta Massif where the main evolutionary pro- 
cess has developed in the genus. 

Although eight species have been described as 
the result of two major expeditions there in 1953 
and 1955, recent explorations during 1983 and 
1984 have provided further opportunities for ad- 
ditional collections and observations of the ge- 
nus. These have resulted in the discovery of at 
least two new taxa pertaining to the genus, one 
with a remarkable dwarf rosette, C. huberi, which 
resembles an eriocaulaceous taxon (Syngonan- 
thus obtusifolius), with which it is often associ- 
ated, and the second one, similarly dwarfed, but 
suspected to be of hybrid origin, namely C. aco- 
panensis. 

Actually, the more abundant collections of 
many more individual plants of the genus on 
Chimanta Massif have furnished increasing evi- 
dence to substantiate grounds which support the 
belief in 1) the occurrence of some hybridization 
taking place be ious taxa and 2) vari- 
ation in vegetative characters which show de- 
grees of intergradation, making it difficult to as- 
sign individual specimens to a definite category. 
Although it is true that the eight previously de- 

4 Asadée + 


4L 


scribed taxa may be readily g t 
entities as such, nevertheless some specimens ap- 
pear as more or less intermediate in character or 
combine characters common to different taxa. 
This is apparent in such collections as Steyer- 
mark, Huber & Carreño 128518 which appears 
intermediate between C. eriocephala Maguire, 
Steyerm. & Wurd. and C. humilis Maguire, Stey- 
erm. & Wurd. The leaves of C. humilis vary in 
width, some having the greater width of C. eri- 
ocephala or C. humilis, others having the nar- 
rower width of C. mirabilis. This latter type is 
exemplified by the collection of Steyermark, 
Huber & Carreño 128511 which shows an inter- 
mediate stage between C. humilis and C. mira- 
bilis. Another collection, Steyermark et al. 
128332-A, has leaves too narrow for C. similis 
but resembles that taxon in other characters. 
The newly described taxon, C. acopanensis, 
was found growing near the newly described C. 
huberi, and in the near vicinity C. humilis 
occurred. The dwarf habit of C. acopanensis 
suggests C. huberi, but the larger leaves and flow- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


er-heads, as well as the densely tomentose in- 
volucral bracts, indicate characters shared with 
C. humilis. Nevertheless, C. acopanensis may be 
readily recognized from other taxa of the genus 
by its combination of a dwarf rosette habit, to- 
mentose involucral bracts, and shape and size of 
leaves and heads 

Likewise in the genus Quelchia a putative hy- 
brid has been recorded as Quelchia x grandifo- 
lia (Maguire et al., 1957b: 436). This manifests 
characters of both Q. eriocaulis Maguire, Stey- 
erm urd. and Q. bracteata Maguire, Stey- 
erm. & Wurd., both of which taxa occur in the 
immediate vicinity. 


NOTE ON GONGYLOLEPIS BENTHAMIANA 
VS. G. PANICULATA 


Aristeguieta (1964: 895) separated G. panicu- 
lata Maguire & Phelps from G. benthamiana 
Schomb. on the basis of leaf length and width, 
length of involucre, and number of seriate bracts. 
In an examination of material in VEN, the size 
of leaves for G. benthamiana varies from 7.5- 
16.5 cm by 2-5.5 cm (Aristeguieta, 1964: 900 
gives 7.5—16.5 cm by 2-5.5 cm) and for С. pani- 
culata varies from 12-27 cm by (2.5-)5-8(-9) 


cm. 

In the key to Gongylolepis, Maguire (in Ma- 
guire et al., 1953: 155), in addition to separating 
these taxa by leaf dimensions, employs an ad- 
ditional character not used by Aristeguieta, 
namely, leaf venation. Thus, for G. paniculata 
the primary veins are stated as “extending little 
beyond the middle, then anastomosing and with 
the secondary veins reticulate, veins on upper 


: $ G. 
surface merely prominulous," whereas i 
L M . Я ctated aS ех". 


the primary veins а 
tending nearly to the margins before anasto- 
mosing, veins on upper surface promi 
strongly reticulate.” An examination of mater 
in VEN verifies this difference in venation give” 
by Maguire. The differences mentioned for 512 
of involucre and number of seriate bracts like 
wise is borne out by an examination of mate 
at VEN. к 

Previously, all material of С. benthamiana 
been known to occur only in Estado ped 
eastern Guayana of Venezuela, from the ee 
Sabana west to Cerro Guaiquinima, Cerro at 
rutani (оп the Brazilian-Venezuelan front. 
the headwaters of Rio Paramichi, an a d 
the Río Paragua), and Cerro Marajanu 0 ке 
Meseta de Jaua in the Upper Caura. In СОП 


~ 


1984] 


G. paniculata is known only from the sandstone 
table mountains of the Territorio Federal Ama- 
топаз. It was, therefore, a great surprise while 
collecting on the savanna-covered sandstone 
substrata of the Serrania Vinilla in Territorio 
Federal Amazonas to find G. benthamiana as 
one of the common species and far removed from 
its occurrence in eastern Guayana. These collec- 

tions, represented by Steyermark, Berry & De- 
lascio 130329, have the leaves with the size and 
venation typical of G. benthamiana, and, addi- 
tionally, the smaller involucres with 6-seriate 
ies. Two other collections from 
the Serrania Vinilla (Huber 6044 and 6175) also 
are typical G. benthamiana, although they were 
originally misidentified as G. paniculata, prob- 
ably use G. paniculata is a widespread species 
in Territorio Federal Amazonas. 

An additional observation made in connection 
with a study of these two taxa is that the heads 
of G. paniculata are narrowed at the base, where- 
as those of G. benthamiana are more rounded 

sally, producing a shallowly campanulate shape 
to the involucre. 

This disjunct distribution separates G. ben- 
thamiana about 300 km southwest of its nearest 
outpost in Estado Bolivar. 


Mikania michelangeliana Steyerm., sp. nov. 
TYPE: Venezuela. Amazonas: Cerro Ма- 
uaca, summit, borde noroeste, meseta 
sureste, valle Yekuana, bordering small 
stream, 2,560 m, 10 Oct. 1983, Steyermark 
129456 (holotype, VEN). 


ai anta scandens, caulibus saltem juvenilibus papil- 
S tomentellisque: з то oyat арїсе acutis 
el acuminatis basi eden 3.2c 


» tis i cunea tis 3—5-ріпегу 

b cm nt 1 S , mar- 
gini us minute denticulatis: аби cymosis 4- 
4.5 cm x 4.4, 


axibus pedicellisque dense brev- 

we сига режији 5 papillatisque; capitulis 4-5- floris 7-9 

jana т rollis 4.5 mm longis; achaeniis 4–4.5 
ongis Бых vel dense papillato-puberulis. 


a А 
en or obscure; petioles 4-6 mm long, gla- 


uid ог sparingly puberulent; inflorescence ter- 
cm, and axillary, cymose, 4-4.5 cm by 4-4.5 

axes short-tomentose mixed with papillate 
> pedicels 2-4 mm long, densely tomentel- 


STEYERMARK— VENEZUELAN GUAYANA 


339 


lose, heads 4—5-flowered, 7-9 mm by 3 mm; in- 
volucral bracts ligulate, subacute at apex, slightly 
unequal, 4-5 mm .8-1 mm, longitudinally 
3-nerved, densely minutely puberulent without; 
corollas infundibuliform, 4.5 mm long, tube in 
upper portion glabrous without, lower constrict- 
ed portion sparsely glandular, lobes broadly lan- 
ceolate, acute, 1 mm long; achenes linear, quad- 
rangular, 4-4.5 mm long, sparsely to densely 
papillate-puberulous; pappus cream-colored, 
bristles numerous, 4—5.5 mm long, serrulate. 


In leaf size and shape this taxon approaches 
M. lucida Blake, and in stem pubescence is sim- 
ilar to that of M. /ucida f. hirticaulis Steyerm. 
From both of these taxa M. michelangeliana dif- 
fers in the more sharply acute leaf apex, the mi- 


short tomentum intermixed with a papillate in- 
dument on most of the stem and axes of the 
inflorescence. 

I take pleasure in associating the name of Ar- 
mando Michelangeli with the new species. 
Through his efforts as administrator of the Ter- 
ramar Foundation, exploration of the summit 
areas of Cerro Marahuaca has been made pos- 
sible. 


LITERATURE CITED 


ALEXANDER, M. P. Differential staining of 
aborted and nonaborted pollen. Stain Technol. 44: 
117-122. 

ARISTEGUIETA, L. 1964. 
ezuela 10(2): 495-941. 

BENTHAM, С. 1841. XXV. On the Heliamphora nu- 


Compositae. Flora de Ven- 


Б, 

Pl р. 278-306. 

BREWER- bes C Plantas carnivoras del Cer- 
ro de la Neblina. Defensa de la Naturaleza 2(6): 
17-26. 


Савы $. 1957. Anatomy of Guayana Muti- 
e. Mem. New York Bot. Gard. 9: 441-476. 


Nat. Pflanzenfam. 3(4): 95-20 
GLEASON, H. 1931. Botanical results of the Tyler- 
Duida Expedition. Bull. Torrey Bot. Club 58: 345— 
4. 
ЕЕЕ . P. Киир. 1939. The flora of Mount 
Auyan tiep Venezuela. Brittonia 3: 141-204. 
Ковизкл, C. E. 1948. Studies in the Theaceae, Буп 
A review of the genus Bonnetia. J. Arnold Arbo 
29: 393-413. 
ager F. E. 1942. The Carnivorous sie азр 
ca Botanica Со., Waltham, Massachuse 


340 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


MAGUIRE, В. 1968. A new Elvasia oe for ——,—— & COLLABORATORS. 1961. The bot- 
Venezuela. Acta Bot. Venez. 3: 297-299. any of the Guayana signa Part IV(2). Mem 
982. Rapateaceae. Flora de Т. 11(2): New York Poh, "Gard. 1 0(4): 1-87. 
85. —203. ‚ К. S. Cowan, J. J. WURDACK & COLLABORA- 
—— ——— & COLLABORATORS. 1967. The botany of the TORS. 1953. The botany of the Guayana High- 
Guayana Highland—Part VII. Mem. New York land. A report of the Kunhardt, the Phelps, and 
Bot. Gard. 17(1): 1-439. the New York Botanical Garden Venezuelan ex- 
& COLLABORATORS. 1972. The botany of the peditions. Mem. New York Bot. Gard. 8: 87-160. 
Guayana a Part IX. Mem. New York , J. А. STEYERMARK, J. J. WURDACK & COLLA 
Bot. Gard. 23: 1-832. BORATORS. 1957b. Botany of the Chimanta Mas- 
& COLLABORATORS. 1978. The botany of the sif—I Gran Sabana, Venezuela. Mem. New York 
uayana Highland—Part X. Mem. New York Bot. Bot. Gard. 9: 393-439. 
Gard. 29: Iren. ScHULTES, R. E. 1951. Plantae Austro-Americanae 
K & COLLABORATORS. 1957a VII. Bot. Mus. Leafl. 15: 29- 
The botany of he Guayana Highland — Part II. STEYERMARK, J. A. COLLABORATORS. 1951. Con 
e ew York Bot. Gard. 9 - tributions to the Flora of Venezuela. Botanical ex 
LLABORATORS. 1958. The bot- ploration in Venezuela, I. Fieldiana, Bot. 28: 1- 
any ofthe Guayana Реге Part III. Mem. New 242. 
York Bot. Gard. 10(1): 1-15 ————, B. MAGUIRE & COLLABORATORS. 1972. The 
А на. 1960. The botany flora of the Meseta del Cerro Jaua. Mem. New 
of the Guayana ey oe ВА IV. Мет. New York Bot. Gard. 23: 833-892, 


York Bot. Сага. 10(2): 1 


— 


NOTES 


A NEW COMBINATION IN DALECHAMPIA 
(EUPHORBIACEAE) 


Fift pecies of Dalechampi. ] from 
Central America. One of these was mistakenly 
described as a Tragia and has not yet been trans- 
ferred to Dalechampia. While preparing the 
treatment of Tragia for a revised synopsis of 
Panamanian Euphorbiaceae (Webster & Huft, in 
prep.), I discovered that Tragia shankii was the 
same as an otherwise undescribed Dalechampia 
that is represented by several collections from 
the Caribbean slope of Costa Rica and Panama 
and from the Province of Chocó in Colombia. 
In order to make the proper name available for 
taxonomic and pollination studies being carried 
out by Dr. Scott Armbruster, I am making the 
combination here, rather than waiting for the 
appearance ofthe Panama paper. This is the “ип- 

escribed species" that is referred to in Arm- 
bruster (1982) as “La Osa” (Armbruster, pers. 
comm.). 


Dalechampia shankii (A. Molina) Huft, comb. 

nov. Tragia shankii A. Molina, Ceiba 11: 

68. 1965. түрЕ: Costa Rica. Limon: drainage 

of Rio Reventazón, 15 m, 23 Oct. 1951, 

Shank & Molina 4427 (holotype, 
F-1563051; isotype, EAP, not seen). 

Dalech 


by its M. xe iio ii may be readily identified 
deeply esed i о (ог sometimes unlobed), 
Pee te eaves, densely hirsute orange in- 
ani » Orange sericeous involucral bracts and 
‘PSules, and narrow, fimbriate, orange sericeous 

Pistillate sepals. 
„нге this species to be a close 
GRAN. Tragia bailloniana Muell. Arg., which 
"d rus the monotypic sect. Zuckertia (Baill.) 
Thoi: E d seems to be quite isolated within 
у Магы, a cg the collection of Standley and 
сыз ed below is apparently the basis for 
dley’s m report of T. bailloniana in Stan- 
en 7? of Costa Rica” (1937: 622). How- 
ж species, which had previously been 
wn only from southern Mexico and northern 


ANN. MISSOURI Вот. GARD. 71: 341. 1984. 


Central America as far south as Honduras, has 
only recently been collected in Costa Rica (Ala- 
juela: along Upper Rio Sarapiqui, near Cari- 
blanco and along road to Colonia Virgen del So- 
corro, 19 Feb. 1982, Burger et al. 11850, F) and 
Panama (Chiriqui: Fortuna Dam site, 15 Sept. 
1977, Folsom et al. 5612, MO). 

The specimens cited below have been var- 
iously distributed as Tragia bailloniana, T. 
shankii, Dalechampia tiliifolia, or as undeter- 
mined Dalechampia. The two collections from 
Panama are not currently available to me and 
are included here on the authority of Armbruster 
(pers. comm.). 

Additional collections. Costra RICA. LIMON: Ha- 
cienda Tapezco-Hda. La Suerta, 29 air km W of Tor- 
tuguero, 10*30'N, 83?47'W, 40 m, 10 Mar. 1978, Da- 
vidson et al. 6828 (F); Montafia de Andromeda, drainage 
of Rio Estrella, 300 m, 26-28 Oct. 1951, Shank & 
Molina 4475 (F); Finca Montecristo, below Cairo, 25 
m, Feb. 1926, Standley & Valerio 48568 (F). 

АМАМА. LE: 16.5 km N of Llano Grande, in 
forest near saw mill, 29 Jan. 1980, Armbruster & Her- 
zig 79-213 (ALA); near saw mill, 16.7 km N of turnoff 
to Coclesito from Llano Grande, 700 ft., 6 Mar. 1978, 
Hammel 1813 (MO). 

OLOMBIA. CHOCO: Rio San Juan, vic. of Palestina, 
0-30 m, 28 May-4 June 1946, Cuatrecasas 21512 (F, 
2 sheets). 

I am indebted to Dr. Scott Armbruster of the 
University of Alaska for valuable correspon- 
dence during the preparation of this paper. 


LITERATURE CITED 
1982. Seed production and dis- 


ARMBRUSTER, W. S. 
persal in Dalech 


Amer J. Bot 


1 1 1 


69: 1429-1440. _ 
STANDLEY, Р. С. 1937. Flora of Costa Rica. Publ. 
Field Mus. Nat. Hist., Bot. Ser. 18. 


— Michael J. Huft, Missouri Botanical Garden. 
Mailing address: Department of Botany, Field 
Museum of Natural History, Roosevelt Road at 
Lake Shore Drive, Chicago, Illinois 60605. 


A NEW COMBINATION FOR A 
NORTH AMERICAN EPILOBIUM 


1 4L Pe M Г. 


In order t several 
pending floristic works, we make the following 
new combination in advance of a complete re- 
vision of Epilobium in North America: 


Epilobium glaberrimum Barbey subsp. fastigia- 
tum (Nutt.) Hoch & Raven, comb. nov. Epi- 
lobium affine Bong. 8.? нип Nutt. in 
Torrey & A. Gray, Fl. N. Am 1: 489. 
1840. ТҮРЕ: руне: of the а River” 
(probably near Walla Walla, Washington), 
1834—36, T. Nuttall s.n. (holotype, BM; 
isotype, NY). Epilobium fastigiatum (Nutt.) 
Piper, Contr. U.S. Natl. Herb. 11: 404. 1906. 
Epilobium glaberrimum Barbey var. fasti- 
giatum (Nutt.) Trel. ex Peck, Man. FI. Pl. 
Oregon 494. 1941 


ч ANN. Missouri Bor. GARD. 71: 342. 1984. 


This includes only partial synonymy. Full ex- 
planation of the rationale for recognizing this 
taxon as a distinct subspecies is given in Hoch 
(1978), and will be included in the revision now 
in progress. 

We gratefully acknowledge support from the 
National Science Foundation through grants to 
both investigators. 


LITERATURE CITED 
Носн, P. C. 1978. Systematics and ero of the 
Epilobium ciliatum complex in merica 
(Onagraceae). Ph.D. dissertation. Washing 
University, St. Louis 


— Peter C. Hoch and Peter H. Raven, Missouri 
Botanical Garden, P.O. Box 299, St. Louis, Mis- 
souri 63 166—0299. 


UPCOMING MEETINGS 


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The Eleventh Congress of the Association will be held at the Missouri Botanical 
Garden, St. Louis, Missouri, from 11 to 14 June 1985. The central theme will be 
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presented on this subject. Several special interest symposia are being organized, 
including Systematics and Floristics of African Bryophytes; African Lichens; Bi- 
ology of Madagascar; and African Ethnobotany and Ethnomedicine. Contributed 
papers on African plant systematics, floristics, ecology, and related fields are 
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AETFAT General Secretary, Missouri Botanical Garden, P.O. Box 299, St. Louis, 
Missouri 63166, U.S.A. 


Second International Legume Conference. 


The Conference, entitled “Biology of the Leguminosae,” will be held on 23-27 
June 1986 at the Missouri Botanical Garden, St. Louis, Missouri. The aim of the 
meeting is to discuss recent advances in our understanding of the biology of 
legumes, gained from both field and experimental research, and covering both 
pure and applied points of view. The multidisciplinary approach of the conference 
is designed to address a wide variety of research interests and to stimulate dis- 
cussion among specialists. Scheduled topics include: life history studies; tree ar- 
chitecture; evolution and biology of inf d pollen; floral organogenesis; 
ecology; ecological biogeography; pollen-stigma-style interactions; structure and 
function of legume fruits and seeds; mycorrhizal relationships; cyanogenesis; evo- 
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changes induced by domestication; computerized data bases and biological re- 
Search; international legume data bases. For further information write to: Dr. 
James L. Zarucchi, Legume Conference Coordinator, Missouri Botanical Garden, 
P.O. Box 299, St. Louis, Missouri 63166, U.S.A. 


| ANN. Missouri Bot. GARD. 71: 343. 1984. 


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-Contents continued from front cover 


A Survey of Seed Surface Morphology in Hesperantha (Iridaceae) War- 
ren L. Wagner & Peter Goldblatt 

A Floristic Study of Volcan Mombacho Department of Granada, Nicaragua 
John T. Atwood ___ 


An Index to the Families in Engler and Prantl’s *Die Natürlichen Pflanzen- 
2 


familien" Thomas Morley - 
Techniques for Collecting Aquatic and Marsh Plants Robert R. Haynes 
Wood and Stem Anatomy of Bergia suffruticosa: Relationships of Elatina- 
ceae and Broader Significance of Vascular Tracheids, Vasicentric Tra- 
cheids, and Fibriform Vessel Elements Sherwin Carlquist a 
The Evolution of Dioecy—Introduction Gregory J. Anderson .. — 
Further Thoughts on Dioecism and Islands Herbert G. Baker & Paul 
Alan Cox .. 
Sexual Dimorphism and Ecological Differentiation of Male and Female Plants 
Thomas К. Meagher ee 
The Adaptive Significance of Sexual Lability in Plants using Atriplex ca- 
nescens as a Principal Example D. C. Freeman, E. D. McArthur & 
KT. Hameo осе eee 
Variation in Floral Sexuality of Diclinous Aralia (Araliaceae) ^ Spencer 
С. Н. Barret ои ОИ 
Evolution of Dioecy in Saurauia (Dilleniaceae) W. A. Haber & K. S. 
Bawa 


The Evolution of Dioecy—Concluding Remarks K S Bawa sS 
Flora of the Venezuelan Guayana—I Julian А. Steyermark a 
NOTES 

A New Combination in Dalechampia (Euphorbiaceae) Michael J. Huft 


A New Combination for a North American Epilobium Peter C. Hoch & E 


Peter H. Raven 
Upcoming Meetings 


254 


265 


278 


ANNALS 


SSOUR] BOTANICAL GARDEN 


VOLUME 71 1984 NUMBER 2 


MUSEUM BUILDING 


MAR 2 1 1985 


| CONTENTS - | 
| Dedication _____ 347 
| HISTORICAL PERSPECTIVES OF ANGIOSPERM EVOLUTION 
i David Dilcher & William Crepet 348 
| Archaeanthus: An Early Angiosperm from the Cenomanian of the Western 
Interior of North America David І. Dilcher & Peter R. Crane ___. 351 
Lesqueria: An Early Angiosperm Fruiting Axis from the Mid-Cretaceous 
Peter R. Crane & David L. Dilcher ____ 384 
Preliminary Report of Upper Cretaceous Angiosperm Pagi Organs 
from Sweden and their Level of Organization Е. M. Рт 2... 403 
Significance of Fossil Pollen for Angiosperm History Jan Mudo 205008 419 
Angiosperm Origins and Evolution Based on Dispersed Fossil Pollen UI- 
trastructure Michael S. Zavada 444 
Ultrastructure of Lower Cretaceous Angiosperm Pollen and the Origin and 
Early Evolution of Flowering Plants James W. Walker & Audrey 
G Wake Ее 464 
Contents continued on back cover 


VOLUME 71 
1984 
NUMBER 2 


ANNALS 


OF THE 
MISSOURI BOTANICAL GARDEN 


The ANNALS, published four times a year, contains papers, pri- 
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EDITORIAL COMMITTEE 


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© Missouri Botanical Garden 1985 


LOS 


Dr. Jan Muller 1921-1983 


—— 


ANNALS 


OF THE 


MISSOURI BOTANICAL GARDEN 


VOLUME 71 1984 NUMBER 2 


Dedication 


This symposium issue is dedicated to Dr. Jan Muller in recognition of his 
work on the systematics and fossil history of angiosperm pollen. His careful 
and analytical studies resulted in many pioneering and landmark papers. 
Jan Muller’s careful observations and critical evaluations of fossil pollen 
records had an important impact upon the way in which his colleagues 
presently apply angiosperm pollen records to the history of this group. His 
leadership in assessing the fossil pollen records of extant angiosperms is 
recognized by research scholars around the world. Jan Muller’s enthusiasm 
for searching out the truth of angiosperm lineages and his honest appraisal 
of the relationships of fossil angiosperm pollen to extant taxa will always 
be appreciated by his colleagues. 


HISTORICAL PERSPECTIVES OF ANGIOSPERM EVOLUTION 


Symposium volumes represent temporal nodes 
that lend themselves to taking stock of various 
disciplines. In the case of angiosperm paleobot- 
any, the last major symposium volume, “Origin 
and Early Evolution in Angiosperms," C. B. Beck 
(editor), appeared eight years ago. Although that 
particular volume (Beck, 1976) stressed origin 
and early evolution only, some appreciation of 
changes in emphasis and approach in angio- 
sperm paleobotany since that time may be gained 
by considering this volume in the perspective of 
its predecessor. 

Historically, angiosperm paleobotany turned 
a corner 15—20 years ago. And in some ways, 
several papers published since that time repre- 
sent a mess change in the Character of the 
field th g t n line 
with ap paleontological нене Pre- 
viously, floristic investigations were emphasized 
and attention to individual fossils, their mor- 
phological characters and critical assessments of 
their affinities were secondary. As a result, gen- 
erally, studies of relatively Recent (Neogene) flo- 
ras had much validity while the identifications 
based on superficial features made many conclu- 
sions based on studies of older fossils erroneous 
(Dilcher, 1974). In addition, little was contrib- 
uted to our understanding of evolution within 
the angiosperms. The confusion resulting from 
such approaches is well known. 

As problems became evident in older paleo- 
botanical research, the direction in angiosperm 
studies shifted to a more careful approach em- 
phasizing the evaluation of the fossils themselves 
and the establishment of their affinities. This 
largely empirical direction was an important ele- 
ment in angiosperm paleobotany for a long time. 
Perhaps the excesses of previous researchers in- 
duced the response of willful myopia in many 
scientists during this conservative phase of an- 
giosperm paleobotany. Whatever the motivating 
factors, it is only 15 to 20 years since the begin- 
ning of the trend in angiosperm paleobotany in 
which the investigation of evolution has been 
based upon речну devised systematic techniques 
and the of extinct angiosperm forms, 
as well as patterns in the fossil record. 

The present collection of papers provides an 
opportunity to gain some overview of the con- 
temporary field of angiosperm paleobotany and, 
thus, to see how emphases have changed. While 


ANN. MISSOURI Bor. GARD. 71: 348—350. 1984. 


these manuscripts do not illustrate all that has 
been done recently in angiosperm paleobotany, 
they provide a representation of current work in 
this field. It is now possible to observe that cer- 
tain areas of emphasis that were gathering mo- 
mentum ten years ago have continued to become 
increasingly important, while other entirely new 
areas of concentration have become significant. 
These following papers, as contributions to an 
international symposium on angiosperm paleo- 
botany, represent a broad spectrum of research 
in both subject and philosophy. It would cer- 
tainly serve our immediate purposes if all of them 
could be nested neatly under the rubric of mod- 
ern angiosperm paleobotany and if each illus- 
trated some extension of a commonly held phi- 
losophy. Yet the fact that this cannot be easily 
done is quite informative. There remain differ- 
ences in approach in the modern scientific com- 
munity studying angiosperm paleobotany, and 
there remain significant differences in attitude. 
These extend at times even to varying interpre- 
tations of particular fossil organs. Certainly, with 
respect to modern angiosperm paleobotany, V. 
Krassilov is an iconoclast whose contribution 10 
this volume reveals more than his attitude. Kras- 
silov’s paper makes it clear that there are certain 
enigmatic early angiosperm fossils that need fur- 
ther investigation and that there is still disagree- 
ment as to the interpretation of angiosperm an- 
cestry within the paleobotanical community. The 
contribution by Hughes also stands somewhat 
apart because he takes an overview pointing t° 
some of the nagging problems in Mesozoic an- 
giosperm paleobotany and makes some inno- 
vative proposals to deal with them. " 
The other papers are easier to group and 1 
lustrate where the field has been going during the 
past few years. Perhaps most obvious is the ua 
tinuity in studies of angiosperm pollen ip 
(1969), Muller (1970), and Brenner (1963, 19 л 
had (and continue to have) important i -— í 
during the late 1960s and early 1970s. роу“ 
contribution was noteworthy because it S 
pattern in the context of evolution while pu 
stressed evolutionary history in the соз = 
Ро сонор. and Muller emphasized p: 
mportance of the critical evaluation іп paly” 
ogy to reveal past record of extant flowering 
plant " 
p of palynology continue to stress pat 


и 


=p — - ——ÀM — 


= 


—— 


— 


— 


1984] 


tern and history, but, in this volume, micro- 
morphology and ultrastructural analysis are also 
important. Walker and Walker illustrate how 
careful analysis of single Lower Cretaceous paly- 
nomorphs can contribute to our understanding 
of variation in early angiosperm pollen, variation 


248 


2 1 4 
unnoticca WITMOUL 


that might | 


mv m 
the application of modern techniques, and point 
out similarities between certain well-known Cre- 
taceous palynomorphs and pollen of modern taxa. 
Zavada concentrates on morphological analysis 
of monosulcate pollen by proposing evolutionary 
trends based on modern taxa and carefully eval- 
uating taxonomic characters used to distinguish 
angiosperm pollen from gymnosperm pollen. 
then examines certain fossil palynomorphs, often 
pre-Cretaceous, in the context of their possible 
significance to angiosperm origins. Muller sum- 
marizes angiosperm history based on the paly- 
nological record and notes significant events in 
angiosperm evoluti d luti y patterns. 
Muller's selective approach to the palynological 
literature, based on careful morphological anal- 
ysis, gives credibility to the utility of the dis- 
persed pollen record in d ti i 
history. 
| А relatively new area of angiosperm research 
involving the study of flowers and inflorescences 
has become a significant part of angiosperm pa- 
leobotany. Since serious investigations of fossil 
flowers and inflorescences have begun (e.g., Cre- 
Pet et al., 1974, 1975; Tiffney, 1977), such in- 
vestigations have become more common and 
àve been conducted at various levels. Further 
evidence of their continuing importance are four 
Papers reporting new floral finds by Dilcher and 
Crane, Crane and Dilcher, and Schaarschmidt 
and Friis. Fossil floral remains have also been 
used in the paper by Crepet to assess the im- 
Portance and success of faithful pollinators in 
flowering plant history. 

Another important and interesting aspect of 
angiosperm paleobotany involves emphasis оп 
fruits. Bruce Tiffney’s contribution to this sym- 
Posium volume incorporates fruit and seed data 
In an analysis of the history and significance of 
animal dispersal of angiosperm fruits. Crepet and 
Tiffney's contributions both emphasize plant- 
animal interactions in an effort to assess the sig- 
nificance of animal involvement in angiosperm 
radiation and speciation from fossil data. Dilcher 
and Crane and Crane and Dilcher combine anal- 
yses of both fruiting material and flower forms, 
demonstrating that some early angiosperms 


е = + 


INTRODUCTION 


349 


shared the characteristic features and apparent 
reproductive biology of the Magnoliidae. Several 
associated plant organs are assumed to represent 
a single taxon based upon stratigraphy and anat- 
omy in an effort to reconstruct a whole flowering 
and fruiting shoot of an ancient angiosperm. The 
flowering shoot has features which indicate that 
the co-adaptive evolution between floral mor- 
phology and pollinators was important by the 
mid-Cretaceous. 

af studies have been extremely important 
and recent emphases on fine venation analysis 
and cuticular features of fossil leaves have prov- 
en essential in interpreting their affinities (Hick- 
ey, 1973; Dilcher, 1974). The significance of pol- 
len and leaf remains from the Atlantic Coastal 
Plain are well known (Hickey & Doyle, 1977), 
and Upchurch has analyzed patterns in the evo- 
lution of the cuticular features of angiosperm 
leaves from these deposits. 

Emphasis on pattern with an eye on evolution 
in an ecological context continues to be impor- 
tant in angiosperm paleobotany. Such emphasis 
transcends the analysis of any one particular type 
of organ. However, sources of data once thought 
beyond the scope of angiosperm paleobotany (e.g., 
leaf cuticles, pollen ultrastructure, and floral 
structure) are proving valuable sources of insight 
into different aspects of angiosperm history that 
will prove important in understanding their evo- 
lution. In addition, it is obvious that morpho- 
logical analysis has become extremely important 
in angiosperm paleobotany giving credibility to 
the assessment of relationships between fossil and 
modern taxa, providing a better idea of past vari- 
ation, and potentially allowing a better assess- 
ment of homologies. 

From the paleobotanical work represented here 
it is possible to speculate on the areas of impor- 
tant directions in angiosperm paleobotany. First, 


p у Р о 
to our understanding of the process of evolution 
and to the understanding of certain evolutionary 
events in the context of ecology. Second, increas- 
Tee P god foe NS hological analysis, char- 


ingly SOp р E 
Rond state analysis, and knowledge of variability 
in extant as well as related extinct taxa combined 
with increasingly sophisticated systematic meth- 
ods have great potential for having fossil angio- 
sperm data make an important contribution to 
the classification of the flowering plants. Finally, 
it should be evident that empirical contributions 
(i.e., studies of fossils, their affinities, analysis of 
their characters in the context of related modern 


350 


taxa including the establishment of homologies) 
will continue to be an important aspect of an- 
giosperm paleobotany. 


LITERATURE CITED 


BECK, С. B. 1976. Origin and Early Evolution of Ап- 
osperms. Columbia Univ. Press, New York. 
BRENNER, G. J. 1963. The spores and pollen of the 
Potomac Group of Maryland. Мауна! Dept. 
Geol. Mines Water Resources 27: 
1967 


= 


їп the Albian to Cenomanian deposits of Delaware 
(USA). Rev. Paleobot. Palynol. 1: 219-227. 


angio sperms from the Eocene of No 
a catkin with e вингса affinities. Amer. J 
Bot. 62: 813-8 


DiLCHER, D. L. T Approaches to the identifica- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


tion of angiosperm leaf remains. Bot. Rev. (Lan- 
caster) 40: 1-157. 
Doy te, J. A. 1969. Cretaceous angiosperm pollen of 
the Atlantic Coastal Plain and its evolutionary sig- 
1- 


old A ; 30: 

Cl sification of the v— 
of dicotyledonous leaves. Amer. J. Bot. 60: 17- 
33. 


& J. А. DoyLE. 1977. Early Cretaceous fossil 

evidence for angiosperm evolution. Bot. Rev. 
(Lancaster) 43: 3-104. 

MULLER, J. 1970. Palynological evidence on early 
differentiation of angiosperms. Biol. Rev. Biol. 
Proc. Cambridge Philos. Soc. 45: 417-450. 

TirrNEv, B. Н. 1977. Dicotyledonous angios 
flower from the Cretaceous of Martha's ems 
Mass. Nature 265: 136-137 


— David Dilcher, Department of Biology, Indiana Uni- 
versity, Bloomington, Indiana 47405; and William 
Crepet, Biological Sciences Group U-42, University of 
Connecticut, Storrs, Connecticut 06268. 


-- 


ARCHAEANTHUS: AN EARLY ANGIOSPERM FROM 
THE CENOMANIAN OF THE WESTERN 
INTERIOR OF NORTH AMERICA! 


DAVID L. DILCHER? AND PETER R. CRANE? 


ABSTRACT 
ccrta ое Аалу чайн Dilcher & Crane, gen. et sp. nov., а multifollicular angiosperm fruit, is 
де he mid-Cretaceous (uppermost Albian-mid-Cenomanian) Dakota Formation of cen- 
tral m alee goes of follicles were borne terminally at the apex of a stout branch with helically 


ged leaves. Each cluster comprised 100-130 
The f follicles were stalked with 


is linked wit 
v. and Archaepetala obscura Dilcher 


CHUAL Y 


a short, rounded tip and dehisced along a single adaxial suture. Ovules 


scales (Kalymmanthus walkeri Dilcher & Crane, gen. et SP. nov.), and leaves (Liriophyllum FA deis 


Dilcher & Crane, sp. nov. 
of distinctive resin-bodies | 


us does not predate other kinds of an 


Liriophyllum populoides Lesq. is shown to be a separate species. The 
us plant is most closely related to Recent M 
ical 10 archet 


predicted by magnoliid flo 


angiospe 
record but conclusively demonstrates the existence of magnoliid- "ike plants and flowers early in 
ап поп 


giosperm evolut 


Hypotheses of flowering plant phylogeny are 
inextricably linked to the evolutionary interpre- 
tation of angiosperm reproductive organs and 
thus to concepts of the primitive angiosperm 
flower. Traditionally such ideas have been based 
Оп comparative studies of living plants, and the 
fossil record has made little contribution. In re- 
cent years, however, knowledge of early angio- 
Sperm reproductive diversity has increased, and 
Paleobotanical data relevant to these problems 
have begun to accumulate. In this paper we de- 
Scribe a new species of mid-Cretaceous е 
sperm known from multifollicular fruits, pe 
anth parts, bud-scales, and leaves, and MUN 


posee ee 


its relevance to concepts of floral evolution in 
flowering plants. 

The earliest speculations on the nature of the 
primitive angiosperm flower developed from the 
pre-Darwinian classifications of the eighteenth 
and nineteenth centuries and polarized into two 
principal hypotheses: either the simple, unisex- 
ual and cesare il wind-pollinated flowers 
ofthe A (Engler, 1897; 
Strasburger et al., 1898; Rendle, 1925, 1930; 
Wettstein, 1935) or the bisexual and predomi- 
nantly insect-pollinated flowers of the magnoliid 
(Ranalean) angiosperms most closely approxi- 
mate to the ‘ancestral’ flower (Bessey, 1897, 1915; 


' We thank C. Beeker , W. L. Crepet, С. J. Gastony, M. B. Farley, E. M. i HR Hattin, E. Kauffmann, and 
eyno 


p; Longstreth for their advice and Á— at various stages of the work; H. 


olds, M. Walker, and F. 


Аена Fort Hays State University, K 


ical Garden and the United Soie National Museum for the loan of specimens; A. Linnenberger and E. 


berger 
Quasthoff for drawi 
oT p provided for P. R. анд 
versity Research Board are gratefully acknowl 


5 research was 


drawing 
supported by NSF grant DEB 77-04846 to D. 1. 


for Permission to one material; and Megan Rohn for 
ng 
during the early part of the study by the British Council and Reading 


9 and 70, and porem 
. Dilcher. 


ва of Biology, Indiana University, Bloomington, Indiana 4 


` Departm 
Illinois 60605 


ANN. Missouri Bor. GARD. 71: 351-383. 1984. 


47405. 
ment of Geology, Field Museum of Natural History, Roosevelt Road at Lake Shore Drive, Chicago, 


352 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


Arber & Parkin, 1907). Subsequent investiga- 
tions and i I i particularly of anatom- 
ical (Bailey, 1944; Eames, 1961; Dickison, 1975) 
and palynological evidence (Wodehouse, 1935, 
1936; Walker 1974a, 1974b, 1976), led to the 
widespread acceptance of the second hypothesis, 
that the Magnoliidae are the most primitive liv- 
ing group of flowering plants and exhibit the most 
primitive floral morphology. This hypothesis is 
central in most of the putatively ‘phylogenetic’ 
classifications of flowering plants that have been 
proposed in the last 50 years (Hutchinson, 1959; 
Cronquist, 1968, 1981; Takhtajan, 1969; Steb- 
bins, 1974; Thorne, 1976; Dahlgren, 1980), and 
although alternative viewpoints have been sug- 
gested (Corner, 1949; Melville, 1962, 1963; 
Meeuse, 1966), none have been widely accepted. 
Along with the development of the magnoliid 
hypothesis has come the recognition of ‘evolu- 
tionary trends' for a wide range of characters. 
The primitive states in these trends have been 
combined into a concept of a hypothetical an- 
giosperm morphotype (Takhtajan, 1969). 

Until recently, direct paleobotanical evidence 
relevant to these evolutionary hypotheses has 
been conspicuously absent. The last two decades, 
however, ha iderable ad in an- 
giosperm paleobotany and an increasing aware- 
ness of the relevance of fossil material to con- 
cepts of flowering plant evolution (Doyle & 
Hickey, 1976; Hickey & Doyle, 1977; Hughes, 
1976; Doyle, 1978; Dilcher, 1979). A major ra- 
diation is regarded as having occurred during the 
Barremian to Cenomanian stages of the mid- 
Cretaceous, followed by further diversification 
throughout the Upper Cretaceous and Tertiary. 
No unequivocal angiosperms have so far been 
reported from pre-Barremian rocks, althou 
there are many earlier, potentially relevant fossil 
plants about which we know too little (Doyle, 
1978; Hill & Crane, 1982; R. A. Scott et al., 
1960). Despite some insight into the timing of 
angiosperm evolution, the systematic origin of 
the group remains a mystery that continues to 
stimulate a variety of speculations (Melville, 
1962, 1963; Meeuse, 1966; Retallack & Dilcher, 
1981a). Such conjectures inevitably reduce to 
discussions of homology, particularly of repro- 
ductive structures, and have been severely lim- 
ited by inadequate knowledge of early flowering 
plants. Few of the mid-Cretaceous angiosperms 
are known in detail from flowering or fruiting 
specimens, and even fewer are known from both 
vegetati d reproducti aterial. The species 


described in this paper is currently one of the 
more completely understood of all early angio- 
sperms. We propose the name Archaeanthus lin- 
nenbergeri for multifollicular fruits and the veg- 
etative branches on which they are borne. This 
species is linked with two kinds of perianth parts 
(Archaepetala beekeri Dilcher & Crane, gen. et 
sp. nov. and Archaepetala obscura Dilcher & 
Crane, sp. nov.) bud-scales (Kalymmanthus 
walkeri Dilcher & Crane, gen. et sp. nov), and 
leaves (Liriophyllum kansense Dilcher & Crane, 
Sp. nov.) as parts of a single fossil plant on the 
AUI. dud jux Mox 


that all these organs contain the same distinctive 
resin-bodies. Liriophyllum populoides Lesq. is 
shown to represent a different species. The re- 
constructed Archaeanthus plant is closely allied 
to the Magnoliidae sensu lato, and in some fea- 
ti 1 а thetical 10 rm 


ene 


morphotype predicted by magnoliid floral the- 


MATERIAL 


With the exception of the specimens of Lir- 
ў Es | CP | ENS 2.1 mmen 


` of Archaeanthus linnenbergeri, from Morrison, 


Colorado, all of the material described in this 
paper is from the Dakota Formation at Linnen- 
berger’s Ranch near Bunker Hill, Russell God 
ty, central Kansas (see Retallack & Dilcher, 
1981b, 1981c, for details of this locality). The 
plant material is preserved as compressions 1n à 
brown-gray clay with variable amounts of sand 
and silt. The specimens typically have good or- 
ganic preservation. The associated macroflora 15 
dominated by about 15 to 20 kinds of ке 
sperm leaves, but although the microflora 15 ps 
preserved, angiosperm pollen accounts for "ч 
about 25% of the total palynomorphs. Most 0 
the Linnenberger Ranch material described E 
this paper comes from a narrow sandy bed, lo al 
in the secti NECS lity; some of this mater! 
has been previously described by Dilcher et e 
(1976, 1978) and Dilcher (1979). The а 
berger plant assemblage is interpreted as а ы 
of local origin, deposited in a fluvial wae nud 
distal flanks ofal t (Ret Пас 
ег, 19815, 19810). даце 
In central Kansas, the Dakota rome Р 
hihite AS “сш 3» 2 1 1; f 


alnoica yi 


ation but has been divided into two мао 
the Terra Cotta Clay Member below, an nó: 
Janssen Clay Member above (Plummer & and 
mary, 1942). These are not mappable units 


=e 


- 


-"—— 


1984] 


are clearly facies-related (Franks, 1975), but the 
Terra Cotta Clay Member typically consists of 
gray to greenish gray clays and shales with abun- 
dant lenticular, fine- to coarse-grained sandstone 
units, whereas the Janssen Clay Member consists 
of gray to dark gray claystones, siltstones, and 
shales with lenticular sandstones. Lignites are 
particularly abundant in the upper parts of the 
Janssen Clay Member (Schoewe, 1952). The Ter- 
ra Cotta Clay Member is interpreted as predom- 
inantly fluvial and overbank, alluvial plain sed- 
iments deposited by streams flowing from the 
north and east, whereas the Janssen Clay Mem- 
ber represents a greater range of paleoenviron- 
ments, some of which, particularly in the higher 
parts of the section, were associated with the 
transgressing mid-Cretaceous Graneros Sea (Sie- 
mers, 1971; Franks, 1975). The sedimentology, 
paleontology, and other aspects of Dakota For- 
mation geology are considered more fully by 
Plummer and Romary (1942, 1947), Siemers 
(1971), Hattin and Siemers (1978), Bayne et al. 
(1971), and Retallack and Dilcher (198 1b, 198 1c). 
The Linnenberger Ranch material comes from 
the Janssen Clay Member, relatively high in the 
Dakota Formation. The classic Dakota Sand- 
Stone Flora described by Lesquereux (1868, 1874, 
1878, 1883, 1892), Gress (1922), and Newberry 
(1868) is probably predominantly from the sand- 
Stone facies of the same Member. 

Toward the south and west, the Dakota For- 
mation overlies the Kiowa Shale (Franks, 1975), 
Which is dated on evidence of marine fauna and 
palynomorphs as late Albian (R. W. Scott, 1970a, 
1970b; Ward, 1981), and in the north and east 
oversteps onto older Paleozic rocks. In the south 
and west it interdigitates with, and is overlain 
by, the Graneros Shale, a shallow-water marine 


of the G cyclothem. Sediments from the 
transitional zone represent a considerable diver- 
sity of marginal marine environments. Marine 
invertebrates securely date the Graneros as Cen- 
отапіап (Hattin, 1965; Eicher, 1975) and ra- 
diometric determinations of the *X bentonite' in 
the upper part of the Graneros (Hattin, 1965, 
1967) give an age of about 94.5 Ma (Kauffman, 
Pers. сотт.). Palynological investigations 
(Doyle, pers. comm.; Ravn, 1981) similarly in- 
dicate a Cenomanian age probably equivalent to 
Zone III of the palynological zonation establish 

by Brenner (1963), Doyle (1969), Doyle and 
Robbins (1977), and others for the mid-Creta- 
Ceous of the Atlantic Coastal Plain. Zavada (pers. 


DILCHER & CRANE—ARCHAEANTHUS 


353 


comm.) has shown that the palynofloras from 
the upper Dakota Formation and Graneros are 
similar and contain about 20-35% angiosperm 
pollen, whereas the upper Kiowa Shale contains 
less than 5%. On the basis of all the evidence 
available, it seems likely that the Dakota For- 
mation of central Kansas extends across the Up- 
per and Lower Cretaceous boundary (Zeller, 1968; 
Kauffman et al., 1976). The fossil plants dis- 
cussed in this paper from the Janssen Clay Mem- 
ber, therefore, date approximately from the Up- 
per and Lower Cretaceous boundary and are of 
uppermost Albian or lowermost Cenomanian age. 

The specimens of Liriophyllum populoides 
originally described by Lesquereux (1883) and 
discussed in this paper are from the Dakota Group 
of Morrison, Colorado, which, on the western 
edge of the Denver Basin, comprises the Lytle 
Formation below and the South Platte Forma- 
tion above (Waage, 1955). The South Platte For- 
mation consists of dark gray to black shales and 
theri dst d ited in a range 


brown g p 
of marine-influenced estuarine, littoral, and al- 
luvial plain environments (Waage, 1955; Wei- 
mer & Land, 1972). The majority of the ‘Dakota 
Sandstone’ plants from Morrison described by 
Lesquereux (1883) and Knowlton (1896, 1920) 
come from the Kassler Sandstone Member in the 
upper part of the South Platte Formation (Lee, 
1920; Waage, 1955), equivalent to part of the ‘J’ 
sandstone (Weimer & Land, 1972) or the lower 
part of ‘genetic unit C’ (Weimer, 1970). They are 
preserved as impressions in a hard, pale gray 
sandstone. The Kassler Sandstone Member 

des | lly into th i kull Creek Shales 


1110 


cheanus (Waage, 1955) and is generally accepted 
as upper Albian in age (Waage, 1955; McGookey 
et al., 1970; Kauffman et al., 1976; Berman et 
al., 1980). 

Specific acronyms are used to designate the 
source of the fossil material studied. IU stands 
for Indiana University, HU stands for Harvard 
University, and USNM stands for United States 
National Museum, which is housed at the Smith- 
sonian Institution. 

SYSTEMATICS 

In this section we describe six species repre- 

ds of Itifolli fruits 


senting four ! g 
(Archaeanthus linnenbergeri), leaves (Liriophyl- 
lum populoides, L. kansense), putative perianth 
parts (Archaepetala beekeri, A. obscura), and 
probable bud-scales (Kalymmanthus walkeri). 


354 


The measurements in the descriptions are based 
on all the material cited. Ranges and common 
dimensions are given in parentheses where avail- 
able. 


Archaeanthus Dilcher & Crane, gen. nov. TYPE: 
Archaeanthus linnenbergeri Dilcher & Crane, 
sp. nov. 


DIAGNOSIS: Reproductive axis a cluster of fol- 
f 


licles (a multifollicular fruit) with evidence o 
having been subtended by other floral organs. 
Receptacle stout, elongated, consisting of a distal 
tapering gynoecial zone bearing helically ar- 
ranged follicles, with a shorter, more or less cy- 
lindrical zone below, showing circular and ellip- 
tical scars. Base of the flower delimited by three 
transverse, narrowly elliptic, slit-shaped scars. 
Follicles ellipsoidal, stalked, with a short, round- 
ed tip and a distinct adaxial suture; containing 
numerous seeds. 

DERIVATION: From archae—Greek, meaning 
beginning or first; anthos— Greek, meaning flow- 
er. 


A h 4L 


li bergeri Dilcher & Crane, sp. 
nov. HOLOTYPE: IU 15703-4152. 


DIAGNOSIS: As for the genus. 

REFERENCES: ‘Magnolia species, Lesquereux 
(1883: 73, pl. 11, fig. 6, brief description and 
drawing). 

‘Reproductive axes of Liriophyllum, Dilcher 
et al. (1976: 854, fig. 1a, b, d, brief description 
and discussion with photographs and a line 
drawing). 

"Reproductive axis’ (Carpites liriophylli Les- 
quereux, 1883), Dilcher (1979: 311, figs. 40, 50, 
51, brief discussion with photographs and line 
drawings. Carpites liriophylli is too poorly pre- 
served to evaluate its similarity with our species). 

OTHER MATERIAL: IU 15703; 2300, 2317, 2318, 
2590, 3022, 3837, 3907, 4105, 4112, 4134—4150, 
4152, 4153, 4155-4158, 4163, 4164, 4166—4170, 
4198, 4532-4534. 

NUMBER OF SPECIMENS EXAMINED: 44. 

FIGURES: 1—37, 60a, f-h. 

DERIVATION: After Albert and Edward Linnen- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Мог. 71 


berger, owners of the central Kansas locality from 
which this material was collected. 
DESCRIPTION: Clusters of follicles (multifolli- 
cles) borne terminally and singly at the apex of 
a substantial vegetative branch 11—16 mm diam. 
Branch bearing helically arranged leaf scars at 
intervals of 28-35 mm. Leaf scars broadly ellip- 
tic, 1.5-3.3 mm long, 2.5 mm wide, pointed on 
either side. Surface of axis with occasional short, 
irregular, longitudinal, and transverse striations. 
Maximum length of branch preserved, 145 mm. 
Total length of the longest specimens seen, in- 
cluding branch and receptacle, 215 mm. 
Receptacle elongated to 137 mm long (longest 
specimen incomplete). Gynoecial zone distal with 
irregular longitudinal ribs, elongating during de- 
velopment; most complete immature specimen 
47 mm long, 7 mm wide at the base; longest 
mature specimen 137 mm long (incomplete), 8- 
12 mm wide at the base. Gynoecial zone grad- 
ually tapering distally and bearing 100-130 fol- 
licles. Immature carpels packed into a loose fas- 
cicle forming an ellipsoidal head ca. 22 mm diam., 
50 mm high. Mature follicles loosely aggregated 
into an elongated conical head, ca. 70 mm diam. 
and to 152 mm high. Follicles borne helically 
leaving elongated, diamond-shaped scars, 1. 
mm long, 0.75-1 mm wide on the mature ге 
ceptacle. Upper part of scars deeply impressed 
into the axis, becoming shallower in the lower 
half R le below th gy 2 chort 
or less cylindrical, 7-9 mm long, tapering from 
11-15 mm wide proximally to 8-12 mm distally 
in mature specimens. Receptacle immediately 
below th gy ial b ing ca 50-60 trans- 
versely elongated, elliptical scars ca. | mm broad 
(interpreted as those of stamens), followed — 
by 6-9 larger, more or less circular scars са. 
mm diam., apparently arranged in pairs ~~ 
preted as those of inner perianth parts). Вазе 0 
receptacle delimited by three prominent, паг- 
rowly elliptical, slit-shaped transverse scars 
pointed at either end, 2-3 mm high, 1 1-13 s 
wide (interpreted as those of outer perianth wa 
Pedicel with a distinct transverse ridge ca- ? 
25 mm below the most proximal floral scars. 
Pedicel gradually broadening toward the ridge. 


+, 
HF ~ 


FIGURES 1-2. Archaeanthus linnenbergeri Dilcher & Crane, gen. et sp. nov., IU 15703-4152.— 1. Branch 


bearing the lower part of a receptacle with 
attached to the receptacle, x 1.—2. Detail 


8 
a cluster of follicles at the apex. Follicles on the extreme le, 
of specimen in Figure 1 showing two scars at the base of the receptac 


| 


1984] DILCHER & CRANE—ARCHAEANTHUS 355 


between t пе. large scars and th 
of the gynoecial z of gynoecial zone. b, c. Un со Ged ae 
топе. Compare with Figures 4 and 66, x2.5.a gy 
ye zone of the е d. Scars b outer perianth ‘whorl. e. Pair tor scars on pedicel attributed to a calyptra. 
scar. 


interpreted as part of a whorl of three. Note the zone of the дај зр 


356 


Ridge bearing at least 2 narrow, transverse scars 
about | mm high (interpreted as those of bud- 
scales). 

Immature carpels slightly reflexed, ca. 16 mm 
long, 1 mm wide, with rounded tips. Mature fol- 
licles ellipsoidal, more or less straight, occasion- 
ally slightly reflexed. Individual follicles 25—35 
(-38) mm long, (1-)4-7(-11) mm wide; length 
of locule (10-)20-29(-31) mm. Follicles con- 
tracted proximally into a stalk, 4.5-8 mm long, 
and distally into a short, rounded apex. Apex 
sometimes shortly two-lobed; lobes formed b 
the two adaxial crests at the apex of the follicles. 
Stalk 1-2 mm wide at its midpoint, broadening 
proximally to 1.5-4 mm at the point of attach- 
ment to the receptacle. Angle of attachment typ- 
ically 50—80°. Follicles, when shed, breaking away 
at the base of the stalk 

Mature follicles with a median, longitudinal, 
adaxial suture along the entire length, flanked on 
either side by a ridge 1 mm high, forming an 
adaxial crest. Cuticle of adaxial crest bearing long, 
simple, unicellular trichomes. Follicles with a 


a 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


single weak abaxial rib extending along the entire 
length. Locule uninterrupted, but in a few spec- 
imens transversely constricted by regular or ir- 
regular, ridges and surface undulations into 10- 
18 weakly delimited oval units (interpreted as 
indicating positions of seeds), 2-3 mm high, !- 
? mm wide. These units more ог less confined 
upper two-thirds of laterally compressed 
RES each unit frequently with a central area 
of dark organic matter. 
Mature follicle wall of at least two distinct lay- 
rs. Endocarp striated, comprised of transverse, 
ы packed fibers, 10-20 um wide. Fibers fre- 
quently separated to form prominent transverse 
cracks in compressed follicles. Exocarp with no 
visible cellular detail. 


fah 1f 


100) ovules borne (presumably along either side 
of the adaxial suture) 1-2 mm below the outer 
surface of the adaxial crest. Ovules arranged close 
together and overlapping, elliptical, ca. 2 mm 
long, ca. 0.75 mm wide; one end pointed and 
oriented adaxially, the other rounded. Ovules 


AES 


ES 3-6. Archaeanthus linnenbergeri Dilcher & Crane, gen. et sp. nov.—3. IU 15703-2300. Co 


FiGUR 
phones showing the upper gynoe 


d carpels, x16. IU 157052208 = 


several mature follicles attached to the receptacle. Note the ridged receptacle with helically arrang 
x2. 


а scars left by the follicle bases, 


FIGURES 7 


several follicles attached to a long 


-12. Archaeanthus А geri ры & Crane, gen. et sp. nov.—7. IU dale putem 
recep pare о x1.— 


of 


15 he mpare Lesquereux, 1883: 7 в. 6), х1.—11. Detail of specimen in Figure 10 showing m 
blunt-tipped carpels, x 4.— 12. Detail ма specimen in Figure 9 br a. Base of gynoecial zone. b, с. 2. 
гена middle zone of receptacle. d. Large scar of outer perianth whorl delimiting the base of the flower, Р 


FIGURES 13-21. 
follicle showing penetration of sedim 
о х2 


Note the blunt, bilobed tip of the central follicle fo 


15703-4167. Isolated follicle with distorted us and blun 


suture, x2.— 19. IU 15703-4157. Detail 
tip formed by the adaxial crests. Note m 
20. IU 15703- 2318'. 


follicle surface, x 


edian | на na groove in the abaxial surface 


haped sT um caused by resin-bodies in the follicle 


Archaeanthus самара ви Dilcher & Crane, gen. et sp. nov.— IU 15703-2317. Isolated 
nt through the adaxial suture, which has preserved a three-dimensio 
me ce as Figure 13 with bo: locule cast ы to show the а п 


n * rock and 
men as Figure 13 removed у of the same 


rmed ha Be ip part of the а те eo oe axial 


ad 


n thee rea, x4 2, ‘a 5 
wall. Note the longitudinal ridge in the abaxial 


DILCHER & CRANE—ARCHAEANTHUS 357 


1984] 


ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


358 


y% 


% 


ee 


wut 


1984] 


DILCHER & CRANE—ARCHAEANTHUS 


359 


360 


upper part of the follicle, x "най 
follicles showing irregular outlines of seeds and one possible seed in situ (h), x 6.—25. IU 15703-2300". 
of follicle showing possible in situ seed (h), x10. 


with a single cutinized membrane, showing dis- 
tinct cell outlines, delimited by very finely un- 
dulating anticlinal flanges. Pointed end heavily 
cutinized toward the tip, cell outlines more or 
less square, ca. 10 um in both dimensions. Blunt 
end with a distinct, regular, oval to circular per- 
foration, ca. 80 um diam. Cell outlines in the 
median part of the membrane and near to the 
perforation elongated, 20-30 um long, 5-10 um 
wide. 


Carpels, receptacle, and branches all contain 
numerous, yellow-brown lustrous, resin-bodies, 
(60—)70—100(-120) um diam. 

DISCUSSION: Archaeanthus linnenbergeri is 
known from 44 specimens, all preserved as 
compressions in a sandy, silty, brown-gray clay. 
Many have appreciable organic material re- 


Three specimens (Figs. 1—4, 9. 12) show the 
manner in which the clusters of follicles (mul- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


24. IU 15703-2300'. Detail of two laterally comp 


tifollicles) and, hence, flowers were borne singl y 
at the apex of a stout, presumably woody 4x15. 
They suggest that tl Itifollicl ay not s 
been shed at maturity. The three helically е. 
ranged scars on the vegetative branch (Fig. 1) " 
the correct size and shape to correspond to p 
flated, petiole bases, such as those of small ж 
iophyllum leaves. The upper scar is substanti : 
larger than the lower two and presumably bo 
a larger leaf. z 
Two specimens (Figs. 10, 11, and IU kes 
4533) are immature, presumably aborted, ро” 
cial portions of the receptacle and are very pe 
ilar to the ‘Magnolia’ receptacle figured by se 
quereux (1883: 73, pl. 11, fig. 6). These фе ш 
show that the gynoecium was siete p 
r, 
development and elongated Basho IU 15703 
4136 (Fig. 5) as the fruits and seeds mater 
The organization of the receptacle at matur 


1984] 


DILCHER & CRANE—ARCHAEANTHUS 


FIGURES 26-31. 
electron micrograph 


x50.—29. TU 15703-2300. Scanning elect 


ron micrograph of a 


Archaeanthus iiri i с Crane, gen. et sp. поу. — 26. IU 15703-2300. Scanning 
f fibers on the surface of a locule cast, х5 
wing impression of adaxial crest 8) and е ien (i). Note the "eere 


0.— 27. IU 15703-2300. 


n-bodies, x12 


IU я 4105. Cuticle of cer hisce showing scp tO cell outlines and the distortions caused by resin- 


de х 300. — 31. IU 15703-4 
жалы caused by ни х 50. 


is clear in the three specimens (Figs. 1—4, 9, 12) 
that have the base of the receptacle preserved, 
=> попе of our specimens show the com- 
€ngth of the mature gynoecium with at- 
A: follicles. The most information can be 
П Оп the axis with the lower part of a recep- 
his Preserved on IU 15703-2300 (Figs. 3, 4). 
IS axis has no attached follicles but is identified 


with A. linnenbergeri by the numerous resin- 
bodies which it contains. It may be the lower 
part of the well-preserved gynoecium with at- 
tached follicles to which it is adjacent. By com- 
parison with IU 15703-4150 (Figs. 9, 12), we 
interpret the four semi lar marks at the bro- 
ken upper edge of this specimen (Fig. 4) to be 
the base of the gynoecial zone. Immediately be- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


Mem- 
FIGURES 32-37. Archaeanthus linnenbergeri Dilcher & Crane, gen. et sp. nov.—32. IU чы d 
branes macerated from follicle fragment int erpreted as the nucellar or inner integumen mem 


or aborted o 


the micropylar ends, and the ro S with a circ 


isodiametric cell outlines, x 200. va IU 15703-4105. Two ovule membran 
tail of Wade chalazal perforatio 
membrane 


showing finely undulating cell outlines, 


low these marks are laterally elongated elliptical 
scars; about 12 are clearly visible, and we esti- 
mate that this zone of the receptacle probably 
contained 50—60 such scars. We interpret them 
as indicating the former position of stamens. Be- 
low this point on the receptacle is another zone 
of larger scars in which two pairs are clearly vis- 
ible. We estimate that in life there may have been 


x 200. —36. IU denen 4105. Detail of аи ‘from central portion 0 
showing finely alain, cell outlines, x 200.—37.S 
x 500. 


reted as 

vules. Note the proa overlapping membranes, the strongly cutinized pointed tips имегр 
ed base ular perforation interpreted as 
. Detail pm eraen end of ovule membrane showi 


the chalazal ends, : же 
; те 
wing sn te es tip and mo 105. 
5703-4 
x30.—35. IU 157034 
mbrane 


6—9 such scars around the receptacle pe ies 
pret them as indicating the former pond 
inner perianth parts. At the base of the ай 
there is an elliptical mark similar to be 
seen at the base of the flower in Figures 15703- 
12. These are particularly distinct in IU ui 
4152 (Fig. 2) and suggest that there was ehe "i 
of three narrowly elliptical scars around 


—X""" c— —— a: 


1984] 


ceptacle base. These scars are similar to that at 
the base of Archaepetala beekeri (Fig. 38). IU 
15703-4152 (Fig. 2) and 2300 (Fig. 4) show a 
distinct ridge on the pedicel 20-25 mm below 
the base of the flower. In both specimens there 
is a suggestion that the ridge bore two scars. By 
analogy with extant Liriodendron tulipifera (Fig. 
63) and Magnolia tripetala (Figs. 61, 66), we 
interpret the ridge as the position of calyptra-like 
bud-scales. Below this ridge, IU 15703-4152 
shows no branching or evidence of other flowers; 
IU 15703-2300 (Fig. 3), however, shows a large 
concave scar which we interpret as a branch point. 
The two specimens of aborted receptacles show 
that the immature carpels were long, narrow, and 
had rounded tips (Figs. 10, 11). As they ripened, 
they increased both in length and width to be- 
come ellipsoidal at maturity. 
Individual follicles are i y found sep- 
arated from the receptacle, and there may have 
been a tendency for them to be shed at maturity. 
They broke away at the very base of each fruit 
stalk (Fig. 20) to leave clear scars on the recep- 
tacle (Fig. 6). A few carpels show one or several 
transverse cracks on their stalk, corresponding 
to the groove reported by Dilcher et al. (1976). 
They are not, however, consistent or significant 
morphological features, and there is no evidence 
for any structures subtending the individual car- 
pels in this region or at the base of the stalk. We 


11 


мн, UI 


The follicles clearly dehisced along an adaxial 
Suture, and the locule of many is filled with sed- 
"ent (Figs. 13-16, 18). There is a prominent 
adaxial ridge on most of the better preserved 
follicles (Figs. 23, 24), and some carpel apices 
Clearly show that this adaxial flange continued 
Over the apex, wrapping around the end and giv- 
'ng a bilobed appearance to the carpel tips (Figs. 
: 7, 19). SEM examinations of sediment with 
Impressions of the flange show that it had a dif- 
ferent texture to the outer follicle wall (Fig. 27). 
Cuticle Preparations show that both flanges were 
furnished with long, simple hairs, perhaps related 
mc stigmatic surface in younger carpels (Fig. 


. We have obtained only a thin cuticle from the 
inner surface of the endocarp (Fig. 30), but there 
T clearly at least two layers in the follicle wall. 

inner layer of transverse fibers is indicated 
by the fine transverse striations seen on the in- 


DILCHER & CRANE—ARCHAEANTHUS 363 


ternal locule casts of some specimens (Fig. 26) 
as well as the transverse cracks (Fig. 21), which 
we interpret as splits between the fibers. The cu- 
ticle of the inner follicle surface shows elongated 
cells with obvious distortions made by resin- 
bodies compressed into it (Fig. 30). Many of the 
resin-bodies are more or less spherical (Figs. 29, 
31); others are elongated and seem themselves 
to have been distorted by the endocarp fibers 
(Figs. 21, 30). Where organic material or impres- 
sions of the outer carpel surface are preserved, 
they show no obvious cellular detail. 

A few specimens of A. linnenbergeri show 10— 
18 more or less oval areas along the length of the 
follicles (Figs. 3, 23). These are always restricted 
to the adaxial two-thirds, or half, of laterally 
compressed follicles and may appear as depres- 
sions or raised areas, depending on how the frac- 
ture plane passed through the compression, and 
the extent to which the locule was filled with 
sediment. We interpret these areas as bulges and 
constrictions in the follicle wall caused by seeds, 
and suggest that about ten to 18 seeds matured 
in each pod. Some ofthe seed outlines are slightly 
pointed toward the adaxial margin, perhaps in- 
dicating attachment. Seed outlines are seen in 


regular, but in others the outlines are more con- 
fused and overlap, perhaps indicating more than 
one row of seeds compressed on top of each oth- 
er. Only two follicles (Figs. 24, 25) show what 
may be seeds in situ, but they add nothing to our 
knowledge of their morphology. We have not 
been able to confidently recognize disp d seeds 
in our collections. 

The membranes that we have isolated from 
the carpels are small (Figs. 32—37), and crowded 
together (Fig. 32). They are variable in size; some 
may correspond to the seed outlines discussed 
above while others may be the remains of abort- 
ed ovules. Each membrane is a single structure 
that we suggest is probably the outer cuticle of 
the nucellus, or possibly the remains of the inner 
integument, which is extremely thin in extant 
Magnolia (Earle, 1938). Macerations of aborted 
ovules from Magnolia tripetala have yielded 
similar internal membranes from around the nu- 
cellus (Fig. 68). There is no megaspore mem- 
brane (Harris, 1954; Hill & Crane, 1982). We 
are not certain whether the ovules were anatro- 
pous or orthotropous. None of our specimens 


364 


show a raphe, but neither do the membranes 
from the anatropous ovules of M. tripetala. As 
far as we can tell, the ovules were oriented with 
the chalazal scar directed away from the suture 
and were therefore probably anatropous. 

he ovules were attached below the base of 
the adaxial flanges and, like the seed outlines, 
are restricted to the upper half of the follicle. The 
ovules were numerous and borne overlapping 
(Fig. 32), presumably on either side of the suture. 
We estimate that each carpel probably contained 
about 100 ovules, but none of the locule casts 
show any indication of placental scars. 


Archaepetala Dilcher & Crane, gen. nov. TYPE: 
Archaepetala beekeri Dilcher & Crane, sp. 
nov. 


DIAGNOSIS: Simple, laminar, entire-margined, 
isolated, fossil petal-like structures 

DERIVATION: From archae —- Greek. meaning 
beginning or first; petalos— Greek, meaning 
broad, flat, outspread. 

DISCUSSION: This genus is established as a broad 
form-genus for accommodating isolated, fossil 
petal-like structures with the above morphology. 


Archaepetala beekeri Dilcher & Crane, sp. nov. 
HOLOTYPE: IU 15703-3179. 


DIAGNOSIS: Lamina elliptical, length-to-width 
ratio approximately 2:1. Base with a prominent 
attachment area, apex rounded. Lamina with a 
broad rib running from the base to the apex. 

OTHER MATERIAL: IU 15703-3882. 

NUMBER OF SPECIMENS EXAMINED: 2. 

FIGURES: 38, 41, 44, 60d. 

DERIVATION: After Mr. Charles Beeker, who 
helped collect much of the material from Lin- 
nenberger Ranch. 

DESCRIPTION: Lamina simple, elliptical, 70-80 
mm long, ca. 40 mm wide (ma aximum); length- 
to-width ratio approximately 2: 1. Margin entire. 
Base with a prominent scar that is rounded above, 


FIGURES 38-46. Ot pa о 


Dilcher & Crane, gen. sp. nov., IU 15703-3179. Showi 
x1.—39. Ka наме walkeri Dilche 
rrow midri — 


703-3822. Poorly prese 
Dilcher & Crane, gen. et sp. nov 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


straight below, and pointed at either end; 14 mm 
wide, 5 mm high. Apex rounded. Lamina with 
a broad midrib of numerous fine striations run- 
ning from the attachment area at the base to the 
apex (further details of venation not seen). Mid- 
rib the same width as the attachment area proxi- 
mally, narrowing distally, 4-6 mm wide in the 
central part of the lamina. Surface of lamina 
wrinkled with fine, irregular areolae ca. 0.3-0.8 
mm diam. and with numerous spherical resin- 
bodies (60—)80-100(-110) um diam. 

DISCUSSION: Archaepetala beekeri is known 
from only two specimens (Figs. 38, 41), but both 
are almost complete. They show evidence of hav- 
ing been at least partially rigid with some three- 
dimensional hie in life. The surface texture 
imparted by wrinkles and irregular small ar- 
eolae is prac е and like that seen in Kalym- 

manthus walkeri, making fragmentary € 
mens difficult to separate. We are uncertain 
to the cause of these areolae, but they could de 
from clusters i harder cells, such as sclerenchy- 
ma, in the lamina. 

The shape ind size of the attachment area on 
A. beekeri is very similar to the three scars that 
occur at the base of the receptacle in Archaean- 
thus linnenbergeri. For this and other reasons 
discussed later (see Reconstruction of the Ar- 
chaeanthus Plant), we suggest that A. beekeri are 
the outer perianth parts of Archaeanthus flowers. 
The irregular wrinkled surface is similar to that 
of certain dried Magnolia perianth parts. 


Archaepetala obscura Dilcher & Crane, 5р. nov. 
HOLOTYPE: IU 15703-2266. 


DIAGNOSIS: Lamina У леву length-to-width 
ratio approximately 1.5: 1; ca. 18 evenly spaced, 
more or less parallel veins уакы slightly from 
the base. 

NUMBER OF SPECIMENS EXAMINED: 1. 

FIGURES: 40, 45, 60c. 

DERIVATION: From obscurus— Latin, meaning 


Dee 


— 


rgans attributed to the Archaeanthus linnenbergeri plant.—38. Archaepetala beekeri 


t the base. 
chment puniat. apes and 


703-2266. Showing poorly 


ám MC int of 
TU 15703-41 15. Showing bilobed apex, broad midrib, and concave S obed 


attachment, x 1.—43. Kalymmanthus walkeri Dilcher & Crane, gen. et sp. nov., IU 15703-4114. Showing 


1984] DILCHER & CRANE—ARCHAEANTHUS 365 


Pex and the split along the line of the midrib, x1.5.—44. ye eger beekeri Dilcher & Crane, gen. et sp. 
703-3179. De vi green obscura Dilcher & Crane, 


(2. nov., IU 15703-2266. Detail showing resin-bodies (arrows), х о. manthus walkeri Dilcher & 
е, ge 


n. et sp. nov., IU 15703-2747. Detail showing resin-bodies (arrows), х 


366 


д Py Pere | 1 асса 


indistinct, 
base of the holotype. 

DESCRIPTION: Lamina simple, obovate, esti- 
mated lamina length 80 mm, ca. 5 
(maximum); Е E ratio approximate- 
ly 1.5:1 gi p 
Lamina with ca. 9 prominent, more or less par- 
allel veins diverging slightly from the base. A 
single, more weakly developed vein present in 
each space between the more prominent veins. 
Prominent veins linked by a reticulum in the 
distal part of the lamina. Texture of lamina 
smooth; the substance of the lamina thin and 
containing numerous spherical resin-bodies, 
(80-)990-100(-130) um diam 

DISCUSSION: Archaepetala obscura is known 
from only a single fragmentary but distinctive 
specimen (Fig. 40), which was folded prior to 
compression. The shape and venation of A. ob- 
scura is very petal-like, but we cannot be certain 
of its botanical nature. However, we suggest that 
it may have formed an inner perianth immedi- 
ately above the tl that, in our view, 
bore the A. beekeri parts. 


unknown) 


Kalymmanthus Dilcher & Crane, gen. nov. TYPE: 
Kalymmanthus walkeri Dilcher & Crane, sp. 


DIAGNOSIS: Lamina broadly elliptical to broad- 
ly ovate, bilobed. Length-to-width ratio approx- 
imately 1.2: 1. Base straight or slightly concave, 
lacking an obvious attachment area. Apices of 
lobes broadly rounded. Lamina with a rib run- 
ning from the base of the sinus. 

DERIVATION: From kalymma- Greek, mean- 
ing a covering or hood; anthos— Greek, meaning 
flower. 

DISCUSSION: This genus is established as a broad 
form-genus for accommodating isolated, fossil 
bud-scale, stipule, or calyptra-like structures. 


Kalymmanthus walkeri Dilcher & Crane, Sp. nov. 

HOLOTYPE: IU 15703-2747. 

DIAGNOSIS: As for the genus. 

OTHER MATERIAL: IU 15703-4114, IU 15703- 
4115 

NUMBER OF SPECIMENS EXAMINED: 3. 

FIGURES: 39, 42, 43, 46, 60e. 

DERIVATION: After Mr. Merle Walker, who aid- 
ed in the discovery of the Linnenberger Ranch 
locality and has given us considerable assistance 
during our collecting in central Kansas. 

DESCRIPTION: Lamina broadly elliptical to 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


ages P ovate, bilobed; 26—65 mm long, 21-50 

ngth-to-width ratio approximately 
IZ L ы entire with a prominent lip 0.5 
mm wide. Base straight or slightly concave 6-15 
mm wide, lacking an obvious attachment scar. 
Apices of lobes broadly rounded; lobes typically 
0.3-0.2 of the lamina length, but sometimes 
splitting beyond the original sinus to the base of 
the lamina. Lamina with a midrib running from 
the base to the sinus, midrib either narrow, ca. 
1 mm wide, or slightly broader and tapering dis- 
tally. Surface of lamina wrinkled with fine, ir- 
regular areolae ca. 0.3-0.8 mm diam., and with 
numerous resin-bodies typically (60—)80-100 
(110) um diam. 

DISCUSSION: Kalymmanthus walkeri is known 
from three specimens (Figs. 39, 42, 43). Other 
specimens with the distinctive areolate surface 
texture do occur at the Linnenberger locality, and 
although they cannot be confidently distin- 
guished from fragments of A. beekeri, some do 
show a marginal lip, like that in K. walkeri. In 
IU 15703-4115 (Fig. 42), however, this m 
lip is not clearly visible, and the same specimen 
has a broad rib running from the base to the sinus 
somewhat similar to that in A. beekeri. We in- 
terpret K. walkeri as bud-scales, probably of both 

At maturity, the 
extent of the split along ; the line of the sinus was 
probably variable. By analogy with living Mag- 
nolia, the bud-scales may be of stipular origin, 
although none of our specimens show any Sign 
of a leaf lamina attached to an extended midrib. 
Our specimens are unlike the putative bud-scale 
described and figured by MacNeal (1958) from 
the Cenomanian Woodbine Sand flora of Denton 
County, Texas. 


oatati 


> 


Liriophyllum Геза. (1878) emend. DEM E 
Crane. ТУРЕ: Liriophyllum populoides 
(designated by Berry, 1902a: 55). 


MENDED GENERIC DIAGNOSIS: Leaf patioan 
EE deeply divided for at least half its d 
Venation pinnate. Midrib stout extending to > 
base of the sinus and forking into two pon 
veins, distinct from the secondary veins س‎ 
which form the leaf margin typically for abo 
0.3-0.16 of the lobe length. Above this point thé а 
lamina arches away from the vein into the sin 
and broadens Ямар» to form each lobe. “ 

SPECIES EXCLU FROM THE а Liri 
T 
phim obcordatum Геза. и d зей 


1iXxinnhvelhim 


1984] 


Liriophyllum sachalinense Krysht. (1937: 85, 
pl. 12, figs. 4—6). 
Liriophyllum populoides Геза. emend. Dilcher 
Crane. HOLOTYPE: USNM 2079. 


EMENDED DIAGNOSIS: Petiole with a proximal, 
laminar, alate appendage in its lower part. Ap- 
> | وو‎ 1 4 1 


I g g its full length, entire mar- 
gined, rounded and tapering above. 

SYNONYM: Liriophyllum beckwithii Lesq. 

REFERENCES: Liriophyllum  beckwithii Lesq. 
(1878: 482—483, brief description). 

Liriophyllum populoides Lesq. (1878: 482—483, 
brief description). 

Liriophyllum beckwithii Lesq. (1883: 75, pl. 
10, fig. 1, generic diagnosis, specific diagnosis, 
discussion, and line drawing). 

Liriophyllum populoides Lesq. (1883: 76, pl. 
11, figs. 1-2, specific diagnosis, description, and 
line drawings). 

Liriophyllum beckwithii Lesq. (1892: 210, 
mention only). 

Liriophyllum populoides Lesq. (1892: 211, 
mention only). 

Liriophyllum populoides Lesq. (Hollick, 1894: 
470-471, pl. 221, brief description, discussion, 
and line drawing). 

Liriophyllum populoides Lesq. (Holm, 1895: 
316, brief discussion of affinities). 

Liriophyllum populoides Lesq. (Hollick, 1896: 
= Pl. 269, fig. 2, brief discussion and line draw- 


Liriophyllum Lesq. (Berry, 1902a: 47-56, brief 
discussion and comparison with putative fossil 
Liri odendron, p. 55, takes Liriophyllum popu- 
loides as the type species of the genus). 

OTHER MATERIAL: Morrison, Colorado, USNM 
i 2078 (two leaves), 2080, 2135, 2142; HU 

81, 2882, 2883, 2884, 2885, 2888, 2892, 2897. 
NUMBER OF SPECIMENS EXAMINED: 15. 
FIGURES: 47—50. 
он: Leaves petiolate. Outline of lam- 
8 БОО to broadly ovate, 90-185 mm long, 
of the | mm wide, broadest in the lower quarter 
“а апипа. Lamina bilobed, deeply divided 

‚ 4t least half its length. Midrib stout 1-2 mm 
bins ©, 23-36 mm long, extending to the base of 
"oct and forking at an angle of 45-70? into 
м ы veins that form the leaf margin 
жь NT part of the sinus. Veins contiguous 
Ped "i Sinus margin for 8-25 mm, typically 
the le -25-0.16 of the lobe length. Above this 
к mina arches away from the veins into the 
a and broadens distally to form each lobe. 

h fork of the midrib enters the distal part of 


DILCHER & CRANE—ARCHAEANTHUS 


367 


the lobe, branching several times, and gradually 
becoming finer. Apex of each lobe rounded, lat- 
eral margins more or less straight, slightly convex 
or prominently concave, and forming two dis- 
tinct lobes on either side of the midrib. Leaf base 
obtuse or acute, straight or decurrent where it 
joins the petiole. 

Secondary venation pinnate, camptodromous; 
2-3 secondary veins on either side of the midrib, 
alternately arranged, more or less decurrent. An- 
gle of divergence of secondary veins 40—50°. Sec- 
ondary veins branching well within the margin. 
(Details of finer venation not preserved.) Ex- 
treme base of lamina with two basal veins of 
secondary or int iat d 
der. Petiole to 27 mm long (longest specimen 
incomplete) with a proximal, laminar, alate ap- 
pendage in its lower part. Appendage 13 mm 
wide, including the petiole, attached along its 
entire length; entire margined, rounded and ta- 
pering above. 


ferfiarv or. 
у-єегиагу OF 


Liriophyllum kansense Dilcher & Crane, sp. nov. 
HOLOTYPE: IU 15703-2272. 


SPECIFIC DIAGNOSIS: Petiole simple, lacking a 
proximal, laminar, alate appendage. 

REFERENCES: Liriophyllum beckwithii Теза. 
Dilcher et al. (1976: 854—856, fig. le, f, descrip- 
tion, discussion, and photograph). 

Liriophyllum Lesq. Dilcher et al. (1978: 11, 
brief mention and line drawing). 

Liriophyllum sp. Retallack and Dilcher (1981c: 
39, figs. 2-14, brief mention and photograph). 

OTHER MATERIAL: Linnenberger’s Ranch IU 
15703; 2267, 2271-2277, 2309, 2456, 2463- 
2466, 2469-2471, 2473, 2475-2477, 2479, 2480, 
2482, 2484, 2485, 2487, 2488, 2492, 2493, 2679, 
2948, 3443, 3813, 3816—3818, 3823, 3826, 3827, 
3836, 3839, 3859, 3885, 3886, 3890, 3894, 3895, 
3992, 4028, 4029, 4051, 4120. 

NUMBER OF SPECIMENS EXAMINED: Fort Harker, 
Kansas, USNM 2718. Fifty-four and numerous 
other fragments. 

FIGURES: 51-59, 60b. 

DESCRIPTION: Leaves petiolate. Outline of lam- 
ina square to very broadly ovate, (60—)100(-140) 
mm long, (64-)120(-186) mm wide, typically 
broadest in the lower quarter of the lamina. Lam- 
ina bilobed, deeply divided for at least half its 
length. Midrib stout 1-3 mm wide (10-)20-30 
(-44) mm long extending to the base of the sinus 
and forking at an angle of (40—)60—70(—80)° into 
two prominent veins that form the leaf margin 
in the lower part of the sinus. Veins forming the 
sinus margin for (15-)25(-48) mm, typically 


368 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


FIGURES 47-53. 47. ae populoides Lesq., USNM 2080. Тш by Lesquereux (1883, pl. 11, за 
2). Note also the structure at the P Carpites heic Мело Moo pl. 11, a 5), which та 
be an isolated Archaeanthus follicle, 907 —48. L. populoides Lesq., USNM 2078. Fig Гене 


peri, pl. 10, fig. 1). Note the two lobes in asa right "fas of the lamina, x0.3. 249. L. populoides 


stake USN 
078. Specimen on the reverse of block in Figure 48, not figured by Lesquereux. Note the long petiole, x0.5.— 


| 
| 


Брза И Ре чаас d) ortae جد تت ر‎ А ت وسن ہت‎ DM 


1984] 


about 0.3–0.25 of the lobe length. Above this the 
lamina arches away from the veins into the sinus 
and broadens distally to form each lobe. Each 
fork of the midrib enters the distal part of the 
lobe, branching 4 or 5 times and gradually be- 
coming finer. Apex of each lobe broadly rounded, 
lateral margins more or less straight, occasionally 
concave or slightly convex. Leaf base shallowly 
cordate, acute or obtuse, straight, or more typi- 
cally decurrent, where it joins the petiole. 
econdary venation pinnate, camptodromous; 
(2-)4(-5) secondary veins on either side of the 
midrib, alternately arranged, frequently more or 
less decurrent. Angle of divergence of secondary 
veins gradually decreasing apically, up to 90? at 
the base, ca. 30° distally. Secondary veins 
branching and becoming finer well within the 
margin to form weak, camptodromous loops, 


gence of tertiary venation variable, but tertiary 
veins frequently more or less decurrent where 
they join th dari i the midrib. Toward 
the Margin, tertiary, quaternary, and quinternary 
veins forming polygonal areolae, frequently more 
or less elongated toward the center of the leaf: 
areolae often more regular, pentagonal and or- 
thogonal toward the margin. Areolae open; vein 
endings simple and compound. Pattern of ve- 
nation equivalent to leaf rank 2 or 3 (Hickey, 
1977). Petiole to 100 mm long, 2-4 mm wide, 
simple, with no alate appendage, swollen to 6 
mm at the base with a terminal crescentic abscis- 
sion Scar. Leaf mesophyll containing spherical, 
yellow-brown resin-bodies (50-)80-100(-110) 
um diam 


DISCUSSION: All of the specimens of Lirio- 
Phyllum Populoides are from the Kassler Sand- 
stone of the South Platte Formation near Mor- 
" | Colorado. Lesquereux (1878, 1883) 
oh three species in the Kassler Sandstone 

cton. Liriophyllum beckwithii and L. po- 
Puloides have a very distinctive morphology and 
venation and are synonymized as variants of one 
Species, 7 iriophyll 3: qu А PEORES 


DILCHER & CRANE—ARCHAEANTHUS 


369 


these diagnostic features, particularly the bifur- 
cation of the midrib, and we have excluded it 
from the genus (Berry, 1902a). We also exclude 
Liriophyllum sachalinense Kryshtofovich (1937), 
which subsequently has been referred to Bau- 
hinia by Vakhrameev (1966), Takhtajan (1974), 
and Tanai (1979). Lesquereux did not designate 
a type species for Liriophyllum, and although 
Andrews (1966) cites the first named species L. 
beckwithii, we follow Berry (1902a) in taking L. 
populoides as the type. The specimens of L. po- 
puloides from the Kassler Sandstone (Figs. 47- 
50) are poorly preserved but are clearly very sim- 
ilar to the Liriophyllum leaves from Kansas. The 
only significant feature in which they differ is the 
presence of an alate appendage attached to the 
proximal part of the petiole in L. populoides. 
Hollick (1894, 1896) was the first to call attention 
to this feature, but it is also shown by a Lirio- 
phyllum populoides leaf (Figs. 49, 50) on the same 
block as one of the specimens figured by Les- 
quereux (1883). The other specimens in Les- 
quereux's original collection have too little of the 
petiole preserved to show whether the appendage 
was present. None of the Liriophyllum kansense 
specimens, some of which have the complete pet- 
iole preserved (Fig. 51), shows any sign of an 
alate petiolar appendage. Although the two 
species do show a suggestion of other subtle dif- 
ferences, for example, the pronounced lateral 
lobes of USNM 2078 (Fig. 48) and variations in 
the prominence of the forks of the midrib, we 
have too little L. populoides material from Col- 
orado to evaluate the patterns of variation in 
these characters more carefully. The difference 
in petiole is our primary reason for formally rec- 
ognizing two distinct species. The alate petiolar 
appendage of L. populoides has been interpreted 
by Hollick (1894, 1896) as an early stage in the 
formation of the prominent stipules of Lirioden- 
dron. In view of the features of the Archaeanthus 
with which these leaves are now known to be 
associated (see Reconstruction of the Archaean- 
thus Plant), such a hypothesis seems more plau- 
sible. We do not pursue this point further here 
but merely point out that we have no good evi- 


CR. o op Lia LLL И 


~ 


e L. populoides Lesq. Same specimen as Figure 49 sh 
— 51. L. ka i Crane, sp. nov., IU 157 
kansense Dilcher & 
It tomy of midrib and the veins forming the sinus margins, х 1.—33. 
15703-2317. Detail of leaf fragment from the same block as Figures 


absence of alate appendage, x0.5.—52. L. 


‘spherical depressions caused by resin-bodies, * 


owing alate appendage attached to petiole — 
a 


03-4029. Complete petiole rr. expan 


370 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


FIGURES 54-59. Liriophyllum kansense Dilcher & Crane, sp. nov.—54. IU 15703-2272. Large leaf showing 


characteristic venation, x 0.5.— 55. IU 157 


703-2463. Leaf fragment showing major venation, х1.—56. 10 1 


5.7 
2477. Fragment of gres leaf base. Note the cordate leaf] the petiole, * 0. 


57. IU 15703-2469. Leaf lobe with well- 
15703-2472. Detail of midrib and fine ve 


99. 
preserved venation, x 1.— 58. IU 15703-2479. Leaf lobe, х1.—5 
nation, x 4.5. 


ens 


IU 


1984] DILCHER & CRANE—ARCHAEANTHUS 371 


FIGURE 60. В li bergeri plant.—a. Archaeanthus stessi i 

lagram showing the tifollicle.—b. L enation.— 
— chaepetala ес is ^ —d. узори ! beekeri, outer perianth part.— e. Kalymmanthus 
walkeri, v! REPO NES discere of the base of the multifollicle. Archaeanthus 
linnenberge. onstruction of a si ingle follicle. ok Archacanths linnenbergeri, section through a follicle. sf, 
Stalked follicies: ss, stamin rs; ip, inner perianth scars; op, outer perianth scars; pe, pedicel; bs, bud-scale 

Scars; ar, adaxial eas ex, exocarp containing resin- -bodies; en, төр of transverse fibers; se, anatropous 
seed borne adaxially 


372 


dence on the vegetative axis of A. linnenbergeri 
r ring-li i h as occur in Recent 


Lesquereux’s Liriophyllum populoides mate- 
rial consists only of poor impressions in a gray 
sandstone and exhibits none of the fine details, 
including the resin-bodies, seen in L. kansense. 
Only the specimens from Linnenberger’s Ranch 
have appreciable organic material preserved with 
the resin-bodies in situ. Resin-bodies have been 
seen in over 40 of the 52 specimens of this species. 
Several other leaf types from the Linnenberger 
locality have yielded well-preserved cuticles, but 
we have not been able to obtain these details 
from Liriophyllum. We suggest that the cuticle 
was probably rather thin in life. 

Prominently bilobed leaves are not common 
in angiosperms but do occur in several genera; 
for example, Bauhinia (Leguminosae) and Lir- 
iodendron (Magnoliaceae). However, the Lirio- 
phyllum 1еаї has a distinctive morphology and 
none of the living plants known to us are closely 
similar. We have considered the possibility of a 
relationship to Liriodendron particularly care- 
fully. The morphological variability in the leaves 
of this genus has been examined in detail by 
Berry (1901, 1902a, 1902b), Holm (1895), and 
ourselves, but despite extensive searches includ- 
ing seedling, sucker-shoot, and abnormally de- 
veloped leaves, we have seen no modern leaf 
with a strong midrib running to the apex and 
dividing into a pair of prominent veins contig- 
uous with the margin. The same feature also sep- 
arates Liriophyllum from fossil species assigned 
to Liriodendron or Liriodendropsis Newb. These 
species were reviewed by Berry (1902a). We have 
collected more typical Liriodendron-like leaves 
from the Saline River locality in Russell County, 
Kansas (IU 15702; see Retallack & Dilcher, 
1981b, 1981c, for locality details), and similar 
specimens are known in the *Dakota Sandstone 
Flora' (Lesquereux, 1883, 1892). Such leaves 
range up into the early Paleogene, where they 
seem to be replaced by other leaf species even 
more similar to extant Liriodendron. Curiously, 
only one Liriophyllum leaf is known from the 
"Dakota Sandstone Flora’ of Kansas and Ne- 
braska. 

The distinct inequilateral development of the 
lamina exhibited by Liriophyllum also occurs in 
several other mid-Cretaceous leaves such as 
Fontainea grandiflora (Newberry, 1895: 96, pl. 
45), Halyserites reichii Sternb., Halyserites ele- 
gans (Vel.) Knobloch, and Diplophyllum creta- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


ceum Vel. & Vin. (Knobloch, 1978). As noted 
by Rüffle (1970), the same feature is shown by 
leaves ofextant Helleb foetidus; it also occurs 
in the enigmatic Scoresbya (Harris, 1932; Krau- 
sel & Schaarschmidt, 1968). None of these leaves, 
however, are similar in other respects to Lirio- 
phyllum 


RECONSTRUCTION OF ARCHAEANTHUS PLANT 


There is evidence that Archaeanthus linnen- 
bergeri, Kalymmanthus walkeri, Archaepetala 
beekeri, Archaepetala obscura, and Liriophyllum 
kansense are different parts of the same fossil 
plant. In addition to their association in a narrow 
horizon of the fossil-bearing sediments at the 
Linnenberger Ranch, K. walkeri and L. kansense 
also occur with an axis and fruiting receptacle 
similar to Archaeanthus linnenbergeri at another 
central Kansas locality near Hoisington, Barton 
County (IU 15706; Crane & Dilcher, 1984; ae 
Retallack & Dilcher, 1981b, 1981c, for locality 
details). One specimen of L. kansense is known 
from the Dakota Sandstone Flora of central Kan- 
sas (USNM 2718). The only other known locality 
for Liriophyllum leaves (L. populoides) is the 
Kassler Sandstone at Morrison, Colorado, and 
it, too, has yielded a probable specimen of 4. 
linnenbergeri. One of the blocks figured by Les 
quereux (1883, pl. 11, fig. 5) also shows an elon- 
gated structure named Carpites liriophylli Геза. 
(Fig. 47). Lesquereux suggested that this 1s а fruit 
of Liriophyllum, although he cites no үа 
other than their association on the same piece 0 


licle. The paucity and preservation of the a 
terial, however, precludes establishing the lin 
more securely. The Magnolia receptacle, h É 
ever, figured by Lesquereux (1883) from Mo 
rison is very like the immature specimens + 
10) from Linnenberger's Ranch, and we syno 
ymize it with Archaeanthus linnenbergert. 5 
At Linnenberger's Ranch, 1. kansense leav 
and 4. linnenbergeri are particularly Я 
in a silty, gray clay, with occasional san pare 
ers, that 15 ca. 30 cm thick and occurs 3 m бе п 
the base of the sandstones which cap the meee 
In this distinct horizon immediately below x 
major plant bearing clays, these two рет. ed 
the commonest plant fossils and occur та ing 
together on the same bedding plane. Connie 
the Linnenberger flora as a whole, the pup 
diversity of the plant assemblage is low, an 


И. А... ааа а... л... аан]. mt X 


1984] 


linnenbergeri and L. kansense are two of the 
commoner elements in the flora. To judge from 
the size range of the plant fragments present, the 
Linnenberger assemblage is mixed and scarcely 
sorted; Retallack and Dilcher (19815, 198 1c) in- 
terpreted the plants as having been deposited 
close to where they grew. 

In addition to evidence of association, Ar- 
chaeanthus linnenbergeri, Kalymmanthus walk- 
eri, Archaepetala beekeri, Archaepetala obscura, 
and Liriophyllum kansense are also linked by the 
numerous amber-colored resin-bodies that they 
contain (Figs. 21, 29-31, 44—46, 53). Frequently 
these protrude from within broken organic frag- 
ments of the various organs and can be picked 
from the surface (Dilcher et al., 1976) or isolated 
by maceration. Even where other organic ma- 
terial has been lost by oxidation, the resin-bod- 
ies, or the small hemispherical depressions that 
they leave in the matrix, can usually 
Very few other types of leaves from the Linnen- 
berger locality contain resin-bodies, but when 
found they are quite different, being much more 
compressed, smaller, and lacking the resinous 
luster. On the basis of association evidence and 
this structural agreement, we suggest that A. lin- 
nenbergeri, K. walkeri, A. beekeri, A. obscura, 
and L. kansense were all parts of the same fossil 
plant species. From their morphology and the 
Scars that they display, we can make some sug- 
gestions as to how these various 

n attached. 

The helically arranged scars on the vegetative 
axis of IU 15703-4152 are clearly leaf scars and 
are of similar size to the petiole bases of L. kan- 
sense. The base of the К. walkeri bud-scales cor- 
responds in size and shape to the scar on the 
pedicel several millimeters below the base of the 
flower (Fig. 60a, f). By analogy with extant Mag- 
nolia tripetala (Figs. 61, 66) and Liriodendron, 
We suggest that the bud-scales were attached there 
and formed a calyptra-like covering over the 
young developing flower. The attachment area 
at the base of А. heekeri (Fig. 38) corresponds in 
Sze and shape to one of the three large scars that 
delimit the base of the flower (Figs. 2, 4, 12). We 
Suggest that 4. beekeri was attached in this po- 
== and formed an outer perianth of three го- 
a. narrowly elliptical sepals. We interpret А. 

cura to have been less robust than A. beekeri 
and to have been attached to the more or less 
circular scars immediately above the three large 
br flower scars. The inner perianth probably 

nsisted of relatively few, either six or nine, 


h 


DILCHER & CRANE—ARCHAEANTHUS 


373 


petals. The male parts of the Archaeanthus plant 
have not been recognized yet, but we envisage 
that they were borne on the small elliptical scars 
immediately below the gynoecial zone, and above 
the scars of the perianth whorl. In Figures 69 and 
70 we give our suggestions as to what the Ar- 
chaeanthus flower may have looked like; more 
detailed reconstructions of the individual parts 
are given in Figure 60. 


BIOLOGY AND ECOLOGY OF THE 
ARCHAEANTHUS PLANT 


The reconstruction of the Archaeanthus lin- 
nenbergeri plant combined with sedimentologi- 
cal data p it lusi the biology 
and ecology of this mid-Cretaceous angiosperm. 
During the mid-Cretaceous, a major epiconti- 
nental sea extended northward from the Gulf of 
Mexico into the western interior of North Amer- 
ica where, at various times, it linked with a 
southward extension of the Arctic Sea. Evidence 
from stratigraphy and sedimentology indicates 
that the Kansas plant beds were deposited in a 
range of coastal plain environments adjacent to 
this seaway and under variable amounts of ma- 
rine influence. Both the Morrison, Colorado, and 
Linnenberger ial dates app i ly from 
the Albian-Cenomanian boundary: a time of 
lowered sea-level, bracketed above and below by 
widespread marine, eustatic transgressive epi- 
sodes. During this period, both areas were situ- 
ated at an approximate pal titude of 36-37°N 
(Smith & Briden, 1977) and were experiencing 
warm-temperate or sub-tropical climates (Kauff- 
man, 1977). 

Retallack and Dilcher (1981b, 1981c) inter- 
preted the plant bearing sediments at Linnen- 
berger’s Ranch as shales associated with levee 
deposits in inter-distributary depressions vege- 
tated by swamp woodland. To judge from the 
almost exclusive angiosperm macrofossil flora, 
the local vegetation was dominated by flowering 
plants; although in the palynoflora, angiosperm 
pollen comprises less than 25% of the total paly- 
nomorph assemblage (Dilcher & Zavada, un- 
publ. data). 

Despite the large collections available and the 
geological proximity of shale and sand facies in 
the Dakota Formation, only one Liriophyllum 
kansense leaf is known from the classic Dakota 
Sandstone Flora, which represents a number of 
localities in and around Ellsworth County, Kan- 
sas. Equally many of the characteristic plants of 


374 


that flora (for example, Betulites and the Plata- 
nus-Sassafras complex) either do not occur or 
are not common at Linnenberger’s Ranch or 
Hoisington. They are found, however, at other 
shale localities. Although the fossils known from 
any locality are an incomplete representation of 
the living vegetation, where local differences ex- 
ist (such as those in the Dakota Formation), they 
may reflect specific associations of plant species 
in particular environments. 

The pollination and dispersal biology of the 
Archaeanthus plant was probably relatively un- 
specialized. The size of the floral and vegetative 
organs and the dimensions of the axes that sup- 
ported them suggests that the plant was woody 
in life. From the size and features of the leaves, 
and from the petiole bases, we conclude it was 
probably a deciduous tree or shrub. The appar- 
ently bisexual flowers, and hence the fruits, were 

rne terminally on leafy, woody axes, probably 
prominently, beyond or near the margin of the 

eafy crown. Such a position combined with the 

large perianth parts indicated by the basal floral 
scars, and the size of Archaepetala beekeri and 
A. obscura, suggests that the flower was probably 
visually conspicuous and insect-pollinated. Co- 
leoptera, Thysanoptera, and incurvariid Lepi- 
doptera have been recorded as pollinators that 
feed on pollen in recent ‘primitive’ angiosperms 
(Thien, 1974, 1980), and all have a fossil record 
extending back into the Cretaceous (Thien, 1974, 
1980; Whalley, 1978). Following pollination, we 
suggest that the stamens and perianth parts were 
shed and that the receptacle elongated as the fol- 
licles and seeds matured. Dispersal was probably 
unspecialized, involving both shedding of the 
numerous small seeds through the open adaxial 
suture, and occasional shedding of the complete 
follicles in a manner analogous to extant Lirio- 
dendron. 


COMPARISON WITH RECENT PLANTS 


Vegetative morphology. Similarity in leaf ar- 
chitecture between Liriophyllum and certain ex- 
tant angiosperms has been mentioned already, 
but we know of no closely comparable Recent 
leaf. Asarum (Aristolochiaceae) shows a similar 
pattern of venation in which the major veins 
form the margin of the leaf for some distance 
before entering the lamina; but in Asarum it is 
the base rather than the apex of the leaf that is 
involved. Judging from the one axis of Archaean- 
thus in which leaf scars are preserved, the phyl- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


lotaxy was helical; a widespread condition gen- 
erally regarded as primitive in flowering plants. 

We interpret the resin-bodies preserved 
throughout the A. /innenbergeri plant as the di- 
agenetically altered contents of oil cells. Ethereal 
oil cells are particularly common in Recent Mag- 
noliidae, especially Magnoliales, Laurales, Pi- 
perales, Aristolochiaceae, and Illiciales (Cron- 
quist, 1981), and are frequently preserved in 
younger fossil material confidently referable to 
these groups; for example, Tertiary lauraceous 
eaves. 


We assume that the vegetative axes of Ar- 
chaeanthus were woody, but we regrettably have 
no knowledge of the secondary xylem, which 
would be of considerable interest. | 

Floral organization. The basic organization 
of the Arch hus 8 consists of numerous, 
helically arranged, separate carpels borne on а 
stout, elongated receptacle probably with nu- 
merous helically arranged stamens below; these 


anth parts arranged in apparent whorls. This 
combination of features occurs most commonly 
in the Magnoliidae, but also occurs in a few fam- 
ilies of the Ranunculidae and Dilleniidae, such 
as the Ranunculaceae, Paeoniaceae, and the Di 
leniaceae, which are often regarded as primitive. 

In most magnoliid families the floral recep- 
tacle is rather short, but in the Magnoliaceae and 
some Аппопасеае it is frequently elongated, and 
elongates further during the maturation of the 


fruits, as we suggest for A. linnenbergeri (Figs: 
tamens 


very common in the Magnoliidae. The lack of 
more detailed understanding of the stamina 
parts of Archaeanthus is currently the most con 
spicuous gap in our knowledge of the plant. Tm 
merous perianth parts are widespread (for ir 
ample, in the monocotyledons, Burger, de 
but they also occur in the Magnoliidae. In 
Lactoridaceae (Magnoliales) there are only ! Т 
tepals, and in Degeneria, three sepals. АЕ 
the Annonaceae and Magnoliaceae, а trimer? 
arrangement of perianth parts is common. m 
A calyptra similar to that envisaged for А.й 


* ri- 
nenbergeri occurs in many Magnoliidae. In D 


connate into a deciduous calyptra. In Lir 
dron and Magnolia the large, frequently ~ 
bud-scales enclosing the developing 10 gy 


interpreted as stipular in origin (How: 


1984] DILCHER & CRANE—ARCHAEANTHUS 375 


PEF IE E E PRN 


eu ES 61—68. Extant Magnoliaceae.—61. Magnolia tripetala L. Fruiti 

D y spaced сае  dehiscing abaxially, x0.5.—62. Michellia champac a L. Luzon, Phillipines, collected by 
rece ll, Missouri Bot. Gard. 865046, нды receptacle (multifollicle). Note spacing of follicles along the 
начало р х 0.5. —63. Liriodendron tulipifera L. 
to reveal ridged receptacle. Note ا‎ and perianth scars; the bud-scale scars are just below the 
of the flower, x 7 04. M Magnolia i sorta L. Cleared petal showing details of venation. Compare with 
ы Magnolia grandiflora L es for eee, with Figures 39, 42, and 43. Note the 
the splitting, x lia tripetala L. Base 
ais E the b es pli м = рута “66. Magno 2 s (b) rs of inner (c) and outer perianth (d) parts, 
pin tl п of the bud-scales (e), x 4. —67. Magnolia nadie L. Stipular bud-scale. Note the attachment 
sola ef E at leaf lamina (arrow), х 0.5.—68. Magnolia tripetala L. Nucellar or inner membrane 

Tom an aborted ovule in an immature multifollicle. Compare Figures 32 and 34, x 30. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


FIGURE 69. Archaeanthus linnenbergeri. Reconstruction of leafy twig bearing a multifollicular axis. 


Both Magnolia tripetala (Figs. 61, 66) and Lir- 
iodendron tulipifera (Fig. 63) show calyptra scars 
low the of the flower. 
Follicles and seeds. The follicles of Ar- 
chaeanthus are assumed to have developed from 
conduplicate carpels with two stigmatic crests 


along the adaxial surface. Although this kim 45 
carpel is basic in the Magnoliidae, adaxial es 
hiscence is much less common. In most "t 
noliaceae, dehiscence is abaxial but 1n K 

the £l 1:. 4 “211 pically. as it does 
in A. linnenbergeri. Adaxial dehiscence also of 


б. 


— 


1984] 


DILCHER & CRANE—ARCHAEANTHUS 


FIGURE 70. Archaeanthus linnenbergeri. Reconstruction of leafy twig and flower. 


Curs in Iilicium, as en as in a few Ranunculidae 
and Hamameli 
Prominently к follicles like those іп Ar- 
“haeanthus occur in 0 wany Annonaceae such as 
кр ахавогеа, Guatteria, Unonopsis, Xylopia 
1 Ties, 1930, 193]. 1934, 1937, 1939), as well as 
мир obaileya, Dum буне and De- 


A enale 


generia. In the } 
erally tightly fused t to the receptacle (Fig. 6 1) z and 
often more or less concrescent. Several of the 
annonaceous genera cited above have follicles 
that break away from the receptacle at the base 
of the stalk at maturity, but the closest analogy 
to the dispersed fruits observed in Archaeanthus 


378 


is in Liriodendron, in which the two-seeded, in- 
dehiscent follicle acts as the unit of dispersal and 
separates from the receptacle leaving narrow dia- 
mond-shaped scars (Fig. 63). Both the shape of 


а S 
tO ШОЗС 


in A. linnenbergeri. 

The number of seeds borne in the A. /innen- 
bergeri follicles is higher than in most Recent 
Magnoliaceae. Multi-seeded follicles do, how- 
ever, occur in Degeneria, some Annonaceae, and 
a few other groups of Magnoliidae. 

Conclusions. Archaeanthus is clearly most 
similar to extant Magnoliidae and shares some 
features with supposedly primitive members of 
the Hamamelidae and Dilleniidae. A summary 
ofthe similarities with a range of families is given 
in Table 1. All of the characters of the fossil with 
the possible exception of the unusual form and 
venation of Liriophyllum occur in the Magno- 
liidae, but no living species comes close to the 


quist (1981), viz. Annonaceae, Austrobaileya- 
ceae, Canellaceae, Degeneriaceae, Eupoma- 
tiaceae, Himantandraceae, Lactoridaceae, 
Magnoliaceae, Myristicaceae, and Winteraceae. 
However, we do not believe that Archaeanthus 
usefully can be assigned to any extant family; 
Archaeanthus is a unique and extinct genus of 
fossil angiosperms. 


EVOLUTIONARY SIGNIFICANCE 


The occurrence of Archaeanthus and the floral 
structure it exhibits, as early in flowering plant 
evolution as the mid-Cretaceous, is of consid- 
erable relevance to concepts of flowering plant 
evolution. The late Albian to mid-Cenomanian 
age established for Archaeanthus places it ap- 
proximately 10 to 15 Ma after the first generally 
accepted angiosperm fossils appear in the fossil 
record (Hughes et al., 1979). Archaeanthus is one 
of the most completely known of all early angio- 
sperms, and in the characters that it exhibits it 
comes close to the hypothetical angiosperm ar- 
chetype developed by adherents of classical mag- 
noliid floral theory over the last 80 years. This 
archetype, although admittedly hypothetical, has 
been most explicitly elaborated by Takhtajan 
(1969) and is summarized in Table 2. The rea- 
soning behind the magnoliid theory is largely 
based upon neontological data, and a range of 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


approaches have been utilized in formulating the 
concepts of primitive and advanced characters 
(Sporne, 1956). In view of this historical decou- 
pling of paleontological and neontological data, 
the correspondence that exists between the hy- 
pothetical archetype and Archaeanthus is signif- 
icant. The details of this similarity are summa- 
rized in Table 2, from which it is clear that 


regarded as ‘primitive’ or generalized among Re- 
cent plants. There are, however, differences: for 
example, Archaeanthus was probably deciduous 
rather than evergreen, had small rather than large 
seeds, and had a lobed rather than a simple leaf, 
but probably Archaeanthus combines more 
‘primitive’ features than any living plant. In terms 
of magnoliid theory it demonstrates that many 
of these generalized characters are also ancient. 
It would be easy to interpret Archaeanthus as an 
ancestor to a range of extant plant groups, but 
we can see little value in such a naive pede 


that the basic magnoliid flower was one of the 
earliest kinds of floral organization to be devel- 
oped during the mid-Cretaceous radiation of 
flowering plants. 

Taken in the broader context of mid-Creta- 
ceous fossil flowers, Archaeanthus fits well into 
a pattern that is rapidly becoming established. 
Other magnoliid flowers similar to Archaeanthus 
occur in the Dakota Sandstone Flora the Janssen 
Clay of Hoisington, Kansas (Crane & Dilcher, 
1984), the Amboy Clays of New Jersey, and the 
Crowsnest Formation of southern Alberta (Crane 
& Dilcher, 1984). None of this material occur 
earlier than sub-zone IIC or possibly sub-z00€ 
IIB of the palynological zonation established for 
the mid-Cretaceous of the Atlantic coastal plain 
(Brenner, 1963; Doyle, 1969; Doyle & Robbins 
1977). However, there is evidence of similar flo- 
ral morphology as early as zone I. The floral pc 
figured by Fontaine (1889, pl. 137, fig. 4) a 
Dilcher (1979, fig. 28) is a cluster of follic 
borne on the swollen apex of a simple ахі. ~, m 
than the swelling at the apex and faint indicato 
of a few scars, no differentiation into recep ie 
and pedicel is clear. The specimen does, ho 
ever, show that clusters of follicles are amon’ о 
earliest of all angiosperm fossil fruit types. ee 
ly later, Vakhrameev and Krassilov (1979) i 
scribed Caspiocarpus paniculiger from the же" 
dle Albian of Kazakhstan, which is thought 
be equivalent to zone IIB in the Atlantic c05 


че a am 3—————— 


~ 


—————— -—— — — — —— — — 


— 


— 


— ~ 


ABLE 1. Comparison of the Archaeanthus linnenbergeri plant with selected Recent families of Magnoliidae, Ranunculidae, and Hamamelidae. Data for 
extant families from D. A. Young (1981). + indicates that at least some members of the extant family display the character indicated. 


Ranuncu- 
Magnoliidae lidae Hamamelidae Dilleniidae 
© 9 g Ф 
5 © 5 © 9 о = 5 5 
B 3 8 S % ES 5 E Кое B DER Е 
E E E S 8 © 2 402 Е S 
бз ne 25s See СИВЕР ЕЩЕ: К Д 
Characters of Fossil Plant 
1 Flowers Bisexual + x + + Т + 0 > + 0 + 0 + "s 0 + + 
2 Receptacle Flat or Convex + + + + + + + + + 0 0 + + 0 + + + + 
3 Perianth Parts Spirally Arranged 0 + + 0 0 0 0 0 Е 0 + + 0 0 0 + + 
4 Perianth Well-Differentiated 
into Sepals and Petals 0 0 0 + F + + + + 0 0 0 0 0 0 0 + + 
5 Stamens Numerous + + + + + + + 0 + $ +} + | 0 ar + + + 
6 Carpels free + 0 + + 0 + + 0 0 + ae + T 0 0 + + + 
7 Carpel Dehiscence Adaxial + 0 0 0 0 + 0 0 0 0 0 + 0 + + 0 + + 
8 Carpels More Than Five + + 0 0 + + 0 0 + + + + + 0 + + + 0 
9 Ovules More Than Two Per Carpel + + + + 0 + 0 + + 0 0 + 0 > + + + + 
10 Style Absent, Stigma Sessile 0 + + + 0 + + + + + + 0 + + + + 0 + 
11 Leaves Simple To; = te 4 + F FE Fy + + to + + 4 0 
12 Phyllotaxy Helical 0 + + + + + + + + + 0 + + + + + + + 
13 Reproductive Shoot Well-Defined + + + + + + + + + T g * Ff + = + 0 0 
14 Flowers Solitary on a Leafy Cyme + + т + + 0 т + EE 0 t + + 0 0 0 + + 


SQH.LINVAVHOMWV —ANVWO $ маноша [#861 


6LE 


380 


Бе BLE 2. Comparison of ће 2 M li 
y Takhtajan (1969). + indicates agree 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


nt. — indica 


geri plant with the angiosperm morphotype elaborated 
cates = ? indicates character unknown їп А. 


ан ( ) indicates uncertainty ae possible agreem 


Vegetative Reproductive 
+ Woody (+) Flowers Entomophilous 
— Evergreen + Radially Symmetrical 
+ Leaves Simple (+) Bisexual 
+ af Margin Entire + Flowers Terminal on Leafy Branches 
+ Leaves Pinnately Veined + Receptacle Elongated 
? Leaves Glabrous — Perianth Parts Numerous 
? Stomata Paracytic — Perianth Parts Passing Gradually into Foliage Leaves 
? Multilacunar Nodes with a Median Double e Stamens Numerous 
race Stamens Laminar 
? Vessels Absent ? Microsporangia Long and Narrow 
? Tracheids with Scalariform Pits ? Pollen Monosulcate 
Wood Parenchyma Absent or Diffuse + Carpels Numerous— Helically Arranged 
Apotra che al + Carpels е 
? Rays Multi High Uniseriate Wings + Carpels Stalked 
? Phloem Cond уза Absent plicate—Suture Adaxial 


~ ~ | 


+ Carpels Сопди 
(+) Carpels Incompletely Closed 
+ Fruits Multifollicles 


vules 
(+) тов Ny sire Median and Lateral Carpel 
Vein 


Seeds pes 
Endosperm Abundant 


Embryo Small and Undifferentiated — — — 


plain zonation. This, too, shows follicles, but they 
are apparently borne in a unisexual, panicle-like 
cluster. 

From these records alone it is clear that fol- 
licles were a very early innovation in flowering 
plant evolution and that the origin of the con- 
duplicate carpel remains an important issue in 
angiosperm phylogeny. Contemporaneous with 
these species, however, are other kinds of floral 
organs that are very different. A well-preserved 
pentamerous flower is known from the Janssen 
Clay Member of southern Nebraska and also oc- 
curs at the Linnenberger Ranch locality (Basinger 
& Dilcher, 1984; Dilcher & Basinger, unpubl. 
data). Each flower had five loosely fused carpels 
with abaxial dehiscence. Leaves and reproduc- 
tive structures very similar to those of extant 
Platanus are common in the Dakota Formation 
(Dilcher, 1979) and also occur as early as sub- 
zone IIB (Krassilov, 1977; G. Upchurch, pers. 
comm.; Dilcher & Schwartzwalder, unpubl. data). 
Other mid-Cretaceous angiosperm reproductive 
structures may also have been unisexual (Dilcn- 


er, 1979; Retallack & Dilcher, 1981b). Such plants 
clearly demonstrate that on present evidence the 
magnoliid floral organization seen in Archaean- 
thus does not predate other very different kinds 
of flowers, including. apparently unisexual и 
їп weve, 
add significantly to our knowledge of e an- 
giosperm reproductive diversity and demon- 
strates the existence of a well-differentiated, rel- 


lution. 


LITERATURE CITED 


ANDREWS, H. N. 1966. Index of generic names of 
fossil plants, 1820-1965. Bull. U.S. Geol. 
1300: 1-354. d 
ARBER, E. A. N. & J. PARKIN. 1907. On the origin 

perms. J. Linn. Soc., Bot. 38: 29-80 


angios in 
BAILEY, I. W. 1944. The development of vessels 


en 


чә. — 


A 


1984] 


angiosperms and its d in morphological 
research. Amer. J. Bot. 31: 28. 

BASINGER, J. Е. & D. L. ns Tab Pré Ancient bi- 
sexual flowers. Science 224: 511—513. 

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LESQUERIA: AN EARLY ANGIOSPERM FRUITING 
AXIS FROM THE MID-CRETACEOUS! 


PETER R. CRANE? AND DAVID L. DILCHER? 


ABSTRACT 


Lesqueria elocata (Lesq.) Crane & Dilcher, an early angiosperm fruiting axis, is described from the 
mid-Cretaceous (Upper Albian-Middle on manian ta ало of central Kansas and the 
Woodbine Formation of northeastern The s s based on three-dimensional molds pre- 
served in sandstone. The fruits (multifollicles) ааа - 175-250 follicles borne helically, i in a tight, 
more or less spherical or ovoid head. The receptacle below the 


assignment of L. elocat ta to} 


ed, with two terminal prolongations, and dehisced along a single 
ial suture. The follicles contained 10-20 seeds arranged i in two longi 


tudinal rows. The former 
be most 


d Lesqueria is shown to 
d 
Гы "Y 


T EET Ai 
sir nilar t 


magnoliid flowering plants. 


Until recently, knowledge of early angio- 
sperms has been almost exclusively restricted to 
isolated pollen grains and leaves. Although some 
conclusions may be drawn about the systematic 
relationships of the plants from which these or- 
gans were derived, progress in interpreting the 
systematic affinities ofthe earliest flowering plants 
has been considerably inhibited by a lack of 
knowledge of their reproductive structures. In 
this paper we describe an early angiosperm fruit 
from the mid-Cretaceous of central United States. 
The fruit ШЫБЫН) comprises a receptacle 
bs a terminal cluster of tightly packed prire 
ly evaluate its evolutionary significance i in pem 
tion to the known fossil record of early angio- 
sperm reproductive structures 

One element in the early formulation of mag- 
noliid floral theory was the superficial similarity 
of generalized Magnolia-like flowers to the ‘flow- 
ers’ of the Bennettitales (Arber & Parkin, 1907). 
Although it is now clear that these two kinds of 
reproductive organs are very different in detailed 
structure, their superficial similarity creates some 


Fh 4 


id-Cretaceous 


difficulties for the determination of imperfectly 
wn fossil material. In his review of the ben- 
nettitalean genus Williamsonia, Seward (1917) 
excluded several species, including W. elocata 
Геза. from the Dakota Sandstone Flora of Kan- 
sas. Wieland (1928) described a species similar 
to W. elocata from the same flora as W. hespera 
and also expressed doubt as to its relationship 
with Williamsonia. In this paper we reinterpret 
both of these species based on five specimens 
from the Dakota Sandstone Flora, including the 
type material of W. hespera, and two specimens 
from the Woodbine Formation of Texas. Both 
are interpreted as поро вену fruits and be 
as a single esqueria elocata (Lesq.) Cran 
& Dilcher. 


= 


MATERIAL 


The seven specimens described in this paper 
are preserved as three-dimensional molds 12 
sandstone. Five are from the classic Dakota 
Sandstone Flora of Kansas, the other two afè 
from the Woodbine Formation of Texas. . 

Almost all of the large plant fossil collections 


Becker and P. Richardson, New York Botanical Garden, C. Mc E De ee Survey of Cana 
and B. Tiffney, Yale „уен. Е. Hueber, United States National Museum, and the Field Museum of Na 
History, for the loan : 


? Depa 
Illinois 60605. 
? Department of Biology, Indiana University, Bloomington, Indiana 47405. 


ANN. MISSOURI Bor. GARD. 71: 384—402. 1984. 


-—— о — —À,.———— = о 


at 


Ww "wge— € 


% 


1984] 


from the Dakota Sandstone (Dakota Formation) 
are preserved as impressions or molds in a fine- 
to medium-grained ferruginous sandstone. 
Although we have seen similarly preserved 
material in situ in sandstones at various central 
Kansas localities, the specimens considered here 
are from the collections of the University of Kan- 
sas at Lawrence (UKDSC), the Field Museum of 
Natural History, Chicago (FM-P), the Peabody 
Museum of Natural History, Yale University, 
New Haven (PMNH), and the United States Na- 
tional Museum (USNM). Large collections of the 
‘Dakota Sandstone Flora’ were assembled by 
Sternberg and others in the mid-nineteenth cen- 
tury (see Andrews, 1980) principally from sur- 
face weathered sandstone blocks in Ellsworth 
County. The locality for these specimens is often 
simply given as Ellsworth County, with no fur- 
ther details. Brief descriptions and discussions 
of the Dakota Sandstone Flora are given by Meek 
and Hayden (1858), Newberry (1859, 1860a, 
1860b), Heer (1861), Marcou (1864), Capellini 
and Heer (1867), Bartsch (1 896), Gould (1900a, 
1900b, 1901), Berry (1920), Tester (1931), and 
Baxter (1954). More extensive reports and illus- 
trations were given by Lesquereux (1868, 1874, 
1878, 1883, 1892), Newberry (1868), and Gress 
1922). The flora is dominated by angiosperm 
leaves and over 400 species have been described 
(Lesquereux, 1892). 

Despite considerable lateral sedimentological 
variation, the Dakota Formation in Kansas is 
generall 


no older than late Albian (Scott, 1970a, 1970b; 
Ward, 1981) and no younger than Cenomanian 
(Hattin, 1965, 1967; Eicher, 1975). It seems like- 
y that the Dakota Formation in this area strad- 
dles the Upper and Lower Cretaceous boundary 
(Zeller, 1968; Kauffman et al., 1976). 
& specimens of L. elocata are known from 
© Woodbine Formation (Woodbine Sand) of 
„кшн Texas. One was kindly donated by Ms. 
· Hamilton (IU 15726-441 9); and the other 
ge 326817) was identified by Brown (1958: 
bi )as Isoetites sp. Fossil plants from the Wood- 
ine Formation have been described by Knowl- 


CRANE & DILCHER — LESQUERIA 


385 


ton (1901), Berry (1912, 1917, 1922), Winton 
(1925), and MacNeal (1958). The flora is dom- 
inated by angiosperms, and over 80 species of 
leaves and other organs have been recognized 
(MacNeal, 1958). The Woodbine Formation 
comprises diverse sediments divided into four 
members, from the base upward; the Dexter 
ember, the Euless Member (more or less lat- 
erally equivalent to the Red Branch Member), 
the Lewisville Member, and the Templeton 
Member. The Templeton, Lewisville, and Euless 
Members are predominantly marine in origin, 
whereas the Red Branch and Dexter Members 
are predominantly non-marine sands, clays, and 
carbonaceous shales. Most of the plants, and 
probably our specimens, are from the Red Branch 
or Dexter Members. Although there are some 
plant species unique to the Woodbine Forma- 
tion, the flora is very similar to the typical *Da- 
kota Sandstone Flora' of Kansas and Nebraska 
(MacNeal, 1958). Marine and brackish water in- 
vertebrates from the upper part of the Janssen 
Member suggest a correlation with the 
Woodbine Formation in northeast Texas (Hat- 
tin, 1965). The age of the Woodbine Formation 
is generally regarded as Cenomanian (Stephen- 
son, 1952; Hedlund, 1966; Pessagno, 1969). All 
ofthe material described in this paper, therefore, 
comes from sediments of similar age, probably 
equivalent to zone III, of the palynological zo- 
nation established by Brenner (1963), Doyle 
(1969), Doyle and Robbins (1977), and others 
for the mid-Cretaceous of the Atlantic Coastal 
Plain. 


SYSTEMATICS 


The measurements given in the description are 
based on all seven specimens, with ranges and 
common dimensions given whenever possible. 


Lesqueria Crane & Dilcher, gen. nov. TYPE: Les- 
queria elocata (Lesq.) Crane & Dilcher. 


DIAGNOSIS: Fruit consisting of a receptacle 
bearing a tight, ovoid, cluster of follicles at the 
apex, and other floral organs below. Receptacle 
stout, elongated, consisting of a distal, swollen, 
ovoid, gynoecial zone bearing follicles; with an 
elongated, more or less cylindrical zone below, 
bearing numerous helically arranged laminar 
flaps. Bases of the flaps diamond-shaped, form- 
ing a distinctive pattern on the receptacle. Base 
of flower delimited by a narrow t se ridge. 
Follicles narrowly ellipsoidal with a distinct 


386 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


adaxial suture; very short stalked and with elon- Williamsonia elongata Lesq. (Seward, 1917: 
gated bifid tips. 462) (rejects the assig tto Williamsonia; or- 
DERIVATION: After Leo Lesquereux who orig- thographic error). 
inally described the type species. Isoetites sp. (Brown, 1958: 359) (brief men- 
tion). 


OTHER MATERIAL: PMNH 2403-2405, Dakota 
Formation, Kansas; FM-P3056, Dakota For- 
mation, Ellsworth County, Kansas; USNM 2782, 
Dakota Sandstone, Fort Harker, Kansas; USNM 


Lesqueria elocata (Lesq.) Crane & Dilcher, comb. 
nov. NEOTYPE: UKDSC 203—Ellsworth 
County, Kansas. 


DIAGNOSIS: As for the genus. 50598, Dakota Formation, Ellsworth County, 

SYNONYMS: Williamsonia elocata Lesq. Kansas; USNM 326817, Woodbine Formation, 

Williamsonia (?) hespera Wieland. 5 miles SE of Dexter, Texas; IU 15726-4419, 

REFERENCES: Williamsonia elocata Lesquereux Woodbine Formation, Denton County, Texas. 
(1892: 89, pl. 2, figs. 9, 9a) (brief description, NUMBER OF SPECIMENS EXAMINED: 7. 
discussion, and line drawings). FIGURES: 1—32, 42A-G, 47. 

Williamsonia elocata Lesq. (Wieland, 1928: DESCRIPTION: Fruit borne at the apex ofa stout 
39-41, fig. 5) (discussion and line drawing). vegetative axis, ca. 10 mm diam., which also 


Williamsonia (?) hespera Wieland (1928: 41— shows the bases, or former attachment, of 4 other 
47, figs. 7-10) (description, discussion, and pho- fruits. Surface of axis with a few transverse 
tographs). grooves and ridges immediately below the re- 


ieee M T TNT шн aera hy 


— 


FIGURES 1-3. .Lesqueria elocata Crane & Dilcher, comb. nov., UKDSC 203, Dakota Sandstone, central 
Kansas.— 1. Ovoid head of clustered, narrowly elliptical, follicles prior to fracturing, А-А indicates plane of 
ве it 


at the receptacle base and point of attachment to the vegetative branch (C); x 1.5.—3. Counterpart of Figure а 
note the attachment of the receptacle to the vegetative branch and the bases of other receptacles projecting into 
the sediment, see Figure 8 for details; х 1.5. 


receptacle, and the molds of individual follicles; x 1.—5. Counterpart of transverse fracture in Figure 4 seen 
m 1 : 


гесе 
at the apex the longest flaps (F) form a collar around the base of the head of follicles; x 2.5.—8. Comp 
photograph, from different orientations of the specimen in Figure 3 showing (C) the base of the receptacle 
(G) the bases or attachment points of three other receptacles; x2 


locule cast interpreted as those of seeds (H); x5.— 11. Part of Figure 9 in different orientation showing de 
outline of a seed in the locule cast formed by the distorted fruit wall (I), and the fine double groove formed by 
the two external adaxial ridges on the follicles (J); х5.—12. Detail of part of Figure 9 showing the impress! 
of the two adaxial ridges; x 30.—13. Detail of part of the specimen in Figure 9 seen obliquely from below and 
showing the grooves (J) left by the adaxial ridges of the follicles, and trati f sedi t through the adaxial 
suture; х 5.— 14. Detail of part of Figure 1 Showing sections of the cavities left by follicles. Note in each follic 


the а of two adaxial ridges which comprise the adaxial crest, one abaxial ridge, and two 
ridges; x 4, 


ы Жн 


pam 


Е" а سی‎ 


— 


— 


КЕСЕ 


—. 


~ 


CRANE & DILCHER—LESQUERIA 


387 


" 


ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL. 71 


388 


нар » (mm 


„ 


we 


CRANE & DILCHER—LESQUERIA 389 


1984] 


390 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


$ 
FIGURES 15-24. Lesqueria elocata е & Dilcher tral Kansas. 
, comb. nov., Dakota Sandstone, cen : 
PMNH 2403, transverse Pies of a head of follicles seen from above, showing cavities left by oil - 
the paired cavities fo by the double follicle tips; x 1.—16 -P3056, transverse fracture thro shed | 
of curved follicles: ie that the fractures become increasingly tangential iad the circumference of the 


1984] 


ceptacle, otherwise more or less smooth. Maxi- 
mum length of vegetative axis preserved, 28 mm 
Total length of longest specimen seen, 88 mm. 

Receptacle stout, elongated, to 56 mm long; 
comprising a distal, swollen, ovoid, gynoecial 
zone bearing follicles, with an elongated more or 
less cylindrical zone below. Gynoecial zone of 
receptacle to 14 mm long, to 25 mm diam. (max- 
imum), bearing ca. 175-250 follicles tightly 
packed into a more or less spherical or ovoid 
head, ca. 37-65 mm diam., and to 35 mm high 
Follicles borne helically, diamond-shaped in sec- 
tion at their attachment to the receptacle. Gy- 
noecial zone abruptly or gradually tapered into 
the apex of the cylindrical zone below. 

Receptacle below the gynoecial zone 40—42 
mm long, ca. 8 mm diam. , broadening slightly 
where it joins the Bui zone and bearin 
110-150 helically arranged laminar flaps which 
have distinctive diamond-shaped bases where 
they are attached to the receptacle. Diamond- 
shaped bases 2-4 mm high, 2-4.5 mm wide 
distally; generally about as wide as high, occa- 
sionally higher than wide; gradually becoming 
Shorter and wider toward the base where they 
аге 1.5-3 mm high, 3.5-6 mm wi 

Distal flaps expanded at their apex into a 
prominent lamina to 20 mm long, and to 17 mm 
wide (largest flap incomplete in length and width), 
occasionally with a weak adaxial keel. Proximal 
flaps short, to 2 mm long (always incomplete). 
Upper flaps crowded and imbricate, forming a 


i - Lamina surface with a fine granular texture, 
showing no Ке venation or other morpho- 
logical fea 

Base = че constricted where it joins 


CRANE & DILCHER—LESQUERIA 391 


the vegetative axis and with a narrow transverse 
ridge below. Base of receptacle showing a central 
pith surrounded by 10 xylem wedges. Xylem cyl- 
inder surrounded by softer tissue. 

Follicles narrowly ellipsoidal, more or less 
straight or with strong upward curvature in the 
distal third, particularly toward the base of the 
follicle cluster. Individual follicles 9-24 mm long, 
1.5-4 mm wide. Follicles contracted just above 
the attachment to the receptacle into a very short 
stalk-like constriction 2 mm long, and extended 
apically into an elongated bifid tip. Stalk 1 mm 
wide at its midpoint, broadening proximally to 
a diamond-shaped attachment to the receptacle, 
1-2 mm high, 1-2 mm wide. Follicles with two 
narrow terminal prolongations 3-5 mm long 
forming a distinct bifid tip. Each prolongation 
triangular in cross section, ca. 0.5-1 mm thick 
maximum); the inner surface of each pair par- 
allel, and ca. 0.5 mm apart. eee attached to 
the receptacle at high angles of ca. or. 

Follicles with a median, чыз e adaxial 
suture along the entire length, flanked on either 
side by a low ridge ca. 0.2 mm high, and 0.2 mm 
broad, forming an adaxial crest. Follicles de- 
hiscing adaxially from the distal end along the 
suture; also splitting apically between the 2 pro- 
longations. Follicles diamond-shaped in trans- 
verse section, to 4 mm high, slightly higher than 
broad. Abaxial follicle surface generally feature- 
less externally or with a single ridge, frequently 
with a weak median groove internally. Lateral 
margins with a prominent ridge in their median 
part; ridge less conspicuous toward the apex and 
base. Internal locule surface smooth or rugulate- 

striate. Locule uninterrupted. 

Follicle wall ca. 0.2 mm thick, thickening at 


~ 


а o 


—18.PM 403-5 seen from above, showing 


Х1.—17. Speci imen in Figure 15 rotated through cp pein 90°, и lateral views of numerous curved 
( 


19. Specimen in Pure 17 rotated through approximately 45°, 81 
, MNH 2405, fracture surface B-B (Figs 


si shows a collar formed Ба 


17, 18, 29 ѕееп same from tp brem 
eli ly arranged flaps „ар per flaps form 
21 Surface 


wıng a xture 
cylin through approximately 45°, showing a lateral view of the surface of section А-А, a curved 
drical portion of the receptacle and the posi ition of fracture р 


e B-B; xL -23. PMNH 2405, same 


nero n as Figure 22 

= the receptacle base which sho 

во E xylem, and an outer 

mo teral view of the surface of sec 
ition of the fracture plane B-B; х1. 


ows three zo nes: a central core 
zone ie hid as cortex; x 1.—24. PMNH 2404, counterpart of Figure 22, 


on A-A, the curved cylindrical portion of the receptacle and the 


ска as pith, a ring of discrete wedges 


392 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог, 71 


M 4 Oot mf? < 


FIGURES 25-32. Lesqueria 50 Crane & Dilcher, comb. nov., IU 15726-4419, Woodbine rom 
Denton C опту, ‘northeast · Те — 25. Lateral view showin њи abraded d outer surface; x 1.— 26. Specim eias 
from below e the сорани d the flaps (F) between the fol ; in 
and the cylindrical portion of receptacle: А-А line of баней біча : . Fracture of specimen — 
А-А (Fig. 26), showing the cavity formed by the swollen ды калин zone “or the receptacle, radiating, 
and the upper part of the cylindrical portion кайг receptacle; x 1.— 28. Counterpart of fracture plane in Ig 
ent x сы, Latex тири cast же the оу 1 


‚а 


1984] 


the distal end. Seeds 10-20, borne in 2 rows along 
either side of the median line, slanted adaxially 
to abaxially, proximal to distal, 3 mm long, 1.5 
mm wide 

DISCUSSION: None of the specimens have plant 
tissues preserved, either organically, or in min- 
eralized form, and all of the details reported in 
the diagnosis and description are preserved as 
cavities or impressions in the encasing sandstone 
matrix. In places, particularly in IU 15726-4419, 
there is a fine-grained ferruginous sheath sur- 
rounding the cavities left by the plant tissue, sim- 
ilar to that reported by Spicer (1977) for Dakota 
Sandstone leaf fossils and leaves from Recent 
depositional environments. None of the impres- 
sions, however, have yielded cellular detail. Al- 
though there has been some distortion, none of 
the specimens were significantly compressed 
during fossilization. 

SC 203 shows the way in which the 
flowers were borne on the vegetative axis (Figs. 
3, 8). At the apex of this vegetative axis there 
are the bases, or positions of attachment of four 
other floral receptacles in addition to the one 
more or less complete fruit (Figs. 7, 8). One of 
these receptacle bases is 12 mm long and clearly 
shows the attachment of the proximal flaps to 
the receptacle. The others are 4 mm long or less 
and abruptly truncated, suggesting that the fruits 
frequently abscised at the receptacle base when 


at this point (Figs. 22-24), and the manner in 
which the sediment differentially penetrated the 
base of the receptacle 3) I vided some 
information on the anatomical structure at the 
base of the flower (Fig. 42D). 

In addition to the receptacles or receptacle at- 
tachments, on UKDSC 203 there are three other 
Projections into the matrix from the apex of the 
vegetative axis. They are smooth walled, taper 
distally, and are all less than 10 mm long. They 
may have been formed by buds, or in the case 
ofthe smallest, perhaps by a petiole base. At least 
9ne of these holes seems to subtend a floral axis, 
d оз others do not clearly show a similar re- 


The complete proximal cylindrical zone of the 


л o з ле Tue 


~ 


Teceptacle immediately below the follicles; x 3.—31. Detail of Figure 28 waiting 
very short constrictions forming the sta 
6.—32. Detail of Figure 27 showing molds of expanded follicle ssa 


three follicles 


(Mp. ~ - Note locule casts (K), 


CRANE & DILCHER—LESQUERIA 


393 


receptacle is preserved іп UK DSC 203 (Figs. 2, 
3), PMNH 2405 (Figs. 20, 22, 24), and USNM 
2782, 50598 but the distal gynoecial zone is most 
complete in IU 15726-4419 (Figs. 27, 28). The 
two specimens from Texas show slight differ- 
ences from the Kansas specimens, for example 
IU 15726-4419 has straighter follicles, and the 
very short cylindrical portion of the receptacle 
preserved in USNM 326817 shows no sign of 
laminar flaps. However, the evidence to separate 


with the Kansas кыгы ot L. eloc 

The gynoecial zone of IU 15726- 44 Т 9i is slight- 
ly compressed laterally! from what we assume was 
Or iginall ya but merges 
gradually at the base with the zone below (Figs. 
27, 28, 30). In UKDSC 203 and USNM 50598 
the transition into the cylindrical portion of the 
receptacle i is more abrupt (Figs. 2, 3). 

T ri ion of the receptacle is 
probably equivalent to the “cylindrical scal 
pedicel” mentioned by Lesquereux (1892). The 
bases of these flaps, which produce the charac- 
teristic diamond-shaped pattern on the recep- 
tacle, change in size and shape from the apex to 
the base (Figs. 7, 22), but the transition is grad- 
ual. In UKDSC 203 the receptacle is interrupted 
approximately in the middle of this zone and 

blocked by a small plug of sandstone that 
must have penetrated through a line of weakness 
in the rotting receptacle relatively early in fos- 
silization (Fig. 7). 

The impressions formed in the matrix by the 
flaps gradually become thinner away from their 
attachment, and there is no indication of a reg- 


while still attached to the receptacle. A few of 
the flaps on PMNH 2405 show a weak adaxial 
keel at their base. Their morphology is otherwise 
unclear and they show no sign either of pollen 
sacs or venation (Figs. 18, 21, 42B, C). We do 
not know their original size or shape, but cer- 
tainly those immediately below the flower were 


alo 
the base of the gynoecium (Figs. 18, 20, 22, 42А). 
The largest collar of persistent flaps is seen in 


longitudinal fracture through 
FU - the expanded follicle 


394 


PMNH 2405, but smaller flaps occur in USNM 
50598, IU 15726-4419 (Fig. 26), and UKDSC 
203 (Fig. 7). A specimen figured by Lesquereux 
(1892, pl. 2, fig. 9a) may be the base of the gy- 
noecial zone, and its collar of persistent flaps, 
seen from below. 

The transition that the bases of the flaps ex- 
hibit along the receptacle could reflect a gradual 
change in the size and shape of the lamina. Two 
interpretations seem possible to us: either there 
was a gradual transition between two kinds of 
perianth parts, or a transition from stamens with 
broad laminar filaments to tepals. We have no 
data to favor one explanation over the other and 
have seen no evidence of pollen sacs on the upper 
flaps. A bisexual flower would be more consistent 
with our interpretation of the systematic affini- 
ties of Lesqueria based on the number and ar- 
rangement of the carpels. Unisexuality is rela- 
tively uncommon among living plants with 
polycarpic flowers, but this possibility cannot be 
excluded. 

The expanded bases of the follicles, the short 
stalks, and their attachment to the receptacle are 
best seen in IU 15726-4419, which clearly shows 
them arranged in helices (Figs. 27, 28, 31, 32). 
The follicle bases are similar in PMNH 2405 but 
less well preserved. Other details of the follicles 
are well preserved in UKDSC 203 (Figs. 4–6, 9) 
although the apices are also seen in USNM 2782, 
50598, 326817, FM-P3056 (Fig. 16), and PMNH 
2405 (Figs. 15, 17). These specimens show nar- 
row bilobed terminal prolongations of the folli- 
cles that probably correspond to the ‘bristles’ 
mentioned and figured by Lesquereux (1892, pl. 
2, fig. 9). In a few follicles the extreme apex of 
each style-like prolongation is slightly expanded, 
and it is possible that this swelling, and perhaps 
also the adaxial crest, may have been stigmatic. 
The two style-like prolongations occur in both 
dehisced and non-dehisced follicles so we dis- 
count the idea that they are formed by splitting 
of a single elongated style at maturity. 

In dehisced follicles the matrix penetrated 
through the open adaxial suture and also distally 
between the two apical prolongations (Fig. 9). 
Where a complete cast of the locule is formed in 
this way, both internal and external features of 
the follicle and the thickness of the follicle wall 
can be interpreted (Fig. 9). Two follicles on 
UKDSC 203 show irregular holes in the locule 
fill arranged in a single line on either side of the 
median plane (Figs. 10, 420). They are slanted 
from proximal to distal, adaxially to abaxially, 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


and we interpret these as molds of seeds. We 
estimate there would have been approximately 
ten to 20 seeds in each follicle. In his original 
description of the species Lesquereux (1892) 
mentioned transverse undulations in some fol- 
licles that may also reflect the positions of seeds. 
In USNM 326817, the cast of the inner locule 
surface shows a distinctive rugulate-striate pat- 
tern oriented proximally to distally, adaxially to 
abaxially, but in all other specimens the locule 
surface is smooth. Reconstructions of the Les- 
queria follicles are given in Figure 42E-G 
In his discussion of W. hespera Wieland (1928: 
46) mentioned “three scale-like bodies about each 
sporophyll or unit." Each of these sporophylls is 
equivalent to what we interpret as follicles. We 
ave seen no good evidence of any organs at the 
base of each follicle but the cavities that Wieland 
interpreted as ‘scale-like bodies’ are visible on 
FM-P3056, and in his original specimen PMNH 
2405 (Figs. 15, 16). In our view these cavities 
are spaces remaining between the follicles that 
were not filled by either sand or mineral depo- 
sition during fossilization, and they are quite dif- 
ferent from the cavities formed as molds around 
the plant tissues. In places mineralization 00087 
to have followed the plant surfaces but did not 
completely fill the cavities between them, pat 
ticularly where no sand had penetrated. Similar 
cavities occur occasionally between the two ter- 
minal prolongations of the follicles, an unlikely 
position for scales. Where they occur, these сау- 
ities are irregularly arranged and are completely 
absent from USNM 2782, 50598, and UKDSC 
203. 


COMPARISON WITH FOSSIL PLANTS 


Although the holotype of Williamsonia elo- 
cata Lesq. is lost, from the original descriptio" 
and illustration we have no hesitation in ое. 
ing our speci to this speci d establishing 
UKDSC 203 from the same geological formation 
and the same geographical area as а пеогуре. 
Williamsonia hespera Wieland (1928) and Iso- 
etites sp. (Brown, 1958) are clearly the sam 
species. Seward (1917) and Wieland (1928) que 
tioned the assignment of W. elocata and w. wi 
pera respectively to the genus Williamso 
confirm their opinions and have no doubt a 
both species belong neither in Williamsonia 0” 
the Bennettitales. The structures at the apex ee 
the receptacle are follicles with a distinct ge^ : 
tudinal adaxial suture and contain seeds. u је 
liamsonia we would expect ‘interseminal 


p- 


e 


oo = о. о. о = = "<= === = nd о ll ll 


МЕ mm аш 


1984] 


among stalked ovules, with bracts (‘perianth’) 
below (Harris, 1969). In our view Lesqueria elo- 
cata is clearly a multifollicular angiosperm fruit. 

The reassignment of ~“ Williamsonia" elocata 
to the angiosperms calls into question the rela- 
tionship of other poorly understood Cretaceous 
Williamsonia-like plant organs for example: Pa- 
laeanthus hollickii Seward & Conway (1935а) 
from the Upper Cretaceous of Kingigtock, West 
Greenland; Palaeanthus tenuistriatus Seward & 
Conway (1935b) from the Upper Cretaceous of 
Igdlokunguak in the same area; Palaeanthus sp. 
Seward & Edwards (1941) from the Palaeocene 
of Kangerdlugssuak, East Greenland; Palaean- 
thus prindlei Hollick (1936) from the Palaeocene 
of Alaska; Williamsonia cretacea Heer (1880) 
from the Upper Cretaceous of Atanikerdluk, West 
Greenland; Williamsonia reisii Hollick (1906; 
Leppik, 1963) from the Upper Cretaceous of Sta- 
ten Island; Williamsonia delawarensis Berry 
(1916) from the Upper Cretaceous of Maryland; 
Velenovskia opatovi isK h (1974) from 
the Cenomanian of Czechoslovakia; and many 
other poorly known species that might be inter- 
preted as angiosperms just as easily as bennet- 
ütaleans on the data available. We have seen 
none of the original specimens, but these and 
similar species would be worth reexamining. We 
have, however, examined specimens of two Wil- 
liamsonia-like fossils, Williamsonia? recentior 
Dawson and the type species of Palaeanthus, P. 
problematicus Newb. 

Williamsonia? recentior Dawson (1886; Sew- 
ard, 1917; Bell, 1956) is from the ‘Upper Blair- 
more Flora' of southwestern Alberta, generally 
accepted as of Albian age (Glaister, 1959; Norris, 
1964; Rudkin, 1964; Mellon, 1967; Price & Mo- 
untjoy, 1970; Stelk, 1975; Stott, 1975; and Singh, 
1975). The holotype of the species (Fig. 37) is 
Preserved as a compression in an indurated grey 
shale. It shows a head of numerous, apparently 
helically arranged, follicles with indications of 
Scars below. The follicles show curvature similar 
to those of Lesqueria. We estimate that the gyn- 
сеста! zone bore about 150 to 200 follicles. The 
general appearance of the head (but not of the 
remainder of the receptacle) is similar to L. elo- 
cata. The scars and remainder of the receptacle 
are more similar to Archaeanthus linnenbergi 
(Dilcher & Crane, 1984). 

The Original material of Palaeanthus proble- 
тапси described by Newberry (1886, 1895) is 
from the Amboy Clays (Raritan Formation) of 
New Jersey, which are generally regarded as of 


CRANE & DILCHER—LESQUERIA 


395 


Middle to Upper Cenomanian age (Christopher, 
1979 and references cited therein). We have not 
seen the specimens described later from Gay 
Head, Martha’s Vineyard (Hollick, 1896, 1906) 
and Glen Cove, Long Island (Hollick, 1912) but 
from the illustrations judge that they may be a 
different taxon. The specimens from New Jersey 
(Figs. 38—41) are preserved in a grey micaceous 
silty-clay, though organic material may о 
have been present, most of it is now missing. 
However, the impressions show heads of about 
50 to 80 follicles, some with a longitudinal adax- 
ial suture; these are surrounded by another zone 
of more or less linear, to narrowly triangular, 
structures. Two of the best of these structures on 
one specimen (New York Botanical Garden, 
11420G, now at PMNH) show a prominent bi- 
lobed expansion at the apex. Several authors have 
discussed the botanical relationships of P. prob- 
lematicus (Newberry, 1895; Stebbins, 1940; 
Cronquist, 1955) and suggestions for closest rel- 
atives have ranged from Williamsonia to the 
Compositae. In our view, P. problematicus is an 
angiosperm fruit of many follicles and is very 
similar to material collected from the Dakota 
Formation of Hoisington, Barton County, cen- 
tral Kansas (IU 15706) (Figs. 33, 34, 36). One 
specimen from Hoisington (Fig. 35) is more sim- 
ilar to Archaeanthus linnenbergeri (Dilcher & 
Crane, 1984). Liriophyllum leaves, probably be- 
longing to the Archaeanthus plant, also occur at 
the Hoisington locality. 

Palaeanthus problematicus and “ Williamson- 
ia” recentior taken in conjunction with Lesqueria 
elocata and Archaeanthus linnenbergeri unam- 
biguously demonstrate the diversity and ubiq- 

ic fl id-Cretaceous 


A 1 


пл, 


uity of polycarp 
early angiosperms. 
COMPARISON WITH RECENT PLANTS 


Among Recent angiosperms, Lesqueria is most 
similar to polycarpic taxa, most of which occur 
in the Magnoliidae. The Lesqueria head of fol- 
licles most closely resembles those of Magnelie- 
па (Magnoliaceae; Canright, 1960) and Talauma 
(Magnoliaceae). Magnelietia hainanensis has a 
tight ovoid cluster of carpels borne on a swollen 
distal portion of the receptacle. The receptacle 
in Himantanara is similar but much smaller. In 
Talauma (Fig. 46) the cluster of carpels at flow- 
ering stage is very similar to the head of follicles 
in Lesqueria. Annona, Dugetia (Figs. 43, 44) 
(Annonaceae; Fries, 1931, 1934), and Schizan- 
dra (Smith, 1947) also show tight clusters of car- 


396 ANNALS OF THE MISSOURI BOTANICAL GARDEN [уо 71} 


сега central Kansas. 37. “Williamsonia” recentior Dawson from the Blairmore Grove 


, 
набу ys (Rari 

late Cenomanian of New Jersey).—33. IU 15706- 3078; x1. i IU 15706- 3077, BE тае IU 15706-3084; | 

NYBO) за: IU 15706-3083; x 1.—37. Geological Survey of Canada 5105; x 1.—38. New York Botanical Garde | 

( uu £n te аа NYBG 11447G, NEU (1895, * 34 ~ T Es sap NYBG 114206, Newberry | 


1984] CRANE & DILCHER—LESQUERIA 397 


Diagram of the Lesqueria receptacle and 
f the receptacle; uf, upper flaps forming 

another receptacle; va, 
tacle.— wing 


F : 
IGURE 42, Lesqueria elocata Crane & Dilchor, comb. nov.—A. 


atta . 
сћед organs: fo, tight clusters of follicles; gz 
ot f (E 


crest; ar, abaxial ridge: Ir i seed 
ER > M, lateral › S, -TT е 
showing position of seeds. ores d 


Lesqueria. All, however, are bisexual and would 
be consistent with an interpretation of the per- 
sistent upper flaps in Lesqueria as stamens. 
Whatever the botanical nature of these flaps, 


еи ? Schizandra the receptacle elongates 
iium qu at maturity. None of these genera, 
i have the gynoecial zone at the apex of 

cylindrical receptacle, such as occurs in 


398 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


a 


Fruits of Recent plants with numerous follicles. MO, herbarium of the Misso 
27650 


FiGures 43-46. 
Garden. —43. Dugetia uniflora (Dun.) Mart., Brazil, M 
MO 2873354; x1.—45 


sp., Panama, MO 2778717; x1 


gradual transitions between different floral or- 
gans are common in plants with numerous floral 
parts. Gradual transitions of stamens into tepals 
occur, for example, in Eupomatia, Paeonia, and 
the nymphaeaceous genera Euryale, Nymphaea, 
and Victoria (Moseley, 1958). However, we know 
of no Recent angiosperm in which the length of 
the non-gynoecial portion of the receptacle is as 
elongated as it is in Lesqueria. Another unusual 
feature is the persistence of the flap-like floral 
organs below the follicles. Many parallels exist 
in the Magnoliidae, however, for the clustered 
arrangement of flowers in Lesqueria. The irreg- 
ular cymose inflorescences of some Annonaceae, 
for example, are quite similar. 

The double follicle tip in Lesqueria is similar 


and Goniothalamus (Annonaceae). The 
fruits of these genera are not follicles, however, 
and the two styles do not persist to fruit maturity. 

Although it is clear from this brief review that 
some Magnoliidae have various features that are 


i Botanical 
9; x 1.—44. Dugetia cordata R. E. Fries, Brazil, 


. Anaxagorea sp., Venezuela, MO 2726969; x1.—46. Young multifollicle of Talauma 


similar to those of Lesqueria, we know of no 
Recent plant that has the combination of nu- 
merous, helically arranged, dehiscent follicles 
with bifid tips borne in a swollen head at the 
apex of a long receptacle bearing numerous, per- 
sistent, spirally arranged, laminar stc 
Further comparison of Lesqueria with pa 
angiosperms is limited by lack of knowledge 9 
other parts of the plant, including wood, ud 
staminate floral parts, and particularly by UM 
uncertainties over the interpretation of the У 
inar flaps. However, it is clear that Lesquer y 
a fruit comprised of many follicles and that үс: 
Lesqueria plant is an extinct angiosperm, P : 
ably most closely related to the magnolialea 

group of the Magnoliidae. 


E 
CONCLUSIONS — EVOLUTIONARY SIGNIFICANC 


| "E to 
Lesqueria elocata contributes эрин al 

our knowledge of the reproductive dive d 

early flowering plants. Along with Archaea 


le- 
(Dilcher & Crane, 1984), Palaeanthus prob 


i 
f 


1984] 


maticus, and “ Williamsonia" recentior, it dem- 
onstrates that the basic floral organization, con 
sisting of numerous, adaxially dehiscent, follicles 
borne helically on the distal part of a receptacle 
with another floral organ(s) below, was wide- 
spread and common at an early stage in angio- 
sperm evolution. These plants also illustrate the 
diversity that magnoliid plants had attained some 
ten to 15 Ma after the first apparently unequiv- 
ocal angiosperm leaves and pollen appear in the 
fossil record (Doyle & Hickey, 1976; Hickey & 
Doyle, 1977; Doyle, 1978; Hughes et al., 1979). 
Today the Magnoliid t 1 
heterogeneous, exhibiting various mosaics of 
primitive and advanced characters (Takhtajan, 
1969; Cronquist, 1981). The fossil evidence from 
Archaeanthus, Lesqueria, Palaeanthus proble- 
maticus, **Williamsonia" recentior, and other 
material suggests that the Magnoliidae were also 
diverse during the mid-Cretaceous. Extinction of 
some of the mid-Cretaceous magnoliid diversity 
may well account for some of the large morpho- 
logical gaps that separate the Recent genera and 
families in this group. 

It is important to recognize that these mag- 
пода flowers occur contemporaneously with 
other very different kinds of angiosperms, in- 
cluding bisexual, unisexual, and evidently insect 
and wind pollinated forms (Dilcher, 1979; 
Vakhrameev & Krassilov, 1979; Retallack & 
Dilcher, 1981; Dilcher & Crane, 1984). However 
the mid-Cretaceous magnoliids are of particular 
Interest in relation to concepts of the primitive 
angiosperm flower. The current, most widely ac- 
cepted view, based almost entirely on compar- 
alive studies of living plants, is that the Mag- 
noliidae, and in particular the Magnoliales, are 
the most primitive living group, and that the 
primitive angiosperm flower was of generalized 
magnoliid construction (Bessey, 1897; Arber & 
Parkin, 1907; Bessey, 1915; Cronquist, 1968; 
Takhtajan, 1969; Hutchinson, 1973; Cronquist, 
1981). The hypothetical primitive flower is en- 
Visaged as radially symmetrical, bisexual, and 
€ntomophilous. The receptacle would have been 
elongated, bearing numerous helically arranged, 
undifferentiated perianth parts, numerous lam- 


1 . 
Паг stamens, and numerous free, conduplicate 
Carpels thot dL: EA d Pos 1 22 


arce and 


4: 
мус з аны 


Suture. The carpels would have contained nu- 
Merous ovules that developed into many large 
5 (Takhtajan, 1969). Although no known 


ination of characters, Lesqueria, Archaean- 
us, Palaeanthus problematicus, and “ William- 


CRANE & DILCHER—LESQUERIA 399 


Figure 47. Reconstruction of the Lesqueria elo- 
cata fruiting axis. 


sonia” recentior conclusively establish that some 
of these allegedly primitive features are also an- 
cient. 

LITERATURE CITED 


Anprews, H. N. 1980. The fossil hunters. Cornell 
Univ. Press, Ithaca and London. 
& 1907. On the origin of 
. 38: 29-80. 


weste. 
Univ. 3: 178-182. 


400 


BAXTER, R. W. 1954. The University of Kansas col- 
lection of fossil plants. I. The eee Sandstone 
flora. Trans. Kansas Acad. Sci. 57: 4 

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— 


PRELIMINARY REPORT OF UPPER CRETACEOUS 
ANGIOSPERM REPRODUCTIVE ORGANS 
FROM SWEDEN AND THEIR 
LEVEL OF ORGANIZATION! 


E. M. FRIIS? 


ABSTRACT 


а г. 1 


Wel d Upper Cretaceous of Sweden provide 
in biti knowledge of structure and evolutionary relationships of Cretaceous angiosperms. The 
material includes a diverse assemblage 


Theories of evolutionary relationships within 
the angiosperms are largely based on compara- 
tive studies of the flower structure. The study of 
fossil flowers is therefore essential to the under- 
standing of the origin and evolution of the an- 
giosperms. However, angiosperm flowers are rare 
in the fossil record, and less than 200 species 
have been described so far 

The amount of зивота он obtainable from 
these fossils is variable, depending largely on the 
mode of preservation. Floral structures and ar- 
rangement of parts are best studied in three-di- 
Wiser: Preserved flowers, but few flowers 


ee е as compressions ог, if com- 
val e as impressions. Such material 
ког Y yields very incomplete information оп 
oral details, but the recent application of 
ale techniques and electron microscopy has 
ks the Considerable potential for studies of 


3 
о 


n the 
of of Noh America (Crepet & Dicker 1977; Cre- 


mes 19 : 
ms Ко 80; Crepet et al., 1980; Dagh 


——À— 


I 
lam ae Беба to W. G. Chaloner, P. Crane, R. Dahlgren, D. 
the pra iy for constructive — 


~ encouragement duri 
viding sa eris from т L.E 


isk, suggesting adaption to insect-pollination. A number of floral 
presented for the fossil flowers of Sweden, and their systematical position is discussed. 


corolla, sometimes together with 
ral diagrams are 


The majority of fossil flowers are known from 
Tertiary deposits, and only about 20 different 
species have been described from the Cretaceous. 
The most important source of information on 
Tertiary fossil flowers is probably the Paleogene 

ic Amber, which accounts for about one-third 
of os known record. Owing to the amorphous 
texture of the amber and that it was fluid at the 
time of incorporation of the fossils, very fine 
details have been preserved (Goeppert & Ber- 
endt, 1845; Caspary, 1872, 1881a, 1881b; Con- 
wentz, 1886; Larsson, 1978). The amber fossils 
are strictly molds, with very little organic ma- 
terial remaining, and thus anatomical details are 


scarce. g 
on the morphology and the structure of the fos- 
er however, it has been possible to establish 
affinity for a large proportion of the 
eon flowers (Conwentz, 1886). 
Anatomical information is usually obtainable 
from petrifactions, but. reconstructions of ar- 
problem- 
atic, and establishment of the botanical affinity 
is often uncertain. One of the few eesti оың 
егѕ 15 Ра 1976) 
from the Eocene of British Columbia. This is 


ee 
-4 


t, and to A. Skarby "m 
mer € up canted: зай as ү! in preparing the 
el microsco 


L ae H. Friis, mes K. Raunsgaard Pederse 
the 


from th Department, University of Copenhagen. I gratefully acknowledge the receipt s a инка fellowship 
‘eat British Council and from the Danish Natural Science R 
Ogisk Institut, Aarhus Universitet, Universitetsparken 8000, Aarhus C, د‎ 


ANN. Missouri Вот. GARD. 71: 403-418. 1984. 


404 


probably the most fully known of these petrified 
structures. Few other species were described from 
the Intertrappean beds in Deccan, India, prob- 
ably of Eocene age (Shukla, 1944; Prakash, 1956; 
Chitaley & Patel, 1975, for example). Cretovar- 
ium japonicum Stopes & Fujii (1911) is imper- 
fectly preserved but is significant in being the 
only petrified floral structure described from the 
Cretaceous. 

No f 11 n have heen de. 


scribed yet from the Lower Cretaceous, but from 
fossil fructifications we know that reproductive 
structures were diverse by the late early Creta- 
ceous (Dilcher et al., 1976; Dilcher, 1979; Vach- 


umented by fruiting as well as floral structures 
from Europe (Velenovsky, 1889; Bayer, 1914: 
Velenovsky & Viniklár, 1926, 1927, 1929, 1931) 
and from North America (Dilcher, 1979; Dilcher 
& Basinger, 1980; Dilcher & Crane, 1984; Crane 
& Dilcher, 1984). 
геи the ие Cretaceous guit 
tly been dis- 
covered from eastern КОА. America (Tiffney, 
1982 and pers. comm.; Hueber, pers. comm.) 
and from Scania, кинен Sweden (Friis & Skar- 
by, 1981, 1982; Friis, 1983). This review is an 
attempt to illustrate the diversity in structure of 
the Upper Cretaceous angiosperms based on the 
study of the well-preserved Swedish material. 
Special attention is directed to the various or- 
ganizational levels of the fossil flowers, and floral 
diagrams of the main basic types are presented 
(Figs. 1-9). Although the taxonomic study of the 
Swedish material is still at an early stage, it has 
been possible to demonstrate relationships be- 
tween some of the fossil taxa and modern plant 
groups at the family or ordinal level. 


MATERIAL 


he angiosperm fossils described here were 
collected from the upper part of the fluviatile 
sequence in Höganäs AB's clay pit at Åsen, 
southern Sweden. The age of the sediments is 
probably Upper Santonian or Lower Campanian 
(Friis & Skarby, 1982). 

The fossils were obtained from unconsolidated 
clays and sands by sieving in water. They were 
then cleaned in hydrofluoric and hydrochloric 
acid. 

The material comprises a diverse assemblage 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


of leaf fragments, twigs, megaspores, sporangia, 
flowers, fruits, seeds, and anthers (Friis & Skar- 
by, 1981, 1982; Friis, 1983). The majority offos- 
sils represents angiospermous plants, and more 
than 100 taxa have so far been recognized. The 
commonest of the angiosperm fou are b. 
and seeds, but the floral st 
an important element of the flora. 

The fossils are mainly preserved as three-di- 
mensional charcoal fossils, probably formed as 
a result of a forest fire (Friis & Skarby, 1981). 


ed study 


Their excellent 
of arrangement t of рай However, the material 
shows certain limitations. The fossil flowers are 
generally found isolated from the rest of the plant 
and the orientation and inflorescence structure 
Dd thus =o The lack of parts in some flow- 

may be primary, but could also be caused by 
audi no fossilization. Very delicate ог 
protruding parts such as stamens and petals may 
be broken in open flowers and the study of such 
parts is often referred to fragments or scars or t0 
flower buds when present. In spite of these lim- 
itations, the material yields useful information 
on the organization ofthe flower structure reached 
by the uppermost Cretaceous and represents à 
significant addition to the known record of an- 
giosperm flowers. 


DIMENSIONS OF THE ANGIOSPERM 
OSSILS FROM SWEDEN 


The fossil angiosperm flowers, fruits, and seeds 
from Asen are all of small size, the largest Tow 
being about 4 mm long, and the dimensions ? 
the fruits and seeds range from 0.2 to 5 mm. ^? 
fragments of larger fruits and seeds have e: 
observed among the fossils, but larger frag 
oftwigs and wood are common in some samp 
The size distribution of the fossils is appare Es 
independent of the texture of the sediment 6 
the absence of larger fruits and seeds cannot 
explained by sortin P 

The ch gi size T the Swedish fossils 1$ con 
sistent with the dimensions quoted for fruits ss 
ind of most other Upper Cretaceous floras 


1950: Hall, 1963). A few fossil doc p 
large angiosperm fruits and seeds have 3 
ported from the Cenomanian of Europe rid 
novsk$ & Viniklár, 1926) and North Ame 


| 


| 


~ 


— 


-— 


FRIIS— ANGIOSPERM REPRODU( 


ORGANS 


1984] 


(Dilcher, 1979), and from the Upper Campanian 
or Maastrichtian of Africa (Monteillet & Lap- 
partient, 1981). 

In Recent plants very small seeds are charac- 
teristic of epiphytes, saprophytes, and parasites. 
Small seeds are also common among herbs as 
well as woody plants inhabiting open country 
and are especially common in plants of early 
stages in vegetation succession (Harper et al., 
1970; Stebbins, 1974). It is possible that the small 
size of the fossil fruits and seeds in many of the 
Cretaceous floras might be explained by paleo- 
ecological conditions. However, a number of 
other factors should also be considered (see Tiff- 
ney, 1984). 


LEVEL OF ORGANIZATION OF THE 
FossiL FLOWERS FROM SWEDEN 


The Swedish material includes more than 20 
different floral structures. The fossil flowers are 
apparently all bisexual and cyclic with a definite 
number of parts in each whorl. The perianth is 
well developed in the majority of the flowers, 
differentiated into calyx and corolla (hetero- 
chlamydous), or consisting of only one periant 
whorl (monochlamydous). A single fossil flower 
type is apparently naked (achlamydous or apo- 
chlamydous). The position of the perianth is hy- 
Pogynous or more commonly epigynous. A va- 
ny of fruit types has been recognized, including 
follicles, capsules, nuts, and drupes. There is a 
great diversity in number of locules, placenta- 
Поп, and number of seeds. The vast majority of 
the seeds are anatropous. So far only a few or- 
thotropous and amphitropous taxa have been 
found. The seed coat varies from a thin mem- 
braneous layer, apparently formed from one in- 
на, to a thick, sclerenchymatous wall 
ormed from one or two integuments. 
Some of the basic floral types found in the 
dud sh material are described below more 
ks У, including, if possible, description of fruits 
los. 5; the organizational level ofthe different 
~ | is illustrated with floral diagrams, and 

Systematical position is discussed. 
маја Ochlamydous flowers. Flowers with 
€veloped calyx and corolla are the most 
ue among the Swedish floral structures. 
a are all actinomorphic, including hypogy- 
as well as epigynous flowers. The sepals and 
Petals are generally free, but in a few flowers the 
Sepals are fused at the bases. Some of the flowers 


ГЕ М, >< ~ 
(9) Сө) се $ 


Ficures 1-9. Floral diagrams of the basic floral 
pes found among the Upper Cretaceous fossils from 
— 1-2. Heterochlamydous, hypogynous 
ous, epigynous flow- 

ers.— 7—9. Monochlamydous, epigynous flowers. 


bear a disk and were probably nectar producing, 
adapted to insect-pollination. The flowers are 
generally pentamerous (Figs. 1, 2, 4-6). One 
flower type differs in being tetramerous (Fig. 3), 
and a small triangular fruit with persistent calyx 
indicates that also trimerous floral types were 
present. 
1.1. Hypogynous flowers with multistaminal 
androecium. One fossil genus including hypog- 
ynous flowers with a multistaminal androecium 
has been recovered among the Swedish fossils 
(Figs. 1, 10—13). It is represented mostly by frag- 
mentary specimens. The flowers are small, about 
4 mm long, borne on a thick peduncle. There are 
two thick bracteoles, five free, coriaceous sepals 
(Figs. 12, 13), and five free petals. The androe- 
cium is composed of 20 stamens in one whorl. 
The filaments are broad with slightly narrowing 
bases and a pronounced contraction at the apex. 
The anthers are elongated and almost as long as 
the filaments; they are apparently ventrifixed and 
open by longitudinal slits (Fig. 11). The surface 
es ad lo a e. ei JE «cas nnd 


edid spiny hairs (Fig. 11). None of the anthers 
have pollen preserved. The ovary is superior and 
three-loculed (Fig. 13), formed by three carpels 

d with three free styles. The surface of the 
ovary is covered with densely spaced, stiff hairs. 


406 


Each locule contains many ovules on pro- 
nounced, axile placentae. The characters of the 
fossil flowers seem to indicate a relationship with 
modern plants of the Theales, such as members 
of the Ternstroemioideae (Theaceae). 
Three-loculed capsules with a hairy surface, 
similar to that of the ovary in the fossil flowers, 
тау represent the mature fruits of similar flow- 
ers. They enclose many small seeds. The same 
seed type is very common in the samples from 
Asen, found separate from the fruits. The seeds 
are about | mm long, anatropous, with a distinct 
raphe, micropyle, and chalaza (Figs. 18—20). The 
seed coat is composed of two layers of cells. The 
outer epidermis is built of thick-walled с cells with 
eed pitted cell walls. Seve erent species, 
robably referable to a single genus, have been 
rocas The species may be distinguished 
from each other by the size and shape of the 
surface cells, the number of cell rows, and the 
thickness of the seed coat. Two different species 
are shown in Figures 18 and 20. The organization 
and structure of the fossil fruits and seeds also 
seem to indicate a relationship with some mod- 
ern Theaceae. Although campylotropous or am- 
phitror d її 1 seed type 
among modern Theaceae, anatropous seeds are 
found in some genera. The outer epidermis of 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Мог. 71 


the seed coat in many modern Тћеасеае is sim- 
ilar to that seen in the fossil seeds in having 
thickened and strongly pitted cell walls. 

Another group of seeds possibly related to the 
Theaceae has been recovered among the Swedish 
fossils. The seeds are anatropous and about 1.5 
mm long. The raphe is embedded in the sclerotic 
mesotesta (Fig. 22). The embryo cavity is elon- 
gated ellipsoidal in shape, marked on the outer 
surface by distinct cell rows (Fig. 21). The inner 
layer of testa consists of lignified cells with an- 
gular lumina, which suggests that they once con- 
tained inorganic crystals. Similar seed types also 
occur in the Lythraceae, but the fossil seems to 
differ from members of this family by the lack 
of a fibrous inner layer. 

1.2. Hypogynous flowers with haplostemo- 
nous androecium. A few other hypogynous, 
pentamerous floral structures are present in the 
fossil flora, but they are mostly incompletely pre 
served, and reconstructions of the complete 
structures have not yet been possible. One 0 


these flowers i is s shown in Figures i and 17. It 
fused in the 


basal рай, und Bii tae five в and five 
stamens. The ovary is composed of three 
carpels and there are three pronounced, 

like placentae with many anatropous ovules. 


a 


о ООН 


FIGURES 10-15. Fossil flowers мн the Upper Cretaceous of Sweden. 10-13. сүрөөсү 


flower with multistaminal an 
anther, f = filament); SEM- De 
Flower with ovary partly preserve 


um oe diagram 


-m Stamens артыг showing | hairy s 


see Fig. 1).—10. Flo 


showing three locules and. man 


VE same specimen as mss 12, x45.— 14. Small eris 


hairy ovary and three stigmas ben. SEM-209,, x 70.—15. Pollen from surface of ovary; same 5 


as Figure 14, x 3,500. 


ydous 
FIGURES 16—22. Fossil Magia and seeds from the Upper Cros E E. de Heterochlamy 


and hypogynous flower wi 


en with ovary 


and sepals partly ae SEM- 196,, x60.—17. Specimen “= ond wes ep Aine saving 
te gynoecium; et x 65.— 18—20. Anatropous seeds probably related 
w surface cells; SEM-130,, x65.—19. I 
to Pared: 18, showing hilum (h), raphe эңе а (ch), and micropyle (m); SEM-130,, х 65.— 

large surface cells; SEM-163,, x65. 21-22. Апаїг 


— 1 triparti 


е. — 18. External view of seed 


of seed with 


21. External view of seed showing surface cells; SEM- 206,, x40.—22. Section of seed sho wing гар 


embryo cavity (е); SEM-206,, x35. 


FIGURES 23-28. Fossil flowers лор the Upper С 


2).— disk 
ten-lobed 
to the Thea 
similar 
External view 


£ ‘Thence. 
he (r) and 


Internal м о 


opous seeds probably related to ^ 


he Saxifragales. (a = anthers: 


d= = disk; f= filament; p 


тасогатп се. 


ыу — x - sio. 23-24. т Friis & a heterochlam 


x55.- 
with 


24. ‘Scandianthus major Friis + кату. SEM-210,, x30. 25-28. soprano ez 


and styles; ЗЕМ-181; Mos —26. Flower: showing disk, sepals, remnants си aap 
#21. 


Stamen enlarged; за 
ovules on axile placenta; SEM. 189,, х 155. 


specimen as Figure 25; x 190.—28. Section of ovary showing many 


у; SEM-2102, 
us flo 


he epigynous 
25. Imperfectly preserved flower bud showing 


80.7 
and styles; SEM-1 S atropos 


| 


) 


o 
2, 
< 
© 
© 
щ 
Р. 
= 
A 
© 
| 
~ 
ш 
ба 
= 
2 
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2 
z 
- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


FRIIS— ANGIOSPERM REPRODUCTIVE ORGANS 409 


1984] 


410 


the base of the ovary there is a ten-lobed disk 
(Fig. 17). A preliminary floral diagram of the 
fossil flower is shown in Figure 2. 

Two or three other pentamerous flowers with 
their ovary composed of three carpels have been 
found. A single hypogynous type with a pentam- 
erous gynoecium has also been recognized. Fig- 
ure 14 shows a minute perigynous flower, about 
1.2 mm long with three stigmatic branches and 
a hairy ovary. Several tricolporate pollen grains 
have been observed on the surface of the ovary. 
This type is represented by a few, incompletely 
preserved specimens and their botanical affinity 
has not yet been examined. 

1.3. Epigynous flowers with diplostemonous 
androecium. 1.3.1. Pentamerous flowers. Prob- 
ably the most fully known flowers from the Cre- 
taceous of Sweden are those of Scandianthus Friis 
& Skarby (1982). The flowers are small, about 
1–2.5 mm long, bisexual, with radial symmetry 
(Figs. 4, 23, 24). They are epigynous with five 
free sepals and five free petals (Figs. 23, 24). 
There are ten stamens in two whorls, diploste- 
monously arranged. The anthers are dorsifixed 
and open by longitudinal slits. The pollen grains 
are small, about 10 microns in diameter, tricol- 
porate, and tectate. There is a pronounced ten- 
lobed disk between the stamens and the к 
cium. The ovar y is inferior 


formed 
by two fused carpels, and with two free styles. 
The placentae are apical-parietal and pendant, 
with many anatropous ovules. The fruit is a cap- 
sule dehiscing apically between the styles. The 
seeds are small, about 0.2 mm long, with a thin 
seed coat possibly formed by only one integu- 
ment. The presence of a disk and the very small 
size of the pollen grains suggest that the fossil 
flowers were insect-pollinated. 

Small insect-pollinated flowers of similar con- 
struction are common in a number of modern 
Saxifragalean families, and comparison with 
modern plant groups indicates a close relation- 
ship to the Saxifragales. The best correlation is 
with members of the families Hydrangeaceae, 
Vahliaceae, Escalloniaceae, and Saxifragaceae 
(Friis & Skarby, 1981, 1982). Although the most 
common organization of the androecium within 
the Saxifragales is obdiplostemonous or haplo- 
stemonous, diplostemonous types occur within 
the group. 

1.3.2. Tetramerous flowers. A single tetram- 
erous flower type has been recovered among the 
Swedish fossils (Figs. 3, 35, 36). The flowers have 
four sepals, four petals, and eight stamens, ap- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


parently lip anged. Between the 
stamens there is an «мык! disc struc- 
ture (Fig. 36). The ovary is semi-inferior and 
three-loculed, with numerous ovules. There are 
three free thick styles. The flower type is repre- 
sented by only a few incompletely preserved 
specimens and the structure is not fully known. 
The characters of the fossils suggest, however, a 
close relationship with some modern plants of 
the puri ais e.g., the Hydrangeaceae. 

1.4 ous flowers with haplostemonous 
тамыры T4 . Anthers antipetalous. The 
fossil flowers illustrated in Figures 25-28 were 
partly described by Friis and Skarby (1982). Ad- 
ditional material has since provided information 
on the corolla and the androecium. The flowers 
are small (about 3 mm long), bisexual, and ac- 
tinomorphic, with an almost epigynous perianth 
insertion. There are five free sepals and five free 
petals, which are rarely preserved. The androe- 
cium is composed of five antipetalous stamens 
in one whorl; the anthers are dorsifixed and open 
by longitudinal slits (Figs. 25, 27). Pollen grains 
have not been observed yet. There is а pro- 
nounced five-lobed disk (Fig. 26). The ovary is 
m two-loculed, and formed by two fu 

rpels. There are two free, thick styles (Fig. 26). 
ты placentation is central with many anatro- 
pous ovules (Fig. 28). The surface of the ovary 
is characterized by distinct longitudinal ridges. 
Like Scandianthus, the fossil flower is ew: 
to have been pollinated by insects because 


pronounced, perhaps nectariferous а Tis 
floral t 


ues 


ern members of the Saxifragales sand is «o 
to belong to this group. he 
1.4.2. Anthers antisepalous. An 

Swedish fossils two different flower јуре 


The flowers 


i les. 
ably also related to the Saxifraga and with 8 


are small (1-2 mm long), bisexual, TM 
more or less epigynous perianth insert pe 
perianth is composed of five free petals ап iv 
free sepals of open aestivation. There are 

antisepalous stamens; the filaments 


filaments. The pistil is bicarpellary; i 
semi-inferior and one-loculed, and its the 
simple. The fruit is a capsule dehiscing along pe 
midline of the carpels. The placentae are pa" pe 
with many anatropous ovules (Fig. 34). The 

are small and have a thin seed coat. 


— 


1984] 


The fossil flowers have many characters in 
common with those of Scandianthus, but differ 
in having only one whorl of stamens and a single 
style. Flowers of similar construction also occur 
in some modern plants of the Saxifragalean com- 
plex, and these fossil flowers should probably 
also be referred to this group. However, a more 
detailed study of their systematical affinity is 
needed before the final affiliation can be made. 

Another group of flowers from the Swedish 
material represented by many well-preserved 
specimens is illustrated in Figures 31-33. The 
flowers are about 1-2 mm long, bisexual with 
radial symmetry. The perianth is epigynous com- 
posed of five free sepals and five free petals. There 
is one whorl of antisepalous stamens. The fila- 
ments are thread-like and the dorsifixed anthers 
open by longitudinal slits (Fig. 33). Pollen grains 
have not been observed. Between the stamens 
and style there is apparently a broad disk. The 
Ovary is inferior and unilocular, formed by two 
carpels, and with one style. The placentae are 
parietal and marginal, with few anatropous ovules 
(Fig. 32). The mature fruit is an elongated cap- 


at the base. Figure 34 illustrates a minute epi- 
8ynous, pentamerous flower about 0.7 mm long 
with well-preserved stamens. It possibly repre- 
sents an immature stage of the flowers described 
above. The flowers show some features compa- 
rable to those of some modern plants of the Ro- 
sanae and Myrtanae, but a аан comparative 
Study has not yet been carri 
2. Monochlamydous flowers. ue Swedish 
material includes a few floral types that bear only 
one whorl of perianth parts. They are all epigy- 
nous with a one-loculed ovary, and one basal 
and orthotropous seed. They produced small tri- 
Porate pollen grains assignable to the Norma- 
polles complex. The flowers are probably “a 
related and belong to the same group. Ba 
the number of parts and floral symmetry, they 
are grouped into three different genera. The sim 
ple construction of the flowers and the structure 
of the pollen grains indicate pa these flowers 
were adapted to wind-pollina 
Dispersed pollen forms included in the Nor- 
Press complex (Pflug, 1953; Góczán et al., 
) Occur as significant ce of many Up- 
рег Cretaceous and Lower : еа palynofloras 
~. Europe and North Am Góczán et al., 
967; Eu 1981; Tschudy, 1981). Pome 
grains of the N 1 ndan 


JF 


FRIIS— ANGIOSPERM REPRODUCTIVE ORGANS 


411 


in the Upper Cretaceous fluviatile deposits of 
Sweden (Skarby, 1968), and anthers including 
Normapolles pollen have been recovered among 
the megafossil plants from Sweden. The fossil 
flowers from Sweden represent the first mega- 
fossil evidence of plants producing this strati- 
graphical important pollen group. 

Comparison with modern plant groups shows 
that the fossil flowers and fruits share characters 
with modern Juglandales (Juglandaceae and 
Rhoipteleaceae) and Myricales (Myricaceae). 
Man e generally include unisexual flow- 

, but exual flowers occur in Rhoiptelea 
о and Canacomyrica (Myrica- 
ceae). However, the fossils cannot with certainty 
be placed in any of these families, and it is thought 
that they represent an intermediate, perhaps an- 
cestral, group with bisexual flowers (Friis, 1983). 

2.1. Epigynous, pentamerous flowers with ra- 
dial flower symmetry. This organizational type 
is represented in the Swedish material by one 
species of Manningia Friis (1983) (Figs. 7, 37- 
39). The structure is known from several devel- 
opmental stages from small flowers to mature 
fruits. The flowers are bisexual and actino- 
morphic with an epigynous perianth composed 
of five free tepals in one whorl. The androecium 
is composed of five antitepalous stamens. No 
anthers in the preserved material are attached to 
the filaments of ihe flower, but fragments of por 
len sacs with p 
len grains have been found inside the perianth 
of many flowers (Fig. 39). The pollen grains all 
belong to the same type. They are peroblate and 
triangular, about 20 microns in equatorial di- 
ameter, with p tthe inner 
apertures and with elongated outer apertures. 
They are assignable to the Normapolles genus 
Trudopollis Pflug (1953). 

The ovary is inferior, one-loculed, and formed 
by three fused carpels. There is one thick style 
with three elongated stigmatic branches, The fruit 

2 2. - Epigynous, hexamerous flowers with ra- 
dial symmetry. One fossil species, Antiquocar- 
ya verruculosa dee (1983), «cuia this 
structural type has been recover ong the 
Swedish fossils posit 8, 43, 44). The iiia are 
bisexual and actinomorphic, with an epigynous 
perianth composed of six small, apparently re- 
duced tepals (Fig. 43). The androecium is hap- 
lostemonous with six antitepalous stamens. The 
stamens are represented only by remnants of fil- 
aments: anthers have not been o .Ina 


p  "Ҹ 


412 


single specimen, pollen grains referable to the 
Normapolles group have been observed attached 
to the surface of the styles. The ovary is epigyn- 
ous, one-loculed, and composed of three fused 

arpels. There are three very short styles, the 
stigmatic parts of which have not been preserved 
(Fig. 44). The fruit is a nut with one basal, or- 
thotropous seed. 

A very similar floral structure has been ob- 
served in the fossil flowers illustrated in Figures 
45 and 46, but these flowers are apparently na- 
ked. Traces of a perianth have not been observed 
in any of the specimens studied (more than 50), 
and it is believed that they represent a reduced 
(apochlamydous) form of the flower illustrated 
in Figures 43 and 44. The flowers bear remnants 
of six stamens at the top of the ovary (Fig. 46), 
but anthers have not been preserved. Pollen grains 
referable to the Normapolles group have also 

en found in these flowers, attached to the sur- 
face of the apical part. The ovary is one-loculed, 
formed by three carpels, and has one orthotro- 
pous and basal ovule. 

2.3. Epigynous, bimerous and bisymmetrical 
flowers. This floral type has been studied from 


horizons of the fluviatile sequence and so far 
several thousands of specimens have been found. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


The material includes three species apparently 
in one genus, Caryanthus Friis (1983). The flow- 
ers are bisexual and bisymmetrical with epigy- 
nous perianth insertion. The ovary is enclosed 
by two thick bracteoles and a small bract united 
with the base of the ovary. The perianth is epigy- 
nous with four tepals in two decussate pairs. The 
androecium is composed of six stamens. No an- 
thers have been observed attached to the fila- 
ments, but pollen grains of the Normapolles type 
have been found inside the perianth of many 
specimens (Fig. 40). The pollen grains are per- 
oblate, triangular, with protruding apertures. The 
outer apertures are elongated and there is a tri- 
radiate fold over the polar area. These grains are 
referable to the Normapolles genus Plicapollis. 
The ovary is inferior and one-loculed, form 

by two fused carpels. The carpels are apparently 
transverse. There are two styles or stigmatic 
branches and a single basal and orthotropous 
seed. The seed coat is thin and membraneous. 


DISCUSSION 


The examination of the plant megafossils from 
sen demonstrates the existence in the Upper 
Cretaceous of a great morphological diversifi- 
cation of the angiosperm reproductive structure. 
The fossil flowers studied are mainly actino- 


ии 


FiGURES 29-34. Fossil flowers from the dana! Cretaceous of Sweden. 29-30. He epigynows 
roecium (floral diagram see Fi ith 
mens if 4 preserved; PUE x75.—30. Section of flower dca pa 


flower with haplostemonous and 
petals (p), and stam 
M-203,, 


placenta with нет ovules; SEM. 197. x75. br Арсы view of newer showing petals 


-- 


. 6).—29. Flow a 


s (Р) 
and a); same specimen as Figure 31, x 85.—34. Small flower bud with stamens and style; SEM-198, * 180. 


fmit A 


FIGURES 35-40. Fossil fl 


erochlamy- 


dous, epigynous and tetramerous flower (fora diagram see Fig. 3).—35. Flower with se d 
— 36. Apical view d bora showing remnants of petals (p), Ер 0 А. (for 


preserved; SEM-214,, x45. 
(st); SEM-213,, x20. 37- 39. Manningia 


Upper Cretaceous of nigga ак ЈЕ ree (0) 


is 
agram see Fig. 8).—37. Flower bud with ie (t) and clusters of pollen preserved; SEM-176;, — 
Apical view M fruit with remnants of tepals 0 = stamens (f); SEM- 179,, x85.—39. Pollen тий © 
7 


Normapolle: wer Figure 37, x 40.06 
grains of e Мене type (Plicapollis) from са part of Caryanthus knoblochii; SEM- 1645, x 3,85 

Ficures 41-46. Fossil flowers and fruits from the Upper Cretaceous of Sweden. 41—42. Caryanthus на 
lochii Friis, monochlamydous, epigynous and bimerous flower (floral diagram see Fig. 7).— 41. Fruit : 
remnants of bracteoles (b), tepals (t), and stamens (f); SEM- 164,, x 55 cia Apical view of fruit ith us and 
of six rn: (f); SEM-165,, x70. 43-44. A tiquocarya ve; losa Frii onochlamydous, epigyno yens; 
hexamerous flower (floral diagram see Fig. 9).—43. Fruit with praet ови (t) and remnants О of s Figure 
SEM-212,, x55.— pical view of fruit showing position of perian stamens; same specimen as SEM- 
43, x 100. 45-46. Antiquocarya nuda, apochlamydous flower (5, 45. F from stamens (fj: 


with scars 
x 45.—46. Apical view of fruit showing position of stamens and тч styles; SEM-200,, х 45. 


O e a 


— ——X 


~ 


—— 


ia 


— 


и 
e 
< 
Q 
са 
о 
шщ 
= 
~ 
Q 
О 
са 
р 
m 
са 
2 
x 
| 
[э 
22 
z 
о 
e 
1 
2 
e 
ш 


Ж, 


2. 
ш 
а 
ра 
< 
о 
У 
< 
ы 
e 
< 
E 
О 
д 
a 
~ 
О 
Ф 
Д 
2 
шщ 
ш 
E 
Lu 
О 
3 
« 
Z 
Z 
< 


FRIIS— ANGIOSPERM REPRODUCTIVE ORGANS 


416 


morphic. One group of bisymmetrical flowers 
with a simple perianth represents, so far, the first 
occurrence of this type of floral symmetry. Ac- 
у to Dilcher (1979), all mid-Cretaceous 

floral structures found exhibit radial symmetry 
(actinomorphic). No zygomorphic or asymmet- 
rical fossil d yet. How- 
ever, evidence from fossil fruits and pollen may 
indicate that zygomorphic flowers developed 
during the Maastrichtian and early Tertiary (e.g., 
ep cue Chandler, 1961; Muller, c 


that flower 


in ge. Tertiary (e.g., Valerianaceae, spec tess 
Srodoniowa, 1979; Muller, 1981) 

The fossil flowers from Asen are all cyclic with 
a definite number of parts. Polymerous flowers 
with helically arranged parts generally consid- 
ered the ancestral type of the angiosperms (e.g., 
Dahlgren, 1983) have not been recognized. How- 
ever, the presence of small, stalked follicles with 
decurrent stigmas comparable to fruits of some 
modern Ranunculaceae may suggest that this 
flower type also existed in the Upper Cretaceous 
flora of Sweden. Records of an elongated fruiting 
axis with helically arranged follicles indicate that 
this flower type had developed in the late early 
Cretaceous (Dilcher, 1979; Vachrameev & Kras- 
silov, 1979). 

The majority of fossil flowers from Asen are 
epigynous, and th || ] 


pigy a single 
perigynous and a few hypogynous types. They 
differ in this respect from the mid-Cretaceous 
floral structures, which are generally hypogy- 
nous. However, the record of a fossil fruit with 
persistent calyx, Kalinaia decapetala Bayer 
(1914), from Czechoslovakia may indicate that 
epigynous flowers had evolved as early as the 
cnomanian. 
Th 


S2 s.a L1 3 


flowers with a well-developed disk indi ad- 
aptation to insect-pollination as well as simple 
constructed Meneses flowers apparent- 
ly adapted to wind-pollinatio 

Although there is no indication of unisexual 
flowers among the Upper Cretaceous fossils from 
Sweden, several mid- and Upper Cretaceous rec- 
ords of small flowers in spikes or heads referred 
to e.g., the Platanaceae and the Myricaceae (Ve- 
lenovsky, 1889; Velenovsky & Viniklár, 1926, 
1929; Krassilov, 1973, 1977; Dilcher, 1979) in- 
dicate that unisexual flowers developed early in 
the history of the angiosperms 

The present investigation has revealed a va- 
riety of floral types, which mainly represent the 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


subclasses Rosidae and Hamamelidae (sensu 
Takhtajan, 1980). The Dilleniidae is represented 
by a single flower type related to the Theaceae. 
This is consistent with the taxonomical results 
obtained from the study of the fossil pollen rec- 
ord (Muller, 1970, 1981). According to Muller 
(1981), the period Coniacian-Campanian (Mul- 
ler's floral phase IIIb) is characterized by a strong 
diversification of the Hamamelidae and to a less- 
er degree diversification of the Rosidae, and also 
by the appearance of the Dilleniidae. Thus, the 
fossil flowers studied probably reveal the major 
morphological diversification of the angiosperm 
flower reached by the mid-Senonian. 


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CASPARY, Einig e Planzenreste aus der de 
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1581 16 Einige pflanzliche АЫ und Ein- 


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est 


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E 

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—757. (tih 
& D. L. DILCHER. ihi Investigations iea: а 
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125. 


— — ics I 


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1980. Investigations of Tertiary жү rms: а 
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2 


119-149. 

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J. F. BASINGER. 1980. [Abstract:] Bisexual 
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—— &P.R. CRANE. 1984 [1985]. Archaeanthus: 

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f 


KRassiLov, V. A. 1973. Upper Cretaceous staminate 
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Miner, E. L. 1935. Paleobotanical examinations of 
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from Greenland. Amer. Midl. Naturalist 16: 595— 
MONTEILLET, ЈЕ os пеат 1981. a 
t ines du Cretacé s de sd 
Paki (Sénégal). Rev. iris و‎ Palynol. 34: 331- 
ора. evidence on early 


MULLER, a 
di iol. Rev. Biol. 
7-450 


Palacontoraphic, Abt. B, Paláophytol. 95: 


PRAKASH, V. 1956. On the structure and affinities of 
Sahnipushpam glandulosum Sp. nov о the 
Deccan Intertrappean series. Palaeobotanist 4: 91- 


ScHEMEL, M. P. 1950. Cretaceous plant microfossils 
from Iowa. Amer. J. Bot. 37: 750-754. 

SHUKLA, V. B. 1944. On Sahnianthus, a new genus 
of petrified flowers from the Intertrappean Beds 
at Mohganon Kalan in the and its relation 
with the fruit Enigmocarpon parijai Sahni from 
the same ee ани Natl. Acad. Sci. India, 
Sect. B, Biol. Sci. 1-39. 

1968. Exirariporopolenites ik 

per Cre f Scania 


Эти G. L. 1974. Flowering Plants—Evolution 
e the нар Ае el. Belknap Press of the 
Hervard U v. Pres: у 

STOPES, M C. "i К. FUN. 1911. Studies on the struc- 
t d affinities od Cretaceous plants. Philos. 
Trans., ag B, 201: 1-90. 

ТАКНТАЈАМ, A.J. 1980. Outline of the с 
of flowering plants oC Bot. 
(Lancaster) 46: 225-359 

TirrNEYv, В. Н. Dicotyledonc ous тн 
flower from the Upper Cre a. 
Vineyard, Mann ки: Нино re 265(5590): 136- 

———. 1984 [1985]. Seed size, dispersal syndromes 

€—— e angiosperms: evidence and hy- 

s. Ann. Missouri Bot. Gard. 71: 551—576. 
1981. Geographic distribution and 


produktivnyye M vetko 
zakhstana. Paleontol. Zurn. 1979: 121- 128. 


418 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


VANGEROW, E. Е. 1954. Меразрогеп und andere 
pflanzliche Mikrofossilien aus der Aachener 
Kreide. Palaeontographica, Abt. B, Paláophytol. 


96: 
ed " 1889. Kvétena Ceského Cenomanu. 
Abh. "ur Bóhm. Ges — Ser ъан 1-75. 
R ra cretacea bohe 
miae. Part + ae ee са елак Geol. D 
tavu. Rozpr. 1-54. 


1 Flora cretacea bohemiae. 
Part 2. Czechoslovakia Statniho Geol. Ustavu 
Rozpr. 1—51. 


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Part 3. Czechoslovakia Statniho Geol. nee 
Rozpr. 1-31 


31. Flora cretacea bohemiae. 
Part 4. Czechoslovakia Statniho Geol. Üstavu 
Rozpr. 1-11 
ZAKLINSKAYA, E. D. 1981. Phylogeny and classifi- 
cation of the Normapolles. Rev. Palaeobot. Pa- 
Iynol. 35: 139-147. 


SIGNIFICANCE OF FOSSIL POLLEN FOR 
ANGIOSPERM HISTORY! 


JAN MULLERT 


ABSTRACT 


^0 £ 


The significance of fossil кок evidence for 139 families for y history 


sed. Deficiencies in the fossil record and uncertainties in its interpretati ion 


e earliest lower 


versity. The succeeding progressive differentiation is clearly shown by the pollen as well as by the 


macrofossil record. The competitive replacement of an 
Strong differentiation takes place in the Maestrichtian and 
с categories were present by the end of the Cretaceous. Differentiation at lower 


was largely foiiis in the Turonian. 
most higher taxon 


cient gymnosperms and ferns by angiosperms 


g 
taxonomic levels continued in the Te ertiary. Some taxa are discussed more in detail and are shown to 


relat tively 


late and, in the monocotyledons, the woody palms are a кшш development. ‘In general, a positive 


correlation exists betw 


dvancement index and tim 


rst appearance. Some evidence for evo- 


na 
lution by gradual devon as well as by Ми сг арсы, is discussed. 


The significance of fossil pollen for the study 
of an angiosperm evolution is based primarily 
upon its abundance and its characteristic and 
diversified morphology. The first provides us with 
a а Май continuous, often independently dated 

biased 


and incomplete taxonomical record. 
Let us look at this bias first. It is evident that 


Preserved in the fossil record than others, and 
this depends mainly on quantity produced and 
distance between source area and place of sedi- 
mentation. Thus, a wind pollinated dominant in 
the coastal vegetation is more likely to leave a 
fossil pollen record than a rare, montane, insect 


M environment but that they must have 
» rae ps elsewhere and that the main features 
ка Ye pollen evolution only reflect adaptation 
anced pollination syndromes. 

indes : certain extent this is true and tends to 
"es s y first date that is too young, unless the 
E: т ence indicates that the transition from 
al n type has taken place in or close to 
Sa of sedimentation, as in Juglandaceae or 

nneratiaceae. Pollen evolution itself is only 
Partly related to pollination, however. Recent 


c‏ س 


the statistical evaluation of the relation between 


ANN. MISSOURI Bor. GARD. 71: 419-443. 1984. 


' The author is much indebted to M. Zandee quogde gud for Theoretical Biology, U 


studies by Heslop-Harrison (1976), Muller 
(1979), Payne (1981), Bolick (1981), and Hesse 
(1981) have indicated a large diversity of func- 
tions for the exine, such as adaptations to har- 
momegathy 
of lipids, which have been linked, next to pol- 
lination, to the extreme diversity of present-day 
exine structure in angiosperms. It was already 
apparent from the first investigations of the fossil 
pollen record that the evolution from simple to 
complex types in response to these factors can 
be traced in surprising detail. In fact, a close 
analysis of the morphology of fossil types in com- 
parison with form and function in recent equiv- 
alents will allow us to detect the evolution of 
many adaptations in the reproductive sphere. 
To demonstrate how far function may deter- 
mine the morphology of the exine, two series of 
photomicrographs of Recent pollen types, with 
contrasting morphology are presented. First, al- 
der pollen (Fig. la, b) is relatively small, dry, 
thin walled, with 4 or 5 small pores and an in- 
tragranular exine structure. Here the main har- 
momegathic movements are being absorbed by 
the ridge-enclosed flexible wall, which is quite 
typical of anemophilous pollen in general. Next, 
Cobaea (Fig. 1c-f) has a large, periporate pollen 
grain obviously adapted to insect pollination. It 
has a thick, rigid wall, in which stress is absor 
all over equally, resulting in a spherical shape. 


niversity of Leiden) for 


ancement index. Requests for ^em should be 


a 
to the Director, Rijksherbarium, ey 6, 23 13 ZT Leiden, The а 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Betulaceae), ps exine ginis —a. Expanded, upon 


FIGURE l. a-b. Alnus Anis pollen dry 
from anther, x 2,500.— b. Contracted after tw о days е е to sunny a mosphere, causing the arcua 
enings to stand out asa rigid KE supporting the ай 


rawn, thin, poss flexible exine. The aperture 


— 


1984] 


The beautiful open structure of the exine is, in 
the living state, covered with oil, making the 
grain both sticky and insulated against water loss. 
It may have evolved both in response to stress 
accommodation and oil retention. These ex- 
amples show that many structures of fossil pollen 
grains can be interpreted better if comparable 
Recent pollen types are studied more in detail 
with regard to their functioning. 

However, there is also a non-functional (no- 
mothetical) element in pollen morphology that 
arises as a consequence of limitations and rep- 
etitions in design due to certain mathematical 
plus physical restraining factors during devel- 
opment (Muller, 1980; Melville, 1981). Such 
characters are, in their evolution, more indepen- 
dent of biological functioning, and thus are prob- 
ably more useful for recognition of taxa and their 
phylogenetic relationships, as first shown by Van 
Campo (1967) in her study of the successiform 
series. 

Although taxonomic identification will rely on 


conse- 
auenti« а Е 
ччепцу 5 


is especially serious if pollen specialization lagged 
behind the evolution of other characters due to 


leaf, fruit, or seed characters. This, however, can 
rarely be proven in the fossil record, although 
Most of the cases in which a discrepancy in time 
of first occurrence has been found between mac- 
ro- and microrecords are probably due to this 
Phenomenon. It may be significant that in the 
few fossil flowers found with pollen, some showed 
а combination of characters not known in the 
Recent relatives. 

The most clear-cut case is perhaps Burretia 


(1961). The fi 


MULLER — FOSSIL POLLEN 


421 


gopsis from the lower Oligocene of the United 
States (Wolfe, 1973), Quercus type pollen is found 
in betulaceous staminate inflorescences, associ- 
ated with fagaceous leaves. Tiffney (1977) has 
found a flower in the upper Cretaceous that con- 
tains tricolpate pollen but has a combination of 
characters that cannot be matched in the living 
angiosperm flora. From the mid-Cretaceous, 
Dilcher (1979) has reported monocolpate-retic- 
ulate pollen from catkins ofan amentiferous type, 
a most unusual association, almost suggesting 
that the older the fossil, the more unusual the 
combination. Some of these fossils undoubtedly 
belong to extinct taxa, which may or may not 
have given rise to lineages leading to Recent ones. 

In general, it may be stated that the degree of 
precision in identification decreases in propor- 
tion to the age of the fossils. This is not to be 
confused with the chance for an erroneous iden- 
tification, but rather that the circle of possible 
affinity increases. Thus, although in the Tertiary 
generic identification is often possible, in the 

retaceous we may only be sure of affinity at the 
family or even higher taxonomic level. 

In the following discussion all these potential 
sources of error have been taken into account as 
far as possible. It proceeds, in general, on the 
assumption that with a large, statistically signif- 
icant of identificati taxon, at least 
some estimate oftime of origin and development 
is possible. Whereas in 1970 (Muller) only 74 
families with 135 pollen types could be identified 
based on fossil pollen, in 1981 (Muller) 139 fam- 
ilies with a total number of 332 pollen types 
could be identified. The present account will deal 
principally with the general results of this last 
compilation, with the addition of some impor- 


for a final interpretation, and it is hoped that 
critical lists for leaf, seed, fruit, and wood re- 
mains will become available in the near future. 

Some remarks on nomenclature and classifi- 


C, 


WIU 


from the Miocene of Europe, described by Mai 
the subfamily Brownlowioideae of Tiliacea , 
whereas the pollen is of the Tilia type, restricted 
at present to the subfamily Tilioideae. In Fa- 


cation of g I | а 
because this will have to reflect the degree of 
precision of the identification. Apart from those 
rare cases in which a fossil pollen grain can be 


— Re а њи 


— 


tected against collapse by the annular thickenings, х 2,500. c-f. Cobaea scandens pollen 
col )-—с. Fresh, covered with a sticky, oily deposit (“*pollenkitt”), x 
umellate structure, supporting the inner wall in whic 


(Polemonia- 
500.—d-f. Acetolyzed, showing the open, 
regularly distributed circular pores are located at the 


bottom of the smaller lumina. d, x 500; e, x 1,500; f, х 4,000. Line equals 10 um. 


422 


identified with a living species, it should be placed 
as a form species in either a Recent genus, a form 
genus, a Recent family, or a higher taxonomic 
category. In the case of extinct groups of pollen, 
the higher taxonomic category must be circum- 
scribed exclusively on the fossil evidence but 
should be related to the general classification even 
if only by stating that they are angiospermous. 
Thus, the group of Normapolles should have at 
least ordinal rank and can be placed in Hama- 
melidanae; the genus Aquilapollenites plus as- 
sociated genera could form an extinct monotypic 
family within Santalales. Tricolpites micromu- 
nus from the lower Cretaceous can be identified 
with Magnoliopsida B-G, for which, unfortu- 
nately, no taxonomic name exists, and Wode- 
houseia is an extinct incertae sedis genus in the 
Angiospermae. At the other end of the scale Flor- 
schuetzia trilobata could represent an extinct ge- 
nus linking Lythraceae and Sonneratiaceae. 

This approach is based on the very sensible 
recommendations made by Schopf (1969) and 
allows us to integrate both fossil and Recent an- 
giosperms in one system of knowledge. This ap- 
proach certainly allows incorporation of correc- 
tions when new evidence comes to light and 
avoids the reproach made against many leaf 
identifications with Recent genera with its atten- 
dant dangers [see Wolfe (1973) and Hughes (1976) 
for a pertinent critique of this habit]. 

Of course, neutral names are preferred for fos- 
sil pollen types, and names like Nothofagidites, 
or Santalumidites should be avoided at all cost, 
since they, more than anything else, suggest too 
strongly what can only be tentative suggestions 
of affinity. 


ORIGIN AND EARLY DEVELOPMENT 
(BARREMIAN-ALBIAN) 


Because at this symposium the pollen floras 
from this period are dealt with in detail by other 
contributors, and because my approach of trac- 
ing Recent pollen types backward in time vir- 
tually deni : ant з O O : 


ly emphasized by Stebbins (1950) and Hughes 
(1976), of recognizing the vital link between 
gymnosperms and angiosperms, I must restrict 
myself to a few remarks only about the earliest 
phase of angiosperm evolution. 

In 1975, Doyle et al. presented their well known 
scheme that could form a basis for separating 
fossil gymnospermous from angiospermous ex- 
ines. However, the discovery by Cornet (1980, 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


1981), of pollen grains with col latet 
from the Triassic, which are unfortunately not 
yet described in detail, casts doubt on the validity 
of at least one criterion leaving only that of the 
laminated endexine, which is very hard to test 
in fossil material. 

At least three different functions have been 
proposed for the columellate exine, so beautifully 
developed in Cobaea pollen (Fig. lc—f). These are: 
to hold pollenkitt and lipid material in connec- 
tion with entomophily and for sealing purposes; 
to store recognition substances for stigmatic ger- 
mination; and to give structural support in con- 
nection with harmomegathy. It will therefore be 
difficult to determine the ecologic significance of 
the columellate structure for Cornet's Triassic 
grains. All known living entomophilous gym- 
nosperms have sticky pollen grains but lack col- 
umellate or even alveolate exines, according t0 
Frederiksen (1980). However, Hesse ( 1980) has 
recently commented on the lack of pollenkitt m 
many gymnosperms. In angiosperms pollenkitt 
deposited on the tectum surface renders the pol- 
len sticky, but if it is deposited in the tectum 
cavities the pollen becomes powdery (Hesse, 
1980). This is contrary to prevailing opinion that 
the reticulate-columellate exines invariably 12" 
dicate stickiness and hence entomophily. In this 
connection it is of interest that Klaus (1979) has 


found evidence for relicts of columellate struc : 


ture in Pinus. The columellate structure of Clas- 
sopollis is also well known, suggesting that the 
difference may not be fundamental. 

If the Triassic columellate grains have bee 


produced by ancestral angiosperms, then this | 


structure may have been lost, probab 


ith the 
the gr with 


iness adaptations. type 
The first recognizable angiosperm atts 

is Clavatipollenites, starting in the 1977), 
hanks to detailed studies by Doyle et al. s alket 

Hughes et al. (1979), and Walker and Wa" 


ly because | 


$ 
1 


i 


| 
| 


: ace | 
1 it is cl that different types | 
(1980), it is clear pi » 


volved. At least one form, C. nes rid 
to be closely similar to Recent Asca of 
in fact be traced to the Recent aet 


and can 
distribution (Muller, 1981, fig. 1). Thi 
and hence 


ову: iot " 
probably also a similar pollination bio 


is pattem | 


| 


— 


1984] 


Recent Chloranthaceae, e.g., in Hedyosmum, 
large amounts of pollen are produced and it seems 
likely that the Clavatipollenites-Ascarina lineage 
may have been adapted to an unspecialized pol- 
lination both by wind and indiscriminate insect 
visitors. According to Dilcher (1979) this may 
represent a basic and primitive strategy in an- 
giosperms. True anemophily with dry, powdery 
pollen would be a secondary specialization from 
this initially indiscriminate system and may, ac- 
cording to Dilcher (1979), already have existed 

course е ts regarding the oth- 
er characters of the plants producing these early 
Ascarina-like pollen types; but that they be- 
longed to the ancestral complex of Chlorantha- 
ceae, or if one would add some more caution, of 
Laurales appears highly probable. 

Other grains belonging to the Clavatipollenites 
complex may be ancestral to Myristicaceae, ac- 
cording to Walker and Walker (1980), but these 
have not yet been traced to younger occurrences. 

Recently, however, a significant discovery has 
been made by Walker et al. (1983), who de- 
scribed undoubted Winteraceae pollen tetrads 
from the late Aptian/early Albian of Israel. This 
takes the record for this family back another 35 
Ma compared to the late Cretaceous record list- 
ed in Muller (1981), indicating that taxonomi- 
cally not closely related members of the Mag- 


niracc 


€ second main angiospermous pollen type 
lo appear is the tricolpate reticulate type in the 
Aptian. Like Clavatipollenites, it is small and 
Similar in the columellate exine structure but has 
three equatorial colpi. It is more likely that this 
change in apertures is related to improved har- 
momegathic efficiency and pollen/stigma inter- 
action rather than to a change in pollination. The 
small size of the pollen would indicate small 
lowers (Muller, 1979; Dilcher, 1979: 323), or 
anemophily (Crepet, 1981). 

In Contrast to the Ascarina type, this group of 
tricolpate grains can be identified only as having 
been derived from non-magnoliid dicotyledons. 
Today, it occurs in Ranunculidae (Menisper- 
maceae Predominantly, but also in Berberida- 
“eae, Papaveraceae, and Fumariaceae), lower 
Hamamelididae (Trochodendraceae, Tetracen- 

«ceae, Hamamelidaceae, and PI ), and 
Dilleniidae (some Dilleniaceae, some Salicaceae, 


MULLER — FOSSIL POLLEN 


423 


Brassicaceae). It appears to be rarer in Rosidae 
(some Oxalidaceae and Olacaceae) and very ex- 
ceptionally is found in Asteridae (some Verbe- 
naceae and Lamiaceae). 

Thus the probability that the earliest Creta- 
ceous tricolpate grains represent ancestral Ra- 
nunculidae and Hamamelidae appears higher 
than that they indicate the presence of early Dil- 
leniidae or Rosidae. 

The retention of this basic pollen type in so 
many Recent genera of diverse affinity is another 
striking example of “stasis” in pollen evolution 
and presumably also in pollination biology. 

Rather soon after the first appearance of the 
tricolpate type, endoapertures developed in the 
Albian. The resulting tricolporate-reticulate pol- 

t t fi tad ds 


len typ p g p 
cialization both in harmomegathic structure and 
increased efficiency of pollen/stigma interaction 
because of the presumed development of spe- 
cialized intine structures. As stressed by Wolfe 
et al. (1975), this change has probably occurred 
independently in several lineages of the ancestral 
tricolpate complex. Menispermaceae, Flacour- 
tiaceae, and Dilleniaceae have retained the tran- 
sitional stages, the former having advanced less 
than the latter two families. In Rosidae, however, 
tricolporate-reticulate types have become dom- 
inant today. Thus, identification of these early 
tricolporate types is possible only in a very gen- 
eral way and probably indicates the presence of 
ancestral Dilleniidae and especially Rosidae. 

The third main early angiosperm pollen type 
is the monocotyledonous one, recognized al- 
ready by Doyle in 1973 from the Aptian. Func- 
tionally it is similar to the C/avatipollenites group 
of types. 

Several other monocolpate types with a pe- 
culiar exine structure, such as Stellatopollis with 
a crotonoid pattern, or types found by Hughes 
et al. (1979) ith a lip Н id p tt ‚ might 
also be monocotyledonous but disappear from 
the record soon afterwards. 

A fourth main category is the periporate group 
from the Albian, identification of which is also 
very uncertain at present. This group is probably 
not related to Caryophyllidae and shows more 
similarity to Alisma (Alismataceae) and Tri- 
menia (Monimiaceae), but has not yet been con- 
nected with younger types. 

Thus, in the Barremian-Albian early phase of 


structure, make their appearance, roughly cor- 


424 


SOUTH AMERICA 


MDH ЕН 


9 25%0 2% 0 


INDIA 


Гана Ена. 


то 25% o 


г. АЁ 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


AUSTRALIA 


[Y 


E= elaterbearing spores F-Ferns С = Gymnosperms A-Angiosperms 
(Galeacornea group) 
+ fonnrec 
Microfloral di % sp position for four major categ Ї 


and pollen. Floral phases based on Muller (1981). 


responding with increases in leaf diversity and 
abundance as Doyle (1977) and Doyle and Hick- 
ey (1976) have pointed out. This would appear 
to invalidate Axelrod’s (1970) claim that fossil 
pollen does not register early angiosperm diver- 
sity. But, if, as Stebbins (1974) contends, angio- 
sperm origin took place in a semi-arid dry land 
environment, admittedly palynology would only 


onstrated by plate tectonics, widely separated а! 
that time. In Australia especially, the delayed 
entrance of angiosperms, possibly due to a cooler 
climate, is clear (Dettmann, 1981). 
In the Cenomanian, the main new develop- 
ment in pollen evolution is the appearance 


triporate types. This has probably taken pla 
= ы 4 ју ina li fi F 


rarely detect traces of it, although the abundance 
of very early angiospermous pollen types in the 
ancient, probably semi-arid rift valley sediments 
of Gabon could support Stebbins’ views, as al- 
ready pointed out by Doyle (1977, 1978). 


tricolporate ty 
via a flattening of the triangular shape and 2 
shortening of the colpi to early Normapolles 
first described by Doyle (1969) from the Сепо- 
manian of the gulf coast of the United State 2 
in the Turonian in a separate lineage leading 


States and 


ich the 
early triporate celtoid pollen types of which 


INCREASE IN ABUNDANCE 
(CENOMANIAN-TURONIAN) 


1 


derivation and place of origin are not yet и 
(Muller, 1968). The Normapolles group > | 
shown to have probably given rise to J ке 
ceous types, and the celtoid types have beco 
fairly early established as Urticales. In 
ancestral t 


both cases. 
mrect have 


been present. 


> · 1 Ly 
ALLAIL 
Vy pv» LU IMBULI ILI 


It is mainly in the Turonian that the ; 
crease in pollen morphological divers! 
comes obvious and that modern types Са 
denly appear, like that of Ilex (Celastranac 
yrtanae). Such sudden ap 


suggest immigration into an environm 
which they are more likely to be preserv 
the place of their actual origin. 

By the end of the Turonian 
breakthrough of the angiosperms ар 
to have been completed, but the іаха 
were, in most cases, different from Recen 
as is becoming also more and more сеа 1981) 
the study of macrofossil records. Tiffney 


real in- 
ty be 


and 


ent if 


the ecological 
pears 


present 
t ones, 


е 


| 


| 
| 


| 


ай 


1984] 


1. 4 Е | 


that this i is aresult of com- 


petitive pressure by increasingly efficient angio- 
and ога 11131] Aditi 


has pointed out that many of the more archaic 
gymnosperms became extinct worldwide at the 
same time. The fossil pollen evidence is well in 
accordance with this view. 


MAESTRICHTIAN EVENTS 


In the Maestrichtian, an accelerated develop- 
ment of modern pollen types appears to have 
taken place indicating increased differentiation 
at the level of families, orders, and superorders 
(Muller, 1981, fig. 3). In view of the relative short 
duration of this period and also because this de- 
velopment clearly antedates the catastrophic 
events at the Cretaceous-Tertiary boundary, a 
special explanation appears necessary. Whether 
the phenomenon is due to a solar radiation max- 
imum as postulated by Hughes (1976) ог to co- 
evolution with insects and dispersal agents, the 
development of chemical defenses, or any other 
factor, is difficult to decide without further de- 
tailed study, although selective pressure on pol- 
len evolution undoubtedly has become high. 

The Maestrichtian is also the last period in 
which, locally, extinct groups of plants, such as 
those that produced the Normapolles types or 
Aquilapollenites were dominant. In the Austra- 

l- ctic region, in contrast, no comparable 
extinction has occurred and the flora developed 
early into a vegetation type that largely still sur- 
vives today (Proteaceae, Nothofagus). 

It is clear that differentiation at ordinal and 
Superordina] level decreases in the succeeding 
Tertiary, but that at the family level much dif- 
ferentiation still took place, as was also empha- 
sized by Tiffney (1981) for the Paleocene/Eocene 
and Eocene/Oligocene transitions. 

ог the ordinal level, this is shown in Figure 
as à cumulative curve in which we can distin- 
guish àn initial slow rate, then a fast, tachytelic 
* ase in the upper Senonian, followed by a slow 

Ut Steady increase in the Tertiary. 


DiscussioN or SELECTED TAXA 


r We can apply this method of analysis to the 
0551 pollen data, as well as to more restricted 
ахопотіс groups among the angiosperms. This 
“specially illuminating if abundant and well- 
€d pollen records exist that inspire con- 
fidence that they reflect taxonomic diversifica- 


MULLER—FOSSIL POLLEN 


425 


tion sufficiently closely. But I must emphasize 
once more that the primary data, as summarized 
on the preceding and following diagrams, and 
discussed more in detail in Muller (198 1a), di- 
rectly reflect only pollen evolution, indirectly re- 
flect adaptive trends in the reproductive sphere, 
and have mostly no relation to what happened 
in the rest of the plant body. This emphasizes 
once more the importance of studying the fossil 
pollen record, taking into account Recent evi- 
dence on form and function, and then integrating 
such information with macrofossil evidence. 

If this is attempted, one can agree with Doyle 
(1978), Niklas et al. (1980), and Tiffney (1981) 
that neither the prejudice of Hughes (1976) against 
the evidence from Recent plants, nor the opinion 
of Heywood (1977) and Stebbins (1974) that fos- 
sil evidence is insignificant for an understanding 
of angiosperm evolution, will appear justified. 

The evidence will be summarized on charts 


of fossil pollen types. On these charts more em- 
phasis is laid on the general evolutionary pattern 
within the group than on first occurrence only, 
which almost never coincides with origin due to 
the inherent deficiencies of the fossil record, even 
for such ubiquitous organs as pollen grains. 


HAMAMELIDIDAE 


Figure 4, as in the following, Takhtajan's 
1969) taxonomic concepts are followed, but it 
is realized that inclusion of Didymelaceae is de- 
batable (Kóhler, 1980) and that Dahlgren (1980) 
and Thorne (1976) have quite different concepts 
for this group. 

The pollen types indicated are often abundant 
in the fossil assemblages due, of course, to the 
predominance of wind-pollination in many of 
the taxa included. Also, most of the pollen types 
are remarkably stable since their first appear- 
ance, no doubt because of the uniform, conser- 
vative anemophilic environment (cf. Crepet, 
1979; Dilcher, 1979). Alnus pollen (Fig. la, b) is 
a typical representative of this group, which ap- 


4 


I 
AJULIOI WILD 


ш Anemophily тау be responsible also for 
the frequent occurrence of an infragranulate ex- 
ine structure. 

However, it is clear that the tricolpate-retic- 
ulate members of the group shown, especially 
those commonly referred to as lower Hamame- 
lididae, are underrepresented. As mentioned be- 
fore, their ancestors could be present as early as 


426 


ercidiphyllales 
ph 
p 
es 
њено даје. 
asuarinales 


yrtales 
lliciales 
11a1 
1 
abales 
eraniales 
antalales 
teal 
recales 
idymelales 
ucommiales 


age in million years 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


= 
LI 
a 
= 
ч 
a 
^ 
а 
z 


olygalales 
ornales 
ti 1 
oale 
hal 
ур! 
р 
1 1a1 
ipsacales 
р 
crophulariales 
vperales 
upteleales 
ifragales 
ag 
iolales 
itat 
Salicales 
Arales 


Pleistocene 25 
Pliocene 5 
upper Miocene 

Кез сс И 


middle Miocene. 


lower Miocene 
22,5 


Oligocene 

39 

upper Eocene 

а е LI 

middle Eocene 
50 


lower Eocene 
55 


маи 
Maestrichtian 
у у | = 


Campanian 
77 


Santonian 
84 


Coniacian — ,, / 


Turonian 


Cenomanian 
100 


FiGURE 3. Pollen records for angiosperm orders. 


the lower Cretaceous, and they may have been 
adapted to entomophily, since in Recent repre- 
sentatives like Hamamelis the reticulum is cov- 
ered by a large amount of extremely sticky “‘pol- 
lenkitt" (Hesse, 1981). 

The problem in the pollen morphological evo- 
lution of this group is in the transition from the 
tricolpate to the triporate “amentiferous” type. 
As already mentioned, Doyle (1969) and Wolfe 
et al. (1975) have suggested that the Normapolles 
could be transitional, but this is probable only 
for Betulales, Juglandales, Myricales, and Casu- 
arinales, not for Fagales. Urticales also may have 
had a different origin as mentioned before. 

Walker and Doyle (1975) and Wolfe et al. 


eri ti Ue PA en alia a eM lile it Ae a kc 


bts whether the | 
(1975) have also expressed dou diss ulate 


tricolporate, subspherical, colume e 
pollen of the lower Hamamelididae hs p. | 
: : : -oblate, 1n | 
given rise to a triangular ob аю, oro НЫ | 
р F : rate | 
via Normapolles. It is clear that the er | 
condition, which according to Doyle ( has been | 
preceded Normapolles development, Hamame | 
preserved in few present-day higher Casta | 
lididae, notably in some Еарасеае ( | 
Lithocarpus). 

However, Endress (1977) has and | 
connection between Hamamelidales, nfo | 
Betulales and of these, only Berle ы type: 
to the above porate amentiferous PO С 


41.1 
эши 


argued fora clos | 


1984] 


Ulmaceae 

Fagaceae 
Myricaceae 
Cercidiphyllaceae 
Juglandaceae 


Celtis t. 
Nothofagus 
Myrica 
Cercidiphyllum t. 
Castanea t. 

Ulmus t. 

Corylus 


MULLER—FOSSIL POLLEN 


Juglandaceae 


427 


Eupteleaceae 
Fagaceae 
Hamamelidaceae 
Hamamelidaceae 
Moraceae 


Hamamelidaceae 
Moraceae 


Didymelaceae 


Carya 


» | age in million years 


Pleistocene 2,5 
Pliocene С 


li 
upper Miocene | 
11 
middle Miocene i 


lower Miocene r 


39 

upper Eocene 
44 

middle Eocene | 
50 


lower Eocene f 
55 


Paleocene - 


65 


Maestrichtian | 
69 


Campanian Г 


Santonian F. 
84 


Coniacian eus 


Turonian F 
BEER CO deer] 
Cenomanian 

100 


Albian F 


FiGURE 4. Pollen records for Hamamelididae. 


Fagales, in fact, have a basically colpate-subpro- 
late type but generally without the reticulate tec- 
tum that is so typical for lower Hamamelididae. 
The loss of the reticulum may be the most direct 
expression of the change towards anemophily. 
Within the Fagales, Nothofagus has a highly spe- 
Cialized, and deviating pollen type. It is thus un- 


— Cecropia t. 


Hamamelididae 


"МР Bs 


like ly that Е Fagal t Кот ate 
reticulate type он а Normapolles кын to 
the Recent types. Rather, a Castanea pollen type 
may be placed at the base. Some of the genera 
that produce this pollen type, such as Lithocar- 

us and Castanopsis, have retained some ento- 
mophilous characters, and the pollen type that 


428 


retains traces of columellar-reticulate structure 
at the poles is remarkably similar to certain mid- 
Cretaceous types. 

Therefore, it is of great interest that Wolfe et 
al. Pe 5) claim, on the basis of foliar morphol- 
ogy, mat Juglandales are allied to Rosidae, in 
whi ch 


in which 
anémephily i is rare. Because the closest connec- 
tion between Normapolles and a Recent taxon 
is with Juglandales and not with Fagales (Skarby, 
1968; Wolfe, 1973; Nichols, 1973), the idea that 
the Normapolles-Juglandales lineage is inter- 
mediate between the Fagales/Betulales/Myri- 
cales/Casuarinales on one hand and the Rosidae 
on the other may seem attractive. It would imply 
a lower Cretaceous differentiation before the ap- 
pearance of the first Rosidae and Hamamelidi- 
dae from the Turonian, and probably even before 
the first appearance of Normapolles in the Cen- 
omanian. A similar view has recently been ex- 
pressed by Cronquist (1981). 

As already stated, it is considered unlikely that 
Urticales have developed from Normapolles in 
view of the early record of Celtis type pollen, 
although Walker and Doyle (1975) judge Planera 
(Ulmaceae) to have colporate pollen and stress 
the presence of arci both in Normapolles and 
Ulmaceae. It is likely that further study of the 
fossil pollen record and especially of transitions 
between types will provide important new evi- 
dence to help solve these questions. In this con- 
nection Zavada and Crepet's (1981) description 
of middle Eocene celtidoid flowers and pollen, 
which suggest a transitional stage between insect 
and wind pollination, are significant. 

Regarding macrofossil evidence, there is broad 
agreement in the timing ofthe early development 
of at least some major groups. Rüffle (1980) raised 
the possibility that certain leaf remains from the 
lower Cretaceous could be referred to Hama- 
melidales (cf. also Doyle & Hickey, 1976; Hickey 
& Doyle, 1977), whereas the well known records 
of Platanus-like leaves from the Cenomanian on- 
wards could be said to agree with the regular 
occurrence of tricolpate-reticulate type pollen in 
this period. 

Fagaceae appear to have roots in the ceno- 
manian, although in general Cretaceous repre- 
sentatives had leaves that deviated considerably 
from the Tertiary ones; whereas, by the middle 
Eocene, the family appears to have diversified 
strongly (Crepet, 1979). Betula leaves from the 
Santonian and betulaceous wood from the Cam- 
panian agree remarkably well with the earliest 
pollen records, which are from the lower Seno- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


nian (Cronquist, 1981; Riiffle & Knappe, 1977). 
For both Juglandaceae and Ulmaceae, the ear- 
liest upper Cretaceous pollen records antedate 
macrofossil finds, which are known only from 
the Eocene onwards. 

Wolfe (1973) stated that forms showing the 
specialization of modern amentiferous families 
and orders do not become differentiated until 
near the end of the late Cretaceous, when pollen 
morphological differentiation is very pro- 
nounced also. 


MALVANAE 


Within the Dilleniidae, the Malvanae form à 
fairly well defined taxon, with very morpholog- 
ically diverse pollen, but with sufficient transi- 
tional types to confirm the coherence, and 10 
anticipate phylogenetic junctions, in the fossil 
record. Anemophily is rare in this group and 
much of the pollen diversity may have a struc 
tural basis or may reflect co-evolution with pol- 
linators, which are known to range from insects 
to birds and bats. It thus forms a striking contrast 
with the preceding group 

The timing and mode of development of the 
pollen record as shown in Figure 5 differ rather 
strikingly from the previous group. ereas 
Hamamelididae are already recorded by pollen 
as early as the Turonian and even earlier as тас" 
rofossils, can, on pollen, be traced only 
to the Campanian and the main development is 
Tertiary. It is obvious that the cumulative curve 
is pigs straight, and that all orders in- 
show a similar pattern. This in 
мыкча Б change in pollen 


at a steady rate, and suggests the action of nots 


МАЛ м1 


force of the wind his been lacking here, j 


can- 
mains wurde c pum of uncharacteristi 
e: 

es and 


that could be considered an 
sil pollen record of а is clearly bi di 
towards the more specializ : 
Bombacaceae has Wolfe et al. (1975) found e 
dence for a relatively unspecialized {УР types 
which the highly жашларыны Tertiary 

can be derived 


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MULLER — FOSSIL POLLEN 


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Pleistocene 2,5 


Pliocene 
upper Miocene 


а MI 
middle Miocene 


lower Miocene 


bs 39 
upper Eocene 
онаа. 
middle Eocene | 
а ^] 


lower Eocene | 
Ја | 


Skee | 
Maestrichtian | 
H69] 


Campanian 
| = 2 À 
Santonian 
Se | 
Coniacian - 
reete cli 
Turonian 
ااا‎ — — 9$ 
Cenomanian 
a 
Albian 


ВАН 109 
Aptian 
114 


FIGURE 5. Pollen records (ог Malvanae. 


The macrofossil record for Sterculiaceae starts 
than th ^l E Ес а 


a leaves from the Cretaceous. Macrofossils of 

eae, Malvaceae, Bombacaceae, and Eu- 
Tos ае, however, start appearing only in the 
n in line with the microfossil evidence. 
a as a whole the macrofossil record appears 

Synchronous with the microfossil record, 
confirming that the pollen data as summarized 


| 


| Malvales 
Euphorbiales 


Thymelaeales 


Malvanae 


in Figure 5 do reflect the general evolutionary 
radiation of Malvanae. 


ASTERIDAE 


ecard far Acteridae 


om q 


a ‘ann which is more or less equivalent to the 
"tubiflorae" of an older generation of angio- 
sperm systems, such as Wettstein's. The pollen 


430 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


FIGURE 6. Pollen records for Asteridae. 


morphological evolution in this group starts 
slowly in the Paleogene, accelerates markedly in 
the Neogene, and is probably continuing today. 
This clearly reflects active evolution in the re- 
productive sphere, and there seems to be little 
doubt that it indicates a process of co-evolution 
with long-tongued insects, although pollen/stig- 
ma Cy, and har- 
momegathy may г also have been i important. Es- 
pecially in Asteraceae, the latter factor may have 
been dominant (Bolick, 1). 

There appears to be some difference in timing 
of main development, with Dipsacales, Gentia- 


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29 50 о 
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eoo 
е 
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lower Miocene 
22,5 | 
Oligocene 
39 
upper Eocene | 
44 | 
middle Eocene 
50 
8 1 
! 
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| 
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| Dipsacales Scrophulariale 
Paleocene | ipsac 
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Campanian " о 
17 і о 
t о 
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i 2? Campanulales 
ee | Polemoniales о mp 
је 
Coniacian — ,, 
Turonian 
Lau NTE 
Cenomanian 
100 


Asteridae ("Tubiflorae") 


nales, and Polemoniales appearing ear ie 
Scrophulariales, Lamiales, and Campan i 
Macrofossil evidence partly supports the Gp 
ing suggested by the pollen record, although * 
rifoliaceae and Apocynaceae are known 
Cretaceous already. | 
е presence of Gentianaceae in the emn 
has recently been documented by hec ower 
Daghlian (1981) based on funnel shaped | 
remains containing рите у are 
pollen, which is comparable not | 
cent genus Macrocarpaea. = idi j 
quoted in Muller (1981). Caprifoliaceae pe 


1984] 


abundant in the Tertiary, Boraginaceae are known 
from the E , Rubi in the Eocene, 
and Bignoniaceae are first recorded from the Oli- 
gocene. The macrofossil record of Asteraceae is 
very limited and appears restricted also to the 
Tertiary. 

The earlier appearance in the macrofossil rec- 
ord of Caprifoliaceae and Apocynaceae agrees 
with the difference in the microfossil record but 
is out of phase. This again may indicate mosaic 
evolution, leaf cl developing earlier than 
pollen characters, because they are obviously not 
likely to have been influenced by evolving pol- 
linators, whereas flower evolution in the Aster- 
idae probably started more or less simultaneous- 
ly with insect evolution. According to Crepet 
(1979), entomophily was already well developed 
in the middle Eocene, and fossil flower types 
from this period indicate the presence of four 
orders of anthophilous insects, whereas the gen- 
tianaceous flower from the Paleocene indicates 
un Ta bee pollination (Crepet & Daghlian, 


The three cumulative curves from the groups 
discussed before are shown together in Figure 7 
for easy comparison. The significance of the pol- 


еп data here is that they suggest differences in - 


timing of evolutionary development in those 
character complexes related to the reproductive 
sphere and, in a more general and indirect way, 
differences in taxonomic diversification. For Ha- 
mamelididae, a fast, tachytelic phase in the upper 
Cretaceous is followed by a bradytelic one char- 
acterized by slow diversificati Mal show 
4 constant rate of diversification, but an early 
tachytelic phase may have gone undetected in 
he pollen record. The curve for Asteridae sug- 
&6sts that this group is still essentially in а tachy- 
ise. phase, adapting since the Tertiary to a large 
Variety of environmental conditions. 


LEGUMINOSAE (FABALES) 


Eois 8 shows the contrasting records for the 
се main groups of Leguminosae. Caesalpini- 
кем appear as the oldest, with a strongly di- 
Versified number of pollen types. Macrofossils 
rom the Maestrichtian confirm the earliest oc- 
currence of pollen for this taxon. 
Mimosaceae are recognizable as soon as their 
characteristic polyads appear in the middle 
. ene, and tetrad pollen has been found asso- 
I with mimosoid flowers from the same pe- 
9d (Crepet & Dilcher, 1977) indicating a phase 


MULLER — FOSSIL POLLEN 


431 


of active evolution in flower structure. An earlier 
tricolpate phase of single grains may have gone 
undetected, however. 

Fabaceae are nearly absent in the fossil pollen 
record, presumably because of the low pollen 
productivity and lack of characteristic pollen 

5 


= 
e 


This picture broadly agrees with Raven and 
Polhill’s (1981) views on the development of the 
legumes as a whole. They assume a Cretaceous 
development for Caesalpiniaceae with a Paleo- 
gene radiation of the main branches of the trop- 
ical, woody legumes (Caesalpiniaceae, Mimo- 
saceae, and Fabaceae) and a proliferation o 
advanced Fabaceae in the Neogene is postulated. 


MONOCOTYLEDONS 


As may be recalled, the first monocotyledon- 
ous pollen types have been recognized in the Ap- 
tian, but these cannot be more closely identified, 
and the same difficulty holds true for most of the 
succeeding Cretaceous types. It may be signifi- 
cant that the pollen of the first modern groups 
appears only in the upper Cretaceous, as will now 
be discussed more in detail. 


RESTIONACEAE (COMMELINIDAE) 


Among the most intriguing monocotyledon- 
ous groups well represented in the fossil pollen 
record are the Resti , Starting in the Maes- 
trichtian. As shown in Figure 9 and discussed 
recently by Hochuli (1979), the fossil distribu- 
tion for this taxon is quite different from the 
Recent one, indicating that the present range is 
a relict one. A Gondwana origin is likely, how- 
ever, from which extensions northwards to Eu- 
rope and North America became possible. The 
Maestrichtian occurrence in West Africa, cou- 

ed with the total absence of restionaceous pol- 


place via Africa. Hochuli (1979) has suggested 
that Rhizocaulon, a macrofossil occurring in the 


pe 
plant shows rather profound points of difference 
with the Recent genera of this family, and its 
pollen has not yet been isolated from its fructi- 
fications. 


POACEAE (GRAMINEAE) 


The first, rather doubtful, fossil grass pollen 
grains appear in the Campanian. They are scarce 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Уо1. 71 


= 
50 10 20 30 40 50 60 70 80 90 100% 
Pleistocene 25 
Pliocene [ 
upper Miocene [ Ре 
11 mto 
middle Miocene | Хе” 
: br f 
lower Miocene | Asteridae P 
22,5 P Р 
Е P d 
^^ 7 
Oligocene | ^ О. 
ra 7 
» 4 
зэ » Pd 
и d 
upper Eocene 
_ x » f° 
middle Eocene р х / о Malvanae ә 
50 + E a 
lower Eocene х 
55 , 
i у“ 
Paleocene x ^6 
65 m 
Maestrichtian | T d 
lanx Lo Hamamelididae 
Santonian 
84 
Coniacian er 
Turonian 
95 
Cenomanian 
100 
Albian 
109 
Aptian 
Pollen morphological differentiation, cumulative 96 curves 
FIGURE 7. Cumulative 96 curves for Hamamelididae (dots), Malvanae (circles), and Asteridae (cros , 

: will 
and badly preserved. Firm records date from the Tertiary. Its pollen record, however, ee (cf 
Paleocene and they become increasingly abun- reflect the adaptation towards anemop y 
dant in the course of the Tertiary. Takhtajan, 1969: 238). 

Although macrofossil remains of this family CEAE 
have been described already from the Creta- VETERA :« family 
ceous, firm records based on caryopses date only The characteristic pollen grains of this idi 
from the Lower Eocene (Daghlian, 1982). This аге first found in the Middle Eocene ad 


confirms the impression that the main devel- 
opment of the family started only in the earliest 


agrees well with the macrofossil Wi 
starts with fruits in the Lower Eocene О 


! 


1984] MULLER—FOSSIL POLLEN 433 


os А 
Caesalpiniaceae Mimosaceae Fabac. 
- 
Е 2 
со . . : a 
e KT - + a ٠ EE | 
= ә ' ч ә - a . x 
a LJ LJ - a ГИ - ә = 
= а n „к ф о a а оне 
e . e = t P 0 x a = = о o ы ш = s 
= - e v . , - = СА: тала ST · @ о з 5:6 
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ا‎ Lj o a л Lal a = a e o o Бл) - - a - 
E í з eo ~ ma ва ua Wu gG 8 45 9 " D ти ы o 
om ~ 8 E 3" # Are 3 4 8 ч зл а нн в & 
- a 9 ~ л ~ - = - ч 
= ТЗ Eo a © a BS ch e 8a P 4 d B8 D 5B S + о 
e = hÀo8 ak B. 8 bp Uc» а "9 о "3 P c E = = 
> oO r- oe – © Ба Аа об бо = =: À <€ + = 
© 
Pleistocene 2 | | 
Pliocene 


upper Miocene 
11 


middle Miocen 


lower Miocene 


Oligocene 


39 


upper Eocene 
44 


middle Eocene 
50 


lower Eocene 
55 


Paleocene 

65 
Maestrichtian 

69 
Campanian 
Santonian 

ва 
Coniacian ш 
Turonian 


Cenomanian 
100 


Albian 


Aptian 


114 


FiGURE 8. Pollen records for Fabales. 


Earlier macrofossil records of Cyperaceae аге The distribution of the recorded types is shown 
considered dubious (cf. Daghlian, 1981). in Figure 10. Again, the more characteristic lep- 
idocaryoid types dominate here, but taking oth- 
ARECACEAE (PALMAE) (ARECIDAE) er, less clearly identifiable types into account, the 
microfossil record suggests a lower Senonian di- 
versification phase in West Gondwanaland, and 
a second diversification in Southeast Asia must 


Whereas the preceding monocotyledonous 
ilies each had a fairly uniform pollen type, 
" 1 di ified in this resr 


434 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


Tert. e ert; o 


T 
ОС a Restio subverticillatus type рс 


Кеѕііопасеае 


аға 


Hypolaena lateriflora type | U.Cret.Tert. x Rhizocaulon 


Restionaceae / 
Centrolepidaceae 


recent distribution of Restionaceae + 


Centrolepidaceae 


FIGURE 9. Recent and fossil distribution of Restionaceae and Centrolepidaceae. 


have taken place in the Tertiary (Muller, 1979b). 
The macrofossil record supports this picture be- 
cause fossil palm wood starts appearing regularly 
in the Senonian, and both leaves and stems occur 
in the Santonian of North America (Daghlian, 
1981). 

A Gondwana origin is postulated by Moore 
(1973) and Dransfield (1981) on the basis of Re- 
cent distribution patterns and a revised taxon- 
omy. It is not at all clear what factors have caused 
this relatively late development, although an ob- 
viously secondary development of the only ma- 
jor woody group of monocotyledons, from semi- 
aquatic herbaceous ancestors in the Lower Cre- 
taceous, which has taken considerable time to 
achieve, is indicated. 


PANDANALES 


According to the pollen records, this group 
starts occurring in the Maestrichtian, although 
fossil fruits have been described from the Lower 
Eocene of India. These, however, are not certain 


to belong to Pandanaceae according to Daghlian 
(1981). 


TYPHALES 


ence, already in the Lower Cretaceous, oan ea 
er branch represented by vaguely identi fe 
types which probably have been produ puc 
ancestral Alismidae and Liliidae, while 50 vi 
what later, in the Upper Cretaceous, firmer 1 
dence for the development of Commelinidae 
Arecidae appears. 


ауа 


j 


1984] 


The relatively late appearance of Gramineae 
and Cyperaceae supports in particular the view 
of Stebbins (1974) that these families are highly 
advanced and actively evolving young branches 
of the monocotyledons. 

It is, however, clear that a much closer study 
of the Cretaceous macro- and microfossil record 
will be necessary to confirm this tentative pic- 
ture. 


EVOLUTIONARY MODEL 


So far, we have disc d large scale taxonom- 
ic diversification. It may be worthwhile to con- 
sider smaller scale phenomena also, because here 
we may have a chance to detect the evolutionary 
process at work. Most angiosperm pollen types 
appear fairly sudden in the geological record and 
that clearly transitional series, even in thick sed- 
imentary sequences known to be nearly contin- 
uous, such as the Eocene Maracaibo basin in 

estern Venezuela or the Neogene northwest 
Borneo geosyncline, with which I happen to be 
familiar, are scarce. 

To generalize too much about evolutionary 
processes on the basis of a single organ, i.e., the 
pollen grain, is dangerous; but because pollen is 
involved in the critical reproductive phase of 
fertilization and clearly shows abundant shifts in 
à suitable series of sediments, some worthwhile 
facts may emerge. Will we find a situation re- 
flecting Darwin's view ofa myriad intermediates 


96-97), and evolution in plants is as likely to 
proceed via punctuated equilibria as it is in an- 
imals (Gould & Eldredge, 1977). 

In theory, an equilibrium situation in pollen 
characters may be disturbed without the rest of 
| Plant being affected, except that the overall 
efficiency and competitive power (level of ad- 
aptation) may change for better or worse, either 
ntraspecifically leading to population shift or in- 
'erspecifically causing competition followed by 
s lacement and extinction. Three different cases 
Will be discussed. 
in Santalales. It has been argued that the ex- 
к group of plants that produced Aquilapol- 
enites type pollen, and that was common in the 
Upper Cretaceous of part of the northern hemi- 
SPhere, was related to Santalales based on its 
resemblance to certain present-day lorantha- 


MULLER — FOSSIL POLLEN 


435 


Areca ipot t. 
Calamus longisetus t. 
Oncosperma 
Eugeissona minor 


Nypa 


м | age in million years 


— Elaeis 
— Korthalsia rigida t. 


—MM——7] Eugeissona insignis t 


middle Miocene F 


lower Miocene f 


@ 
> 
Е 
o 
o 
2 
[^] 
< 

Pleistocene 

Pliocene 4 

upper Miocene f 

11 

Oligocene E 


39 


upper Eocene | 
44 


middle Eocene f 
50 


lower Eocene | 
55 


Paleocene - 


65 


Maestrichtian | Arecaceae 


Campanian | 
7 


Santonian E 
Coniacian saf 


Turonian 
95 
Cenomanian | 
100 
Albian 


109 


Aptian — T 


Ficure 10. Pollen records for Arecaceae. 


ceous and santalaceous pollen types (Jarzen, 
7) 


— 
~ 


By comparison with Recent harmomegathic 
types, the peculiar morphology of this genus can 
be described as a multidimensional harmome- 
gathic stress system. The oblate, disc-shaped pol- 


436 


len types of certain Loranthaceae, in contrast, 
show a concentration of harmomegathic move- 
ment along the polar axis and could be derived 
from an Aquilapollenit l type by a fairly 
simple structural change. This change may have 
en accompanied by a change in pollination 
mode, since the Aquilapollenites types 
abundant in the Upper Cretaceous than the suc- 
ceeding loranthaceous types, which first occur in 
the Lower Eocene but remain scarce. Actually, 
the crucial transitional stages have not been dis- 
covered yet, suggesting that small populations 
were involved. Probably only a minor part of the 


ХУМА 121i 


branching 


T 
LAE C 


ffina 


о 1ew adapt d t ofits species 
die out of the top Cretaceous. An alternative 
interpretation of the evidence would be to as- 
sume an independent origin of Loranthaceae from 
a much earlier ancestral santalaceous complex 
that also gave rise to the Aquilapollenites group 
in mid-Cretaceous times. Wiggins (1982) sug- 
gested that Expressipollis striatus from the Cam- 
panian of Alaska can be assigned to Lorantha- 
ceae, and this species thus could form part of a 
transitional series. 

This separate develop is even more likely 
for Olacaceae and Santalaceae, because some of 
their genera have retained a basic tricolporate 
pollen type that shows no obvious relation to 
Aquilapollenites. Moreover, in Olacaceae ad- 
vanced pollen types, like the Anacolosa type are 
quite different from Aquilapollenites and appear 
already in the Maestrichtian, suggesting an even 
earlier origin for this family. 

Anacolosidites striatus from the Campanian of 
Alaska, claimed by Wiggins (1982) to represent 
Olacaceae, is more probably loranthaceous. 

Thus, although the Aquilapollenites complex 
could be placed taxonomically in Santalales as 
an extinct family, with closest affinity to Loran- 
thaceae, its exact phylogenetic relationship with- 
in the order remains to be discovered. 

2. Juglandales. Rather more firmly estab- 
lished is the connection between J uglandales and 
the preceding Normapolles group, the morpho- 
logical link between which has already been dis- 
cussed in a previous paragraph. As in the pre- 
ceding case, most Normapolles plants became 
extinct, some as late as Eocene, but a few appear 
to have given rise, by abandonment of the highly 
specialized apertural adaptations typical for the 
group, to a new line of evolution. Nichols (1973) 
has studied these early Juglandales in detail and 
it appears here also that the transitional popu- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


lations may have been small. The subsequent 
evolution leading towards pollen types such as 


it difficult to establish precise taxonomic sepa- 
rations. Structurally, these later pollen types do 
not diverge strongly and all remain typical wind 
pollinated forms. Taxonomically the Norma- 
polles group can be recognized as an extinct fam- 
ily within Juglandales. 

3. Sonneratia. On a much smaller scale is 
the origin of the genus Sonneratia. As shown in 
Figure 11, two Recent pollen types, which are 
restricted to two good species that hybridize but 
produce infertile offspring, were found to origi- 
nate via a short-lived phase of small transitional 
populations, from an extinct ancestral type ге- 
sembling certain lythraceous pollen types (Mul- 
ler, 1978). This diagram clearly shows the typical 
branching pattern of the punctuated equilibrium 
model of Eldredge and Gould (1972). 

The critical transition of the pollen characters 
involves a short period of morphological recon- 
struction that can be interpreted as a rearrange- 
ment of the harmomegathic stress system (Mul 
ler, 1981b). The striking subsequent increase in 
abundance testifies to the ecologic success of the 
new taxa, which presumably competed y 
with the less specialized parent plant. However, 
what other factors have been involved remains 
quite unknown in the absence of macrofossils. 

As far as pollen characters are concerned, t 


variability still present, and the hybride e 
tween several species of the genus (Muller, , 


appear in the fossil record about at the same 
as the first pollen records (Muller, 1978). p 
The critical factor for this evolutionary " 
velopment is, of course, reproductive isolatio 
Pollen variability, as present in the Recent gw 
of Sonneratia, in itself does not promote "d 
tion except when crosses tend to increase 4 
infertility. The changes anticipated in A 
the Recent populations of S. alba and 5. ¢ sit 
laris could conceivably lead to another ~ 
species in this way, but to be evolutionarily 
cessful, the new species has to change its 200 


| 


| 


1984] 


also, in order to invade a new niche or to replace 
its parent, as probably happened in the early 


iocene. 
The lesson from this is that pollen develop- 
ment, in addition to seed and embryo develop- 
ment, is closely related to the coming into ex- 
istence of reproductive isolation, much more 
probably than wood or leaf characters. After all, 
a cross between two leaf types almost always will 
result in a new leaf shape, which must be of about 
equal efficiency as the parent leaves, but cannot 
influence reproductive isolation, except very in- 
directly ifa shift in niche results. Taxonomically, 
the pre-Miocene taxa appear to be intermediate 
between Lythr. 18 ti d may 
represent a distinct genus, ancestral to the youn- 


ger species of Sonneratia. 


the punctuated equilibrium model in showing 
evidence for small transitional populations, fol- 
lowed by more gradual evolutionary change. 
SO agree in the presence of extinct ancestral 
complexes that link younger descendants. 
bviously, a similar process could be postu- 
lated for the earliest evolution of the angiosperms 
as a whole. 


AGE AND ADVANCEMENT INDEX 


Mo oí Takhtajan (1969), but taxonomic 
: xis are subjective, especially at higher 
vels and many different systems exist. 


а with the character complexes of the taxa, 
ОГ this purpose Sporne’s (1982) advance- 


Xe approach has always been the danger 
TCular reasoning and any support from fossil 


MULLER —FOSSIL POLLEN 


437 


[2] 
ы 
с 
Ф 
> 
| а 
© 
Е Sonneratia Sonneratia 
= caseolaris alba 
2 type type 
с 
0 
mE 
w | 
~ | 
ор 
ue Gr 
жг у p 
8 | e E 
2 : 2“ 
Ф | SE: 
Sp = 2 
N $ р, 
[^] E: 2 :: 
— o 
o i» 
8 o. 
о ae 
ш 


\Florschuetzia semilobata 


\ 
\ 
<> 
EY 
x 
v 
\ 
\ 


Florschuetzia trilobata 


FicunE 11. Pollen records for Sonneratiaceae in 


West Malesia. 


evidence would be decisive in testing the pre- 
diction that families with a high A.I. would ap- 
pear later in the record than those with a low 
A.I. Sporne (1980) himself had already tested 
the earlier data published in 1976 and found that 
the prediction could be confirmed. On the basis 
of the present data and of Sporne’s latest list of 
1980, I retested the prediction and the resulting 
scattergram is shown in Figure 12. Obviously, a 
large amount of scatter is present, which is no 
doubt due to a number of disturbing factors: en- 
tomophilous taxa will be recorded later than an- 
emophilous ones, coastal species tend to be re- 
corded earlier than inland species, and families 
that contain both unspecialized and advanced 
pollen types tend to be recorded only when the 
latter have evolved. Nevertheless, the expected 
correlation, if weak (r = —0.3), is there and highly 
significant (P > 0.95). If we look at the averages 
for certain periods we can see that they are sit- 
uated approximately on a straight line. 


438 


Advancement 
index 


110 100 90 80 


FIGURE 12. 


Maestrichtian to Aptian/Albian (Walker et al., 1983). 


Perhaps the results become more meaningful 
in Figure 13, which shows the relation between 
АЛ. and first occurrence for about 52 selected 
families. For these families, the pollen record is 
exceptionally reliable or extensive. 

noted that, if Sonneratiaceae are 
merged with Lythraceae, the correlation im- 
proves. In fact, the difference in A.I. between 
these two closely related families is very much 
influenced by the woody character of the former 
and the many advanced herbs in the latter. 

Most striking is the contrast between the Cre- 
taceous plus Paleocene and the post-Paleocene 
families, but clearly families like Winteraceae 
and Schisandraceae are prime examples of fam- 
ilies with a low A.I., which can only be detected 
when their specialized pollen types appear. Mag- 
noliaceae, as stated before (Muller, 1970) are 
probably completely underrepresented and, were 
it not for the significant ancestral chlorantha- 
ceous and winteraceous grains in the lower Cre- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


20 10 
60 50 40 30 age in mill. years 


: ; onous 
Relation between age of first pollen record and Sporne’s advancement index for dicotyled 

on 7? = —0.3; P < 0.05, df= 116. ме 
aleocene (Crepet & Daghlian, 1981) and a change of Winteraceae 


Data based on Muller (1981) 


taceous, our survey would hardly have wam 
any significant information on аё earliest р 
of angiosperm development at all. : 
опита test which of the character we 
plexes used by Sporne (1980) show the c T 
correlation with age of first pollen record. ve 
has been attempted by Baas (1982) for Xy : 
characters. He comes to the conclusion that! 
ilies recorded from the Cretaceous show a : 
incidence of primitive vessel, fiber, and "m 
chyma features than those that appear in the Ter 
tiary, thus confirming the well-known 
trends” in xylem evolution. 

The apparent straight line relation bene a 
of first occurrence and A.I., if прање a 
strongly suggests a Jurassic ‘origin’ for š 
giosperms as a whole. This can also be po + 
а different way, by plotting the time of bbins 
pearance on the diagram, published by е 968), 
(1974, fig. 11-1), based on Cronquist к й 
which includes the monocotyledons and 


мај UIOS 


1984] MULLER—FOSSIL POLLEN 439 
Advancement Oligocene- 
Dein Cretaceous Paleocene Eocene Pliocene 
Acanthaceae 
Abels Compositae 
66-70 Plantaginaceae 
Chenopod./ Loranthaceae 
61-65 Am Е Nyctaginaceae 
Haloragaceae Santalaceae 
Proteaceae Apocynaceae Convolvulaceae 
Lythraceae 
56-60 Malpighiaceae 
Umbelliferae 
Onagraceae Icacinaceae Thymelaeaceae 
51-55 Chloranthaceae Polygalaceae angiaceae 
Ulmaceae Anacardiaceae 
ee) 
Juglandaceae Casuarinaceae Lecythidaceae Sonneratiaceae 
Мупсасеае Malvaceae Trapaceae 
46-50 Sapotaceae Rubiaceae 
Leguminosae 
Symplocacea 
Olacaceae 
| 
Aquifoliaceae Didymelaceae Caryocaraceae 
M Tiliaceae Guttiferae 
41-45 Sapindaceae 
Fagaceae 
Bomba 
Ericac./Clethrac. 
eH]  ——— 
z Annonaceae Euphorbiaceae Rhizophoraceae 
6-40 Betulaceae Hamamelidaceae 
Buxaceae 
DM ] 
31-35 Winteraceae 
26-30 Schisandraceae 


FIGURE 13. Age of first pollen record and Sporne's advancement index for selected families. 


however, ere also, Asteridae stand out as the 
ре and most advanced angiosperms. As is 
ell known, this group also has the highest pro- 
кы of herbaceous types within the dicoty- 
Ons, supporting the notion, first formulated 
by Sinnott and Bailey (1914) nearly 70 years ago, 


ons the woody palms appear young and 

сте probably derived from herbaceous ог 

Pc ancestors, as also postulated already by 
Same authors. 


As in the correlation diagram shown previ- 
ously, this diagram also shows the central hole 
of very low A.L, through which, metaphorically 
speaking, the earliest angiost havee ged 
undetected as yet by any pollen or macrofossil 
record and not having survived unchanged in the 
Recent flora. 


илл BL 


CONCLUSIONS 

The signifi f the fossil pollen data, which 

I have attempted to show here, thus covers the 
whole spectrum, from a broad view of the de- 
velopment of the angiosperms as a whole with a 
first pollen record from the Barremian but prob- 
ably originating earlier; to the early split between 


440 


monocotyledons and dicotyledons; to the split 
within the dicotyledons between woody Ranales 
and a more advanced group; to the achievement 
of dominance in the vegetation by successful 
competition with gymnosperms and ferns; to the 
crystallization of most orders of angiosperms in 
the course of the Cretaceous, and of many mod- 
ern families and genera in the Cretaceous and 
Tertiary; and finally to the origin of some modern 
species in the younger Tertiary. 

Of course, any taxon starts as a species, and 
the connection with the Recent flora just repre- 
sents a fleeting moment in time, frozen in our 
Recent taxonomy. To adopt the rules of modern 
taxonomy to fossil groups takes special care but 
is possible, as long as we always remember that 
a taxon is constructed by the independent evo- 
lution of character complexes. Wood and pollen 
evolution, as well as leaf and pollen evolution, 
thus, have hardly any common factors, but flow- 
er and pollen evolution are much more closely 
linked and it may be argued that much of what 
we see in the fossil pollen evolution reflects, in 
essence, the struggle for outbreeding by improve- 
ment of the changes for cross pollination. 

The palaeobotanical data as a whole show more 
and more clearly the different timing of first oc- 
currence of characters as well as the shorter or 
longer period of evolutionary coherence that fol- 
lows. Clausen and Hiesey (1960) have shown 
that a genetic basis can be found for the dif- 
ference between a variable and a uniform period 
in the life of a taxon, and Gould and Eldredge 
(1977) have drawn attention to the significance 
of periods of stasis in their interpretation of the 
fossil record. 

Possibly the pre-magnoliid plants from the 
early Cretaceous ancestral to Chloranthaceae and 
Winteraceae have existed for an even longer time 
than their pollen record indicates. 

In general, Chloranthaceae are considered to 
combine a primitive wood anatomy and pollen 
morphology with highly reduced and specialized 
reproductive structures (cf. Stebbins, 1974: 123). 

Leroy (1983) has recently challenged the cur- 
rent interpretation of the chloranthaceous flower, 
which he considers to be primitive and primarily 
anemophilous. In particular, the strobiloid na- 
ture of the male flower of Hedyosmum would 
bring this genus close to the elusive angiosperm 
ancestors. 

In Winteraceae, a more specialized pollen type, 
which had already evolved in the Aptian/Albian, 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


is combined with primitive reproductive struc- 
tures and vesselless wo 

In both cases, it would appear that reproduc- 
tion has not changed much since the lower Cre- 


pollinating agents as today. 

At the other extreme, we have seen that the 
‘tubiflorous’ families, adapted to specialized in- 
sect visitors, and Sonneratia, adapted to bat pol- 
lination, are young groups, and that in the latter, 

stasis’ i haracters | tb hi 
yet. 

More indirectly, the fossil pollen evidence in- 
dicates the younger are of the herbaceous dicot- 
yledons and confirms the predicted correlation 
with advancement indices. 

For the monocotyledons, the secondary de- 
velopment of the woody palms is clearly shown, 
as well as the young development of Gramineae 
and Cyperaceae, which may have played a role 
in the extinction of the Restionaceae in the 
northern hemisphere. : 

The recognition of extinct groups of ango- 
sperms on the basis of the pollen record is раг" 
alleled by recent palaeobotanical research on 
macrofossils and tends to challenge further the 
formerly widely held idea that the middle Cre- 
taceous angiosperm flora contained many mod- 
ern taxa, some exceptions (Platanus) notwith- 
standing. But even these early extinct groups ca? 
be related to present-day taxa and thus incor- 
porated in the body of taxonomic knowledge. 

The question of external factors providing рё 
riodic impulses for accelerated angiosperm ene 
lution concentrates on the modernization in the 
Maestrichtian, in which many unrelated taxa âp- 
pear to be affected. Опе can think of climatic 
factors, such as a radiation maximum, decre: 
of grazing pressure of dinosaurs, and evolution 
of chemical defenses, to mention a few possibil- 
ities. Rather more firmly established is the role 
of changing climates in the evolution of -— 
ceous groups in the course of the Tertiary, i 
the co-evolution with specialized insect and ba 
groups in the mid-Tertiary. 

To a certain extent, the fossil pollen data ee 
vide support for a view of angiosperm evoluti 
as a fairly gradual additive process, proposed 
recently by Tiffney (1981). Ји 

Remaining is the mystery of the origin 0 
angiosperms. If I were bold enough to €X 74) 
an opinion here, I would follow Stebbins (19 
and Doyle (1978) and say that they prob? 


Li 


in pollen 


f the 


OT. NN NN Ri Lama nga pet 


› 


| 


— 


C-— 


1984] 


lived in a semi-arid inland environment in West 
Gondwanaland, not that they were coastal plants, 
as recently proposed by Dilcher and Retallack 
(1981). Thus, the lack of transitional types with 
gymnosperms, although regrettable, becomes at 
least understandable. 


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their distribution. Gentes Herb. 2: 27 

MULLER, J. 1968. P. f 


s( us-Eocene 
Ж Sarawak, Malaysia. Мег Коше, 14: 1– 


9. A palynological study ofthe genus Son- 
NA (Sonneratiaceae). Pollen & Spores 11:220- 
29 


1970. miim a evidence on early differ- 
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. 1978 Ме ew Observations o on pollenmorphol- 


Gonnentiacea) Rev. Palaeobot. Pinet 26: 277- 


: pet 79a. Form and function in angiosperm pol- 

len. Ann. Missouri Bot. Gard. Par 593-632. 

‚ 1979b. Reflections on foss m pollen. 

IVth Int. Palynol. Conf. Lay rere 1: 

568-579. 

. 1981a. Fossil pollen records of extant angio- 
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and function in 
е Lythraceae and рабы, Rev. Pa- 
ia ts Palynol. 35: 93-123. 

AS Y. ота, 1966 


Hybrids and сһго- 
mosomes the genus уво д (Sonnerati- 
асеае). hi 14: a 7-343. 


NICHOLS, D. J. 1973. 
pecies of Momipites (* E ngelhardtia”)a ud ation 
genera. .& 

NiKLas, К. H., B. Н. элё gis. E M 1980. 
Apparent changes in the eb of fossil plants. 

W. C. Steer . Hech - 

lace (editors) Evolutionary Biology. Volume 12. 
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PAYNE, W. W. 


I: вел and function in an- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


giosperm pollen жай! evolution. Rev. Palaeobot. 
Palynol. 35: 39- 

RAVEN, P. & D. I. АЫ 1974. Angiosperm bio- 
geography and =“ continental movements. Ann. 
Missouri Bot. Gard. 61: 539-673. 

& R. M. POLHILL. 1981. Biogeography of the 

sae. Pp. 27-34 in К. М. Polhill & P. H. 


RUFFLE, L. 1980. Wachstums-Modus und Blatt-Mor- 
phologie bei altertümlichen Fagales Pm 


341 in 100 Jahre Arboretum (1879-1979) Berlin. 
КОРЕ, R. & Н. KNAP cklungsge- 


schichtliche und ыо ч neo zur Ober- 


ogy. Pp. TII 
овон eon Aspects of Palynology. Wiley, 
Ne ew Y 
SINNOTT, Е. r3 & I. W. ВАПЕУ. 1914. invest 
on the phylogeny of the angiosperms. A 
gm 


Bot. (London) 28: 547—600. ) 
SKARBY, A. 1968. Extratriporopollenites e 
f Scania, Sw 


1 
· 1970. The Pacific as a key to по 
plant history. Univ. of Hawaii, Harold L. Lyo 


r. Lec а 
SPORNE, K. В: 1976. Character correlation э ~ 


in assessing their significance. Pp. 312-329 in С 


; . A re-investigation of 
lation among dicotyledons. New Phytol. 85: 419- 
449. 


82. The advancement index vindicated. 
New ol. 9: 137-145 
STEBBINS, MERE 1950. Variation oe Bo in 
Plants. Columbia Univ. Press, othe 
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Species Level. Harvard Univ. Press, Cambri 
Sante В. М. 1981. The. сав status of меш 
seed ferns. Rev. Palaeobot. Palynol. 32: 63- 
TAKHTAJAN, A. 1969. оңун iem | Origin 
persal. Oliver & Boyd | 
x A phylogenetic classification o 
‚ 35-106 in M. К. Hec 
utionary 


pon R.F. 1976. 
giospermae. 
WC Steere & B. Wallace (editor), Evol 
Biology 9. Plenum Press, New 
977. Dicotyledonous eem 


Diversity and major events xc ne 
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(editor), оя pea ology an 


ork. E 
1967. Pollen et classification. 


Bot. Gard. 62: 664-723 


- 
| 
| 


ee 


1984] MULLER — FOSSIL POLLEN 443 


& A. G. WALKER. 1980. [Abstract:] Pollen 
шер! in extant primitive angiosperms апа its 
bearing on the biological interpretation of the fos- 
sil ттд record of the earliest flowering plants. 
Abstr. та Sap Palynol. Conf. Cambridge, Yes 
. G. WALKER. 1983. 
teraceous pollen] in the lower Cretaceous of bra 

fam 


ily. Science 220: 1273-127 33: : 
WicGiNs, V. Р. 1982. hg Na striatus n. sp. to 
Anacolosidites striatus n. sp. per Cretaceous 


ZAVADA, M. S. & W 


example of suggested pollen aperture evolution. 
Grana 21: 39-4 
Wo tre, J. A. 1973. Fossil forms of Amentiferae. Brit- 
tonia 25: 334-355. 
‚ J. A. DOYLE & V. M. РАСЕ. 1975. The bases 
of angiosperm phylogeny: paleobotany. Ann. Mis- 
souri Bot. Gard. 62: 801-824. 
. L. СКЕРЕТ. 1981. Investigations 
of angiosperms from the middle Eocene of North 
Celtidoideae. Amer 


68: 924-933. 


ANGIOSPERM ORIGINS AND EVOLUTION BASED ON 
DISPERSED FOSSIL POLLEN ULTRASTRUCTURE! 


MICHAEL S. ZAVADA2 


ABSTRACT 


Wall ultrastructure of fossil-dispersed pollen has recently played an important role in increasing our 

derstanding of tl igi d early luti fangiosp The criteria currently used to determine 
the affinities of fossil-dispersed pollen is discussed in relationship to homologies of gymnosperm and 
angiosperm wall layers based on biochemical, developmental, and morphological data. The bearing 
of these data on our present interpretation of angiosperm origins and early evolution is discussed 
along with new data on the wall structure of early Mesozoic dispersed pollen. 


The phylogenetic significance of pollen was first among the primitive dicotyledons and mono- 
recognized by Wodehouse (1928, 1936) long be- cotyledons based on comparative palynological 
fore palynology became a separate botanicalsub- studies of extant giosp iS р ted before 
discipline. Since Wodehouse's time numerous the fossil evidence is reviewed. This is followed 
comparative morphological pollen studies have by an examination of the criteria used to distin- 
been initiated with the intent of elucidating tax- — guish fossil angiosperm pollen from pollen of 
onomically significant pollen characteristics and other major plant groups (e.g., gymnosperms). 
the phylogenetic relationships of various plant The establishment of good taxonomic criteria to 
groups. One ofthe most intensely studied groups distinguish pollen of major plant groups 1s b 
with regard to pollen morphology and phylogeny essary before tl phylogenetic implications of the 
is the ranalean complex (e.g., Walker, 1974a, fossil pollen record can be fully appreciated. The 
1974b, 1976). The monocots have not received value of the dispersed Mesozoic pollen record m 
the attention lavished on ranalean taxa, but there larifying angiosperm origins and evolution 18 
have been significant studies of monocot pollen then discussed against the background of these 
that provide a basis for a preliminary phyloge- data. 
netic overview (Kuprianova, 1948; Zavada, 
1983a). One objective of paleopalynologists is 
to provide additional data that can eera sup- РЕ палто 
port, refine, or refute these proposed phyloge- SEAN Анон 
netic schemes based on studies of extant pollen. Although there are numerous studies of pollen 
Until recently, corroborative fossil evidence has morphology and wall structure of ranalean t4*% 
been scanty. However, this situation is beingim- Walker’s (1974a, 19745, 1976) studies are = 
proved by the employment of new techniques most comprehensive. He has determined tha 
that allow a wider range of morphological fea- monosulcate, predominantly atectate or бошо 
tures to be used in elucidating the taxonomic апа lled pollen рга! th t primitive am": 
phylogenetic relationships of fossil-dispersed dicotyledons. This implies that pollen with bee 
pollen [e.g., single pollen grain investigations with features should be encountered in the geolog? 
scanning electron microscopy (SEM) and trans- section prior to derived pollen types; 56» ™ d 
mission electron microscopy (TEM)]. The intent tiaperturate, tectate-columellate, perforate, 
of this paper is to review data on fossil-dispersed imperforate pollen. Among monocotyledon® 
pollen and provide new data that bear upon our monosulcate pollen is also viewed as prine 
current understanding of the origin and early (Киргіапоуа, 1948; Walker & Doyle, 197 
evolution of angiosperms. A brief summary of however, comparative morphological studies 
the phylogenetic relationships believed to exist have shown that in monocotyledons the tectale 


[e] 


1 wish to thank David Dilcher, Thomas N. Taylor, and James Walker for their critical review oC 
manuscript. I would like to give special thanks to William L. Crepet for his many helpful suggestions 
discussion, and to S. Ash, J. E. Canright, and D. Dilcher for providing samples. 

* Department of Botany, Ohio State University, 1735 Neil Avenue, Columbus, Ohio 43210. 


ANN. MISSOURI Bor. GARD. 71: 444-463. 1984. 


ees 


1984] 
go 
Oo o 
O 
.Multiaperturate 
Inoperturate eg. Triporotes, Polyforates 


Monads-Polyads 
Monoporate V, VI 
Ill Ai 
Zonasulcate 
a © Y 
at Ulcerate Disulcate 
ДЇ) 


Trichotomosulcate 
V, VI 


Monosulcate 


TEXT-FIGURE 


1. Major evolutionary trends of ap- 
ertures in monocots. 


I. Alismatid 1, monosulcate > inaperturate. 
Il. Zingiberidean trend, monosulcate — inapertur- 
te 


Ш. Orchidacean trend, monosulcate — ulcerate — 
rturat 


IV, Commelinidean trend, monosulcate — ulcerate 
у (irregular colpoid) > monoporate. 
- Arecidean trend, monosulcate — multiaperturate 
orms. 
VI. Liliacean trend, monosulcate — disulcates, tri- 
sSotomosulcates, zonasulcates > multiapertur- 
a 


ҮП. Alismatacean trend, monosulcate > multiaper- 
turates (polyforates). 


ıa 10001у1еіопоцѕ pollen might be presumed to 
ке ve а granular or atectate wall structure similar 
по found in the Nymphaeaceae (Ueno & 
rig 1961; Ueno, 1962; Rowley, 1967; 
Pao ; 1965, 1968). However, comparative 
ion Ological studies of monocotyledon wall 
dh e (Zavada, 1983a) show that the tectate- 
be s late wall is primitive in extant mono- 

Y'edons. It is possible that primitive tectate- 


ZAVADA —FOSSIL POLLEN 


EXINELESS 


eg. Cannaceae Orchidaceae 


Mayaca-type 


eg.Haemodoraceae 


Stemona-type 


eg. Centrolepidaceae Burmannia-type 


Arisaema-type 


tectate-perforate 


tectate-imperforate 


eg. Butomaceae, Arecaceae, Apostasieae 
TExr-FicURE 2. Major evolutionary trends of wall 
cture types in the monocots. The primitive tectate- 
columellate (perforate or imperforate) wall structure 


monocotyledonous atectate or granular and fi- 
nally extreme reduction of the exine, in which it may 
be completely absent. 


th 
the tectate-columellate wall appears to be an ear- 
ly evolutionary development. Thus, a shift from 
the atectate- or granular-walled nymphaeacean- 
like ancestor to the primitive tectate-columellate 
type found in tyledons parallels the phy- 
logenetic trend in the ranalean taxa, and places 
the primitive monocotyledons on the same evo- 
lutionary level as the derived ranalean taxa with 
monosulcate, tectate-columellate pollen; a view 
that seems reasonable in light of the proposed 
dicotyledonous origin of the monocotyledons. 
Comparing evolutionary trends of aperture 
and wall structure in dicotyledons and 
monocotyledons, we find other striking parallels. 
Walker (1974a, 1974b, 1976) has determined that 
atectate- or granular-walled pollen among some 


This is accompanied by reduction or loss of the 
aperture, or an increase in the number and types 


446 


of apertures. The monocotyledons exhibit the 
same range of trends but with differing emphasis 
(Text-Figs. 1, 2; Zavada, 1983a). Dicotyledons 
more frequently exhibit a tendency toward in- 
creasing the number and types of apertures and 
the complexity of pollen wall structure (e.g., 
Compositae). Monocotyledons, in contrast, fre- 
quently exhibit a tendency toward reduction or 
loss of the aperture (e.g., Alismatideae, Com- 
melinideae, Orchidaceae, Zingiberideae) and re- 
duction in the complexity of the exine or loss of 
the exine altogether (e.g., Alismatideae, Orchi- 
daceae, Zingiberideae). 

е might expect to observe a progression of 
pollen aperture and wall structure types similar 
to the proposed evolutionary trends in geologic 
time. Before we can adequately evaluate these 
schemes in the context of fossil evidence, we 
must provide criteria to unequivocally identify 
angiosperm pollen in a field of superficially sim- 
ilar non-angiosperm palynomorphs (e.g., mono- 
sulcate gymnosperms). 


POLLEN WALL HOMOLOGIES AND IDENTIFICATION 
OF FossIL-DISPERSED POLLEN 


The monosulcate aperture is generally consid- 
ered to be most primitive among angiosperm 
aperture types (Kuprianova, 1948; Walker, 
1974a) and appears to be a good character in 
identifying early angiosperm pollen. However, 


nosperms, and its continuous stratigraphic oc- 
currence since the Permian makes this criterion, 
in itself, questionable. This has long been rec- 
ognized by palynologists. However, the presence 
of the monosulcate aperture in conjunction with 
pollen wall structure, may provide a basis on 


gymnosperm and angiosperm taxa and proposed 
palynological criteria to distinguish between these 
groups. Doyle et al. (1975) further discussed these 
criteria and their application to the interpreta- 
tion of the fossil record. Van Campo (1971) and 
Doyle et al. (1975) recognized three basic pollen 
wall structure types; alveolar and/or endoreticu- 
late, tectate-granular, and tectate-columellate. 

e alveolar wall structure is known only in gym- 
nosperms and the tectate-columellate wall struc- 
ture is known predominantly from angiosperms. 
These appear to be good palynological characters 
for separating monosulcate pollen of these groups. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


The tectate-granular, however, is found in both 
gymnosperms and angiosperms. To further com- 
plicate matters, this is a wall structure type com- 
mon among the most primitive angiosperms. To 
distinguish between gymnosperm and angio- 
sperm pollen with tectate-granular walls, Doyle 
et al. (1975) emphasized the significance of the 
endexine [thought by Doyle et al. (1975) to be 
in part equivalent to the nexine of Erdtman 
(1952)]. Gymnosperms have lamellated endex- 
ines (nexines) and angiosperms have non-la- 
mellated endexines (nexines), except in the aper- 
tural region where it is lamellated. These pollen 
wall criteria are presumably the basis for deter- 
mining affinities of dispersed fossil palyno- 


orphs. 

Pollen wall structure terminologies are a com- 
plicated and intimidating aspect of palynology. 
Widely used nomenclatural schemes are, for the 
most part, based on structural aspects (as op- 
posed to developmental aspects) of the various 
wall layers, but there has been noticeable disre- 

d in defining the homologies for the various 
wall layers of the pollen of major plant ме 
х Зен «cian 


especially gy р БЛОЗЕ : 

dition, many of the terms proposed by various 
authors to describe pollen wall structure are used 
interchangeably, implying homologies exist 1n 
contradiction to their original definitions [e-8- 
Faegri’s endexine (in part) = Erdtman’s nexine]. 
This has resulted in an ambiguous situation for 
palynologists who wish to establish taxonomic 
and phylogenetic relationships among various 
plant groups based on pollen wall structural data. 
To help clarify this situation it is necessary 10 
describe in detail the two most widely be 


ture. 7 1 је" 
The two most widely used wall ee 
menclatural systems are those of Faegri an 1952 
sen (1950; also Faegri, 1956) and Erdtman j a 
1963, 1969). Faegri and Iversen de dt 
ished th jor wall layers, the outer °F 
eee = : се preis ka hes and the 10- 
ner cellulosic intine. The terms ektexine 


intexine, but Erdtman (1952) later abando 
these terms. Erdtman (1952) also identified a 
primary wall layers, the sporopolleninous ме 
and nexine, and the cellulosic intine. The in si 
recognized by Faegri and Iversen У 
Erdtman (1952), easily corrodes in aceto ure 
and fossilized pollen. It has been generally 


| 


— 


— 


1984] 


nored in phylogenetic and taxonomic schemes 
and will not be discussed further. 

Faegri and Iversen (1950) distinguished the 
outer ektexine from the inner endexine by dif- 
ferences in their affinity for the stain basic fuch- 
sin. The ektexine and endexine also exhibit dif- 
ferences in their affinity for the transmission 
electron microscopic stains uranyl acetate and 
lead citrate, and various other cytochemical stains 
(e.g., Aniline blue-black, Coomasse blue; South- 
worth, 1973), further substantiating Faegri and 
Iversen’ latural distincti tween these 
wall layers. Rowley et al. (1981) have speculated 
that the difference in stainability between these 
wall layers may be due to differences in the gly- 
cocalyces associated with these wall layers, or the 
chemical nature of sporopollenin. In addition, 
Bailey (1960) and Southworth (1974) found dif- 
ferences in the solubility of the ektexine and end- 
exine in fresh material treated with hot 2-ami- 
noethanol. The ektexine is readily soluble and 
the endexine exhibits less solubility. This 
Prompted Southworth (1974) to speculate that 
there are differences in the chemical nature of 
the sporopollenin between these two wall layers 
(cf. with one of the alternative explanations of- 
fered by Rowley et al., 1981). Regardless of the 
reason, Southworth’s data further substantiates 
the terminological distinction of the ektexine and 
endexine (sensu Faegri & Iversen, 1950). Faegri 
and Iversen (1 950) considered the ektexine to be 
à three-layered structure, based solely on mor- 
phology. The outermost tectum is the sculptured 
layer of the ektexine. The middle layer or in- 
frastructural layer can be alveolar, endoreticu- 
late, columellate, or consist of spherical or irreg- 
Чапу shaped granules or anastomosing rods. The 
Innermost layer of the ektexine is the footlayer; 
= layer can be amorphous or lamellated (but 
иу їп angiosperms), but is unsculp- 


Erdtman (1952) first identified the sexine and 


Hints nexine 2 for the inner portion ofthe nexine 
115 different from nexine 1 in its response to 


ZAVADA —FOSSIL POLLEN 


447 


ERDTMAN FAEGRI Ё IVERSEN 


1952 1963 1969 1950 
tectum 


SEXINE EKTEXINE 


~ infrostructural 
loyer 


r 


e 
ЕМОЕХ!МЕ 


© 
2 
о 

= 


NEXINE ы МЕХІМЕ | 
3 


INTINE 


INTINE 


TEXT-FIGURE 3. Pollen wall homologies. Equiva- 
lent terms in the Erdtman (1969) and Faegri and Iver- 
sen (1950) terminological schemes. 


basic fuchsin. Thus, Erdtman (1969) fully real- 
ized the significance of the differential stainabil- 
ity of pollen wall layers and proposed a system 
of terminology identical to Faegri and Iversen 
(1950): Erdtman’ ine pl ine 1 are equiv- 
alent to Faegri and Iversen’s ektexine, and Erdt- 
man’s nexine 2 is equivalent to Faegri and Iver- 
sen’s endexine (Text-Fig. 3). 

There has been a quantum increase in the taxo- 
nomic and phylogenetic palynological literature 
since the inception of these terms, unfortunately 
without rigorous application of the criteria on 
which these terms were originally based. Thus, 
these terms have been confused and their use in 
suggesting homologies among wall layers in dif- 
ferent taxa have been equivocal. This is often 
reflected in descriptive morphological studies 
confusing the two different nomenclatural 
schemes. Some workers have rejected these 
schemes outright and proposed their own paly- 
nological lexicon (e.g., Tsinger & Petrovskaya- 
Boranova, 1961; Wittmann & Walker, 1965; 
Reitsma, 1970), further confusing attempts to 
establish homologies among wall layers in dif- 
ferent taxa. It is paramount that before any at- 
tempt is made to consider the phylogenetic sig- 
nificance of pollen wall structure, consistent use 
of terminology be established. Further, wall ter- 
minology should accurately reflect structure, his- 
tochemistry, and development so that homolo- 
gies for various wall layers may be established 
reliably between angiosperms and gymno- 
sperms. Although the developmental aspects of 
the pollen wall have been generally ignored by 
descriptive palynologists, the value of develop- 
mental data have long been recognized in estab- 
lishing homologies (e.g., Nageli, 1842; Stebbins, 
1974). A sufficient body of literature on pollen 
wall development has emerged over the past 25 
years for providing insight into the homologies 
between gymnosperm pollen wall layers. 


448 


= ben bees in gymnosperms and 
divided into three phases 
(este ta аны 1971). The phases are: pre- 
meiotic, tetrad, and the free spore phase. The 
premeiotic phase encompasses the develop- 
mental interval between the initiation of the pol- 
len mother cells and meiotic cytokinesis. The 
е phases in gymnosperms and апріо- 
are generally similar and are not directly 
Eig to the development of the sporopolleni- 
nous exine. Thus, they need not be discussed 
further in the present context. However, there 
are significant differences in wall ae aei 
between angiosperms and gymnosperms 
the tetrad and free spore phases. 

In cycads and conifers, for example, the spo- 
LM sexine begins development im- 
ош 
in the callose special wall. There i is no deposition 
of a dense staining fibrillar primexine with 
embedded radially directed даљ ад e (procolu- 
mellae), as in many angiosperms. A dispersed 
fibrillar material is deposited падине the callose 


па tely асл th 


g. Audran (1981), Dickinson 
(1971), Willemse( (1 97 1), and Vasil and Aldridge 
(1970) have interpreted the dispersed fibrillar 
material as homologous with the primexine of 
angiosperms. The differences in electron density 
between the dispersed fibrillar material in cycad 
and conifers, and the primexine of angiosperms, 
and that accretion of the sporopolleninous sexine 
begins immediately, without any recognizable 
nonsporopolleninous matrix, suggest that the fi- 
brillar material in gymnosperms is not entirely 
comparable with the primexine of angiosperms. 
Upon completion of the sexine, development 
of the nexine (footlayer) begins by accumulation 
of sporopollenin on unit-like membranes. These 
sheets of sporopollenin are successively ap- 
pressed to one another but retain their lamellated 
appearance, even at maturity, in both apertural 
regions and nonapertural regions. After forma- 
tion of the nexine, the callose special wall is de- 
е € the microspores are free in the Spo- 
most gymnosperms no additional 
белиндей пара wall layers form during the free 
spore phase (however, see Rohr, 1977). The en- 
tire e sporopoleninous wall,  Sexine, and nexine are 
dran, 1981; 


Zavada, 1983b). 


e Lx v 


1 4 
a V іа SCU 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


by the sequestering of the four microspores by 
callose. Prior to the appearance of the sporo- 
polleninous wall, a distinctive fibrillar wall not 
found in gymnosperms (see above), the primex- 
ine, is formed. Embedded in the primexine 
shortly after it Bete: distinct are nonsporo- 
polleninous radially directed probacules (pro- 
columellae). Subsequently, the probacules be- 


1984). The tectum is then formed by the lateral 
accumulation of sporopollenin at the distal ends 
of the bacules. Finally, the footlayer (nexine 1) 
develops on unit-like membranes (as in gym- 
nosperms) and at times appears lamellated in 
apertural and nonapertural regions at maturity 
(e.g., Magnoliaceae, Praglowski, 1974; Annon- 
aceae, Le Thomas, 1981). Next the bases of the 
bacules become fused to the footlayer (nexine 1). 
Upon completion of the footlayer (nexine 1), the 
callose wall is destroyed and the pollen grains 
are free in the anther locule. During the free spore 
phase and in contrast to most gymnosperms, an 
additional sporopolleninous wall layer can de- 
velop—the endexine. Along with the footlayer, 
the endexine has been considered equivalent t0 
the nexine in gymnosperms (Doyle et al., 1975). 
Endexine appears to have two modes of depo 
sition in angiosperms. In one instance, endexine 
is the result of the accumulation of unit-like 
membrane 
layer (nexine 1) formation. This imparts 
Il 


& Larson, 1966; Helloborus, Echlin & GodW™ 
1969; Passiflora, Larson, 1966; Austrobaile® 
Zavada, 1984) for- 
Another etree aspect of endexine "i 
n some taxa, endexine is x 


ed with acetolysis solution, the intine ps false 
and fragments the endexine. This gives 


калшы. 


——À а = 


1984] 


impression that endexine is scanty or absent in 
acetolyzed material (e.g., Austrobaileya, Zavada, 
1984). 

Although the mode of deposition of the var- 
ious wall layers in angiosperms may vary, the 
timing of their development is consistent among 
the angiosperms thus far studied. 

Criteria currently used to distinguish fossil 
gymnosperm from the most primitive angio- 
sperm pollen (e.g., tectate-granular) depend on 
characteristics of the nexine of gymnosperms and 
the endexine of angiosperms (Doyle et al., 1975). 

he use of nexine and endexine synonymously 
implies that these wall layers are homologous. 

owever, evidence presented above, including 
the chemical difference between nexine of gym- 
nosperms (which is composed entirely of nexine 
1 or footlayer) and the endexine of angiosperms, 
born out by their differential stainability with 
various cytochemical and TEM stains, by differ- 
ential solubility in 2-aminoethanol, and by the 
different mode of deposition of the endexine in 
Some angiosperms, suggests the nexine of gym- 
hosperms and endexine of angiosperms are not 
homologous wall layers. Thus, the criteria cur- 
rently used to distinguish dispersed angiosperm 
Pollen from dispersed gymnosperm pollen, which 
imply the nexine and endexine are homologous, 
Must be rejected (e.g., Doyle et al., 1975). This 


mellated or homogeneous has what appears to 
bea developmentally and cytochemically equiv- 
alent wall layer in Ginkgo biloba (Rohr, 1977). 
: addition, the columellate infrastructure and 
endexine are relatively advanced features among 
а mme (Walker, 1976) and are not likely 
— imitive fossil angi pollen 


To make this situation worse, wall structure 
characteristics of primitive angiosperms are in- 
distinguishable from those of many gymno- 
‘perms (eg. the granular type occurs in both 
2 unm and angiosperms). Thus, there are 
= ble taxonomic features that can be used 
Sunguish primitive angiosperm pollen and 
&ymnosperm pollen, and it will be difficult to 
a the origin of the angiospermous con- 
n on palynological data alone. 
к аа these difficulties, studies of fossil pol- 
Structure can still be enlightening in a 


ZAVADA— FOSSIL POLLEN 


449 


few respects. First, these studies can help deter- 
mine general patterns of pollen wall evolution. 
Second, these studies can be used to corroborate 


11 


g ary trends of d 

on neontological data, i.e., to identify primitive 

and derived character states. Further, first oc- 

currences of key wall structure types can provide 

a temporal framework for the evolutionary trends 

in pollen proposed on neontological grounds. 
Р ада сн ы, 5i 


idiec 


pollen found in fossil fructifications might reveal 
the affinities of the dispersed pollen. Once a dis- 
persed pollen grain can be associated with a 
megafossil, the morphological features of the pol- 
len and the megafossil can then be used to eval- 
uate their relationship to angiosperms. 

In the following sections new data is presented 
on fossil pollen wall structure for a number of 
saccate and non-saccate dispersed pollen. The 
significance of these data to early angiosperm 
evolution and origins will be discussed in con- 
junction with data from other studies on fossil 
pollen wall structure. 


MATERIALS AND METHODS 


Pollen was recovered from sediment by treat- 
ment with HCl, HF, Schulze’s solution, and KOH. 
After each treatment the residue was washed with 
distilled water until neutral (pH 7). After the final 
washing the residue was centrifuged in the heavy 
liquid ZnCl,, sp. gr. 2, and the supranatant was 
collected, dehydrated in an alcohol series and 
embedded in polystyrene after Frangioni and 
Borgioli (1979). The suspension was smeared on 
a microscope slide and allowed to harden, then 
photographed. Pollen grains were then cut out 
OI 


styrene in Beem* capsules for transmission elec- 
tron microscopy (TEM). Sectioning was done on 
an LKB-1 ultramicrotome and pollen was stained 
for 15 minutes in both uranyl acetate and lead 
citrate. Sections were viewed with a Philips EM- 
300. Pollen was prepared for scanning electron 
microscopy (SEM) by dissolution of the polysty- 
rene embedded pollen in toluene until the pollen 
was free of all embedding material, or the pollen 
residue prior to embedding in polystyrene was 
ted directly SEM stubs, coated with gold- 
dium, and viewed with a Coates and Welter 
field emission electron microscope. 
The identification of pollen wall layers and 


mentioned, is based on staining properties with 


450 


various cytochemical and TEM stains, solubility 
in 2-aminoethanol, development, and morphol- 
ogy in extant pollen. Although it is difficult to 
study developmental aspects of fossil-dispersed 
pollen, few of the pertinent biochemi 

been used in attempts to interpret wall structure 
in fossil pollen. Thus, identification of wall layers 
in fossil pollen depends primarily on morphol- 
ogy and staining properties with TEM stains. In- 
terpretation of fossil pollen wall structure based 
on staining properties with TEM stains must be 
viewed with some reservation because their re- 
action to the stains are known to differ from 
extant pollen. Rowley et al. (1981) have pro- 
posed that staining is effectuated by the labile 
exine moiety (glycocalyx) and not by the rela- 
tively inert and decay-resistant sporopolleninous 
wall fraction. Thus, the depositional microen- 
vironment and diagenetic processes associated 
with fossilization can have profound effects on 
the staining properties of fossil pollen walls. 
Southworth (1974) found that fresh pollen is 
readily soluble in 2-aminoethanol, but that pol- 
len taken from old herbarium material exhibits 
less solubility. This suggests that even recent ma- 
terial undergoes biochemical changes that affect 
the physical and chemical properties of the exine. 
Stanley (1966) has demonstrated that fossil pol- 
len from various geologic stages can exhibit dif- 
ferential staining with the nonspecific stain Safra- 
nin-O, further suggesting that fossilization affects 
the physical and biochemical aspects of the ex- 
ine. Until the microenvironmental and diage- 
netic factors influencing staining can be more 
fully understood, interpretations based on these 
criteria are tentative. 


l tests have 


POLLEN WALL STRUCTURE OF DISPERSED 
FossiL POLLEN 


PRAECOLPATITES SINUOSUS, PERMIAN 


This form genus was recovered from Permian 
sediments of the Olive River Basin, Cape York 
Peninsula, Queensland, Australia. Foster and 
Price (1982) examined this taxon using light, 
scanning electron, and transmission electron mi- 
croscopy. Pollen is elongate, probably multiaper- 
turate (2—4 sulcate) and exine sculpturing is ver- 
rucate-granulate. The pollen wall is 2-3 um thick 
and is considered to have two prim TS, an 
inner laminated layer (possibly footlayer, intex- 
ine of Foster & Price, 198 2) and an outer struc- 
tured layer (exoexine of Foster & Price, 1982). 
The inner part of the outer layer is composed of 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


а granular infrastructure, which is overlain bya 
tectum that is occasionally perforated with small 
channels. Foster and Price (1982) considered the 
wall structure of this taxon to be similar to the 
granular wall structure types found in extant ran- 
alean taxa (e.g., Magnoliaceae). 


MARSUPIPOLLENITES TRIRADIATUS, PERMIAN 


This form genus is from the Blair Athol Basin 
of central Queensland, Australia. It was studied 
in detail using light, scanning electron, and trans- 
mission electron microscopy by Foster and Price 
(1982). Pollen is spherical to slightly elongate and 
has a distal sulcus and a proximal triradiate scar. 
Exine sculpturing is verrucate to granulate. The 
pollen wall is composed of two primary layers 
and an inner unsculptured layer (intexine of Foster 
& Price, 1982) and an outer layer that has а 
granular infrastruct d а tectum occasionally 
perforated by small channels (Foster & Price, 
1982). The wall structure of this taxon also shows 
striking similarities to the granular infrastructure 
of some ranalean taxa. 


MONOSULCITES SPP., 
UPPER PALEOZOIC-TERTIARY 


This widespread Mesozoic form genus 15 
monosulcate, ovoid to boat-shaped, and exime 
sculpturing is psilate. Trevisan (1980) invest 
gated the wall structure of one form from 
Lower Cretaceous of Italy, and, in the presen 
study, one form was investigated from the York- 
shire Jurassic. Both are identical in every respect. 
Pollen wall structure consists of two layers, - 
inner continuous lamellated footlayer (Layer 
of Trevisan) and an outer massive layer. The 
inner portion of the outer massive layer const 
of closely packed, somewhat homogeneous = 
ules. This imparts a spongy appearance we 
inner portion of the outer massive yore pe 

: : ars 

рона portion of this wall layer мын т 
massive layer thins in the region of the — 
however, the basal layer (footlayer) سا‎ 
constant thickness throughout. Trevisan s 
noted a thin electron dense marginal layer 0 
exine, also present in my material. This of 
considered a distinctive layer, but an аги tes). 
preservation (see discussion on Е ucommidii 
Taylor (1973) investigated pollen from the ^^ 


ue 
taceous taxon Cycadeiodea dacotensis, whic 
similar in many respects to the dispe (1980. 


investigated in this study and by Trevisan 


— ол 


ceno come"  ]——— "A oM — — — — 


~. 


1984] 


CLASSOPOLLIS SPP., 
TRIASSIC-LOWER CRETACEOUS 


This form genus has been associated with a 
few gymnosperm fructifications and probably 
represents a diverse group of plants (e.g., Chei- 
rolepis muensteri, Harris, 1957; Pseudofrenelop- 
sis, Alvin et al., 1978). Pollen has a distal ap- 
erture in addition to a proximal triradiate suture 
and frequently occurs in tetrads. Pollen wall 
structure has been investigated by Pettitt and 
Chaloner (1964); they offered two interpretations 
of the complex wall structure. One interpretation 
viewed the pollen wall consisting of an outer tec- 
tum, a columellate infrastructure with the colu- 
mellae fused to a thick three-layered footlayer. 
The outermost portion of the footlayer is a thick 
homogeneous layer. The middle of the footlayer 
consists of large, irregular shaped, inwardly di- 
rected columns which rest on a thick lamellated 


1984). Regardless of what interpretation is fa- 
Vored, the wall structure of this taxon is unique 
among fossil and extant gymnosperms. It rep- 
resents a gymnosperm pollen type with a colu- 
mellate infrastructure, a characteristic thought 
only to occur in angiosperms. 


EUCOMMIIDITES SPP., 
TRIASSIC-LOWER CRETACEOUS 


м” form genus occurs abundantly in Lower 
у P рн sediments. Pollen is elliptical to broad- 
NECS and has three apertures. One aperture is 
к, Spicuous, broad, sulcus-like aperture and 

two other apertures are thin and fold-like 


ae using TEM (Doyle et al., 1975; Trevisan, 
0; Present study Figs. 1-3). Three forms are 

AJ based on pollen wall structure. 
4 urassic form investigated in the present 
Y and a Lower Cretaceous form investigated 


ee A of Trevisan) is unsculptured, often la- 
ted, and doesn’t thin in the apertural region 


ZAVADA —FOSSIL POLLEN 


451 


(Figs. 2, 3). Based on its position and lamellated 
nature it can be considered footlayer (nexine 1). 
The middle layer or infrastructural layer (layer 
B, of Trevisan) consists of irregular shaped col- 
umellae, often interspersed with irregularly 
shaped granules (Fig. 3). The columellae and 
granules are fused to a thick tectum (layer B, of 
Trevisan), which is homogeneous in the lower 
portion and comprised of compacted supratectal 
granules in the outer portion (Fig. 3). Trevisan 
considered the outer layer of granules a distinct 
(layer C) layer due to its differential stainability 
with SEM and TEM stains. She divided this C 
layer into a three-layered structure consisting of 
С, C;, and С,. Erdtman (1963) proposed the 
term stegine for the outer margin of the exine 
that stains differently from the more central re- 
gion. This phenomenon may not be indicative 
of true biochemical differences in the exine. It 
may be due to differential chemical extraction of 
the more labile moiety (glycocalyx) of the exine 
during fossilization or affected by preparation of 
the sediment to recover fossil-dispersed pollen 
(cf. Rowley et al., 1981). This differential mar- 
ginal staining is common in many of the fossil 
taxa investigated (see below), and probably 
pratis Са distinctive biochemical layer 

Trevisan (1980) described a second form of 
Eucommiidites (E. sp. 2). She considered its wall 
to consist of three layers, an A layer similar in 
all respects to the A layer of E. sp. 1 and appears 
to represent footlayer (nexine 1). The middle B 
layer is further divided into B,, B,, and B;. Layers 
B, and B, represent a granular infrastructural 
layer and B, a homogeneous layer comprising 
the tectum. The outer C layer is distinguished 
once again on its differential staining from the 
inner portion of the tectum, and is a similar sit- 
uation to that observed in the C layer of E. sp. 1. 

Doyle et al. (1975) described a third form of 
Eucommiidites from the Lower Cretaceous. Its 
wall consists of three layers. An inner lamellated 
layer, which Doyle et al. (1975) term endexine, 
probably represents footlayer (nexine 1), in light 
of its position, staining characteristics and pre- 
sumed gymnospermous origin. The infrastruc- 
tural layer i prised of sph ical g les that 
are overlain by a homogeneous tectum that is 
traversed by small perforations. 

The three taxa of Eucommiidites all have three- 
layered exines, a lamellated footlayer [nexine 1, 
A layer of Trevisan, endexine of Doyle et al. 
(1975)], an infrastructural layer consisting of 
spherical granules (Doyle et al., 1975), or a ho- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


—— 


omma === 


нь най 


1984] 


mogeneous to granular layer (Trevisan, 1980, Е. 
sp. 2) or a columellate to granular infrastructure 
(Trevisan, 1980, E. sp. 1, form investigated in 
the present study), and a tectum that may or may 
not have supratectal ornaments and can be mi- 
nutely perforate. 

Only four individual pollen grains of this form 
genus have been studied with TEM thus far. These 
studies have revealed that three distinctive taxa 
exist based on pollen wall ultrastructure, sug- 


eisa 

tendency toward the columellate infrastructure 

in E. sp. 1 of Trevisan and the form investigated 

in А present study (which are considered here 
the same taxon 


EPHEDRIPITES SPP., TRIASSIC-RECENT 


This form genus, as Mchedlishvili and Shak- 
moundes (1973) have pointed out, does not form 

а natural group. Trevisan (1980) sectioned two 
species from the Lower Cretaceous and in the 
Present study one species from the Triassic Chinle 
Formation was investigated (Equisetoporites 
chinleana). 

The pollen is oval to elliptical one 
25-60 um long, monosulcate to inaperturate 
possibly multiaperturate) with conspicuous ње: 
gitu ridges. It is superficially similar to pol- 
len of ка extant taxon Ephedra (however, сот- 
pare Figs. 8, 9 with Fig. 5 of Gnetum and Fig. 7 
of Epa) Trevisan (1980) sectioned a mono- 
sulcate form and distinguished two major wall 
layers; an inner continuous lamellated layer (lay- 
er A) and an outer complex layer that comprises 
the ridges and grooves. The inner A layer, based 


а 


ZAVADA —FOSSIL POLLEN 


453 


on its position in relationship to the outer wall 
layers and lamellated nature, probably is foot- 
layer (nexine 1). The outer layer, the infrastruc- 
tural layer, and tectum is further subdivided into 
layers B,, B,, B,, С, and D by Trevisan (1980) 
Layer B, isa thin, continuous layer that underlies 
the B, layer, which is composed of fragmented 
ex à LAE. units. The B, layer is similar 
anular infrastructural layer in extant 

E ord (Fig. 7) and Gnetum (Figs. 5, 6). Layer 
B, is homogeneous and thins in the regions of 
the grooves (as does the tectum in extant Ephed- 
ra pollen). The outer margin of the tectum stains 
differently than the inner portion, in a similar 
manner to that observed in other fossil taxa (see 
above) and is distinguished as layer C by Trev- 
isan (1980). On the surface of the exine are scat- 
tered *globulets" 0.01—0.09 um in diameter, 
which Trevisan terms the discontinuous D layer. 
The peti are possibly the remains of a ta- 
petal depo 

The cp Chinle form genus Equisetopo- 
rites chinleana (Daugherty, 1941) also falls with- 
in the morphological circumscription of Ephed- 
ripites and has been reported as tectate- 
columellate by Cornet (1979). Pollen of this type 
has been found associated with the gymnosper- 
mous taxon Masculostrobus clathratus (Ash, 
1972). My investigation of this taxon has shown 


ever, see below; Fi 
layered structure contine of a thin, lamellated 
footlayer (Fig. 8), which is fused to short stout 
columellae (Figs. 8, 9) (their stout appearance 
may be a result of compression). The columellae 
are overlain Y a thick oo tectum, 

g. 8). Both 


which F 


+ 


ү URES 1-9. 1 
Of the same grain pictured in Figure 1. Not 


5-7. Pollen n of 
>, fine granul 3 


mi 


-3. Eucommiidites sp.— 1. Yorkshire Jurassic, x 400. — 
te the three apertures (arrows) A the three-layered exine, 
howing three-laye 


.—5. Transmission electron ш. 
ar layer beneath the homogeneous tectum ee a spine, х32,2 


Transmission electron micrograph 
х 4,040. — 


netum showing thick footlayer (nexine 
00.—6. ning electron 
7. Transmission сев micrograph 


rastructural 


Of the р polyplicate pollen of Ephed lifc 
am d thick t ч 


(Compare 
5 and 7, ide 7), and that the wall 


. Transmission electron micrograph of the same grain pict 


e tectum i is continuous in the groove ibus x21 ‚000. 8-9. Equisetoporites chin- 
of the same grain pictured hin lam 


- Transm 
foot р 
di (nexine 1 у , Stout columellae, and thick outer tectum. Note tectum 
"ream Fi à; structure is remarkably different from =, — taxa in Пи 


in Figure 4, showing t саса 
is discontinuous in the grooves 


n Figure 4, tangential 
200. 


Section oft the pollen wall showing the columellate structures underlying the tectum 1 (arrow), x14, 


454 


eod tectum and columellae are absent in the re- 
ofthe grooves (Figs. 8, 9). The grooves might 
менне ode itd weak areas of the polien 
wall and might hav 
this form would be multiapertürate; Fig. 8). | The 
tectate-columellate structure in this Triassic form 
genus represents the earliest occurrence of this 
wall structure type in the fossil record, a wall 
structure type thought to be restricted to angio- 
sperms 


BISACCATE POLLEN WITH GRANULAR 
INFRASTRUCTURE, TRIASSIC-CAMPANIAN 


In all extant plant groups bisaccate pollen has 
alveolar (more precisely endoreticulate) wall 
structure. жет o the Paleozoic saccate gym- 


endore 


ticulate wall ооа (e.g g., see Millay & Taylor, 

1974). Thus Mesozoic saccate pollen, Ae 
little studied, is generally dan a morpho- 
ogically | ver, Pas con- 
tinuing studies of Triassic, ан and Creta- 
ceous saccate pollen have confirmed the existence 
of the granular infrastructure among pollen of 
this type. 

In all the forms investigated, the corpus is cir- 
cular to elliptical with a distally located sulcus 
flanked by two relatively small sacs (Figs. 10— 
17). Pollen ranges from about 30 um to greater 
than 50 um in size (including sacs). The sacs may 
appear fully functional, as in many ofthe Triassic 
and Lower Jurassic forms (Figs. 10, 11), or may 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


be small, apparently highly reduced, vestigial 
structures (Figs. 12-17). Pollen with the small, 
highly reduced sacs often appears to be morpho- 
logically similar (except for the sacs) to mono- 


12-17, 19, 20). The pollen wall in all of the taxa 
investigated is a three-layered structure (Figs. 23- 
30, including the non-saccate genus Verrumono- 
colpites). The inner layer is homogeneous or la- 
mellated (Figs. 23-30) and, based on its position 
and similar staining properties to the outer wall 
layers, represents footlayer (nexine 1). The in- 
frastructural layer consists of spherical 0 —- 


ularly 
23-30), and i in some of the Cretaceous forms 
approaches the columellate condition (Figs. 24, 
25). The outer layer, tectum, is thick and may 
(Figs. 25, 27) or may not be perforated (Figs. 29, 
31). Exine sculpturing is usually scabrate (Figs. 
19-22, 26, 29, 31). The sacs in many cases result 
from a separation of the footlayer and intra- 
structural layer, identical to sac formation ш ех" 
tant endoreticulate (alveolar) walled gymno- 
"erm a (Figs. 27, 28). However in pe 
rms, i.e., 
15, 30) С Granabivesiculites inchoatus pec 
13, 24), the sacci result from a build up of exinal 
material. 

Pollen wall structure of these saccate gymno- 
sperms is similar in many respects to gran 
wall structure of extant ranalean taxa. 


5 


Ed Pie 


FIGURES 10-22. Fossil мм pollen. —10. Bisaccate grain Да the Triassic Chinle Fm rkshire 
е grain is pictured in Fig. 23), x —11. Bisaccate grain from the Yo 
Jurassic, showing relatively аш sacci (similar to Bacubivesules i inchoatus of the Ceno Dakota 
m inchoat Da 
nabivesiculites олы Сепотапіап Dakota 
EE a electron са hs of 
man 


electron micrograph of t 


Minnesota, Fig. 12), x 400.— 12. 


4. Gra nabivesieulite es d Ceno 


electron micrographs of a ма ain 
Cenomanian Dakota Fm., Min 


micrographs of the same grain are p igs. 2 of 

are Figs. 19 and 20), x400.— 15. Рапаин і прв of 
wing small pustule-like sacci (transmission electron m! 

the same grain are pictured i in Figs Ej and 30), x 400. --16 6. Ves estigi 


— 
. (transmission 


ta Fm., 
manian 
kota Fm., Minne showing 
Т , Minn 


Figs. 24 
the same grain are pic Mi in 

ta Fm., Mire apie: — sacd 
in Fi 


scanning 
hoatus, 


Albi 
у, x 400.—17. drea 


pannosus, Mapa manian Dakota Fm. of Minnesota, showing very rudimentary he flanking the sulcus, 
ian Dako 


18. Vi 


wing iib sacci 
Granabivesiculites Sp., same 


о , scannin, icuus, 
with Figure 20 of алымсынган sp., х9,460.— 22. V. consp! 


, Minnesota, showing sulcus (trans 
tured | in Fig. 31) Be species is similar to many of the saccate forms P 
ian Fm. of Minneso 2650.20. 
ulcus Similar to the grain pi in Figure 14; я. f exin? 
: ing n micrography showing deta P а. | 
pturing of roe a ека conspicuus (Fig. 21), a showing | 
m. of Minne electron microgra same – 


grain as in Figure 21, scanning electron micrograph showing sulcus and exine sculpturing, х1, 


1984] 


ZAVADA— FOSSIL POLLEN 


456 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


чили — у= د‎ 


———— 


1984] 


CLAVATIPOLLENITES SPP., LOWER CRETACEOUS 
(BARREMIAN-CENOMANIAN) 


This form genus appears to encompass a di- 
verse array of taxa (Walker & Walker, 1984). 
Pollen is monosulcate to ulceroid, and ovoid to 
spherical. Exine puto is reticulate. Pollen 


Walker (1984). Pollen wall structure is tectate- 
columellate with a homogeneous footlayer. In 
the apertural region the footlayer appears la- 
mellated and is underlain by an endexine (nexine 
2) that exhibits | endosculpturing. РОМЫ me 


ing fossilization. Endexines of сат taxa, es- 
pecially when interbedded with intine, exhibit 
corrosion upon treatment with acetolysis solu- 
поп (e.g., ‚ Helleborus, Echlin & Godwin, 1969; 


ins. 
vatipollenites shares many character states with 
pollen of the Chloranthaceae (Kuprianova, 1981; 
Walker & Walker, 1984). 


RETIMONOCOLPITES PERORETICULATUS, 
LOWER CRETACEOUS (APTIAN) 


| This widespread and diverse form was inves- 


cture consists of a thick homogeneous i inner 
ayer, рч. which is underlain in the aper- 

n by a thin endexine (nexine 2). The 
sculptured outer layer of the wall forming the 
reticulum is attached directly to the footlayer 


ZAVADA— FOSSIL POLLEN 


457 


with no apparent infrastructural layer. The pres- 
ence of an endexine suggests that this form is 
angiospermous, however, the unusual direct at- 
tachment of the wall layer comprising the retic- 
ulum is unknown in extant angiosperms (Doyle 
et al., 1975; Walker & Walker, 1984). 


STELLATOPOLLIS SPP., ALBIAN-CENOMANIAN 


This form has been investigated using SEM 
and TEM by Doyle et al. (1975) and Walker and 
Walker (1984). Pollen is monosulcate and ellip- 
tical to subcircular; exine sculpturing is semitec- 
tate, reticulate, with the muri of the reticulum 
bearing supratectal projections, triangular to el- 
liptical in surface view. Pollen wall structure con- 
sists of a thick inner footlayer (nexine 1), believed 
to be underlain 


columellate infrastructure. The p 
exine (nexine 2) and the не infrastruc- 
ture suggests that this form is angiospermous. 


LILIACIDITES SPP. 
(MONOCOTYLEDONOUS POLLEN TYPES), 
APTIAN/ALBIAN-UPPER CRETACEOUS 


т. s :1 += я 4z PSUEY EN 


the pres- 
ent study from the Cenomanian of Kansas were 
studied by Doyle (1973) and Walker and Walker 
(1984) using SEM and TEM, respectively. Pollen 
is predominantly monosulcate, but serial sec- 
tions of single pollen grains investigated in this 
study have shown them to be inaperturate (Figs. 
33-35). Pollen is elliptical, large, averaging 36 
um along its long axis, and is invariably folded, 
giving the impression that an aperture is present 
(Fig. 32). The exine is reticulate, and the retic- 
ulum becomes finer toward opposite ends of the 


B 

— 

T Ficures 23-27. Transmission — micrograph of fossil saccate pollen.— 23. Bisaccate оез from the 
riassic Chinle me grain in Fig. 10). Transmission electron micrograph of the us showing 


thin fi PU MM 
ootlayer (nexine 1), granular infrstructum and thin t 


ectum, х x11, 00. - -24. "Granabivescultes inchoatus, 


шел 


same grain Ee 13,t 
1), gran d in Figure 1 
impie separation of 

13 the foo 


ctural layer and thick occasionally perforate tectu: 
ootlayer and the outer wall layers, x 6,060.— 
. Transmission electron micrograph showing details of the 


m. Note a sacci do not result from a a 
25. G. inchoatus, same grain pictured in 
wall structure, note that some 

24,150.— 26. Granabivesiculites Sp., Мауи 


по in Figures 14 and 27. Transmission electron micrograp showing Пеп w киш 
mine шм region, X. x 24,150.—27. Granabivesiculites sp., same grain к= in Figures 14 an б Tan 
ы оп electron п micrograph showing a sa ow) which results from separation of the e нала na D 


p 
and the outer portion of the wall, and "еа the sulcus (5), х 12,500. 


458 ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL. 71 


mi- 
FIGURES 28-31. Transmission с micrograph of fossil saccate pollen.— 28. Transmission ue the 
crograph of vestigial saccate pollen me grain pictured in Fig. 16), showing sulcus, separatio х1 000 = E 
Satie (nexine 1), and outer wall layers (arrows) resulting in the sac wid th e granular i infras tructure, > 
29. Punctamultivesiculites inchoatus me 


grain pi igure 15,t 
ОНЕ € the Biswas 


owing 
nspicuus aph sho endexine ^ 
structure; thick footlayer inii 1), which is underlain bya thin, калд леша зага у ар y 
granular infrastructural layer and thick tectum, x 29,000. 


ий. 4 J"——! ———— 


) 


1984] ZAVADA —FOSSIL POLLEN 


FIGURES 32-35. 
ticulu 


4 mes finer toward the 
to 1 aph of serial sections of the same 
ayer, а columellate layer, and a relatively thick tectum. Note 


Sulcus (arrows there is no modification of the exine, thus is inape 


micrograph of the same grain pictured in F 


32. Monocotyledonoid pollen grain from the Cenomanian Dakota 
polar areas and appears to be monosulcate, x 400. — 
in Figure 32. 


459 


D 
+ “ee d a 
k H 
A 
9 


Fm. of Kansas. Note the 
33-35. Transmission 
The wall structure consists of a very thin 


i : igure 32. 
isolated islands of sporopollenin (arrows), columellae, х 10,600. 


Pollen grain (Fig. 32), a characteristic of some 
monocotyledonous pollen. Pollen wall structure 
Consists of a ДАТ 3c 7X a ^ 12: 
ha dev 33-36). The columellae are not fused 
ali е thin footlayer, a feature observed in some 
‘sMatidean taxa. This form exhibits many 
or 10с01у1еіопоцѕ features, however, the lack 
а sulcus makes the combination of features 
туей in this taxon unique among primitive 
monocotyledons. 


ec- 


DISCUSSION 


It has already been demonstrated that, based 


len, however, indicates that the clear demarca- 

tion in pollen wall structure between extant 
d angi b his cri- 

Bye Р 3 : 

terion doesn't exist among the Mesozoic taxa. 


o r 


460 


The columellate wall structure occurs among 
esozoic dispersed pollen known to be associ- 
ated with normen: megafossils. For mam- 
ple, the T 
leana clearly exhibits the angiospermous 
columellate "idee ausis This pollen type is as- 
sociated with the gymnosperm fructification 
ин clathratus (Ash, 1972). Two oth- 
er form genera, Classopollis (Pettitt & Chaloner, 
1964) and Eucommiidites (E. sp. 1 of Trevisan, 
1980; present study) also have columellate in- 
frastructure and both are associated with gym- 
nospermous megafossils (e.g., Cheirolepis muen- 
steri, Harris, 1957 and Hastystrobus тишти, 
Konijnenburg-van Cittert, 1971, respectively). 
us, the use of the columellate infrastructure 
to determine taxonomic affinities of fossil-dis- 
persed pollen breaks down when the dimension 
of time is involved. Endexine (nexine 2) is thought 
to be an SIVE angiosperm бише skoet 
tunately, it has а 
ically equivalent wall ‘layer in. Ginkgo biloba 
(Rohn, 1977), in addition, it is a derived feature 
and not likely to be found in early angiosperm 
pollen and has a tendency to corrode (see above). 
Despite difficulties in determining the taxo- 
nomic position of fossil- dispersed pollen, there 
are a few significant aspects ofthe disp ossil 
pollen record. First, the temporal occurrences of 
presumably primitive pollen wall characteristics 
based on neontological studies, precede the first 
occurrences of derived wall characteristics. This 


morphological studies of extant pollen (e.g., 
Wale Аа, 1974b, 1976) Secondly, the oc- 


tural features prior to the alleged Lower Сге 
ceous origin of the angiosperms, suggests the 
selective pressures important to the derivation 
of angiospermous pollen features may also have 
acted on earlier Mesozoic gymnosperms. 
Comparative morphological studies of extant 
pollen have shown the granular or atectate wall 
structure to be most primitive (Walker, 1976). 
The first occurrence of this wall structural type 
is in the Permian and is exemplified by the form 
genera Praecolpatites and Marsupipollenites 
(Foster & Price, 1982) and the early Mesozoic 
genera Monosulcites and Eucommiidites (E. sp. 
2 of Trevisan, 1980; Doyle et al. , 1975). All these 
genera are presumably gymnosperms or have 
been associated with gymnosperm fructifications 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


(Foster & Price, 1980; Taylor, 1973; Doyle etal., 


— 
0 


Although the granular wall structure is known 
from some extant nonsaccate gymnosperms, it 
has not been observed in extant saccate pollen. 
The appearance of the granular wall structure in 
Triassic to Cretaceous saccate pollen, contem- 
poraneously with endoreticulate saccate pollen, 

especially interesting. Among the gran 
walled saccate pollen types we also note a Trias- 
sic-Cretaceous trend in the reduction of the size 
of the sacci. This trend may have culminated in 
the loss of sacci altogether in some Jurassic/Cre- 
taceous taxa. For example, the Jurassic/Creta- 
ceous form genus Verrumonocolpites, aside from 
lacking sacci, is similar in every respect to the 
granular walled saccate pollen. Its morphology 
and wall structure is also similar to pollen in the 
extant Magnoliaceae and Annonaceae (e.g., the 
annonaceous taxon Miscogyne ellistianum, 
Walker, 1976). Another significant aspect is that 
most HEE that are leading contendat 
Caytona mit As a result, it is reasonable 10 
assume that the transition to angiospermy in- 
cluded the reduction of the sacci. Even though 
little is known about the wall structure of fossil 
saccate gymnosperms, it is also reasonable to 
assume that this transition is accompanied by а 
change from the endoreticulate to the primitive 
granular or atectate angiosperm wall structure. 


Such a a change i in wall structure is s assumed k 
(881 


— 
n 


© 


canca 


thus far studied have endoreticulate wall struc- 

ture. However, the presence of saccate granular- 

walled pollen in the fossil record prior to the first 

unequivocal angiosperm pollen makes the 520 

cate-nonsaccate transition conceptually more 

palatable. Thus, by the Permo-Triassic, me gu 
ular 


of morphologically divae dispersed pollen gen 
era that persisted through the Jurassic and Lower 
Cretaceous. | U 
The next major palynological event 15 the ni 
per Triassic appearance of the columellate in 4 
structure in the form genera Equisetoporites е" 
Classopollis (Chaloner, 1976). The ар frst 
of the columellate structure post-dates the a 
appearance of the granular types. Although 


еаг- 
ee relationship of these taxa to pe 


У ДИМА 


the 
ен the latter temporal occurrence of 
columellate infrastructure parallels the progres 


——— 


—-— 


>" 


——— =" а —— 


— aiE 


1984] 


sion of evolutionary events proposed for pollen 
evolution by Walker (1976). However, the phy- 
logenetic relationships of the granular and col- 
umellate wall structure is substantiated by the 
occurrence of the granular and somewhat colu- 
mellate structures found in a few species of Eu- 
commiidites (such structures also coincidentally 
occur in some extant families, e.g., Annonaceae, 
Le Thomas, 1981). All of these dispersed pollen 
taxa are associated with gymnosperm megafos- 
sils and none are considered ancestral to the an- 
giosperms. This suggests that the selective pres- 


tually 21057 y were 
In operation as early, or earlier, than the Upper 
Triassic. The appearance of the angiosperm-like 
wall structure takes place during the Upper 
Permian (represented by granular-walled pollen), 
then the columellate type appears subsequently 
in the Upper Triassic. These palynological events 
appear to have occurred in a number of form 
genera, which may not be closely related. A shift 
toward more angiospermous features among 
8ymnosperms during the early Mesozoic is also 
born out by the megafossil record (e.g., Sanmi- 
guelia, Caytonia). However, one aspect of the 
Pre-Cretaceous occurrences of angiospermous 
features in gymnosperms is that we never find 
an array of primitive angiosperm features oc- 
curring concomitantly. In many instances the an- 
B&ospermous features appear to be isolated de- 
velopments or occur with features that are 
Considered advanced. Even the most angio- 
Sperm-like pre-Cretaceous pollen, Equisetopor- 
“es, is tectate-columellate with a thin footlayer, 
and lacks a sulcus. The grooves in this pollen 
Could be interpreted as apertures, in which case 
it would be called multiaperturate, but in either 
4 these characteristics аге thought to be in- 

Сапуе of the more advanced columellate an- 
Bosperm pollen and would not be expected to 
Occur in the fircs + tate 1 Md. am E pollen. 
taceous taxon Classopollis also ex- 


The рге-С 


hibits а nnl 


оик 
usual apertural arrangement and other exinal 
elaborations not 


кее ыз forms, ie., Retimonocolpites, Cla- 
*nites, and Liliacidites, that we see the 

t number of coincident angiosperm fea- 
ures Occurring in combinations expected of an- 
Bosperm pollen. But, even among these earliest 
s, Blosperm pollen grains, there are notable dif- 
erences between their morphology and our 


ZAVADA —FOSSIL POLLEN 


461 


concept of the morphologically primitive an- 
giosperm pollen as based on comparative 
morphological studies of extant pollen. Reti- 
monocolpites peroreticulatus, for example, is 
similar to many reticulate, monosulcate angio- 
sperm pollen types but lacks a columellate in- 
frastructure, a binati fc} teristi 

known in extant angiosperms (Doyle et al., 1975). 
Liliacidites (present study), thought to represent 
an early monocotyledon, exhibits some mono- 


one exclusively angiosperm morphological fea- 
ture, and the scattered occurrences of pre-Cre- 
taceous angiosperm features (and in some cases 
features that are presumably advanced among 
angiosperms) in a few apparently unrelated form 
genera makes is difficult to speculate on the role 


organs. This is the basis on which the Lower 
Cretaceous origin of angiosperms is widely ac- 
cepted. The occurrence of angiospermous pollen 
and leaves, and their subsequent persistence, 
tends to support the Lower Cretaceous origin 
(Doyle & Hickey, 1976). The acceptance of pre- 
Cretaceous occurrences of plant organs with an- 
giospermous features (e.g., Sanmiguelia, Equi- 
setoporites) awaits their association with other 
plant organs exhibiting angiospermous features, 
thus, mutually validating their identification as 
an angiosperm. 

The broad definition of angiospermy that is 
currently adhered to involves characteristics of 


+: 
WIC SUD- 


= 4 


1: у Ран 


Тћезе 


su о —— 3 
selective pressures, however, were not necessar- 


ily contemporaneous in effect, or interrelated. 
TI +h x 14 yz Ф г 1 а ~ 


acquisition of the wide range of features we use 
to define angiospermy seems unlikely. It is more 
likely that angiospermy was achieved by the cu- 
mulative acquisition of angiospermous features 


we currently use to define angiospermy. As Ste 

bins (1981) has suggested, the initial radiation 
and continuing success of angiosperms is due to 
the cumulative effect of a number of indepen- 


462 


dently derived advantageous angiosperm fea- 
tures that involve pollination biology; seed de- 
velopment, morphology and dispersal; vegetative 
anatomy and morphology; and biochemistry. 


angiosperms, seems more related to our broad 
definition of angiospermy and in some respects 
to our deep-seated hypothetical notions that have 
prevailed in past years, than to major inadequa- 
cies of the fossil record. Undoubtedly, further 
palynological investigations of dispersed pollen 
will lead us to the most likely angiosperm ances- 
tor(s) and possibly into pre-Cretaceous sedi- 
ments, but our own definition of angiospermy 
seems to relegate the further elucidation of an- 
giosperm origins to a concerted effort by paleo- 
botanists and palynologists. 


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lasso, pollis 


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CORNET, T 1979. tract:] Angiosperm-like pollen 
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DAUGHERTY, L. J. 1 41. Тһе Оррег Тгіаѕѕіс Pe of 
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Doy te, J. A. 1973. The Мама their evo- 

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E J. H ICKEY. 1976. Pollen = мн from 

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Есним, P. & Н. GODWIN. 1969. The ultrastructure 


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| 
| 


| 
| 


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PRAGLOwSKI, J. 1974. World Pollen and Spore Flora 
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· 1968. Etude de l'ultrastructure des apertures. 
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^  — 1981. Why аге те so many species of flow- 

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ZAVADA, M. S. dien p morphology of 
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=21. 


ULTRASTRUCTURE OF LOWER CRETACEOUS 
ANGIOSPERM POLLEN AND THE ORIGIN 
AND EARLY EVOLUTION OF 
FLOWERING PLANTS! 


JAMES W. WALKER AND AUDREY G. WALKER2 


ABSTRACT 


In the last d d ifi t formation has been i dab tth evolut uon of flowe ing 
plants through studies of Early Coetacadies angiosperm | pollen and the mi te of living primitive 
flowering plants. Although most recent palynological studies of extant primitive angiosperms have 
used both scanning and transmission electron microscopy, few ultrastructural studies of early fossil 


re seed hughesii, t two aff. Clavatipollenites exem ЕК erm Stephanocolpites 

fredericksburgensis, Retimonocolpites dividuus, R. peroreticulatus, two aff. Ret colpi 5 speci 

Stellatopollis Hake на пп, and three species of Liliacidites These rii were нне using a 
nig : А 


dL А 


ob безу та xists irit ges some Early Cre taceoi огрев 

and pollen мабла br certain ees pri rimitive angiosperms. Clavatipoliénites hughes, gn 

asteroides, pat Stephanocolpites fredericksburgensis exhibit у varying degrees 

structural level respectively to pollen of the extant angiosperm genera Ascarina, Hedyosmum, 7s 
i d un 


extent. pens monosulcate itn grains with distinctive crotonoid vien din described as 
Порой, barghoornii have no counterpart among the pollen of extant angios 

he question of the origin and early evolution of the angiosperms is dealt with i in ins second part 

of the paper, and the fossil pollen record of early flowering reh is considered in light of what is 

known about pollen evoluti Analysis of the taxonomic distribution 

of characters ba Бф primitive angiosperms suggests that angiosperm pollen is primitively €— 

, large- to medium-sized, psilate or at best only weakly sculptured, noninterstitiate 


oli 
cluded that Clavatipollenites and other currently known types of Early Cretaceous angiosperm рой 
grains represent relatively advanced р е angios Пеп that is alrea 


d 
giosperms is considered. Des conclusion is drawn that the ancestory of the angiosperms must be 
sought in e p terido osperms or in a derivative group. А 5-stage model of early angiosperm evolution 
is proposed, base 
eee and the е кы r MM of living primitive angiosperms. From ап о 4 
re-Barremian basal complex of en mophilous flowering plants, whose living descendants d 
such angiosperms as the Magnoliales, Laurales, and Win terales, | we e envision evolution ofa major. 


advanced magnoliid angiosperms, ‹ uch as the Chl th 4 | папом 
angiosperms, such as the Тесс аме Cercidiphyllales, and Hamamelidales. The evolution 9 


" We thank С. J. Brenner eed University of New York, New Paltz), B. Cornet, R. W. Hedlund An 
Production Company, Tulsa), and R. R. Jordan (Director, Delaware Geological Survey) for proviene This 
outcrop, and prepared palynological samples from which pollen s used in this study were obtain 
work was supported by NSF Grants DEB 79-04213, DEB 80-10893, and DEB 82-09195. The scanning € 
microscope used was purchased in part with funds from NSF Grant BMS 75-02883. 

: Departsient of Botany, University of Манасы. Amherst, Massachusetts 01003. 


ANN. Missouri Вот. Garp. 71: 464—521. 1984. 


ow о E eal 


ori il 


1984] 


WALKER & WALKER —LOWER CRETACEOUS POLLEN 


465 


wind-pollination so early within the angiosperms may have been connected with the increasing aridity 
arance of C. 


returned to entomophily. 


Palynology has rapidly become an important 
source of taxonomic and phylogenetic informa- 
tion for angiosperm systematics, and, indeed, few 
other fields of botanical inquiry provide so much 
systematic data from so little material (cf. Walker 
& Doyle, 1975). In the last decade, for example, 
significant new insight has been gained into the 
early evolution of flowering plants through in- 
vestigations of early fossil angiosperm pollen 
(Brenner, 1967, 1976; Doyle, 1969, 1970, 1973, 
1977a, 1977b, 1978a, 1978b; Doyle et al., 1977; 
Doyle & Hickey, 1976; Doyle et al., 1982; Doyle 
& Robbins, 1977; Doyle et al., 1975; Hickey & 
Doyle, 1977; Hughes, 1976, 1977; Hughes et al., 
1979; Kemp, 1968; Laing, 1976; Muller, 1970, 
1981; Walker et al., 1983), as well as from studies 
ofthe pollen of extant primitive flowering plants 
(Le Thomas, 1980, 1981; Le Thomas & Lugar- 
don, 1974, 1976a, 1976b; Lugardon & Le Thom- 
as, 1974; Praglowski, 1974a, 1974b, 1976, 1979; 
Walker, 1971a, 1971b, 1971c, 1972a, 1972b, 
1974a, 1974b, 1976a, 1976b, 1979; Walker & 
Doyle, 1975; Walker & Skvarla, 1975; Walker 
& Walker, 1979, 1980, 1981, 1983). 

Although most recent palynological investi- 
gations of livi imiti i have used 

1 2 à 


eor = r 
E + £ lartran 


microscopy, few ultrastructural studies of Early 
Cretaceous angiosperm pollen grains exist (e.g., 
Davies & Norris, 1976; Doyle et al., 1975; Hughes 
et al., 1979). Moreover, most workers have em- 
Ployed scanning electron microscopy (SEM) 
alone, and few (e.g., Doyle et al., 1975) have used 
transmission electron microscopy (TEM) as well. 
This I$ no doubt due to the difficulties inherent 
їп examining dispersed fossil pollen grains wit 

electron microscopy, and by TEM in particular. 
For this reason we have begun an ultrastructural 
investigation of Early Cretaceous angiosperm 
a en, using a technique that we have developed 
ОГ working with single fossil pollen grains by 
Which we are able to undertake light, scanning 
electron, and transmission electron microscopy 
ke the same pollen grain. The purpose of this 
paper 15 to discuss the results and evolutionary 
Implications of a preliminary study of Lower 


derived anemophilous 


rms, and, thus, most of the dicots probably represent flowering plants that have secondarily 


Cretaceous angiosperm pollen from the Potomac 
Group of eastern North America and the Fred- 
ericksburgian of Oklahoma, using this technique. 


ULTRASTRUCTURAL STUDY OF LOWER 
CRETACEOUS ANGIOSPERM POLLEN 


Our initial study of Early Cretaceous angio- 
sperm pollen has centered mainly on the Poto- 
mac Group of the Atlantic Coastal Plain of east- 
ern North America. We chose the Potomac Group 
for a detailed investigation for several reasons. 
First, much of the important light-microscope- 
based evolutionary studies of early fossil angio- 
sperm pollen (e.g., Brenner, 1967; Doyle, 1969, 
1970, 1977a, 1977b; Doyle & Hickey, 1976; 
Doyle & Robbins, 1977; Hickey & Doyle, 1977) 
are based on the pollen of the Potomac Group. 
Second, Potomac Group pollen is especially well 
preserved, not only at the light microscope level 
(cf. Brenner, 1963), but also ultrastructurally. 
Third, we have been able to acquire numerous 
Potomac Group rock samples, the most impor- 
tant of which are more than 50 closely spaced 
core samples from two shallow wells drilled 
through the Potomac Group near Delaware City, 
Delaware, which were kindly provided by Dr. 
Robert R. Jordan, Director of the Delaware Geo- 
logical Survey (see Doyle & Robbins, 1977, for 
a detailed light microscope study of angiosperm 
pollen from these two Delaware wells). In ad- 
dition to Potomac Group pollen, we have also 
examined pollen grains isolated from prepared 
samples taken from the Fredericksburgian (АІ- 
bian) of Oklahoma. These samples, which were 
kindly provided by Dr. R. W. Hedlund, are im- 

rtant because they are the same samples from 
which the type specimens of both Asteropollis 
Hedlund & Norris and Stephanocolpites freder- 
icksburgensis Hedlund & Norris were obtained. 

The Potomac Group (Table 1) dates from about 
the Late Barremian-Early Aptian through the 
Early Cenomanian according to Doyle and Rob- 
bins (1977), and consists of four formations— 
the Patuxent, Arundel Clay, Patapsco, and Elk 
Neck Beds (or “Maryland Raritan”). The Late 


466 


TABLE 1. 
stages in Ma, after van Eysinga, 1978.) 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


Stratigraphy of the Potomac Group, based on Doyle and Robbins (1977). (Boundaries between 
8 


SERIES STAGE SUBSTAGE || FORMATION ||7 ОМЕ | SUBZONE 
Upper Р upper Upper 
Cretaceous беленин | Lowi ATE Elk Neck Beds ТЧ 
(100 m.y.) lower Lower 
("Maryland 
upper Raritan") C 
Upper 
lower upper 
II 
Albian iddle 
ce Patapsco B. 
мане arise oUm lower 
T _ |: масш e 
Were lower A 
(109 my.) Lower 
Arundel Upper 
Cretaceous Upper Clay 
Aptian r 
Lower 
к. I 
(114 m.y.) 
Patuxent Er 
Formation 
Barremian 
(18 m.y.) 


Barremian to Early Cenomanian represents a time 
span of approximately 18 Ma from about 116— 
98 Ma, following van Eysinga (1978). The Po- 
tomac Group has been divided into three major 
zones based on pollen and spore types (Brenner, 
1963; Doyle, 1970, 1977a; Doyle & Robbins, 
1977). Zone I (from ? Upper Barremian through 
Lower Albian) is characterized by monosulcate 
angiosperm pollen, Zone II (Middle and Upper 
Albian) is characterized by tricolpate to tricol- 
poroidate angiosperm pollen, and Zone II (Low- 
er Cenomanian) is characterized by tricolporate 
angiosperm pollen that is frequently triangular 
in equatorial outline. Triporate Normapolles en- 
ter above Zone III in the Middle Cenomanian. 
The most detailed palyno-zonation of the Po- 


tomac Group is that of Doyle and Robbins asi’ 
who recognized subzones as well, dividing 20 a 
I and III into lower and upper subzones, ei 
Zone II into subzones ПА, IIB, and me 
discussion of the geological setting “ um e 
e sere а — " palsopely um of Brenne! 
the reader the pape! í 
(1963), Doyle (19772), Doyle and Hickey ( 4 ) 
Doyle and Robbins (1977), Hickey and 


tti- 
attempt investigation of the more advanced и 
colpate and tricolpate-derived pollen ty ar dif- 


pollen grains we have studied fall into 


— 


— 


— 


A mgm ag 


—_ 


—— _ ы 


1984] 


ferent currently recognized form genera: Clava- 
tipollenites, Asteropollis, Stephanocolpites, Reti- 
monocolpites, Stellatopollis, and Liliacidites. 


MATERIALS 


Lower Cretaceous pollen grains examined in 
this study were obtained from outcrop and core 
samples (Potomac Group zonation follows Doyle 
& Robbins, 1977): 

(1) Cleaves 27: E. T. Cleaves (1968) sample 
no. 27, outcrop sample from the undifferentiated 
Potomac Formation, Maryland; Lower Zone I of 
the Potomac Group fide Doyle et al. (1975), Bar- 
remian-Lower Aptian (ca. 115 Ma old). 

(2) Brenner 10: G. J. Brenner (1963) station 
no. 10, outcrop sample from the Arundel Clay, 
Maryland; Upper Zone I of the Potomac Group, 
Upper Aptian-Lower Albian (ca. 110 Ma old). 

(3) Cornet Beltway: B. Cornet outcrop sample 
from Rt. 495 (Beltway), Exit 25, Maryland; Zone 
IIB of the Potomac Group fide Cornet, Middle- 
Upper Albian (ca. 105 Ma old). 

(4) Hedlund 3916: R. W. Hedlund collection 
3916 cited in Hedlund and Norris (1968), out- 
crop sample from the Fredericksburgian of Okla- 
homa; correlative with Middle Zone IIB of the 

otomac Group fide Doyle and Robbins (1977), 
upper Middle Albian (ca. 105 Ma old). 

(5) D12-515: Tidewater Oil Company well 
D12 (Delaware Geological Survey no. Dc53-7), 


near Delaware City, Delaware, core sample from 
51 8 fant Thi ~ 1 é éin 


20083); Widile Zan. Bog vey sampe no. 
› of the Potomac Group 
fide Doyle and Robbins (1977), upper Middle 
Albian (ca. 105 Ma old). 

(6) D13-535: Tidewater Oil Company well 
D13 (Delaware Geological Survey no. Ес14-1), 
pind Delaware City, Delaware, core sample from 

( are gi vey sample no. 
ЖАЗ, Upper Zone IIB of the Potomac Group 
a Doyle and Robbins (1977), lower Upper Al- 
ian (ca. 103 Ma old). 
numbers in text and figure legends are 
Palynological accession numbers given to each 
plant collection from which modern pollen was 
obtained. “Ер” numbers represent fossil paly- 
nomorph accession numbers given to every in- 
dividual fossil palynomorph isolated. 


METHODS 

PP dae we initially began this investigation of 
e fossil angiosperm pollen our sole interest 
In studying the ultrastructure of the pollen 


WALKER & WALKER—LOWER CRETACEOUS POLLEN 


467 


grains we examined. However, since most of the 
literature and almost all the nomenclature of dis- 
persed fossil pollen and spores is based on light 
microscope studies alone, it was soon apparent 
that it would also be highly desirable to have 
photomicrographs of the same pollen grains that 
we examined with electron microscopy. More- 
over, during our palynological studies of extant 
Myristicaceae (Walker & Walker, 1979), a family 
whose pollen is similar at the light microscope 
level to some types of Lower Cretaceous angio- 


nevertheless, was always distinguishable by ex- 
ine structure when examined with the transmis- 
sion electron microscope (cf. Figs. 1-6). Thus, 
when investigating dispersed fossil pollen grains 
for taxonomic and evolutionary (as opposed to 
stratigraphic) purposes, we felt that it was highly 
advantageous to be able to undertake combined 
light, scanning electron, and transmission elec- 
tron microscopy of the same pollen grain to es- 
tablish unequivocally that one was actually deal- 
ing with pollen produced by one and the same 
biological entity. To this end we developed a 
technique that allows us to obtain photomicro- 

phs (PMG), scanning electron micrographs 
(SEMG), and transmission electron micrographs 
(TEMG) of the same individual pollen grain. We 
believe that this technique is a virtual necessity 
for the evolutionary study of small, light-micro- 
scopically similar, dispersed fossil pollen grains 
such as those that constitute most of the earliest 
known part of the fossil record of the flowering 
plants. 

Our technique for working with single fossil 
pollen grains is as follows. Fossil pollen was ex- 
tracted from Potomac Group outcrop and core 
samples using a slightly modified version of the 
sample preparation outlined by Brenner (1963). 
Rock samples are first crushed in distilled water 
with a mortar and pestle. The disaggregated ma- 
terial is then centrifuged and ZnCl heavy liquid 
solution (specific gravity 2) is used to separate 
organic from inorganic matter by flotation. The 
float is pipetted off, and a few drops of 10% НСІ 
are added to prevent zinc hydroxide precipita- 
tion. The sample is then washed twice with dis- 
tilled water, and, after centrifugation, HF is added 
to remove clay particles. After washing and fur- 
ther centrifugation, the sample is oxidized briefly 
(2-3 minutes) with a 5.25% solution of sodium 


468 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Мог. 71 


: —2. Exine 
FIGURES 1-6. Myristicaceae. 1-3. Compsoneura. 4—6. Virola.—1. Whole grain SEMG, x2 = 360.- 
surface SEMG, x 12,000. —3. Nonapertural exine section TEMG, х15,100.—4. Whole grain SEMG, х2, 
pe 


5), pollen of the two closely related genera can g y by ine, while 
in TEMG (cf. Figs. 3 & 6). Pollen of Compsoneura (Fig. 3) has a relatively thick, non-lamellate nexin ies 
pollen of Virola (Fig. 6) is characterized by a very thin, finely lamellate nexine. In addition, pollen r pollen 
Virola (Fig. 6) have conspicuous, spherical, intra-exinous cavities within the sexine that are lacking in t 

of Compsoneura (Fig. 3). 


is 
hypochlorite. This is followed by another wash gave excellent results, and have adopted па 
cycle and treatment with 10% NH,OH for three modification since we consider it highly wa pre 
minutes. Finally, the material is washed again, for ultrastructural studies to have as gentle 
and the pollen/spore samples are stored in glyc-  paratory process as possible. grains 
erin-water. We found that a shorter period of In order to get single angiosperm pollen de on 
oxidation than the 20 minutes used by Brenner {ог study, open glycerin spreads are та 


1984] 


= | 4n. A 


that have had their pollen extracted and prepared 
as outlined above. These slides are then carefully 
scanned under low power (160-200 x) of a light 
microscope and individual pollen grains are 
picked out with an eyelash attached to a wooden 


isgiven its own “FP” (fossil palynomorph) acces- 
sion number. Isolation of angiosperm pollen 
grains from gymnosperm pollen as well as spores 
may take considerable time since in some Po- 
tomac Group samples angiosperm pollen makes 
up less than 1% of the total pollen grains and 
spores present. 

Each grain is then photographed under a Leitz 
NPL Fluotar 100 x oil immersion objective with 
a Leitz Dialux 20 brightfield light microscope 
and a Leitz Vario Orthomat camera, using Ko- 
dak High Contrast Copy Film or Kodak Tech- 
nical Pan Film 2415. Following photomicros- 
copy, the cover slip is removed from the original 
slide and the pollen grain is transferred to a clean 
microscope slide and washed with 70% ethanol 
several times using a micropipette to remove the 
glycerin. The washed pollen grain is then placed 
on an SEM specimen holder and sputter-coated 
with gold-palladium for about three minutes. Af- 
ter scanning electron micrographs of one side of 
the grain are taken with a JEOL JSM-35 SEM 
using Polaroid Type 665 positive/negative film 
(with 0° tilt and an accelerating voltage of 30 kV), 
70% ethanol is used to loosen the grain, and it 
5 turned over with an eyelash under a light mi- 
Nera The grain is then re-coated in the sput- 

Oater and i ide i i 
Pip cog d its other side is photographed with 


After scanning electron microscopy has been 
completed, the grain is treated with dilute aqua 
= to remove the heavy metal coating. This is 
Ren by Preparation for transmission elec- 

microscopy. First, the grain is placed in agar 

a tas in а 1% aqueous solution of OsO, for 
ours at room temperature. Then, it is washed 

four times with distilled water bloc stained 
ке aqueous solution of uranyl acetate 
e га hours at room temperature. After wash- 
am е times with distilled water, the grain is 
in : rated In an acetone series and embedded 
чк 5 low viscosity embedding medium, 
15 Cured in an oven at 70°C for 12 hours. 

= block containing the single pollen grain is 
a down to the grain itself (one of the most 
t parts of the entire procedure) and the 


4 


WALKER & WALKER—LOWER CRETACEOUS POLLEN 


469 


grain is then sectioned with a Reichert ultrami- 
crotome using a Dupont diamond knife. The sec- 
tions are picked up on formvar-coated, single- 
slot grids, and then stained in 1% KMnO, fol- 
lowed by Reynold's lead citrate. The sections are 
then examined and photographed with a Zeiss 
9A transmission electron microscope, using Ko- 
dak Electron Image Film 4463. Prints were made 
on Agfa Brovira paper with Omega Pro-Lab 4 x 
5 standard and point-source enlargers equipped 
with Schneider Componon-S lenses. 


POLLEN WALL ARCHITECTURE 
AND STRATIFICATION 


While palynological characters such as aper- 
ture type, pollen shape, and pollen size can be 


(LM) alone, g elect 
andt issi 1 microscopy (ТЕМ) аге 
required to obtain a thorough understanding of 
the morphology of the pollen wall itself. Since 

pt dt inology dealing with the pollen 
wall are considerably varied, basic features of 
pollen wall morphology will be briefly outlined 
at this point to provide a general background for 
our ultrastructural study of Lower Cretaceous 
angiosperm pollen. 

As with plant cells in general, the living pro- 
toplast of each pollen grain is surrounded by a 
predominantly cellulosic cell wall layer, which 
in pollen is known as the intine. Pollen grains, 
however, have an additional wall layer external 
to the intine that is known as the exine. The 
exine, unlike the cellulosic intine, is made-up of 
sporopollenin, which is a highly chemically and 
biologically resistant material consisting of ca- 
rotenoid polymers (Shaw, 1971). The exine rep- 


important part of the pollen wall since the intine 
is generally not preserved in fossil pollen and is 
usually destroyed as well during the commonly 
employed preparatory treatment used for mod- 
ern pollen known as acetolysis. Moreover, the 
exine is generally a complex layer, both exter- 
nally (sculpturally) and internally (structurally), 
whereas the intine with a few notable exceptions 
is usually simple morphologically. For these rea- 
sons the following discussion will be restricted 
to consideration of the exine alone. Exine mor- 
phology will be discussed under the following 
four headings: nonapertural exine sculpturing, 


and aperture ultrastructure. Certain aspects of 
pollen wall architecture and stratification in gen- 


470 


TABLE 2. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


Composite nonapertural pollen wall section with exine surface views at top, showing basic pollen 


wall stratification and exine structure (including major exine interstitial and tectal types). 


Exine 
EEA [O @| Structural 
< jt © @ 2 Layers 
бы D-2 D-3 
x | tectum 


; 


о 2 —- м < о 


| interstitium 


nexine 


П 
i 
1 
3 
a 
"a. 
ЕЁ 
3 32 + E 
S 8 
5L Кї! Sel ESL 
or 
ке, 
Bis 
Fa 
Ts 
! 
' 
1 
' 
[ 


Pollen Wall Strata Exine Interstitial Types Exine Tectal Types 
: e A- noninterstitiate (atectate) (1) atectate (A) 
ektexine X 
i e (2) tectate 
endexine C - granular interstitiate (а) tectate imperforate (B,C) 
D- columellate (b) tectate- perforate (0-1) 
intine 


Ж foot- layer 


semitectate (D-2) 


intectate (0-3) 


eral are summarized in Table 2, which will be - 


referred to throughout the following discussion. 

Nonapertural exine sculpturing. Nonaper- 
tural exine sculpturing refers to all external sur- 
face features of the nonapertural exine, and usu- 
ally is taken to include only features of the outer 
exine surface, although sometimes the inner sur- 
face of the exine may have important sculptural 
details as well (cf. Van Campo, 1978). Although 
it can be studied by light microscopy alone, non- 
apertural exine sculpturing, particularly in small 
pollen grains, is best observed with scanning 
electron microscopy (cf. Walker, 1972a). Pollen 
grains that are (1) psilate (smooth), (2) foveolate 
(pitted), (3) fossulate (grooved), (4) scabrate (with 
fine surface features), (5) verrucate (warty), (6) 
baculate (with rod-like elements), (7) pilate or 
clavate (with rod-like elements that have swollen 
heads), and (8) echinate (spiny) include the most 
commonly encountered types of nonapertural 
exine sculpturing. 

Pollen that is reticulate, i.e., has an open net- 
work or reticulum on the surface of its exine 
(Table 2, D-2), represents another common type 
of nonapertural exine sculpturing, and, indeed, 
atimant, lpt : и ee ae Low 


g c of all 


er Cretaceous angiosperm pollen erint e 
ined in this study. The reticulum in AU 
ullam cancict £f 11.1 with sp 
between the muri, which are designated as the 
lumina. In the Lower Cretaceous аарчы 
pollen grains examined the muri may be y" 
i.e., psilate (Fig. 89), covered with small € 
i.e., spinulose (Fig. 46), covered with pem 
і.е., granulose (Fig. 24), divided into di 2 
bead-like subunits, i.e., beaded (Fig. 21), oF СО 
ered with fine, band-like lines, i.e., banded "t 
66). In one pollen type the muri are covered oid" 
triangular elements, resulting in a € 
sculpturing pattern (Fig. 83), named after : (i 
ilar type of sculpturing found in the pollen Ee 
euphorbiaceous genus Croton. Most of the ur 
pollen types investigated have an imo ИН 
ulum with a variety of lumina sizes pe is 
(Fig. 9), but in a few instances the retic oc 
regular with either circular (Figs. 83. pe 
lygonal (Fig. 101) lumina. Sometimes eec 
pollen grain has both coarsely and a E 
ulate areas on its exine surface (Figs. 88- „phic W 
some pollen types exhibit strongly dimo ~ 


| 


| 


— 


1984] 


a few instances the muri are nodose, i.e., swollen 
at the points where the underlying columellae 
meet them (Fig. 34). 

Nonapertural exine structure. Nonapertural 
exine structure refers to all internal morpholog- 
ical features of the nonapertural exine. Although 
light microscopy can give some idea of exine 
structure, internal exine features are best ob- 
served in scanning electron and transmission 
electron micrographs of exine sections. In some 
pollen grains the nonapertural exine is morpho- 
logically uniform (Table 2, A). We designate such 
pollen as noninterstitiate (or atectate). The non- 
apertural exine of most pollen grains, however, 
is interstitiate (Table 2, B-D-2), and has an inner 
structural layer or zone that we have termed the 
interstitium (Walker & Walker, 1981). There are 
several exine interstitial types, including cavitate 
interstitia with a series of structural cavities (Ta- 

е 2, B), granular interstitia composed of gran- 
ules (Table 2, C), and columellate interstitia that 
consist of a series of upright, rod-like structural 
elements known as columellae (Table 2, D-1, 
D-2). It is the presence of an interstitium that 
allows recognition of a basal exine layer, the nex- 
Ine, and a roof-like layer, the tectum, in the typ- 
ical pollen grain (cf. Table 2). The interstitium 
plus the tectum constitutes the so-called sexine. 
The thickness of the nexine, interstitium, and 

n rt 


apertural exine in a particular pollen grain, and 
the columellae account for 3096 while the tectum 
makes up only 10% of the exine thickness, the 
Pollen grain would be described as having a very 
thick nexine, an average interstitium, and an ex- 
tremely to very thin tectum. 
Several different exine tectal types are possible 
- interstitiate pollen grains. In tectate pollen, 
Le., in Pollen that has a roof or tectum as part 
= "une, the tectum may be solid, resulting 
R lectate-imperforate exine (Table 2, B, C), or 
mall holes, i.e., tecta] perforations, may be pres- 
ent in the tectum, resulting in tectate-perforate 
Pollen (Table 2, D-1). If the tectal perforations 
are as large or larger than the remaining solid 
areas ОЁ the tectum that lie between them, the 
Pollen is semitectate (Table 2, D-2). While semi- 
“== Pollen is invariably reticulately sculp- 
а well, tectate-perforate pollen grains may 


WALKER & WALKER—LOWER CRETACEOUS POLLEN 


471 


TABLE 3. Pollen exine layers (nexine, interstitium, 
and tectum) thickness classes. 


Percent of Total 
Nonapertural Exine 


Thickness Thickness Class 
>75% extremely thick 
50-75% i 
41-49% moderately thick 
25-40% average 
15-24% moderately thin 
10-14% very thin 
<10% extremely thin 


be reticulately sculptured or not. In some pollen 
the nonapertural exine is represented simply by 
a solid basal layer and overlying sculptural ele- 
ments; such pollen may be described as intectate 
(Table 2, D-3), but this condition is rare. 

Exine stratification. Ехіпе stratification re- 
fers to chemical differences that may be evident 
in various layers or strata of the exine. Exine 
stratification is best observed in exine section 
transmission electron micrographs as layers of 
differing electron opaqueness, although basic 
fuchsin staining and light microscopy can also 
be used to reveal chemical differences in exine 
layers, even in fossil pollen grains (cf. Leffingwell 
et al., 1970). Using the methods outlined above, 
it is apparent that the exine in many pollen grains 
consists of two chemically different layers—an 
outer, generally denser layer designated the ekt- 
exine, and an inner, generally less dense layer 
known as the endexine (cf. Table 2, A, B, D). As 
a rule, chemically uniform exine appears to be 
wholly ektexinous and without endexine (Table 
2, C). In fossil pollen ektexine-endexine polarity 
is frequently reversed, with the inner endexine 
appearing denser than the outer ektexine (cf. 
Trevisan, 1980). 

Endexine may be found throughout the exine 
or it may occur only as part of the apertures. In 
gymnosperms, the endexine is generally lami- 
nated (Van Campo, 1971) with a series of parallel 

inati that ti tł hout both 


Gill 


the apertural and nonapertural regions of the 
endexine (cf. Table 2, A, B). In angiosperms, on 
the other hand, endexine is either absent entirely 
(Table 2, C) or present but non-laminated (Table 
2, D) (cf. Doyle et al., 1975). Sometimes, how- 
ever, the nexine of a wholly ektexinous, non- 
stratified exine may be lamellate. This, for ex- 
ample, is common in such primitive angiosperm 
families as the Annonaceae (Le Thomas, 1980, 


472 


1981) and Myristicaceae (Fig. 6) (Walker & 
Walker, 1979, 1980, 1981, 1983). In other in- 
stances, the endexine under apertures in angio- 
sperm pollen may be lamellate, but this type of 
lamellate endexine is generally composed of dis- 
continuous lamellae that apparently are funda- 
mentally different from the truly laminated end- 
exine of gymnosperms. When endexine is present 
in nonapertural regions of the exine, it most com- 
monly comprises only part of the nexine, 1.е., the 
morphologically defined basal layer of an inter- 
stitiate exine, and, when this is the case, the upper 
ektexinous part of the nexine is termed the foot- 
layer (Table 2, B, D-1). Rarely, is the nexine 
wholly endexinous, and a foot-layer absent (Ta- 
ble 2, D-2, D-3) 

Aperture ultrastructure. Generally, pollen 
apertures represent sculpturally (i.e., externally) 
as well as structurally (internally) distinct areas 
of the exine. Externally, apertures usually appear 
as differently sculptured areas of the exine (Figs. 
8, 13, 39, 52), while internally they commonly 
represent disorganized regions of the sexine un- 
derlaid by thinner nexine, relative to the nexine 
in nonapertural regions of the exine (Fig. 85). 
Sometimes, however, an aperture may be rep- 
resented internally only by a thinning of the nex- 
ine, and by little or no discernible disorganiza- 
tion of the overlying sexine (Fig. 91). In pollen 
grains with endexine, frequently the endexine is 
thicker under the apertures (cf. Figs. 48, 49), or 
as previously indicated, endexine may be re- 
stricted to apertural areas and absent entirely in 
the nonapertural exine (cf. Figs. 16, 17). Al- 
though the endexine in angiosperms is usually 
homogeneous (Fig. 11), sometimes it is hetero- 
geneous and stratified (Figs. 17, 43), and in some 
instances the foot-layer and endexine may be 
conspicuously interbedded (Fig. 49). 


RESULTS 
CLAVATIPOLLENITES COUPER 


The most widely discussed type of Early Cre- 
taceous angiosperm pollen consists of medium- 
sized, slightly boat-shaped to globose, monosul- 
cate pollen grains referred to under the form ge- 
nus Clavatipollenites Couper. Couper's diagnosis 
of the genus (Couper, 1958) was based on the 
type species, Clavatipollenites hughesii Couper. 
The holotype of C. hughesii comes from the 
Wealden of England and, according to Kemp 
(1968), is probably Upper Barremian in age. 
Couper described Clavatipollenites as *mono- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


sulcate, sulcus broad and long; grains broadly 
elliptical to almost spherical in equatorial con- 
tour; exine clearly stratified, consisting of an in- 
ner unsculptured layer (nexine) arising from 
which is a sculptured layer (sexine) made up of 
clavate projections, tending to expand and fuse 
together at their tips to form a tectate exine." 

In 1968, Kemp redescribed Clavatipollenites 
hughesii and published photomicrographs of ad- 
ditional pollen grains of this species, some of 
which were obtained from the same core sample 
that originally provided the holotype of C. 
hughesii. Although Clavatipollenites as originally 
described by Couper (1958) and redescribed by 
Kemp (1968) encompassed only monosulcate 
pollen, some workers, e.g., Doyle and Robbins 
(1977), have broadened the circumscription of 
the genus to include trichotomosulcate pollen 
grains as well. Pollen ofthe C/avatipollenitestype 
(at least as judged by light microscopy) is вео“ 
graphically widespread in the middle and late 
Early Cretaceous, occurring according to Doyle 
(1969) in the Barremian through Albian of West 
Africa, the Aptian and Albian of Central Amet- 
ica, the presumed pre-Albian of southern Argen- 
tina, the Albian of Australia, the Aptian and Ak 
bian of Portugal, the Barremian through Albian 
of England, the probable late Barremian through 
Albian of central Atlantic North America, and 
the Middle through Late Albian of the Cana 
Plains. 

Pollen grains from the Potomac Group that 
would be described as Clavatipollenites from light 
microscope study alone fall into two different 
groups when examined ultrastructurally. Pollen 
in the first group is the same we believe as 
type species of the genus, C. hughesii. 
group contains a diversity of pollen types 
this time we will refer to simply as the 
(= affinity) Clavatipollenites group. — fi 

Clavatipollenites hughesii. Preliminary cdi 
ies suggest that Clavatipollenites mess 


aff. 


per, i.e., pollen strictly referable to 
the genus Clavatipollenites from the з 
England, also occurs in the Potomac ee 
least in Lower Zone I, which is probably P? 
remian to Lower Aptian in age. A pol we 
that we consider to belong to C. Aughesi! 1$ MO) 
in Figures 7-11. The photomicrographs (Р 
scanning electron micrographs o: 2 
transmission electron micrographs (TEMO 
is the case with all Lower Cretaceous angio pe 
pollen included in this study, were all ob - 
from the same pollen grain. For this reason 


| 


— 


1984] 


1 1 


t whatsoever that all 
features observed in Figures 7-11 belong to: one 
and the same biological entity, irrespective of 
whether these characters were observed by means 
of light (Fig. 7), scanning electron (Figs. 8, 9), or 
transmission electron (Figs. 10, 11) microscopy. 
he conspicuous columellae, which have fre- 
quently been described as clavae by those work- 
ing with light microscopy alone, and which are 
responsible for the name та itself, 
can be clearly seen at the top right in 
Scanning electron microscopy, pecan snore 
that C. hughesii is not intectate with clavate 
sculpturing, as originally supposed by Couper 
(1958) when he described Clavatipollenites as 
“made up of clavate projections, tending to ex- 
pand and fuse together at their tips to form a 
tectate exine." It is clear Кот SEM and TEM 
examination that C. hughesii is tectate-perforate 
to semitectate (Figs. 9, 10), and not intectate. 
SEM also reveals that C. hughesii is character- 
ized by an irregular reticulum composed of bead- 
€d to spinulose muri (Fig. 9). TEM further dem- 


aperture of C. hughesii (Fig. 11), while in non- 
apertural regions endexine is absent (Fig. 10). 
The aperture of C. hughesii is externally ver- 
Tucate (Fig. 8), while internally it consists of a 
very thick, apparently ho omogeneous endexine 
and a thin, occasionally lamellate foot-layer 
overlaid by a thick sexine organized into ver- 
rucae (Fig. 11). Doyle et al. (1975), however, 
contended that C. hughesii has only low verru- 
cate apertural sculpturing, and that the promi- 
nent apertural details observed with light mi- 
croscopy (cf. Fig. 7) are at least partly internal. 
This conclusion is based on SEM and TEM study 
E pollen grains designated as Clavatipollenites 
cf. hughesii, which were isolated from the same 


scribed е endexine under the aperture of C. hugh- 
esii as “endosculptured,” and suggested that this 
internal Sculpturing is “responsible for much of 
the granular ar appearance of the sulcus membrane 
3 seen with light microscopy." Our whole grain 
EMG of С. hughesii, in which the aperture is 
= ог less fully expanded, clearly shows that 
* aperture is conspicuously verrucate (Fig. 8). 
Moreover, TEMG of this grain (Fig. 11) dem- 


WALKER & WALKER —LOWER CRETACEOUS POLLEN 


473 


onstrate that the endexine under the aperture is 
not “endosculptured,” even though light mi- 
croscopy of the same grain (Fig. 7) reveals a high- 
ly *granular" aperture. We believe that the so- 
called endosculpturing of the apertural endexine 
described by Doyle et al. (1975) was probably 
just a preservational artifact due to selective deg- 
radation of part of the endexine, and that the 
granular appearance of the aperture of C. hugh- 
esii observed in photomicrographs is due to an 
externally verrucate surface, and not to any in- 
ternal sculpturing. In this connection, it is inter- 
esting to note that a similar condition, presum- 
ably also representing differential preservation 
with the endexine uniform in some grains an 
ragged in others, was EER in Stephano- 
colpites fredericksburgensis (cf. below). 

Aff. Clavatipollenites group. os have dis- 
covered that many Potomac Group pollen grains 
that appear to be essentially the same as C. 
hughesii in the light microscope, are actually quite 
different from C. hughesii when examined ultra- 
structurally. For the present, we have chosen to 
refer to these pollen types simply as the “aff. 
Clavatipollenites group.” Two examples of this 
ype of pollen, which we have designated as aff. 
Clavatipollenites Couper spp. 1 and 2, are shown 
in Figures 18—22 and Figures 23-26, respective- 
ly. Aff. Clavatipollenites sp. 1 (Figs. 18-22) is 
trichotomosulcate, while aff. cee oe ye 
2 (Figs. 23-26) is monosulcate. Bot 
pollen are medium-sized and more or а oD. 
bose, although sometimes aff. Clavatipollenites 
sp. 2 is slightly boat-shaped. In contrast to C. 
hughesii, which has a truly spinulose reticulum, 
muri of the aff. Clavatipollenites group are fun- 
damentally beaded (Figs. 20, 21), although in aff. 
Clavatipollenites sp. 2 it appears that the bead- 
like subunits of the muri have broken-up into 
coarse, double-rowed granules (Fig. 24). In ad- 
dition, pollen of the aff. Clavatipollenites group 
on the whole seems to have somewhat larger 
теста! perforations than C. hughesii, and, there- 
fore, is basically semitectate (Figs. 18, 19, 23) 
rather than tectate-perforate (Fig. 8). While well- 
developed columellae are present in both pollen 
types, the nonapertural nexine is only average in 
thickness in pollen grains of the aff. C/avatipol- 
lenites group (Figs. 22, 26), while in C. hughesii 
it is moderately to very thick (Fig. 10). The most 
distinctive feature of the aff. Clavatipollenites 
group, however, is a lack of endexine, even under 
the aperture (Figs. 22, 25), which is markedly 
different from C. hughesii, with its well-devel- 


e 


ANNALS OF THE MISSOURI BOTANICAL GARDEN [Vor 71 


"E 
so Sl 


Potomac 
ollenites hughesii Couper (FP-364; Cleaves 27) from Lower Zone I of the 
Group, Barremian-Lower i ole grai 

80 E 


FIGURES 7-11. Clavatip SEMG. 
ptian (ca. 115 Ma).—7. Wh , X2,190.—8. Whole 11. Part of 
х 2,380.—9. Exine surface SEMG, x12,000.— 10. Nonapertural exine section TEMG, х Mies 200. 
whole grain exine section TEMG, with aperture on top and appressed non-apertural side below, X19, 


oped apertural endexine (Fig. 11). In both aff. 
Clavatipollenites sp. 1 and 2, the aperture is ev- 
ident internally, simply by a thinning of the nex- ge 
ine and disorganization of the overlying sexine. 


ASTEROPOLLIS HEDLUND & Ku e 

In 1968, Hedlund and Norris дон — d 

nus Asteropollis from the Рейне mie 
(Albian) of Oklahoma. They diagno 


1984] WALKER & WALKER—LOWER CRETACEOUS POLLEN 475 


ш FiGURES 12-17. Ascarina diffusa A. C. Smith of the Chloranthaceae (P-1091; Kajewski 863, Arnold Arbore- 

i ae — 12. Whole grain PMG, x1,880.— 13. Whole grain SEMG, х 2,150.— 14. Exine surface SEMG, х 12,000.— 

н ls hole grain exine section TEMG, with aperture at top, х 2,680.— 16. Nonapertural exine section TEMG, 
000. — 17. Apertural exine section TEMG, x11,800 


teroides, they noted that the pollen has a “sulcus 
with four or five equally developed branches al- 
most reaching the equator" and that it is colu- 
mellate and uniformly microreticulate. From a 


len of their monotypic new genus as “radiosym- 
ut oblate, with circular amb; tetra- or pen- 

Stomosulcate; heteropolar." In their 
description of the type species, Asteropollis as- 


476 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


4 с 
GURES 18-22. Aff. Clavatipollenites epee sp. 1 (FP-43; Cornet Beltway) from Zone IIB of the po 
Group, Middle- -Upper Albian (ca. 105 5 Ma 8. Whole grain SEMG, showing apertural side, х Boe 
Је, x 2,000. — 20 de, X 

21. Exine vg" SEMG on. nonapertural side, x 12,000. — 22. ith — 
at top right, x 4,820 


Whole grain exine section US. wl 


survey of 38 grains of Asteropollis, Davies and Hedlund and Norris (1968) in their origina | 
Norris (1976) found that approximately 30% were scription of the genus. Thus, Asteropollis 15 - 
tetrachotomosulcate, 5096 were pentachotomo- sically pentachotomosulcate. In addition 
sulcate, and 2096 were hexachotomosulcate. the Fredericksburgian, pollen of Asteropollis has ao 
latter condition not having been reported by found in the Potomac Group of eastern Nort 


| 


1984] WALKER & WALKER—LOWER CRETACEOUS POLLEN 477 


FIGURES 23- 
Group, Middle-U : baueri Markgraf (P-2734; Tessmann 
d -Upper Albian (ca. 105 Ma) (23-26) and Virola weberbaueri ; 
коросо) of the Myristicaceae (27–30).—23. Whole grain SEMG, х 1,810. — 24. Exine surface SEMG, 
5224. — 25. Whole grain exine section TEMG, with aperture at top, . : 
EMG, x11,200.—27. Whole grain SEMG, х2,440.—28. Exine surface SEMG, х 24,000. —23. grain 
“me section TEMG, with aperture at top, x 2,510.—30. Nonapertural exine section TEMG, х 17,900. 


ЕР-41; Cornet Beltway) from Zone IIB of the Potomac 


30. Aff. Clavatipollenites Couper sp. 2 ( 


America (Doyle & Robbins, 1977), and, accord- from the same outcrop sample (Hedlund 3916) 
ing to Dettmann (1973), it also occurs in the as the holotype of the genus is shown in Figures 
Albian of eastern АЗИЛ. 31-37. According to Doyle (1977a), the Fred- 

A pollen grain of Asteropollis that was isolated ^ ericksburgian Antlers-'*Walnut" sequence of 


478 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Уог, 71 


- AS x SN 
M 


» 
ДРАГУ, 


FIGURES 31-37, “fs ag asteroides Hedlund & No а mye 
rris (FP-338; Hedlund 3916) from the Fre 5 
gian о seen a, correlative “= Middle Zone IIB of the Potomac Group, upper Middle Al it 
Ma). hole grai n PMG, 1,440.—32. Whole grain SEMG, showi wing apertural side, х 1, 450.— 
к pce showing саре) side, х 1,450. —34. Exine surface SEMG, х 12,000. —35. Whole gain: к” 
section with apertural pery on to 3 — хан 
Apertural exine section TEMG, 1,100. oe камен оше МИН КИНЕ 


1984] 


WALKER & WALKER —LOWER CRETACEOUS POLLEN 


479 


FiGURES 


> 


X 
pertural exine section TEMG, x 9,350. 


Pe sii that this grain was obtained from is 
= ated with Middle Zone IIB of the Potomac 
= да and, hence, is upper Middle Albian in 
~ е grain shown in Figures 31–37 is pen- 
м кае (Figs. 31, 32), although, as 
ins Чу indicated, Asteropollis may also be 
aperty j achotomosulcate. SEMG of both the 
con (Fig. 32) and nonapertural (Fig. 33) sides 
"el. that Asteropollis has a modified sulcate 
mos а (being tetra-, penta-, or hexa-choto- 
uicate as the case may be) and is not colpate 


Е "y "ww 
: rd ^ 


wot 


38-43. H edyosmum orientale Merr. & Chun of the Chloranthaceae (P-1102; Poilane 3287 1, Paris). — 
—39. Whole grain SEMG, x 1,810.—40. Exine surface SEMG, x 12,000.—41. 
С, with aperture at top, х1,950.—42. Nonapertural exine section TEMG, 


as suggested by Srivastava (1975). SEM reveals 
that Asteropollis has an irregular reticulum, with 
weakly beaded to spinulose muri that are con- 
spicuously nodose (Fig. 34). Structurally, Astero- 
ров is tectate-perforate to semitectate (Figs. 32- 
34). TEM demonstrates that Asteropollis has an 
average to moderately thick nonapertural nexine 
(Fig. 36), while SEM and TEM together give the 
impression that columellae in this genus are 
composed of granule-like subunits (Figs. 34, 36). 
A thin, somewhat patchy (real or ? artifact) end- 


480 


exine is present in both the nonapertural (Fig. 
36) and apertural (Fig. 37) exine. The aperture 
itself is evident internally as a lamellate zone in 
the nexine that consists of a thin endexine and 
a somewhat thicker foot-layer overlaid by a dis- 
organized region of sexine (Figs. 35, 37). 


STEPHANOCOLPITES FREDERICKSBURGENSIS 
HEDLUND & NORRIS 


From the same outcrop sample of the Fred- 
rgian of Oklahoma from which they iso- 
lated Asteropollis, Hedlund and Norris (1968) 
described another Early Cretaceous pollen type 
under the name Stephanocolpites fredericksbur- 
nsis. Unfort y, according to J. i d 
Hills (1976), the form genus name Stephanocol- 
pites, which was proposed for any pollen with 
more than three meridional colpi, is illegitimate 
because the holotype of the type species is a Re- 
cent pollen grain of Lycopus europaeus of the 
Labiatae. Nevertheless, for the present we will 
continue to refer to this pollen type as Stephano- 
colpites fredericksburgensis. Hedlund and Norris 
(1968) noted that the radiosymmetric, prolate to 
spheroidal, isopolar pollen of S. fredericksbur- 
gensis has four or five brevicolpi that are less 
than half the polar diameter in length, and that 
it is baculate (i.e., columellate) and uniformly 
microreticulate. Out of 62 grains examined, Da- 
vies and Norris (1976) found that about 70% 
were tetracolpoidate and 30% were pentacolpoi- 
date. Doyle and Robbins (1977) have reported 
that S. fredericksburgensis also occurs in the 
Middle-Upper Albian of the Potomac Group. 
Material of S. fredericksburgensis that we stud- 
ied (Figs. 44—50) was isolated from the same out- 
crop sample (Hedlund 3916) that provided the 
holotype of the species. Figures 44—49 were all 
obtained from the same grain of S. fredericks- 
burgensis, while the whole grain exine section 
TEMG shown in Figure 50 is from another grain. 
A pentacolpoidate grain is shown in Figures 44 
and 45. SEM reveals that the pollen is irregularly 
reticulate with spinulose muri (Fig. 46), and that 
it has small tectal perforations, and consequently 
is tectate-perforate (Figs. 45, 46). TEM shows 
that the nonapertural nexine is moderately to 
very thick and that columellae are present (Fig. 
48), and also reveals that well-developed endex- 
ine is present throughout the exine, in nonaper- 
tural (Fig. 48) as well as apertural (Fig. 49) re- 
gions. While some grains of S. fredericksburgensis 
have a relatively uniform endexine (Fig. 48), in 
others the endexine is ragged (Fig. 50). Although 


d 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


grains of the latter type have been described as 
internally sculptured by Davies and Norris 
(1976), we believe that this ragged endexine may 
be simply a preservation artifact. It will be re- 
called that a similar occurrence of uniform and 
ragged endexine in different grains of the same 
llen was also encountered in the case of Cla- 
vatipollenites hughesii. Ultrastructurally, the ap- 
ertures of S. fredericksburgensis are represented 
by areas of thick endexine conspicuously lamel- 
late at the top and interbedded with the foot- 
layer, that in turn are overlaid by somewhat ге- 
duced sexine composed of laterally thickened 
elements (Fig. 49), the last being especially evi- 
ent in exine section SEMG that show the tran- 
sitional region between apertural and попарег- 
tural exine (Fig. 47). 


RETIMONOCOLPITES PIERCE 


The form genus Retimonocolpites was de- 
scribed by Pierce (1961) for “reticulate, mono- 
colpate pollen.” Several different pollen types 
have been included in this form genus, and there 
has been some question about what it should 
encompass. During the present study we exam- 
ined four different pollen types that, at the light 
microscope level at least, are referable to Reti- 
monocolpites, including R. dividuus and R. per 
oreticulatus. Two undescribed types of pollen that 
we have studied are simply referred to for now 
as aff. Retimonocolpites spp. 1 and 2. 

Retimonocolpites dividuus. Since there have 
been a number of divergent opinions concerning 
the circumscription of the form genus Retimon" 
colpites, we thought it was particularly important 
to study the type species of the genus, Retimo 
colpites dividuus Pierce. A grain of R. dividuus 
is pictured in Figures 57—62. This particular f 
was isolated from the D13-535 core sample ? 
the Potomac Group, which, according to = 
and Robbins (1977), is Late Zone IIB he d 
Late Albian in age. The characteristic light 
croscope appearance of R. dividuus is show? 
high (Fig. 57) and low (Fig. 58) focus. wr 4 
the coarse reticulum becomes locally ‹ pa 
from the rest of the grain, and sometimes ГР. 
even finds completely psilate “пехіпеѕ 0 M 
dividuus from which the reticulum is entirely 
tached (cf. Brenner, 1963, under discum 
Liliacidites dividuus, Kemp, 1968, under ne ni 
sion of Clavatipollenites rotundus). One 9 


| 


| 


— чє” 


1984] 


(Fig. 59) апа TEM (Fig. 61) indicate that this 
border is not due to thickening of the nexine, but 
apparently results from infolding of the thin- 
walled exine itself (cf. Kemp, 1968, under dis- 
cussion of Clavatipollenites rotundus). SEM fur- 
ther shows that the pollen, which is decidedly 
semitectate (Fig. 59), has an irregular reticulum 
ith muri covered by fine bands that are fre- 
quently discontinuous (Fig. 60). TEM reveals that 
the exine is composed of an extremely to very 
thin nexine, short columellae, and a thick tectum 
(Figs. 61, 62). Endexine was not observed. Ex- 
ternally, the aperture is represented by a definite 
interruption in the reticulum (Fig. 59), while in- 
ternally it is scarcely evident (Figs. 61, 62). 

Aff. Retimonocolpites sp. 1. During our ul- 
trastructural study of Potomac Group angio- 
"perm pollen we encountered a pollen type that 
clearly illust the advant f combined light 


SEM, and TEM examination of the same pollen 
gram. This pollen type, which we have desig- 
nated aff. Retimonocolpites sp. 1, is shown in 
Figures 63-68. Although this pollen type looks 
somewhat different from R. dividuus at the light 
microscope level (Fig. 63), scanning electron mi- 
croscopy (Figs. 64—66) reveals a pollen type that 
greatly resembles R. dividuus, even down to its 
finely banded reticulum (Fig. 66). Transmission 
electron microscopy, however, indicates that aff. 
Retimonocolpites Sp. 1 has a very thick nexine 
and much stouter columellae (Figs. 67, 68) com- 
Pared to R. dividuus (Figs. 61, 62). This partic- 


Was done by Hughes et al. (1979). Grains that 
Mtn] similar in the scanning electron mi- 
ix ope may be vastly different when examined 

transmission electron microscopy. 
Retimonocolpites peroreticulatus. Another 
of Early Cretaceous angiosperm pollen that 
мо included under the form genus Reti- 
аа, pites is represented by pollen grains 
чи as Retimonocolpites peroreticulatus 
: ner) Doyle. This species was first described 
ма е (1963) under Peromonolites, which 
кы genus proposed by Couper (1953) for 
Ио ороо spores. Doyle in Doyle et al. 
Pt Sferred the species to Retimonocol- 
. “© Save a number of reasons for consid- 
е ап angiosperm pollen grain rather than 
a. including the different nature of its 
=» from a true perisporium, its 
orm shape, its apparent true aperture 


WALKER & WALKER —LOWER CRETACEOUS POLLEN 


481 


rather than tetrad scar, and its similarities to 

certain undoubted angiosperm pollen types, in- 

cluding members of the form genera Clavatipol- 

lenites and Retimonocolpites. Doyle et al. (1975), 

who examined R. peroreticulatus and a possibly 
| pem ee T 11 tvpe PA Ја ГА э] № 


vle 
, 


which is somewhat larger and has a less coarsely 
developed reticulum, noted that in addition to 
the Potomac Group, pollen of this general type 
occurs in the Albian of Oklahoma, western Can- 
ada, and Peru, as well as in the Barremian of 
England and the probable Barremian-Aptian of 
central Africa. 

though we have also studied R. peroreticu- 


sample 3916), which according to Doyle and 
Robbins (1977) is correlative with Middle Zone 
IIB of the Potomac Group. The coarse, detached 


can be seen in the whole grain PMG shown in 
Figure 69. Whole grain SEMG of the apertural 
(Fig. 70) and nonapertural (Fig. 71) sides of the 
grain show no evidence of any columellae, and 
this is confirmed by whole grain exine section 
TEMG (Fig. 73). The grain has a well-developed 
aperture, which consists of a sharply defined, 
bordered slit in the reticulum itself (Fig. 70) and 
a definite thinning of the underlying nexine (Fig. 
73). Exine surface SEMG reveal that the retic- 
ulum is covered by distinctive recurved spines 
(Fig. 72). TEMG sections of the whole grain (Fig. 
73) show that the smooth central body, i.e., the 
nexine proper, is moderately to very thick, as is 
the reticulum itself. The impression is given that 
the reticulum is directly united with the under- 
lying nexine at only a few points (? possibly only 
at the aperture), and this may be why the retic- 
ulum so frequently appears for all intents to be 
free of the central body. Although we found no 
evidence of endexine in the grain of R. perore- 
ticulatus shown in Figures 69-73, Doyle et al. 
(1975) encountered endexine under the aperture 
of a grain that they considered was probably the 
related R. reticulatus. 

Aff, Retimonocolpites sp. 2. A pollen type 
(Figs. 74-80) that was isolated from an Upper 
Zone I Pot G outcrop sample (B 
10) is virtually identical with R. peroreticulatus 

г a eer ae и ак 


оша X ЈУ 


24 he 


ехсер WCLi-Ue atic TN 18. 
77) and a somewhat tighter reticulum (Figs. 75, 
76). We have designated this pollen type as aff. 
Retimonocolpites sp. 2. Although aff. Retimono- 


FIGU 


ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


рћ 
lund 3916) from the Frede 
upper Middle Albian - 
Exine surface SEMG, 
the right) exine, x12 8 
TEMG, х 10,700. 2.40. W 


справа of Okl correlative with Middle Zone Цем of the Poi 


105 44, Waste, tira PMG, x1,500.—45. Whole G, > 
0007 Бе зеспоп ЗЕМО, showing non-apertural (to di left) e ape 

—48. pertural exine ao Feci x 10,800.—49. Apertura xine 
hole pit exine section TEMG, x 4.240 


Het 
ites ie Vinten Hedlund & Norris (44—49, FP-292, 50, 0, ЕР-306; 


Group: 
46. 
ural (9 


> 


1984] WALKER & WALKER—LOWER CRETACEOUS POLLEN 


FIGUR E 

Whole “а ? : - Chloranthus japonicus Sieb. of the Chloranthace 

grain exi С, x 1,770.— 52. Whole grain SEMG, x 2,170.—53. 
ne section TEMG, x1,700.— 55. Nonapertural 


‘ection TEMG, x 10,600 


col 
eter fo looks quite different from R. per- 
74), SEM An the light microscope (cf. Figs. 69, 
blance betwe TEM reveal a remarkable resem- 
а similar c these two pollen types, including 
uibs c) age with distinctive, recurved 
мше am E 72, 77) and a similarly thick 
monocolpit igs. 2» 78, 79). Although aff. Reti- 
Маи es sp. 2 has а weakly developed end- 
nder the apertural (Fig. 80) and nonaper- 


t 


‘Ural (Fj ee 
ig. 79) exine, and no endexine was found 


483 


exine 


ae (P-2791; Furuse s.n., Stockholm).—51. 
Exine surface SEMG, x 12,000. — 54. Whole 
section TEMG, х 10,600.—56. Apertural exine 


in R. peroreticulatus shown in Figures 69-73, we 
suspect that further studies will discover that R. 
peroreticulatus has a thin endexine. The major 
difference between aff. Retimonocolpites sp. 2 and 
R. peroreticulatus is that the former has well- 
developed columellae ( Fig. 77) and the latter has 
none (Figs. 71, 72). Pollen of the aff. Retimono- 
colpites sp. 2 type. which may actually be a more 
primitive pollen type that is closely related to R. 
peroreticulatus, is significant, at the least, in that 


484 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


FIGURES 57-62. Retimonocolpites ом 2 (FP-372; D13- d from Upper Zone IIB of the Po 
Group, ктк Upper Albian (ca. 103 Ma).—57. Whole grain PMG, high focus, x 1,780.—58. 

PMG at low focus, x 1,780.— 59. Whole grain SEMG, x1:940.— SEMG, x 12,000. нем и 
grain enine E x 5,900.—62. Part of whole grain exine де аи TEMG, showing infolded, presump 


it represents a model of a more normal colu- STELLATOPOLLIS DOYLE 

mellate pollen type from which the bizarre. non- One of the most distinctive types of Early pe 

columellate А. peroreticulatus could h : d by larg 
у ave  taceous llen is represente 

evolved. oe ж ark- 


monosulcate pollen grains that have а rem 


485 
S POLLEN 

ALKER—LOWER CRETACEOU 

W. 

WALKER & 

1984] 


% 


ће Potomac 
Zone IIB of t 
Itway), from SEMG, showing 
rce sp. 1 (FP-190; VG, x 2,080 -or са wine surface SEMG, 
FIGURES 63-68, Aff bian са. 108 ма) 63 Whole grain PMG, х 2,0 x 2,080.— 
Group, Middle- -Upper Albian ( 
a үү. side, x 2.080, — 

‚00 


1 exine section 
Nonapertura 

3,530.—68. 

ТЕМО, showing aperture, x 

ection 

0.—67. Whole = exine se 

TEMG x 12,200. 


ably well- 
Pollen of t 
&Xine c 


iddle Albian 
Potomac Group, dene г REE of En- 
to the d Brazil, the of 
an n-Aptian 
reticulate of gaan e Barremia 
tectate- gland, an t 
his type, with a ro ular to 1 Afric he type species 
i bearing triang uatoria llen of t 
Composed of muri be ts. has been de- — зарез sates po ollis barghoornii Doyle, 
elliptica] supratectate ен (90 5) under the he form genus, epe core sample of the Po 
n РУ Doyle in Doyle et al. ing to Doyle the from the D12- 
name lat Doyle. беди es addition taken 
“tal. (1975), Stellatopollis is , 


" turing. 
-developed ‘“crotonoid sculp 


486 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


FIGURES 69-73. Retimonocolpites peroreticulatus (Brenner) Doyle (FP-341; рата 391 = ra the e 
ericksburgian of Oklahoma, correlative with Middle Zone IIB of the Potomac Group, upper Em | 
105 Ма).—69. Whole grain PMG, х2,610.—70. Whole grain SEMG, showing ел d eve е, 2н grain 
Whole grain SEMG, showing nonapertural side, x 2,610.—72. Exine surface SEMG, х11,500.— 73. "Who : 
exine section TEMG, with aperture at top middle, x 8,640. 


SN eee fS. 
tomac Group (Figs. 81-86), which is the same Doyle et al. (1975) also examined material р + 
core sample from which the holotype of the barghoornii that was isolated from this core х 
species was obtained. In their ultrastructural in- ple, and our observations agree with theirs. 


vestigation of early fossil angiosperm pollen, grains of 5. barghoornii аге 50 large (о 7 


1 


| 


1984] WALKER & WALKER—LOWER CRETACEOUS POLLEN 487 


FIGURES 74-8 U Zone I of the Poto- 
0. Aff. Retimonocolpites Pierce sp. 2 (FP-102; Brenner 10), from Upper 
SEM Group, Upper Aptian-Low ы Albun (ca Er Ма). — 74. Whole grain in PMG, x1,920.—75. Whole КЕ 
Exin O Showing apertural side, x4 /040.— 76. Whole grain SEMG, showing nonapertural side, x2,040.— 
79 as surface SEMG, x11 ,800.— 78. Whole grain exine section TEMG, w ith aperture at top middle, x 6, 430. = 
napertural exine section TEMG, х 18,500. —80. Apertural exine section TEMG, x 18,500. 


488 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


FIGURES 81-86. Stellatopollis barghoornii 
mac — upper Middle Albian (ca. 105 
X 1,140. — 83-84. Exine surface SEMG, x12 rd 
center, x 4,300. — 86. Nonapertural exine section T 


Doyle (FP-377; D12-515), from Middle Zone IIB of SEM 
5 Ma).—81. Whole grain PMG, x1,030.—82. Whole grain 


85. Who ie grain exine section TEMG, with apert 
EMG, x11,900. 


[VoL. 71 


e Ро!" 
th MG. 


ure at top 


1984] 


um) that the **crotonoid" sculpturing, which ap- 
pears so beautiful in SEMG (Fig. 82), is clearly 
evident in PMG as well (Fig. 81). Exine surface 
SEMG show that the triangular projections that 
form the “crotonoid” sculpturing pattern are at- 
tached to an underlying reticulum that is formed 
by muri that are distinctly circular (Figs. 83, 84). 
TEM sections further reveal that short columel- 
lae occur below the reticulum itself (Fig. 85). The 
moderately thin nexine in the nonapertural exine 
is composed of a thick foot-layer and a relatively 
thin endexine (Fig. 86). In the apertural region 
the sexine is highly disorganized (Fig. 85), and, 
as Doyle et al. (1975) have indicated, endexine 
probably occurs under the aperture, although we 
were not able to confirm this with the material 
we have examined so far. 


LILIACIDITES COUPER 


_ In 1953, Couper described the form genus Lil- 
lacidites Couper from the Upper Cretaceous- 
Eocene of New Zealand. His diagnosis of the 
genus was pollen “free, anisopolar, bilateral, 


the circumscription of Liliacidites, we believe that 
three Potomac Group pollen types that we have 
investigated fall under this form genus sensu lato. 
Eu sp. 1. One type of Liliacidites that 
in site Studied, which we have designated as 

;lacidites Sp. 1 (Figs. 87-91), is the same as 
iliacidites sp. Е of Doyle and Robbins (1977). 
у inis distinctive feature of this large, strong- 
еба "shaped, monosulcate pollen is the differ- 
into On of its irregularly reticulate sculpturing 
the адь, (Fig. 89) and fine (Fig. 90) areas, with 
shaped grain (Figs. 87, 88). In addition, the muri 
“©mselves are psilate, and within the coarse re- 


ш ИТ пехїпе is extremely to very thin, and 
by chart, overlaid by a thick tectum supported 
The; columellae. Endexine was not observed. 
sists ^^ apre appears to be very broad and con- 
tid ds thinner nexine relative to the nonaper- 
кп ine overlaid by a relatively unreduced 
. 12е (the infolded aperture can be seen on the 
"ight side in Fig. 91) 


WALKER & WALKER —LOWER CRETACEOUS POLLEN 


489 


Liliacidites sp. 2. А second type of Liliaci- 
dites, which we have designated Liliacidites sp. 
2, is shown in Figures 92—97. This species is the 
same as Liliacidites sp. E of Doyle and Robbins 
(1977) and was obtained from the same Potomac 
Group core sample (D13-535) as the grain pic- 
tured by them. Unlike Liliacidites sp. 1, which 
is boat-shaped and monosulcate, Liliacidites sp. 
2 is glob d trichot te (Figs. 92, 93). 


M 


In the grain shown in Figures 92-97 one arm of 
the trichotomosulcus is notably smaller than the 
other two (Fig. 93). This is common in other 
types of trichotomosulcate pollen (cf. Wilson, 
1964), and may be indicative of an evolutionary 
stage that is intermediate between monosulcate 
pollen and pollen that has a fully developed, 
equal-armed, trichotomosulcus. Liliacidites sp. 
2 is similar to Liliacidites sp. 1 in that it also 

ticulate sculpturing differentiated into 
coarse and fine areas (Fig. 95), although instead 
of having the fine reticulum at the ends ofa boat- 
shaped grain, as in Liliacidites sp. 1, in Liliaci- 
dites sp. 2 the fine reticulum is around the 


are psilate, as in Liliacidites sp. 1, in Liliacidites 
sp. 2 they are more or less circular (Figs. 94, 95) 
rather than irregular. Strongly dimorphic lumina 
can occasionally be seen within the coarse retic- 
ulum (Fig. 95). TEM sections of Liliacidites sp. 
2 reveal that, as in Liliacidites sp. 1, the nexine 
is thin and the columellae are short (Fig. 96). In 
the grain shown in Figure 96, the two sides are 
tightly appressed, with the nonapertural face on 
top and the apertural side on the bottom. A sec- 
tion through part of the finely reticulate spot on 
the nonapertural side of the grain is present at 
the top right of Figure 96 just below the line 
dividing Figures 94 and 95, while a section 
through part of the trichotomosulcus can be seen 
below and slightly to the right of this. It is in- 
teresting to note that the exine is considerably 
thicker on the nonapertural face because the tec- 
tum is thicker on this side. TEMG in the aper- 
tural region (Fig. 97) reveal the presence of end- 
exine in Liliacidites sp. 2, at least under the 
aperture itself. Externally, the aperture is appar- 
ent as a broad, more or less psilate area (Fig. 93), 
while internally it appears as a thinner region of 
the exine that seems to consist largely of endex- 


ine. 

«Liliacidites" minutus. The third type of 
Early Cretaceous angiosperm pollen that for the 
present at least is included under the form genus 


490 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Уог. 71 


% 
„Жм. 


f 


, 


Group. 
FIGURES 87-91.  Liliacidites Couper sp. 1 (FP-392; D13-535), from Upper Zone ПВ of the у 
lower Upper Albian (са. 103 Ма). —87. Whole grain PMG, х1,340.—88. Whole grain SEM ‘ane reticulum. 
Exine surface SEMG, showing coarse reticulum, x 12,000.—90. Exine surface SEMG, showing 
х 12,000.—91. Whole grain exine section TEMG, with infolded aperture at right, x 8,130. 


Liliacidites is apparently the same as pollen de- 
scribed by Brenner (1963) as Clavatipollenites 
minutus Brenner and pictured in Doyle and Rob- 
bins (1977). Although this pollen type is prob- 
ably best treated as a distinct genus, for the time 
being we will refer to it as '* Liliacidites" minutus. 
"Liliacidites" minutus (Figs. 98-102) is charac- 
terized by its small size (generally about 15 um 
long) and psilate reticulum (Figs. 99-101). The 
relatively coarse reticulum of “L.” minu us, 
which is clearly evident even in PMG (Fig. 98), 


ce that is consid- 
nites. 
dilê 


Ыр Ө 
dimorphic lumina (Fig. 101), although 1t a 
from them in that its reticulum is Ри А 
strongly polygonal. TEM sections (Fig. 1 ig 
veal that “L.” minutus has a тобе : 
nexine, however, that is different from di 
nexine of Liliacidites spp. 1 and 2. TA nid 
nexine is overlaid by short columellae 


1984] WALKER & WALKER—LOWER CRETACEOUS POLLEN 491 


yj TURES 92-97. Liliacidites Couper sp. 2 (FP-366; D13-53 >) from Upper Zone IIB of the Potomac Group, 

wer Upper Albian (са. 103 Ma).—92. Whole grain PMG, х1,350.—93. Whole grain SEMG, showing apertural 

2 ii ,620.—94. Whole grain SEMG, showing Mo DE side, х 1, 620.—95. Exine surface SEMG, 

es .—96. Whole grain exine section TEMG, with aperture at bottom right, х 5,680. —97. ET exine 
on TEMG, with apertural region at bottom and appressed non-apertural side above, x14 


492 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


„1+ . . ) 
FIGURES 98-102.  *Liliacidites" minutus (— Clavatipollenites minutus Brenner) (FP-194; Cornet Belt 
per Albi 


00.- 
bian (ca. 105 Ma).—98. Whole grain PMG, = side, 
99. Whole grain SEMG, showing apertural side, x 3,100.—100. Whole grain SEMG, showing nonapert t top 

3,100. — 101. Exine surface SEMG, x12,000.— 102. Whole grain exine section TEMG, with aperture 4 
0 


tectum. Endexine was not observed. Although МАјок FEATURES OF LOWER CRETACEOUS 
"Liliacidites" minutus does not agree with typ- ANGIOSPERM POLLEN 
ical Liliacidites pollen, such as Liliacidites spp. 


1 and 2, in all respects, this pollen type appears The major features of the 13 types of Lo 
to have a greater overall similarity with Lilia- Cretaceous angiosperm pollen grains that we bà - 
cidites than with Clavatipollenites, and for this investigated with combined light, scanning e 
reason we have chosen to include it under our tron, and transmission electron microscopy y 
discussion of the pollen of Liliacidites. summarized in Table 4. Characters of these Бай) 


1984] 


Cretaceous pollen grains are considered under 
the following seven headings: aperture type, pol- 
len shape, pollen size, nonapertural exine sculp- 
turing, nonapertural exine structure, exine strat- 
ification, and aperture ultrastructure. 

Aperture type. The majority of pollen grain 
types included in this study (nine out of 13) have 
a monosulcate aperture, e.g., Clavatipollenites 
hughesii (Figs. 7, 8), Retimonocolpites peroretic- 
ulatus (Fig. 70), Stellatopollis barghoornii (Figs. 
81, 82), and “Liliacidites” minutus (Fig. 99). Two 
pollen types, aff. Clavatipollenites sp. 1 (Fig. 18) 
and Liliacidites sp. 2 (Fig. 93) have trichotomo- 
sulcate apertures, while pollen grains of Astero- 
pollis asteroides are basically pentachotomosul- 
cate (Figs. 31, 32), although sometimes they may 
be tetra- or hexachotomosulcate. Stephano- 
colpites fredericksburgensis is the only type of 
pollen included in our investigation that has sev- 
eral equatorial apertures instead of a single polar 
aperture. According to Davies and Norris (1976), 
F нивеа: is basically tetracolpoi- 

е. less 1 1 Nm с. ми 


in Figures 44 and 45. 
_ Polle " Shape. Shapeofthe pollen grains stud- 
led varies from strongly boat-shaped in Liliaci- 
dites sp. 1 (Figs. 87, 88, 103) and moderately 
boat-shaped in aff. Retimonocolpites spp. 1 (Figs. 
63-65) and 2 (Figs. 74—76) to globose in Astero- 
pollis asteroides (Figs. 31-33), Stephanocolpites 
fredericksbur gensis (Figs. 44, 45), aff. Clavati- 
pollenites sp. 1 (Figs. 18, 19), and Liliacidites sp. 
2 (Figs. 92-94) Nu nites n ss 
be 69-7 1), R. dividuus (Figs. 57—59), and Stel- 
e ollis barghoornii (Figs. 81, 82) all vary from 
bi Иве ca to globose, while Clavatipollenites 
(E esti (Figs. 7, 8), aff. Clavatipollenites sp. 2 
100) 23), and “Liliacidites” minutus (Figs. 98- 
n from slightly boat-shaped to globose. 
"eii п size. Most of the grains examined are 
altho retard with a range of about 20-30 um, 
"-— Liliacidites sp. 2 (Figs. 92—97) and to 
62) av хіепі Retimonocolpites dividuus (Figs. 57- 
is "age a little above this size range. Reti- 
. onocolpites peroreticulatus (Figs. 69-73), which 


1 
“= somewhat below 20 um, is basically 


mu, tue Pollen grains of “Liliacidites” mi- 
15 Бе 98-102) аге small (usually around 


po аретита! exine sculpturing. Most of the 
types studied are irregularly reticulate, e.g., 


WALKER & WALKER—LOWER CRETACEOUS POLLEN 


493 


Clavatipollenites hughesii (Fig. 9), Asteropollis 
asteroides (Fig. 34), Stephanocolpites fredericks- 
burgensis (Fig. 46), although Stellatopollis barg- 
hoornii is regularly reticulate with circular muri 
(Figs. 82-84) and Liliacidites sp. 2 is more or 
less regularly reticulate with muri that are almost 
circular (Figs. 94, 95). “‘Liliacidites” minutus, 
which is irregularly to more or less regularly re- 
ticulate (Figs. 99, 100), is distinctive in that its 
muri are mostly decidedly polygonal (Fig. 101). 
Liliacidites spp. 1 and 2 are characterized by 
differentiation of their reticulate sculpturing into 
coarse and fine areas (Figs. 89, 90, 95). In Lil- 
iacidites sp. 1 the finer reticulum is at the ends 
of the boat-shaped pollen (Figs. 87, 88, 103), 
while in Liliacidites sp. 2 the area around the 
aperture (Fig. 93) and the middle of the non- 
apertural side of the grain (Fig. 94) are both sur- 
rounded by a finer reticulum. 

The nature of the muri or walls of the reticu- 
lum varies considerably. In Clavatipollenites 
hughesii, the muri are beaded to spinulose (Fig. 
9), while they are weakly beaded to spinulose in 
Asteropollis ides (Fig. 34), and spinulose in 
Stephanocolpites fredericksburgensis (Fig. 46). 
Muri with recurved spines are found in both Re- 
timonocolpites peroreticulatus (Fig. 72) and aff. 
Retimonocolpites sp. 2 (Fig. 77). Banded muri 
occur in aff. Retimonocolpites sp. 1 (Figs. 63—68) 
and in Retimonocolpites dividuus (Figs. 57—62), 
being distinctly banded in the former (Fig. 66) 
while finely and discontinuously banded in the 
latter (Fig. 60). Beaded muri characterize aff. 
Clavatipollenites sp. 1 (Figs. 20, 21), while aff. 
Clavatipollenites sp. 2 has beaded-granulose muri 
(Fig. 24). Stellatopollis barghoornii has muri 
covered by psilate, triangular supratectal ele- 
ments, which form a “crotonoid” sculpturing 
pattern (Figs. 83, 84). In all three species of Lil- 
iacidites the muri are psilate and the lumina are 
generally strongly dimorphic, with small lumina 
mixed in with much larger ones (Figs. 89, 95, 
101). Nodose muri with node-like, swollen areas 
at points where columellae and muri meet occur 
in Asteropollis asteroides (Fig. 34) and aff. Re- 
timonocolpites sp. 1 (Figs. 63-66). 

Nonapertural exine structure. Most of the 

llen types investigated are semitectate, except 
Stephanocolpites fredericksburgensis, which is 
tectate-perforate (Figs. 45, 46), and Clavatipol- 
lenites hughesii (Figs. 8, 9) and Asteropollis as- 
teroides (Figs. 32-34), which are tectate-perfo- 
rate to semitectate. The coarse and finely 
reticulate Liliacidites spp. 1 and 2 are basically 


TABLE 4. Major features of Lower Cretaceous angiosperm pollen. 


Pollen Type 


Aperture Type, dps Shape, 
and Pollen Siz 


Nonapertural Exine Sculpturing 


(1) Clavatipollenites hughesii 
(2) Asteropollis asteroides 


(3) Stephanocolpites fredericksburgensis 
(4) Retimonocolpites peroreticulatus 


(5) aff. Retimonocolpites sp. 2 
(6) aff. Retimonocolpites sp. 1 


(8) aff. Clavatipollenites sp. 2 
(9) Stellatopollis barghoornii 
(10) Liliacidites sp. 1 


(11) Liliacidites sp. 2 


(12) “Liliacidites” minutus 


(13) Retimonocolpites dividuus 


Monosulcate; slightly boat-shaped to globose; 
й m 
(4-)5(-6)-chotomosulcate; globose; medium- 
sized 


2. 
4(—5)-colpoidate; globose; medium-sized 
cue ege а to globose; small- to 
mediu 
Monosuleate boatshaped medium-sized 
on cate; boat-shaped; medium-sized 
Tri мај ж: globose; medium-sized 
Mono ulate seh boat-shaped to globose; 
mediu 
iad alae ЊЕ. 4 to + globose; large 


Monosulcate; strongly boat-shaped; large 


Trichotomosulcate; globose; a little above medi- 
um-sized 


Monosulcate; slightly boat-shaped to globose; 
small 


Monosulcate; boat-shaped to globose; + medi- 
um-sized 


Irregularly reticulate, muri beaded to spinulose 
pee reticulate, muri weakly beaded to spinulose, 


nodos 
пр reticulate, muri spinulose 
Irregularly reticulate, muri with recurved spines, reticu- 

m + free from nexine 

Irregularly reticulate, muri with recurved spines 
Irregularly reticulate, muri У banded, nodose 
Irregularly reticulate, m d 
Irregularly reticulate, muri ашышы 


Regularly reticulate, muri circular, with psilate, triangu- 
lar supratectal elements, i.e., *crotonoid" 

Irregularly coarsely and finely reticulate, muri psilate, lu- 
mina within coarse reticulum strongly dimorphic 

+ regularly coarsely and finely reticulate, muri psilate, + 
circular, lumina within coarse reticulum occasionally 
strongly dimorphic 

Irregularly to + regularly reticulate, muri psilate, mostly 
decidedly polygonal, lumina dimorphic 

Irregularly reticulate, muri finely and discontinuously 
banded 


tót 


N3QG3IVO TVOINV.LOd ІҸПОЅЅІИ JHL AO STVNNV 


IL 10A] 


TABLE 4. (Continued). 


Nonapertural Exine Structure 


Exine Stratification 


Aperture Ultrastructure 


(1) Tectate-perforate to semitectate; nexine 
m 


rately to very thick, columellae well- 


developed 


(2) Tectate-perforate to semitectate 
nexine average to madda] thick. 
columellae seemingly composed o 
granules 
(3) Tectate-perforate; nexine moderately to 
very thick, columellae present 


(4) Semitectate; nexine moderately to very 
thick, columellae absent 


(5) prea nexine average to moderately 
, well-developed columellae 


rese 
(6) d itectate; nexine moderately thick, 
well-developed columellae present 


(7) Semitectate; nexine average, well-devel- 
olumellae present 
(8) Semitectate; nexine average, well-devel- 
oped columellae present 
(9) Semitectate; nexine moderately thin, 
columellae very short, tectum and 
overlying elements thick 


(10) Semitectate to tectate-perforate at ends 
of grain; nexine extremely to very 
thin, columellae short, tectum thick 


Thick endexine under aperture only 
Thin endexine throughout 


Well-developed endexine throughout, conspicu- 
ously interbedded with foot-layer under aper- 
ture 


Thin endexine possibly present 
Thin endexine throughout 
Endexine not observed 


Endexine not observed 
Endexine not observed 


Thin endexine probably throughout 


Endexine not observed 


Aperture externally verrucate, internally with a very 
thick, apparently homogeneous endexine and a thin, 
occasionally ae foot- d overlaid by a thick 
sexine organiz TTU! 

Aperture ра: internally as а OR nexine consist- 
ing of a thin endexine and a somewhat thicker foot- 
layer overlaid by a disorganized sexine 


Apertures internally with a thick endexine conspicuously 
lamellate at top and interbedded with foot-layer, sex- 
ine somewhat reduced, composed of laterally thick- 
ened elements 

Aperture represented externally by a definite, distinctly 
bordered slit in the r "ag evident internally by a 
definite thinning of the n 

Aperture evident лаар im a це fied рашы of the 
nexine and a disorganization of the se 


Aperture appearing externally as an interruption in the 
reticulum, evident internally by a marked thinning of 
the nexine 

Aperture evident internally by a thinning of the nexine 
and a diso ization of the sexine 

Aperture evident internally by a сеч of the nexine 
and a disorganization of the sexin 

Aperture probably appearing e 

organized, non-“crotonoid” region of the exine, evi- 
dent internally by a thinning of the nexine, which be- 
comes lamellate, and a marked disorganization and re- 
duction of the sexine 

Aperture evident internally as a broad, infolded region 
of the exine with a thinner nexine but apparently un- 
reduced sexine 


аи as a differently 


N3TIOd SNOFJOVLAAD AAMOT— AAATVM 9 AAATVM [r861 


Sót 


(Continued). 


TABLE 4. 


Aperture Ultrastructure 


Exine Stratification 


Nonapertural Exine Structure 


Aperture appearing externally as a broad, + psilate area, 


Well-developed endexine, at least under aper- 


(11) Semitectate to tectate-perforate around 


evident internally as a thinner region of the exine that 


appears to consist largely of endexine 


tural side; nexine very to moderately 

thin, columellae short, tectum thick 

(especially on non-apertural side) 
(12) Semitectate; nexine moderately thick, 


Endexine not observed 


Aperture appearing externally as an interruption in the 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


columellae short, tectum thick 


reticulum, evident internally by a thinning of the nex- 


1 


Aperture represented externally by a definite interruption 


ne 


Endexine not observed 


(13) Semitectate; nexine extremely to very 


columellae short, tectum thick 


> 


thin 


dent internally, “border” observed in PMG presum- 


ably due to infolding of the exine 


(Мог. 71 


semitectate, with tectate-perforate areas at the 
ends of the boat-shaped pollen of Liliacidites sp. 
1 (Figs. 87, 88, 90) and around the aperture and 
in the middle of the nonapertural side of Lilia- 
cidites sp. 2 (Figs. 93, 94). 

Nexine thickness in the nonapertural exine (cf. 
Table 3) ranges from very thick to extremely 
thin. Clavatipollenites hughesii (Fig. 10), Ste- 
phanocolpites fredericksburgensis (Fig. 48), and 
Retimonocolpites peroreticulatus (Fig. 73) have 
a moderately to very thick nexine, aff. Retimono- 
colpites sp. 1 (Fig. 68) and “‘Liliacidites” minutus 

ig. 102) have a moderately thick nexine, and 
Asteropollis asteroides (Fig. 36) and aff. Reti- 
monocolpites sp. 2 (Fig. 78) ws an A to 
moderately thick nexine. An average 
characterizes the pollen of aff. Ciavatipolenies 
spp. 1 and 2 (Figs. 22, 26). By contrast, the nexin 
is moderately thin in Stellatopollis barghoomi 
(Figs. 85, 86), very to moderately t thin in Lilia- 
cidites sp. 2 (Fig. 96), and extremely to very thin 
in Retimonocolpites dividuus (Figs. 61, 62) and 
ee ge sp. 1 (Fig. 91). 
of the pollen types have well-developed 
ыы It 
the tectum is thick) i in Stellatopollis barghoornii 
(Figs. 85, 86), Retimonocolpites dividuus (Figs. 
61, 62), and in all species of Liliacidites (Figs. 
91, 96, 102). Liliacidites sp. 2 is noteworthy in 
E^ the tectum is considerably thicker on the 

napertural side of the pollen grain (Fig. 
кей олсо» peroreticulatus is а in 
that columellae are absent and the rel is 
more or und 
69-73). The columellae are seemingly pa 
of granules in Asteropollis asteroides (Figs: 34, 
36 


Exine stratification. Endexine was s not 0b- 
served in the pollen of aff. Спауапроћен Р n pe 
1 (Fig. 22) and 2 (Figs. 25, 26), a ‚ Кепто p 
colpites sp. p 67, 68), '"Retimonocolpités 

| , 62), Liliacidites sp. 1 (Fig. 9 


peroreticulatus, although it cannot be See 


ји only 
shown in Figure 73. Thick en vatipollnii 
xine, 


at least undef the aperture, Was found 1n m 
cidites sp. 2 (Fig. 97). A thin op Ree 
the grain (in both apertural and nonape 

gions) characterizes різна е asteroides ee 
36, 37) and aff. Retimonocolpites Sp- 2 (Figs. rolls 
80), and is probably present in Stellato, 


| 


1984] 


coe as well (cf. Fig. 86, in which definite 
xine can be seen in sections of the nonaper- 
ie exine). In Stephanocolpites fredericksbur- 
gensis, a well-developed endexine is present 
throughout the grain (Figs. 48, 50), and the end- 
with the foot- 


layer under the aperture (Fig. 49). 

Aperture ultrastructure. Considerable varia- 
tion exists in the pollen grains examined with 
regard to aperture ultrastructure, with reference 
both to external sculpturing and internal struc- 
ture. Externally apertures may appear either as 
differentially sculptured areas of the exine or as 
definite interruptions in the reticulum itself. In 
Clavatipollenites hughesii the aperture is con- 
spicuously verrucate (Fig. 8), while in Liliacidites 
sp. 2 the aperture appears as a broad, more or 
less psilate area (Fig. 93). The aperture is marked 
by an interruption in the reticulum itself in aff. 
Retimonocolpites sp. 1 (Fig. 64), “Liliacidites” 


(Fig. 59), while in Retimonocolpites peroreticu- 
latus the aperture is represented externally 
ае Соору bordered slit іп the reticulum 
(Fig. 7 he aperture probably appears exter- 
nally as E organized, non-“‘crotonoid” 
region of the exine in Stellatopollis barghoornii 
(cf. Fig. 8 

Apertures are just as varied internally or struc- 


by a thinning of the nexine and a disorganization 
of the sexine relative to the nonapertural exine, 
s &. aff. Clavatipollenites sp. 1 (Fig. 22) and Stel- 
atopollis barghoornii (Fig. иза n: endexine is 
Present in the pollen grain, it be restricted 
to the aperture, as in Clavatipollenite ийе}, 
which ha 
(Fig. 11), and in Liliacidites эр. 2 (Fig. 97), or it 
а De thi thicker under the perire as in Ste- 
h pi gs. 48, 49). 
ter opollis asteroides (cf. Figs. a SN and in 
са monocolpites sp. 2 (cf. Figs. 79, 80) end- 
AMI about equally developed in 
а and nonapertural areas. The nexine un- 
а aperture is lamellate in Asteropollis as- 
(Fig. ned (Fig. 37) and Stellatopollis barghoornii 
se "e while in Clavatipollenites hughesii oc- 
Hy in t the foot-layer appears lamellate (Fig. 
Qu noc pU fredericksburgensis the 
rri endexine is conspicuously lamellate at 
49). к, and interbedded with the foot-layer (Fig. 
relativel Some pollen types the apertural sexine is 
ely unreduced but differently organized as 
Mpared with the nonapertural sexine, e.g., the 


WALKER & WALKER —LOWER CRETACEOUS POLLEN 


497 


apertural sexine is organized into verrucae in 
Clavatipollenites hughesii (Figs. 8, 11) and into 
laterally thickened elements in cc ops 
fredericksburgensis (Figs. 47, 49). The broad a 
erture in Liliacidites sp. 1, which we have „а 
observed expanded, and which can be seen in- 
folded on the right side of the grain pictured in 
Figure 91, consists of an extremely to very thin 
nexine overlaid by a conspicuously well-devel- 
oped and little reduced sexine. By contrast, the 
aperture of Liliacidites sp. 2 shows considerable 
reduction of its sexine (Figs. 93, 96, 97). The 
bordered ture that i i in PM 


that is р G 
of Retimonocolpites dividuus (Figs. 57, 58) is 
scarcely evident in TEMG (Figs. 61, 62), and is 
apparently the result of infolding of the thin- 
walled exine itself. 


DELIMITATION OF LOWER CRETACEOUS 
ANGIOSPERM POLLEN 


Asteropollis, Stephanocolpites fredericksbur- 
gensis, and Stellatopollis, even at the light mi- 
croscope level, are reasonably distinct taxa of 
Lower Cretaceous angiosperm pollen because of 
their characteristic apertures (4—6-chotomosul- 
cate in Asteropollis, 4—5-colpoidate in S. fred- 
ericksburgensis) and sculpturing (monosulcate 
and *crotonoid" in Stellatopollis). In contrast, 
delimitation of Clavatipollenites, Retimonocol- 
pites, and Liliacidites based on light microscope 


This is evident by the fact that the type species 
of the genus Retimonocolpites, R. dividuus, has 
been formally transferred to Liliacidites by Bren- 
ner (1 963), as Liliacidites dividuus (Pierce) Bren- 


n with 
R. dividuus has been described by Kemp (1968) 
as Clavatipollenites rotundus Kemp. Some au- 
thors, by contrast, have at times referred to pol- 
len of the Liliacidites type under the name Re- 
timonocolpites (cf. Doyle, 1973). 

As might be expected, our same grain com- 
bined light and electron microscope study of 
Lower Cretaceous angiosperm pollen grains has 
revealed a number of differences that can be used 
to delimit Clavatipollenites, Retimonocolpites, 
and сся Clavatipollenites, at least in the 
restricted sen: C. hughesii, has a beaded to 
spinulose ee is tectate-perforate to 
semitectate (Fig. 9), a thick nexine (Fig. 10), well- 
developed columellae (Fig. 10), and a thick plug 
of endexine under the aperture (Fig. 11), while 
Retimonocolpites, at least in the sense of its type 


498 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


TABLE 5. Systematic affinities of Lower Cretaceous angiosperm pollen. 


I. CHLORANTHACEOUS POLLEN TYPES 


(1) Clavatipollenites hughesii (chloranthaceous, extremely similar to Ascarina) 
(2) Asteropollis asteroides (chloranthaceous, with a large number of similarities to Hedyosmum) 
(3) Stephanocolpites fredericksburgensis (chloranthaceous, with certain similarities to Chloranthus) 


II. MYRISTICACEOUS-LIKE POLLEN TYPES 


(1) aff. Clavatipollenites sp. 2 (similar to some myristicaceous pollen 
(2) aff. Clavatipollenites sp. 1 (certain similarities to myristicaceous pollen) 


. MONOCOTYLEDONOUS POLLEN TYPES 
(1) Liliacidites sp. 1 (monocotyledonous) 
(2) Liliacidites sp. 2 мраве 
(3) *Liliacidites" minutus sibly m 


ocotyledon: 


(pos us) 
(4) Retimonocolpites dividuus pede око) 


z 


(1) Retimonocolpites idis ee 
(2) aff. Rei ёна E 

3) aff. Reti ка, E 
(4) Stellatopollis не зе 


. POLLEN TYPES OF UNCERTAIN OR UNKNOWN AFFINITY 


species, R. dividuus, differs considerably in its 
banded, semitectate reticulum (Fig. 60), thin 
nexine (Fig. 61), short columellae (Fig. 61), and 
apparent lack of endexine (Fig. 62). Some au- 
thors, e.g., Doyle et al. (1975), have suggested 
restricting Liliacidites to monosulcate pollen 
grains that exhibit a differentiation into coarsely 
and finely reticulate areas such as observed in 
Liliacidites spp. 1 (Figs. 87, 88, 103) and 2 (Figs. 
93, 94). However, unless one wishes to create a 
separate genus for “Liliacidites” minutus (Figs. 
98-102), which is probably warranted, the most 
important features of Liliacidites as presently de- 
‚ sem 


itectate 


rotos and trorigly dimorphic lumina (cf. 
Figs. 89, 95, 101). 

Although for the present we prefer to keep the 
13 taxa of Lower Cretaceous angiosperm pollen 
grains that we have investigated in six form gen- 
era delimited largely on the basis of light mi- 
croscopy, we believe that the majority of these 
13 taxa probably represent good genera in a bi- 
ological sense. For example, Retimonocolpites 
рет is certainly sufficiently distinct 

m R. dividuus to warrant its recognition as a 
wa genus. However, until more examples 
of Lower Cretaceous angiosperm pollen grains 
have been investigated ultrastructurally, espe- 
cially using same grain combined light, scanning 
electron, and transmission electron microscopy, 
we believe that for now it is prudent simply to 


refer to the pollen grains that we have studied 
under established form genera such as Clavati- 
pollenites, Retimonocolpites, and Liliacidites. 


SYSTEMATIC AFFINITIES OF LOWER 
CRETACEOUS ANGIOSPERM POLLEN 


t 
The Lower Cretaceous angiosperm pollen tha 


we have examined can be placed into four he 
ferent groups based on systematic a ote di 


oup of pollen grains is clearly related 
primitive dicotyledon family Chlorantha E: 
while a second group exhibits certain res? 
blances at least to pollen of the family Myristi- 
сасеае. A third group consists of pollen gum 
with features that are characteristic of Ww 
yledon pollen. Finally, there is a fourth gro p^ 
pollen types that are of uncertain Or ger 
systematic affinity. Table 5 summarizes iris. 
sible systematic affinities of the Lower e 
ceous angiosperm pollen included in this $ 


CHLORANTHACEOUS POLLEN TYPES 


^ 
A number of workers, including come en 
Kuprianova (1967, 1981), Kemp а ) 
(1969), and Muller (1981), have єр 


these suggested relationships have vial ав 
been based on light microscope com 


—, >, 


1984] 


WALKER & WALKER—LOWER CRETACEOUS POLLEN 


499 


TABLE 6. Major features of pollen of the family Chloranthaceae. 


Pollen Feature Ascarina? Hedyosmum” Chloranthus: 

Aperture Type, Monosulcate; slightly 5(-6)-chotomosulcate; globose; (4—5—)6-colpoidate; globose; 
Pollen Shape, d to gl + medium-sized medium-sized 
and Pollen Size bose; medium-sized 

Nonapertural Ex- Irregularly reticulate, Irregularly reticulate, muri Irregularly reticulate, muri 
ine Sculpturing muri beaded to spinu- conspicuously spinulose, no- untly spinulose to + 


lose 
Tectate-perforate to 
semitectate; nexine 


Nonapertural Ex- 
ine Structure 


y to very 
thick, columellae well- 
eveloped 


Exine Stratifica- Thick endexine under 
tion aperture onl 
lam 
Aperture Ultra- Aperture externally fine- 
structure i 


verrucate, internal- 


sexine organized into 
verrucae 


Tectate-perforate to semitec- 
tate; nexine average, colu- 
mellae well-developed 


Thick endexine under aperture 
only; foot-layer under aper- 
ture conspicuously coarsely 

ellate 

Aperture represented external- 
ly as more tightly organized 

egions of the reticulum, ev- 


granulose 

Semitectate; nexine moder- 
ately thin to average; colu- 
mellae present 


Endexine throughout, finely 
lamellate, especially under 
aperture 


Apertures represented exter- 
nally as solid, + scabrate 
areas in the reticulum, evi- 
dent internally by develop- 
ment of a finely lamellate 
endexine, extreme thinning 
of the foot-layer, and re- 
duction and disorganiza- 
tion of the sexine 


relative to the non-apertural 


sexine 


a 
b 


Ultrastructure based on Н, 


alone, we decided to examine pollen of the Chlo- 
INS with SEM and TEM to see if there 
Ti trastructural similarities as well. 

five * Chloranthaceae is a very small family of 
genera and approximately 70 species. The 

is rest iy H edyosmum, with some 40 species, 
PE gu to the American tropics except for 
бана Н. orientale, which is found only in 
51а. Ascarina, with 11 species (Smith, 


= and г Indomalaysian. Major features of 
cone, (4; е three main genera of Chlorantha- 
ики. carina, Hedyosmum, and Chloranthus) 
C marized in Table 6. Three taxa of Lower 
р um angiosperm pollen grains, C/avati- 
frederick, Asteropollis, and Stephanocolpites 
similar; urgensis, exhibit various degrees of 

ty to particular genera of Chloranthaceae. 


ب 
Ultrastructure based on Ascarina diffusa A. C. Smith‏ 


ith. 
* Ultras edyosmum orientale Merr. & Chun. 
tructure based on Chloranthus japonicus Sieb. 


Clavatipollenites and Ascarina. Many people 
have noted a similarity between C/avatipollenites 
and pollen produced specifically by the chloran- 
thaceous genus Ascarina. From light microscopy 
alone it is apparent that pollen grains of both 
Clavatipollenites (Figs. 7-11) and Ascarina (Figs. 
12-17) are monosulcate, slightly boat-shaped to 
globose, and medium-sized. Moreover, both types 
of pollen have well-developed columellae, which 
in optical section appear more as sculptural cla- 
vae (cf. Figs. 7, 12) than as internal structural 
elements. SEM and TEM examination, however, 
reveals an even more remarkable similarity be- 
tween A ina and Clavatipollenites in the strict 
sense of C. hughesii. Clavatipollenites hughesii 
and Ascarina are identical in all following 
ultrastructural features; an irregular reticulum 
with beaded to spinulose muri (cf. Figs. 9, 14), 
a tectate-perforate to semitectate exine (cf. Figs. 
8, 9, 13, 14), a moderately to very thick nona- 


500 


pertural nexine with well-developed columellae 
and a thin tectum (cf. Figs. 10, 16), thick endex- 
ine present under the aperture only (cf. Figs. 11, 
15, 17), and a somewhat verrucate aperture com- 
posed of tightly organized sexinous elements (cf. 
Figs. 8, 11, 13, 17). Thus, in ultrastructural as 
well as light microscope observable characters, 
Clavatipollenites hughesii is for all intents iden- 
tical to the pollen of Ascarina. Pollen of the two 
genera differs only in minor details, and not in 


any substanti р gical features. We agree 
with Muller (1981) that Clavatipollenites has lit- 
ad tss ‚1 11 Ра P E f ) which 


was suggested by Endress and Honegger (1980). 

Asteropollis and Hedyosmum. Since the dis- 
tinctive, fundamentally pentachotomosulcate 
aperture of Asteropollis (Figs. 31-37) is partic- 
ularly suggestive of the aperture in the pollen of 


amine pollen of Hedyosmum (Figs. 38—43) ul- 
trastructurally. Although Hedyosmum pollen ap- 
pears to be basically pentachotomosulcate (Fig. 
39), sometimes, just like Asteropollis, it exhibits 
variation in the number of apertural arms pres- 
ent (cf. Fig. 38, which shows a PMG ofa pollen 
grain of Hedyosmum that has a six-armed ap- 
erture). In addition, in both genera the pollen is 
globose and 


tate exine (cf. Figs. 32-34, 39, 40), а nonapertural 
nexine that is more or less average in thickness 
(cf. Figs. 36, 42), and a conspicuously lamellate 
apertural foot-layer (cf. Figs. 37, 43). Although 
both Asteropollis and Hedyosmum have a spi- 
nulose reticulum, the spinules are better devel- 
oped in Hedyosmum (at least in the species shown 
in Fig. 40). Also, columellae are not as well-de- 
veloped in Asteropollis (Fig. 36) as they are in 
Hedyosmum (Fig. 42). Finally, Hedyosmum 
(again at least in the species examined) has end- 
exine only under the aperture (Figs. 41—43), while 
in Asteropollis traces of endexine are evident in 
both the apertural (Fig. 37) and nonapertural (Fig. 
36) exine. Thus, while not agreeing in every mor- 
phological feature, Asteropollis, nevertheless, does 
exhibit a number of ultrastructural resemblances 
to pollen of Hedyosmum, in addition to its strik- 
ingly similar aperture type. 

Stephanocolpites fredericksburgensis and 
Chloranthus. Stephanocolpites fredericksbur- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


gensis has been compared to the pollen of the 
genus Chloranthus because both pollen types are 
polycolpoidate. In light of this we decided to 
study pollen of Chloranthus japonicus with SEM 


and TEM in order to determine how 5. freder- — 


icksburgensis (Figs. 44—50) compares ultrastruc- 
turally with the pollen of Chloranthus (Figs. 51- 
56). Chloranthus pollen appears to be mostly 
6-aperturate (Figs. 51, 52), although sometimes 
it is 4—5-aperturate as well. Davies and Norris 
(1976) found that S. fredericksburgensis was most 


commonly 4-aperturate. The pollen of Chloran- — 


thus japonicus is semitectate (Figs. 52, 53) rather 
than tectate-perforate, as in 5. fredericksburgen- 
sis (Figs. 45, 46), and the spinules on its reticu- 


lum are much coarser (cf. Figs. 46, 53). More- _ 


over, the nonapertural nexine is moderately thin 
to average in C. japonicus (Figs. 54, 55), while 
it is moderately to very thick in 5. fredericks- 
burgensis (Fig. 48). Chloranthus japonicus, just 
as S. fredericksburgensis, has endexine thro gr 
out the grain, under both the apertural (cf. Figs. 


49, 56) and nonapertural (cf. Figs. 48, 55) re- | 


gions. Although S. fredericksburgensis resembles 
pollen of Chloranthus in its aperture type. 


its | 


ultrastructure is somewhat different (at least 43 


judged by C. japonicus). Moreover, S. freder- 
icksburgensis exhibits some general chlorantha- 
ceous attributes, including a spinulose reticulum 
(Fig. 46), a thick nonapertural nexine (Fig. le 
which is reminiscent of Ascarina (Fig. 16) n 
Clavatipollenites hughesii (Fig. 10), and a 2 
spicuously lamellate apertural foot-layer (Fig. a 
which is similar to the foot-layer that occurs á 
the apertural region of the pollen of неро 
(Fig. 43). The definite presence of ms 
the pollen of S. fredericksburgensis may also : 
taken to support the idea of a general c: 
thaceous relationship. Thus, while Stepha 
pites fredericksburgensis shows some TeS? 4 
blance to the pollen of Chloranthus, 1t be 
number of features that can only be descri ttri- 
generalized chloranthaceous palynological 2 
butes. 


MYRISTICACEOUS-LIKE POLLEN TYPES 
NETT we 
Unlike Clavatipollenites hughesii, Mem и“ di 
have seen, strikingly resembles eni "ul 
Chloranthaceae, particularly of the genu ed the 
rina, pollen grains of what we have term 


Bo 
1981, 1983) than to the Chloranthaceae. 


| 


1984] 


aff. Clavatipollenites spp. 1 (Figs. 18-22) and 2 
(Figs. 23-26) appear more myristicaceous than 
chloranthaceous in their beaded (Figs. 21, 24) 
rather than spinulose reticulum, average (Figs. 
22, 26) rather than thick nonapertural nexine, 
and apparent total lack of endexine (Figs. 22, 25, 
26). Aff. Clavatipollenites sp. 2 (Figs. 23-26), for 
example, is very similar to pollen of Virola we- 
berbaueri Markgraf (Figs. 27-30) of the Myris- 
ticaceae, both having the same distinctive type 
of beaded-granulose reticulum with granules in 
rows (cf. Figs. 24, 28). We have designated pollen 
of the aff. Clavatipollenites group as *myristi- 
caceous-like” instead of ‘“‘myristicaceous” to 
emphasize our belief that this type of early an- 
giosperm pollen was not necessarily produced by 
members of the family Myristicaceae as such. 
The reason for suggesting this is that myristica- 


p y distinctive 
as chloranthaceous pollen, and, moreover, the 
Myristicaceae, unlike the Chloranthaceae, pro- 
duces exceedingly small amounts of pollen, so 
that it is rather unlikely that myristicaceous pol- 
len grains would occur in such relative abun- 
dance as does pollen of the aff. Clavatipollenites 
group in Lower Cretaceous rocks. 


MONOCOTYLEDONOUS POLLEN TYPES 


Several types of Lower Cretaceous angiosperm 
pollen grains that we have examined have fea- 
tures characteristic of monocot pollen. While 
none of these fossil pollen grains can be com- 

directly with the pollen of any particular 
extant monocotyledon, they do seem to represent 
monocotyledonous rather than dicotyledonous 
ties types. In Figures 103-110 various Lower 
Pedir angiosperm pollen grains (Figs. 103- 
b ) are compared with similar pollen produced 
Mid. living monocots (Figs. 107-110). 
ion features observed in these 
ао ае angiosperm ‘pollen eme mii 
e and fine areas (cf. Figs. 103, 107); (2) psi- 
ai vin (cf. Figs. 104, 105, 108, 109); (3) di- 
(4 "Ai lumina (cf. Figs. 104, 105, 108, 109); 
deriy; ed” muri due to lateral extension of un- 
је = columellae (cf. Figs. 104, 108); (5) more 
NE regular, decidedly polygonal lumina (cf. 
. 105, 109); (6) a thin pollen wall in general, 

: y relative to pollen grain size, combined 
With a very SRL. os 1 : : во же 
relative to the rest of the exine (cf. Figs. 106, 


110); and (7) : : 
и a total | . Figs. 
106, 11 0). ack of endexine (cf. Figs 


WALKER & WALKER—LOWER CRETACEOUS POLLEN 


501 


Differentiation of reticulate sculpturing into 
coarse and fine areas, as stressed by Doyle (1973), 
appears to be a с! teristi tyled 
pollen feature. We have never encountered this 
character in any monosulcate dicot pollen, and, 
moreover, it is very common in monocots as a 
whole, occurring often in the pollen of families 
such as the Liliaceae, Amaryllidaceae, Brome- 
liaceae, But ,and A g oth 
Psilate muri, “‘frilled’’ muri, and dimorphic lu- 
mina are also rather frequently encountered in 
the pollen of monocots, as is a thin exine with a 
very thin nonapertural nexine. While not partic- 
ularly common in monocot pollen as a whole, 
polygonal reticula do occur in some monocoty- 
ledonous pollen grains, and, moreover, are rarely 
encountered in monosulcate dicot pollen. Final- 
ly, a total lack of endexine seems to be charac- 
teristic of monocot pollen in general, and is cer- 
tainly true of various primitive monocot pollen 
types that we have studied (Walker & Walker, 
unpubl. data). 

Two fossil pollen types that we have investi- 
gated (Liliacidites spp. 1 and 2) appear to be 
definitely monocotyledonous, while two other 

5 are probably (Retimonocolpites dividuus) 
or possibly (“‘Liliacidites’’ minutus) monocoty- 
ledonous. 

Liliacidites spp. 1 and 2. Liliacidites sp. 1 
(Figs. 87-91) has the following monocotyledon- 
ous features: (1) reticulate sculpturing differen- 
tiated into coarse (Fig. 89) and fine (Fig. 90) areas, 
with the finer reticulum at the ends of the strongly 
boat-shaped grain (Figs. 87, 88); (2) psilate and 
*frilled" muri (Fig. 89); (3) lumina that are 
strongly dimorphic within the coarse reticulum 
(Fig. 89); (4) a thin exine with a particularly thin 
nonapertural nexine (Fig. 91); and (5) no endex- 
ine (Fig. 91). The trichotomosulcate Liliacidites 
sp. 2 (Figs. 92-97) also has many monocotyle- 
donous features, including a coarse and fine re- 
ticulum, which in this instance is finer around 
the aperture (Fig. 93) and in the center of the 
nonapertural side (Fig. 94). In Liliacidites sp. 2 
the muri are also psilate (Figs. 94, 95), but they 
are not “Шей” as in Liliacidites sp. 1. Fur- 
thermore, Liliacidites sp. 2 also has dimorphic 
lumina within its coarse reticulum (Fig. 95) and 
a thin exine with a very thin nonapertural nexine 
(Fig. 96). Surprisingly, however, endexine ap- 
pears to be present in Liliacidites sp. 2, at least 
under the aperture (Fig. 97). 

Retimonocolpites dividuus. Another Lower 
Cretaceous angiosperm pollen type, Retimono- 


502 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Уог. 71 


an (ca. 103- 
105 Ma) (103-106) and extant monocot pollen (107-110).— 103. SEMG of осина, Couper 


FIGURES 103-110. Liliacidites Couper from Zone IIB of the Potomac Group, Middle-Upper Albi 
? 
sp. 1 (FP-388; D13-535), x1,390.— 104. Exine surface SEMG ر‎ ual uper sp. 1 ( а 
х 12,000. — 105. Exine surface SEMG of “‘Liliacidites” minutus (= Clavatipollenites лаб Brennen) epa 
Cornet Beltway), x 12,000.— 106. Nonapertural exine section TEMG of Liliacidi tes Coupe M fact 
535), x16,500.— 107. Whole grain SEMG of Hemerocallis of the Liliaceae (P-1538), X675. "108. xin ү 
SEMG of Butomus of the Butomaceae (Р-31 17), x12,000.— 109. Exine surface SEMG of Xerophyllum © 14), 
Te 500 (P-3819), x 12,000.— 110. Nonapertural exine section TEMG of Hechtia of the Bromeliaceae (Р-31 
х 


| 
: 
| 


——————————— ДР" — "а 


— —————— 


— — 


————————  —_ 


1984] 


colpites dividuus (Figs. 57—62), probably has 
monocotyledonous affinities as well, although it 
lacks some of the monocot pollen features pre- 
viously enumerated. The chief argument for a 
probable monocotyledonous relationship of Re- 
timonocolpites dividuus is its extremely to very 
thin nonapertural nexine combined with short 
columellae, a thick tectum, and an apparent lack 
of endexine, all of which give it a striking resem- 
blance to the pollen of Liliacidites spp. 1 and 2 
(cf. Figs. 61, 62 of R. dividuus with Figs. 91, 96 
of Liliacidites spp. 1 and 2). Moreover, Doyle 
and Robbins (1977) have reported a Potomac 
Group pollen type (**Retimonocolpites sp. A") 
that looks just like R. dividuus except that it has 


dicotyledonous pollen type, even though it clear- 
ly represents a genus that is distinct from Lil- 
iacidites itself. 

"Liliacidites" minutus. While possibly 
monocotyledonous, “Liliacidites’” minutus (Figs. 
98-102) has fewer monocotyledonous features 
than Liliacidites spp. 1 and 2 and Retimonocol- 
pites dividuus. Its chief monocotyledonous fea- 
tures are its psilate muri and dimorphic lumina 
(Figs. 99-101). The reticulum of “L.” minutus, 
however, is not diff: : Tiit nd fine 
areas, as in Liliacidites spp. 1 and 2, and, more- 
a the reticulum is decidedly polygonal in out- 

. ough no endexine was observed, the 
moderately thick nonapertural nexine of “L.” 
e 102) is very different from the non- 
91, 96) nexine of Liliacidites spp. 1 and 2 (Figs. 
62) and Retimonocolpites dividuus (Figs. 61, 
Мета other feature, however, that links the three 
e uer is their colorless, transparent ex- 
ies: oes not take up stains such as safranin 

с fuchsin long after other pollen and spore 
have become heavily stained. 


POLLEN TYPES OF UNCERTAIN OR 
UNKNOWN AFFINITY 


Four Lower Cretaceous angiosperm pollen 
Мен. we have studied (Retimonocolpites 
hia atus, aff. Retimonocolpites sp. 2, aff. 
— ~ sp. 1, and Stellatopollis barg- 
Pollen E. no close counterparts among the 
d о living primitive angiosperms. Reti- 

nocolpites peroreticulatus (Figs. 69-73) is es- 
Pecially difficult to place with its loose, non-col- 


WALKER & WALKER—LOWER CRETACEOUS POLLEN 


503 


umellate, spine-covered reticulum, although its 
thick nexine and sp ticul gg 
sible chloranthaceous affinity. If it is, indeed, re- 
lated to R. peroreticulatus, aff. Retimonocolpites 
sp. 2 (Figs. 74-80) may have a similar affinity. 
Aff. Retimonocolpites sp. 1 (Figs. 63-68) may 
also be part of this same complex. Its moderately 
thick nonapertural nexine (Figs. 67, 68) is similar 
to that of R. peroreticulatus (Fig. 73) and aff. 
Retimonocolpites sp. 2 (Fig. 78), although its 
banded reticulum (Fig. 66) is somewhat remi- 
niscent of Retimonocolpites dividuus (Fig. 60). 
Finally, Stellatopollis barghoornii (Figs. 81-86) 
is particularly difficult to place, and could have 
either dicotyledonous or monocotyledonous af- 
finities. 


PRIMITIVE ANGIOSPERM POLLEN AND THE 
ORIGIN AND EARLY EVOLUTION OF 
FLOWERING PLANTS 


Scanning electron and transmission electron 
microscopy, particularly when used together to 
examine the same fossil pollen grain, reveal a 


1 


аф +1 "8 
пое 111 gy OI Lally 


Cretaceous angiosperm pollen. The evolutionary 
implications of what we have learned in this ul- 
trastructural study of Lower Cretaceous angio- 
sperm pollen will now be discussed. First, we 
will review major evolutionary trends in the pol- 
len of living primitive angiosperms. Then, we 
will evaluate the fossil pollen record of early 
flowering plants in light of what is known about 


pollen evolution in living primitive angiosperms 


in order to obtain a better understanding of the 
evolution of early fossil angiosperm pollen. Fi- 
nally, we will discuss a model for the early evo- 
lution of flowering plants based on a synthesis 
of our knowledge of both extant and fossil prim- 
itive angiosperm pollen. 


POLLEN EVOLUTION IN LIVING 
PRIMITIVE ANGIOSPERMS 


Since the trends in pollen evolution in living 
primitive angiosperms that we recognize are 
based on the putative phylogenetic relationships 
of primitive angiosperms, we shall first discuss 


our concept y p 8 
~ > РВИ EEE s ; th 1 


before reviewing the major evolutionary trends 
in the pollen of living primitive angiosperms. 
The putative phylogenetic relationships of the 
26 families that we delimit as the subclass Mag- 
noliidae are shown in Figure 111. These families 


504 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


HAMAMELIDIDAE 


PIPERACEAE | 


SAURURACEAE | 


CHLORANTHACEAE LACTORIDACEAE 
MYRISTICACEAE 
HERNANDIACEAE 


MONIMIACEAE 


CANELLACEAE 
GYROCARPACEAE 


ARISTOLOCHIACEAE 


GOMORTEGACEAE 


ANNONACEAE 


ATHEROSPERMATACEAE 
LAURACEAE SCHISANDRACEAE 


AMBORELLACEAE ILLICIACEAE 


TRIMENIACEAE 


WINTERACEAE 
IDIOSPERMACEAE 


EUPOMATIACEAE 
CALYCANTHACEAE 


AUSTROBAILEYACEAE 
HIMANTANDRACEAE 


DEGENERIACEAE 


MAGNOLIACEAE 
v. [NYMPHAEIDAE | P 


-— 


FiGURE 111. Putative phylogenetic relationships of the families of primitive angiosperms (subclass ме 
noliidae). 


of dicotyledonous angiosperms, which are clas- по other living flowering plants have any pe 
sified in Table 7, have been designated in whole acters more primitive than those pos ljidae. 
or part by various taxonomists as the Ranales, least some members of the subclass Magno М 
Polycarpicae, Apocarpicae, Monochlamydeae, As delimited by us (Table 7), the subclass three 
Magnoliales, Magnoliiflorae, Magnoliidae, Mag-  noliidae consists of 26 families grouped i WU 
nolianae, or Annoniflorae, and are generally re- — infraclasses (the Magnoliiflorae, Ari m 
garded by the majority of modern phylogenists rae, and Piperiflorae), five superorders, an nary rel 
as the most primitive group of living flowering orders. Our concept of the evolutionary it 
plants (cf. Cronquist, 1968, 1981; Dahlgren, 1975,  tionships of the families of primitive sum- 
1980; Hutchinson, 1973; Takhtajan, 1969, 1973, sperms (the subclass Magnoliidae) may be ~ 
1980; Thorne, 1974, 1976). As a group these marized as follows. The order Magno oliales 
families possess many features that are usually central and most primitive order in the su 
considered to be primitive angiosperm charac- " is divisible into two groups. One, the su 
ters— vesselless wood, monosulcate pollen, lam- Magn : 

inar, 3-trace stamens, apocarpous gynoecia, un- tive families Magnoliaceae, Degeneriaceat, 
sealed carpels, and free, spirally arranged floral man . mort 
parts indefinite in number. In fact, it appears that the suborder Annonineae, consists of the 


~ 


=- —— 


— — 


— 


————— 


—Á— == RENI on 


1984] WALKER & WALKER —LOWER CRETACEOUS POLLEN 


advanced families Annonaceae, Canellaceae, and 
Myristicaceae. The superorder Lauranae, which 
shows definite connections with the Magnoliales, 
particularly through its most primitive family 
Austrobaileyaceae, represents a terminal evolu- 
tionary line that has given rise to no other groups 
of living angiosperms. The family Winteraceae 
has been removed from the order Magnoliales 
sensu stricto and made the type of an order Win- 
terales, to which the families Illiciaceae and 
hisandraceae have also been added, ou 

in a suborder of their own. Finally, the family 
Aristolochiaceae has been made the type of its 
own infraclass, the Aristolochiiflorae, while the 
families Chl t d Lactorid h 
both been taken out of the order Laurales sensu 
lato, where they have frequently been placed, and 
have been included with the families Saurura- 
ceae and Piperaceae in the infraclass Piperiflorae, 
each in its own monotypic order. 

Unlike the terminal Lauranae, the Winterales 
(which are phenetically closest to the Magnoli- 
ales but cladistically closer to the Aristolochii- 
florae and Piperiflorae), Aristolochiiflorae, and 
Piperiflorae exhibit definite connections with 


Hamamelididae, and through it to the bulk of 
"s. dicots, including the subclasses Dilleniidae, 
oo and Asteridae (cf. Walker, 1976b, fig. 
). In fact, the Piperiflorae appears to be the sis- 
ler-group of the subclass Hamamelididae. Char- 
Ri of the family Chloranthaceae that indicate 
Ni saan with the subclass Hamamelididae 
inf apetaly, anemophily, frequent catkin-like 
Orescences, and often unisexual flowers. 
Moreover ° two tp . > P TH » the 
Hamamelididae, the Trochodendraceae and Tet- 
like traceae, are both primitively vesselless just 
the chloranthaceous genus Sarcandra, and 

и бе ћауе the same distinctive tooth type 
( eir leaf margins as does the Chloranthaceae 
д dpi Chloranthoid tooth of Hickey & 
Ming ~ 5). Finally, there are striking similar- 
= e the pollen of chloranthaceous gen- 
of = ‚45 Ascarina and Hedyosmum and pollen 
Primitive hamamelidid families such as the 


> 


"ипо 


with the same type of spinulose muri, well-de- 


505 


TABLE 7. Classification of the families of primitive 
angiosperms (subclass Magnoliidae). 


Subclass Magnoliidae 
Infraclass 1. Magnoliiflorae 
Superorder 1. Magnolianae 
Order 1. Magnoliales 
Suborder 1. Magnoliineae 
1. Magnoliaceae 
2. Degeneriaceae 
3. Himantandraceae 
4. Eupomatiaceae 
Suborder 2. Annonineae 
5. Annonaceae 
6. Canellaceae 
7. Myristicaceae 
Order 2. Winterales 
Suborder 1. Winterineae 
8. Winteraceae 
Suborder 2. Illiciineae 
9. Illiciaceae 
10. Schisandraceae 
Superorder 2. Lauranae 
Order 1. Austrobaileyales 


Order 3. Laurales 


15. Am 


19. Hernandiaceae 
Suborder 2. Laurineae 
20. Lauraceae 
21. Gyrocarpaceae 
Infraclass 2. Aristolochiiflorae 
1. Aristolochiales 
22. Aristolochiaceae 
Infraclass 3. Piperiflorae 
Superorder 1. Chloranthanae 
Order 1. Chloranthales 
23. Chloranthaceae 
Superorder 2. Piperanae 
Order 1. Lactoridales 


Order. 2. Piperales 
25. Saururaceae 
26. Piperaceae 


506 


veloped columellae, and the presence of endex- 
ine (cf. Walker, 1976b). 

The putative phylogeny of primitive angio- 
sperms outlined above is based on an analysis 
of the taxonomic distribution of characters both 

within and without the subclass Magnoliidae, i.e., 
on both in-group and out-group analysis. тано 
nomic characters from many fields, including flo- 
ral morphology, vegetative morphology, vege- 
tative anatomy, palynology, and cytology, were 
examined, and using the principle of reciprocal 
illumination (Hennig, 1966), the putative phy- 
logeny of the Magnoliidae shown in Figure 111 
was established. We intend to discuss the basis 
for our classification and phylogeny of primitive 

angiosperm families at a later date. Based on our 
ien: phylogeny, which, again, we would like 

to emphasize is based on character analysis from 
many different fields, we shall now consider the 
taxonomic distribution of individual palyno- 
logical characters in order to determine the most 
probable direction or polarity of major evolu- 
tionary trends in the pollen of living primitive 
angiosperms. Our discussion will be organized 
under seven different categories of pollen char- 
acters, including aperture type, pollen shape, pol- 
len size, nonapertural exine sculpturing, exine 
Poma type, exine tectal type, and exine strat- 
ificatio 


don type. Although some other miscel- 
laneous aperture types characterize a few prim- 
itive angiosperms (cf. Walker, 1974b, 1976a; 
Sampson, 1975), most members of the subclass 
Magnoliidae have pollen with one of the follow- 
ing aperture types: (1) monosulcate pollen (with 
a single, furrow-like aperture), (2) zonasulculate 
pollen (with a ring-like aperture), (3) ulcerate pol- 
len (with a pore-like aperture), (4) inaperturate 
pollen (without any apertures), (5) disulculate 
pollen (with two furrow-like apertures), (6) tri- 
colpate pollen (with three furrow-like apertures), 
or (7) polycolpate pollen (with more than three 
furrow-like apertures). 

Monosulcate pollen occurs in some or all 
members of every family of the Magnoliales ex- 
cept the Pupomatilceds, which has zonasulculate 
pollen g 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


ба 


largest family of p 

130 genera and. 2,300 species, has a few oti 
aperture signs most of its pollen i is either mon- 
osulcate o D 

ysis ан the family indicates that monosulcate 
pollen is the primitive type (Walker, 1971b; Le 
Thomas, 1980, 1981). Outside the Magnoliales, 
monosulcate pollen is found in the Austrobail- 
eyaceae in the Lauranae, rarely in the Aristolo- 
chiiflorae (in the primitive genus Saruma), and 
in at least some members of every family of the 
Piperiflorae. In contrast to the Magnoliales, most 
members of the Lauranae have inaperturate pol- 
len, although the Calycanthineae is characterized 
by disulculate pollen and the Austrobaileyaceae, 
as previously mentioned, has monosulcate pol- 
len. An ulcerate aperture type is a constant tea- 
ture of the Winteraceae. Tricolpate pollen occurs 
in the Illiciaceae and in а few Schisandraceat, 
while polycolpate pollen is found in many Schis- 
andraceae and in some Aristolochiaceae and 
Chloranthaceae. 

The overwhelming presence of monosulcaté 
pollen in the primitive order Magnoliales, along 
with its occurrence in such primitive -— 
as the Austrobaileyaceae in the Lauran 
Saruma in the Aristolochiiflorae, ems sug- 
gests that monosulcate pollen represents the 
primitive aperture type for the Magnoliidae. 
Outgroup comparison further confirms this inas 
much as monosulcate pollen is clearly the ње“ 
itive type in us angiosperms 

sperms А 

фейк ылары Н With regard to shape, p 

grains in general are either boat-shaped or gl 


eter anal 


pollen grains are characteristic © 
the Magnoliaceae, Degeneriaceae, and many 
nonaceae. Pollen may be weakly 
some Myristicaceae, as well as i 
ranthaceae and in some Piperales; el 
the Magnoliidae pollen grai 
bose. The perabas of boat-shaped ар 
tirely to the order Magnoliales, as well as its 
ence in primitive monocots, such as the nail 
But , Araceae and Palm ae, айл 


па few 
sewhere in 


in the families Magnoliaceae, Degeneriace ceae, ri 
Himantandraceae, and is also clearly the basic 
type in the Canellaceae and Myristicaceae as well, 
although occasionally pollen in the Canellaceae 
may be trichotomosulcate (with a three-armed 
aperture), and sometimes pollen of the Myristi- 
caceae is ulcerate. Although the Annonaceae, the 


types of y sugges 
о. é . iv е fea- 
shaped pollen grains represent a primiti 


um), large (50-99 um), very larg 


or gigantic (200 um or larger). Large or large 


= = 


1984] 


medium-sized pollen characterizes a number of 
primitive ctm within the Magnoliidae, in- 
agnoliaceae and Degeneriaceae 


the Annonineae, and the Austrobaileyaceae and 
Calycanthaceae within the Lauranae. On the oth- 
er hand, the somewhat more advanced Winter- 
ales have medium-sized pollen, the highly ad- 
vanced Chloranthaceae and Myristicaceae have 
medium-sized to small pollen, and the exceed- 
ingly Nivenoed _Piperales have minute haenen 
Thus. e most 


primitive angiosperm pollen w was gemi or large- 
to medium-size 

Nonapertural e: exine sculpturing. Many ofthe 
most primitive members of the subclass Mag- 
noliidae have pollen grains that are remarkably 
psilate, even when examined with scanning elec- 
tron microscopy. Psilate е өг this extreme 
type occurs in at least so of virtually 
every family of the ње Mud Other ex- 
ine sculpturing types, Mica do by verrucate 
or echinate pollen, for mple, occur sporad- 
ically in several санав. of the Magnoliidae, in- 
cluding advanced members of the Annonaceae 
and Myristicaceae. Reticulate pollen, by con- 
trast, is rare within the Magnoliales, occurring 
only in a few Annonaceae and in some Myris- 
ticaceae. On the other hand, reticulate pollen is 
basically the only pollen type in the Winterales 
and in the Chloranthaceae. The st rong concen- 
bete of psilate or at most foveolate (pitted) to 
ossulate (grooved) pollen in the primitive order 

agnoliales, and the occurrence of other sculp- 
wring types і in more advanced members of the 

Е was 

poii vely psilate, or at most st only weakly sculp- 
ured, e.g., foveolate, fossulate, or scabrate. 

Exine interstitial type.  Noninterstitiate to in- 


terstitiat te-granular pollen characterizes many 
members of F 


8 


шы the Degeneriaceae i and Eupomatiaceae 
ш noninterstitiate pollen grains, while most 
mbers of the Magnoliaceae have pollen with 
-— interstitium. Within the family An- 
intesti € many primitive genera have a granular 
Ium, while a few are almost nonintersti- 
e ча the СапеПасеае and Myristicaceae 
њаро те primitive members with interstitiate- 
wan ке Pollen. Pollen with well-developed col- 
а by contrast, characterizes advan 
Мыл ort naceae, Canellaceae, and 
"n Le. as well as most members of the 
vanced orders Winterales and Chlo- 


WALKER & WALKER —LOWER CRETACEOUS POLLEN 


507 


ranthales. Thus, the taxonomic distribution of 
exine interstitial types strongly suggests that col- 
umellate pollen is advanced within the Magno- 
liidae, and that primitive angiosperm pollen is 
noninterstitiate to interstitiate-granular. 

ollen of living primitive angiosperms, how- 
ever, exhibits several different types of granular 
interstitia, e.g., in the Magnoliaceae the granular 
interstitium occurs more or less in the middle of 
the exine, in the Annonaceae the interstitium 
develops in the lowermost part of the exine, and 
in the Myristicaceae the interstitium is found as 
a series of granules that in their most primitive 


dioc 


ar to be pendent from the 
inner face of the incipient tectum, and not at all 
or only weakly attached to the basal nexine. Thus, 
the morphological diversity of interstitial types 
within the Magnoliidae indicates that noninter- 
stitiate pollen probably represents the basic 
primitive type from which the various kinds of 
interstitiate-granular дент, grains have been de 
rived. C 
evolved independently a meds of times from 
granular pollen types. 
Exine tecta! type. Atectate to tectate-imper- 
members of the 
including most Magnoli- 


fo ate p 
order Magnoliales, 


rim 
ceae, and some primitive Canellaceae and My- 


risticaceae. By —— pollen pun in ad- 
nellaceae 


end Myristicaceae are те Finally, 


pollen varies from tectate- perforate to semitec- 
tate. The heavy concentration of atectate to tec- 


bers diets the highly primitive order ciue 
suggests that atectate to tectate-imperforate pol- 
len represents the primitive exine tectal type in 
the —— and, hence, probably in the an- 

osperms a hole. 

Exine осто Except for the Canella- 
ceae, which may have pollen with endexine un- 
der the eden pollen o d the oases Magnoliales 


is tota y has 
a Sell ektexinous exine. By contrast, at least 
some endexine is present throughout the pollen 
of many Lauranae, well-developed endexine oc- 

curs throughout the pollen ofthe Winterales, and 
endexine is present either only in the apertural 
region or throughout the pollen in the Chlo- 
ranthaceae. Thus, the taxonomic distribution of 


508 


endexine within the Magnoliidae, along with the 
fact that endexine appears to be absent in almost 
all monocots, strongly suggests that endexine is 


noliidae initially evolved in the apertural areas 

e.g as in the Canellaceae and in primitive 
Chloranthaceae such as Ascarina) and subse- 
quently developed in nonapertural regions as well 
(e.g., as in the Winterales and in advanced Chlo- 
ranthaceae such as Chloranthus). 

The presence of a distinctive, laminated type 
of endexine in both extant and fossil gymno- 
sperms (cf. Doyle et al., 1975) suggests either that 
angiosperms arose from some group of gymno- 
sperms that had not yet evolved endexine or that 
endexine was secondarily lost in the group of 
gymnosperms that gave rise to the flowering 
plants. In any case, clearly the endexine present 
in gymnosperm and angiosperm pollen is not 
homologous. 

Nature of primitive angiosperm pollen. Major 
evolutionary trends in the pollen of living prim- 
itive angiosperms of the subclass Magnoliidae, 
many of which have been previously discussed 
by the senior author in past contributions (Walk- 
er, 1974a, 1974b, 1976a, 1976b; Walker & 
Skvarla, 1975), are summarized in Table 8. 

Analysis of the taxonomic distribution of pal- 
ynological and non-palynological characters 
within living primitive angiosperms strongly 
Suggests that primitive angiosperm pollen is 


basically atectate, and without endexine. This 
type of pollen is found today only in the other- 
wise primitive angiosperm families Magnoli- 
aceae, Degeneriaceae, and Annonaceae. Ata 
somewhat higher level is the pollen of the fam- 
ilies Canellaceae and Myristicaceae, which, al- 
though monosulcate and sometimes psilate, is at 
best only weakly boat-shaped, and at the same 
time is medium-sized to small. Moreover, pollen 
of these two advanced magnolialean families is 
never noninterstitiate as in some of the more 
primitive Magnoliales, and in the Canellaceae at 
least endexine is present, although only under 
the pollen aperture itself. 


i , and in 
having well-developed endexine throughout. All 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


of these features (along with certain other non- 
palynological attributes, such as complicated, 


into a distinct calyx and corolla, 1-trace (rather 
than 3-trace) stamens, basically whorled carpels, 
a short receptacle, baccate fruits, and estipulate 
dvaras iei oe н 
relative advancement of the Winteraceae com- 
pared to the order Magnoliales sensu stricto. In 
a similar fashion, pollen of the family Chloran- 
thaceae is also quite advanced. For example, it 
may be polychotomosulcate ( Hedyosmum), 
polycolpoidate (Chloranthus), or inaperturate 
(Sarcandra). Furthermore, chloranthaceous pol- 
len is at best only weakly boat-shaped, being moy 
commonly globose, while at the same time it i5 
medium-sized to small, has reticulate sculptur- 
ing and well-developed columellae, is tectate- 
perforate to semitectate, and has well-developed 
endexine either only under the aperture or 
throughout the grain. 


FOSSIL POLLEN RECORD OF EARLY 
FLOWERING PLANTS 


The major characteristics of the Lower Cre- 
taceous angiosperm pollen grains that we have 
examined ultrastructurally are summar ed in 
Table 9. A comparison of Table 8, which lists 
the major luti t ds evident ın the un 
len of living primitive angiosperms of the sut 
class Magnoliidae, with Table 9 reveals that 1n 
almost every respect these early fossil р 
grains represent advanced rather than pam 
angiosperm pollen s. Lower c 
giosperm pollen grains, for example, are | у 
strongly boat-shaped (notable exceptions be 
the clearly specialized Stellatopollis barghoor к 
and the monocotyledonous Liliacidites SP- à 
instead, they are mostly weakly boat-shaped 
globose or even wholly globose. Again, €* né 
for the two species named above, most mony 


„че 


is 
sulcate Lower Cretaceous angiosperm wer 
medium-sized to small, rather than e 


all early fossil angiosperm pollen that we i 
examined is reticulately sculptured, and -€— 
psilate or otherwise weakly sculptured. All и" 
the obviously specialized Retimonocolpites m 
reticulatus have columellae, and none have f the 
ly granular interstitium. Moreover, wang © 
monosulcate pollen grains inves ted te pet 
tate-imperforate; instead, they are tecta 


E 


———— 


—— 


— 


—D — 


— 


1984] 


TABLE 8. Major evolutionary trends in the pollen of living 


WALKER & WALKER—LOWER CRETACEOUS POLLEN 


509 


Maenoliidae 


Character Primitive State(s) Advanced State(s) 
Aperture Type Monosulcate Other aperture types, including trichotomosulcate, ul- 
cerate, and inaperturate 
Pollen Shape Boat-shaped Globose 
Pollen Size Large- to medium-sized Medium-sized to small or very large 
Nonapertural Exine Psilate, foveolate, fossu- Other sculpturing types, including verrucate, echinate, 
Sculpturing bra and reticulate 
Exine Interstitial Noninterstitiate to inter- Interstitiate-columellate 
Type stitiate-granular 
Exine Tectal Type Tectate-perforate to semitectate 


Exine Stratification 


Atectate to tectate-imper- 
orate 


Endexine absent 


Endexine present only under aperture to present 


throughout grain 


forate to more commonly semitectate. Finally, 
many of the fossil angiosperm grains examined 
val ~ д 2 41 sd њосес 


have a well_de 


IS present not only under the aperture but 
throughout the nonapertural exine as well. 
Detailed examination of monosulcate Lower 
E 4 4 кү sd 


Crotanan H 


21057 pollen p y 
consideration of palynological trends observed 
Ш extant primitive angiosperms also indicates 
that the earliest currently known angiosperm pol- 
en grains represent advanced rather than prim- 
Шуе types of monosulcate angiosperm pollen. 
Our present study, for example, has shown that 
Lower Cretaceous angiosperm pollen grains that 
may appear at the light microscope level as “‘sev- 
eral ally intergrading morphologic 


: 361), and Liliacidites Couper (1953)" (cf. Doyle 
= 1 976) аге in reality not an inter-related 
tines опагу series but a mixed collection of dis- 
~ types that are easily discernible 
ры Observed at the ultrastructural level. More- 

E some of these Early Cretaceous angiosperm 
a “n grains, including one of the oldest known, 

“vatipollenites hughesii, are clearly related to 
wen: —— dicot family Chloranthaceae, which 
dis the most advanced families of the sub- 

agnoliidae. 

_ The reason that the more primitive “magno- 
not за > of angiosperm pollen grains have 
even olde discovered in Barremian-Albian or 

T rocks is probably the result of a num- 
the Асот. First, as Muller (1970) suggested, 
с. 8nolia-type of pollen may fossilize badly 

tat all. Second, Magnolia-type pollen may 


be present in the Lower Cretaceous but in such 
low amounts that it has not been discovered yet. 
This was, for example, true of the highly dis- 
tinctive pollen of the primitive angiosperm fam- 
ily Winteraceae, which was only recently discov- 
ered in the Lower Cretaceous of Israel (Walker 
et al., 1983). Furthermore, Muller (1963) has 
shown that only 39% of the genera and 58% of 
the families of angiosperms known to be in Sa- 
rawak could be detected in a palynological ex- 
amination of a peat swamp near Marudi, Sara- 
wak. Moreover, even easily recognizable 
columellate angiosperm pollen types, such as 
Clavatipollenites hughesii, sometimes comprise 
less than 1% of the total pollen grains and spores 
present in a particular Lower Cretaceous rock 
sample. Third, and timportantly, Magnolia- 
type angiosperm pollen would have either a gran- 
ular interstitium or none at all (i.e., it would be 
noninterstitiate), and, hence, it would be vir- 
tually impossible to distinguish it at the light 
microscope level from similar psilate, boat- 
shaped, monosulcate pollen produced by a va- 
riety of gymnosperms. 
Fi ыл 1 


Росо 1 Ф 
tricolpate 


len 
& Robbins, 1977), and the marked poleward mi- 
gration of tricolpate and tricolpate-derived an- 
giosperm pollen types (cf. Hickey & Doyle, 1977, 
fig. 64) all strongly suggest a true evolutionary 
origin and progression, it must be stressed that 
this is an evolutionary origin and progression of 


510 


TABLE 9. Major characteristics of Lower Creta- 
ceous angiosperm pollen. 


Character Character State(s) 


Aperture Types Mostly monosulcate, some- 


Pollen Shapes Boat-shaped to frequently 
globose 


Pollen Sizes Momy medium-sized to 
mall, occasionally large 

ie یا‎ Exine ем reticulate 
Sculpturi 

Exine Interstitial Interstitiate-columellate? 
Types 

Exine Tectal Types — Tectate-perforate to more 
commonly semitectate 

Endexine not observed or 
commonly with endexine, 
either only under aperture 
or throughout grain 


Exine Stratification 


* Columellae absent in Retimonocolpites peroreticu- 
atus. 


tricolpate and tricolpate-derived pollen-bearing 
angiosperms, and as such has nothing to do with 
the Bini. ofthe more primitive monosulcate 
pollen-bearing flowering plants, i.e., virtually all 
of the magnoliid dicots, the nymphaealean di- 
cots, and the monocotyledons. That an earlier 
stage of monosulcate pollen-bearing angio- 
sperms is yet to be discovered is indicated by the 
fact that closely comparable monosulcate angio- 
sperm pollen grains representing the earliest 
known types of angiosperm pollen occur in pre- 
Aptian palynofloras (presumably Barremian in 
age) of such widely separated areas as the Lower 
Cocobeach System of equatorial Africa, the Up- 
per Wealden of Europe, and the basal Potomac 
Group of eastern North America (Doyle et al., 
1977). 


ORIGIN AND EARLY EVOLUTION OF 
FLOWERING PLANTS 
In the following section we shall develop a 
model for the early evolution of flowering plants, 
| | река ~ +h z JI OX P... 1. å 1 


ha 


angiosperms from studies of both living primi- 
tive angiosperms and of the early fossil record 
of flowering plants. First, however, the question 
of the origin of the angiosperms will be discussed. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


ORIGIN OF THE ANGIOSPERMS 


Probably more papers have been written on 
the subject of the origin of the angiosperms than 
on any other major aspect of angiosperm evo- 
lution. In the past many authors have stressed 
the supposedly rapid rise of the flowering plants. 
Pnt, as Hickey and Doyle have show, dE idea 


arly fog 


ie angiosperm — (Doyle & ee 1976; 
Hickey & Doyle, 1977). Furthermore, Doyle 
(1969), Doyle and Hickey (1976), and Hickey 
and Doyle (1977) have provided convincing pa- 
leopalynological, as well as fossil leaf evidence, 
for the progressive evolution of tricolpate and 
tricolpate-derived pollen-producing flowering 
plants starting in the Aptian. Unfortuo ЫН 
we have. омей in the previo. section of 
paper, t ries 
known for the more primitive mon 
len-producing angiosperms, and in fact no Mag- 
nolia-type fossil pollen has yet been found in the 
pe Cretaceous for reasons that we have dis- 
cussed. Thus, until fossil evidence is discovered 
that relates to the earliest stage of angiosperm 
evolution, we are forced to rely solely on extrap- 
olation backwards from living primitive angio- 
sperms that do produce monosulcate pollen, 1 
the subclass Magnoliidae, and on extrapolation 


angiospermous features, to d more nsi 
about the origin of the flowering plants. 
With Beck's (1960a, 1960b) discovery of the 
organic connection between Archaeopteris 
Callixylon and the subsequent recognition of à 
previously unknown group of vascular plants, 
the progymnosperms, which combined pteti- 
dophytic reproduction with gymnospermovs 
anatomy, a new chapter was opened in our un 


iiia as well as about living 
gymnosperms suggests the following 
peu gymnosperm evolution. 


scenario 


anneart 


that the pes! arose ведро. in the tw 
ferent lines of gymnospermous seed-plants, = 
of which, the coniferophyte line and the though on 
phyte line, were already recognized, altho " 
a somewhat different basis, in Chamber 
(1935) classic work on guns delim 

The two lines of gymnosperm y be char- 
ited as follows. The ا‎ s a is 


Ee -—- її: ч чч ә е е өтт тч - 


чш VG ———————————— _— — —— 


=> 


OD 


—— 


epee atti ee 


einn 


= 


1984] 


acterized by simple leaves that are frequently 

small by reduction, dense pycnoxylic wood with 

generally low, uniseriate rays, cauline (i.e., stem- 
ya | 1 "P Em — ¢ Ы . ап 


ovules) that are usually in cone-like, compound 
strobili, and bilateral seeds with a two-parted in- 
tegument that are basically unitegmic and never 
cupulate. By contrast, members of the cycado- 
phyte line of gymnosperms have basically com- 
pound leaves (although leaves may be second- 


WALKER & WALKER—LOWER CRETACEOUS POLLEN 


511 


cadeoids (e.g., Williamsoniella), tetrasporangiate 
pollen-producing organs in the caytonialean pte- 
ridosperms, megasporophyll-infolded ovules in 
the glossopterids, and bisexual strobili in certain 
cycadeoids, e.g., Williamsoniella and Cycadeo- 
idea. Thus, there is no great mystery concerning 
the origin of the angiosperms, as has often been 
invoked by writers in the past. The angiosperms 
are no more isolated than many other groups of 
vascular plants. In fact, there are a number o 
bl tic M. i such as the 


arily simp I ), 
loose manoxylic wood with generally high mul- 
tiseriate rays (as well as uniseriate rays), phylline 
(ie., leaf-related) reproductive organs that аге 
basically non-strobilate except in certain ad- 
won A 1 l4 d then 41 TR 21:212 1 гь 


simple and never compound), and radiosym- 
metric seeds with a multi-parted integument that 
are basically cupulate and often, in more ad- 
vanced members, bitegmic due to cupule reduc- 
tion. The coniferophyte line consists of basically 
tall, often much branched, monopodial trees, 
while the cycadophyte line, at least in its most 
Primitive representatives, is represented by fun- 

етапу weakly to unbranched, slender trees 
and shrubs. Microsporangia are frequently syn- 
angiate in the cycadophyte line, and not so in the 
coniferophyte line, while saccate or winged pol- 
len is common in the coniferophyte line, and less 
50 in the cycadophyte line. Finally, the conifer- 
ophyte line appears to be derived from the ar- 
chaeopterid progymnosperms, while the cycado- 
Phyte line seems to be connected to the 


al perms, corystosperms, and ca oni- 
©ап pteridosperms), the glossopterids, the cy- 
сада, and the сусадео! 45. 
“= reference to the origin of the angio- 
hex : there seems little doubt that the flow- 
a re plants were derived from the cycadophytic 
€r than the coniferophytic line of gymno- 
inire Angiosperm features that suggest this 
(bis manoxylic wood, phylline reproductive 
that are in simple rather than compoun 
~ bitegmic ovules, and microsporangia that 
more or 
advanced 
exhib 
simpl 


less synangiate. Moreover, many 
groups of cycadophytic gymnosperms 
t angiospermous characteristics, including 
€ leaves in the glossopterids and some Cy- 


Czekanowskiales and Vojnovskyales, whose re- 
lationships are much more conjectural than those 
of the angiosperms. 

Some of the best prospects for resolving the 
remaining uncertainty concerning angiosperm 
origins lie in expanded studies of Mesozoic cy- 
cadophytic gy I in general, particularly 
with ultrastructural examination of in situ pollen 
grains from known pollen-producing organs of 
groups such as the peltasperms and other pte- 
ridosperms, as well as in continued ultrastruc- 
tural investigation of Lower Cretaceous mono- 
sulcate angiosperm pollen, especially from 
Barremian and even older rocks. For now, how- 
ever, the most that can be reasonably concluded 
is that the ancestry of the angiosperms must be 
sought in the pteridosperms sensu lato orin some 
as yet unknown derivative of this group of cy- 
cadophytic gymnosperms. 


EARLY EVOLUTION OF THE FLOWERING PLANTS 


The early evolution of the flowering plants can 
be divided into five different major stages (Fig. 
112), based on the early (Barremian to Middle 
Cenomanian) fossil pollen record of the angio- 
sperms and the phylogenetic relationships evi- 
dent among living primitive angiosperms. Stage 
1 is represented by the evolution of angiosperms 
with primitive monosulcate pollen of the Mag- 
nolia-type. Since more advanced monosulcate 
angiosperm pollen of the Clavatipollenites-As- 
carina-type occurs in the Barremian, it is fair to 
assume that this initial phase of angiosperm evo- 
lution began in the pre-Barremian. Stage 1 was 
characterized by the evolution of the “Lower 
Magnoliidae," i.e., by the evolution of dicots 

: ат nene 


angiosperms as the Magnoliaceae and Degener- 
iaceae. That both advanced monosulcate dicot- 
yledonous and monocotyledonous pollen occurs 
together in the earliest known angiosperm paly- 
nofloras of the Barremian suggests that the mon- 


512 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


STAGE 5 HIGHER Middle 
Triporate Pollen HAMAMELIDIDAE C enomanian 

STAGE 4 Middle-Late 
Tricolpor(oid)ate ROSIDAE DILLENIIDAE Albian 


Pollen \ 


= - 


Del бе. 


Tricolpate Pollen HAMAMELIDIDAE 
A 
STAGE 2 
HIGHER Barremian 
Advanced Monosulcate MAGNOLIIDAE 
Angiosperm Pollen 
наннан 


MONOCOTS 


LOWER 
STAGE | MAGNOLIIDAE 


Primitive Monosulcate 
Angiosperm Pollen 


Pre-Barremian 


FIRST 
ANGIOSPERMS 


_ он 


FIGURE 112. Outline of the early evolution of flowering plants based on the early (Barremian— 
Cenomanian) fossil angiosperm pollen record and putative ө Дик relationships of major groups 
angiosperms. 


ocots had already separated from the dicots by 
Barremian time. 

Stage 2 of early angiosperm evolution, which 
begins in Africa and South America, as well as 
in England and eastern North America, in the 
Barremian (cf. Hickey & Doyle, 1977), is rep- 
resented by the evolution of flowering plants with 
advanced monosulcate pollen, and includes both 


—Middle 
f living 


dicotyledonous pollen types, such as Clavatipol 
lenites, and monocotyledonous pollen type5 ayy 
as Liliacidites. This stage was characteriz ө 
the evolution of the “Higher Magnoliidae, oliid 
cluding the evolution of the advanced magno 
family Chloranthaceae. 

The development of tricolpate po 
tutes Stage 3 and probably is indicati 


Џеп consti- 
ve of the 


= 


нь iil 


1984] 


origin of the “Lower Hamamelididae,” i.e., the 
Trochodendraceae, Tetracentraceae, Cercidi- 
phyllaceae, Eupteleaceae, Hamamelidaceae, and 
Platanaceae. Stage 3, i.e., the evolution of tri- 
colpate pollen-producing dicots, begins in the 
Early Aptian of Africa-South America (i.e., West 
Gondwana), and somewhat later in Europe-North 
America (i.e., West Laurasia), where tricolpate 
pollen first appears in the Early Albian (cf. Hick- 
ey & Doyle, 1977; Doyle et al., 1977). 

The appearance of tricolpor(oid)ate (i.e., tri- 
colporoidate to tricolporate) pollen in the Mid- 
dle-Late Albian suggests that this may represent 
the beginning of the differentiation of the sub- 
class Rosidae and possibly Dilleniidae as well, 
since both are characterized basically by tricol- 


the Rosidae (and possibly Dilleniidae) consti- 
tutes Stage 4 in the early evolution of the flow- 
ering plants. 

The final phase of early angiosperm evolution, 
Stage 5, begins in the Middle Cenomanian with 
the appearance of triporate pollen, especially of 
the Normapolles type, in Europe and North 
America. Stage 5 probably represents the initial 


M opea of the “Higher Hamamelididae,” 
ie. 


earlier in the Turonian-Coniacian, while 
Ager of such “higher” hamamelidid families as 
© Fagaceae, Betulaceae, and Myricaceae first 
Nie later in the Santonian (cf. Muller, 1981) 
"и Suggests that the initial differentiation of the 
-Osldae began sometime before that of the 
Higher Hamamelididae.” 


A MODEL FOR THE EARLY ADAPTIVE 
EVOLUTION OF THE ANGIOSPERMS 
The Picture f 1 А a + 
о; “~ еепуацаозр 
lined in Fig. 112 suggests the following model o 
MEI adaptive evolution of the flowering 
Mt x Stebbins (1976) has stressed, the char- 
Bere at most strongly set the flowering plants 
9m gymnosperms are all features of the 
"Productive rather than vegetative part of the 
мы life-cycle. Although it will probably 
ке Possible to know with certainty the ex- 
Sequence by which the gymnospermous fore- 
em TS of the flowering plants acquired their an- 
Permous features, it is likely that entomophily 


WALKER & WALKER—LOWER CRETACEOUS POLLEN 


513 


was one of the earliest characteristics of the pro- 
to-angiosperms since so many basic angiosperm 


sponses to the evolution of insect pollination. 
Evolution of the perianth in flowering plants in 
particular provides further evidence in support 
of the evolutionary scheme outlined in Figure 
112. The taxonomic distribution of perianth types 
among primitive dicots of the Magnoliidae (Fig. 
111), as well as throughout the major groups of 
dicots in general (Fig. 112), provides strong evi- 
dence that perianth evolution, which undoubt- 
edly reflects basic changes in angiosperm polli- 
nation biology, has gone through at least six 
different major evolutionary stages (grades), as 
pictured in Figure 113. 

Grade I in the evolution of the angiosperm 
perianth is represented, we suggest, by flowers 
whose sterile floral parts consisted simply of flo- 
ral bracts, i.e., the flowers were composed of leaf- 
like elements associated with fertile floral parts, 
the stamens and carpels, but these sterile floral 
parts could only be distinguished arbitrarily as 
bracts versus tepals. The primitive magnoliid 
families Austrobaileyaceae (Endress, 1980) and 
Trimeniaceae (Money et al., 1950) may possibly 
be living representatives of this earliest stage in 
the evolution of the angiosperm perianth. 

Grade II is typified by the evolution of a dis- 
tinct perianth that initially was undifferentiated, 
and consisted wholly of tepals that were either 
entirely sepaloid or completely petaloid. With 
the development of this tepalar perianth into a 
speed Lu E re P o з. 


те" 


calyx of sepals and a distinct corolla of tepalar 
petals, i.e., petals derived evolutionarily from an 
undifferentiated tepalar perianth, Grade III was 
reached. Most of the living primitive angio- 
sperms of the subclass Magnoliidae ћ Grade 
П ог Ш perianth. Undifferentiated tepalar peri- 
anths of the Grade II type, for example, occur in 
some of the Magnoliaceae, most of the Lauranae, 
the Illiciaceae, and the Schisandraceae, while a 
Grade III perianth that is differentiated into te- 

s and distinct sepals characterizes 
Magnoliidae such as the Degeneriaceae, Annon- 
aceae, Canellaceae, and Winteraceae. 

Flowering plants with Grade I-III perianths 
constitute what we shall term the “basic ento- 
mophilous angiosperms.” In addition to most 
members of the Magnoliidae, this group includes 
the Nymphaeales, most of the monocotyledons, 


514 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


т SECONDARY.: АРЕ ЕТАШҮ 
| STAMINODIAL PETALS | Sepals 
Petaloid Calyx 
Grade 4 
у | 
! Sepaloid 
| Floral Bracts 
me 
Grade 
IV РЕАКТ APE TALT ' 
Giaa [TEPALAR PETALS | ББ 


Grade 


Floral Bracts 


= 


a Carpels Stamens Floral Bracts 


КО | (sterile) 
/ A S 


р ME 


Leaf-like Precursors 


FiGURE 113. Evolution of the perianth in flowering plants. 


— — 


mm 


gage 


ea 


1984] 


and probably a few members of the dicot sub- 


velopment of tepalar petals in the earliest flow- 
ering plants, it appears that the main line of an- 
giosperm evolution (at least in the dicots) lost 
these original tepalar petals and reverted back to 
the wind pollination that characterized their 
gymnospermous ancestors. These early ane- 
mophilous-apetalous Grade IV flowering plants, 
which we designate the “рптагу anemophilous 
angiosperms” to distinguish them from later, 
separately derived anemophilous angiosperms, 
include advanced Magnoliidae, such as the 
Chloranthaceae, and almost all the Hamameli- 
didae. The reason for this initial early return to 
anemophily may well have been tied in with the 
increasing aridity (and subsequent possible de- 
cline in insect pollinators) that apparently oc- 
curred soon after the earliest appearance of an- 
glosperm pollen of the Clavatipollenites-type in 
the Barremian (cf. Hickey & Doyle, 1977; Doyle 
et al., 1977). 

Although Dilcher (1979) has suggested that the 
flowers of such angiosperms as the Trochoden- 
drales, Cercidiphyllales, Eupteleales, Hamame- 
lidales, and Pi sd 


E а as some Hamamelidales апа Piperales, 
ave bisexual rather than unisexual flowers 


as implied by Di 
toos y Dilcher (1979) anyway. In order 


prov; dae Hamamelididae, however, does not 
any evidence for the idea that the Chlo- 
€— “Lower Hamamelididae” represent 
eee branch of angiosperms that evolved 
Th ent of the “Lower Magnoliidae.” 
Ны. Chloranthaceae, which, unlike the “Lower 
Melididae,” at least has some members 


WALKER & WALKER—LOWER CRETACEOUS POLLEN 


315 


with monosulcate rather than tricolpate pollen, 
is characterized by a suite of advanced features, 
including a unicarpellate gynoecium, solitary 


and opposite leaves. Moreover, the small scales 
(“tepals”) that are sometimes present at the top 
of the chloranthaceous ovary seem to indicate 
that the flowers are fundamentally epigynous, 
which is hardly a primitive attribute. 

The fossil record of angiosperm leaves also 
suggests that the Chloranthaceae — Lower Ham- 

elididae" are advanced rather than primitive 
angiosperms. As Hickey and Doyle (1977) have 
shown, most of the earliest fossil angiosperm 
leaves (as well as those of most living members 
of the Magnoliidae) are brochidodromous and 
have entire margins. The leaves of the Chloran- 
thaceae, on the other hand, are basically semi- 
craspedodromous and have distinctive marginal 
teeth that have been named Chloranthoid Teeth 
by Hickey and Wolfe (1975). The Chloran- 
thaceae share these Chloranthoid Teeth with the 
relatively advanced magnoliid families Illici- 
aceae and Schisandraceae, the Ranunculidae, and 
certain *Lower Hamamelididae," such as the 
Trochodendraceae, Tetracentraceae, and possi- 
bly the Cercidiphyllaceae. Reference to Figure 
111 shows that our phylogenetic placement of 
the Chloranthaceae positions it in close prox- 
imity to all angiosperms that have Chloranthoid 
Teeth. 

Thus, the preponderance of evidence from both 
living and fossil primitive angiosperms supports 
th lusion that the Chl ti *Lower 
Hamamelididae" are secondarily apetalous-an- 
emophilous, and that they are derived from the 
*Lower Magnoliidae," and not from some sep- 
arate line of proto-angiosperms. 

The early reversion of flowering plants back 
to wind-pollination in the Barremian-Early Ap- 
tian provides some understanding of why pollen 
of the Clavatipollenites-type is so abundant in 
the Middle Lower Cretaceous. Plants that pro- 
duced pollen of the Clavatipollenites-type were 
in all probability the earliest angiosperms that 
produced pollen with well-developed columellae 
that at the same time were wind-pollinated (cf. 
Walker, 1976b). Although, in general, we agree 
with Hickey and Doyle (1977) that the “well- 
developed reticulate exine sculpture of Clavati- 
pollenites, Retimonocolpites, Liliacidites, and 
Stellatopollis" provides “strong evidence that the 
flowering plants which produced them were in- 
sect-pollinated,” for Clavatipollenites-Ascarina, 


516 


at least, this is probably not true. Van der Ham- 
men and Gonzalez (1960), for example, have 
shown that the chloranthaceous genus Hedyos- 
mum, which also has pollen with well-developed 
reticulate sculpturing, is wind-pollinated; and in 
addition they have indicated that the genus has 
a high pollen production, and that its pollen fos- 
silizes well. That reticulate sculpturing is not al- 
ways an indication or entomophily, and con- 
versely that psilat 

of anemophily, i is also suggested by the fact that 
members of such primitive angiosperm families 


yet are ento- 

us. Moreover, pollen of Ascarina lucida, 
a common coastal plant, occurs as up to 1296 of 
the total pollen and spores present in coastal 
Pliocene-Pleistocene sediments of New Zealand 
(Mildenhall, 1978). As Muller (1981) has indi- 
cated, this "throws an interesting 


nc 
ites.” Thus, Clavatipollenites was not the pollen 
of the earliest angiosperms, instead, it was prob- 
ably the pollen of the first anemophilous angio- 
sperms. 
Neither comparative morphology of living 


evidence for Stebbins’s (1965, 1974) idea that 


Р1О5$р were weeay С 
in a semiarid rather than mesic environment, as 
Suggested by Hickey and Doyle (1977). Semi- 
xerophytic Magnoliidae are rare, and more im- 
portantly they are obviously advanced within the 
subclass as a whole. Moreover, the Potomac 
Group pollen and leaf sequence so eloquently 
correlated by Doyle and Hickey (1976) has noth- 
ing to do with the earliest phase of angiosperm 
evolution since it represents Stages 2 and 3, and 
not Stage 1, in the early evolution of the flowering 
plants (cf. Fig. 112). 

Hickey and Doyle (1977: 62ff.) admit as much 
when they say that “it must be realized that they 
[these data] apply directly to only one subgroup 
of the angiosperms, the tricolpate dicots, and 
cannot automatically be extended to the angio- 
sperms as a whole." What the Potomac Group 
pollen and leaf quens does provide is data 
concerning the adaptive radiation of the “Higher 
Magnoliidae" and the “Power Hamamelididae,” 
and this of course has nothing to do with either 
the evolution of the “Lower Magnoliidae” or 
with the origin of the angiosperms themselves. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


Apparently, soon after the origin of the wind- - 
pollinated Chloranthaceae — Lower Hamameli- 
ФИШЕР" in hê Barremian-Early Aptian, condi 
favored, and the result was a mae тай 
10 race ain among the dicotyledonous an- 
giosperms. The majority of the dicotyledons, in- 
св Û ње subclass Rosidae (and its derivative 
the Asteridae) as well as the subclass Dilleniidae, 
have probably evolved as part of this secondary 
reversion to entomophily. 

Petals evolved again in these “secondary en- 
tomophilous angiosperms,” but this time they 
developed from stamens (Fig. 113, Grade у) 
rather than from tepals, as they had in the orig- 
inal “basic entomophilous angiosperms.” Thus, 
the staminodial petals of the Rosidae-Dilleni- 
idae-Asteridae are apparently not homologous 
with the more primitive tepalar petals of 
“Lower Magnoliidae,” Nymphaeales, and mon- 
ocots. Although most secondarily pe taliferous 
dicots presumably regained their petals thro 
sterilization of stamens, in a few instances petal- 
like floral parts were formed from petaloid ca- 
lyces, e.g., Aristolochia, and in a few angio- 
sperms, such as Mirabilis (Nyctaginaceae), 
transference of function even went so far that 
floral bracts assumed the appearance of a calyx, 
while the calyx itself took over the function of @ 
corolla. Finally, a few advanced members of the 
Dilleniidae-Rosidae-Asteridae, such as the Sal- 
icaceae, the Garryaceae, and Fraxinus of the Ole- 
aceae, again became an emophilous-apetalous 
representing yet another d (cf. Fig. 113, Grade 
VI) in the evolution of the angiosperm perianth. 


anemophilous. Furthermore, it is apparent к= 
a major line of anemophilous angiosperms a 
cluding the magnoliid family Chloranthacea¢ ый 
the related “Lower Hamamelididae,” er 
the Barremian-Early Aptian from mor ii 
tive “basic entomophilous angiosperms 0 
“Lower Magnoliidae.” It was from these 


dicots was probably their secondary " imd of 
entomophily concomitant with the evo! 
staminodial petals that replaced the 0 


> "qm 


| 


| 


1984] 


palar petals of their distant entomophilous 
ancestors in the “Lower ашн " these 
ecd tepalar petals having been lost when cer- 

Higher Magnoliidae," ан the Chlo- 
hi eg reverted to wind-pollination in the 
Barremian 


SUMMARY AND CONCLUSIONS 


In the last decade significant new information 
has been gained about the early evolution of 
flowering plants through studies of Early Creta- 
ceous us angiosperm pollen and the pollen of living 

Although most recent 
Mino шд studies of extant primitive angio- 
sperms have used both scanning electron and 
transmission electron microscopy, few ultra- 
structural studies of early fossil angiosperm pol- 
еп grains exist. This paper represents an attempt 
to remedy this situation. Thirteen different types 
of Lower Cretaceous angiosperm pollen grains 
from the Potomac Group of the Atlantic Coastal 
Plain of eastern North America and the Fred- 
ericksburgian of Oklahoma were investigated ul- 
trastructurally, using a technique that we have 
developed for studying single dispersed fossil 
o: кем by combined light, scanning elec- 

hi 


an 


ы is invaluable for the evolutionary study 
of small, light-microscopically similar dispersed 
fossil pollen grains, such as those that constitute 
the bulk of the ise. known microfossil record 
of the flowering plant 

After discussion of boots and methods and 
4 brief review of concepts and terminology deal- 
ing with pollen wall morphology, results are pre- 
» based on our examination of the follow- 


WALKER & WALKER —LOWER CRETACEOUS POLLEN 


517 


aperture, while Retimonocolpites, based on its 
type species, R. dividuus, has a banded, semitec- 
tate reticulum, a thin nexine, short columellae, 
and apparently no endexine. The most important 
features of Liliacidites sensu lato are a psilate, 


mina, while Liliacidites sensu stricto is probably 
best restricted to pollen that has reticulate sculp- 
turing differentiated into coarse and fine areas. 
Other features frequently observed in pollen of 
the Liliacidites-type include “‘frilled’’ muri due 
to lateral extension of underlying columellae, a 
thin pollen wall, especially relative to grain size, 
a very thin nonapertural nexine relative to the 
rest of the exine, and a general lack of endexine. 

This study further reveals that a close simi- 
larity exists between some Early Cretaceous an- 


tures that are presently restricted to the pollen 
of living monocotyledons. Retimonocolpites di- 
— probably also hex mon xr dein af- 
finities. Other Lo pollen types, 
"EC эй лийше Ө сазнање and Reti- 
monocolpites peroreticulatus, have no counter- 
parts among the pollen of extant angiosperms 

In the last part of the paper the question of the 
origin and early evolution of the flowering plants 
is examined. First, the phylogeny and classifi- 
cation of the — of the primitive angio- 
nerm subclass M d, and the 


~ Asteropollis mote rites 
re Sredericksburgensis, Retimonocolpites di- 
AX Retimonocolpites peroreticulatus, two aff. 
nil a ies: spp., Stellatopollis barghoor- 

three species of Liliacidites. Use of same 
N combined light, scanning electron, and 
Bi Mission electron microscopy provides a 
uw Improved means of delimiting Early Cre- 
Gio = spe llen form genera such as 
айы. а lenites, Retimonocolpites, and Lilia- 

lavatipollenites, in the restricted sense 
of its 5 type 5 


ине ыы. a thick nexine, well-developed col- 
llae, and a thick plug of endexine under the 


following major taxa are recognized within the 
agnoliidae: infraclasses Magnoliiflorae, Aris- 
tolochiiflorae, and Piperiflorae; superorders 


ranthanae, an 
ales, Winterales, Austrobaileyales, Trimeniales, 
Laurales, Aristolochiales, Chloranthales, Lacto- 
ridales, and Piperales. 

Next, major evolutionary trends in the pollen 
of living primitive angiosperms are considered. 
Taxonomic distribution of characters of living 
primitive angiosperms suggests that angiosperm 
pollen is primitively monosulcate, boat-shaped, 
large- to medium-sized, psilate, or at best only 
weakly sculptured, noninterstitiate to possibly 


518 


interstitiate-granular, atectate, and without end- 
exine. This type of pollen is found today only i in 


The fossil pollen record of early flowering plants 
is then considered in light of what is known about 


and the point is stressed that Clavatipollenites 
and other currently known types of Early Cre- 
taceous angiosperm pollen grains represent rel- 
atively advanced primitive (і.е., monosulcate) 
angiosperm pollen that is already too specialized 
to Lote able T үем anything about the origin (or 

Fi nally, what can be deduced about the ‹ origin 
and early evolution of the flowering plants from 
fossil and living primitive angiosperms is con- 
sidered. It is concluded that the ancestry of the 
angiosperms must be sought in the pterido- 
sperms sensu lato, or more probably in some as 
yet unknown derivative of this group of cycad- 
ophytic gymnosperms. Following this, a 5-stage 
model of early angiosperm evolution is pro- 
posed, based on the early (Barremian to Middle 
С аса л d Po c : 


plants and the inferred phylogenetic relation- 
ships of living primitive angiosperms and their 
immediate derivatives. 

Stage 1 of this model constitutes the yet un- 
discovered pre-Barremian evolution of angio- 
sperms with primitive monosulcate pollen of the 
Magnolia-type, and represents the evolution of 
the *Lower Magnoliidae," i.e., dicotyledonous 
angiosperms whose descendants include such 
living primitive flowering plants as the Magno- 
liaceae and Degeneriaceae. The fact that mono- 
cotyledonous pollen and advanced monosulcate 
dicot pollen occur together in the Barremian sug- 
gests that monocots had already separated from 
dicots by then. Stage 2, which begins in the Bar- 
remian, is represented by the evolution of an- 
giosperms with advanced monosulcate pollen, 
and includes both dicotyledonous pollen types, 

such as Clavatipollenites, and monocotyledon- 


" including the family Chlorantha- 
ceae. The development of tricolpate pollen in the 
Early Aptian of Africa-South America, i. P. West 


the origin of the *Lower Hamamelididae" (i.e., 
angiosperms whose descendants include such 
families as the Trochodendraceae, Tetracentra- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 | 


ceae, Cercidiphyllaceae, Eupteleaceae, Hama- 
melidaceae, and Platanaceae) from the “Higher ' 
agnoliidae." The evolution of tricolpor(oid)ate | 
pollen in the Mid e-Late Albian constitutes Stage 
4, which probably represents the beginning of 
the differentiation of the angiosperm subclasses 
Rosidae and Dilleniidae from the “Lower Ham- 
amelididae" since both of these dicot subclasses 
The final 
phase of early angiosperm evolution, Stage 5, ¦ 
begins in the Middle Cenomanian wi 
appearance of triporate pollen (especially of the 
N lles type i nd North America, 


i.e., West Laurasia). This stage probably repre- 
sents the initial differentiation of the “Higher 
Hamamelididae," whose descendants include 
such angiosperm families as the Betulaceae, Cas- 
чаас, as and jens 


n out- 


lined above suggests the following model for the 
early adaptive evolution of the flowering plants | 
From an original complex of “basic епіоторі" 
ilous angiosperms” that had “tepalar” petals, sand | 
whose living descendants are today included in | 
such orders as the Magnoliales, Laurales, an and | 


advanced magnoliid angiosperms, 
Chloranthaceae, as well as related “Lower pe 
amelididae," such as the T rochodendrales, Ct : 
cidiphyllales, and Hamamelidales. The pe: | 
for this early reversion back to the wind eo 
nation that characterized the вутпоря КЫ 
ancestors of the flowering plants may have 
connected with the increasing aridity (and ed 
sible decline in insect d d wee] 
occurred soon after the earli wem 3 | 
Ат 


angiosperm pollen of the кт 
in the Barremian of Africa + Go 
at the time that major splitting of ind 
wana was taking place. The major! ae | 
dicots, including the subclass Rosidae ber 
he e as well, apparen 

in the miu Albian fro 
emophilous angiosperms. This mar y 
ginning of the first major adaptive radiati 


ел" | 
tricolpate (as opposed to monosulcate) P^ r 


[m2 


m 
i s po in 
or smulus for this medii e 
j have been 


history of flowering plants may f dico e 
secondary return of the main line фи 
donous flowering plants back to €n ы 


1984] 


This secondary return to entomophily appears 
to be correlated with the evolution of new “‘stam- 
inodial” petals that replaced the more primitive, 
i “basic ento- 


” such as the Chloranthaceae, changed 
from оу to anemophily. 


LITERATURE CITED 


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BRENNER, G. J. 3. The spores and pollen of the 
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‚ P. BIENS, A. ранга». JARDINE. 1977. 

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xplor.-Prod. Elf-Aquitaine 1: 451-473. 

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0. 
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———————— 


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1984] WALKER & WALKER—LOWER CRETACEOUS POLLEN 521 


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Evolutionary Significance of the Exine. Academic 

Press, London 


CUTICLE EVOLUTION IN EARLY CRETACEOUS 
ANGIOSPERMS FROM THE POTOMAC GROUP OF | 
VIRGINIA AND MARYLAND! 


GARLAND R. UPCHURCH, JR.? 


ABSTRACT 
Studies of angiosperm leaf cuticles from the Lower Cretaceous Potomac Group reinforce previous 
evidence for a Cretaceous adaptive radiation of the flowering plants and suggest unsus ed tre 
in the evolution of stomata and trichomes. Early Potomac Group angiosperm leaf cuticles (Zone I of 
оу у 1:++1 2 3 zu di Tt 3 dios ^ $ тра 


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leaf affinities to Platanaceae and Rosidae. The stratigraphic trend in cuticle types supports the concept 


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itive for the flo ering plants, may actually be derived from the variable condition found in Zone I 
leaves. 


Within the past 15 years there has been a major 
reevaluation of the Cretaceous flowering plant 
record and the role of fossils in angiosperm phy- 
logeny. Formerly, it was thought that fossils could 
provide little evidence on the course of angio- 
sperm evolution, since even the earliest known 
remains were believed to represent modern fam- 
ilies and genera (Axelrod, 1952, 1970). This view, 
based on older studies of leaf remains such as 
those by Fontaine (1889), Ward (1905), and Ber- 
ry (1911) for the Potomac Group, has been 
strongly contradicted by more recent analyses of 


1; Wolfe et al., 1975; 
Doyle & Hickey, 1976; Hickey & Doyle, 1977; 
Hickey, 1978). These newer studies show that 
practically all of the older leaf identifications are 
incorrect and that successively younger Creta- 
ceous angios floras show the progressively 
higher levels of advancement predicted by many 
modern systems of classification (cf. Cronquist, 
1968, 1981; Takhtajan, 1969, 1980; Thorne, 
1976). These results indicate that the Cretaceous 


was a period of major angiosperm diversification | 
and that paleobotanical studies should continu? | 
to yield new evidence on the course and timing 
of flowering plant evolution. КТЕ 
One largely untouched 0 | 
lar anatomy. Despite the fact that cuticles have 
long provided important characters for the SYS | 
tematic placement of Mesozoic gymnosperms 
Tertiary angiosperm leaves (e.8.. 


solely on leaf architecture (e... venation, we 
I began a study of angiosperm leaf cun | 
the Lower Cretaceous Potomac Group 0 ја i 
ginia and Maryland to test previous ideas O 


i ; ticular | 
early flowering plant evolution. At first, CU d 


0 
Brenner, or probably middle to late Albian), е | 
later on, organically preserved leaves | 
lected from the lower part as well (Рајупог ded | 
of Brenner, ог probably Aptian). This | 


' I would like to thank James Doyle, Leo Hickey, and Charles Beck for their guidance and ence ing eat) | 
during the course of this project; James McClammer for his help in the field; and my wife Amy for YP od | 


drafts of this manuscript. This work represents doctoral research conduc 
postdoctoral research conducted at the Smithsonian Institution 


1 of Graduate Studies and Scott Turner Fund, University of Michigan, and a ро 


fellowship from the Smithsonian Institution 
2 Paleont 


Colorado 80225. 


ANN. Missouri Bor. GARD. 71: 522—550. 1984. 


ogy and Stratigraphy Branch, U.S. Geological Survey, M.S. 919, 25 Denver Federal Center: 


ted at the University of Michi”. 
esearch was supported by grants Бог ! 


репу | 


1984] 


the opportunity to compare the stratigraphic 
changes seen in the systematic affinities and 
structural diversity of angiosperm leaf cuticles 
with those observed for leaf architect d pol- 
len morphology. This report summarizes the re- 
sults of this investigation and their possible sig- 
nificance for flowering plant evolution: included 
are а comparison of the diversity of cuticular and 
leafarchitectural features, nt of mod- 
егп affinities based on cuticular anatomy, and 
two major evolutionary trends suggested by the 
morphological relationships of cuticular features 
in conjunction with their stratigraphic distribu- 
tion. 


MATERIALS AND METHODS 


All organically preserved leaf types known from 
Zone I and Subzone II-B were prepared using a 
combination of standard methods (cf. Dilcher, 
1974). For light microscopy, cuticles were de- 
mineralized in HF, macerated in Schulze's so- 
lution followed by dilute alkali, stained in an 
aqueous solution of Safranin O, and mounted on 
slides in glycerine jelly. Preparations for scanning 
electron microscopy (SEM) varied according to 
the surface studied. External features were ob- 
served on unmacerated, demineralized leaf frag- 
ments. Internal features were observed on mac- 
erated cuticle that was dried down to SEM stubs 
coated with Duco cement in a chamber saturated 
with acetone vapor. All specimens were coated 
with gold and observed at 15 kV. 


DERE slurry through 100 mesh screen. 
Fg ed plant fragments were prepared as 
егіпе a a centrifuge, and mounted in glyc- 
n "s k on slides or in glycerine between pairs 
а dii n-sealed cover slips. Naturally macer- 
aa cle was mounted in glycerine in paraffin- 
ed slides pending further study. 

i ns aaa leaf cuticles were examined 
Ging | eas on the relationships of Potomac 
‘ete rb to modern forms. Taxa were se- 
м + Study based on two criteria: 1. their 
лоб Primitiveness according to the phylo- 
Такма; schemes of Cronquist (1968, 1981), 
2 tc 1 969, 1980), and Thorne (1976), and 
байра Similarity to Potomac Group angio- 

sin leaf venation and pollen morphology. 


UPCHURCH—CUTICLE EVOLUTION 


523 


Observations were made on cuticle slides in the 
Indiana University paleobotanical collections, 
cleared leaves at the United States National Mu- 
seum, and cuticles prepared by myself for light 
and scanning electron microscopy. Light micro- 
scope preparations were made from leaf frag- 
ments that were macerated in modified Jeffrey’s 
solution (Stace, 1965), stained in Safranin O, then 
mounted in glycerine jelly or Piccolyte. SEM 
preparations were made in a manner similar to 
that for the fossils, except that unmacerated leaves 
were either boiled or shaken ultrasonically in eth- 
anol for 30 minutes to remove the waxes and 
adhering debris. All specimens were coated with 
carbon, then gold/palladium, and observed at 20 
V. 


RESULTS 
ZONE I ANGIOSPERM LEAVES 


Zone I angiosperm leaves exhibit low diversity 
in their venation, shape, and marginal configu- 
ration compared to later Cretaceous and modern 
flowering plants. All Zone I leaves are simple 
and have pinnate venation, although in some 
groups the secondary veins are clustered or 
strengthened near the base of the leaf (also re- 
ported by Hickey & Doyle, 1 977). Most leaftypes 
possess festooned brochidodromous secondary 
venation (or secondaries that form several orders 
of loops within the margin) (e.g., Fig. 2), but 
Vitiphyllum multifidum and a new serrate form 
have simple craspedodromous secondary vena- 
tion (or secondaries that run directly into lobes 
or teeth) (Fig. 1). The teeth of at least some leaf 
groups are a variant of the Chloranthoid type of 
Hickey and Wolfe (1975), with a biconvex shape, 
a large gland, and a pair of lateral veins that 
follow the margin and fuse with the gland (Fig. 
4). Zone I leaves also show a low systematic di- 
versity compared to later Potomac Group an- 
giosperms: only 12 leaftypes are recognized from 
Zone I, as opposed to over 30 from Subzone II-B 
(Hickey & Doyle, 1977). 

The most distinctive feature of Zone I leaf ar- 
chitecture is the low degree of organization in 
the vein network. Secondary veins are irregularly 
spaced, enclose areas of variable size and shape, 
and often branch decurrently (e.g., Fig. 2). Ter- 
tiary and higher order veins are poorly differ- 
entiated from tl lari dł d 
course. This “first rank” pattern of venation oc- 
curs today in such primitive families as Winter- 
aceae and Canellaceae and is considered primi- 


524 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


буа 


obovatum, UMMP 64865, х3.—6. Cf. Ficophyllum. UMMP 65101, x3. 


tive for the dicots by Hickey (1971, 1977). Some 
authors (Wolfe et al., 1975) have suggested that 
several Zone I leaf types actually may be more 
primitive than anything extant, because they show 
even less vein regularity than any modern an- 
giosperm. 
All Zone I leaves with cuticle come from a new 
locality at the north end of Drewrys Bluff, on the 
James River near Richmond, Virginia. These 
leaves are dated palynologically as upper Zone I 


of Brenner, or probably Aptian (Doyle, 


(Мог. 71 


int 


ed in in 
4859, x1.5.—4. DBLT #1, close-up sh nee 
MP 64887, x8.—5. Cf. Celastrop 


pw 


comm.), and thus are similar in age to af 

sperm leaves reported from the southern d 

the exposure (Hickey & Doyle, 1977). rd 
ocality, tw f 


types are present at this 1 


are serrate. The most abundant form 1 


is an ш” 
per 


scri 
Drewrys Bluff Leaf Type #1 (DBLT #1), ye 
has simple craspedodromous secondary 


tion and Chloranthoid teeth (Figs. 1, 


4). The oth- 


1984] 


er serrate leaf type has festooned brochidodro- 
mous venation, as in other Potomac Group 
species of Celastrophyllum, but differs in its low 
number of secondary veins and lack of a distinct 
petiole (Celastrophyllum sp., Fig. 2). Of the three 
entire- ined forms, Eucalyptophyllum ob- 
longifolium has a midrib composed of two fusing 
vascular strands, numerous irregularly spaced 
secondary veins that connect with a prominent 
intramarginal vein, and only three orders of ven- 
ation (Fig. 3). This suite of features in combi- 
nation with the leaf’s elongate areolation, is un- 
known in extant flowering plants (Wolfe et al., 
1975; Hickey & Doyle, 1977). The other two 
groups are less unusual. One has an obovate 
shape, closely spaced, brochidodromous second- 
ary veins, and random reticulate tertiary vena- 
tion: it resembles the Celastrophyllum obovatum 
complex from Baltimore but differs by its much 
smaller size (cf. C. obovatum, Fig. 5). The other 
consists of fragments comparable to some spec- 
imens of Ficophyllum Font. in their reticulate 
pattern of tertiary and higher order venation (cf. 
Ficophyllum, Fig. 6). Certain characteristic Zone 
leaf types, such as pinnately lobate forms (Vi- 
tiphyllum Font.), elongate obovate leaves (Ro- 
8ersia Font.), and reniform leaves with basall 
Congested secondary veins (Proteaphyllum reni- 
forme Font.), are absent. Roughly one-third of 
the leaf types from Zone I are known with cuticle, 
since about 12 have been previously recognized 
for this interval (Hickey & Doyle, 1977). 
Dispersed angiosperm cuticle is known from 
two Zone I localities on the James River: 1, the 
Drewrys Bluff angiosperm leaf bed, palynologi- 
cally dated as upper Zone I, and 2, Dutch Gap 
Canal, Palynologically dated as lower Zone I 
"n^ Doyle, 1977; Upchurch & Doyle, 
vint t least six cuticle types not known from 
‚© leaves are present in these assemblages. 
= : brings the total number of cuticle types up 
1, which suggests that much of the systematic 


~ of Zone I leaves may be represented in 


‘ystematic value in extant angiosperms, while 
lim. ГЕ most variable in traits that tend to have 
195 pu significance (cf. Metcalfe & Chalk, 
> Stace, 1965; Van Staveren & Baas, 1973; 
Reo y & Baas, 1973). In particular, Zone I leaf 
€s are relatively uniform in plan of stomatal 


UPCHURCH —CUTICLE EVOLUTION 


525 


construction, hair base structure, and types of 
secretory cells. More variation is present in pat- 
terns of cuticular sculpture, particularly on the 
outer cuticle surface. Traits such as cuticle thick- 
ness and cell contour are highly variable and of 
little value except in the identification of species; 
hence they are not discussed in the following 
paragraphs. 

The stomatal complex shows a typically an- 
giospermous plan of construction. In the guard 
cells of all species the stomatal poles are level 
with the stomatal pore, rather than raised, as in 
most gymnosperms (Harris, 1932). The stomata 
of most forms are level with the epidermis, but 
are distinctly sunken in Eucalyptophyllum (Fig. 
7). The guard cells often bear cuticular ridges on 
their outer walls, or outer stomatal ledges (Fig. 
7, OSL), and in many groups there are lamellar 
thickenings (Fig. 8, L), which are typical of prim- 
itive extant Magnoliidae (Baranova, 1972; Up- 
church, unpubl. data). These lamellar thicken- 
ing ly associated with outer stomatal 
ledges, or else tend to intergrade with them. In 
addition, Dispersed Cuticles #1 and #3 bear 
strongly developed, T-shaped thickenings at the 
stomatal poles, or T-pieces (Figs. 8, 12). Such 
thickenings are present in diverse angiosperms, 
including the primitive family Illiciaceae (Bailey 
& Nast, 1948). 

The arrangement of the subsidiary cells in all 
investigated species of Zone I angiosperms ex- 
hibits unusually high variation compared to that 


absence of subsidiary (or specialized) cells and 
their arrangement relative to the guard cells. In 
contrast, the stomata on a single Zone I angio- 
sperm leaf fit into several of the conventionally 
recognized types as well as intermediates. This 
situation makes it necessary to analyze stomatal 
structure in a new way. In brief, a population of 
about 50 to 100 stomata is examined for ten 
features that contribute to the variation in sto- 
matal structure for at least one species of Zone 
1 angiosperm leaf. The range of variation in each 
is then recorded and the data are displayed in 
tabular form to facilitate comparisons between 
species (e.g., Tables 1-4). The ten major com- 
ponents of stomatal variation fall into three ma- 
jor categories: 1. the number and position of the 
contact cells (or those cells abutting on the guard 
cells), 2. the position of specialized contact cells, 
and 3. the position of specialized non-contact 


526 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


FIGURES 7-12. Zone I angiosperm leaf cuticles.—7. Euca/ hyll ing electron microgra ph of out 
surface, lower cuticle. Note sunken stoma and two types of striations. UMMP 64862, x 1,000.— 8. D 
MP 


x800.—9. Eucalyptophyllum, paracytic stomata. UMMP 64862, x400.— 10. 

and other stomatal types. UMMP 64862, х 400.—11. Dispersed Cuticle #3, paracytic stoma. Also note in 
solid papillae with radiating striations. UMMP 65126-56, x 400.— 12. Same, close-up of another stoma show 
concentric striations and T-pieces. UMMP 65126-56, x1 000. — 


1984] UPCHURCH —CUTICLE EVOLUTION 527 
TABLE 1. Stomatal features of selected Zone I angiosperms. 
Dispersed Dispersed 
Eucalyptophyllum cf. Ficophyllum Cuticle #1 Cuticle #3 
Number of contact 4-6 4-5 4-5 4-7 
cells 
Number of lateral 2-4 2-3 2-3 2-4 
contact cells (LCCs) 
Stomata with special. sometimes sometimes sometimes always 
ized LCCs? 
LCC specialization one or both guard one or both guard one or both one or both guard 
pattern within sto- cells cells guard cells cells 
ma 
LCC specialization either full or partial either full or partial mostly full either full or partial 
pattern along length length length length length 
of guard cells 
Number of polar con- 2-3 2 2-3 2-3 
tact cells (PCCs) 
Stomata with special- sometimes sometimes sometimes sometimes 
ized PCCs? 
PCC specialization one or both poles one or both poles one or both one or both poles 
pattern poles 
Other specialized sometimes never sometimes sometimes 
cells? 
Position of other spe- variable — mostly lateral ^ lateral 
cialized cells 
Number of variable 10 y 10 8 
features . 
Stomatal types? P, Lc, C, and inter- Р, H, A, and inter- Р, Lc, and H, P (common); H and 
mediates (com- mediates (com- all inter- transitional be- 
mon); H and A mon); weakly C grading with tween Le and C 
rare) (rare (rare 


“Key: P = paracytic; Le = laterocytic; C = cyclocytic; H = hemiparacytic; A = anomocytic. 


cells, The stomata of Zone I angiosperms are 
Me for at least seven of these features, with 

ucalyptophyllum showing variation in all ten. 
Some of these features are variable in a number 


к: alized polar contact cells, and the pres- 
Се or absence of specialized non-contact cells. 
within extant species; 
(orLC l components of lateral contact cell 
found C) specialization. First, modified LCCs are 
leaf sba many stomata, yet in others on the same 
ey are lacking entirely (e.g., Fig. 10); the 


ма is Dispersed Cuticle #3, which always 


Sesses modified LCCs, they may occur along both 
Buard cells (e.g., Fig. 13, P, Lc) or else just one 


of them (Fig. 13, H). Finally, when a guard cell 
is flanked by one or more specialized LCCs, they 
often extend only part of the length of the stoma, 
rather than the full length (e.g., Fig. 14, arrow). 
This variation produces stomata that could be 
classified as anomocytic (Fig. 10, A), hemipara- 
cytic (Fig. 13, H), paracytic (Figs. 9, 11, 13, P), 
laterocytic (Fig. 13, Lc), weakly cyclocytic (Fig. 
13, C), and intermediates. This extreme plastic- 
ity in subsidiary cell organization, which is rare 
: P С у ae ја А : 


+ 


а low degree of regularity, analogous to that pres- 
ent in the venation of these and other Zone I 
leaves. 


f * Б $42 aS 1 Г. 


А ѕигуеу of extant р | t 
groups with stom tal variation approaching that 
seen in Zone I. Most Magnoliales are paracytic 
(Baranova, 1972; Bongers, 1973; Koster & Baas, 


528 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Уо 71 
TABLE 2. Stomatal features of selected Magnoliales. 
Family Winteraceae Myristicaceae Magnoliaceae 
Drimys pn 
Genus (Old World) Knema Manglietia Liriodendron 
Number of contact cells 4-6 4, rarely 5 3-5 4-5 
Number of lateral contact cells (LCCs) 2, rarely 3 2, very rarely 2-3 
3 
Stomata with specialized LCCs? always always always always 
Both guard cells of stoma with special- always always always always 
ized LCCs? 
ОСС specialized full length of adjacent always always always always 
guard cell? 
Number of polar contact cells (PCCs) 2-4 2, rarely 3 1-2 2-3 
Stomata with specialized PCCs? never never never never 
PCCs specialized at both poles? -— — E m 
Other specialized cells? sometimes sometimes sometimes sometimes 
Position of other specialized cells lateral lateral lateral lateral 
Number of variable features -3 -3 ~3 4 
Stomatal types* P, rarely Lc P, rarely Lc or P, rarely Lc P and Lc 
subdivided P E 
* Key: P = paracytic; Lc = laterocytic. 
TABLE 3. Stomatal features of selected Magnoliales. 
Family Canellaceae _ Winteraceae _____ 
Drimys eae 
Genus Pleodendron Warburgia (New World) Takhtajania 
Number of contact cells 4—6 6-9 4-5(-6-7) 4-5 
Number of lateral contact 2-3(-4) 3-5 2-4 2-3 
cells (LCCs) 
One ог more specialized always always always sometimes 
LCCs in each stoma 
LCCs specialized for both always always always sometimes 
GCs? 
LCCs specialized full usually, not al- always often, not al- sometimes ызаны ое 
length GC? ways ways tact cell ov ps 
GC side) 
Number of polar contact 2-3 3-4 2-3 2 
cells 
PCCs specialized in each rarely sometimes never never 
stoma? 
PCCs specialized at both sometimes sometimes — a 
poles? 
Other specialized cells? sometimes always one or more sometimes never 
Specialization pattern lateral lateral; sometimes lateral 9 
polar also 
Number of variable fea- 7 5 (4-)5 
tures 
Stomatal types* P LoC Lc, C Р Lc A, P 
> = to 
Remarks LCCs strongly 4 stomata 1 pho 
compressed 


* Key: P = paracytic; Le = laterocytic; C = cyclocytic; A = anomocytic. 


1984] 


TABLE 4. Stomatal features of selected Laurales and Illiciales. 


UPCHURCH—CUTICLE EVOLUTION 


529 


Austro- Schisan- 
Family Amborellaceae Chloranthaceae baileyaceae draceae 
Austro- 
Genus Amborella Chloranthus Sarcandra baileya Schisandra 
Number of con- 4-6 4-5 4—6 4—6 4—6 
Number of lateral 2-3 2-3 2-4 2-4 2-4 
contact cells 
Stomata with spe- always always always always always 
cialized LCCs? 
Both guard cells sometimes sometimes always sometimes always 
of stoma with 
specialized 
LCCs? 
LCCs specialized always for one guard sometimes always sometimes sometimes 
full length of cell, other one vari- 
adjacent guard 
cell? 
Number of polar 2-3 2-3 2-3 2-4 2-4 
contact cells 
(PCCs) 
Stomata with spe- sometimes occasionally sometimes never never 
cialized PCCs? ш 
PCCs specialized ^ sometimes usually always ша m 
at both poles? 
Other specialized sometimes sometimes sometimes sometimes sometimes 
cells? 
P sition of other ^ mostly lateral lateral mostly lat- lateral lateral 
specialized cells eral 
umber of vari- ~8 8 5 6 5 
able features 
'omataltypes Р (common): Іс, Н, Р, Іс (соттоп); Н, P,Lo C Р, Іс(сот- Р, Le 
С, and intermedi- C, and intermedi mon); H 
ates (uncommon) ates between Lc (uncom- 
mon) 


and C (rare) 


AMA ae 
Key: Р = paracytic; Lc = laterocytic; С = cyclocytic; Н = hemiparacytic. 


meee 1981) and those that are not show 
regularity than Zone I forms in the ar- 
с and specialization of their contact cells 
£8 2, 3). Greater variation is present in some 
rales (including Chloranthaceae) and Illici- 
but few taxa approach the extreme condi- 
und in Zone I. The closest approaches are 
15, бе E vesselless family Amborellaceae (Figs. 
(Chior, anthus serratus), which are identical to 
e. Cuticle 43 in almost all of their sto- 
1 Зу (Table 4). Austrobaileyaceae = 
4 bl one 


tion fo 


; 
orms in most respects, but differ by having 


uniformly unmodified polar contact cells (Table 
4). Finally, the vesselless genus Sarcandra 
ranthaceae) resembles Zone I angiosperms 


terns of specialization in polar and non-contact 
cells, but differs by having a much more uniform 
pattern of lateral t cell modification (Table 
4). These similarities suggest that many Laurales 
and Illiciales are closer to Zone I angiosperms in 
their level of stomatal advancement than most, 


from Zone I angiosperms, in contrast to the di- 
verse array found in Tertiary and extant flow- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


FIGURES 13, 14. Drawings of Zone I angiosperm stomata.— 13. E ердә. m a hemipara- 
x 


cytic (H), laterocytic (Lc), and weakly cyclocytic (C) stomata. UMMP 64892 


0.—14. Cf. Ficophyllum, 


aracytic and unclassifiable stomata. Note how the lateral contact cells in one stoma are modified for only 
part of the length of the adjacent guard cell (arrow). UMMP 65107, х 250. 


ering plants (cf. Roselt & Schneider, 1969; Dil- 
cher, 1974). Unlike many angiosp hair bases, 
which show complex plans of construction, both 
Zone I types are simple, consisting of a single 
foot cell (to which the hair was attached) and 
several unmodified base cells. The first type, 
found in Eucalyptophyllum and DBLT #1, con- 
sists of a small, thickened, polygonal foot cell 
and several base cells that underthrust it (Fig. 
19). No attached hairs or distinct abscission scars 

known, raising the possibility that the “foot 
cells" are actually idioblasts, but circular depres- 
sions occur on the outer walls of some cells. Sim- 
ilar “foot cells” are found in a variety of extant 
angiosperm families, including Chloranthaceae, 
Illiciaceae, and Dilleniaceae (Upchurch, unpubl. 
data). The second type of hair base, found only 
in Dispersed Cuticle #3, is similar to the first in 
its size, shape, and degree of base cell under- 
thrusting. It differs in having a thickened cuticle 
only on the outer wall of the foot cell and in 
having a trichome abscission scar, which consists 
of a pore (Fig. 20). Similar hair bases are found 
in an Eocene species of Schisand (Schisan 
dra europaea, cf. Jáhnichen, 1976), but these dif- 
fer from the Potomac Group type in having a 
more circular pore and strongly specialized base 
cells. 


Secretory cells are present on the lower epi- 
dermis and in the mesophyll of many Zone I 


leaves and these strongly resemble the = e 
found in extant primitive angiosperms (T a И 
Two major types occur on the lower epidermis. 


The first, found in Eucalyptophyllum and two — 


i to 
dispersed cuticle groups (Fig. 21), has a round 


mewhat angular outline and a йш, ЖОШ 
includ- 
ühni 


chen, 1976; Upchurch, unpubl. data). ke e 
ond type of secretory cell, ies d 
Eucalyptophyllum, DBLT #1, and Disper 

ticle *6, and here termed the radiostriat ШЕ 
(Fig. 22), has an angular outline and pue 
that radiate from its periphery. Similar 0 et 
are present on the lower epidermis of a few 
noliales, many Laurales (Fig. 23), 
of Illiciales, and Saururaceae of the Pipe 
(Bailey & Nast, 1948; Upchurch, un о 
Finally, mesophyll secretory cells are pe 
cf. Ficophyllum and both species of a 
phyllum (Fig. 24). These cells аге roune, 

10 um in diameter, and contain dar k su f divers 
They resemble the mesophyll oil cells he А 
modern Magnoliidae in their "m нш 


ntents 


1976; Upchurch, unpubl. data). er 

Several types of cuticle sculpture are pp 
Zone I angiosperms. Surface sculpture che 
to three of the four major types listed by 


1984] UPCHURCH—CUTICLE EVOLUTION 


FIGURES 15— 20. Гале аЙ epe 


—15. 
sh 
о = Variation in the pattern of lateral contact cell COs specialization along the 
opoda, lower cuticle, stomata showing 
F. Thorn 


m, #28348, x400.— 
pesti — cuticized tangential 
stoma. Arnold 
MMP 


y Herbarium, В. F. Thorn be ine x400.—16 үзүү tric. 


heat tum, L. J. Bass #18160, x —18. Austrobaileya sp., 
64860" "Ter, L. J Bass #18160, x 400.— 19. аец a 


531 


Amborella trichopoda, lower ics stomata 
he of each guard cell. 


532 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


TABLE 5. Secretory cell types of Zone I angiosperms. 


(Мог. 71 


Systematic 
Distribution, Systematic Distribution, 
Location Description Zone I Modern Flora 
1. Lower round-subangular in sur- Eucalyptophyllum Laurales: Calycanthaceae 
epidermis face view, outer cuticle Dispe Cuticle #5 Chloranthaceae 
smoot Dispersed Cuticle #6 Illiciales: Illiciaceae 
Schisan 
2. Lower strongly angular in surface — Eucalyptophyllum Magnoliales: Annonaceae? 
epidermis view, outer cuticle with DBLT Eu matiaceae 
radiating striations Dispersed Cuticle #6 Laurales: iro ОВО 
Gomortegaceae 
Monimiaceae 
Trimeniaceae 
Illiciales: Illiciaceae 
Schisandra 
Piperales: Saururaceae 
3. Mesophyll spherical, with thin walls Celastrophyllum sp. мие all families 
d dark contents cf. C. obovatum Laurales most families 
cf. Ficophyllum Iliciales: both families 


Piperales 
Aristolochiaies: single family 
cniales: Зе ee 


(1974). Psilate (or smooth) sculpture occurs in 
several different cuticle types. Papillate (or 
knobbed) sculpture is present in several dis- 
persed cuticle types and commonly the papillae 
are partially solid, as in Dispersed Cuticle #3 
(Fig. 11). Finally, striate (or ridged) sculpture is 
present in many Zone I groups; this is organized 
into two distinct patterns. The first, found in both 
DBLT #1 and Dispersed Cuticle #3, consists of 
striations which traverse cell boundaries and dis- 
play two orientations near the stomata: some 
striations are oriented concentric to the stomatal 
pore while others either have a random arrange- 
ment or radiate from the stomata (Fig. 25). This 
condition is characteristic of many extant prim- 
itive dicot groups, including Illiciales, many 
Laurales (Fig. 26), and at least some Piperales 
(Saururaceae, Upchurch, unpubl. data). The sec- 
ond, found only in Eucalyptophyllum, consists 
of two distinct size-classes of striations that dis- 
play markedly different behavior: the smaller ones 
traverse cell boundaries and radiate from the sto- 
mata, while the larger ones are confined to one 
cell each and enclose polygonal areas that mimic 
the shape of the underlying cell (Fig. 7). To date 
this pattern has not been observed in any extant 
group of angiosperms, but individual elements 
occur in scattered families, including Chloran- 
thaceae (Upchurch, unpubl. data ta). 


SUBZONE II-B ANGIOSPERM LEAVES 


Subzone II-B angiosperm leaves show а much 
greater diversity of leaf architectural features 
Zone I forms, but still less than in Late Creta- 
ceous and modern flowering plants. Unlike де 
I angiosperms, Subzone II-B leaves n ње 
simple and compound forms and po e с 
new types of primary venation. Be u 


ith pri- 
has actinodromous primary venation, with P' 


35). The “platanoids” are palinactiaodro ш 
with primary veins that all diverge from p 
points (e.g., Fig. 31), and Menispermites 

macensis is acrodromous, with latera! p A: 
that curve towards the apex (Hickey x 
1977). Secondary venation is also more 


ondary venation, with secondary 
only one order of loops (cf. Hickey 
1977; Upchurch, unpubl. data). Some. 
dopsis leaflets have сосаи мо E ва 
ary venation, with secondaries that gra 

towards the apex and do not join wi deos 
praadjacent secondary veins (Fig. eos dan 
ers possess mixed craspedodromous ойгото 
venation, with a mixture of crasped 


1984] UPCHURCH—CUTICLE EVOLUTION 533 


Am 21-26. Cuticles of extant and Zone I angiosperms. —21. secca ушт, epidermal secretory 
234, WS). UMMP 64862, x400.—22. Dispersed Cuticle #6, radiostriate secretory се (arrow). UMMP 
cedi E 2 Austrobaileya sp., scanning electron mi A o ph of к= анн hm Tiris 
64865, x пр а 1. as res x 400. cde СЕ Celastrophyllum obovatum СИМЕ 64884-G157. 
Pes —26. mins sp., scanning electron micrograph of stomata showing concentric striations. Arnold 
retum, L. J. Bass #18160, х 400. 


534 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


tifid lea 
FIGURES 27-32. Organically "dicssa Subzone II-B leaf types.— 27. чира МА Pis seconda 
UMMP 65110, x1.—28. Leaflet of cras 
venation. Bend 63111, x2.— 29 T 1 
pedodrom ndary venation. UMMP 65112, x2.—30. Platanoid #3, basal portion о Р 65104, * 
х1.—31. Pateioid #2. ОММР 65105, х1.—32. Platanoid bw berum portion of leaf. UMM 


1984] 


and camptodromous secondary veins (Fig. 29). 
Finally, there are more tooth types present in 
Subzone II-B than in Zone I: in addition to con- 
vex-convex (A-1) teeth there are concave-convex 
(C-1) teeth with features of the Rosoid tooth type 
of Hickey and Wolfe (1975) in some pinnately 
compound specimens of Sapindopsis (Fig. 29) 
and straight-convex (B-1) teeth in a new serrate 
leaf from the Red Point locality of Hickey and 
Doyle (1977). 

A key difference between Zone I and Subzone 


т Ва: 


: А, ше B tenacity 
in the latter for greater vein regularity: generally 
the veins have a more regular course and the 

ish from 


different vein orders are easier to distingui 

one another. While the older “first rank" syn- 
drome is retained in many leaf groups, some, 
such as many pinnately compound Sapindopsis, 
are “second rank,” with secondary veins that are 
regularly spaced and enclose areas of similar size 
and shape. Others, such as Platanoid #3, have 


rank” syndrome. This greater venational regu- 
larity suggests that many Subzone II-B leaves are 
more advanced than their Zone I counterparts. 
However, the fact that leaves with “fourth rank” 
venation, with an organized system of areoles, 
do not appear until the Late Cretaceous indicates 
Subzone II-B angiosperms still do not have 

е level of advancement of many Late Creta- 
1978) and modern flowering plants (Hickey, 


Rise pa angiosperm leaves are known from 
Do x ү major leaf localities of Hickey and 
in ies > Опе, the Bank near Brooke locality 

егп Virginia, falls in the lower ог middle 
Part of Subzone II-B. The other thre e, all found 


" Maryland, are assigned to the upper part of 


(Fig. 2 ng to Sapindopsis variabilis Font. 
'8. 27), 2) pinnately compound leaves and iso- 


b ^ 
Y Hickey and Doyle (1977) (Figs. 28, 29), (3) 
types of palinactinodromous, trilobate 


| 2 
“aves and similar fragments belonging to the 


UPCHURCH—CUTICLE EVOLUTION 


535 


**platanoid" complex (Figs. 30-33), (4) actinod- 
romous cordate leaves belonging to Populophyl- 
lum reniforme Font. (Fig. 35), (5) a leaf with a 
lobate base referable to Menispermites poto- 
macensis Berry (Fig. 36), and (6) a new species 
of small, elongate leaf with numerous straight- 
convex (B-1) serrations (Fig. 34). These forms 
represent a large part of the range in morphology 
seen in Subzone II-B leaves, even though they 
constitute only a small fraction of the species (cf. 
Hickey & Doyle, 1977). 

Subzone II-B angiosperm leaves show greater 
diversity in their cuticular structure than Zone I 
forms, particularly in stomatal organization. 
Three new patterns of variation in subsidiary cell 
arrangement are present in addition to the older 
one, but all of the stomatal types in each new 
pattern occur as variants in the Zone I pattern. 
New types of secretory structures (and their ho- 
mologous hair bases) also are found and these 
how numerous similarities to Zone I types, sug- 
gesting their derivation from them. The system- 
atic distribution of new cuticular features shows 
a strong correspondence with many of the leaf 
architectural groups recognized by Hickey and 
Doyle (1977); as a result they are described by 
group rather than by character. 

The fewest new stomatal features are found in 
Populophyllum reniforme Font., a cordate, ac- 
tinodromous leaf from the Bank near Brooke 
(Fig. 35). The guard cells differ from those in 
many Zone I forms by possessing outer stomatal 
ledges but lacking lamellar thickenings entirely 
(Figs. 37, 38). In addition, the guard cells often 
appear to be embedded in the adjacent cells, un- 
like earlier forms (Fig. 38). But despite these new 
features Populophyllum retains the pattern of 

11 tand ializati ound 


wn 


contact се 
in Zone I, having up to ten variable features in 
some specimens (Table 6). This pattern most 
closely resembles that of cf. Ficophyllum in its 
low percentage of paracytic stomata, but differs 
by its specialized non-contact cells. 

More new stomatal features occur in the new 
serrate leaf from Red Point, which has a char- 
acteristically papillate lower epidermis (Figs. 39, 
40). The guard cells possess lamellar thickenings 
identical to those found in Zone I, but lack sto- 


having a papilla that overarches the adjacent 
guard cell (Fig. 39). This stomatal pattern has 


536 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


enation 


FIGURES 33-36. Organically preserved Subzone II-B leaf types. — 33. Platanoid #3, close-up of “USM 
Serra 


showing tertiary (3°) and higher order 
22285 


65102, x1 


only five variable features, as opposed to seven 
to ten in Zone I forms (Table 6), and is best 
classified as weakly cyclocytic. 

The second new stomatal pattérn occurs in 
Menispermites potomacensis Berry from Stump 
Neck (Figs. 41-43). The guard cells in this species 
are smaller than those in all other Potomac Group 

angiosperms (8—15 um long), but, as in most oth- 


arrangement and specialization, but less than that 


r venation. UMMP 65104, x5.—34. New 
22856, e —35. Populophyllum reniforme. UMMP 65108, x1.—36. Menispermites potomacensis. 


te, Red Point. UMMP 


ver 
seen in Zone I (Table 6). ames andae 
number more than one per guar PCCs at 


extend the full length of the psc pe 
always bete and number io ua 


e features and 
ior type 
g. 42, H): 


pattern possesses only five variable 
has stomata that conform to three та) 
paracytic (Fig. 41, P), hemiparacytic (Fig- 
and anomocytic (Fig. 43, A). tures 

The largest number of new cations e 
is shared by two groups of Subzone Il- 


1984] 


3 

6 

| 5109, х250.—38. Populophyllum reniforme, scanning electron E A 
dd И 


OM been related to one another on the basis 
а architecture: pinnatifid and pinnately 
ee leaves assigned to Sapindopsis (Figs. 

) and trilobate, palinactinodromous leaves 


UPCHURCH—CUTICLE EVOLUTION 


Cuti - i rms.—37. Populophyllum reniforme, 
uticles of Subzone II-B angiospe А gie hats ger 


ensis. UM) outer and inner lamellar thickenings. USNM 222856, 
~ * . ane 
x 600, UMMP 65102.—41. Paracytic stoma, x 600.—42. Hemiparacytic stoma, х 600.—43. 


stomata. UMMP 
wing Outer stomatal 


omocytic stoma, 


of the “platanoid” complex (Figs. 30-33). In both 
groups the guard cells lack lamellar thickenings 
and tend to be slightly sunken (Fig. 44). The 
contact cells also show greater regularity in ar- 


538 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 

TABLE 6. Comparison of Zone I and Subzone II-B stomatal patterns. 

Zone I New Sapindopsis/ 
Taxon Pattern Populophyllum Serrate — Menispermites  Platanoids 

Number of contact cells 4—5(—7) 4-7 6-7 4—5 4-6(-8) 
Number of lateral con- 2-3, 2-4 2-5 3-5 2-3 2-4(-5) 

tact cells (LCCs) 
Specialized LCCs in sometimes/ sometimes always sometimes always 

every stoma? always 
LOCS TT length sometimes sometimes always always almost always 

of stom 
Number n polar con- 2, 2-3 2-3 1-3 2 2-3 

tact cells 
PCCs specialized in sometimes sometimes always never sometimes 

each stoma? 
PCCs specialized at sometimes sometimes always = sometimes 

both poles? | 
Other specialized cells? ѕотейтеѕ/ sometimes some- sometimes sometimes | 

times 
Position variable variable variable lateral lateral 
Number of variable fea- 7-10 10 5 5 6(-7) | 
Stomatal types* — А (соттоп); Р, H, weakly C P, H, and A P, Le, and | 
C weakly C 


(rare) 


а Key: P = paracytic; Lc = 


rangement and specialization than in Zone I 
forms, but less than in Menispermites and the 
new serrate (Table 6). Specialized LCCs occur 
next to every guard cell on a leaf and they almost 
always extend the full length of the stoma (Figs. 
45, 46). PCCS and other associated cells, in con- 
trast, show the same variation as in Zone I. This 
pattern has six to seven variable features and 
produces stomata that conform to three major 
types: paracytic (Fig. 46, P), laterocytic (Figs. 45, 
46, Lc), and weakly cyclocytic (Fig. 45, C). 
This same group of leaves also possesses four 


and pinnately compound species of Sapindopsis 
(Table 7). In this pattern there are some secretory 
cells that strongly resemble their counterparts in 
I (e.g., Figs. 47, 48), but these intergrade 

with other types of secretory cells and even rare 
hair bases on the same leaf. Secretory cells (or 
SCs) range from level with the epidermis, as in 
Zone I, to raised, and i in the latter case each SC 
ositioned over the 

junction of ` two or more sübiénding cells (Fig. 
50). These subtending cells are unspecialized ad- 


laterocytic; C = cyclocytic; H = hemiparacytic; A = anomocytic. 


jacent to some SCs (Fig. 51) but modified adja- 
cent to others (Fig. 50). SC shape in surface view 
is often angular or circular, as in Zone І = | 
‚ 48) but many times it is broadly to narrowly | 
elliptical (Fig. 52) to lobate (Fig. 53) and in som? 
cases one or more heavily oa lateral e 
trusions also 54). The outer 
ofthe SC is commoniy level iih the 
but sometimes it is strongly protru | 
this latter condition is found only on 
epidermis. Finally, many secretory cells poe | 
radiating striations and/or a ring of ore | 
cuticle (e.g., Figs. 51, 56), but this is some ў | 
missing (e.g., Figs. 47, 55). Hair bet е | 


pe surface, 


ding (Fig. 55} 
the lowe! | 


oy | 
resemble certain types of protrudi cdi | 
cells that lack striations, but differ rom 49. | 


having an apical hair saure scar 
The three other plans of secre 
construction, found in the 
represent portions of the spectrum О 
present in Sapindopsis. The largest "i 
variation is present in Platanoid #1 (Ta sar | 
whose secretory cells differ from those in 
indopsis in only three respects. First, the aie | 
always raised, rather than level with e ni st | 
mis in some cases (Fig. 57). Second, the 


tory ce cell/hair 
**platanoi E codi | 
of varia 


amount i | 


1984] UPCHURCH—CUTICLE EVOLUTION 539 


FIGURES 44-50. Sapi | 1 1 lectron micrograph showing slightly sunken 
. Sapindopsis, lower cuticle.—44. Scanning elec 

UM and round, slightly Madero secretory cell. UMMP 651 13-G72, х 1,000. —45. Stomatal complexes. 

MMP 65120, x 500.—46. Stomatal complexes. UMMP 65116, x 500.—47. Epidermal secretory cell of the 


bles protruding secretory cells. The flat top is 


ne L UM ‘ ae i i m 
MP 65118, x600.—49. Hair base which rese 0 Radiostriate epidermal secretory cell that is 


540 ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL 71 


Е bten 
FIGURES 51-56. Secretory cells, Sapindopsis.—51. Round radiostriate secretory cell cope a 
by several cells. UMMP 65121, x600.—52. Attachment scar of an elongate secretory cell. 


always circular to elliptical, rather than angular 
in some cases. Finally, the subtending cells are 
never modified in non-veinal regions (Fig. 58), 
but often are smaller than the adjacent cells in 
veinal regions (Fig. 59). 

The other two plans of secretory cell/hair base 
construction represent different subsets of the 
variation present in Platanoid 41 (Table 7). In 
Platanoid #2, there are only secretory cells. These 
are raised above the epidermis and are always 


e < 


дей 
65112, 


Е 
symmetrically positioned over the june in 
at least two cells (Figs. 61, 62). Also m (Fit 
this species are mesophyll secretory се a. 
60). In Platanoid #3, there are only orate 
These are similar to the hair bases of Plata! 


has a ring of thickened cuticle (Figs. i : 
addition, the base cells show a patte 


c—nmonnnens— — A лаьли Ó— MÀ ————— —— 12!22210 


1984] 


UPCHURCH —CUTICLE EVOLUTION 


541 


TABLE 7. Secretory cells and homologous epidermal structures of Zone I and Subzone II-B angiosperms. 


Zone I Platanoid Platanoid — Platanoid 
Taxon Angiosperms Sapindopsis #1 #2 #3 
Type of epidermal structure Secretory cells SCs and rare SCs and SCs only Hair bases 
(SCs) only hair bases rare hair only 
bases 
Position relative to epidermis level level-raised raised raised raised 
Specialization of adjacent/un- — variable variable — variable 
derlying cells, veinal re- 
gions 
Specialization of adjacent/un- none variable none none none 
derlying cells, non-veinal 
regions 
Shape of SC or foot cell, sur- polygonal or polygonal to circular to circular circular 
face view rounded circular and elliptical 
elliptical 
Lateral protrusions from SC none sometimes sometimes none none 
or foot cell? 
SC or foot cell shape, outer flat flat to protrud- protruding protruding protruding 
wall ing 
Cuticular sculpture smooth or smooth to smooth to smooth smooth 
riate striate striate 
Ring of thickened cuticle? sometimes sometimes never sometimes 


present in one 
species 


а oe MS E 


variation that is identical to that for the cells that 
subtend the secretory cells in Platanoid #1: they 
are scarcely modified in non-veinal regions (Fig 
63), but are often smaller than the adjacent cells 
underneath major veins (Fig. 64). This suite of 
characters is identical to that found in the hair 
ases of all extant Platanaceae (Figs. 65, 66). 


DISCUSSION 


The stratigraphic distribution of cuticle types 
Supplements previous evidence from palynology 
and leaf architecture on the direction and timing 
ofearly flowering plant evolution. First, cuticular 
NE strongly supports the concept of a Cre- 
‘aceous (rather than pre-Cretaceous) angiosperm 
adaptive radiation. Zone I flowering plants show 
a limited range of structural diversity compared 
to later Potomac Group forms, and these in turn 
are less diverse than Tertiary and modern an- 
Blosperms. The guard cells of all Zone I species 

T Outer stomatal ledges, which are often as- 
Sociated with maceration-resistant lamellae; in 
espe: Subzone II-B forms bear either outer 

отапа! ledges or lamellar thickenings, but nev- 
both. The stomata of Zone I angiosperms all 
conform to a similar pattern of variation in sub- 


sidiary cell specialization, which is characterized 
by a large number of stomatal types. In contrast, 
the stomata of Subzone II-B angiosperms con- 
form to both the Zone I pattern and three new 
ones, each of which possesses one or more of the 
stomatal types found in the earlier leaves. Fi- 
nally, the epidermal secretory cells of Zone I 
leaves conform to two basic types, while those 
of Subzone II-B leaves (along with their homol- 
ogous hair bases) conform to many different types 
that fall into four major patterns of organization. 
This increase in structural diversity through time 
is similar to that seen for leaf architecture and 
pollen morphology: Subzone II-B angiosperms 
are structurally diverse compared to Zone I forms 
but have features that can be derived from the 
earlier types. 

The similarities seen between Potomac Group 
angiosperm leaf cuticles and those of modern 
groups also provide evidence for classical theo- 
ries of flowering plant evolution, which postulate 
subclass Magnoliidae (but not necessarily the or- 
der Magnoliales!) as the most primitive living 
group. A survey of many primitive and inter- 
mediate level angiosperm families (Tables 2—4, 
8) suggests that Zone I forms, when comparable 
to extant families and orders, most closely re- 


542 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Уо1. 71 | 


Ficu piri iion M parce lower cuticle.— 57. Platanoid #1, epidermal secretory cells Apis and diverse pers 
papillate cells. UMMP 5106, x400.—58. Platanoid #1, strongly protruding secretory cell is nume 

' 65 106, x 400. — -59. аав #1 же ызы} cells beneath a primary у vein: mr ) 

Also note the h ory po (arrow 

Platanoió 


pi 
A Nune coi secretory pt UMMP 64105, x400.—61. Platanoid #2, laterocytic stom: a and nu umerous i at- 
electron ha е е secretory cells (light areas). UMMP 64105, x600.—62. Platan oid #2, “pr 
4.000. psed secretory cell and the attachment scars for two others (arrows). UMMP 


1984] UPCHURCH—CUTICLE EVOLUTION 543 


FIGURES 63-68. Platanoid #3 and extant Platanaceae.—63. Platanoid #3, hair нр ти epee 
“towing symmetrical positioning of the hair over the base cells. Note the flat top of the foot cell and the ring 
of thickened at its base. UMMP 65103, x600.— 64. Platanoid #3, hair bases beneath a primary vein (arrows). 

8 у | dos МЕ 4 1 h th thare UMM 
r 


- ba e latanus chiapensis, hair bases 
the siller size of the base cells. Michigan, D. E. Breedlove #9796, x 160. 66. Plata тесе 
: : i lectron micrograph of later- 

cells. Michigan, D. E. Breedlove #9796,  160.—67. Platanoid #3, scanning е 
Ytic and ви болшы ы tana 65103, х1,000.—68. Platanus sp., laterocytic stomata. Note the 
thinly Cutinized tangential walls of the subsidiary cells (arrows), x 400. 


544 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


TABLE 8. Stomatal patterns of Sapindopsis and selected Rosidae. 


Rhamnaceae 
Sapindaceae Cunoniaceae Rosaceae 
Taxon Sapindopsis Allophylus Weinmannia Members Quillaja 
Number of contact cells 4-8 4–6(–7) 4–5 4–6 5-6(-7) 
Number of lateral contact 2-5 2-4(-5) 2-4 2-3, 2-4 3-5 
cells (LCCs) 
Specialized LCCs in always always always always always 
every stoma? 
Specialized LCCs for always always always always always 
each GC? 
LOG NEE length almost always almost always almost always always always 
of st 
св 2. i polar contact 2-3 2-3 2-3 2-3 2-3 
cells 
PCCs specialized in each sometimes sometimes sometimes sometimes sometimes 
stoma? 
PCCs specialized at both sometimes sometimes sometimes sometimes never 
poles? ; 
Other specialized cells? sometimes sometimes sometimes never sometimes 
Position lateral lateral late - lateral 
Number of variable fea- — 6(-7) 6(-7) 5 5 
tures З 
Stomatal types* P, Lc, and P, Lc, and P, Lc, and P,Lc and 1сапй es 
weakly C weakly C weakly C weakly C tional to 


a Key: P = paracytic; Lc = 


laterocytic; C = cyclocytic. 


semble Laurales (including Chloranthaceae) and 
Illiciales, but cannot be assigned to a single fam- 
ily. Two leaf groups and one dispersed cuticle 
type deserve special mention. The first, Drewrys 
Bluff Leaf Type #1 (Figs. 1, 4, 25), is similar to 
Chloranthaceae. The combination of stomata 
longer than 30 um, striations that run concentric 
to the stomatal pore, and radiostriate epidermal 
secretory cells is found only in some Laurales 
and Illiciales. The “hair bases" of DBLT #1 to- 
day occur in many angiosperm families, but in 
Magnoliidae have been observed only in Illici- 
aceae and Chloranthaceae. Finally, the Zone I 


only from Amborellaceae and 
certain Chloranthaceae, while other Chlorantha- 
ceae and Schisandraceae differ in only two to 
three features (Tables 1, 4). These similarities, 
along with the Chloranthoid teeth, strongly sug- 
gest affinities with the family Chloranthaceae; 
however, simple craspedodromous secondary 
venation is absent from the family (Hickey & 
Wolfe, 1975; Upchurch, unpubl. data). Hence, 
DBLT #1 may belong to a group that includes 
the ancestor of modern Chloranthaceae but rep- 
resents an extinct taxon within the alliance. 


The second leaf group, Eucalyptophyllum o 

Mb gus “бы 3, 7, 9, 10, 19), most ¢ a 
ranthaceae and Illiciales but 

a кезе ee A ve duis unknown from either group. 


s- 
This taxon has always been difficult to od y 
4 f ven 


1 rms 
al features is unknown in extant uo E 
(Wolfe et al., 1975; Hickey & Doyle, ! x d 
ticular anatomy, however, clearly 1n indica 


lum possesses the same stomatal features, 
base" type, and epidermal secretory cell os 
other Zone I and certain extant flowering P a 
In fact, this combination of features today is 
stricted to Chloranthaceae, and Illiciales lest 
only in their less variable stomatal Me 

In spite of these similarities, however, e 
differs from both modern taxa in its ре" 
sunken stomata, truncate stomatal poles € 
of striations, and distinctive leaf archit 
Hence, Eucalyptophyllum probably 7 
an extinct group of at least ordinal rank ( 
ey & Doyle, 1977) that is related in 


t 
11, 12, 21), most strongly resembles exta? 


— — 


— 


— — M — PÁ—À 


———— 


a 


UPCHURCH—CUTICLE EVOLUTION 


545 


FiGURES 69-71. Lower cuticles, extant Rosidae.—69. Weinmannia crenata (Cunoniaceae), stomata showing 


Sapindopsis pattern of variation in subsidiary cell arrangement. 


Michigan, B. A. Krukoff #11053, x600.—70 


Allophylus apetata (Sapindaceae), stomata showing Sapindopsis pattern of variation in subsidiary cell arrange- 
ment. Indiana University Cuticle Slide #308, Yale, Wright #1604, х 600.—71. Flindersia schottiana (Rutaceae), 
abaxial secretory cells. Compare these with the one in Figure 55. National Cleared Leaf Collection #5958, x 600. 


ales. The striation pattern around the stomatal 


: ; 4). In addition, the one known hair 
base is similar to the type found in Schisandra 
europaea, ап Eocene member of the order. De- 
bu these similarities, however, the fossil has 
к ler stomata than modern Illiciales (27 џт 
the | versus 30-70 um) and appears to lack both 
d amellar guard cel] thickenings and epidermal 
cells Characteristic of the order. Hence, Dis- 
acis Cuticle #3 may be related to Illiciales but 
esents an extinct taxon within the alliance. 
inte cm m esults indicate the need for caution in 
TPreting similarities between the pollen of 
sud an modern angiosperms. While mono- 
cf. А Р роПеп grains assigned to Clavatipollenites 
й ughesii as described by Doyle et al. (1975) 


closely resemble Ascarina of the Chloranthaceae 
(Walker, 1976; Walker & Walker, 1984; Muller, 
1981), no angiosperm leaf with preserved cuticle 
or di d cuticle type p Il ofthe char- 
acters needed to be assigned confidently to extant 
Chloranthaceae. Since the Ascarina-type pol- 
len is inferred to be ancestral to the other pollen 
types within the family (Walker, 1976), similar 
pollen could also have been characteristic of the 
larger Early Cretaceous ancestral complex from 
which the Chloranthaceae are derived, which may 
have been much more primitive than the modern 
family in non-palynological characters. 

In contrast to Zone I forms, Subzone II-B an- 


33 and extant Platanaceae (Hamamelididae). 
Platanoid #3, like many other Potomac Group 
platanoids, shares several important venational 
characters with extant Platanaceae, which in- 
clude probable palinactinodromous primary ve- 
nation, closely spaced, percurrent tertiary veins, 
and orthogonal higher order venation (Figs. 30, 


546 


32, 33). Cuticle structure shows an equally strong 
h groups, contact cell ar- 
rm to the 


have thicker cuticular flanges along their tangen- 
tial walls (cf. Figs. 67, 68). Hair base structure is 
even more similar. In both groups the basal cell 
of each hair has the shape of a flat-topped cone 
and is the only cell present in the mature leaf. 
This cell often possesses a ring of thickened cu- 
ticle where it joins the underlying cells, which in 
veinal areas tend to be smaller than the adjacent 
cells (Figs. 63-66). These features of both leaf 
architecture and cuticle structure readily distin- 
guish Platanaceae from other groups and thus 
strongly suggest a relationship between this fam- 
ily and Platanoid #3. e resemblances, in 
conjunction with the similarities shown between 
Platanoid #3 and the other platanoids (cf. above), 
support the concept that the Potomac Group 
platanoids represent the Early Cretaceous com- 
plex that gave rise to modern Platanaceae (cf. 
Hickey & Doyle, 1977). 

Cuticular anatomy is also consistent with the 
proposed relationships of Sapindopsis and sub- 
class Rosidae (Hickey & Wolfe, 1975; Hickey & 
Doyle, 1977), but it is not known whether the 
similarities shared by the two groups are restrict- 
ed to the subclass. Pinnately compound orga- 
nization of the Sapindopsis-type is almost en- 
tirely restricted to Rosidae and inferred 
derivatives (Hickey & Wolfe, 1975) and adme- 
dially oriented tertiary venation of the type pres- 
ent in many Sapindopsis leaflets is common 
within the subclass (Upchurch, unpubl. data). In 
addition, some West Brothers specimens possess 
teeth with numerous Rosid features, which in- 
clude a concave-convex (C-1) shape, symmet- 
rically placed medial vein, and a pair of con- 
verging lateral veins, as in the Rosoid tooth type 
of Hickey and Wolfe (1975) (Fig. 29). The sto- 
matal structure of Sapindopsis has many coun- 
terparts in extant Rosidae and some of its secre- 
tory cells resemble those of a few Rosids. In 
Sapindopsis each guard cell is flanked by at least 
one specialized lateral contact cell (LCC) and 
these cells generally extend the full length of the 
stoma. Polar contact cells (PCC) and other as- 
sociated cells are variable in their number and 
patterns of modification. All modified cells are 
weakly differentiated from the surrounding cells 
but characteristically have a thinner cuticle, at 
least adjacent to the guard cells. Many Rosidae 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


have similar stomatal patterns, except that the 
region of thin cuticle, when present, is almost 
always restricted to a distinct zone next to the 
guard cells. Some Cunoniaceae (Fig. 69) and Sap- 
indaceae (Fig. 70) conform to the basic Sapin- 
dopsis stomatal pattern, while Rhamnaceae and 
primitive Rosaceae such as Quillaja differ only 
in lacking specialized non-contact cells (Table 8). 
Other Rosidae with comparable stomatal pat- 
terns include Nyssaceae, Alangiaceae, and сег- 
tain members of Rutaceae, Cornaceae, Celastra- 
ceae, and Anacardiaceae (cf. den Hartog & Baas, 
1978; Upchurch, unpubl. data). Implications of 
secretory cell structure are problematic, since 0 
i has been observed with the 


Flindersia (Rutaceae, Fig. 71) are similar in shape 
and position to some protruding Sapindopsis se 
cretory cells (cf. Dilcher & Mehrota, 1969; van 
Staveren & Baas, 1973). Other Rosidae, such 8 
Sapindaceae, Anacardiaceae, and certain Juglan- 
daceae, bear multicellular, generally abaxial 
glands that are either uniseriate or have а unl 
seriate stalk, suggesting that they may be derived 
from the protruding type of secretory st 
found in Sapindopsis. Additional studies ofl 
cuticles from extant angiosperms, along with 4 
detailed phylogenetic analysis of possible e 
indopsis relatives from the Late Cretaceous (s 
as Anacardites and “Rhus” powelliana), ~ 
needed to test further the idea of a Sapindopsi* 
Rosidae relationship. 

The morphological relationships 
Group cuticle types, in conjunctio 


of Potomac 
n with their 
reviously 


: ;eraphic 
' ing plants. First, stratigraP 
mis of carly flowering рай i ME 


I pattern of secretory cell (SC) construction. E^ 
its two distinct types of SCs, gave rise ke 
highly variable Sapindopsis pattern je 
increase in developmental plasticity; СОЛУ 

the related platanoid patterns appear tO of this 
rived through the canalization of one part uil 
variation (Fig. 72). The epidermal X— 
structures of Zone I angiosperms are all ak 
lular and level with the leaf патке. ae d 
form to two distinct types: one ni е Oe is 
ions. The $07 


indopsis pattern produces variants 


3 e with 
tical to Zone I forms, but these inte 


Өч 


‚ӨӨ ера 


ro m 


1984] 


E 74. Evolution of epidermal secretory cells 
omologous hair bases in Potomac Group angio- 
Sperm 1 n 


aa a divergent types of secretory cells, and 
be. ses of uniseriate hairs. Some secretory 
~ lng are level with the epidermis and have 
д _ е, but most rest at least partially 
мк а of other epidermal cells and have pro- 
abl 8 outer walls; in addition, they have a vari- 
mie of Positioning relative to the sub- 
of SC g cells. Hair bases resemble this latter type 
>~ except that each foot cell bears an apical 

T abscission scar. The pattern of variation for 
== cells and hair bases in Platanoid #1 is 
1 9 that for Sapindopsis except that the 
“= — of secretory cells appear to be ab- 
ме е secretory cells of Platanoid #2 and the 
bases of Platanoid #3 are interpreted as in- 
aa fixations of different portions of the 
M in Platanoid #1 because they resemble 
Pss ^e of structures found in the latter 
aue indeed these proposed homologies 
8 secretory cell and hair base types are cor- 


UPCHURCH—CUTICLE EVOLUTION 


547 


FIGURE 73. Evolution of patterns of variation in 
ent, Potomac Group angio- 


tern. Legend: A = Zone I pattern. B = Menisp 
potomacensis pattern. C — Sapindopsis/Platanoid pat- 
tern. D = New Serrate, Red Point pattern. 


rect, then the deciduous hairs of extant Plata- 
naceae are an evolutionary modification of the 
radiostriate epi il cells p in diverse 
Magnoliidae. In addition, this proposed series 
would indicate that the transition between these 


Hnermal 


ships of the different patterns of variation in sto- 
431 + 1 уде!" an 12243 di 4 


ma gg y trend 
towards decreased stomatal variation in early an- 
giosperms, with the later patterns representing 
independent fixations of a portion of the varia- 
tion found in Zone I (Fig. 73). The Zone I pattern 


an average of nine out of ten variable features, 
ranging from seven in cf. Ficophyllum to ten in 
Eucalyptophyllum. Stomatal types on a single 
leaf include paracytic, hemiparacytic, laterocy- 
tic, weakly cyclocytic, and (in most groups) an- 
omocytic. Subzone II-B patterns of stomatal 
variation, in contrast, show an average of only 
six non-uniform features, with three new, less 
variable patterns present in addition to the older 
one. The number of non-uniform features ranges 
from five in the new serrate from Red Point to 


548 


ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 
TABLE 9. Stomatal features of Late Cretaceous angiosperms. 
Araliephyllum Debeya Araliopsis Dewalquea Dryophyllum 
Taxon polevoi tikhonevichii wellingtoniana westerhausiana cretaceum 
Number of contact 4–5(–6) 4—6(—7) 5-7 5-8 5-8 
cells 
Number of lateral 2(-3) 2-4 2-4 3-4 3-5 
conta 
(LCCs) 
Specialized LCCs in always always always always always 
every stoma? 
Specialized LCCs sometimes always always always always 
for each GC? 
LCCs specialized always always mostly always always 
full length of sto- 
ma? 
Number of polar 2-3(-4) 23 2-4 3 2-4 
contact cells 
PCCS specialized in never sometimes sometimes sometimes sometimes 
each stoma? 
PCCs specialized at — sometimes sometimes sometimes sometimes 
both poles? 
Other specialized sometimes sometimes sometimes sometimes sometimes 
cells? 
Position lateral lateral variable variable variable 
Number of variable 5 6 1 6 7 
features 
Stomatal types? P,H Lc, weakly C Lc, C Lo C . ЖШН 


* Key: P = paracytic; Lc = laterocytic; C = cyclocytic; H — hemiparacytic. 

variation than their Subzone II-B counterparts 
The stomata of these angiosperms have an av- 
erage of 5.5 non-uniform features, ranging 
three in Debeya insignis to seven in Агар 
wellingtoniana апа Dryophyllum cretaceum (Ta 
bles 9, 10). Usually a leaf possesses no mo 


ten in Populophyllum, and the stomatal types 
present in each new pattern represent a subset of 
those found in Zone I. Judging from the illus- 
trations of Krassilov (1973), Némejc and Kvacek 
(1975), and Rüffle and Knappe (1977), Late Cre- 
taceous angiosperms show even less stomatal 


TABLE 10. Stomatal features of Late Cretaceous angiosperms. 


Grevilleophyllum Con 


Proteophyllu 1 
Taxon ит ap 

Number of contact cells 4—6 4–6 4–6 
Number of lateral contact cells (LCCs) 2 2 2-4 
Specialized LCCs in every stoma? always always always always 
Specialized LCCs for each GC? ways always sometimes always 
LCCs specialized full length ы stoma? always always always эн 
Number of polar contact ce 2-4 2-4 + 25 
РСС specialized іп each inei sometimes never never alway? 
PCCs specialized at both poles? never = — 
Other specialized cells? sometimes sometimes sometimes E 
Position lateral lateral form 
Number of variable features 3 
Stomatal t P P P, Le 6 


* Key: Р = paracytic; Lc = 


laterocytic; С = cyclocytic. 


1984] 


two distinct stomatal types, but these belong to 
the categories found in the Potomac Group. This 
progressive decrease in stomatal variation, 
analogous to the contemporaneous trend to- 
wards greater а vein regularity, suggests that the 

fmany 


extant angiosperms were derived from less uni- 
form patterns through the canalization of the 
variation in subsidiary cell arrangement. If in- 
deed this trend turns out to be valid for the an- 
giosperms as a whole, then the uniformly para- 
cytic condition of many is вук үени 
primitive for the angios tajan 
(1969, 1980), Baranova vier be ie 
(1976), would be derived. Thus, groups such as 
ee Austrobaileyaceae, Schisandra- 
ceae, and certain Chloranthaceae would be more 
primitive in their stomatal structure than Mag- 
noliales. In addition, this would suggest that 
agnoliales with relatively low stomatal regu- 
larity, such as Canellaceae and the New World 
and Madagascar groups of Winteraceae, are more 
primitive in stomatal anatomy than uniformly 
paracytic groups such as Annonaceae and My- 
risticaceae. Tests of this hypothesis will come 
from the study of other Early Cretaceous angio- 
Sperm leaf floras from low and middle paleolati- 
tudes along with the detailed cladistic analysis 
of modern and select fossil flowering plants. 


LITERATURE CITED 


AXELROD, D. 1. 1952. A theory of angiosperm evo- 
lution. Evolution 5: 29-60. 
1970. Mesozoic paleogeography and early 
pem history. Bot. Rev. (Lancaster) 36: 277- 
Вац кү, I. W, The comparative morphology of 
the лама П. J. Arnold Arbor. 25: 104-121. 
~~ & С. Nast. 1948. Morphology and relation- 
" of Illicium, Schisandra, and Kadsura, 1. Stem 
... ànd Leaf. J. Arnold Arbor. 29: 77-89. 

& B. G. L. Swamy. 1949. The morphology 
and relationships of Austrobaileya. J. Arnold Ar- 
bor. 30: 211-226. 

BARANOVA, M. A. 197 
leaf epidermis in the Magnoliaceae and some re- 
69. 


. Systematic paleontology, Lower 
Clar nous fossil plants. Pp. 214-508 in W. B. 
logi ry аай tae Saisies Maryland 

BoNGERs, J. M urvey, Baltim 


: 1. 
The Evolution апа Classifica- 
м of “Flowering Plants. Houghton Mifflin Co., 


UPCHURCH —CUTICLE EVOLUTION 


549 


. 1981. An Integrated System of Classification 
of Flowering Plants. Columbia Univ. Press, New 
York. 


Юпснев, D. L. 1974. Approaches to the identifica- 
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MrHROTA. 1969. А study of leaf 
compressions of Knightiophyllum from Eocene 
deposits of southeastern North America. Amer. J. 
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Doy te, J. A. 1969. Cretaceous angiosperm pollen of 
the Atlantic Coastal Plain and its иав sig- 
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& L. J. HICKEY. 1976. iig and leaves from 


be: 
206 in C. B Beck (editor), Origin and Early Evo- 
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67 М. VAN CAMPO & B. LUGARDON. 1975. Ob- 


wer Cretaceous angiosperm pollen. Pollen & 
Spores 17: 429-486. 

FONTAINE, W. 1889. The Potomac or Younger Me- 
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Harris, T. H. 1932. The fossil flora of Scoresby 

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. 1964. The Yorkshire Jurassic Flora, II. Cay- 


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HARTOG, R. M. N & P. Baas. 1978. idermal 
|| а Bot 

Мееп!. 27: 355-3 
Hickey, L. J. 1971. “Abstract DA signif- 
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1977. Stratigraphy and. paleobotany of the 
Golden Valley Formation (Early "eres d west- 
ern North Dakota. Mem. Geol. Soc. Am 
78. Origin of th e major features a angio- 
sperms leaf architecture in the fossil record. Cour. 
Forsch.-Inst. Senkenberg 30: 27-34. 
J. A. ЮоүіЕ. 1977. 


Early Cretaceous fossil 
evidence for angiosperm evolution. Bot. Rev 
4. 


тес. Н. 19 п des Geiseltales. 
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Koster, J. & P. Baas. 1981. Comparative leaf anat- 
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кнн, У. 1973. Cuticular structure of Creta- 


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1950. Kritische Un- 

utik analyse teriárer Blat- 
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7-92. 


H. WEYLAND. 


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550 


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ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


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“= 


SEED SIZE, DISPERSAL SYNDROMES, AND THE RISE ОР 
THE ANGIOSPERMS: EVIDENCE AND HYPOTHESIS! 


BRUCE Н. TIFFNEY? 


The seeds and fruits of angiosperms serve the 
functions of nurturing, protecting, and dispersing 
the embryonic plant, and thus form an evolu- 
tionarily sensitive portion of the life cycle of the 
whole organism. Two of these functions also en- 
hance the probability of fossilization of these dis- 
seminules. Protection is often achieved through 
lignification of the fruit or seed wall, predisposing 
the organ to preservation. Dispersal increases the 
probabilit y ofa propagul iving at a fossilizing 
environment. It is, therefore, not surprising that 
fruits and seeds are a major source of informa- 
tion on the fossil record of the angiosperms, par- 
ticularly from the Tertiary (Tiffney, 1977a). 

This information has generally appeared in de- 
scriptive reports of fossil floras and their com- 
position [e.g., the Eocene London Clay Flora 
(Reid & Chandler, 1933) and the middle Tertiary 
floras of central Europe (Mai, 1964)]. These flo- 
nstic studies have formed the basis for synthetic 
undertakings such as the elucidation of biogeo- 
graphic patterns (Wood, 1972; Wolfe, 1975; Tiff- 
ney, 1980; Mazer & Tiffney, 1982) and the in- 
ference of climatic history (Leopold, 1967; Mai, 
aan тв 1975; Gregor, 1980а; Collinson et 
an : 1). Consideration of evolutionary ques- 
= as been largely restricted to the demon- 
(e on of species sequences within single genera 

5 Stratiotes L., Chandler, 1923; Aldrovanda 


~ Dilcher, 1981, unpubl. data). However, 
í - and seeds additionally offer an excellent 
pe aan point for paleobiological inquiry based 
a — ecological studies. Of particular note 
a y considerations: (1) the relation of seed 
” 0 the habit and habitat of the parent plant, 
nd (2) dispersal syndromes. 

Harper et al. (1970) [after Salisbury (1942)] 


ا 


1 
I thank Leo J. Hickey (Yale University) for his devil 


have demonstrated a strong correlation between 
seed weight and the stature and successional sta- 
tus of the parent plant. Herbaceous plants, and 
those of early successional stages, tend to have 
small propagules, while dominant forest trees and 
plants of late successional status tend to have 
large propagules. Some shrubs and “weedy” trees 
tend to have propagules of intermediate sizes. 
The mode of dispersal of a living plant may often 
be inferred from the morphology of the fruit or 
seed, together with the mode of its presentation 
to the dispersal agent (Ridley, 1930; van der Pijl, 
1969). While fossilization precludes knowledge 
of the mode of presentation, many of the mor- 
phological characters of the fossils permit infer- 
ence of the mode of dispersal in at least a broad 
sense. These two features, propagule size and 
dispersal, have been examined only in modern 
plants and generally have been treated separate- 
ly. In the present paper I extend observations on 
propagule size and dispersal type through the 
fossil record and pror that these (1) have been 
related throughout the history of the angio- 
sperms and (2) underwent an intensive period of 
change in the latest Cretaceous and early Ter- 
tiary. My emphasis will be on propagule size; the 


SUD) $ 3 Б. мат 
rants a separate study and is not treated in detail 
here. 


METHODS 


In the following discussion, I will use the gen- 
eral term “‘diaspore”’ to indicate the reproductive 
unit that is dispersed or sown. Thus, in the case 
ofa capsule, which releases its contents, the term 
will apply to the morphological seed. In the case 
ofa drupe or berry, the term will encompass fruit 
tissue. However, in cases in which reference is 


's advocacy, which has clarified my thinking; Karl J. 
"ага км РЦ E P + ^ ғ, PONE РЕГ Robi 


bin 


Gowen T 77 


iffney for drafting the 


баешы figures, and Leo J. Hickey, Karl J. Niklas 
.VeTsity of Californi i · Handel (Yale University), Stev 
a ке ee th mer Aarhus = ity) for a critical reading of the manuscript. R 


i Niklas, Daniel Axelrod, and Maureen Stanton 
en Manchester and David L. Dilcher 
i esearc 


diana University), and Else M ( 
Partially supported by NSF grant DEB 79-05082. 


06511. 


ANN. MISSOURI Вот. GARD. 71: 551-576. 1984. 


body Museum and Department of Biology, Yale University, 


P.O. Box 6666, New Haven, Connecticut 


! mill. 


Lt 
100,000 | 
10,000 | 
„ооо Г 
Е 1 
F i00 р !! 
э I 
a 
э 
о 
= о | 
Ф 
Е 
3 
o 
> ор 
Cod Ворен 
EET саз |: е 
v 
1 1 


1 1 J 
OO! 01 10 IO 100 


Weight in Grams 


0.01 at | 
0.0000! 00001 0.001 


FIGURE 1. Log-log plot Е Зи versus volume for 

the propagules o angiosperms. The five 

categories of seed weight (after Harper et al., 1970) on 
eh 


use of the regression line. Cat- 
egories of Mobs I. open habitat; II. woodland m: 
III. mem bs dms IV. woodland shrubs; V. wood- 


we 


land tr 


to a specific morphological structure, and par- 
ticularly when discussing the nutrient reserves of 
a dispersed seed, I will use the appropriate mor- 
phological term. 

Salisbury (1942), Harper et al. (1970), and oth- 
er workers have quantified diaspore size using 
weight. This approach cannot be applied to a 
comparative study of fossil seeds because they 


a specific gravity of about 1.2, silicon dioxide has 
one of 2.65, and pyrite of 5.01. Linear measure- 
ments (e.g., length) are also inappropriate be- 
cause they do not account for variation in three- 
dimensional shape. I have, therefore, chosen to 
estimate size from volume. This also permits the 
culation of diaspore size from published re- 
ports as well as from actual specimens. The use 
of volume involves two HP елан As that 
weight апа seeds, 
and (2) that the volumes may be IE in 
an accurate and repeatable manner. To test these 
assumptions, the diaspores of 52 modern species 
were weighed to the nearest one thousandth of 
d measured to the nearest tenth of a 
millimeter. The results are plotted in Figure 1. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


A regression of weight versus volume yields r = 
0.928, indicating a significant correlation be- 
tween the two. This correlation further suggests 
that the measurement of volume was sufficiently 
accurate for the purposes of this study. 
Diaspore volumes of seven Cretaceous and 20 
representative Tertiary and Quaternary floras 
were then calculated from specimens and the lit- 
erature (Таш 2). In order to obtain accurate 
t of the individual 
diaspores, only floras with three-dimensional, 
well-preserved fossils were used. Volumes were 
obtained only for those fossils that represented 
diaspores as defined above. Calculations wert 
based on average width, length, and thickness 0 of 
the specimens as described. In cases where one 
or more dimensions were not cited, the missing 
value(s) was estimated from illustrations. In cases 
of extreme compaction, thickness was assumed 
to be a value equal to 0.66 x the width. This 
value was arrived at empirically, and is an out- 
growth of the % power law governing the relation 
of surface area to volume. The volume of spher- 


ical diaspores was estimated at 5лт3. On those — 


occasions where spines or other projections е 


| 


ic ages of the deposits are those provided ke | 
authors, with modification in light of recent | 


(Gregor, 1980b) as appropriate. The conversion 
of stratigraphic age to absolute age is m 
van еам (1975) and Gregor (19800). о 
ment of absolute age is necessary to permit 
culation of regression values and aids in 
ative location of the floras. However, * 
are approximate and should be reco; 
such. Regression values were calc 


numbers with regard to these fossils may 
a false sense of precision. the num 
used are certainly valid withi 
work of the present — - 
volve subjective judgements and 
agit as educated mui en 
absolute 


- о 
поша be 1" 


DATA 


CRETACEOUS FRUITS AND SEEDS 


te, 
dimensional fruits and seeds have, tO бу re this 


been found іп the Late Cretaceous. 


Whil 
in the relative кате | 
ften 1" 


convey | 


| 


| 


1984] 


time, the record of angiosperm reproductive 
structures involves isolated fossils. 

A summary of the better documented fruits 
and seeds of Early Cretaceous and Cenomanian 
age (115-95 million years ago, henceforth Ma) 
is presented in Table 1. The majority of these 
are preserved as casts or impressions; of the 
compressions, only a few can be or have been 
studied in anatomical detail. As a result, many 
of the earliest reported forms cannot be clearly 
assigned to the angiosperms and may well be 
gymnospermous. This has been suggested in the 
case of Onoana californica Chandl. & Axelr. 
(Chandler & Axelrod, 1961), and by inference 
Onoana nicanica Krass. (Krassilov, 1967), by 
Wolfe et al. (1975). The same arguments apply 
to several other Early Cretaceous endocarp-like 
forms including '*Carpolithus" (Chandler, 1958), 
Nyssidium Saml. (Samylina, 1961), Prototrapa 
Vas. (Vasil’yev, 1967), Araliaecarpum Saml. and 
Caricopsis Saml. (Samylina, 1960) and Knella 
Saml. (Samylina, 1968). Retallack and Dilcher 
(1981) have similarly viewed many of the above 
reports as potentially non-angiospermous. These 
reports will not be considered further. 

, +he remaining reports tabulated in Table 1 fall 
Into two categories. The first includes several 
Structures reported by Fontaine (1889) under the 
genus “Carpolithus” and interpreted by Dilcher 
(1979) and Retallack and Dilcher (1981) to rep- 
resent multifollicles. I have not personally ex- 
amined these specimens and accept the judge- 
ment of these authors. The second category 
includes well-preserved fruits, often containing 

‘ds. These involve clearly angiospermous ma- 
terial such as Caspiocarpus paniculiger Vach. & 
Krass. (Vachrameev & Krassilov, 1979), Ra- 
пипсшаесатрих quinquiecarpellatus Saml. (Sa- 
mylina, 1960), Carpites liriophylli Lesq. (Dilcher 
e. al., 1976) and a host of forms from the Dakota 

ormation of central North America. 

: The majority of these Early Cretaceous angio- 
ini fruits are small, individual carpels ranging 

9m 1 to 15 mm in length and from 0.5 to 8 
mm in width, or are capsules of from 10 to 12 
mm in diameter, In the five cases where seeds 
are known from these fruits, the seeds are small, 
ranging from 0.2 mm? (Caspiocarpus paniculi- 
8er) to approximately 7.5 mm? (estimated for the 

unpublished five-carpellate fruit” from the Da- 
re обје еј Dilcher, 1979). The one exception 
Е 1s tendency to small size is Carpolithus cur- 
atus Font., which is a carpel about 40 mm long 
and 15 mm wide. This specimen is not well pre- 


TIFFNEY —RISE OF ANGIOSPERMS 


553 


served, and there is no indication as to the size 
of the included seeds. 

The most common fruit morphology is a de- 
hiscent follicle, borne on a central axis, although 
capsules are also frequently observed. This is in 
keeping with the classic hypothesis that the con- 
duplicate carpel, and dispersal by morphological 
seeds, are the primitive conditions in the group 
(Cronquist, 1968; Takhtajan, 1969). The one po- 
tential exception to this pattern is the report of 
a fleshy fruit from the Cenomanian (98 Ma; 
Dilcher, 1979). However, the status of this fossil 
is not clear because Retallack and Dilcher (1981: 
49) imply that no fleshy fruits are known from 
Cenomanian and older sediments. The reported 
seeds are all apparently thin-walled and without 
any distinctive features related to dispersal. The 
capsular-follicular morphology of the fruits and 
the small, unspecialized, nature of the seeds are 
characters indicative of a general adaptation to 
abiotic dispersal mechanisms, a conclusion also 
reached by Retallack and Dilcher (1981). 

Individual fruits are also reported in the Late 
Cretaceous, often as constituents of compression 
orimp ion nd several reports exist 
of isolated occurrences of seeds or seed-like ob- 
jects (Miner, 1935; Schemel, 1950; Hall, 1963, 
1967; Binda, 1968; Colin, 1973; Knobloch, 1981). 
However, of greater importance to the present 
work are several fairly diverse (10—50 species) 
floras of thr 1i i lly preserved fruits and 
seeds from fluvial and lacustrine sediments. The 
most important of these are listed in rows 1—7 
of Table 2; several others of lower diversity have 
not been included but are of a similar nature 
(Knobloch, 1971, 1977). Although some of these 
seeds have been assigned to extant families (Car- 
yophyllaceae, Cyperaceae, Menispermaceae, 
Myricaceae, Theaceae, Urticaceae: Knobloch, 
1977; Jung et al., 1978) and orders (Juglandales: 
Friis, 1984), the majority have been placed in 
the organ genus Microcarpolithes Vangerow 


leaf floras 


п . The type speci 
gerow (Hall, 1 963) has been shown to be an insect 
coprolite (Knobloch, 1977).] 

The average size of the seeds in these floras is 
approximately 1.7 mm? (see Table 2, column 
хапа Fig. 2, floras 1-7). This small size does not 
appear to be a function of mechanical sorting, or 
of ecological separation, for a variety of reasons. 
The Santonian-Campanian floras (about 77 Ma) 
reported by Friis (1984) from Asen, Sweden, and 


TABLE 1. Summary of individually reported fruits and seeds of presumed angiospermous affinities from Early Cretaceous and Cenomanian localities. 
Judgement of angiospermous affinities in the “comment” column is by the present author unless otherwise noted. “Мо distinguishing angiospermous features 


only implies that the specimen is not clearly angiospermous 


ээ 


= Мате Locality Type Size Reference Comment 
Tithon “Tyrmocarpus” Tyrma R., Siberia “capsule-like ca.6 mm Krassilov (1973) No distinguishing angiosper- 
"wish (134) fruit” diam. Hughes (1976) mous features 
Valangian (127) Carpolithus Vaucluse, France unclear 22mm x 12 Chandler (1958) The original (now lost) was a 
mm ' sandstone cast with no dis- 
tinctively angiospermous fea- 
tures 
Barremian (117)? Nyssidium orien- ^ Siberia, U.S.S.R. unclear — in- 10 mm x 6 Samylina (1961) No distinguishing angiosper- 
tale Sam. ferred as endo- mm mous features. Illustrated 
carp specimens show little relation 
Barremian (117)^ Nyssidium Sp. Siberia, U.S.S.R. unclear— in- 10 mm x 5 Samylina (1961) to Nyssa. Found in a totally 
ferred as endo- mm gymnospermous flora. 
Barremian (117)^ Onoana californi- California, U.S.A. unclear—in- 20mm x 15 Chandler and Ax- Мо distinguishing angiosper- 
ca Chand. & ferred as endo- m elrod (1961) mous features (Wolfe et al., 
1975). 
Late Barremian- Carpolithus gemi- Virginia, U.S.A. multifollicle 6mm x 9 Fontaine (1889) Footnote f. 
Early Aptian natus Font тп“ 
(112)? 
Late Barremian- Carpolithus sessi- Virginia, U.S.A. multifollicle 12 mm x 4 Fontaine (1889) Footnote f. 
Early Aptian lis Font. 
(112)4 
Late Barremian- Carpolithus virgi- Virginia, U.S.A. multifollicle 7-10 mm x Fontaine (1889) Footnote f. 
Early Aptian niensis Font. 4—6.5 mm 
(112) 
Aptian (110) Onoana nicanica Primorye, U.S.S.R.  unclear—in- 8-10 mm x Krassilov (1967) No distinguishing angiosper- 
Krass ferred as endo- 5.5—7.5 mm ures (cf. Wolfe et al., 
carp 1975). Preservation poor.* 
Aptian-Albian Prototrapa doug- Victoria, Australia endocarp 1-3 mm x Vasilyev (1967) Resemblance to Trapa is super- 
107.5) asi Vass. 0.5-1.5 mm ficial; angiospermous affinities 
unclear. Impression. 


vss 


N3G3IVO TVOINV.LO€ THNOSSIW JHL ЧО STVNNV 


IL 104] 


TABLE 1. (Continued). 
Age“ Name Locality Type Size Reference Comment 
Aptian-Albian Prototrapa prae- Victoria, Australia endocarp 2mm x | Vasil’yev (1967) Resemblance to Trapa is super- 
(107.5) pomelii Vass. mm ficial; angiospermous affinities 
unclear. Impression. 
Aptian-Albian Prototrapa tenui- Victoria, Australia endocarp 1.2mm x 0.5 Vasilyev (1967) Resemblance to Trapa is super- 
(107.5) rostrata Vass. ficial; angiospermous affinities 
unclear. Impression. 
Albian (105) Araliaecarpum Siberia, U.S.S.R. unclear; possibly 6 mm x 6 Samylina (1960) Affinities unclear to present au- 
kolymensis ам mm thor. 
: docarp? 
Albian (105) Caricopsis com- Siberia, U.S.S.R. unclear 3-5 mm x 2 Samylina (1960) Affinities unclear to present au- 
pacta Sam. thor. 
Albian (105) Carpolithus con- Virginia, U.S.A. multifollicle 7.5 mm x 3.6 Fontaine (1889) Footnote f. 
jugatus Font. те 
Albian (105) Carpolithus cur- Virginia, U.S.A. multifollicle 42 mm x Fontaine (1889) Footnote f. 
Font. 14.2 тте 
Albian (105)* Carpolithus fasi- ^ Virginia, U.S.A. multifollicle 15 mm x 8 Fontaine (1889) Footnote f. 
culatus Font. пите 
Albian (105)* Carpolithus ter- Virginia, U.S.A. multifollicle 8-11 mm x Fontaine (1889) Footnote f. 
natus Font 4—7 mm* 
Albian (105) Carpolithus ka- Kazakhstan, multifollicle — Vachrameev Original article not seen; data 
ratscheensis U.S.S.R. (1952) from Retallack and Dilcher 
Vachr. (1981). 
Albian (105) Caspiocarpus Kazakhstan, dehiscent follicle Fruit—1 Vachrameev and Clear angiospermous affinities. 
paniculiger USSR. mm х 0.5 Krassilov (1979) 
Vachr. & mm 
Krass. Seed—0.8 x 
0.5 mm 
Albian (105)" Knella harrisiana Kolyma R., unclear — endo- 16 mm x 5 Samylina (1968) Poor preservation, angiosper- 
Sam USSR. carp? 


mous affinities not demon- 
strated. See also Hughes 
(1976). 


ЅИЧЯ45ОІОМУ 30 3574 — ASNAALL [7861 


SSG 


TABLE 1. (Continued). 
Age? Name Locality Type Size Reference Comment 
Albian (105)° Ranunculaecar- Kolyma R., Dehiscent folli- ^ Fruit— 10 Samylina (1960) Angiospermous affinities fairly 
pus quinquie- U.S.S.R. cle m x 5 certain. 
carpellatus mm x 2 
Sam. mm 
Seed—1.5 
mm х 0.6 
Cenomanian (97.5) Carpites liriophyl- Dakota Group, Dehiscent folli- Fruit— 15-20  Dilcher et al. Clear angiospermous affinities. 
li Lesq. U.S.A. mm x 3-4 (1976); Dilcher 
mm (1979) 
Seed — 1.4 mm 
x 0.6 mm 
Cenomanian (97.5) Carpites tiliaceus Dakota Group, Five-valved cap- ca. 10 mm Lesquereux Clear angiospermous affinities. 
Lesq. U.S.A. sule diam." (1892); Dilcher 
(1979) 
Cenomanian (97.5) Laurus macrocar- Dakota Group, Syncarpous fruit 12mm x 8.3 Lesquereux Clear angiospermous affinities. 
pa Lesq. U.S.A. n (1874); Dilcher 
(1979) 
Cenomanian (97.5) Platanus primae- Dakota Group, Spherical mass head ca. 3-4 Lesquereux Clear angiospermous affinities. 
va Lesq. U.S.A. of individual mm diam.^ (1892); Dilcher 
fruits (1979) 
Cenomanian (97.5) “Salix? Dakota Group, Dehiscent folli- 3.3 тт x 1.5  Lesquereux Clear angiospermous affinities. 
U.S.A. cle mm^ (1892); Dilcher 
(1979) 
Cenomanian (97.5) un-named Dakota Group, Fleshy fruit 5—6 mm Dilcher (1979) Dilcher (1979) interprets as an- 
U.S.A. diam." giospermous. 


966 


N3Q31IVD TVOINV.LOS INNOSSIN JHL AO STVNNV 


IL 70А] 


TABLE 1. (Continued). 
Аре“ Мате Locality Type Size Reference Comment 
Cenomanian (97.5) “unpublished Dakota Group, Five-valved cap- Fruit—10 mm  Dilcher (1979) Clear angiospermous affinities. 
5-carpellate U.S.A sule diam. 
fruit" Seeds— 3.3 
mm x 2.5 
mm x 1.2 
тт! 
Cenomanian (97.5) *un-named follic- Dakota Group, Dehiscent folli- — Fruit—2.7 Dilcher (1979) Clear angiospermous affinities. 
ular axis asso- U.S.A. mm x 2.0 
ciated wit mm 
Magnoliaephyl- Seed—0.8 
lum” mm x 0.5 
тт" 
Сепотапіап (97.5) “un-named glo- Dakota Group, Globose mass of Head ca. 10 Dilcher (1979) Fairly clear angiospermous affin- 
bose heads” U.S.A. individual mm x 7.5 ities. 
ruits mm Фіат." 
Cenomanian (94) Platanaceae Dakota Group, Spherical mass Not given Schwarzwalder Infructescences and leaves de- 
U.S.A. of individual and Dilcher monstrably related to Platana- 
ruits 1981) ceae. 


а Absolute ages after bes Eysinga (1975). 
> Age after Hughes 
* Retallack and AS doin consider the angiospermous affinities of this species to be unproven. 


4 Age after Doyle and Hickey 


* Measurements are арр! 
f The identification of 


rial. 
* Age after Vachrameev and Krassilov 


the sa 


ilov (1979). 
^ Measurements are approxima te; made from Dilcher's (1979) illustrations. 
e as 


i This unpublished specimen m s Carpites tiliaceus Lesq. (Dilc 


(1976). 
roximate; made from Fontaine" 5 d illustrations. 
by Retallack and Dilcher (1981), although Fontai 


(1990 el J i4 4 ж 
` “= 


her, 1979). Since the measurements given for both seed and Hess are made 


from Dilcher s illustrations, they must be viewed as approximate. The measurements for the seed are taken from the presumed seed-cavity cas 


SWUsadSOIONY 30 ASIA — AANSSIL [7861 


LSS 


TABLE 


standard deviation, CV = covariance 


Data on individual Late Cretaceous and Tertiary fruit and seed floras. N = total number of seeds measured in flora, Х = average value, s.d. 


Estimated se 
Numeric Largest Smallest 
Stratigraphic Age Age* Locality Reference М X(mm) s.d. (s. vu /3) (mm? (mm?) 
1. Santonian-Campanian 77 Asen, Sweden is (1984) >50 " ES a 27 0.025 
2. Santonian-Campanian 77 Gay Head, Massachu- Tiffney (unpubl. data) 41 57 10.5 1.82 35 0.03 
setts, U 
3. Santonian-lower Cam- 77 Staré Hamry 1, Knobloch (1977) 19 1.4 07 05 3 0.41 
panian Czechoslovakia 
4. Senonian 75* Aachen, West Germany — Vangerow (1954) 11 0.2 0.17 0.83 03 0:03 
5. Senonian 15 Petrovice, Czechoslo- Knobloch (1964) 11 0.3 025° 0.625 0.73: 0:41 
vakia 
6. Campanian-Early 73-63” Horní, Bečva, Czecho- Knobloch (1977) 29 55 40:91 64.2015 
Paleocene slovakia 
7. Late Senonian 69 Kössen, Austria Knobloch (1975) 9 13 0.9 0.69 3 0.15 
8. Senonian 69 Kóssen, Austria Jung et al. (1978) 13 15 L2. -0.82 3 0.15 
9. Maastrichtian-Middle 67-61%" Rusava, Czechoslovakia Knobloch (1977) 20 1.2 8 0.66 3 0.06 
10. Late Paleocene 55 Woolwich and Reading Chandler (1961) 18 129 234 1.82 731 1.2 
s, England 
11. е (Еагіу 52 London Clay, England Reid and Chandler (1933) 202 1,957 5,932 3.03 61,318 0.25 
12. бра (Middle 45 Geiseltal, East Germany Маі (1976) 25 308 643 21 3,182 zt 
Eocene) 
13. Auversian (Late 42 Clarno, Oregon, U.S.A. Scott (1954); Bones 33. 3,129 10,626 26 59.150 0.25 
Еосепе) (197 
14. Middle Oligocene 32 Haselbach, East Mai and Walther (1978) 79 268 1,220 4.5 9,294 0.07 
rman 
15. Middle Oligocene 30 Bovey Tracey, England Chandler (1957) 33 68 225 3.3 1,300 0.35 
16. Late Oligocene 25 Tomsk, Siberia U.S.S.R. Nikitin (1965) 95 19 123 6.4 1,200 0.07 
17. Lower to Middle 18.5 üzek and Holy (1964) 22 19 38.6 2 180 1:27 


Chomutov-Most-Teplice 
i hoslo- 


OEE РЦ T E 


ae m—»—»———————————— 


ип наь san 


855 


N3QG31VD TVOINV.LOd ГУПОЅЅІИ AHL ЧО STVNNV 


2 
: 


Tame 2. (Continued). 
Estimated Co. 
Numeric var. Largest Smallest 
Stratigraphic Age Age" Locality Reference N (тт?) s.d. (s.d./X) (mm?) (mm?) 
18. Lower Miocene 18 Rusinga, Kenya Chesters (1957) ae 159 2,044 16 10913. 63 
19. Middle 18 Wiesa, East Germany Mai (1964) 71 1,410 3,263 24 13,68 0.25 
(Lower Miocene) 
20. Middle to Upper 18 Hartau, East Germany Mai (1964) 51 774 2,303 3 11,600 1 
lali (Lower 
Miocene) 
21. Upper Ottnangian 17.5 Turów, Poland Czeczott and Skirgiello 41 2.501 4,340 L7 130% 2 
Мпосепе) (1959, 1961а, 19615, 
1967, 1975, 1980а, 
19805) 
22. Carpathian 17 Nowy Sacz Basin, ucka-Srodoniowa 79 7 224 3.3 179 0.014 
Miocene) Poland (1979) 
23. Badenian (Middle 14.5 "Gdów Bay," Poland Kancucka-Srodoniowa 52 95 366 3.9 2,125 0.04 
Miocene) (1966) 
24. Pliocene 23 Kranichfeld, East Mai (1965) 35 13 63 5 1,215 0.1 
Germany 
25. Pliocene 3.5 d West van der Burgh (1978) 83 100 2453 25 1,400 0.9 
26. Plio-Pleistocene 1.8 Riper East Mai et al. (1963) 66 68.1 301 4.4 2,125¢ 0.014 
27. Holocene 0.035 "анау Haven, Connecti- Pierce and Tiffney 43 1,077 4,116 3.8 25,000 11 
0.068 (unpubl. data) 
* Numerical ages after van Eysinga (1975), millions О (Ма). 
* Estimated from ible smallest 


and 
чоет атрад ки э my ne чон: эл бе э Pe  IF85À 
* Deposit cited as 


sizes of angiosperm fruiting remains presented in Friis (1984). The largest fruiting remain is a seed- 


"Senonian;" 75 Ma is taken as the midpoint of the Senonian. 
* Exact stratigraphic position of deposit not determined; possible range indicated. 
* This value is for a nut of Corylus. 
' Value for Juglans cinera; the next largest value is 8,000 mm" for Carya. 


SW3JdSOIONV ЧО 3SI3— ASNHAILL [r861 


6565 


560 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Мог 71 


100,000F 
, п 13 
: 27 
I9 2i 7 
10,000 |- 14 то 26 | Т 
ЕФ 23 Y 
16 " 
* { ЈЕ r li ТҮ. ме E 
1,000 - f Ж Tl le 
^1 2 
2 
M 1 17 4 E ut 
E 
gor у l $ 1 H 
Ф 
Е • 
Ф 2 
Е 
Е + 
5 
> 
ки N Е 
| | 
d: _ 
"1 | 1 1 „————— | 
80 70 60 50 40 30 10 0 


Millions of years before present 


FIGURE 2. Plot of seed volume (vertical axis, logarithmic) versus time (horizontal axis) for 27 Cretaceous 
and Tertiary fruit and seed floras. The vertical line for each flora indicates the range of diaspore volume; the 
central dot, the average diaspore volume. The lines I-V at the far right correspond to the volume equivalents 
of the ecological classes of Harper et al. (1970) as derived in Figure 1. (I. Open habitat; II. woodland margn 
III. woodland ground; IV. woodland shrubs; V. woodland trees.) Note that the average volume is not avail- 
able for flora *1, and that in several cases (floras 1-3, 7, 8, 17-22, 24, 25), more than one flora occurs à 3 
single time.— 1. Åsen, Sweden (Friis, 1984).—2. Gay Head, Massachusetts, U.S.A. (Tiffney, пор data). 


12. Geiseltal, East Germany (Mai, 1976).—13. Clarno, Oregon, U.S.A. (Scott, 1954; Bones, 1979).— 14. Har 
elbach, East Germany (Mai & Walther, 1978).—15. Bovey Tracey, England (Chandler, 1957).—16. То D 
Siberia, U.S.S.R. (Nikitin, 1965).— 17. Chomutov-Most-Teplice Basin, Czechoslovakia (вијек & Holý, 1968) – 
Pres те Kenya (Chesters, 1957). — 19. Wiesa, East Germany (Mai, 1964). —20. Hartau, East any 


4. Kranichfeld, East Germany (Mai, 1965).—25. Bergheim, West Germany (van der Burgh, 1978).—26. 
Pues West Germany (Mai et al., 1963).—27. New Haven, Connecticut, U.S.A. (Pierce & Tiffney, " 


by Tiffney (unpubl. data, see Tiffney, 1977b) from {тот a single, ecologically-specialized ма 
Massachusetts, U.S.A., аге both in fluvial de- community, or a combination of aquatic and is 
posits containing large pieces of wood and, inthe — er-floodplain communities. At the outset, FE 
case of Tiffney's material, conifer cones (Miller noteworthy that in one case (Petrovice, С a 
& Robison, 1975). The same situation exists in slovakia, flora #4) Knobloch (1964) described : 
lagoonal sediments of a similar age from Cliff- seed flora of 11 species of Microcarpolithes сой 
wood Beach, New Jersey, U.S.A. (Tiffmey, un- parable in all respects with other cen p. 


productive remains from these deposits cannot same sample as a flora of large leaves 

be explained by mechanical sorting. Araliophyllum sp. Ett., Debeya bohemica 
It is possible that a uniformly small seed size Pseudoprotophyllum senonense Knob.» yl 

could result from the derivation of the fossils phyllum triangulodentatum Knob., Lauroph 


1984] 


lum elegans Holl., Proteophyllum sp., Platano- 
phyllum sp., Cinnamomophyllum sp., and three 
species of Dicotylophyllum. This clearly suggests 
that at least some of these seeds were borne by 
woody, nonaquatic vegetation. The question re- 
mains, do these floras sample only unstable 
floodplain forests? The answer lies in an exam- 
ination of Tertiary and modern deposits, where 
we have a better idea of the community affinity 
of the fossils through their taxonomy. The fluvial 
deposits of the Tertiary (e.g., Bergheim, or those 
described by Gregor, 1978, 1980b) often include 
a wide range of fruit and seed sizes that are pre- 
sumed on taxonomic grounds to be derived from 
several separate communities, including upland 
mesic ones. This is further supported by the New 
Haven, Connecticut flora (#27), which is of Ho- 
locene age and includes many upland taxa. Even 
those Tertiary floras least affected by transport 
include occasional samples of plants growing in 
the mesic sites surrounding the water. For ex- 
ample, the Oligocene (30 Ma) lacustrine Bovey 
Tracey flora of England (Chandler, 1957) in- 
cludes larger seeds of such trees as Magnolia L., 
Fagus L., and Nyssa Gronov. ex L. In conclu- 
ston, it seems unlikely that these Cretaceous flo- 
ras are solely records of aquatic or floodplain 
vegetation. 

The morphology of these Late Cretaceous fruits 
and seeds is somewhat more diverse than that 
of the Early Cretaceous and Cenomanian re- 
mains. Follicles and capsules are still common 
(Massachusetts and New Jersey deposits), but 
some evidence is at hand for nuts and drupes 
iN 1984; Tiffney, unpubl. data). While many 
Bi * seeds in these deposits have thin or fragile 
e others have rather thick walls and well- 
ud ге surficial sculpture. The dehiscent fruits 
ч in-walled small seeds suggest the continu- 
H mportance of abiotic dispersal hanisms. 
Ыкы the Presence of drupes and seeds with 
ad walls is circu ial evidence for at least 
"И ME for adaptation to animal dispersal, 

9r its presence in a limited degree. 

Exceptions exist to the general rule of small 
м diaspores. Monteillet and Lappar- 
trikes 1) reported a Late Campanian to Maas- 
"e S (70-66 Ma) flora from Senegal, includ- 
" ven species of angiosperm fruits with an 

ставе volume of 51,950 mm}. The fossils are 
ees LL e and in the cases of “Annona” 
ed Pans Schott, and perhaps “Cordyla” Lour. 
аша richilia” P.Br., І am not convinced that 

Pecimens are of plants. The illustrated spec- 


TIFFNEY —RISE OF ANGIOSPERMS 


561 


imens of Borassus L., Meliacea (? new form ge- 
nus), and perhaps Nauclea L. are more convinc- 
ing. Chesters (1955) has also reported large fruits 
of Annonaceae, Icacinaceae, and possible other 
angiosperms from the Maastrichtian (68 Ma) of 
Nigeria. Although large fruit size is no guarantee 
of large seed size (Nauclea has tiny seeds, Willis, 
1973); it appears that larger diaspores were be- 
coming more common in the late Cretaceous. 


TERTIARY FRUITS AND SEEDS 


Individual large diaspores are known from the 
Paleocene (Brown, 1962; Koch, 1972a, 1972b), 
but the only published fruit and seed floras are 
those of the Woolwich and Reading beds of 
southern England and possibly Horní Весуа and 
Rusava, Czechoslovakia. The Rusava flora 
(Knobloch, 1977) is between latest Cretaceous 
(67 Ma) and middle Paleocene (60 Ma) in age, 
while Horní Becva is inferred from Table 1 of 
Knobloch (1977) as being between Campanian 
(73 Ma) and Early Paleocene (63 Ma) in age. Both 
floras are quite similar to those of Staré Hamry 
land Petrovice, to which they are geographically 
close. 
By contrast, the flora of the Late Paleocene (55 
Ma) Woolwich and Reading beds (Chandler, 
1961) includes a diverse array of large and small 
diaspores with an average volume of 129 mm’. 
This sets the pattern for the remaining Tertiary 
floras, which vary in percentage composition of 
larger and smaller diaspores, but which always 
include both. The basic trends can be discerned 
from columns “x,” “largest diaspore,” and 
“smallest diaspore" in Table 2, and from floras 
10—27 of Figure 2. Very large diaspores first ap- 
pear in numbers in the Early Eocene (52 Ma) 
London Clay flora and dominate the Middle 
Eocene (45-42 Ma) Geiseltal and Clarno floras 
and the mid-Oligocene (32 Ma) Haselbach flora, 
resulting in high average diaspore sizes for these 
floras. From the Late Oligocene, there is a general 
tendency for the average diaspore size of a flora 
to decrease through Pliocene/Pleistocene time, 
although this trend is not statistically significant. 
This decrease in average diaspore size is not due 
to a decrease in the size of the largest diaspores 
in each flora (by regression of largest seed size 
versus age (P = 0.1; r = 0.40, N = 18), but to the 
occurrence of fewer large diaspores in each flora. 

Herbaceous angiosperms began to diversify 
dramatically in the latest Paleogene and the early 
Neogene (Tiffney, 1981). Herbs normally have 


562 


small seeds (Harper et al., 1970), and their in- 
creasing importance during this time is reflected 
1 е reduced average diaspore volumes of the 
floras commencing with the Lagernogo Sad de- 
posit (Tomsk, Siberia; age from Dorofeev, 1963) 
and carrying through the later Tertiary floras from 
the Chumotov-Most-Teplice basin (Czechoslo- 
vakia), Nowy Sacz basin (Poland), and Kranich- 
feld (East Germany). While the average diaspore 
volume (ADV) of these floras is small relative to 
that of other Tertiary floras, it is markedly larger 
than the ADV of the Cretaceous floras. The large 
average volumes for the Miocene Gdów Bay (Po- 
land) and Pliocene Rippersroda (East Germany) 
floras are due to the presence of a few large di- 
aspores. Deletion of Corylus L., Fagus L., and 
Carya Nutt. from the former flora brings the 
average volume down їо 9.2 mm», and deletion 
of Trapa L. and Corylus L. from the Rippersroda 
flora brings the average volume down to 21.5 
mm^. The large average volume for the Pliocene 
Bergheim flora (Mine Fortuna-Garsdorf 1) of 
West Germany results from the river sands of 
this deposit having a large allochthonous com- 
ponent derived from upland forest trees (e.g., 
Magnolia L., Persea Mill., Corylus L., Castanea 
Mill., Quercus L., Halesia J. Ellis ex L., Styrax 
L.). In spite of these individual differences in 
ecological and taphonomic setting, it is interest- 
ing that each of these floras shows a greater range 
of diaspore size and a higher average diaspore 
volume than the Cretaceous floras. 

The dispersal mechanisms and syndromes of 
Tertiary angiosperm fruits and seeds may be in- 
ferred from their morphology and from their liv- 
ing relatives. Neither source is totally satisfac- 
tory; many morphological features are not 
preserved, and present dispersal adaptations of 
a genus or family are no guarantee of past mech- 
anisms. However, both lines of evidence suggest 
that a wide range of fruits and seeds adapted to 
animal dispersal were present by the Eocene and 
Oligocene. This included a variety of sizes from 
the smaller berries of the Vitaceae to the larger 
aggregate fruits of the Annonaceae or the drupes 
of the Mastixiaceae. This diversity of fruit types 
and sizes offered opportunities to a range of dis- 


lack, 1981; Tiffney, 1981), an array of small 
seeds and fruits became available, which was 
probably important to ground-dwelling rodents 
and granivorous birds. Thus, the Tertiary ap- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


pears to be the time in which major dispersal 
patterns (diaspore morphologies, relations with 
particular agents) first achieved their modem 
form and diversified among angiosperms. 


SUMMARY 


Cretaceous diaspores are generally small. Cre- 
taceous seed floras are marked by a small average 
diaspore volume (ADV) and a limited range of 
diaspore volume (RDV). Early Tertiary floras 
exhibit a major increase in ADV. Succeeding flo- 
ras show a broad trend of decreasing ADV, but 
with no decrease in RDV. The change in ADV 
through the Tertiary is a result of changes in the 
relative proportions of large and small diaspores 
in each flora. Small diaspores show no trend in 
size change through the Cretaceous and Tertiary, 
and after their appearance in the Tertiary, large 
diaspores also show no trend in size change. The 
increase in diaspore size is paralleled by an ap- 
parent change from the dominance of abiotic dis 
persal mechanisms in the Cretaceous to the in- 
creasing importance of biotic dispersal agents 
commencing in the earliest Tertiary. 


dispersal cannot be ascribed to taphonomic ог 

ecologic factors because similar depositional i 

vironments are sampled in both сен 

Tertiary deposits. Certainly the depu 0 "e 
M } + 4 trate that е 

апа 1 ша: 

and seeds could have been carried into the de- 


posit and preserved if present. Many of - 2 
tiary deposits (e.g., Nowy Sacz, i " 
demonstrate that even deposits domina 


es 
Climate could have influenced the yen 
tion ofthe vegetation or the presence of dis 
agents. However, Cretaceous climates 
first appearance of the angiosperms thro have 
the latest Cretaceous are generally felt to о 
been as warm as those of the early Tertiary ( pat- 
in, 1977; Barron et al., 1981; Thompson ё 
гоп, 1981), although there is good eviden 


ey, 1981). In addition, the Europe 


that were cooler | 


, 


and Quaternary include pene ‘ston 


but floras from these epochs have 
large diaspores. Perhaps the only 
bias is that all the fruit and seed data i 
from northern hemisphere, primarily E terns i 
localities. It is possible that different ра 


o 


| 


| 


1984] 


the evolution of diaspore size could have taken 
place in other portions of the world, but this 
cannot be evaluated from existing paleontolog- 
ical data. However, extant tropical (Levin, 1974) 
and temperate (Salisbury, 1942; Harper et al., 
1970) angiosp fruits and seeds app tly ex 
hibit the same range of sizes. 

The timing of this transition from small to 
large diaspores, and from the dominance of 
abiotic dispersal to the increased importance of 
biotic dispersal, is not clear from present knowl- 
edge. Since the mid- to Late Cretaceous and the 
early to mid-Tertiary of Europe both possessed 
warm climates, they presumably had a similar 
potential to host tropical plants. If plants with 
large diaspores were present in the Cretaceous 
tropics, they should have been seen in the Eu- 
ropean Cretaceous, much as they were in the 
Tertiary. However, a Cretaceous-Tertiary 
boundary cooling at higher latitudes (Hickey, 
1981) could have masked the evolution of an- 
giosperms with large diaspores in the tropics in 
the latest Cretaceous. These could have then ap- 
peared in northerly latitudes with the return of 
subtropical climates in the early Tertiary. 


INTERPRETATIONS 


The observed pattern in seed size can be ex- 
plained most simply as a response to one or both 
of two ecological factors. The first is the relation 
between seed size and the habit or ecological site 
ofthe parent plant. The second is the importance 
of dispersal agents, which exert pressure on the 
morphology and size of fruits and seeds, as evi- 
denced by the existence of distinct “dispersal 
Syndromes" in the angiosperms (van der Pijl, 
inm Each of these factors will be treated in 


SEED SIZE AND PARENT PLANT HABIT/HABITAT 


а агрег et al. (1970) and Silvertown (1981), 
i wing оп the classic work by Salisbury (1942), 
ма demonstrated a correlation between the 
i it, habitat, and diaspore weight of individual 
plants. Short-lived or weedy plants of open or 
unstable habitats generally have many small di- 
rs that may be dispersed widely, often by 
1С mechanisms (wind, water). These seeds 
Provide very little nutrient reserve to the ger- 

minating seedling, so that seedlings g пу 
vive only in open, sunny habitats. However, the 
ђе and wide dispersal of these dia- 
increase the 11] d that a few seedlings 


eur. 
ous 


TIFFNEY —RISE OF ANGIOSPERMS 


563 


will germinate in suitable habitats. At the other 
end of the scale, dominant, long-lived, forest trees 
of large stature tend to bear fewer, larger dia- 
spores, often involving large seeds. Because of 
their mass, such diaspores are often dispersed by 
biotic vectors, although less frequently they may 
be transported by gravity or water. A large seed 
provides a massive reserve of nutrients to the 
young seedling and enables it to become estab- 
lished in the shade of the deep forest. Between 
the two extremes are groups of plants with in- 
termediate habit, habitat, diaspore, and seed size 
including (in order of d ing stat d seed 
size) woodland shrubs, woodland herbs, and herbs 
of woodland margins. 

It should be noted that this is a general ten- 
dency, rather than an invariant rule. Habit and 
habitat adaptation may interact in a complicated 
manner and influence seed weight. Several early 
seral (weedy) trees have seeds as small as those 
of herbs, but possess a tree habit. However, such 
species (e.g., Populus L., Betula L., and Fraxinus 
L. in temperate forests; Cecropia Loefl. in the 
New World tropics) are often fast-growing and 
short-lived, and tend not to form time-stable, 
closed communities. Further, other features, in- 
cluding water availability and degree of season- 
ality, may influence diaspore and seed size (Bak- 
er, 1972; Levin & Kerster, 1974), and seed sizes 
in each ecological class appear to be slightly larg- 
er in tropical communities than in temperate ones 
(Levin, 1974). However, an overview of this 
variation suggests that the basic pattern of cor- 
relation of seed size with the habit and ecology 
of the parent plant holds as a broad principle in 
a wide range of environments. 

A graphic summary of the average diaspore 
volume and range of diaspore volume for several 
modern ecological groups is presented in Figure 
2 (cf. Harper et al., 1970). The values for each 
ca were originally calculated by weight 
(Salisbury, 1942; Levin, 1974), but I have con- 
verted this to cubic millimeters by use of the 
graph presented in Figure 1. 

Comparison of the values for the average and 
range of diaspore volumes (ADV, RDV) for each 
of these ecological groups with the ADV and 
RDV for the fossil floras reveals a clear pattern. 
Cretaceous floras (41-7) have ADV s equal to or 
less than that for modern plants of open com- 
munities. Further, only in the case of the flora 
from Massachusetts (#2) does the RDV exceed 
that seen in modern plants of open habitats. The 
sedimentary context (Doyle & Hickey, 1976; 


564 


Hickey & Doyle, 1977), and the small seeds of 
the earliest angiosperms, support the contention 
that they were “weedy?” plants of unstable or 
transient habitats outside of the climax gymno- 
sperm forest (Takhtajan, 1976; Hickey & Doyle, 
1977; Doyle, 1978; Niklas et al., 1980; Tiffney, 
1981). Note that this statement does not exclude 
the possibility that the Cretaceous floras included 
trees, for the ADVs of several Cretaceous floras 
overlap with the lower end of the range of tree 
diaspore volumes. However, although trees and 
shrubs may have been present in these com- 
munities, the small sizes of the diaspores in- 
volved imply that these were likely early succes- 
sional plants rather than canopy dominants. An 
example may be provided by Platanus L., which 
is probably present as early as the Cenomania 
(97 Ma) (Dilcher, 1979; Schwarzwalder & Dil- 
cher, 1981). Plat i ly ional 
in modern floras (Braun, 1950) and has been 
demonstrated to occupy unstable, stream-side 
habitats in the Eocene (Wing, 1981 

By contrast, the Tertiary floras possess a wide 


11 £ 


tree 


hve eco- 


logical categories of diaspore size. This suggests 
that each flora has the potential to contain plants 
of any and all habits and habitats. It is not pos- 
sible to be certain that any one flora was domi- 
nated by plants of a particular habit or habitat 
from diaspore size for three reasons. First, the 
diaspore sizes for the five modern ecological cat- 
egories do overlap. Second, taphonomic factors 
have resulted in the mixing of disseminules from 
different communities in the fossil record. Third 
the average diaspore volume (ADV) for each fos- 
sil flora is not a fully trustworthy indicator of the 
dominant physiognomy of the community; one 
or two large fruits can drastically affect the ADV 
of a flora. For example, the elimination of the 
three largest diaspores (two species of Carya and 
one of Juglans) from the New Haven flora (Fig. 
2, #27; ЇЧ = 43 species) drops the ADV from 
1,077 mm? to 133 mm’. The degree of influence 
of large specimens on the ADV may be approx- 
imated by the coefficient of variation (s.d./X, see 
Table 2). Large values of the coefficient of vari- 
ation indicate that the mean is not that of a ran- 
domly distributed population but is an artifact 
of a polymodal distribution. The value of this 
coefficient is high through the Tertiary and shows 
no significant directional change during this time 
(commencing with the Woolwich and Reading 
beds, a regression of the coefficient of variation 
with time yields P > 0.20; r = —0.27, N = 18). 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


In a broad manner, the ADV decreases through 
the Tertiary, although not in a statistically-sig- 
nificant manner (regression of ADV versus time 


close to that for trees in the modern day. This is 
not unexpected, as both floras are presumed on 
taxonomic bases to be related to the modern for- 
ests of Indomalaysia (Chandler, 1964). From this 
high, the ADV falls off through the Tertiary to 
values close to those for modern plants of open 
environments (note flora #22, Nowy Sacz, and 
#24, Kranichfeld). This trend indicates an in- 
creasing dominance of smaller-seeded plants and 
parallels the climatic deterioration and increase 


hardt, 1978). These cooler and more variable 
temperate climates could be expected to result 
in the evolution of new, open, unstable com- 
munities, populated by plants with a rapid life 
cycle. This is what is observed in the taxonomic 
composition oflate Tertiary communities, which 
show a diversification of herbaceous angio- 
sperms (Niklas et al., 1980; Tiffney, 1981). How- 
ever, it is of great importance to note that while 
small-seeded forms dominated in the later Ter- 
tiary, large-seeded trees remained as part of the 
flora, although diminished in importance. 

In summary, the diaspore size data sugges! 
that Cretaceous angiosperms were small and/or 
opportunistic plants, and that only in the latest 
Cretaceous or early Tertiary did the group clearly 
evolve to include physiognomically-dominan! 
trees of stable, climax forests. This does not ex 
clude angiosperms from forming forests 1n x 
Cretaceous, but the diaspore size data Mec 
that such forests would be restricted pe unstable 


© 
zh 
© 
8 
[^2] 
S 
© 
E 
a 
8 
a 
3 
€ 
8 
3 
B 


associated with sediments indicative of -— 
environments (e.g., river margins), while = 


LI 2 5 
nosperms should be associated with e ГА 


Jr 


back swamps or uplands). c least 
The foregoing interpretation rests pee: 
. pe^ F . inerati 


does the correlation of diaspore size e 
habitat witnessed in the modern day rae : 
respect to Cretaceous angiosperms, 10 


MEE, = 


) 


H 


———<—— ل‎ н нна 
~ 


—À 


= 


f 


1984] 


there are few modern homologues? I cannot an- 
swer this question directly, but suggest that Cre- 
taceous angiosperms do indeed follow the same 
pattern as modern ones since the relation of di- 

pore si d habit i lds across a wide 
range of t groups. Chaloner and Sheer- 
in (1981) have successfully applied this concept 
to an explanation of early land plant reproduc- 
tive strategies, in which the evolution of larger 
plant size is directly correlated with an increase 
in disseminule size. Also, while the fact that these 
Carboniferous plants are extinct makes the in- 
ference of successional status tenuous, it appears 
that the dominants of the relatively more stable 
lowland swamp communities (e.g., medullosans 
and certain arborescent lycopods) had larger dis- 
seminules than plants of less stable habitats (e.g., 
calamitaleans, cordaitaleans, and conifers). The 
Mesozoic flora was dominated by the gymno- 


Ме а (1981) suggested that cycadeoids may 
he been restricted to unstable stream margins 
n the Cretaceous, while conifers dominated the 


à о 
Pros a (Niklas et al., 1980; Tiffney, 1981). 
а ар if this was an unrelated event or a 
The la се tof the expansion of the angiosperms. 

*r possibility deserves consideration, be- 
cause the dominant 


itio by physiological factors. These ele- 

ents of eire "EQ" ant + that the 
ма of diaspore size and the habit and/or 
lend = и the parent plant generally holds for 
о f» ts and may be assumed to have done 

Т early angiosperms. 

nd, the association between diaspore size 
Detain hin: was demonstrated using tem- 
1970) е (Salisbury, 1942; Harper et al., 
эы It hold with warm-temperate to often 
' taxa, which commonly occur in the Ter- 
Positive Z the answer is circumstantial but 
: the relationship of seed size to habit/ 


TIFFNEY —RISE OF ANGIOSPERMS 


565 


habitat of the parent plant seems to be general 
among land plants, and anecdotal evidence sug- 
gests that it holds in the modern tropics (van der 
Pijl, 1969; Stebbins, 1971; Opler et al., 1980; 
Janzen & Martin, 1982). In one case where seeds 
of plants of the five ecological categories were 
measured (Levin, 1974), the average seed size in 
each category was a bit larger (two to five times) 
than observed in the temperate flora. While in- 
teresting, the magnitude of this variation is too 
small to affect the hypothesis of Cretaceous and 
Tertiary angiosperm seed size presented here. 


SEED SIZE AND MODE OF DISPERSAL 


Seed (diaspore) dispersal is an important ele- 
ment in the life cycle of seed plants (cf. Levin & 
Kerster, 1974). Abiotic dispersal (wind, water) 
is successfully employed by a wide range of an- 
giosperms, including many trees. However, there 
is little question that biotic dispersal is of greater 
importance, if not dominant, among angio- 
sperms in the modern day. Biotic dispersal agents 
exert a strong selective pressure on angiosperm 
ү. эң لے‎ A 2 а 1 1 ae A 


by the evolution of a wide range of adaptations 
or animal dispersal (cf. Ridley, 1930; van der 
Pijl, 1969). I am unaware of any estimate of the 
absolute proportion of the world’s angiosperm 
flora that is animal-dispersed, but in the few re- 
ports of individual communities, the proportion 
of biotically-dispersed species is often high (Jones, 
1956; Smythe, 1970; Stiles, 1980; Handel et al., 
1981) and reaches 90% in some Central Amer- 
ican examples (Frankie et al., 1974; Janzen, 1977). 
This may be affected by edaphic factors, how- 
ever, as suggested by Janzen’s (1977) observation 
that a low degree of biotic dispersal occurs in 


о 


poor soils. 

There are five animal groups commonly in- 
volved in the dispersal of angiosperm fruits and 
seeds; ants, fish, reptiles, birds, and mammals 
(including bats). All have, to greater or lesser 
degrees, affected the size and shape of angio- 
sperm disseminules. The history and general in- 
fluence of each group is considered in turn. 

Ants. Ant dispersal (myrmecochory) is pri- 
marily known among forest floor herbs, partic- 
ularly in the temperate zone (van der Pijl, 1969; 
Handel et al., 1981) although it is also reported 
from other areas (e.g., Berg, 1975). Morpholog- 
ical adaptations to ants usually involve small 
diaspore size and the presence of an oil body or 


566 


elaiosome as a food source on the exterior of the 
diaspore. Although ants are known from the Cre- 
taceous (Burnham, 1978), they would affect only 
small seeds. 

Fish. Fish are generally assumed to have a 
minor role in the dispersal of angiosperms (Rid- 
ley, 1930; van der Pijl, 1969), although a recent 
study of Amazonian plant communities (Gold- 
ing, 1980) suggested that fish may disperse dia- 
spores, particularly in time of high water. The 
degree to which this dispersal syndrome involves 


р апа 517е, ап‹ 


its import tside the Amazon basin, are not 
clear. It may not be so much a “coevolved syn- 
drome” as a glorified case of scavenging. Fish 
have been around since the Paleozoic (Romer, 
1966) and may well have served as generalist 
dispersal agents in swamps and rivers since the 
Carboniferous. 

Reptiles. Reptilian dispersal (saurochory) is 
a recognized syndrome, often involving brightly 
colored and odoriferous seeds or fruits borne near 
the ground and of a wide range of sizes (van der 
Pijl, 1969). The important modern representa- 
tives include turtles and tortoises, which first 
spread as a group in the Triassic (Romer, 1966), 
and lizards, particularly iguanas. The latter group 
appears in the Eocene, although its forerunners 
may go back to the Upper Jurassic (Romer, 1966). 
Perhaps the decline of the reptiles at the end of 
the Cretaceous, just as the angiosperms were 
undergoing a major expansion, explains the rel- 
ative lack of dispersal syndromes involving the 
two groups in the modern day. The possibility 
must also be entertained that the primary dis- 
persal vectors of the large seeds of the physiog- 
nomically-dominant Mesozoic gymnosperms 
were reptiles, and that the decline of the reptiles 
may have influenced the demise of some gym- 
nosperm groups in the late Cretaceous (Krassi- 
lov, 1978). If so, this would also imply that Late 
Cretaceous and early Tertiary plant communities 
were in a state of flux, and open to angiosperm 
invasion. 

Birds. Birds are among the most important 
of angiosperm dispersal agents, affecting very 
small to very large diaspores in temperate and 
tropical communities (Ridley, 1 930; van der Pijl, 
1969). There are many morphological adapta- 
tions of angiosperm disseminules to bird dis- 


z y 
drome involves odorless, brightly colored, edi- 
ble, fleshy fruits with hard, resistant, inner seeds. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


These are often clearly displayed; and, in dehis- 
cent fruits, the seeds often dangle from the fruit 
at maturity. 

The fossil record of the birds has been re- 
viewed at the family level by Brodkorb (1971), 
to which I have added data provided by Ки- 
rochkin (1976) (Fig. 3). Bird families often con- 
tain organisms of diverse dietary habits, but, 
based on information provided by van Tyne and 


sumed), “omnivorous” (some plant material 
consumed), or “vegetari 
material consumed). Figure 3 presents a sum- 
mary of the diversity of bird families from the 
Early Cretaceous to the present, broken into these 
three dietary groups. No fossil families are in- 


cluded; they are few in number, and it would be | 


difficult to ascertain their dietary affinities. The 
family level is used for ease of tabulation. A ge 
neric or specific level summary is beyond the 
scope of this paper and would not greatly alter 
the trends seen in Figure 3, although the family 
level does mask the effect of the late Tertiary 


diversification of the species-rich, pmo | 
omnivorous or vegetarian, passerines (Brodkorb, | 


1971). 

Cretaceous families for which diets may 0 
surmised from modern relatives are predomi- 
nantly carnivorous and marine; one omnivorous 
family is present (Cracraft, 1973; Brodkorb, 
1 Th 


ilies (which first appear in the Eocene) rises 
sistently, while that of the carnivorous 
falls. i 
Uk fossil rec 
тропа"! 
in Te 
š . : rtan 
whereupon they became increasingly impo 


present day. However, the available fo { 
of any group may be seen either as 4 real id " 
tion of evolutionary events, or as 100 bia: xi 
be trusted directly. Cracraft (1973) Met the 
the fossil record to be less important th 


ison of the timing of Cretaceou 
continental movements with the т 


) 


1984] TIFFNEY —RISE OF ANGIOSPERMS 567 


C (78) 46.4% 


y (50) 29.7% 


=, 
І 
| 


ЈУ (40)23.8 % 


C І 
та __ | 529% : 
Ee 


C bx 
(58.6 ?6) : 


Lecco 
VE ii (64.1%) | : 
(66.6 95) |: 
Or 
_-7 426.4%) 
0 
27.6% : 
f ) v 
4 (20.6%) 
ж zn 
BB. 
(28.2%) 
y Ww 
/ (13.8%) 


C 
| 


_ FIGURE i: 
into three di 
of fam 
Pre. 
Mio = Mine 


— (83.3, 
(100°) 


jet 


-O 
(30%) 


ri 
/ 
£ 


| 
. 

oe 
жү 


(7.7 %) 


E 
PEE 
V 


5. 5%) 


© 
X 

\ 
o 


Pre- 
Maast. Maast. 


Pe 


Eo Oligo 


Mio 


Plio 


NOW 


FAMILIES OF BIRDS WHICH ARE CARNIVOROUS (C), OMNIVOROUS (0), 


OR VEGETARIAN (V). 


_ Cumulative diversity of modern families of birds through the Cretaceous and Tertiary broken 


trichtian, Pe = 


Eo = Eocene, Oligo = Oligocene, 


ilies | in each epoch. Data а Brodkorb (1971, 1976); Kurochkin (1976); van Tyne and Berger (1976). 
Maas Paleocene, 


рге- AE 
ne, Plio — Plioce 


568 


butional patterns of bird families. On this basis, 
he inferred that the immediate ancestors, if not 
the actual families, of modern birds were present 
by the mid- and Late Cretaceous. Brodkorb (1971) 
also suggested that modern families were present 
in the mid- and Late Cretaceous. He reasoned 
that the modern appearance, specialization, and 
diversity of early Tertiary birds argue for con- 
siderable antecedent evolution of the group. 

Neither author accepts the fossil record at face 
value. This logic is reminiscent of the school of 
paleobotany that sought the origins of the angio- 
sperms in the latest Paleozoic and early Mesozoic 
on the basis of their “diverse” Cretaceous record 
(Axelrod, 1960, 1970). Subsequent study of the 
angiosperms (Doyle & Hickey, 1976; Hickey & 
Doyle, 1977; Doyle, 1978) has demonstrated that 
the initial radiation of the angiosperms was con- 
fined to the Cretaceous and matches the known 
fossil record of the group. I choose to accept the 
fossil record of the birds as indicative of a major 
radiation in the Tertiary, perhaps with its begin- 
nings in the latest Cretaceous, paralleling that of 
mammals (Colbert, 1969) and of modern angio- 
sperm families (Niklas et al., 1980; Tiffney, 1981; 
Muller, 1981). A recent consideration of avian 
evolution (Cracraft, 1982) does not alter this view, 

cause it emphasizes the aquatic and presum- 
ably carnivorous nature of Mesozoic birds as they 
are presently understood. 

Mammals (excluding bats). The dispersal of 
angiosperm seeds by mammals is probably only 
a little less important than that by birds (Ridley, 
1930; Martin et al., 1951; van der Pijl, 1969; 
Halls, 1977). Van der Pijl gives the impression 
that it is of greater importance in the tropics than 
in the temperate regions. The fruit and seed char- 


varied and may involve internal or external 
transport. Mammals often possess a good sense 
of smell and thus many mammal-dispersed fruits 
have a distinctive odor (van der Pijl, 1969). The 
thickness of the seed wall tends to vary with seed 
size. Small seeds that would probably be passed 
through the digestive tract do not require hard 
coats, whereas large ones with edible contents 
require protection against direct predation. One 
important aspect of mammal dispersal is that 
mammals can move Seeds of quite large sizes, 
often from witl py (Ridley, 1930; 
van der Pijl, 1969). Mammal-dispersed fruits of 
more open habitats are often adapted to external 
transport (van der Pijl, 1969), 

The Tertiary is the “аре of mammals," and is 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


the time of radiation of a host of important dis- 
persalist groups (Romer, 1966; Colbert, 1969). 
Rodents, lagomorphs, primates, artiodactyls, and 
perissodactyls all commences radiations | in the 
Eocene. Other. 
eages appeared i in the mid-Tertiary. While mod- 
ern terrestrial mammals are almost entirely 
products of Tertiary radiations, the possibility 
remains that some Crqtaceols lineage of mam- 
mals could have been i 
Lillegraven (1979) suggested that perhaps mam- 
mals and flowering plants were establishing the 
basic features of their coevolutionary relation- 
ship in the Cretaceous. Ce y, several major 
groups of Cretaceous mammals are presumed to 
be omnivorous and a few herbivorous (Kron, 
1979; Clemens & Kielan-Jaworowska, 1979; 
Clemens, 1979), although all are generally of small 
size (Lillegraven, 1979). While I do not Ф 
that Cret 1s had 
with angiosperms, it seems unlikely to me that 
such interactions were significant and wide- 
spread. The known Cretaceous thick-walled seeds 
are not especially common, and they show no 
trends in morphology or size to suggest their spe- 
cialized adaptation to biotic dispersal. Further, 
if such interactions were established to a signif- 
icant degree in the Cretaceous, it is surprising 
that they should not have carried over into the 
Tertiary and the present. Instead, today the fruits 
of primitive families or of primitive lineages in 
families are more commonly abioti y-dis- 
persed, while derived families and lineages а 
dispersed by organisms of Tertiary origin (Schus- 
ter, 1976). Parallel to this pattern is а secon 
one, ipei un by the Rosaceae, for the #0" 
graphic co-occurrence of fleshy-fruited angio- 
sperm а and “advanced” (products of Ter- 
tiary radiations) mammalian lineages (Schuster, 
1976). This information, while importantas 


dis- 


ats. | 

angiosperm propagules in the warmer regions 
the world where fruiting occurs throu; (a 
year. This is borne out by a wide range 9 
ecdotal and scientific observations Со 
1970; Smith, 1976). Bat-dispersed disse 
are normally large, odoriferous, fleshy 
a hard stone, or a similar seed wi 
or aril (van der Pijl, 1957, 1969). 

The fossil record of bats (Smith, 1 
ited and often fragmentary. Bats firs 


tha 12 
че Laity 


ruts i 
a sarco 


976) isi 
first ар рреаг 1? 


АП indicat! tive 


= 


— —À ~ 


~ =” 


1984] 


ofan insectivorous diet. The first frugivorous bat 
was thought to be Archaeopteropus transiens 
Meschin. of the Italian Oligocene (Jepsen, 1970), 
but more recent investigation reveals that the 
dentition of this specimen is that of an insecti- 
vore (Smith, 1976). At present, the earliest rec- 
ord of a frugivore is of a phyllostomatid bat from 
the late Pleistocene (Smith, 1976). 

While some authors feel that bats may have 
been present in the Late Cretaceous (Jepsen, 1970; 
Smith, 1976), the absence of pre-Eocene bats, 
and the rapid diversification of the group in the 
Eocene and Oligocene, suggests that bats were 
unimportant, if extant, in pre-Eocene time. Fur- 
ther, the earliest bats were insectivores, and fru- 
81уогу appears to be a derived condition (Smith, 
1976). It is thus likely that the morphological 
characters of the bat-dispersed fruit evolved as 
à dispersal 


aptations and of restricted influence on the an- 
Blosperms. It appears that the important groups 
of modern biotic dispersal vectors all underwent 


Phology and size. Such changes are seen in the 
carly Tertiary. 


CONCLUSIONS 


Two separate features have been explored in 
an attempt to explain the observed pattern of 
lat m Size change. The first involves the re- 

onship between seed size and the habit and 
tat of th 


Conclusions +h 


acnn 
Yv JUSI 19 


Не __ А 
om omically-dominant plants of stable forest 
"nme The second approach turns to the 
the fo m of dispersal strategies as inferred from 
the 551 record of the dispersal agents and from 
morphology of the disseminules themselves. 
aoa that biotic dispersal vectors influ- 
in enn fruit and seed morphology only 
кашг test Cretaceous or early Tertiary. Each 
the с" Provides an adequate explanation of 
explain Tved pattern, although the first does not 
its timing. However, the two are not mu- 


TIFFNEY — RISE OF ANGIOSPERMS 


569 


tually exclusive and may be synthesized to pro- 
vide a new p pective on angiosperm evolution. 
As a preamble to this synthetic interpretation, it 
is necessary to explore briefly the assumption 
that canopy dominance generally requires large 
seeds, which, in turn, normally require biotic 
dispersal agents. 
or an angiosperm to achieve dominance (in 
a physiognomic, not a numerical, sense) of the 
community, its seedlings must be able to grow 
in the shade of the parent (or other) trees, thus 
insuring the continuity of the population. Any 
increase in seed size in an abiotically-dispersed 
plant would provide the seedlings with more nu- 
trients and the capability of growing in a more 
shaded habitat. Logically, one could envision a 
slow increase in the seed size and shade tolerance 
of seedlings in one population, ultimately leading 
to in situ dominance of the community. How- 
ever, larger seeds generally have a reduced radius 
of dispersal, particularly in closed communities 
or in the absence of means of water transport. 
Thus, in an abiotically-disr 1 plant, increased 
seed size would result in smaller population sizes 
and perhaps increased endemism and a higher 
potential for extinction. All this implies that an- 
giosperms required the presence of biotic dis- 
persal agents in order to attain canopy domi- 
nance in a closed community. This conclusion 
pp tin light of р forest trees 
that have lost their dispersal agents. Ginkgo L. 
attained a wide distribution in the Mesozoic, and 
maintained it into the Tertiary (Tralau, 1968), 
but is now a highly restricted endemic in its nat- 
ural state. Its fleshy and odoriferous seed seems 
well-adapted to attracting reptiles, and perhaps 
these were the vectors by which it spread in the 
Mesozoic. The loss of these vectors in the early 
Tertiary would be of little immediate impor- 
tance, because the genus had a wide distribution 
in this time of warm climate. However, with the 
climatic changes of the later Tertiary, its range 
became severely restricted, and, in the absence 
of a dispersal vector, it was unable to re-expand 
its range in periods of favorable climate, thus 
coming to the brink of extinction in the Holo- 
cene. Similar, although less dramatic, examples 
of the effect of the loss of a dispersal agent on 


H 
Hfın 


examples support the tentative conclusion that 
attainment of canopy dominance and the main- 
tenance of a stable population structure in closed 


570 


forests are generally linked to the establishment 
of biotically-mediated dispersal. 

The scenario involving seed size and dispersal 
in the evolution of the angiosperms is simple. 
Our understanding of Early Cretaceous land plant 
communities is limited but conveys the impres- 
sion that there were few existing seed plants of 
an early successional nature. The angiosperms 
first appeared about 120 Ma as an “r” strategy 
(weedy g list) group with small stature, rapid 
life cycle, and small, abiotically-dispersed seeds. 
They spread to occupy a wide variety of early- 
successional sites (Doyle & Hickey, 1976; Hickey 
& Doyle, 1977; Doyle, 1978). This diversifica- 
tion was probably paralleled by the appearance 
of a variety of adaptive vegetative morphologies 
and may have resulted in the “blocking out" of 
the general character complexes of several mod- 
егп suprageneric groups. Evidence from leaf ar- 
chitecture (Doyle & Hickey, 1976; Hickey & 
Doyle, 1977) indicates that the angiosperms had 
attained shrub and tree stature by the late Albian 
or early Cenomanian (about 100 Ma). These 


Aminata 


y un 
environments (e.g., aggradational river bottoms) 
but probably were displaced by the large-seeded 
and domi tgy р in more stable hab- 
itats. Some angiosperms may have formed an 
understory of shrubs and small trees in open- 
canopied gymnosperm forests such as those of 
the uplands of New Caledonia in the present day 
(L. J. Hickey, pers. comm.). 

Therefore, while Cretaceous angiosperms were 
probably diverse in certain habitats and perhaps 
numerically-dominant over the gymnosperms, 
they did not dominate the world vegetation in 
the physiognomic sense that they do in the mod- 
ern day. Rather, they were a more specialized 
weedy" group that initially radiated to fill a 
specific aspect of the community, but that did 
not continue their radiation at the same rate 
throughout the Cretaceous. This implies that an- 
giosperm diversity should have risen slowly, 
rather than dramatically, during the later Cre- 
taceous, which is what is observed (Krassilov, 
1977; Niklas et al., 1980; Tiffney, 1981). That 
the Cretaceous angiosperms included few if any 
large canopy trees capable of sustaining a closed 
climax forest is inferred strictly from the paucity 
of large angiosperm diaspores. While large seeds 
would have permitted tl i : 
physiognomic dominance 


. 


their sıze 


Ћ 
of the community, 
ation with biot- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


ic dispersal agents. Both the record of diaspore 
size and of animals in the Cretaceous suggest that 
the appropriate dispersal agents for angiosperms 
were few, and that the advantages of large seeds 
were outweighed by the disadvantage of their 
poor dispersal. 

This impasse was broken by the radiation of 
birds and mammals (including bats) in the early 
Tertiary or perhaps latest Cretaceous, leading to 
the swift development of many biotic dispersal 
syndromes, which in turn influenced the evolu- 
tion of the angiosperms in the Tertiary. 

The total diversity of angiosperms increased 
dramatically in the early Tertiary (Niklas et al., 
1980; Tiffney, 1981). This is to be expected as à 
result of the development of plant-animal dis- 
persal interactions for three reasons. First, CO- 
evolution favored increasing specialization and 
speciation (cf. Regal, 1977). Second, greater dis- 
tance of dispersal favored allopatric speciation, 
an ultimate example of which is the modern east- 
ern North America-eastern Asia pattern of dis- 
junction (Wood, 1972; Wolfe, 1975). Finally, the 
establishment of dispersal syndromes with ani- 
mals opened the way for angiosperms to explore 
all possible habits and habitats within the com- 
munity. This is partially reflected in the high 
value of the coefficients of correlation (Table 2) 
in the Tertiary, indicating the increased poly- 
modality of diaspore size in Tertiary floras. In- 
creased seed size led to an arborescent com 
munity with decreased light penetration, 
diversified biotic competition, and presumab!) 
tighter species packing, all features favoring in- 


creased diversity. Further, all the changes in the 
eraction 


(Crepet, 1979, 1984). эше 
The latest Cretaceous and early Tertiary is als? 
remarkable as a time of rapid “modernization 
of the world's flora. This involves two eee 
the sudden appearance of large numbers of m ў 
егп famili d E (Niklas et al., 1980; Mul 
ler, 1981; Tiffney, 1981) and their swift $ 19 
over the Northern Hemisphere (W olfe, "i d 
Both follow logically from the establishme 
dispersal relationships. The rapid «ро ИШ of 


i i s to th 
evolutionary spiral that extend ows from 


day. The rapid spread of these taxa foll dis pers | 


their association with the effective 


| 


| 


— 


1984] 


agents, although three other factors were of im- 
portance. First, the Late Paleocene and the Eocene 
were periods of warm climate in the northern 
hemisphere (Buchardt, 1978; Wolfe, 1978). Sec- 
ond, apparently both North Atlantic and North 
Pacific land bridges were available to terrestrial 
organisms in the Early Tertiary (Lehmann, 1973; 
McKenna, 1975; Tiffney, 1980). Finally, and 
perhaps most importantly, the newly-evolved 
angiosperm taxa probably included many ad- 
aptations to previously unfilled “niche 
spreading at a time when several gymnosperm 
groups had recently declined or gone extinct 
(Krassilov, 1978; Niklas et al., 1980; Tiffney, 
1981; Vachrameev, 1 982). 

The question remains: what initiated the in- 
creased level of interaction between plants and 
dispersal agents in the latest Cretaceous and early 
Tertiary? Did external factors (e.g., the decline 
of the reptiles) lead to the evolution of new groups 
of bir 5 and mammals, which in turn spurred 
angiosperm evolution? Alternatively, did angio- 


Synergistic nature of coevolutionary relation- 
ships. Further, while I have emphasized the his- 
== importance of the development of angio- 
: p? dispersal syndromes in this paper, it is 
my one of three coevolutionary features that 
2 have had a strong influence on the course 
Nie Blosperm evolution. Pollination syndromes 
ave perhaps had an even greater influence in 

view of the vast array of phological and eth 
= Permutations involved. Indeed, the in- 
i. um of angiosperms with modern polli- 
adio rud have been established at a slightly 
perdi te than the interactions with modern 
mei agents (cf. Crepet, 1984). Additionally, 
ux cdm between herbivores and plants have 
ales i п explored in the fossil record but must 
ave been of significance (cf. Niklas, 1978). 


LED I would like to explore briefly three 
СШагу points 


i 


th 191, the evidence presented here suggests that 
ше Durian Theory” (Corner, 1949, 1964) is 
nable. The *Durian Theory” assumes that 


Crate size, probably animal dispersed, and 


w : А 
45 contained in a dehiscent fruit borne of a 


TIFFNEY —RISE OF ANGIOSPERMS 571 


large, pachycaulous tree. According to the fossil 
record of angiosperm seeds, such a combination 
of characters could have evolved only in the Ter- 
tiary, following the establishment of widespread 
biotic dispersal syndromes. Certainly no evi- 
dence is seen of **moderate-sized" angiosperm 
seeds in the Cretaceous: they are all small. Fur- 
ther, no evidence is seen of widespread animal 
dispersal in the Cretaceous, or of pachycauly, 
although the scarcity of Cretaceous angiosperm 
wood (Wolfe et al., 1975) renders the last a state- 
ment based on negative evidence. 
Second, tl ini d i 


d i. 


did not appear to have undergone any significant 
directional change of size during the time period 
measured. Two regressions were run: (1) the size 
ofthe smallest seed ofeach ofthe floras examined 
(Table 2) against time, and (2) the size of the 
largest seed from each ofthe Tertiary floras against 
time. The first regression was not significant 
(0.20 > P > 0.10; r= 0.29, N = 26); the Rusin- 
ga flora was excluded on account of its anoma- 
lously large “smallest seed" —probably a func- 
tion of the collection of the flora from surficial 
lag deposits. In the second case (N — 18, r — 0.40), 
the r value is marginally insignificant (P — 0.10), 
however, this figure may be influenced by the 
temperate adaptations of the source plants of the 
later Tertiary. This suggests that the two seed 
classes have achieved some form of balance be- 
tween the selective features that affect size. The 
time stability of small seed size implies that the 
appearance of larger seeds in the early Tertiary 
did not alter 11 lecti d tage of ||| d 
size in certain environments. This could be fur- 
ther extended to imply that the basic habitats 


altered during the history of the angiosperms, 
although in some times habitats favoring op- 
portunistic forms are less widespread (early Ter- 
tiary) than in others (late Tertiary, Pleistocene). 
With respect to the larger seeds, it appears that 
there has been no distinct trend of size increase 
through the Tertiary. This could imply that there 
is an optimal upper limit for seed size, one that 


and efficiency of dispersal, and that was achieved 
by the early Tertiary. However, this observation 
may be influenced by climate. The fossils are 
primarily from Europe and sample a tropical 
vegetation in the early Tertiary, but an increas- 
ingly more temperate one through the later Ter- 
tiary. Limited data (Levin, 1974) suggest that 
modern tropical lowland communities have 


572 


1 + 


slightly larger р ` 
If so, then possibly the size of the largest seeds 
did increase slightly through the Tertiary. 
Finally, both Harper (1961) and Margelef 
(1968) have suggested that the evolutionary his- 
tory of a group should tend to parallel its succes- 
sional history, and that an evolving group should 
“climb its own seral tree." This is what is seen 
in the fossil record, with the angiosperms initially 
appearing as weedy plants and in due time evolv- 
ing to become dominant members of the climax 
ommunity. The fossil record suggests that this 
transition required the appearance of dispersal 
vectors to permit the dispersal of large seeds of 
the plants of later seral stages. This implies that 
the unique characters of the angiosperms (rapid- 
ity of life cycle, potential for insect pollination, 
specialized conducting tissue, etc.) were not suf- 
ficient separately or jointly to directly ensure the 
final dominance of the group. However, the de- 
velopmental plasticity of the angiosperms did 
permit them to evolve a diversity of fruit and 
seed dispersal adaptations in response to the ap- 
pearance of dispersal agents. This observation 
raises interesting questions about the structure 
and function of pre-angiosperm communities. 
Were dispersal agents involved in previous cli- 
max communities? Do climax communities in 
which dispersal agents are not available have a 
different, perhaps more open, canopy structure 
than those in which dispersal agents are present? 
[For example, could the seeming diversity of 
lowland Carboniferous coal swamps as contrast- 
ed to the upland Carboniferous vegetation be 


у ity of anisms per- 
mitting the dispersal of large seeds in the lowland 
community (water, fish) and their absence in the 
upland communities?] 


SUMMARY 


Analysis of Cretaceous and Tertiary fruit and 

seed floras from the Northern Hemisphere re- 
veals a change in the average size and range of 
size of angiosperm diaspores through time. Cre- 
taceous floras are composed almost entirely of 
small diaspores. Early Tertiary floras are domi- 
nated by large diaspores but include Many as 
small as those of the Cretaceous. Later Tertiary 
floras are pri ily composed of smaller dia- 
spores but consistently include a few very large 
ones. Analyses suggest that the minimum dia- 
spore size for angiosperms has not changed since 
their appearance in the Cretaceous, and that their 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


maximum size has not increased greatly, if at all, 
from the time of appearance of large diaspores 
in the earliest Tertiary to the present. There are 
two major features that influence diaspore size: 
(1) the relation between seed size and the eco- 
logical characteristics of the parent plant, and (2) 
dispersal mechanisms. The observed pattern in 
angiosperm diaspore size through time may be 
interpreted in light of these two selective forces. 
Cretaceous angiosperms were primarily small- 
seeded, abiotically dispersed shrubs or oppor- 


habitats in the gymnosperm-dominated vegeta- 
tion, but probably not forming a closed-canopy 
climax community. The relative paucity of dis- 
persal agents in the Cretaceous limited the suc- 
cess of large angiosperm diaspores and the closed- 
canopy forest that they could be expected to give 
rise to. The latest Cretaceous or early Tertiary 
radiation of birds, bats, and terrestrial mammals 
reversed this situation, permitting a biotic inter- 
action favoring large, animal-dispersed propa- 
gules. This in turn allowed the establishment of 


can max 
nomically- as vell as numerically-do 
angiosperms, and similar in structure for the first 
time to those ofthe modern day. This interaction 
of seed size and dispersal agents may have oc 
curred with, or slightly later than, the establish- 
ment of interactions between angiosperms and 
modern pollinators. Regardless of sequence, the 
establishment of biological interactions between 
angiosperms and their pollinators and disperse’ 
was reflected in the rapid appearance of ae 
families and genera, and of their swift gni 

around the northern hemisphere, in the lates 
Cretaceous and early Tertiary. 


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THOMPSON, S. L. & E. J. BARRON. 1981. Comparison 
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89: 143-16 
TIFFNEY, B. H. 1977a. Fossil angiosperm fruits and 
seeds. J. Seed Technol. 2: 54—71. 


1977b. Dicotyledonous angiosperm flower 
from the Upper Cretaceous of Martha’ s Vineyard, 
Мама ee Nature 265: 136—137. 
. 1980. [Abstract: ] The Tertiary flora of eastern 
orth America and the North Atlantic land bridge. 
— Int. Congr. Syst. Evol. Biol. 373. 

1. Diversity and major events їп the evo- 
дал ы of land plants. Pp. 193—230 in K. J. Niklas 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


(editor), ar aie Paleoecology and Evolu- 
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TRALAU, H. 1968. Evolutionary trends i in the genus 
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. 1982. Ancient angiosperms and the evolution 

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H: 


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VAN DER BURGH, J. 1978. The Pliocene flora of For- 
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9. Principles of Dispersal in Higher Plants. 
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VAN TYNE, J. & A. J. BERGER. 1976. Fundamentals 
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CO Ce ROBO QN фо» Сыйырды Nn Ьл stro d ae nA сыды ыйды а lala 


— 


төз — 


mm 


NEW PALEOBOTANICAL DATA ON ORIGIN AND 
EARLY EVOLUTION OF ANGIOSPERMY 


VALENTIN A. KRASSILOV! 


ABSTRACT 
Thea bl f angi rigin since 1975 are summarized. Jurassic 
Hirmerella i is assigned to proangiosperms based on its fruit-like гин Achenes with persistent 
es be lo 


vules to one and fusion of interseminal scales. Angiosperm fruits, grass-like leaves, and 
several kinds of spikes and coheed sins are found in the Lower Cretaceous of Mongolia. A middle 
Albian fructification from with bitegmic ovules is related to Ranunculidae. Some minor 
findings are mentioned in со The “spotted layer" of Caytonia is interpreted as inner integ- 
ument. Mescgenous stomata and incipient vessel members are revealed in bennettites. Possible links 
of proangiospermous Caytonia, певане, апа со with angiosperms аге indicated. 


I have reported on proangiosperms—a rather 
loose group, comprisi ng Caytonia, Leptostrobus, 
and Крон which, together with some 
other plants, such as bennettites, formally not 
included in the group, provided a "character 
pool” for arising angiosperms (Krassilov, 1977a). 
Since then another proangiosperm plant, sup- 
Posedly of bennettitalean affinity, was found in 

isa, е province. Early Cretaceous 
angiosperms and angiosperm-like plants were 


studied (Vakhrameev & Krassilov, 1979). Some 
а data on Hirmerella, Caytonia, and bennet- 
d des also, I believe, relevant to the problem 

B&osperm ancestry. These results and their 
implications are discussed below 


OVULIFEROUS SCALES” OF HIRMERELLA 


This name is applied to ovulate cones of a 


шы oo features (columellate ectexine, 
mom be with equatorial har- 
в €gathus of Nymphaea. Ovulate organs of 
genus also have angiosperm-like features. 


(courtesy of Dr. Maria Reymanowna, Krakow 
and Dr. Maya Doludenko, Mosco Ре 
is that there 
per ce closely packed and filling : a nel. h 
both British and Polish fruits there were sides 
of 
1). If the ovules were merely embedded in | the 

“scales” there would be no internal cuticle lining 
the locule 

A lot of pollen grains stick to the papillate 

surface of the “scales,” but none have been ob- 
served within the nucelli, which had inconspic- 
uous beaks. 


lly differs from all known co- 


nifers and is perhaps closer to Ephedra, which 
sometimes show two ovules per cupule (Mehra, 
1950). Based on its fruit-like diaspores, Hirme- 
rella can be included in proangiosperms. It may 
represent an extinct order of gnetophytes. 


BAISIAN ACHENES 


One of the most fascinating discoveries was 
made recently in the Lake Baikal province. Low- 
er Cretaceous paper shales and marls cropping 
out along the Vitim River near Baisa camp are 
well known as the richest Mesozoic locality of 
terrestrial иси апа diverse lacustrine fauna. 
of trivial Ear- 
iy: ‘Cretaceous Siberian aspect (ginkgoaleans, 
czekanowskias, pinaceous conifers). However, a 
the Paleon- 
tological 1 Institute, Moscow, were lucky to find a 
single angiosperm-like leaf described by Vakh- 


жыш a AAN 
1 : 
Institute of Biology and Pedology, 690022, Vladivostok-22 U.S.S.R. 


ANN. MISSOURI Bor. GARD. 71: 577-592. 1984. 


578 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Vo.. 71 


GURE l. Hirmerella sp., med Liassic of Odrovaz (Poland). —A. Two overlapping асы ae » 5x, -D. 
liferous scale" shown in — B. Upper portion of a nucellus, 500 x.—C. “Ovuliferous les of the locul 
Scanning electron micrograph of | pollen grains on the cuticle of a “scale,” 500 x.—E. Joint cutic 
and integument, 170x.—F. Cuticle of the locule, 170 x 


Я Dicotyle 
rameev (in Vakhrameev & Kotova, 1977) as Di- gists with hopes of collecting Re concen- 
cotylophyllum pusillum phyllum. We failed to find it but ins "p 
In 


te 
979, I visited this locality together with trated on abundant enigmatic йл “hairs.” 
Dr. V. V. Zherikhin and other paleoentomolo- previously t 


| 


| 


| 


1984] KRASSILOV—ORIGIN OF ANGIOSPERMY 


m 2. Achene-like fossils from the Lower Cretaceous of 
(oti epidermal cells, “coronas,” and long hairs from the гесе 
m), 1 8 X 


were shown to be achene-like diaspores, 
"Shaped, with a persistent receptacle bearing 
trusses of unicellular hairs (Fig. 2). Detached 
"eptacles also occur abundantly on the bedding 


Baisa, Lake Baikal province. Two achenes 
ptacles (top), 12x, and a detached receptacle 


planes (Fig. 2). The external coat (*cupule") shows 
large tubular epidermal cells arranged in longi- 
tudinal rows. These are clearly marked on 
impressions and can be seen under low magni- 
fication. The apical portion ("corona") is de- 
marcated by a transverse groove and pitted. The 


580 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Vo.. 71 


FIGURE 3. Achene-like рат Ap the Lower eei of Baisa, Lake Baikal province. — А, B. Split e 
5 iil ovules, 12x.—C. ule m the achene shown in A, 15x.—D. Scanning electron microgra S 
receptacle Eco short su aii 1405 х gir mars electron micrograph of nucellus with pollen n grains a 
top, 60 x.—F. Scanning electron micrograph of epidermal cells, 400 x. 
receptacles show laminar appendages that appear A few longitudinally split а have an 1" 
mostly as short rounded lobes. In a favorably пег cavity with a single ovule em е: 
preserved specimen there аге six small lanceolate — locule. The ovules are elliptical with an 
bracts at the base (Fig. 3D). Hairs arise in fas- — spicuous micropyle. d 
cicles from these appendages. Externally, the cupules are scarcely cutinize 


1984] KRASSILOV —ORIGIN OF ANGIOSPERMY 581 


electron micro; 


graph of pollen grains on the top of a nucellus, 


FIGURE 4, Achene-like fossils from the Lower Cretaceous of Baisa, Lake Baikal province.—A. Scanning 


same as in Figure ЗЕ, 400 x.— B. Top pollen grain 
. о Дане] niacretae. || + ; 0, 


showing sulcus, 600 x.—C 


с ан I was unable to obtain an outer 
ya di € large-celled epidermis is underlain 
tissue = fibrous layer and much thicker stone 
erated f ragments of vascular bundles were mac- 

Tom the cupule wall. They consist of tra- 


cheids with spiral thickenings. The ovules yield- 
ed two joint integumental cuticles and a nucellus 
that is thicker at the base but thin and unfortu- 
nately ill-preserved above. However, in one of 
the nucelli a cluster of pollen grains was observed 


582 


ave 

| 1 Ју t. и 
D 1 ү 

н, Ў 


Wa 
ү ГАРИ 
/ 


FIGURE 5. Suggested relationships of the Baisian 
achenes. — A. Bennettitalean flower with hairy bracts, 
ovules, and interseminal scales. — B. Bennettitalean in- 
terseminal scales fused around the ovule as in Ben- 
netticarpus crossospermum Harris. —C. Baisian 
achene. — D. Cyperaceous achene (Eleocharis sp.). 


at the apex (Fig. 4). They are elliptical, up to 140 
um long, monosulcate, smooth, alveolar, show- 


ino clavate 1 
v. ۷ 


chamber exudate?). 

Superficially, these fossils look h like some 
cyperaceous achenes, especially those with abun- 
dant hypogynous hairs or bristles as in Eriopho- 
rum or Carpha (they might have been mistaken 
for such if met in geologically younger sedi- 
ments). In Eriophorum vaginatum L., fascicles 
of bristles on a conical receptacle represent re- 
duced perianth lobes. The shape and dimensions 
of the Baisian and Eriop/ } } 
alike as well as the large tabular epidermal cells 

Fig. 5). 

The outer coat of a cyperaceous achene is cur- 
rently interpreted as either a prophyll-derived 
m 


Baisian achenes might have similar origin. How- 
ever, On closer inspection they turned out to be 
neither cyperaceous nor even fully angiosper- 
mous because pollen grains occurred on the nu- 
cellus. 

Among the Mesozoic plants, only bennettites 
stand for comparison. Their “flowers” have sim- 


lutionary mode in bennettites (Stidd, 1980). It is 
conceivable that the bracts were transformed into 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


vestigial outgrowths bearing fascicles of hairs. 
Similarly, numerous ovules might have been re- 
duced to one while interseminal scales coalesced 
around it in a kind of a cupule. The clearly de- 
marcated apical portions of the Baisian cupules 
are analogous to a “corona” of Williamsonia 
formed of the tips of interseminal scales. The 
nucelli and pollen grains are rather of bennetti- 
talean aspect. 

If these considerations were valid, then the 
Baisian plant could be seen as a development of 
certain bennettites toward proangiospermy. 
Whether they progressed further in the direction 
of monocots, as the similarity to cyperaceous 
achenes suggests, is an open question. An answer 


to this problem depends on further paleobotan- | 
ical discoveries, as well as on new approaches [0 


the cyperacean morphology which, after so many 
efforts along conventional lines, is still in a mess. 


ANGIOSPERMS AND ANGIOSPERM-LIKE FOSSILS 
FROM THE LOWER CRETACEOUS OF MONGOLIA 


Lower Cretaceous lacustrine paper shales arè 
widespread in Central Mongolia, Mongolian Al- 
tai, and Gobi. They were extensively studied by 
the Soviet-Mongolian paleontological expedi- 
tion. On the evidence of fossil ostracodes, 1" 
sects, fishes, and recently discovered abundant 
plant remains, these beds were assigned mostly 
to the Neocomian-Aptian. Fossil plant assem- 
blages are dominated by conifers 


giosperm 


larger fruit (Fig. 6B) has a spherical endocarp 


(Вгасћурћу“ , 


— ———— 


| 


) 


x ; ta 
about 6 mm in diameter divided by a thick ey | 


into two locules. The endocarp is embra de: 
a symmetrical membranaceous wing with pe 
ulate venation and is crowned by а Very > . 
style bearing a funnel-shaped stigma 
son with superficially similar winged leat 
as Eucommia, Pterocaryopsis, Ptelea, РЇ Ё: 
carpum, Zygophyllum, Dadonaea, Kon Өй 
Abronia, Dipteronia, showed that this foss 
i i any of the known 
or families. There are, however, some 
resemblance with Ptelea and Еисоттіа P? 
ed that in the hypothetical ancestral 5 
the latter both locules were equally ? 
The smaller fruit (Fig. 6A) is elliptical, 


long, having a short stalk and sessile stigm4 


| 


. Compa | 
fruits, suh — 


| 


| 
t 


3 


1984] KRASSILOV—ORIGIN OF ANGIOSPERMY 583 


toe f Angiosperm fruits and angiosperm-like fossils он the Lower Cretaceous of a SE 

sh 2 showing a smooth wing, 10x.— B. Larger fruit wing a а а m 5x.—C. Sam 
Spike of E: le bearing гн gute 10x.—D. Grass-like iaf showing li — —E. Potamogeton- like 
socie of nutlets, 3 Sparganium ae Grass- - leaf showing 
d, 3x 


„Арата ТАТЕ 


"uricle (left side of a sheath), х HL. Terminal inflorescence (7) of three spikes ase 


= 


584 


wing is narrow, smooth, and encircles the en- 


obscure but they widen the range of pre-Albian 
fruit diversity. 

Another locality, Manlai in eastern Gobi, 
yielded fragments of articulate stems with 
sheathing leaves (Fig. 6D). The leaf blade is ses- 
sile, flat, having thick parallel veins and longi- 
tudinal striation. At the sheath-blade junction 


They are срив to auricules of bambusoid 
grasses. Th leaf 

is rather like i in Ancistrachne and related south- 
ern hemisphere grasses. 

There are also several kinds of what appear to 
be reproductive structures (Fig. 6F-H); (1) асуте 
of three stalked spikes or spikelets, terminal on 
a stem, with three hair-like appendages (inflo- 
rescence bracts?) at the base, superficially resem- 
bling inflorescences of Bulbostylis and some oth- 
er Cyperaceae; (2) Potamogeton-like spike with 
five whorls of three nutlets each; and (3) Spar- 
ganium-like fructification consisting of an axis 
bearing two sessile heads of about ten mucronate 
nutlets each, the lower one apparently in the axil 
of a leaf-like bract. 

These fossils are approximately contempora- 
neous with the Baisian achenes. They may in- 
dicate initial diversification of marshy herba- 
ceous monocotyledons or plants of the Baisian 
evolutionary level. Because they are not suitably 
preserved for detailed study, it is unsafe to draw 
any definite conclusions. 


MIDDLE ALBIAN CASPIOCARPUS 


Caspiocarpus from the western Kazakhstan is 
hitherto the most ancient structurally preserved 
fructification that proves the existence of true 
angiosperms in the late Early Cretaceous (Vakh- 
rameev & Krassilov, 1979). Its age is determined 
rather rigorously as middle Albian (Vakhra- 
meev, 1952). The fossil axis bearing two leaves 
and two paniculate reproductive structures was 
originally assigned to Cissites cf. parvifolius 
(Font.) Bell, the name being applied to the leaves 
(Vakhrameev, 1952). The details of panicles re- 
mained unknown until, in 1977, I was fortunate 
to obtain a few transfer and cuticular prepara- 
tions revealing some essential characters. The 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


main axis is flat, grooved, 2 mm wide, branching 
at an acute angle. Each of the two branches bears 
a terminal panicle. One of them (the left one in 
Fig. 7A) is placed 5 mm above the leaf node. 
The panicles were shown to consist of two larger 
basal racemes and a number of much shorter 
crowded racemes above them. The latter are 
about 4 mm long bearing up to ten (mostly four 
or five), spirally arranged, overlapping follicles 
that are better seen in the loose apical portion of 
the right panicle (Fig. 7C). The follicles are el- 
liptical, to 1 mm long, shortly beaked, attached 
by a short stalk and mostly opened. 

It is seen on the casts and cleared preparations 
that they opened along the ventral suture and, 
in the upper quarter, also along the dorsal one 
(Fig. 8A). Their valves а are mostly spreading at at 
about 60° 
pressure. No vestiges of stamens or perianths 
were found. The rounded pits on the casts of the 
follicles seen under SEM are hair bases or (less 
фора Moman (Fig. QU 


but аюы па“ 


iles. In one 

oft iiim i found three ovules; two in one half of 

the follicle, one above the other (Fig. 8B), anda 
d ( 8C)j )J d to them. The ovules 

are about 0.8 mm by 0.5 mm, pointed, and 
broadly truncate at the hilar end. Two integu- 

ments are discernable, the inner one wedging out 


them 


consists of two layers of tabular cells. Short uni- 
cellular hairs are scattered in the upper portion 
(Fig. 8D). The inner integument shows three lay- 
ers of narrow spindle-shaped cells in the 
region. Some ovules are divided longi pean 
into two halves (Fig. 8C). My suggestion on 


feature represented a raphe in the cleared 0 


dehet | 
was justly criticized by Retallack and Dilchet | 


(1981), but at present I have no better explana 
tion. ES 
The taxonomic position of Caspiocarpus uM 
certain. Because the seeds were retain 
dehiscent carpels, one can assume that they 


стя by their funicles—a т } 


пип 


vet- 
Mu Berberidaceae, the follicles open at both 
tral and dorsal sutures (Tamura, 1963). bi 
The ovules are also of ranunculoid aspect, 


"e | 


} 
| 
{ 
| 


| 


| 
| 


i 


- wa 


1984] KRASSILOV—ORIGIN OF ANGIOSPERMY 585 


y iac ۷ 
E 


ions "vdd Caspiocarpus from the middle Albian of Kazakhstan.— A. Shoot ipw two leaves (light impres- 
win, o nspicuous on light matrix) and two panicles (1 = a leaf node), 2x.—B, C. Apex of the right panicle 

ча - гер loosely wine follicles, 25 and 12 x.— D, Е. Parts of the right panicle зана short lateral racemes 
ollicles, 10 x —F. Scanning electron micrograph of pits (hair bases or stomata?) on the follicle, 2,000 x. 


nash With fairly thin integuments. In most Ra- drastis, Paeonia, and some other genera within 

Dculaceae the outer integument is typically Ranunculidae. Extreme reduction of the outer 
an the inner one, but the reverse re- integument is peculiar for Ranunculus and es- 
чы Occur in n Berberidaceae, Aquilegia, Hy- pecially for Circaeaster where it is only two cells 


ш 
la th 


586 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


FIGURE 8. Caspiocarpus from the middle Albian of Kazakhstan.— A. Small cleared follicle, 


150 x.—B. Two ovules, 100 x 
wedging out of the inner integum 


. Third ovule from the same follicle, 100 x. eris of the same 0 
ent and one of the integumental hairs, 1 


[Vor. 71 


rsal vit 
а 


M " J]-—— —— 


1984] 


thick. Integumentary hairs are characteristic of 
Helleborus. Branching racemose inflorescences 
are known in Aconitum and Cimicifuga, but 
Thalictrum has panicles. Leaves of Cissites mor- 
photype occur in such extant Ranunculaceae as 
Delphinium, Aconitum, and Ranunculus. I be- 
lieve, therefore, that Caspiocarpus was most 
closely related to Ranunculidae, though possibly 
not assignable to any existing family. 


DISCUSSION 


Hickey and Doyle (1977) have stated that “‘the 
identification of any Jurassic plants as proan- 
giosperms (as attempted by Krassilov, 1973, 
1975) will probably be a difficult task requiring 
a detailed comparative analysis of all organs as 
rigorous as that which was required to establish 
the relationship between cordaites and conifers 
(Florin, 1971) or the role of Devonian Aneuro- 
phytales and Archaeopteridales as progymno- 


which did 4 


his conclusions from his studies of the seed scale 
complexe 1 4 2s 4.5 o. 


tween cordaites and lebachiacean plants (prob- 
ably a specialized line of cordaites with reduced 
leaves), but which left the problem of conifer 
ancestry unsolved. Evidence that progymno- 
sperms are related to gymnosperms comes most- 
ly fr от wood anatomy. 

Similarly, the proangiosperms, as I understand 
them, share with true angiosperms a few char- 
Pd of critical importance, and among them 
pes angiospermy itself. They have a kind ofovary 
that is supposedly monocarpellate involuted 
\Caytonia, Dirhopalostachys) or bicarpellate with 
ks Carpels (Leptostrobus). The question is 

nether any kind of angiospermous ovary could 
arise from these structures or whether they rep- 
irs S "blind alleys" of angiospermization 
f € mainstream progenitors are still to be 
ound, 
we (1931) has suggested derivation of a 

unculoid follicle from two joined caytoni- 
а С fused to the rachis. His ideas were 

: y leading contemporaneous morphol- 
торош use in Caytonia the ovules are orthot- 
—— supposedly unitegmic whereas in 
tegmi Old angiosperms they are mostly bi- 
Cult < and anatropous. To overcome the diffi- 

Y Of a de novo formation of the second in- 
deriv €nt, Gaussen (1946) has postulated its 
ation from the caytonialean cupule while 


KRASSILOV —ORIGIN OF ANGIOSPERMY 


587 


the rachis expanded into a carpel. Stebbins (1974) 
and Doyle (1978) have supported this suggestion 
but Retallack and Dilcher (1981) found it intu- 
itively unattractive. In their opinion, the outer 
integument might have been derived from a glos- 
sopteridalean leaf bearing an epiphyllous ovulate 
structure. But in the case of Caytonia there is no 
need of going to those lengths because its ovules 
are, in fact, bitegmic. 

I suggested (Krassilov, 1970) that the enig- 
matic “spotted layer" of Caytonia (supposedly 
an aleurone layer) might be a vestigious inner 
integument. Recently I studied a few Caytonia 
ovules from Yorkshire kindly sent to me by T. 
M. Harri d nothi tiall 


4 


s. I found ср, 


some fine external features of the micropyle (Fig. 
9). I also reaffirmed my suspicions about the 
“spotted layer." The aleurone layer is a layer of 
endosperm. It is situated inside, not outside the 


two layers of cells and it is cutinized. Its small 
spots and larger patches of dark matter look not 
like aleurone grains but rather like metamor- 
phosed oil cells and blocks of tannin filling inner 
integuments of angiosperm seeds. Harris (1964) 
noticed that the "spotted layer" never extended 
into the micropyle. Thus, the micropyle was 
formed by the outer integument only. I discussed 
the problem of bitegmy elsewhere (Krassilov, 
1970). Double integuments can be traced back 
to early Carboniferous Eurystoma angulare 
(Camp & Hubbard, 1963). In many Paleozoic 
seeds the inner integument had been lost in fu- 
sion with the nucellus (hence, vascularized nu- 
celli), but it was restored in gnetalean plants, 
some bennettites (Vardekloeftia, Harris, 1932), 
and Caytonia. About half of the dicotyledons 
and three quarters of monocotyledons have bi- 
tegmic ovules that are consentaneously recog- 
nized as the primitive condition. However, in 
the families that appeared early in the fossil rec- 
ord, such as Ranunculaceae, Menispermaceae, 
Piperaceae, Fabaceae, Rosaceae, and Poaceae, 
there are both uni- and bitegmic ovules. Such 
flexibility might be due to frequent atavistic mu- 
tations. Even vascularized nucelli have been re- 
stored in some angiosperm lineages (e.g., Thy- 
meliaceae). Tritegmic forms, as in Sarcandra, 
can also be expected among early angiosperms. 

It was shown (Krassilov, 1978) that the 
“mouth” of Caytonia can be shifted from its 
position at the base of the pedicel. One can imag- 
ine that a continuation of this process (due to 


588 


FIGURE 9. Caytonia sewardii Thomas from the Jurassic of Yorkshire. Scanning electron microgra 
ovules, 100 x, and scanning electron micrograph of details of the micropyle of the left ovule, 1, 200 and 


adaptation to some pollination vector?) could 
bring the "mouth" into apical position, at the to pseudoanatropous position by 
same time affecting the position of ovules. The ij 

resultant urn-shaped ovary, styleless, with sessile 
stigma, would not be unlike those of a vesselless 
angiosperm, Sarcandra irvingbailleyi Swamy (Fig. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


11). In this species, the ovules are bitegmic (oc- (Vasil & Johri, 1964). 


casionally tritegmic), orthotropo 


1977b) occur as an atavistic or recurren 
in Annona, Lilium, and some other ang! 


(Мог. 71 


ph of two 
4,000* " 


us but brought 
the curvature 


osperms 


| 


1984] KRASSILOV—ORIGIN OF ANGIOSPERMY 589 


FIGURE 10. Caytonia sewardii Thomas from the J urassic sd fona: — А. Nucellus of an ovule shown in 
9, t, wi remnants of a “spotted layer," ou ent is removed completely, 70 x.— B. 


right, 
o Potted layer" of another ovule, 150x.—C. Cells of the осн ec " 300 x.—D. “Spotted layer" wedging 
ut below the micropyle, 150 x 


590 


FiGURE 11. Suggested derivation of a Sarcandra- 
like carp from Caytonia-like cupule by the shifting 
of am 


This simple mode of transforming the cayto- 
nialean cupule into a carpel is partially supported 
by the evidence of the shifted “mouth” in the 
mid-Jurassic Caytonia sewardii, but final proof 
or repudiation should come from eb оны 
of the late Jurassic and Cretaceous speci 

Dirhopalostachys is a raceme of paired Follicle 
like one-seeded beaked cupules having a ventral 
suture (Krassilov, 1975). The pairing of cupules 
reminds one of the Hamamelidaceae — one of the 


FIGURE rpels 
1961) and Dies (after Krassilov, 1975). 


of Kingdonia, left (after Foster, 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


FIGU 
ed (top) and normal stom: 
iopteris ет аи 800 and 1,600 x. 


URE 13. Scanning electron micrograph 0 of abo 
ata of a benn 


bort- 
ettite Nilsson- 


: m the 
most ancient angiosperm families. However, 


leaves of Dirhopalostachys. A 
the apetalous flower of Kingdonia arose 

androgynous reproductive struct 
rmous plan 


certainly deserves further study. 
essential features of Dirhopalostachys ап : 
nia, and first of all the mode of pollinatio , 
still to be learned. 


are 


~ 


FIGURE 14. Vessel-like members from the midrib 
a a bemetitalean заана pinna showing їег- 
al perforations, 300 and 600 


Paleobotanical discoveries have substantiated 
At. 43 theoretically concpivable райгкауз 
t con- 


For In the course of my studies of the 
ate Jurassic Leptostrobus (bivalvate capsules 
with papillate stigmatic fringes), I suggested that 
е so-called "conduplicate" carpel in Wintera- 
ceae is derivable from the leptostrobalean pro- 
totype and actually consists of two open carpels 
fused by their margins (Krassilov, 1970). The 
conduplicate nature of the winteraceous carpel 
Was questioned by Tucker and Gifford (1964) 
and recently Leroy (1977) has shown that, at least 
in some winteraceous genera, the ovary is bicar- 
Pellate, with both ventral and dorsal grooves cor- 
WE to the contacts of open rua as it 


B 
aisian achenes to ovulate structures of bennet- 


scales, vaguely preconceived by end (1946). 
Evolutionary potentials of bennettites look not 
ntly other points of 

cam and angiosperms 
e to light. Florin (1933) ed that ben- 
en stomata were mesogenous (“‘synde- 
~ Pd )as in many angiosperms, but his views 
ISputed because he deduced from mature 
Me apparatuses, which can be ontogenet- 
Y mesogenous, perigenous, or mesoperige- 


KRASSILOV —ORIGIN OF ANGIOSPERMY 


591 


nous. Recently, I described a few aborted sto- 
(Fig. 13) that confirm mesogenous 


were short vessel-like members showing termi- 
nal perforations (Fig. 14). 

Thus, bennettites were capable of developing 
vessels in the primary xylem, reticulate venation 
( Dictyozamites), paracytic stomata, bisexual 
flowers, and achene-like fruits. It seems unjust 
to rule them out as possible ancestors of angio- 
sperms. There are also indications that angio- 
sperms first appeared in cycadophyte shrublands 
dominated by various bennettites and then pen- 
etrated coniferous forests (Krassilov, 1973). 


CONCLUSION 


Not long ago, the origin of angiosperms seemed 
mysterious because there were no acceptable 
candidates for ancestors. Now the problem is 
that there are too many of them. 

Traditionalists often pose as defenders of re- 
spectable theories (such as monophyletic origin 

of angiosperms) against irresponsible specula- 
tions. Actually, they defend old irresponsible 
speculations from the new ones. In the case of 
angiosperm ancestry, however, new Speculations 
even seem somewhat As more 
lineages approaching angiospermy emerge from 
the fossil record, the polyphyletic hypothesis ap- 
pears more plausible. It is significant "m that 
most proangiosperm rec ar ound 
the supposed Asiatic center of o origin. 

Further progress depends on detailed studies 
of the Late Jurassic and early Cretaceous Cay- 
tonia, Dirhopalostachys, bennettites, czekanow- 

skialean, and Classopollis-producing plants as 
well as the middle Cretaceous angiosperms. 


LITERATURE CITED 


Camp, W. H. & M. M. HuBBARD. 1963. On origin of 
the ovule and cupule in Lyginopterid pterido- 
ad 5-768. 


CANRIGHT, ЈЕ mparative morphology 
and relationships т the нее. 3. Carpels. 
Amer. J. Bot. 47: 145-155. 

Юоү1є, J. А. 1978. Oran of angiosperms. Annual 

1. Syst. 9: 365- 

FAGERLIND, F. 1946. Strobilus und Bliite von Gne- 
tum und die Móglichkeit, aus ihrer Struktur den 

Риђи der Angiospermen zu deuten. Ark. Bot. 

ЗЗА: 1- 


592 


FLORIN, К. 1933. Studien über die Cycadales des Me- 
sozoikums nebst Erórterungen über die Spaltóff- 
nungsapparate der Bennettitales. Kongl. Svenska 
Vetenskapsakad. Handl. 12: 1-134. 

. Evolution in cordaites and conifers. 

cta 85-388. 

Foster, A. S. 1961. The floral morphology and re- 

lationships of Kingdonia uniflora. J. Arnold Ar- 

bor. 42: 397-410. 


. Lab. Forest. Toulouse, 2, Etud. 

1: 1-26. 

932. The fossil flora of Scoresby 
Sound, East Greenland, 2. Meddel. Grenland 85: 

1-112. 

—— —. 1964. The Yorkshire igs dnd 2. British 
Museum (Natural History), Lo 

The Yorkshire Jurassic? Flora 5. British‏ ,س 
Museum (Natural History), Lo‏ 

HICKEY, (s J. &J B Dovrr. 1977. "Fari Cretaceous 

ti Bot. Rev 


(Lancaster) 43: 2-1 04. 
KrassiLov, V. A. 1970. On the origin and homology 

of — organs of Anthophyta. Zurn. Ob- 
l. [J. Gen. Biol.] 31: 679-689. (In Rus- 
— 197 3. Mesozoic plants and the problem of 
angiosperm ancestry. Lethaia 6: 163-178. 

1975. Dirhopalostachyaceae—a_ new family 


of angiosperm ancestry. Palaeontographica, Abt. 
B, rese 153b: 100-110. 
1977a. The origin of angiosperms. Bot. Rev. 
(Lancaster 43: тш —176. 
tributions to the knowledge of 
the на RE Palaeobot. Palynol. 24: 155- 
178. 


1978. Bennettitalean stomata. Palaeobota- 
nist 25: 179-184. 
1 Early oe flora of Mongolia. 
Palaeontographica 181B: 1-43. 
Leroy, J. F. 71. А idee with ope 
rpels in Winteraceae (Magnoliales) evolution- 
es implications. Science 196: 977 
LONG, А. G. 1966. Some Lower teni us fruc- 
tifications from Berwickshire, together with a the- 
oretical реко of the evolution of ovules, cu- 
carpeis 


pules rans. Roy. Soc. Edinburgh 66: 
345-375. 
MEHRA, P. N. 1950. Occurrence of hermaphrodite 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Уог. 71 


flowers and the development. of female e 
phyte in 
Bot. (London) n.s. 14: 165-180. 

RETALLACK, G. & D. L. DILCHER. 1981. Arguments 
for a glossopterid ancestry of angiosperms. Paleo- 
biology 7: 54-67. 

SCHWEITZER, Н. -Ј. 1977. Die raéto—jurassischen Flo- 
ren des Iran und Afghanis tans. 4. Die rátische 
Zwitterblüte Zr. spec und 
ihre Bedeutung fiir die Phylogenie der Angiosper- 
men. Palaeontographica, Abt. B, Palüophytol. 
161b: 98-145. 

SrEBBINS, G. L. 1974. Flowering Plants: Evolution 
deis Species Level. Harvard Univ. 


S uno. M. 1980. The neotenous origin of the pollen 
organ of the gymnosperm Cycadeoidea and im- 
plications for origin of higher taxa. Paleobiology 
6: 161-167. 
TAMURA, M. 
e: of the Ranunculaceae. des 
1. Osaka Univ. 11: 115-1 
TuS H.H. 1931. The early ош of the an- 
giosperms. Ann. Bot. (London) 45: 647-672. 
кы, S. С. & E. M. Girrorp. 1964. Carpel vas- 
tion of Drimys lanceolata. Phytomor- 
es 14: 197-203. 
AKHRAMEEV, V. A. 1952. Stratigraphy and fossil 
flora from the Cretaceous deposits of western Ka- 
zakhstan. Regional Stratigraphy 1: 1-340. (In Rus- 


1963. Morphology, ecology and phy- 
Rep. 5. Coll. М. 


sian). 
& I. Z. Korova. 1977. Ancient sonm 
and associated plants from the Lower Creta 


of Transbaikalie. Paleontol. Zurn. 1977(4): ga 
6 nR 
£ ^ Gee ce HS Reprod 
aue of angiosperms from the Albian 0 of Ka- 
zakhstan. Ри. Zürn. n 121-128. (In 
Russian). 

VasiL, J. К. & M. M. Jonri. 1964. The dM 


bryology of a vesselless dicotyledon— Sara f 
irvingbaileyi Swamy, and systematic per 
e Chloranthaceae. Phytomorphology ! 
441. 
Vink, W. 1978. The Winteraceae of the Old e 
3. Notes on the ovary of Takhtajania. Blum 
521-525. 


| 


— — 


MESOSPERM PALYNOLOGIC EVIDENCE AND 
ANCESTORS OF ANGIOSPERMS 


NORMAN Е. HUGHES! 


ABSTRACT 


Late D and mid- Cretaceous appear to have been times of evolutionary innovations of : seed 


plant po 


г 


the lat Jurassic This incongruity sugge ests 


that oa of pollination «сареи of Mesozoic seed plants is far from complete; some plants 
ibe h 


have been descri with stigmatic gti 


and investigation of their morphological intermediate 


position needs much fuller attention. The 


difficult because of the 


suggested that all Mesozoic seed plants should be placed in a Mesosperm Grou 
ould be used for fossil plant remains before E былк unless at least 
rgans in the same beds 


no living angiosperm taxon s 
two separately preserved plan 


arch for 
lack of a у definition of an angiosperm in in Cretaceous. time. It 


p of fossils and oe 
le 


can be shown to ssociated in supporting 
ils. 


that taxon. All Mesozoic seed pee taxa should be based solely on evidence pum foss 


In this short paper my object is to attempt to 
clear some of the obscuring fog around the prob- 
lem of angiosperm ancestors. Hitherto, on the 
basis of the current wies. of the terms 
'gymnosperm' and ‘angiosperm,’ I have sup- 
ported (Hughes, 1976) the view that certain Cre- 
taceous Barremian pollen represented the earli- 
est angiosperms and that any ancestor should 
Properly be sought among gymnosperms in ear- 
lier Cretaceous rocks. Progress, however, has been 
relatively slow because only a small proportion 
of those interested in the problem work with 
newly discovered fossil evidence. At the Ninth 
Botanical Congress (Montreal 1959), the struggle 
for understanding against obscure diversion (cf. 
Scott et al., 1960; Hughes, 1961) centered on 
Supposed CAMAS PER upland plants; more re- 
cently diversions take the form of lightly docu- 
di. curiosities of comparative morphology 
1979: (e.g., Klaus, 

Cornet, 1980). 

d this age of advanced techniques of study of 
i available abundance of microfossils, a solu- 
on to the whole problem actually seems to be 

attainable b e by] 
ords of fossils alone. The dangers to such con- 
tinuous Progress by hard work appear to lie in 
4 Jeppe resulting from ill-defined 
terms and in e impatience commonly ex- 
through unnecessary neobotanical as- 
Sociation theories. After examining briefly the 
иту Progress with fossil gymnosperms, I shall 
ЧТ to definitions of terms and to those classi- 


af anand rec 


So ЗМИВ 


fication procedures that appear to obstruct un- 
derstanding 


LATE TRIASSIC POLLEN INNOVATIONS 


Schulz (1967) described pollen of Clavatipol- 
lenites type from the late Triassic of Poland. Klaus 
(197 ofthe tri-saccate 
Dacrycarpites europaeus Madler (1964) to in- 
clude various angiosperm aperture and exine 
characters that he compared with the pollen of 
Schizandra and other living plants; but these 
‘prae-angiospermid’ characters were observed on 
‘occasional aberrant’ grains. Cornet (1980) re- 
ferred to a wide range of late Triassic angiosper- 
mid apertures but the information is provided 
only in unillustrated abstract form and is thus 
difficult to use. If the material referred to by these 
authors were subjected to rigorous recording with 
adequate specimen numbers and statistical as- 

sistance, it seems ыан that some new infor- 
mation would em 

In addition, on јан is the time of origin 
of basti рита, and рн 

г; Scot 


allo 
(1 960) ) compared E quisetosporites with E arit 
In comparison, therefore, with the periods of 
geologic time just before and just after, these late 
Triassic floras appeared to have been involved 
in unusual innovations of pollen characters (Text- 
fig. 1 

Es period of time also produced the mega- 
fossil Sanmiguelia claimed by Cornet (pers. 


' Department of Earth Sciences, Downing Street, Cambridge СВ2 3EQ, England, United Kingdom. 


ANN. MISSOURI Bor. GARD. 71: 593-598. 1984. 


594 ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL. 71 
Stratigraphic * Atlantic-area' Seed Plant Events 
Scale Megafloras Pollen Flower Fruit Leaf Wood 
Cenomanian x F5 W2 
pa Potomac 35° Cr N 12 WI? 
110 
Barremian P2 Frl 
Hauterivian 
Valanginian 
Berriasian Wealden 40° Cr N 
135+ 
Morrison 40° Jr N F4 
Jurassic 
Mid 
Jurassic Yorkshire 40° Jr N F3 
Early 
Jurassic 
Scania 40° Jr N 
195+ F2 
Rhaetian East Greenland 45° Tr N PI ГІ 
Norian 
Carnian ЕІ 
TEXT-FIGURE 1. Stratigraphic table of seed plant occurrences and of Atlantic-area floras with аре 
paleolatitudes. P1 = Late Triassic pollen innovations; P2 = tectate columellate monocolpate pollen; РЗ igs 
colpate pollen. F1 = Sturianthus; F2 = Williamsonia, ЕЗ = Williamsoniella; FA = Cycadeoidea; F5 = angi 


spermid inflorescences. Ег1 = 
undisputed vessel-bearing wood 


comm.) to be of angiosperm nature. Just such a 
claim was also made by the original author 
(Brown, 1956) but had subsequently been doubt- 
ed because of the state of preservation (Doyle, 
1973). The new better preserved material could 
change opinions. i 


CRETACEOUS BARREMIAN POLLEN 
INNOVATIONS 


Tectate columellate monosulcate pollen has 
now been recorded (Hughes et al., 1979) from 
the British Wealden strata in a succession of many 
palynologic samples from Berriasian age on- 
wards in which the entry and diversification of 
such pollen within Barremian time is firmly doc- 
umented. Unfortunately, there are no useful 
megafossil plants from the Barremian strata con- 


cerned. 

Pollen of this type has been recorded by Doyle 
and Robbins (1977) and others from the Poto- 
mac Group of eastern North America where there 
are well known megafossils redescribed by Hick- 


noana. 11 = Sanmiguelia; L2 = Potomac leaves. W1 = Aptiana Stopes; W2= 


ey and Doyle (1977). The stratigraphic infor 
mation about these non-marine beds is not ше 
plete, but some of the earliest megafosst® 
probably came from approximately Barremian 
Aptian boundary times (Potomac—Zone 1); theft 
is however an unconformity below and pe 
downward succession into earlier beds. Do 
(1982) records a valuable advance in know «til 
down-dip, but much more information 5 
eeded. i 
With the arrival of ‘angiospermid pollen 2 
is a sudden incoming and diversification of 5 
numbers of ‘Ephedripites’ pollen. This 15 E 
innovation, but the other palynomorphs се 


taceous representative species of Classopollis (t 
Alvin, 1982) and Eucommiidites. 
Although the equivalent beds in 
(Doyle et al., 1977) have produced ^ 
number of types of ‘angiospermid 
that the critical palynomorph zones od 
C-VI are of Barremian rather than of 


~ 


PALYNOLOGIC EVIDENCE 59 5 


AVV JUI1LO 


1984] HUGHES 


tian age. There are, however, zones C-IV and 
below, which comprise a downward succession 
and lack this pollen. 

The striking fact about all these Cretaceous 
successions is that these major Barremian pollen 
innovations are the first since Rhaetian times. 
Palynomorphs from many described Hettangian 
to Hauterivian samples may bear spore inno- 
vations such as Cicatricosisporites in the late Ju- 
rassic and Aequitriradites in the early Cretaceous 
but there are virtually no new or unusual pollen 
types representing the seed plants. 


JURASSIC PLANT MEGAFOSSILS 


The relative lack of new variety in seed plant 
pollen in the Jurassic is contrasted with what is 
known of the major plant groups themselves. 
The Bennettitales diversify in the Jurassic into 
Williamsoniaceae, Wielandiellaceae and, to- 
wards the end of the period, Cycadeoidaceae. 
The Nilssoniales are apparently distinct and di- 
verse throughout; despite attempts using single 
Plant Organs as far back as the Permian to iden- 
tify them with living Cycadales, the situation re- 
mains confused and it seems more helpful to 
confine any discussion of true Cycads to the Ce- 
Фа (cf. Krassilov, 1978: 896). The large group 
di rd c hd including Karkenia and Pseu- 

orellia, became important in late Jurassic and 


id own as Jurassic Coniferales. Entirely 

‚+ BTOUDS such as the Pentoxylales also arose 

In this time interval. 

б, = strong suspicions that some of these 
088115 such as Caytonia and Leptostrobus 


= have evolved far enough to be concerned, but 
уы IS without any apparent response in 
Thi €n morphology before Barremian time. 
S CA aj uii incongruity of evidence between 
emer. megafossils may have some other ex- 
ар п, but it is probably due to our lack of 
reciation of the scope and diversity of the 
“sozoic gymnosperms. One of the main causes 


of this lack is the continued fitting of all fossil 
plant evidence of this age into a neobotanical 
hierarchical classification that is inappropriate 
and irrelevant but is almost always used by cus- 
tom; the continuation of this procedure perhaps 
represents the biggest outstanding failure of pa- 
leobotany. 

Also, as can be seen in Text-figure 1, the main 
floras, on which most of the interpretations are 


are well documented, but the palynologic evi- 
dence is more fragmentary as yet. 


DEFINITIONS OF MAJOR GROUPS 


The term ‘angiosperm’ is easily and acceptably 
defined in the world of present-day plants on the 
basis of a combination of the fossilizable char- 
acters of the flower, fruit, pollen, leaf, and wood. 
However, in mid-Cretaceous time there is пог- 
mally available, at any one locality, only one 
plant organ such as pollen or fruit or leaf with 
its one set of characters. For example, it is by no 
means certain that the unseen Albian plants pro- 
viding tectate columellate tricolpate pollen also 
possessed reticulate-veined laminate leaves; in 
fact what is known of the order of appearance of 


organs and gg gruity of de- 
velopment. Thus it is questionable whether the 
Barremian tectate monocolpate pollen men- 
tioned above should be included in Angiosper- 
mae; but if it is not so included, then no other 
comparable single organ occurrence can be in- 
cluded either and the question of evolution from 
ancestors becomes unanswerable. Although an 


aivitiaty ME H 
len in Angiospermae can be made, the case will 
remain unsatisfactory because the whole of the 
rest of the Barremian plant concerned could well 


propriate flower, fruit, leaf, or wood has yet been 
found at this stratigraphic level. 

Correspondingly, the term 'gymnosperm,' in 
the Mesozoic, is dependent on antithesis and is 
negative in that it includes any seed plant not 
shown to be an angiosperm. Further, the term 
‘flowering plant’ must now include Bennettitales 
and several other pre-Cretaceous gymnosper- 
mous fossils and so cannot be used in place of 
angiosperm. 

Thus, if the major terms cannot be defined for 
Cretaceous time it is meaningless to nominate 


596 ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL 71 


MESOZOIC SEED PLANTS 


Recommended classification 


Terms for Cenozoic use only 


MESOSPERM GROUP 
Brachyphylls 
Cheirolepidiaceae 
Linearphylls 
*Ginkgoaceae' (temporary use) 
Czekanowskiales 

nnetti 

Nilsoniales 
Са — 


Пи group 

Pentoxylales 

For 

Cretapoll group mp 

Cretaphyll group a idis 

ANGIOSPERMAE 
(Only for those pre-Cenozoic records in which two 
separate organ fossils have been accepted as asso- 
ciated thus confirming th e presence of a formally 
recognized angiosperm taxon.) 


Gymnospermae 


Coniferales 
Ginkgoales 


Cycadales 


Dicotyledones (Magnoliopsida) 


Monocotyledones (Liliopsida) 
Magnoliales 


b 
TExT-FIGURE 2. Scheme of classification of elnar seed pens. List of gomme is representative only, • 
се 


includes some formal groups with latinized п 
Th 


15an ی‎ 


e names in the right-hand column are о in this scheme D Mesozoic use. 


аву Cretaceous, J uas or r Irinteie fossil as the 
must ap- 


ply also to the ما‎ pollen. 


PROPOSAL FOR MESOZOIC 
CLASSIFICATION OF SEED PLANTS 


The failure of definitions just mentioned can 
be overcome simply by classifying fossils by those 
features alone that are observed, omitting all ref- 
erence to features that are merely supposed. In 
the present case, there appears to be no dispute 
that the fossils concerned represent seed plants 
and that their g 
Hence, it would be logical to attribute all sichi 
Mesozoic seed plants to a new ‘Mesosperm 
Group, which is a name for a group defined to 
receive all fossil orders or families of Triassic, 
Jurassic, or Cretaceous age displaying any un- 
disputed seed plant characters; the name ‘Me- 
sosperm Group’ is neither latinized nor typified 
so that it remains outside the current neobotan- 
ical hierarchy. Thus, the formal name Gymno- 
spermae would not be defined or required in the 
Mesozoic and would be restricted merely to Re- 
cent and Cenozoic plants; any Paleozoic use could 
be similarly avoided with ease. For the Mesozoic, 


the use of such subordinate subjective units 35 
Coniferales, Cycadales, Ginkgoales, and Aural: 
cariaceae at the family. level could also with вс 
vantage be avoided for the same reason. p 
dicated on Text-figure 2, all currently used “У 
seed plant groups would be included in the 
sosperm Group 


N 
ANGIOSPERM TERMINOLOGY TRANSITIO 
FROM MESOZOIC TO CENOZOIC 
jo- 
Even from the late Cretaceous most ang 


rm of 
spermous plant evidence is still in the fo 


t, pol 
individual records of separated beers p iis 


to formal inclusion in Angios 
be the accepted proof of associ 


n Skarby (1981). Such a criterion co 


ly enhance the value of fully wor 
Cenozoic angiosperm records wo 
nience be free of this restriction. 


sciri on a oii ERR S 


the Me — 


iation of two SP 


As | 
uld for con | 


1984] HUGHES— MESOSPERM PALYNOLOGIC EVIDENCE 597 


REFERENCE TO CRETACEOUS ANGIOSPERMID 
CHARACTERS 


From Barremian and Aptian times onwards 
to the end of the Cretaceous, numerous pollen 
or leaf or other fossils have already been attrib- 


n themse 
directly reflecting the indication of affinity is un- 
desirable because it depends, in virtually every 
case, on the characters of only one organ. 
Clearly, such weakly based records should not 
be accorded the same status as the important 
cases of accepted confirmation mentioned in the 
previous section. The undoubted cumulative 
value of such unconfirmed records can best be 
expressed by neutral group terms such as ‘Cre- 
perm’ and *Cretaphyll" for communication and 
listing purposes (see Text-fig. 2); in construction 
of these words the use of general age and general 
morphology indications seem unlikely to mis- 
lead, but the lack of a latinized ending empha- 
sizes the distinct origin and purpose of such 
names. The extension of that system of names 
to include *Triassopoll ог ‘Juraphyll’ as required, 
appears reasonable. Undoubtedly, some authors 
cerned with ‘Cretaphylls’ and *Cretapolls' may 
consider their single organ evidence to be very 
Strong but the requirement to prove association 
appears to be an appropriate restraint that will 
recall for all users the true state of the record. 
In this connection, the very well-documented 
DU of Muller (1981) appears to present 
€w cases for exemption from this structure, 
4 he limited his Cretaceous ‘acceptances’ 
i = Muller (1981: 6) himself drew atten- 
е problem of lack of information about 


ADVANTAGES OF PROPOSED 
MESOSPERM GROUP SCHEME 


in ; The scheme outlined above and illustrated 
^ a 2 involves minimum disturbance 

addi t practice and literature, and calls for 

“ао ac ~ only in classifying Cretaceous 


2) The status of records is automatically and 
much more clearly indicated. 
LE Altho ugh not directly suggesting a -poly- 


the matter truly open by removing all trace of 
classificatory bias towards a monophyletic the- 
ory that has no base in geological history nearer 
to the Cretaceous than 60 million years. 

4) The idea, developed for many years in his 
writings by the late Professor Tom Harris, that 
paleobotanists are only on the edge of under- 
standing the true biologic range of Mesozoic seed 
plants, will be strengthened. 


CONCLUSIONS 


1) Clearly some more-botanically-based col- 
leagues will tend to be dismissive of this scheme, 
but I ask them to look beyond the apparent icon- 
oclasm. The purpose is to tackle the problem of 
which the solution has eluded both botanists and 
geologists for a very long time, by attempting to 
reorganize the available data, separately from all 
theory, so that entirely new studies may be en- 
couraged. 

2) No solution to the main problem is offered 
here. Such a solution will appear only gradually 
when all available evidence has been encom- 
passed. I am personally convinced that there is 
no abnormal tangible factor dam beyond or- 
dinary paleontological experi 

3) Although perhaps а. анаа data 
handling is unattainable, it appears worthwhile 
in this way to attempt to free a virtually dead- 
locked topic. 


LITERATURE CITED 


ALVIN, A E L. 1982. oe cera biology, struc- 
t logy. Rev. Palaeobot. Palynol. 


37: 71- -98. 

Brown, R. W. 1956. Palm-like pes from the Do- 
lores formation (Triassic), South-western Colo- 
rado. U.S. Geol. Profess. Pap. anil 274-H: 205- 


209. 
CORNET, B. 1980. Tropical Late Triassic monosulca 
and polyaperturate angiospermid pollen and dur 
morphological uaa with associated auric- 
ulate ренин pollen. Abstr. 5th Int. Palynol. 


Conf. 
ПОУТЕ, J. А. 1973. Fossil evidence on early evolution 
of the moncotyledons. Quart. Rev. Biol. 48: 399- 
413. 


Palynology of continental Cretaceo 


——. 1982. 
Test Well, a 


sediments, Crisfield Geothermal 
Maryland. Maryland Geol. Surv. Open File 
Rep. ‘Waste Gate Formation,’ Part 2: 51-87. 


598 


І. J. Hickey 1976. Pollen and leaves from 
n ir 


lution of Angiosperms. Columbia Univ. Press, New 


ork. 

& E. 1. RoBBINs. 1977. Angiosperm pollen 
zonation of the continental Cretaceous of the At- 
ynology 1 


Explor.-Prod. Elf-Aquitaine ы Piat 
FRus, E. M. 198 Upper Cre 
га wers, fruits and seeds fon RE Abate. "3th 
ere Mes ney. 
4 [1 98s]. Preliminary report of Upper 
E ан ngiosperm reproductive organs from 
oi den and their level of organization. Ann. Mis- 
uri Bot. Gard. 71: 403-418. 
Hickev, L. J. &J. A. DOYLE. 1977. Early € Саен 
ol t. Rev 


(Lancaster) 43: 3- 104. 
HUGHES, N. F. Aedes Fossil evidence and angiosperm 
ancestry. Sci. Progr. (London, 1906+) 49: 84-102. 
1976. биен of Angiosperm Origins. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


Cambridge Univ. Press, Cambridge 


— RB E. Dre EWRY, SJE LANG. 1979. Bare. 
513-535. 
Kaus, №. Zur цм 


rA triadischer, ngiospermider Pollena- 
rund Strukturanlagen Beitr. Paláontol. де 
cid yi 135-177. 


KRASSILOV, V. A. 1978. Late Cretaceous бс 


event. d 21: 893-905. 

MULLER, J. 1981. Fossil pollen records of extant an- 
giosperms. Bot. Rev. (Lancaster) 47: 1-1 

SCHULZ, B: 967. _ Sporn ae е Unter 

кеі 
des Germanischen Beckens. Paláontol. yes Ser. 
2, 3: 427-633. 

Scorr, R. A. 1960. Pollen of Ephedra from the Chinle 
formation (Upper Triassic) and the genus Equi- 
setosporites. Micropaleontology 6: 271-276. 

us, tGHOORN & Е. B. LEOPOLD. or 
8 > Ал DEN 


, 


How old are t giosp 
284—299. 
SKARBY, А. 1981.- Upper Cretaceous Normapolles 


anthers, South Sweden. Abstr. 13th Int. Bot. Congr. 
Sydney 


Se ди 


———X 


FLOWERS FROM THE EOCENE OIL-SHALE OF 
MESSEL: A PRELIMINARY REPORT 


FRIEDEMANN SCHAARSCHMIDT! 


ABSTRACT 


A ] а 


nd a male, branched, 


E inflorescence are described from the Middle Eocene oil-shale at Messel near Darmstadt, 
Germ 


OrL-SHALE OF MESSEL 


The oil-shale of Messel, located northeast of 
Darmstadt (Federal Republic of Germany), oc- 
cupies an area of about 1 km in diameter and, 
like a few other small oil-shale deposits in the 
neighborhood, is surrounded by lower Permian 
sediments. All are tectonic trenches that origi- 
nated during sinking of the Rhine valley during 
the early Tertiary 

The Messel oil-shale originally had a thickness 
of more than 150 m before it was mined. During 
mining a large collection of plant and animal 
fossils were assembled. Among the animal fos- 
sils, the vertebrates are of particular significance 
because y ek e very well Persetved, sometimes 
showin ng fi hairs. and feath- 
ers E 1980). The vertebrates are also 
important for the determination ofthe age (Lute- 
tian, Middle Eocene; Tobien, 1968), and the oc- 
currence of crocodiles has been taken as indi- 
cating a tropical to subtropical climate (Berg, 
1966). Like the vertebrates, other fossils such as 
id ава plant leaves are also well preserved, 


oft 5 Es and flora ofthe “Messel lake” through 
further investigations. Because of plans to fill the 

pen cast mine with refuse, the Forschungsin- 
stitut Senckenberg, Frankfurt am Main, and sev- 
eral other institutes have been actively е 
from the locality 


PLANT FOSSILS 
e: Plant a ly leaves, were collected 
ng the mining period. They were first de- 


th scribed by Engelhardt (1922) and deposited in 
M Hessische Landesm useum Darmstadt and in 
e М. барша Senckenberg, Frankfurt 


am Main. A more recent revision of the Lau- 
raceae from the locality is published by Sturm 
(1971). One of the difficulties in preserving the 
Messel fossils is that the oil-shale splits into small 
fragments during drying. Recently however, the 
transfer of animal specimens onto synthetic res- 
ins has allowed larger specimens to be salvaged. 
In the last few years, we have collected a lot of 
new plant material that consists mainly of leaves; 
but also fruits as well as five flowers have been 
collected. Plant remains are not distributed ho- 
mogeneously in the oil-shale, but there is no area 
in the mine where a special leaf layer can be 
found. The leaves occur singly and scattered 
throughout the sediment and, due to their rarity, 
we have collected only about 3,000 over the last 
seven years. During this period several new tech- 
niques for their preparation and investigation 
have been devised (Schaarschmidt, 1982). 

The quality of preservation of the leaves is 
quite variable but can be easily gauged with the 
use of epi-fluorescence microscopy. Some have 
well-preserved cuticles but in others the cuticles 
had been more or less destroyed by decay before 
fossilization. The water of the Messel lake had 
little current (Franzen, 1982), and therefore the 
leaves may have been very slowly deposited. For 
the same reason flowers are seldom preserved 
and those present are of fairly large size. 

In this paper, I present a preliminary report of 
the first three flowers, which were found in Mes- 
sel until 1980. Since this time, the number of 
collected specimens increased enormously. Par- 

ticularly, excavations during the summers of 1983 
and 1984 brought a lot of small flowers, and by 
help of fluorescence, it was possible to identify 
d remains. The more than 1,000 flow- 

collected so far belong to about 70 genera of 
а families. 


Eco Sc a 
| Natur-Museum Senckenberg, Senckenberganlage 25, 6000 Frankfurt 1, Federal Republic of Germany. 


ANN. MISSOURI Bor. GARD. 71: 599-606. 1984. 


E 


600 


R 1 af the M 1:51 а 
5 


FIGURE 1. 
ox 


TECHNIQUE 


Engelhardt (1922) published only drawings of 
the leaves, as did Sturm (1971) using an im- 
proved drawing technique, because of the diffi- 
culties of photographing the black leaves on the 
black oil-shale. Frequently it is not easy to see 
the leaf margin or the venation of dry prepared 
specimens. We have tried several techniques for 
examining the leaves, and some of these have 

so been helpful for the study of the flowers 
(Schaarschmidt, 1982). 


FiGures 2, 3. Tiliaceae flower, x3,—2. 
tals, оуше (С isi Мр sa 
ec fo (G) and style visible (points = single pollen grains, circles = groups of pollen grains) 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


2. Drawing 


[Уо1. 71 


Because the Messel oil-shale breaks during 
drying, the flowers and other delicate samples 
are stored in a fluid, either glycerine (disinfected 
by Thymol) or in liquid Polyethylene-Glycol 200, 
400, or 600. Specimens stored in this way are 
easy to photograph. If necessary, contrast was 
increased by two polarizing filters, one attached 
at the lamp, the other below the camera objective 
(Schaarschmidt, 1973). For one specimen, we 
obtained clear pictures in infrared light by use 
of the Wild infrared image intensifier M 520, 
provided for testing by Ernst Leitz KG, Frank- 

in. For fine details, we successfully 
used the fluorescence technique (Friedrich & 
Schaarschmidt, 1977, 1979) and were able to 
observe grains, either isolated or in the anthers, 
sufficiently well for preliminary determination. 
Anther wall details could also be seen with this 
technique. 

e have constructed special macrofluores- 
cence equipment for lower power observation 
(Schaarschmidt & Friedrich, 1981, Schaar- 
schmidt, 1982). At the microscope, we have used 
the following filters: for excitation, a band pass 
filter, BP 350—460 and as barrier filter, a long- 
wave pass filter, LP 515. 


MAGNOLIALES FLOWER 


Material. 
SM.B. 13476 à; 
Description. The fragment ofa disc 


Forschungsinstitut Senckenberg: 


-like flow- 


х 


), 4 
according to the fossil. Three sepals (one E 


| 


| 


1984] SCHAARSCHMIDT— EOCENE OIL-SHALE 601 


lcm 


F H 
IGURES 4, 5. Sapindales inflorescence; 


x 5.—4. Dra 


Кс A $ 


WS 
E 


P^ 


wing according to the fossil; main axis broken in the 
10 


mi : 
"даје part and drifted to the right; scales black.—5. Recons 


eo of 32 mm and shows two groups 
С у arranged stamens (Figs. 1, 6). In in- 
ly My fluorescent light, the anthers are clear- 
+ to consist of four thecae (2-2.5 mm long), 
a = by a long longitudinal slit (Fig. 7). 

н ent 1s attached basally or dorsally. The 
Miss has an unknown number of rounded 
(Fig. "nh 15 not much longer than the stamens 
wa 115 not possible to decide whether these 
чы ог petals. If carpels were present they 
the Gans е been in the center of the flower, where 
il is absolutely black. In this area, there 


seems to be some indistinct objects shaped like 
Ranunculus carpels. 

The pollen grains are clearly visible in flu- 
orescent light. Isolated grains are distributed all 
over the flower, and the pollen sacs are full, sug- 
gesting fossilization before anthesis. The prolate 
tricolporate pollen grains average 22 um in di- 
ameter. The three equatorial colpi have indis- 
tinct pores and the exine is fine scabrate (Figs. 
8-11). 

A reconstruction of the flower is given in Fig- 
ure 1. 


—— — D—— 


602 ANNALS OF THE MISSOURI BOTANICAL GARDEN Vol | 


FIGURES 6-13. 6-11. Magnoliales flower.—6. 7 1 in i ight; ; 7, x5.—8. sa 
.—6, 7. The specimen in infrared light; 6, x 2.5; 7, hofthe structu? 


i 1% 
electron micrograph of the polar view ofa pollen grain; x 2,500.—9. Scanning electron micrograp 


1984] SCHAARSCHMIDT — 


Systematic position. This type flower occurs 
only in the Polycarpicae (Ranales sensu lato), but 
there seems to be no family that includes all the 
following features of the specimen: helical ar- 
rangement of the stamens, long thecae, a short 
perianth, and tricolporate pollen grains. 

The first two characteristics occur in the Nym- 
phaeaceae, but generally they have longer petals 
and inaperturate or monosulcate pollen. Tricol- 
pate pollen occurs in Nelumbo (Erdtman, 1952: 
287). The same g t and truction of 
the stamens also occur in the Magnoliales. In the 
Magnoliaceae, the pollen grains are monosulcate, 
but tricolpate pollen does occur in the Illiciaceae 
and Schisandraceae (Erdtman, 1952: 254—258). 
Flowers of some Dilleniaceae are also similar; 
the Dilleniaceae produce tricolpate pollen grains 
(Erdtman, 1952: 148) and in the Paeoniaceae 
tricolporate pollen is found. Despite these sim- 
ilarities, without knowledge of the gynoecium it 
I$ not possible to assign the flower to an extant 
family. However, at least, in so far we know it, 
inm be a flower of one family of the Magno- 

iales, 


TiLIACEOUS FLOWER 


Material. Landessammlungen für Natur- 

de, Karlsruhe, 1 flower. 

Description. Flower with a pedicel 15 mm 
long, four pointed and recurved petals. Three 
petals are obvious and the tip of a fourth petal 
can be seen at the upper margin of the flower 
(Figs. 2, 3, 12). The petals may have been thin, 
because they are folded. In front of the left and 
middle petals are remains of two sepals. They 
are strap-shaped. Ovary and style are preserved 
but still covered by parts of the flower. No sta- 
Mens are visible. 

Pollen grains are scattered on the surface of 

€ calyx. These pollen grains are all of one mor- 
Phological type (Fig. 13). The grains are tripore- 
ovate and of the tilioid type. Because of their 
uniformity and because of the absence of other 

€rent pollen grains, I believe that they were 
Produced by this flower, which would also in- 
dicate bisexuality. The pollen grains are 36-42 
ит (average 39.5 um diameter) and rounded to 
gular in outline in polar view. The tilioid 
— OS TTS, 


~ 


хе сори and the ехіпе; х 
N. 12, 13. Tili 
cence; x $00. iliaceae flowe 


EOCENE OIL-SHALE 603 


pores are located at the straight flank (i.e., plan- 
aperturate). 

Systematic position. The systematic position 
is clearly identified by the pollen as tilioid type 
pollen, which occur only in the Tiliaceae (Mai, 
1961: 56), although not in all genera of the fam- 
ily. On the other hand, most of the flowers in 
this family are pentamerous, but a few subfam- 
ilies such as the Tetralicoideae and the Tilioideae 
pro parte (e.g., Sparmannia) are tetramerous 
(Burret, 1926). 

Mai (1961) described a flower of the Tiliaceae: 
Burretia instructa Mai (Brownlowioideae) from 
the Miocene of Central Germany, but this is quite 
different from the Messel fossil. It is pentamer- 
ous, unisexual, and has a fused calyx. The Messel 
flower is tetramerous, bisexual, and has free se- 
pals, and may belong to a genus of the Tilioideae 
with flo SL ia, 
which does not have tilioid pollen grains. Also, 
the Tilia flowers described by Hall and Swain 
(1971) have no similarity to the Messel flower. 

Tilioid pollen is abundant in the Tertiary. At 
Messel, Intratriporopollenites pseudinstructus 
Mai (1961, text-fig. 3), occurs in the dispersed 
palynoflora and is similar to the pollen grains 
found in the flower. 


SAPINDALES INFLORESCENCE 


Material. Forschungsinstitut Senckenberg, 
SM.B. 13477. 
Description. The specimen is a catkin 28 mm 


long consisting only of stamens. In the lower part 
it is branched several times. The middle part is 
broken, slightly distorted, and displaced to the 
right, perhaps by a weak current during deposi- 
tion (Figs. 4, 5, 14). 

The stamens are arranged in groups, which 
may be simple flowers (Fig. 15). Unfortunately, 
it is impossible to count the exact number of the 
stamens but the number appears to be between 
three and six. Each flower has one or two pointed 
scales about 1 mm long at the base. The scales 
are not conspicuous and both can be seen only 
in laterally compressed flowers. 

The anthers are 2.5 mm long, with a short 
filament. They open by longitudinal slits. In flu- 
orescent light the epidermis of the anthers is vis- 


5,000.—10, 11. Polar and lateral views of the pollen grains in transmitted light; 
г.— 12. The whole specimen; х 3.— 13. Polar view of a pollen grain, epi-fluores- 


аа а е а a део‏ ققق 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


FIGURES 14-24. Sapindales inflorescence. — 
16. Pollen grains in stamens, epi-fluorescence; x 


ГЩ. . T rnt | , 
14. Cluster of flowers, the scale of one flower visible; x20 lle? 


500.— 17. The specimen in flat light; x 5.—18-20, 23, ЖИШШ 


En. d 


| 


"-— 


— = (—— 


1984] 


ible and consists of longitudinal cells. The epi- 
dermis of the scales has polygonal cells. 

The pollen grains are fairly small, 18 um in 
diameter, circular in equatorial and polar views, 
and distinctly tricolporate (Figs. 15—24). 

Systematic position. Because ofthe very sim- 
ple construction, it is not easy to find the right 
position of the inflorescence. There are two or- 

come into question. Both 
have bisexual flowers but with the tendency to 
unisexuality and wind pollination. 

In one order, Hamamelidales, the single flower 
of the Messel inflorescence resembles most the 
Cercidiphyllaceae, which also has flowers with 
two scales at the base. But in contrast to o 
specimen, the inflorescences of the Cercidiphyl- 
laceae are close clusters, they have more stamens 
per "flower" (8-11), and their pollen grains are 
only tricolpate (Erdtman, 1952: 106-107). The 
other families of Hamamelidales, Platanaceae, 
and Hamamelidaceae, are M po more different, as 
well, in their s, especially 
in the construction of the inflorescences, which 
are normally clusters or globose heads. Only a 
few genera of Hamamelidaceae have spikes, but 
none have branched catkins. The related Eucom- 


SCHAARSCHMIDT — 


EOCENE OIL-SHALE 605 


Messel inflorescence also had a calyx before fos- 
silization. On the other hand, the relationship to 
Pistacia is not probable, because in this genus 


no ll e than three 
" apertures (Erdtman, 


3240. ds d 


“not sharply delimited" 
1952: 48). 

There are still more families in the Sapindales 
in which unisexual panicles occur — sometimes 
the flowers аган petals—for i instance: Staphy- 

leaceae, Sabia 
and Meliaceae. But we lave not уе found а liv- 


inflorescence. Therefore, we classify it as a Sap- 
indales inflorescence 


CONCLUSIONS 


There is, with a few exceptions, a long gap 
between the excellent published record of fossil 
flowers by Conwentz (1886) from the Eocene 
Baltic amber and the modern systematic inves- 
tigation of early Tertiary flowers, especially from 
the Middle Eocene Clairborne formation by Cre- 
pet, Dilcher, and others. It is rapidly becoming 
clear that fossil flowers are available for inves- 
tigation and yield important information for our 

1 + Ai f a1 1 evoaliiti seems 


ers. The pollen grains are 3-colporoidate (Erdt- 
man, 1952: 164), but the flowers are also in 
clusters. It seems that the Messel inflorescence 
does jg eds to the Hamamelidales or any 
related amily. 

The ы order with a tendency towards uni- 
Sexuality are the Sapindales. Most families have 
Panicle-like inflorescences, occasionally with 
unisexual flowers that lack a perianth. It seems 
that the most similar inflorescences occur i in the 
following families. Se 
have paniculate inflorescences. The male flowers 
of Dodonaea, for instance, contain about seven 
stamens, petals are absent but the four small, 
conspicuous sepals don’t correspond with our 
flowers, More similar are the male catkin of Pis- 
tacia (Anacardiaceae). The five stamens are of 
similar shape and size, and at the base of the 
single flowers a scale-like bract is visible. How- 
ever, the flowers of Pistacia have a reduced 
S-lobed Calyx. It may be that the flowers of the 


env. ШИИ C S 


-— 
Brains in 
X 5,000. 


in lateral and polar view in transmitted light; x 1,000.—21 
View of a pollen grain; x 2,500.— 22. Scanning electron micrograph 


that, by the early Tertiary, anemophilous flowers 
were already highly developed, and at nearly the 
same level of their living relations (Crepet, 


maceae (Zavada & Crepet, 1981). Against that, 
the entomophilous flowers have still been more 
primitive. Therefore, it i is generally not as easy 
asint tł 

with living plants. Most of the fossil entomoph- 
ilous flowers are radially symmetrical; bilateral 
symmetry is still at the beginning. It is also sig- 
nificant that the fossil record of early angio- 
sperms shows both catkins and oligomerous ra- 
dial flowers. Polycarpous fl found rarely 
as fossils generally. For instance, Seward and 
Conway (1935: 22. pl. 4. fig. 20) and Bock (1962, 
text-figs. 498, 499) published seed axes called 
Magnoliaestrobus from Cretaceous of Greenland 
and Oligocene of Hungaria; Dilcher (1979: 315. 
figs. 40, 50, 51) and Dilcher and Crane (1984) 


1. Scanning electron micrograph of the polar 
of the structure of the colpus and the exine; 


606 


have described an archaic elongated axis with a 
high number of carpels from the middle Creta- 
ceous. Now i in Messel the male part of a flower 
of thi first found, which 
was interpreted : as the most primitive angio- 
sperm group by many botanists in the past. 

Although in the Messel oil-shale flowers are 
very rare, we hope to contribute more results to 
this important field of angiosperm paleobotany 
in the future, because the plant remains of Messel 
are well preserved and allow several fine-detailed 
investigations. 


LITERATURE CITED 


BERG, D. 1966. Die Krokodile, deg tnis Asia- 
tosuchus und aff. Sebecus?, au m Еохап von 
Messel bei Darmstadt/Hessen. pe Hess. Lan- 


desamtes Bodenf. 52: 1-105. 

Bock, W. 1962. Systematics of diuo and evo- 
lution. Geol. Center Res. Ser. 2: 1 ү» 

ee M. 1926. eitráge 7 s der Tili- 


che 86 Die Бре des Bernsteins uiid 
ihre Beziehungen z ora der Tertiárformatio 

d der Merc Wilhelm Engelmann, Leipzig 

CREPET, W. L. 1979. me aspects of the pollination 


biology of Middle Potene angiosperms. Rev. Pa- 
laeobot. Palynol. 27: 213-238. 

. DAGHLIAN. 1980. Castaneoid inflo- 
rescence from the Middle Eocene of Tennessee and 
the diagnostic value of pollen (at the oy 
level) in the Fagaceae. Amer. J. Bot. 67: 739— 

‚ D. L. Опснев & R. W. POTTER. 1975. in 
vestigations of angio sperms from the Eocen 


Early angiosperm r 
tion: an introductory report. Rev. Palacobot: Pal- 
ynol. 27: 291-328. 

Р. К. CRANE. 1984 [1985]. Archaeanthus: 
an early angiosperm from the Cenoma anian of the 
western interior of North America. Ann. Missouri 
Bot. Gard. 71: 351-383. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


ENGELHARDT, Н. 1922. Die alttertiáre Flora von 
Messel bei Darmstadt. Hess. Staatsverl. Darm- 


ERDTMAN, G. 1952. Pollen Morphology and Plant 
унета Angiosperms. Almqvist & Wiksell, 
Stockhol 

FRANZEN, J. L 1982. Senckenberg-Grabungen in der 
Grube Messel bei Darmstadt. 3. Ergebnisse 1979- 
1981. Cour. Forsch. Inst. Senckenberg 54: 1-118. 

FRIEDRICH, W. L. & F. SCHAARSCHMIDT. 1977. Zwei- 


fossilen Pflanzen. Cour. Forsch.-Inst. Senckenberg 
24: 31-49 


1979. Epi fluorescence of fossil 

plants. ica. 24: 16-18. 

HarL, J. W. & A. M. Swain. 1971. Podun О 
of Tilia from the Tertiary of western United Sta 
Bull. Torrey Bot. Club 98: 95-1 

KOENIGSWALD, W. v. 1980. Fossillagerstátte Mes- 
sel— Literaturübersicht der Forschungsergebnisse 
aus den Jahren 1969-1979. Geol. Jahrb. Hessen 
108: 23-38. 

Mai, D. 1961. Über eine fossile Tiliaceen-Blüte und 
tilioiden Pollen aus gen. deutschen Tertiar. Geo- 
logie 10(Beih. 32): 5 

SCHAARSCHMIDT, F. n pU О in un- 
gewohnlichem Licht. Natur & Mus. 103(7): 247- 
253, 


1982. Präparation und Untersuchung ма 

eozünen Pflanzenfossilien von Messel bei 7 

stadt. Cour. Forsch.- Inst. Senckenberg 56: 59-7 
W. L. FRIEDRICH. NOU. [Abstract:] Epi 

fluorescence of fossil p s. 13th Int. Bot. 

Congr. Sydney. 

Soka АС. С. & У. Conway. 1935. ET Cre- 


4ne Fl Abt. 
uraceae. diee 


armsta: 
B, Paltopytal 134: 1-60. 

Tosen, Н. 1968. Das biostratigraphische Alter der 
mitteleozinen Fossilfundstátte Messel bei Darm- 
stadt (Hessen). Notizbl. Hess. Landesam 


ZAVADA, 
of angiosperms from the Middle Eocene 0 
America: flowers of the Celtidoideae. Amer. 
68: 924—933 


| 


ADVANCED (CONSTANT) INSECT POLLINATION 
MECHANISMS: PATTERN OF EVOLUTION AND 
IMPLICATIONS VIS-A-VIS ANGIOSPERM DIVERSITY! 


WILLIAM L. CREPET? 


ABSTRACT 
The fi ic relati angiosperm flower and insects, combined wi 
the correlation between i insect аа апа тапу > the most diverse angios perm fam 
that i insect pollination has had an impo a 


1 
consistent with these correlations— urthermon re, mode егп angiosperm diversit уш ау 


related to insect pollination by the s tant pollinators. Until 
the present оше, paleontologica data hive mitigated this possibility тё ean that both 
advanced insect pollinators and their co-adapt rm fi to have been 


of major significance in angiosperm radiatio ites E of paleobotanical and бб надай ра 
нач together with paleobotanical data indicate that hymenopteran and lepidopteran pollinators, and 

angiosperm taxa having flowers adapted to them, existed at a time of major angiosperm radiation. 
Although angiosperm success cannot be confidently related to one feature, the importance of insect 
Pollination in the diversification of the group can no lon жы be minimized in the context of the fossil 


record. Angio tracheophyta by their overwhelming diversity [250/ 
300 families of vascular plants are angiosperms; 240, 000/300, 000 орнай of flowering plants are 
bers of individuals and 


angiosperms (Burger, 1981 1)]. T giosp 


val lation 


Furthermore, 


in vegetative and. feproductive morphology, anatomy, and habit. 


acters related to floral morphology and function 
including the ме ан сопашоп, еп- 
aes ovules, monosulcate granular-walled pol- 
еп, double fertilization, and insect pollination. 


per iin | 1981). There are numerous ex- 
cid of radiations in angiosperm taxa asso- 
ated with adaptations for various animal pol- 


na 
te one species at a time) or more or less ab- 


Eso uo S A 


solutely (oligotropic-monotropic) faithful, and 
flowers may be adapted to bee (and other) pol- 
linators in a variety of ways (Heinrich, 1979, 
1981; Macior, 1974). Correlations between var- 
ious diverse angiosperm taxa and animal polli- 
nators, particularly constant pollinators, suggest 
mM a may be a порана relationship 


Tant, 


1949; Grant & Grant, 1965; Baker & Hord. ‚ 1968; 
Crepet, 1979). Certain aspects of insect polli- 
nation may include characteristics pu provide 


Б из ро1 11111 
д 


пр 
1 


as well tł i i elated to spe- 
ciation (and the production of diversity. 
At the species level, these include: 


a. Reliable directional pollination with its en- 
ergetic advantages (Pohl, 1937; Cruden, 1977). 

b. The production of outcrossed offspring in a 
population of relatively widely dispersed in- 
dividuals (Burger, 1981). 


Crane, Field Museum of 


author gratefully Rui eir the assistance and/or thoughtful criticism of the following: Dr. C. 
B. H. R. 


' The 
Michener, Uni ersity of Kansas; Tiffney, 


Yale University; Dr. Peter 
ry; Dr. К К. McGinley, United States National Museum; Drs. 


D. 1. Dilcher an d S. R. Manchester, 
f N. A. Noridge, 


Indiana быы 


er of Connecticut. Research supported by NSF  DEB-8110217. 
Ological Sciences Group U-42, University of Connecticut, Storrs, Connecticut 06268. 


ANN. Missouni Bor. GARD. 71: 607-630. 1984. 


608 


c. Successful pollination under environmental 
conditions inappropriate for wind pollina- 
tion. 


Potential advantages at the level **Angiosper- 
mae” (i.e., those related directly to diversity) in- 
clude: 


a. The filling of *empty" niches as a result of 
ъз апа #479 above 


b. The deflecti of faithful ү llinat fi their 
host plant through stochastic change in key 
floral features (altered developmental pat- 
terns) could provide the means for restricting 
gene flow from parental populations to iso- 
lated (peripheral or sympatric) demes (see the 
scenarios outlined in Fig. 1A and B based on 
Grant, 1949; Gottlieb, 1982; Tiffney, 1984). 


The combination of these features of angio- 
sperm reproductive biology represents a mech- 
anism for increasing the frequency of the for- 
mation of small, genetically isolated populations 
in which evolution can proceed rapidly (due to 
founder effect/drift, the potentially rapid fixation 
of mutations, etc.), thus maximizing the proba- 
bility of speciation and conforming with the 
punctuated equilibria model of Eldredge and 
Gould (1972) and Gould and Eldredge (1977). 
The net result: augmented speciation in angio- 
sperms consistent with their present diversity (Fig. 

}, 


Many features of the angiosperms can be геа- 
sonably regarded as having contributed to their 
present diversity. For example, Mulcahy has 
considered the advantages conferred by a repro- 
ductive system that allows for gametophytic as 
well as sporophytic competition (1979) and Tiff- 
ney (1 не pointed out Че speciation- “Promoting 
quality of 
the discussion below and Crepet, 1982). Burger 
(1981) and Stebbins (1981) have independently 
summarized and evaluated the various features 
of angiosperms likely to have been im mportant in 
their present success. Stebbins pointed out the 
need to consider the fossil record in assessing the 
impact of insect pollination on present angio- 
sperm diversity. He noted that the types of pol- 
linators most likely to be directly involved in the 
establishment of diversity (1.е., constant polli- 
nators) evolved too late to have participated in 
major angiosperm radiation and considered in- 
sect pollination to have been supplemental, and 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


not essential. Stebbins (1981) considers attri- 
butes he views as following from the reduction 
of the female gametophyte as having been of 
major significance in angiosperm success. These 
include the closed carpel, double fertilization, 
and the stylar canal. Few would debate the po- 
tential advantages of these features (the ultimate 
role of the carpel, for example, in fruit dispersal), 
but Stebbins’s implicit separation of these char- 
acters from co-evolution with insect pollinators 
is open to question. 

d neontological 
information suggests an alternative interpreta- 
tion of the timing of the evolution of constant 
pollinators and of the radiation of the angio- 
sperms. It is my intention to offer a preliminary 
account of the diversification of advanced ad- 
aptations to insect pollination likely to have in- 
volved constant pollinators and of the possible 
implications with regard to angiosperm history. 
The bases for my argument include: 


1. The growing тир record of flowers, inflores- 
cences, and frui 
2. Bee bioge sean and its evolutionary Sig- 
nificance, as recently discussed by Michener 
1979). 


3. Recent data on patterns of бого 
the angiosperms (e.g., Niklas et al., 198 
Muller, 1981; Tiffney, 1981). 

. Improved understanding of the bep 
value of pollen and leaves combined with 


e occurrences 
O MOIR on th OEE 


A 


taxa from the same localities or times. 


PALEOBOTANICAL EVIDENCE ON THE 
STATUS OF ADVANCED POLLINATION 
ca- 
Angiosperms with floral morphology - 
tive, of pollination by MAE constant ? 


© IVI 


fossil record of flowers and fruits combin 
a better understanding of the taxonomic signif- 
icance of fossil leaves and pollen ai 
Flower and inflorescence fossils have bee 
portant in assessing the status of families ee 
advanced pollination mechanisms at ke 4 
times in the past. They provide the де 
floral morphology that can be used, with Flor 
cautions, to infer pollination mechanisms. the 
data have also been important in confirming 


PARENTAL SPECIES 


A. Peripheral Isolates 


. Isolation of demes often through 
the agency of animal fruit dis- 
amine at the periphery of sirap pa- 

tal species with some geo- 
و‎ эсас нарат дый 
to gene flow. 

2. Change in a key floral feature due 
to mutation or to the b wn 


— 


cy ech isolatio 
3. The peripheral deme is then free 
fro 


rgen 
cilitated by founder effect/genet- 
ic drift. 

. Genetic isolation from parental 
species is maintained by polli- 
nator constancy in the event of 
possible recontact. 


. 


~ 


w 


A 


B. Sympatric “Isolates”* 


. Isolation of a sympatric deme is ini- 


tiated by a mutation in a key floral 
feature causing a change in pollinator 
behavior or mechanical isolation. 


. Typical foraging behavior of constant 


pollinators facilitates the spread ofthe 


individuals comprises a deme isolated 
by pollinator constanc 


. Founder effect/genetic drift may be 


important in divergence from paren- 
tal species. 


* “В” is based in part on Grant, 1949. 


FIGURE 1. 
and animal seed 


-— 


~ 


> ~ 


С. Allopatric Speciation 


. Deme isolated by geography 


(distance or topography), 
— the agency of animal 
dis 


2 ы divergence associ- 


ated iic new environment via 
selec 


: ы of founder aya ose 
drift depe size of dem 


develop before recontact with 
parental population. 


pin possible scenarios for the isolation of small populations due to the combination of faithful pollinators, stochastic floral change, 
spersal. 


NOLLVNITIOd .LO3SNI —.LHd3?1O [7861 


609 


610 


existence of taxa or of floral character complexes 
at times when most modern paleobotanist Id 
be reluctant to risk inferring their presence on 
the basis of other organ evidence alone (e.g., Pa- 
leocene Gentianaceae, Crepet & Daghlian, 
1981а). Floral data have, in addition, added to 
the significance of the dispersed palynological 
record by allowing an assessment of the accuracy 
with which particular palynomorphs reflect par- 
ticular suites of associated floral characters and 
by increasing the taxonomic significance of as- 
sociated palynomorphs that have been enigmatic 
when dispersed. 

Increasing numbers of in-depth studies of the 
pollen of extant taxa in conjunction with the in- 

d | fcl ] to classify pol- 

len based on scanning electron and transmissio 
electron microscopy have been important in 
making fossil pollen a valuable diagnostic fea- 
ture. Fossil leaf studies have also been important 
in improving our understanding of angiosperm 
history. Careful studies ofleaves have shown that 
they too may be good taxonomic characters if 
fine venation patterns and/or cuticular details are 
determined and analyzed in the context of vari- 
ation in similar features in extant related taxa 
(Hickey, 1973; Dilcher, 1974). 

A significant problem in interpreting the fossil 
record of angiosperms has been attempting to 
deduce the character state of one particular organ 
from another more commonly preserved organ, 
in this case, floral structure from pollen, fruit, or 
leaf evidence. While one character state can nev- 
er be predicted from another with absolute cer- 
tainty, neontological data and increasing knowl- 
edge ofthe various organs of particular taxa from 
specific geological horizons suggest that in re- 
cognizably modern families there is a high degree 
of correlation among the states of the various 
organs of a taxon [e.g., the Ulmaceae where 
Eocene celtidoid flowers and pollen both seem 
reflective of an insect-pollinated ancestry for the 
now wind-pollinated taxon (Zavada & Crepet, 
1981); the Araceae (Crepet, 1978; Dilcher & 
Daghlian, 1977); the Juglandaceae (Crepet et al., 
1975; Manchester, 1981); the Fagaceae (Crepet 
& Daghlian, 1980; Jones, 1979), etc.]. 


МУЦИ 


publ. data). Both flowers and pollen must be 
adapted to the physical and behavioral charac- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог, 71 


teristics of biotic pollinators or to various phys- 
ical agencies that might effect pollination. The 
correlation between fruits and flowers in the past 
is more complex. Evidence presented by Tiffney 
(1984) and considered later in this article sug- 
gests the possibility that faithful pollinators tem- 
porally preceded animal fruit dispersal. 

Fruit structure, then, might “lag” evolution- 
arily behind floral features. Thus, fruit structure 
of a modern family represented in the fossil 
record might be too conservative an indicator of 
the floral condition at a given point in the past. 
On this basis, it seems unlikely that a modem 
taxon recognized from a particular geologic ho- 
rizon on the basis of fruit evidence would have 
floral features significantly different from what 
might be expected based on the modern сћаг- 
acters circumscribing the taxon. 

It is perhaps more difficult to imagine the rea- 
sons for correlation between leaf and floral struc- 
ture other than that both are complex organs and 
might be united to some extent by character cor- 
relations associated with cladogenesis. Yet; 
growing fossil evidence suggests correlation be- 
tween leaf and floral structure in the history of 
extant families. 

As more attention is being devoted to all the 
organs representing a particular taxon from à 
particular horizon, the possibility that taxa гер- 
resenting unique mosaics of modern characters 
existed in the past may be evaluated. Such com- 
binations, if sufficiently different, might be a 
leading in the context of the evolution of po 
nation mechanisms, but only a few such instances 

be 


; 10 
therefore pollination mechanism, been foun 
vary significantly from what might have been 
expected from other organ evidence. 


particular sufficiently complex organ taxon - 
been demonstrated adequately, it is fairl me 
assume that basic floral morphology and ol 
pollination mechanism were at а similar a 
tionary state. In the present paper, rem 
organ taxa other than flowers and inflo 


ntempor? 


in this manner are backed up by со 

neous floral evidence. Two 
The paleobotanical data. Method 

major sources of data other than discrete rep% 


-———— ——— —— s —— summ 


— 


чил — 


1984] 


and work in progress were used in assessing the 
A E ~. *4L A ! 115 4 


syndromes (Muller, 1981; Reid & Chandler, 
1933). These were selected because of the proven 
taxonomic value of pollen and fruits, their likely 
correlation with floral structure, and because the 
quality of the identifications is high in each case. 
Data were selected from individual reports ac- 
cording to the significance of the taxa involved 
and only if the reports involved clear demon- 
stration of affinities on solid morphological-an- 
atomical grounds. More data on the occurrences 
of advanced families will doubtlessly come to 
light in the future and some of the taxa reported 
in Muller (1981) and Reid and Chandler (1933), 
even as modified by Chandler (1961), may not 
stand up to further investigations, but the data 
presented are a reasonable state of the art rep- 
resentation of the occurrences of various floral 
characters at various times in the past. 

ata. Table 1 is a summary of all data on 
the occurrences of families with pollination syn- 
dromes typical of the Apoidea and Lepidoptera 
and even some birds/bats. Families with appro- 
priate syndromes are listed chronologically 
(however, see footnote a, Table 1) and families 
may be listed more than once to include as many 
reliable reports as possible based on as many 
different types of fossil evidence as possible. The 
table includes the ages, order, family, type of 
fossil evidence, characters related to the ad- 
vanced syndrome and type of syndrome, and 
pollinators usually associated with the family. 
E ore summarizing the pattern of evolution 
i various pollination syndromes, I would like 
О discuss the appearances of several individual 


di un not of the features represented by 
id laxa serves to corroborate the general 
woe of the evolution of advanced polli- 
10n syndromes gained from Table 1. 
: „дађаіез-Мітозасеае. Mimosoids have 
i 8 blossoms and are pollinated by a va- 
ML faithful pollinators including bees, lep- 
du га, and bats. Brush-type blossoms are 
(Fi mon in Middle Eocene Claiborne deposits 
18. 2) and inflorescences similar to modern ra- 
ы mimosoid inflorescences are known from 
k iddle Eocene and younger deposits of the 
"ur United States (Crepet & Dilcher, 
» Daghlian et al., 1980). Spicate inflores- 


CREPET—INSECT POLLINATION 


611 


cences are 6 cm in length with sessile, alternate, 

perfect flowers (Fig. 3). Floral envelopes consist 

of a lobed calyx and a corolla with four ovate 

lobes (Crepet & Dilcher, 1977). There are eight 

exserted stamens with bilocular, versatile, lon- 

gitudinally dehiscent anthers (Crepet & Dilcher, 
7). Th i i 


differences suggest that they represent an extinct 
genus. Floral structure and palynological config- 
uration (i.e., why invest units of pollen grains 
rather than single grains in unfaithful pollina- 
tors), suggest that the Eocene mimosoids were 
also pollinated by faithful pollinators, implying 
a prior history of co-evolution. Recent discov- 
eries of Paleocene mimosoids support this pos- 
sibility (Table 1). 

Fabales-Caesalpiniaceae. While Paleocene 
inflorescences are the first reliable reports of the 
Mimosaceae, the Caesalpiniaceae have been re- 
ported as early as the Maestrichtian on the basis 
of highly distinctive Sindora pollen (Table 1). 
The presence of the Caesalpiniaceae and of myr- 
taceous pollen (Table 1) in the Maestrichtian also 
suggests that the brush-type blossom, or one that 
closely approximates it, originated rather early. 

Fabales-Papilionaceae. Studies of paleocene 
flowers now in progress reveal that the typical 
highly derived zygomorphic papilionaceous 
flower already existed at that time. Details wil 
l tedi 1 blication (Crepet, 


unpubl. data). 

Asteridae. А recently discovered flower from 
the Lower Eocene of the Gulf Coastal Plain has 
several important implicati ith regard to the 
tempo of evolution of bee pollination. Flowers 
are distinctive in having an open, funnelform, 
ympetalous, seven-parted corolla (Fig. 6) and 
unusual pollen (Fig. 7). Pollen preserved within 
compressed anthers is 22 um in diameter, intec- 
tate, triaperturate, and has prominent gemmae 
(Figs. 7, 8). Pollen is well known as the dispersed 
Upper Cretaceous-Eocene palynomorph, Pistil- 
lipollenites macgregorii. Pollen is most common 
in the Paleocene-Lower Eocene. 

The combination of floral and palynological 
features is suggestive of affinities with the mod- 
ern Gentianaceae although the taxon is clearly 
extinct. Floral structure is typical of bee polli- 
nation (e.g., Faegri & van der Pijl, 1971) in the 
angiosperms in general and in the Gentianaceae 


Ф 


TABLE 1. Summary of evidence related to the geological occurrences of angiosperms associated with advanced pollinators. 
Subclass Order Family Evidence Geography 
Upper Eocene 
Asteridae? Gentianales 1. Apocynaceae 1. Rauwolfia-type pollen 1. a) Cameroon b) Venezuela” 
Rubiales 2. Rubiaceae 2. Gardenia-type pollen 2. Germany 
Rosidae Fabales 3. Mimosaceae 3. Acacia-type poll 3. Cameroon 
4. Mimosaceae 4. Adenanthus-type 4. Cameroon 
5. Mimosaceae 5. Calpocalyx ngnouniensis-type 5. Cameroon 
pollen 
6. Mimosaceae 6. Parkia-type pollen 6. Cameroon 
Myrtales 7. Combretaceae 7. Terminalia-type pollen 7. Cameroon 
8. Lythraceae 8. Crenea-type pollen 8. Northern South America 
Rosales 9. Escalloniaceae 9. Quintinia-type pollen 9. New Zealand 
Santalales 10. Loranthaceae 10. Amylotheca-type pollen 10. New Zealand 
Middle Eocene 
Asteridae Dipsacales 11. Caprifoliaceae 11. Viburnum-type pollen 11. France 
Scrophulariales 12. Bignoniaceae 12. Dolichandrone-type pollen 12. Southeastern Vc States 
Solanales 13. Convolvulaceae 13. Merremia macr vela: pollen 13. a) Brazil b) N 
Rosidae Euphorbiales 14. Euphorbiaceae 14. a) Paleowetherellia fru 14. a) Egypt b) Taina 
manean зо 
Fabales I» n: p 15. Brachystegia-type pollen 15. Nigeria 
16. Mimosa 16. Eomimosoidea plumosa floral, pol- 16. Texas 
en 
17. Mimosaceae 17. Pentaclethra macrophylla-type pol- 17. Cameroon 
Myrtales 18. Myrtaceae 18. Eugenia-type pollen 18. Tennessee 
Polygalales 19. Malpighiaceae 19. Brachypteris-type pollen 19. Brazil 
Sapindales 20. Sapindaceae 20. Diplopeltis huegelitype pollen 20. Central America 
Zingiberidae али ар 21. Heliconiaceae 21. а) Heliconiaceous flow 21. a) Tennessee 
b) Heliconiaceous чийсе: b) Deccan Intertrappean 
22. Musaceae 22. Musaceous fruits 22. Deccan Intertrappean 
23. Zingiberaceae 23. Zingiberaceous fruits 23. Central Europe 


но ли 


19 


NAUVO TVOINV.LOS RNOSSIA FHL ЧО STVNNV 


IL 10A] 


TABLE 1. (Continued). 
Subclass Order Family Evidence Geography 
Lower Eocene 
Asteridae Gentianales 24. Apocynaceae 24. Ochrosella ovalis fruit 24. London Clay 
25. Apocynacea 25. Ochrosoidea sheppeyensis fruit 25. London Clay 
26. Gentianaceae 26. Pistillipollenites pollen, floral 26. Northeastern Texas 
Lamiales 27. Boraginaceae ia ehretioides fruit 27. London Clay 
Solanales 28. Convolvulaceae 28. Merremia tridentata pollen 28. Cameroon 
29. Solanaceae 29. Cantisolanum daturoides fruit 29. London Clay 
Rosidae Euphorbiales 30. Euphorbiaceae 30. Euphorbiospermum ambiguum 30. London Clay 
seed 
31. Euphorbiaceae 31. Euphorbiotheca minor fruit 31. London Clay 
Fabales 32. Caesalpiniaceae 32. Caesalpinia-type pollen 32. Assam 
33. Mimosaceae 33. Mimosites browniana bowerbank, 33. London Clay 
fruit 
Myrtales 34. Lythraceae 34. Minsterocarpum alatum fruit 34. London Clay 
35. Pachyspermum quinquelocularis 35. London Clay 
rui 
36. Myrtaceae 36. Palaeorhodomyrtus subangulata 36. London Clay 
bowerbank, fruit 
37. Onagraceae 37. Palaeeucharidium cellulare fruit 37. London Cla 
Santalales 38. Loranthaceae 38. Arceuthobium-type pollen 38. North-central Europe 
39. Loranthaceae 39. Loranthus elegans-type pollen 39. Germany 
Zingiberidae Zingiberales 40. Cannaceae 40. Cannaceous leaves 40. Texas 
41. Zingiberaceae 41. Zingiberaceous leaves 41. Texas 
Paleocene 
Asteridae Gentianales 42. Apocynaceae 42. Alyxia-type pollen 42. Northwest Borneo 
43. Gentianaceae 43. birra Uu pollen and associ- 43. Mississippi Embayment 
ated floral type 
Rosidae Euphorbiales 44. Euphorbiaceae 44. espere of the tribe Hippo- 44 


. Mississippi Embayment 


NOLLVNITIOd .LOdSNI —.L3d 3:12 (7861 


£19 


TABLE 1. (Continued). 
Subclass Order Family Evidence Geography 
Fabales 45. Caesalpiniaceae 45. Crudia-type 45. Nigeria 
46. Пе 46. Maniltoa eee PRIN pollen 46. Texas 
47 47. Flowers and inflorescences 47. Mississippi Embayment 
48. ата 48. Flowers 48. umi Embayment 
Myrtales 49. Myrtaceae 49. Leptospermum and Metrosederos- 49. a) New Zealan 
t en b) ган Ridge 
50. Myrtaceae 50. Syncolpites lisamae pollen 50. Australia 
Polygalales 51. Polygalaceae 51. Monnina-type pollen 51. Chile 
Proteales 52. Proteaceae 52. Adenanthus-type pollen 52. Australia 
53. Protea 53. Banksia-type pollen 53. Australia 
54. Proteaceae 54. Beauprea-type po 54. South Australia 
55. Protea 55. Symphyonema-type pollen 55. Queensland 
56. Proteaceae 56. Xylomelon-type pollen 56. Australia 
Cretaceous 
tage 
Maestrichtian Asteridae Gentianales 57. Gentianaceae 57. Pollen associated with flowers 57. Northeastern Texas 
Coniacian Rosidae Euphorbiales 58. Euphorbiaceae 58. vi алы wood 58. м Arizona Б) South Africa 
Maestrichtian Fabales 59. Caesalpiniaceae 59. Sindora-type pol 59. Siberia 
Santonian y 60. Myrtaceae 60. Syncolporites я) pollen 60. G 
Maestrichtian 61. Ona 61. Epilobium-type pollen 61. a) as b) Brazil 
Maestrichtian Proteales 62. mye 62. Helicia-type pollen 62. California 
Maestrichtian 63. Proteaceae 63. Guevina-type pollen 63. penal South America/Cen- 
tral ас 
Upper Senonian 64. Proteaceae 64. Guevina-type pollen 64. New pbi 
Lower Senonian Sapindales 65. Sapindaceae 65. Cupanopsis-type pollen 65. a) Gabon 6) India 
Maestrichtian Zingiberidae Zingiberales 66. Zingiberaceae 66. Zingiberopsis leaves 66. Wyoming, Colorado 


#19 


Мачу О 'TVOINV.LOS ІҸПОЅ5ІИ JHL 30 STVNNV 


IL 10A] 


TABLE I, 


(Continued). 


Floral Structural Features Related to 
Advanced Pollination Syndrome 


Typical Pollination Syndrome 


Literature Cited 


Upper Eocene 


Middle Eocene 


1. Funnel or salverform, sympetalous 
corolla 
2. Funnelform, sympetalous corolla 


3. Brush-type flowers, often with tubular 
го 


Yaw = 
4 
£ 
8 
88 


; лнур flowers formed by pro- 
longed hypanthium 
8. Tubular flowers by an extended hy- 
panthium, some brush-types 
9. Flowers pendent, with a prolonged 
hypanthium 
10. Tubular and brush-type flowers 


li. — corolla, tubular, often 
bilabia 
tz. шы, irregular, sympetalous corol- 
trumpet-type, often bilabiate 
13. Punnelform, sympetalous corolla 


14. Tepals connate toward base 

15. Flag-type flowers, strongly irregular, 
not papilionaceous 

16. As above 


17. As above 
18. Predominantly brush-type flowers 


1. 


Melittophily, Psycophily 


. Melittophyly, Psycophily, Orni- 
thophil 


. Chiropterophily, Melittophily, Orni- 
ily 


thophily, Psycophi 
As above 


Psycophily 


. Chiropterophily, Melittophily, Orni- 
ophily 


thophily, Psyco 


. Myophily, Ornithophily, Phalae- 
nophil 


. Melittophily, Ornithophily 


. Hymenoptera (wasp), edes Or- 


nithophily, Phalaeno 


. Chiropterophily, E ый 
. Myophily, Melittophily 


. Hymenoptera (wasp), Myophily, Or- 
ithophily 


nitho 


. Chiropterophily, Melittophily 


. Chiropterophily, Melittophily, Orni- 
cophily 


thophily, Psy 


. As above 
. Chiropterophily, Ornithophily, Mel- 
hi 


ittophily 


~ — 


e 


MPH» 


. a) Salard-Cheboldaeff (1978) b) Mul- 
. data) 


ler (unpu 


. Krutzsch (1970) 


Salard-Cheboldaeff (1978) 


Salard-Cheboldaeff (1978) 
Salard-Cheboldaeff (1978) 
Salard-Cheboldaeff (1979) 
Salard-Cheboldaeff (1978) 


Germeraad et al. (1968) 


. Mildenhall (1980) 


. Mildenhall (1980) 
. Gruas-Cavagnetto (1978) 
. Frederiksen (1973, 1977) 


. a) Pares wren г al. (1974a, 1974b) 


b) Legoux (1 


. a) Chandler on ) 


b) Manchester and Dilcher (1979), 


Crepet and наф 19815) 
. Legoux (197 
: E Crepet and ла m 


b) Daghlian et a 


80) 
5 ROME (1978, 1979) 
. Elsik and Dilcher (1974) 


NOLLVNITIOd .LO3SNI — L3dH31O [7861 


$19 


TABLE |. 


(Continued). 


Floral Structural Features e to 
Advanced Pollination Syndrom 


Typical Pollination Syndrome 


Literature Cited 


Lower Eocene 


19. Irregular, tending to zygomorphy 
20. Irregular, some flag-types 
21. Strongly irregular, tubular corolla 


22. Irregular, strongly nectariferous, brief- 
y tubular 


23. Zygomorphic, flag-type, tubular corol- 
la 


24. As above 


26. Slender sympetalous corolla, bell- or 
trumpet-shaped 

27. Corolla generally salverform, some- 
times tubular or funnelform 

28. As above 

29. Various funnelform, tubular, trum- 
pet-like flowers 


37. Funnelform to tubular flowers 

38. As above 

39. As above 

40. Erect, tubular, highly irregular sym- 
metry 


4l. As above 


— 


9. Melittophily 

20. Melittophily 

21. Lepidoptera, Melittophily, Myophily 
22. Chiropterophily, Ornithophily 


23. Melittophily, Ornithophily, Psy- 
cophily 


24. As above 
4 уе 
26. Melittophily, Psycophily 
27. Melittophily 
. As abov 
29. Melisteiptaly. Myophily, Phalae- 


nophily, Chiropterophily 
30. As above 


ЗТ. пона Myophily, Ornithophi- 
ly, Phalaenophily 


39. As above 
40. Melittophily, Ornithophily, Psy- 


41. As above 


42. As above 
43. As above 


. Pares Regali et al. (1974a, 1974b) 
. Kemp (1976) 
21. 


a) Crepet and Daghlian (unpubl. data) 
b) Trivedi and Verma (1971) 


. Jain (1963) 


. Koch and Friedrich (1971) 


. Reid and Chandler (1933) 
. Reid and Chandler (1933) 
. Crepet and Daghlian (198 1a) 


. Chandler (1961) 


28. Salard-Cheboldaeff (1975) 


. Reid and Chandler (1933) 


. Reid and Chandler (1933) 
. Reid and Chandler (1933) 
. Baksi (1972, 1973, 1974), Sah (1974) 
. Reid and Chandler (1933) 
. Reid and Chandler (1933) 


35. Reid and Chandler (1933) 


. Reid and Chandler (1933) 


37. Reid and Chandler (1933) 


. Krutzsch (1970) 

. Krutzsch (1970) 

. Daghlian (unpubl. data), ve (1930), 
81) 


Berry (1916), Daghlian (19 
ta) 


. Daghlian (unpubl. data 


. Muller (1968) 
. Elsik (1968) 


919 


Nadav) TVOINV.LOd ІУПОЅЅІИ JHL 30 STVNNV 


IL 10A] 


TABLE 1. 


(Continued). 


Floral Structural Features Related to 
Advanced Pollination Syndrome 


Typical Pollination Syndrome 


Literature Cited 


44. As above 44. As above 44. Crepet (unpubl. data) 
45. As above 45. As above 45. Adegoke et al. (1978) 
46. As above 46. As above 46. Elsik (1968) 
47. Asa 47. bove 47. Crepet (unpubl. data) 
48. Papilionaceous zygomorphic flowers 48. Melittophily 48. Crepet (unpubl. data) 
А above 49. As above 49. a) Mildenhall (1980) b) Harris (1974) 
50. As above 50. 50. Harris (1965a), Martin (1978) 
52. Flag-type, strongly irregular symme- 51. Melittophily 51. Doubinger and Chotin (1975) 
try 
52. Brush-type flowers 52. Ornithophily (some mice and small 52. Harris (1965a), Martin (1978), Stover 
marsupi and Partridge (1973) 
53. As above 53. As above 53. Martin (1978) 
54. As above 54. As above 54. Harris (1965a) 
55. As above 55. As above 55. Harris (1965b) 
56. As above 56. As above 56. Stover and Partridge (1973) 
Cretaceous 
Stage 
Maestrichtian 57. As above 57. As above 57. Crepet and Daghlian (1981a) 
oniacian 58. As above 58. As above 58. a) Bailey (1924), Webster (1967) 
b) Madel (1962) 
Maestrichtian 59. As above 59. As above 59. Van Campo (1963), Krutzsch (1969) 
Santonian 60. As above 60. As above 60. Boltenhagen (1976a, 1976b) 
Maestrichtian 61. As above 61. As above 61. a) Chmura (1973) 
b) Pares Regali et al. (1974a, 1974b) 
Maestrichtian 62. As above 62. As above 62. Chmura (1973), Germeraad et al. 
09 (1968), Couper (1960) 
Maestrichtian 63. As above 63. As above 63. Chmura (1973), Germeraad et al. 
| (1968), Couper (1960) 
Upper Senonian 64. As above 64. As above 64. Chmura (1973), Germeraad et al. 
(1968), Couper (1960) 
Lower Senonian 65. As above 65. As above 65. a) Belsky et al. (1965), Boltenhagen 
1976b) b) Vinkatachala and Sharma 
uos (1974 
Maestrichtian 66. As above 66. As above 66. Hickey and Peterson (1978) 


* Subclasses are arranged alphabetically within each geologic time unit; their position within that unit is not indicative of their order of appearance. 


NOI.LVNITIOd .LOS3SNI —.Lddd?1O [7861 


119 


618 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


` 
ЕА 
Zi 
Фр: ھر‎ 


FIGURES 2-5. 2. Brush blossom. x 2.5. UCPC (University of Connecticut Paleobotanical Collection) BS 
3-5. Eomimosoidea plumosa. —3. айыны О note the floral envelopes (fl), style and stigma (s), stame доре 
UCPC H45.—4. Fl v ой б 
(fl), the stamens (st), and that the carpel is hairy. x 7. UCPC W29.—5. Scanning electron micrograP ph of 
of tricolporate pollen grains. x 2,500. gu 


1984] CREPET—INSECT POLLINATION 619 


FIGURES 6-9. 6. Flower we seven-parted sympetalous corolla. Note the compressed ring of anthers (a). 
х3.2. UCPC Ma322. — 7. Scan ing electron micrograph of pollen (when argui Pistillipollenites о) 
€ from the flower зари | in Figure 6. Note the gemmate proces x 3,180. —8. Transmiss 


lipollenites macgregorii is known to extend into 

e Maestrichtian, suggesting that a pollination 
syndrome associated with bee pollination and, 
therefore, bees existed at that time. Surprisingly 
advanced Maestrichtian floral morphology may 
be an indication that bee pollination existed pre- 


Seely where lepidopteran pollination is also 
Соттоп (Weaver, 1972). 
Pollen is Particularly important because its 
unique nature makes its occurrence a reliable 
indication that the same taxon and thus, floral 
Structure, is involved whenever it occurs. Pistil- 


620 


vious to that time. Pollen morphology provides 
additional corroboration for this assumption. 
Pollen with ornamentation similar to that of P. 
macgregorii is found in four extant taxa (No- 
wicke & Skvarla, 1974; Nilsson, 1970; Poole, 
1981). In two of these families (Gentianaceae, 
Euphorbiaceae), variation in pollen is sufficiently 
well known that the sequence of evolution lead- 
ing to gemmate pollen can be reconstructed C Ж 
Nilsson, 1970). In each case gemmate, intectate 
pollen results from a breakdown of the muri of 
reticulate pollen accompanied by the elaboration 
of the tectum in localized areas. The progession 
suggests that gemmate pollen is a derived type 
and likely to be the end product of an evolu- 
tionary lineage; possibly one that originated pre- 
vious to the Maestrichtian. 

Sympetalous, funnelform-salverform flowers 
ofas yet unknown affinities that have floral tubes 
narrow enough to suggest lepidopteran pollina- 
tion (Figs. 9, 10) exist in Middle Eocene sedi- 
ments of both the Green River Formation and 
the Claiborne Formation. In these cases the flow- 
ers also appear to be radially symmetrical, sug- 
gesting probable butterfly, as opposed to moth, 
pollination. 

Zingiberidae. The taxa composing the Zin- 
giberidae are remarkable for their often radical 
zygomorphy and their adaptations to a variety 
of advanced pollinators, including bees. Despite 
the derived nature of the flowers of this taxon, 
the Zingiberidae seem to be remarkably ad- 
vanced by the Eocene. Fruits provide some of 
the most compelling data on the status of the 
group at this time. The Musaceae have been re- 
ported from the Eocene Deccan Intertrappean 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог, 71 


One of the most exciting recent developments 
relating to monocot history has been the discov- 
ery of zingiberalean leaves of Maestrichtian age. 
These are well documented and suggest the pres- 
ence of highly advanced pollination syndromes 
during the Maestrichtian (Hickey & Peterson, 
1978). 

Euphorbiaceae. The Euphorbiaceae are one 
of the largest families of flowering plants and one 
in which diversity has been associated with ad- 
aptation to a wide range of insect pollinators 
(Stebbins, 1981). The state of the Euphorbiaceae 
by the Middle Eocene is a good indication of the 
rapidity of radiation of pollination mechanisms 
associated with insect pollination. The number 
of discrete fossil euphorbiaceans is small, but 
their nature makes it possible to infer something 
of the history of the family. Fruit and flower 
fossils of Middle Eocene age reveal that one of 
the most advanced tribes of the Euphorbiaceae, 
rse and essentially 


by Manchester and Dilcher (1979) suggest that 
taxa similar to the hippomanean genera p 
pomane and Hura were extant at that time. In- 
florescences provide corroboration that this ех- 
tremely derived tribe was modern by the Middle 
Eocene (Crepet & Daghlian, 1981b). Inflores 
cences were preserved at two ontogenetic stages: 


has striate muri. Inflorescence, cymule, and 
len morphology are similar to those of the pos 
Gymnanthes and Senefeldera in the Hippo™ of 
(Crepet & Daghlian, 1981b). The apponi à 
such modern taxa by the Eocene suggests pe by 
lier origin for the family. This is $0ррог" 6 
reliable reports of Cretaceous woods 1967) 
those of certain modern genera (W eben гоб 
and by recently discovered Paleocene ‘alll 
manean inflorescences (Crepet, unpubl. in 
What is known of the history of the "e 
biaceae gives the general impression (cons! 
with other paleobotanical data) that there 


EEE EEE a 


1984] 


Ficures 10-13. 


CREPET—INSECT POLLINATION 621 


10. Another type of flower with a narrow corolla tube. x3. UCPC G399.—11. Flower of 
20.—12. Part of an imma nflorescence of Hippomaneoidea. чое dua cup- 
у х inflo- 


beridae. x 2.3. UCPC 520.—12. Part o ture in 
shaped bract (b) and the anthers (a) desig from =, bract. х7.75. are dion 13. Am 


ce of Hippomaneoidea showing the 


622 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


есте ра ) У 
Аб 


— 


М 

2 ay 

> Ls ^ 
= 


: ded 
: * ; храп 
FIGURES 14-16. Hippomaneoidea. — 14. Higher magnification view of UCPC W55 showing dee cymule 
cymules— one compressed laterally and one compressed in face view. Note that the laterally comp 


is com 
isolated from UCPC W55. x2 500.— 


relatively early (Upper Cretaceous— early Paleo- 
gene) radiation associated with insect pollina- 
tors. 


SUMMARY OF PALEOBOTANICAL EvIDENCE 


Evidence based on carefully investigated organ 
taxa including flowers and inflorescences sug- 
gests that families with pollination syndromes 
reflective of pollination by Apoidea and Lepi- 
doptera existed by the Middle Eocene. Such ad- 
vancement indicates an earlier radiation of 
pollination mechanisms involving faithful pol- 
linators. The earlier Paleogene and Upper Cre- 
taceous records are consistent with this possi- 
bility (Table 1) and the nature of pollination 
syndromes associated with families that occur 
during the Maestrichtian suggests that co-evo- 


| à f pollen 
posed of at least three florets (f) of 3-4 anthers each. x 16.— 15. Scanning electron micrograph of po 


: . C 
; ,500. . Transmission electron micrograph of pollen isolated from U 
illustrating the tectate-columellate wall structure. x4,800 


PC W55 


PRESS ER Behe 


erms and 
lutionar I up i 
faithful Роне began at an earlier ps "e 
risky to suggest that the appearance of a e 
vanced taxon at a given time implies a тг + 
previous history. The projection of poe 
models into geologic time by Eldredge and nsis- 
(punctuated equilibria, 1972) and their со E 
tency with angiosperm reproductive ec in- 
the angiosperm fossil record (Crepet, * ces 0 
troduces the possibility that the appearan i 
relatively modern syndromes at p eric rior 
are the culminations of events initiated ae 
to their appearances in the fossil record. intef- 
theless, the complexity of plant-pollina aa p in 
actions and the involvement of n ШЫ 
their origin do suggest that advanced po! super” 
at least at higher taxonomic e earlier 
family Apoidea, may even have exist 


a 


1984] 


than the uppermost Cretaceous, even if their 
evolution proceeded as in the punctuated equi- 
libria model. 


EVOLUTIONARY HISTORY OF 
FAITHFUL POLLINATORS 


The two most important groups of pollinators 
in terms of promotion of speciation are the Apoi- 
dea, and to a slightly lesser degree, Lepidoptera. 
The discussion of advanced pollinators is con- 
sequently directed primarily toward these two 
groups. Coleoptera and Diptera are certainly im- 
м рч 112 1 PES ы ® 4L Ра X ` 


associated with heightened promotion of specia- 
tion events. Both orders were well developed 
during the entire Mesozoic, especially the Co- 
leoptera, and perhaps both were important in the 
establishment of basic angiosperm floral fea- 
tures. They undoubtedly contributed to Early 
Cretaceous radiation and spread of the angio- 
sperms. Birds and bats are also important pol- 
linators; however, they are not numerically as 
significant as insects, and birds tend to be pro- 
mıscuous pollinators (Stiles, 1981), while fidelity 
in bats is poorly understood (Koopman, 1981). 
However the history of bats and birds suggests 
that neither were important pollinators until late 
Paleogene times (see review by Tiffney, 1984). 


APOIDEA 


It is interesting to examine data on the pattern 
ofevolution ofthe Apoidea and to contrast these 
With the inferences obtained from the fossil rec- 
ord of plants. Although the most obvious place 
to begin is the fossil record of bees, that record 
is limited and most insights into the pattern of 
their radiation have been gained from a careful 
consideration of biogeography in light of their 
neontological features, including behavior, level 
of sociality, nesting habits, etc. (Michener, 1979). 

The earliest record of fossil bees is either Eocene 
ог Oligocene depending on the interpretation of 
the age of the Baltic amber. A diversity of fossil 

кй from various localities occurs at the same 
time including derived and ancestral tribes and 
subfamilies (by the Oligocene the Halictinae, An- 
“reninae, Ctenoplectrinae, Melittinae, Anthidi- 


5 
£ 
© 
= 
5 


wn 
(Michener, 1979). The presence of two of the four 
tribes of the Apidae by the Oligocene, including 
Опе of the two most highly derived tribes of ex- 
tant bees (the Apini and Meliponini) is an in- 


CREPET —INSECT POLLINATION 


623 


dication that bee origin may have occurred con- 
siderably earlier than the Oligocene. Certainly, 
the known fossils do not help to unravel the pat- 
tern of evolution in bees. The strongest evidence 
related to the antiquity of the Apoidea comes 
from the interpretation of their disjunct distri- 
butions. 

Michener (1979) noted that the distributions 
of most present day bees are probably the result 
of slow spreading over continents and presently 
moderate barriers, since most bees are not good 
dispersers. Most bees do not fly during bad 
weather, so they are not likely to be dispersed by 
storm winds and most bees have a tendency to 
return to their nesting sites. Dispersal is even 
more restricted in highly social bees due to their 


ments or by dispersal across oceans at a time 

when they were relatively narrow. 

The Colletidae. The Colletidae are a family 
4 124 1 д 244 * | 


af chort-t 
OL эпо А, 
a me с E г 44 


tological grounds (important primitive features 
include bifid glossae similar to those of the sphe- 
cid wasps and methods of carrying pollen, i.e., 
in the crop in two subfamilies (Hylaeinae and 
Euryglossinae) rather than on body hairs or more 
specialized structures (scopae; Michener, 1979; 
Thorp, 1979)). One tribe in particular has a dis- 
tribution most easily accounted for by continen- 
tal movements—the Paracolletini. These are 
presently restricted to temperate parts of three 
southern continents (Australia, Africa, and South 
America). Michener (1979) suggested that this 
disjunction may extend to the Upper Cretaceous 
when oceanic gaps were narrower. The colletids 
are an unusual family of bees inasmuch as in 


presence of myrtaceous pollen in the Santonian 
(Table 1) supports Michener’s suggestion. 

The Fideliidae. The most primitive family of 
long-tongued bees, the Fideliidae, are closely re- 
lated to the Megacheilidae (they are apparently 
sister groups, Michener, 1974). They are ground- 
nesters and particularly poor candidates for dis- 
persal for that reason (i.e., flotation is out as a 
means of dispersal). Two species live in arid 
western South Africa and one is native to arid 
central Chile. Michener (1979) pointed out that 
the last direct migration route was closed in the 


624 


lower Upper Cretaceous and that it would have 
been inaccessible to these bees anyway, because 
it was through the tropics. He concluded that the 
family had a distribution during the Upper Cre- 
taceous and dispersed across oceans that were 
narrower than at present. 

The Meliponini. One of the most important 
indicators of apoidean antiquity is the present 
distribution of the Meliponini. They are partic- 
ularly important due to their phylog ic status, 
their degree of eusociality, and their inability to 
disperse. The best biogeographical evidence in- 
volves the subgenera of the genus Trigona (Mich- 
ener, 1979). The Meliponini are as highly social 
as the Apini, and, together with the Apini, rep- 
resent the most derived bees. The discovery of 
a genus as modern as Trigona in the Upper 
Eocene-Oligocene Baltic amber suggests an ear- 
lier origin for the family. In fact, the distribution 
of the modern subgenera of Trigona is explicable 
only by a mid-Upper Cretaceous origin of the 
subgenera. Before considering the details of their 
distribution, it is instructive to examine the fea- 
tures that make the Meliponini particularly bad 
dispersers. As highly eusocial bees, they are dis- 
persed by swarms and not individuals. Swarms 
are so highly organized that Michener (1979) 
considered it impossible for them to cross sizable 
bodies of water. Even the pattern of swarming 
mitigates against dispersal. Individuals from a 
parent colony go back and forth to provision the 
new nest before the queen migrates. The appar- 
ent isolation of species and subspecies in Brazil 
by rivers (Michener, 1979), and the absence of 
meliponines from the Antilles, even though these 
islands are relatively close to major continental 
populations, represent good evidence for their 
lack of dispersability. 

Despite these difficulties, the genus Trigona is 
worldwide in its distribution with similarities 
at the subgeneric level between South American 
taxa and those of all other southern continents 
except Antarctica. There are three disjunctions 
in poorly dispersing subgenera as follows: 


Plebeia: found in American tropics, Australia, 
and New Guinea. 

Tetragona: American tropics, the oriental re- 
gion, and Australia. 

Hypotrigona-Trigonisca: American tropics, Af- 


rica, and the oriental region. 


In view of their inability to traverse even rath- 
er insignificant bodies of water, Michener (1979) 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


proposed that the principal subgenera of Trigona 
originated in the Middle or Upper Cretaceous 
when Africa and South America were joined or 
not yet widely separated at tropical latitudes. 


LEPIDOPTERA 


The fossil record of the Lepidoptera is better 
than that of the Apoidea, but it is still far from 
complete. Nonetheless, certain important as- 
pects of the history of the Lepidoptera are evi- 
dent from the fossil record. 

The first reliable report of the Lepidoptera is 
based on several moths preserved whole in 100- 
130 Ma amber. These are related to the extant 
Micropterigidae (Lepidoptera, Zeugloptera; 
Whalley, 1977). Even though these fossils are the 
first evidence of the Lepidoptera, they are well 
defined micropterigids and are similar to the 
modern genus Sabatinca. Whalley (1977) pro- 
posed an origin for the Lepidoptera in the Ju- 
rassic based on the specialized nature of these 
fossils. Micropterigids are considered to be an- 
cestral based on neontological features (Com- 
mon, 1975) and are interesting! they have 
well-developed mandibles and no proboscis. 
Thus, it appears that the earliest lepidopterans 
were pollen feeders, if not predacious, and not 
nectar feeders. 

There are several other reports of Cretaceous 
Lepidoptera in amber. One is of the head of a 
ditrysian larva from 73 Ma, another is of и 
cropterigid scales from 100 Ma (Mackay, 1977; 
Kühne et al., 1973). In general, reports of Cre- 
taceous Lepidoptera are rare, but what infor- 
Bataa: Hah] ӨР 4 their tim 


of origin and degree of diversification (Monotry- 
sia and Ditrysia are differentiated by the Uppe" 
Cretaceous). 

A variety of fossil lepidopterans are know? 
from the Paleogene, including one monotrysia? 
moth, 41 ditrysian moths, and 27 butterflies 
(Durden & Rose, 1978). Perhaps the most 12" 
teresting of these are three papilionid butterflies 
known from the Middle Eocene Green Rivet 
Shale. 

A variety of ler p ё 
the later Tertiary and most are similar to 
modern counterparts (Common, 1975). Co™ 
mon (1975), in his review of the fossil rocon d 
the Lepidoptera, concluded that the haustella : 
Lepidoptera were well established in the Cret 
ceous and that it is likely that the simple pro" 
boscis had evolved by the time angiosperms ap 


wn from 


“4 i 1, 


-——-— 


EEE EO ÉÁHÁÁÁ—"——— — m 


1984] 


peared. He further assumed that the radiation of 
ditrysian forms paralleled that of the angio- 
sperms. These seem to be reasonable assump- 
tions based on the fossil record. Lepidoptera oc- 
cur relatively early and ditrysian forms (1.е., 
usually with a proboscis) occur at least by 73 Ma. 
Further, a variety of Lepidoptera are present in 
the Paleogene, including the highly specialized 


vanced lepidopteran pollinators were available 
during the Upper Cretaceous. 


PATTERNS OF ANGIOSPERM DIVERSIFICATION 


The tempo of angiosperm diversification is an 
essential datum in assessing the possibility of a 
relationship between advanced faithful pollina- 
tors and angiosperm diversity. Until recently 
(Niklas et al., 1980; Muller, 1981; Tiffney, 1981), 
there has been no really rigorous attempt to chart 

heco печете Т. сс а 
tions that angiosperms arose de novo as modern 
taxa and almost instantaneously became domi- 
nant have been debunked by Doyle and Hickey 
(1976), but the angiosperms have been consid- 
ered generally to be dominant worldwide by the 

od 


sn in the literature as part of their general 
ама of patterns of diversification in vascular 
Plants. The results suggest that angiosperm di- 
versity 1 2 at 1 1 4 . +. 


4 4. 45 
AHU осама 


slowly g 
Nun Cretaceous with angiosperms becoming 
RS y Een during the Upper Cretaceous 
над Ieving world dominance by the upper- 
1980) ^c or Early Tertiary (Niklas et al., 
dd xy provide a well thought out discus- 
п defending their use of fossil species as the 
dum for their diversity curves, and in context 
а al., 1980), species аге clearly the fossil 
ih choice. One of the justifications for using 
tivity ve Involves inherently greater subjec- 
ма. ај designation of higher taxonomic 
| tenis 15 may be true for higher taxonomic 
dni at are extinct and it is certainly true in 
taxa, but with fossil angiosperms there are 
reasons why higher taxonomic levels, particu- 


in d can be identified with great confidence 
€ fossil record. This provides an element of 


CREPET—INSECT POLLINATION 


625 


a eet PR esso E 
reliability g 
dundancy associated with the use of form taxa. 
Second, the biological validity of angiosperm 
families can be assessed on the basis of neon- 
tological data, since these families exist in the 
present as well as in the past. Third, using 
appearances of families as indices of diversity 
minimizes aberrations that might be associated 
with having relatively few megafossil localities 
at certain times. Finally, dominant angiosperm 
diversity is the result, not only of having certain 
ly | famili d , but predom- 


extremely B! g 

inantly, of having a great number of families. In 

fact, the average number of species/family in the 
H . nl LIP EQ E 2 Hf 


ily ratio in gymnosperms (Stebbins, 1981). Thus, 
rate of appearances of families is a reasonable 
index of angiosperm diversification. Naturally, 
it is a compromise inasmuch as some diversity 
is masked, especially diversity preceding the 
origination of modern families. 

Muller recently provided an account of the 
diversification pattern of angiosperm families 
based on his analysis of the palynological liter- 
ature (1981). Muller's analysis is attractive be- 
cause criteria for accepting or rejecting data on 
the occurrences of particular families are clearly 
discussed and because pollen has proven taxo- 
nomic value. Muller's analysis (1981) parallels 
that of Niklas et al. (1980) in illustrating a steady 
rise in total angiosperm diversity during most of 
the Cretaceous, but reveals a slightly earlier 
(Campanian) and more dramatic peak in diver- 
sification that reaches a maximum during the 
Maestrichtian and extends into the Paleogene. 
Interestingly, diversification patterns for orders 
and superorders, which would presumably in- 
clude most angiosperms left out in a consider- 
ation of only modern families, are very similar 

f di ification based on families 


alone (Muller, 1981). 

Both analyses of angiosperm diversity are 
valuable attempts to clarify a pattern that has 
been predominantly subjectively interpreted. 
Both have their strengths and weaknesses, but in 
each instance the major dramatic radiation of 
ngiosperms is revealed at a date later than has 
commonly been supposed. 


БУ 


SUMMARY OF DATA 
1. Families having flowers adapted for polli- 
nation by Apoidea and Lepidoptera probably ex- 
isted during the uppermost Cretaceous. The taxa 


626 


present at that time indicate a probability of ear- 
lier co-evolution of angiosperms with apoidean 
and lepidopteran pollinators. 

2. Rigorous analysis of the biogeography of 
bees suggests that at least three families of the 


Apidae were so well developed by that time that 
it is likely that three subgenera of the genus Tri- 
gona already existed. 

3. The fossil record of the Lepidoptera indi- 
cates an origin for the order previous to 100 Ma 
with both monotrysian and ditrysian forms pres- 
ent by the Upper Cretaceous. 

4. Angiosperm diversity increased steadily 
during the lower and part of the upper Creta- 
ceous. They may have commenced a major di- 
versification as early as the Campanian, but were 
certainly experiencing a major radiation by the 


uU 
Cretaceous-T eruary boundary 


the Tertiary. 


CONCLUSIONS 


It is not reasonable at the present time to at- 
tempt to attribute angiosperm success to any sin- 
gle characteristic. In fact, many of the features 
ofangiosperms that have been discussed by Steb- 
bins (1981), Burger (1981), and Mulcahy (1979) 
have undoubted significance in angiosperm su- 
premacy. Nonetheless, data on the progression 
of evolution of insect pollination mechanisms in 
angiosperms suggest that the inception of ad- 
vanced insect pollination syndromes was either 
coincident with, or just prior to, a major ra- 
diation of flowering plants. Advanced insect pol- 
lination can no longer be excluded on the basis 
of paleontological evidence from having partic- 
ipated in a major radiation of angiosperms. On 
the contrary, paleontological data are consistent 
with neontological evidence in suggesting an im- 
portant role for advanced insect pollinators in 

tablishing contemporary angi I diversity. 

There were undoubtedly several milestones in 
the evolution of angiosperm pollination mech- 
anisms during the Cretaceous and Paleogene oth- 
er than the appearance of advanced faithful pol- 
linators, and these also must have affected 
angiosperm diversity. What can be inferred from 
the fossil record at the present time suggests the 
following sequence of events in the evolution of 
angiosperm pollination mechanisms: 

l. The origin of insect pollination. Angio- 
sperm origin involved co-evolution with insect 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


pollinators (dipteran or coleopteran) that result- 
ed in the ancestral angiosperm flower. The first 
angiosperms had features conducive to success- 
ful radiation, including a truncated life cycle, en- 
closed ovules, insect pollination, and gameto- 
phytic competition (Stebbins, 1981; 
Hickey, 1976; Burger, 1981). Evidence for the 
early predomi f coleopt /dipt pol 
lination in angiosperms is provided by the fossil 
record, which illustrates the existence of all ma- 
jor magnoliidan pollen types during the Aptian/ 
Albian (Zavada, unpubl. data). 

uring the mid-Cretaceous, wind pollina- 
tion evolved in angiosperms possibly as a result 
of the combination of seasonally dry tropical- 
subtropical environments and competition for 
insect pollinators (Whitehead, 1969; Crepet, 
1981). These taxa were pre-adapted to invade 
subsequent appropriate habitats, including those 
created by climatic decay. 

3. The appearance of advanced faithful insect 
pollinators in the Upper Cretaceous/Paleogene. 

4. The origin of bat and bird pollinators. These 
pollen vectors probably became significant no 
earlier than the mid-Paleogene (e.g., Stiles, 1981; 
Koopman, 1981; Tiffney, 1984) and, while cer- 
tainly contributing to angiosperm diversity by 
increasing the adaptive sp iated with an 
imal pollination, they are not as significant nu- 
merically as insect pollinators. 

5. Finally, the ultimate refinements of the spè- 
cific plant-pollinator interaction (e.g. the Or- 
chidaceae) and of the non-specific plant polli- 
nator interaction (e.g., the Compositae; Proctor, 
1978). These alternative developments must have 
occurred late in the Tertiary, but there is little 
germane fossil evidence at this time. 


. 1 e 
seed dispersal vectors were of utmost impo pur 
. . WO + з iff tion du 


the uppermost Cretaceous-Lower Teri КЕ 
mainsa viabl d iting p йн | 
sider the present chapter in conjunction with ; 

of Tiffney, 1984). Animal dispersal maxim!" 
the probability that, given a heterogeneous "€ 
restrial biospace, a small population will be ко 


— 


пи 


LE ATT 


1984] 


lated in a new environment (Tiffney, 1984; see 
discussion also by Vrba, 1980, fig. 1C). Constant 
pollinators, stochastic floral change, and animal 
seed dispersal vectors may interact in a variety 
of ways to further promote speciation (Fig. 1A- 
C). Because these elements of angiosperm repro- 
ductive biology are conducive to the stochastic 
isolation of small populations and because of the 
apparent importance of stasis in angiosperm his- 
tory (Crepet, unpubl. data), I consider the punc- 
tuated equilibrium model of evolution to have 
merit with regard to the angiosperms. Differ- 
ences in the timing of events; i.e., the coincidence 
of the appearance of advanced insect pollination 
mechanisms with the onset of the major angio- 
sperm radiation during the Campanian accord- 
ing to Muller (1981), versus a slightly later date 
for maximal angiosperm diversification as re- 
ported by Niklas et al. (1980) and Tiffney (1981), 
are probably not significant given the constraints 
imposed by the degree of resolution presently 
ayain bio from the fossil record. What is impor- 


41 ба 311 
па ЈУ 


о data do show an ` uppermost Cretaceous- 
Early Tertiary and not an earlier peak in angio- 
Sperm diversification rate. 

It now appears that the inception of advanced 
pollination mechanisms preceded widespread 


Suggest advanced insect pollination alone might 

ve been responsible for the onset of a major 
angiosperm radiation while synergism with an- 
imal seed dispersal vectors became an important 
factor at a slightly later time. 


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Volume 70, No. 4, pp. 577- 
October 1984. 


Volume 71, No. 1, pp. 1 
December 1984. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


WHITEHEAD, D. R. 1969. Wind pollination in the 
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924—933 


; 9 
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Contents continued from front cover 


Cuticle Evolution in Early Cretaceous Angiosperms from the Potomac Group 
of Virginia and Maryland Garland R. Upchurch, Jr. 
Seed Size, Dispersal Syndromes, and the Rise of the Angiosperms: Evidence 
and Hypothesis Bruce H. Tiffney 
New Paleobotanical Data on Origin and Early Evolution of Angiospermy 
Valentin A. Krassilov 
Mesosperm Palynologic Evidence and Ancestors of Angiosperms Nor- 
man F. Hughes 
Flowers from the Eocene Oil- Shale of Messel: A Preliminary Report 
Friedemann Schaarschmidt ... 
Advanced (Constant) Insect Pollination Mechamisms: Pattern of Evolu- 


322 


551 


tion and Implications Vis-à-Vis Angiosperm Diversity William L. 
607 


Crepet .. ЫЕ 


\NNALS 


SOURI BOTANICAL GARDEN 


UME 71 1984 NUMBER 3 


j Џ 


< m E 
y TER . ү 
Grove) do ^s "aro t 
"mi «охда i 
С Quite, | 
шона EARLY МАР ОЕ GARDEN 


APR 2 5 198 


CONTENTS 
GARDEN LIBRAM 

The Order Myrtales: A Symposium Peter H. Raven 631 
The Order Myrtales: Circumscription, Variation, and Relationships Rolf 

Dahlgren & Robert F. Thorne _____-- 633 
Myrtales and deine ae Phylogenetic Analysis L. A. 8. Johnson & 

B. G. Brigg = 700 
Alzateaceae, a cm Family of Myrtales in die Adijerican Tropics X Shirley 

А. Graham ا‎ (e y 


A Commentary on the Definition ofthe Onder Милка Arthur Cronquist 780 
Wood Anatomy and Classification of the Myrtales Ger J. C. M. van 


КШ & Pile te le 783 
Leaf Histology and Its Contribution to невине in the UM 
Richard C. Keating асе awn WH 


Ultrastructure of Sieve-element Plastids „ Myrtales а d Allied а 
H.-Dietmar Behnke ОЕА 8 


Contents continued on back cover 


аьло дарн... DUE I E ER, 
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ANNALS 


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MISSOURI BOTANICAL GARDEN 


VOLUME 71 


1984 


NUMBER 3 


THE ORDER MYRTALES: A SYMPOSIUM 


PETER H. RAVEN! 


This symposium was held at the XIII Inter- 
national Botanical Congress, Sydney, Australia, 
21-28 August 1981. Much development of the 
material was carried out subsequent to the Con- 
gress, and some of the papers published here 
have been added to round out the picture of the 
Overall group. 

z concensus of the participants in the sym- 

um, Myrtales are a clearly defined group in- 
Чы the following families and subfamilies: 


Onagraceae 

Trapaceae 

Lythraceae subfam. Lythroideae 
ubf: 


subfam. Punicoideae 
Oliniaceae 
Combretaceae subfam. Combretoideae 
ubfam. Strephonematoideae 
Alzateaceae 
Rhynchocalycaceae 
ceae 


Heteropyxidaceae 
Myrtaceae 


Concerning differences in the delimitation of 
these groups, the following points are pertinent. 


Memecylaceae are regarded as a subfamily of 
Melastomataceae by R. F. Thorne, and Prernan- 
dra is apparently intermediate between these two 
groups. Р ach 
with a single genus, are considered ин 
of Myrtaceae by Thorne. They clearly are most 
closely related to that family, constituting with 
it a distinctive early offshoot within the order 
Strephonema might be segregated as a distinct 
family on the basis of several features, but clearly 
is more closely related to the other genera of 


Despite the many distinctive features that dis- 
tinguish it from Myrtales and link it with Eu- 
phorbiaceae, Cronquist includes Thymelaeaceae 
in Myrtales; his point of view is apparently unique 
among students of the order and participants in 
this symposium. Contemporary systematists who 
have considered the order Myrtales, Thymelae- 
aceae, and Euphorbiaceae from many points of 
view apparently agree unanimously, with the ex- 
ception of Cronquist, in grouping the last two 
families and not linking them with Myrtales. 

With the single exception just reviewed, no 
participant in the symposium argued for the in- 
clusion of any family in the order Myrtales other 
than those listed above, and none have suggested 
that any of these families ought to be excluded 


' Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166. 


ANN. MISSOURI Вот. GARD. 71: 631-632. 1984. 


632 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог, 71 


from the order. In fact, there is no convincing 
case even for a relatively close relationship be- 
tween the order Myrtales, as here defined, and 
any other family of plants. Consequently, Myr- 
tales may be regarded as a highly distinctive 


group, one of the most clearly delimited of all 
orders of angiosperms. 

The organization and coordination of this 
symposium were assisted by a grant from the 
U.S. National Science Foundation. 


THE ORDER MYRTALES: CIRCUMSCRIPTION, 
VARIATION, AND RELATIONSHIPS! 


ROLF DAHLGREN? AND ROBERT F. THORNE? 


ABSTRACT 


yy РЕА До 1 ftl 1 


The соге families are p Mo Lythraceae, Oliniaceae, Combret taceae, Alzateaceae, 
Rhynchocalycaceae, debeam Сг rypt е roniaceae, Melastomataceae, Memec ylaceae, Psiloxylaceae, 


e form 


Heteropyxidaceae, and Myrtaceae 
two somewhat 


t peripheral groups within ‘the order. Alzateaceae and “Rhynchocalpeaea are newly 
n Lythra 


e. Cryp sii 


ee at the familial leve 


grammatically. 


on for this are given. The distribution of a numbe 
attributes in = aforementioned families are е discussed, and som 


e distributions are illustrated aii- 
, foliar sclereids, phyllotaxy, stipular structures, 


merous condi m ons of perianth, inferior versus superio or ovary plac 
ns, anther connectives, Pollen pseudocolpi, embryology, seed coat 


fra opmental succession of stamen 
truc che 


J 


ment, floral tube, pleiomery and 


mistry „etc 


her 


h Myrtale 
are iiss considered. The Myrtales show affinities to Rosales, and fewer ones to Gentianales, Колы, 


and possibly Theales 


CIRCUMSCRIPTION OF MYRTALES IN SOME 
CURRENT SYSTEMS OF CLASSIFICATION 


The historical background of the order Myr- 
tales will not be outlined here. We shall restrict 
ourselves to the circumscription of the order in 
the following classifications: Emberger (1960), 
Melchior (1964), Soó (1967), Hutchinson (1926, 
1959, 1973), Thorne (1968, 1976, 1981), Cron- 
quist (1968, 1981), Takhtajan (1969, 1980), 
Stebbins (1974), Dahlgren (1975a, 19802), and 
Briggs and Johnson (1979). 

Emberger (1960) included in this order: Ly- 
thraceae, Crypteroniaceae, Heteropyxidaceae, 
Sonneratiaceae, Punicaceae, Rhizophoraceae, 


сеае"), and Guns and, as annex families, 
added Hippuridaceae, Callitrichaceae, and Di- 
alypetalanthaceae. Penaeaceae and Oliniaceae 
were placed in the adjacent order Thymelaeales, 


Pirna. E 


Dr. Peter 


ANN. MISSOURI Bor. GARD. 71: 633-699. 1984. 


which also included Thymelaeaceae, Geissolo- 
mataceae, and Elaeagnaceae. 
wide circumscription may be taken as a 


tales and to exclude Hippuridaceae and Gun- 
(i ch th d from 


Haloragaceae), and also to exclude Lecythida- 
ceae, Rhizophoraceae, and Haloragaceae sensu 
stricto. Dial lant} | ti | 


very loosely attached to the order. Trapaceae are 
usually included in Myrtales and Heteropyxi- 
daceae have usually been included in Myrtaceae, 
whereas, Psiloxylaceae are a recent addition to 
the Myrtaceae. Other later systems usually do 
not deviate greatly from this pattern 

In Melchior’s (1964) edition of Engler’s *Syl- 
labus der Pflanzenfamilien,” the following fam- 
ilies are included in the order: Lythraceae, Tra- 
paceae, Crypteroniaceae, Myrtaceae (incl. 


pum. A. 


mprovements а new 


nhagen, Den sirig 


634 


Heteropyxidaceae), Dialypetalanthaceae, Son- 
neratiaceae, Punicaceae, Lecythidaceae, Melas- 
tomataceae, Rhizophoraceae, Combreta 
Onagraceae, Oliniaceae, Haloragaceae (incl. 
Gunneraceae), and Theligonaceae, and in sepa- 
rate suborders Hippuridaceae and Cynomori- 
aceae. Inclusion of the last-mentioned familiy 
has gained no support. Penaeaceae, as in Em- 
berger’s (1960) classification, were placed in 
Thymelaeales, as were also Geissolomataceae, 
Dichapetalaceae, and Elaeagnaceae. 

Soó (1967, 1975) subdivided his order Myrt- 
ales into three suborders: Myrtineae, with 


Haloragineae, with Haloragaceae, Gunneraceae, 
and Hippuridaceae. Crypteroniaceae were omit- 
ted, and Penaeaceae were included in Thyme- 
laeales. 

Hutchinson (1926) in the first edition of his 
"Families of Flowering Plants" placed the fam- 
ilies Lythraceae, Crypteroniaceae, Sonnerati- 
aceae, Punicaceae, Oliniaceae, Onagraceae, Hal- 
oragaceae (including Gunnera and Hippuris), and 
Callitrichaceae in a separate order Lythrales; and 
Myrtaceae, Lecythidaceae, Melastomataceae, 
Combretaceae, and Rhizophoraceae in another 
order, Myrtales. These orders were at least partly 
distinguished by being chiefly herbaceous or 
chiefly woody, respectively, although this dis- 
tinction had to involve many exceptions. 

In the second edition of the same work (Hutch- 
inson, 1959), with the same basic principle of 
division, the chiefly herbaceous Lythrales were 
restricted to Lythraceae, Onagraceae, Trapaceae 


~ 


сеае. Crypteroniaceae and Oliniaceae in that edi- 
tion were placed in Cunoniales and Penaeaceae 
in Thymelaeales. It is obvious that Hutchinson’s 
strict adherence to the division of herbaceous 
versus woody plants has resulted in a less natural 
classification. 

In the third edition of the same work, Hutch- 
inson (1973) presented a new classification, in 
which an extended woody order Myrtales in- 
cluded Myrtaceae, Barringtoniaceae, Anisophyl- 
leaceae, Sonneratiaceae, Lythraceae, Rhizo- 
phoraceae, Lecythidaceae, Combretaceae 
Punicaceae, Napoleonaceae, and Melastomata 


~ 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


ceae. Crypteroniaceae and Oliniaceae were re- 
tained in Cunoniales and Penaeaceae in Thy- 
melaeales. The herbaceous order Onagrales was 
there restricted to Onagraceae, Trapaceae, Hal- 
oragaceae (incl. Hippuris and Gunnera), and Cal- 
litrichaceae; whereas Dialvpetalanthaceae were 
placed beside Rubiaceae in Rubiales, a very rea- 
sonable position in the light of some of its attri- 


utes. 

Thorne (1968, 1976, 1981) by preference has 
wider ordinal and familial concepts. He restricts 
the superorder Myrtiflorae to the Myrtales, in 
which he now treats Lythraceae (incl. Punicoi- 
deae and Sonneratioideae), Penaeaceae, Olini- 
aceae, Trapaceae, Crypteroniaceae, Melasto- 
mataceae (incl. Memecyloideae), Combretaceae 


pl ideae), Myrtaceae (incl. Psi- 


(incl. St 
loxyloideae), and Onagraceae. In the 1976 ver- 
sion of his classification he had included Thyme- 
laeaceae in Myrtales, but in the latest treatment 
(Thorne, 1981) has returned Thymelaeaceae to 
Euphorbiales where he earlier (1968) had placed 
hem. These families comprise what we shall treat 
as the ‘core group’ of families in Myrtales. Thorne 
has placed Rhizophoraceae and Haloragaceae 1n 
separate suborders of Cornales, and, in all ver- 
sions of his classification has treated Lecythi- 
daceae in Theales as the separate suborder Le- 
cythidineae. He has included Dialypetalanthus 
among taxa incertae sedis, however, he now ге 
gards this genus as closely related to, or perhaps 


J 


[md 


approximately the same circumscriptic 
accepted by Thorne in 1976. Cronquist P 
Lecythidaceae in the separate order Lecythida 
and Haloragaceae, Hippuridaceae, Gunneraceae, 
and Theligonaceae in an order named Halora- 
gales. Further, Rhizophoraceae, as in Thorne? 
classification, were placed in Cornales, though 
Cronquist (1981) now prefers to treat RhiZo" 
phoraceae in their own order, Rhizophorales. 
In his classification of 1981, Cronquist pla : 
Dialypetalanthaceae in his Rosales, Thee 
ceae in Rubiales, and Hippuridaceae 11 Cal i: 
trichales, leaving Haloragaceae and Gunnera 
ceae in the order Haloragales. З 
Takhtajan (1959, 1966, 1969) included ee 
Myrtales Lythraceae, Sonneratiaceae, Pum! 


laced 
les, 


wp t EN nn ннн 


1984] DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 


ceae, Rhizophoraceae, Anisophylleaceae, Com- 


Cronquist, таз); Pakhtajan’ s Hippuridales 
= Hal Gunner- 
aceae, and Hippuridaceae and were placed next 
to Myrtales. Thymelaeales, with only Thyme- 
laeaceae, were placed in sequence with Euphor- 
biales and were not considered by Takhtajan as 
related to Myrtales. 

In a revised version of his angiosperm classi- 
fication, Takhtajan (1980) widened the circum- 
scription for his order Myrtales, which was di- 
vided into four suborders: Myrtineae, with the 
families of his order Myrtales from 1969 plus 
Crypteroniaceae; рон vies —€— 


and Lecythidineae, with Lecythidaceae eel l. As- 
teranthaceae, Barringtoniaceae, 
Napoleonaceae). This new ыыы ар- 
proaches closely that of Dahlgren (1980а); 
wherein, however, the Lecythidaceae are placed 
in Theales and the ordinal circumscription is 
slightly different. 

Stebbins (1974) basically followed Cronquist 
(1968), but did include Rhizophoraceae in Myr- 
tales. Like Cronquist, he treated Lecythidaceae 
in an order of their own. 

gren, in his classification of 1975a, gave 
Myrtales the following —— us Lythra- 
сеае (incl. Sonneratiaceae), Punicaceae, Rhizopho- 
гасеае (incl. Anisophylleaceae), E 
Combretaceae, Oliniaceae, Melastomataceae, 
Penaeaceae, Myrtaceae (incl. Heteropyxis), and 

паргасеае, and in this order also included Di- 
alypetalanthaceae, but remarked that the posi- 
tion of that family was uncertain. Trapaceae were 
excluded from the order as a consequence of the 
lack of endosperm formation and other details 
[but were reinstated in Myrtales in his later sys- 
tem (Dahlgren, 1980a; Dahlgren et al., 1981)]. 
Haloragaceae (excl. Hippuris and Gunnera) were 
treated in a separate order next to Myrtales, and 


cent to Euphorbiales. 

In the revised classification of 1980a, Dahlgren 
included in Myrtales the families Myrtaceae, Psi- 
loxylaceae, Oliniaceae, Melastomataceae, Pen- 


635 


aeaceae, Crypteroniaceae, Lythraceae, Sonnera- 
tiaceae, Punicaceae, Combretaceae, Onagraceae, 
and Trapaceae. Haloragaceae and Rhizophora- 
ceae were placed in separate orders next to Myr- 
tales in the Myrtiflorae; whereas, Anisophylle- 
aceae and ено with some 


reservations be possibly corn 
alean 

s and Johnson (1979) suggested a new 
classification of the former myrtalean families, 
distributing them in two orders, Myrtales sensu 
stricto and Lythrales, although these have widely 
different circumscriptions than have the corre- 
sponding orders in Hutchinson’s system of 1959. 
Myrtales sensu stricto of Briggs and Johnson in- 


according to them, are possibly related to Myrt- 

ales and Lythrales, and Rhizophoraceae are sus- 

pected to be heterogeneous with possibly a thea- 

lean affinity. Thymelaeales, in accordance with 

various previous authors, are believed to be al- 

lied to Euphorbiales and Malvales. Lecythid- 
1 elided and П: 1 1 1 


are regarded as gentianalean or rubialean (these 
orders are united in some systems). This classi- 
fication will be discussed further in this paper. 
Here, the order will be circumscribed largely 
as by Dahlgren (1980a), and by Thorne (1981), 
although the familial rank will be treated some- 
what differently. One of us (Dahlgren) prefers 
smaller, homogenous families and recognizes as 
many as 14 families [Onagraceae, Trapaceae, Ly- 
thraceae (incl. Punicaceae and Sonneratiaceae), 
Oliniaceae, Combretaceae, Alzateaceae, Penae- 


Memecylaceae, Melastomataceae, Psiloxyla- 
ceae, Heteropyxidaceae, and Myrta 
convenience this treatment will be used through- 
out this survey. Thorne, on the other hand, in- 
cludes Heteropyxidaceae and Psiloxylaceae in 
Myrtaceae and Memecylaceae in Melastomata- 
ceae. In all other respects, we are in agreement. 
DEFINITION OF THE ORDER 

Members are woody or herbaceous, terrestrial 
or rarely aquatic, ranging from huge trees to small 
annual herbs. The tap root is usually well de- 
veloped. 


636 


Vascular strands are bicollateral in all the fam- 
ilies and (as far as known) in nearly all species. 
Nodes are largely unilacunar (but trilacunar in 
Alzateaceae). Vessel elements have simple per- 
foration plates (or very rarely scalariform per- 
foration plates) and vestured pits (van Vliet, 
1978). (Internal phloem and vestured pitting in 
this order are extremely important and define 
the order along with other distinctive features.) 
Wood rays vary between uni- and pluriseriate 
(even within most families), are mostly to 3 cells 
wide, and heterocellular to homocellular; ray cells 
often have gummy deposits; some of the axial 
parenchyma in scattered families generally con- 
sisting of vertical crystalliferous strands (Cron- 
quist, 1981). Phloem of young twigs is often 
tangentially stratified into hard and soft layers. 
Sieve-tube plastids accumulate starch but never 
protein. 

Leaves are typically opposite but quite often 
alternate, rarely verticillate, simple, either peti- 
olate or sessile, rarely (in Onagraceae; Cronquist, 
1981) lyrate-pinnatifid. The leaf margin is gen- 
erally entire, but several genera of the Onagra- 
ceae and certain Lythraceae are provided with 
teeth (*Fuchsioid teeth") similar to those in Ro- 
saceae, and Trapa has unique teeth having a dou- 
ble apex (Hickey, 1981, unpubl. data). Primary 
venation is pinnate, secondary venation most 
often brochidodromous, and tertiary venation 
obliquely and irregularly percurrent (Hickey & 
Wolfe, 1975). Stipules are present in nearly all 
families as rudimentary, either lateral or axillary, 
structures, the latter frequently dissected into 


Inflorescences are variable but fundamentally 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


derivable from an anthotelic primary condition 
(see Briggs & Johnson, 1979). Suppression or 
amplification explain diverse inflorescences. De- 
rived are, for example, the racemes (often as- 
sociated with zygomorphic flowers). 
owers are usually bisexual, generally adapted 
to insect or bird pollination, actinomorphic or 
weakly (to rarely strongly) zygomorphic, mostly 
4- or 5-merous although sometimes 3-, 6-, or 
pleiomerous, perigynous to epigynous or some- 
times semi-epigynous, without, or more often 
with, short to long hypanthium (an expanded, 
cup-shaped floral tube or receptacle) (Bunniger, 
1972; Bunniger & Weberling, 1968), beari 
mostly on its rim calyx-lobes, petals, and sta- 
mens, some of which may be reduced or absent 
(filaments are often more or less free from the 
hypanthium in Lythraceae and some Combre- 
taceae, however). Calyx lobes are green or col- 
ored, sometimes conspicuously carnose, rarely 
shed as a cap at anthesis. Petals are usually pres- 
ent, then mutually free, unguiculate to basally 
cuneate, mostly red, violet, white, or yellow. Pet- 
als, when 5, are mostly with convolute aestiva- 
tion, but when 4, with decussate aestivation. 
The androecium is haplo- or diplostemonous 
(sometimes superficially ова лови НОО 
ondarily pol 1 ith tripetal ог, m 
и و‎ 1 р juence, in the 
latter case often in а few clusters developed from 
the same number of primordia, associated with 
trunk-bundles. Reduction in stamen number 
within isomerous whorls is rare. Stamens have 
narrow to relatively broad, terete or flat filaments 
and basifixed or dorsifixed anthers, in some fam- 


: an 
longitudinal slits or, in certain Myrtaceae 


Pollen grains are mostly free (tetrads are a 
ent in genera of Onagraceae, however), basic * 
3-colporate, but rarely colpate or porate. In -— 
eral families they are provided with conspicuov® 
pseudocolpi alternating with the true apert 
m н rarely, viz. in some genera of Le 
witht 


Viscin threads artie from the pollen кыш 
nearly all Onagraceae (exception: Circaea a лек 
L.); this family also is more variable їп apertu " 
condition than the other families. Pollen "d 
are usually 2-celled when dispersed (cf. ТО 
Raven, 1984c). 


, 


-—— 


1984] DAHLGREN & THORNE—MYRTALES 


An annular disc structure is often present 
around the style or ovary, inside the stamens (or 
hypanthium). 

he pistil is syncarpous, consisting of two or 
more (frequently four or five) carpels and pro- 
vided with one, two, or more locules, rarely with 
incomplete septa. The style (almost lacking in 
Psiloxylon) varies from apically branched 
(branches isomerous with carpels) to simple, with 
lobate to simple stigma, or with stigmatic areas 


rarely р ( еп 

aeaceae; see below this family). The stigma is 
usually of the “dry” type (Heslop-Harrison & 
Shivanna, 1977), but at least in Melastomataceae 
and Onagraceae often of the “wet” type (Raven, 
pers. comm.). Placentation is mostly central and 
axile, or more rarely free-central (as in a few 
Lythraceae) or basal (as in most Penaeaceae) in 
the bi- to multilocular ovaries; parietal (as in a 
few Myrtaceae), or apical (as in all Combretaceae) 
in the unilocular ovaries. 

Ovules are solitary to numerous per carpel, 
anatropous or rarely hemianatropous or cam- 
Pylotropous, crassinucellate, and generally bi- 
legmic (unitegmic in some Myrtaceae). А pri- 
mary parietal cell is cut off from the archesporial 
cell in all families studied (although this has not 
been verified satisfactorily for Myrtaceae). Em- 
bryo sac formation is mostly according to the 
Polygonum type, except in Penaeaceae (with the 
letrasporic, 16-nucleate Penaea type), Onagra- 
ceae (with the monosporic, 4-nucleate Oenothera 
type), and Alzateaceae (with a bisporic, Allium 
type embryo sac; Tobe & Raven, 1984a). En- 
dosperm formation is nuclear (but there is rapid 
endosperm nucleus degeneration in Trapaceae). 
The embryology of Myrtales has been reviewed 
by Tobe and Raven (1983a). 

Fruits are most varied: capsules, berries, nuts, 
or Samaras developed from superior or inferior 
Ovaries. 

The seed coat varies among the families of the 
order and tends either to have a fibrous exoteg- 
Ea (i.e., outer layer of the inner integument) 

€n combined with a sclerotic mesotesta (mid- 
i layer of the outer integument) or to lack a 


М rid during seed development. The embryo 
di ously differentiated, straight or more rarely 

"ved or twisted, with anisocotyly in Trapaceae. 
fa * embryo stores fatty oils and aleuron in most 
milies but does store starch in Trapaceae, and 
In Some Myrtaceae and Melastomataceae. 


RIPTION 637 


Galli- and ellagitannins are normally present; 
flavonols (including methylated flavonols) are 
common, but flavones are rare or lacking. Proan- 
thocyanins are present in some families. Triter- 
penes are common and triterpene saponins are 
present in at least some families. Various alka- 
loids are sporadically formed but are diverse and 
without great taxonomic significance. Cyanogen- 
ic compounds likewise are sporadically present 
in the order. Aluminum accumulation is con- 
spicuous in at least three related families, and 
silica grains occur in certain Myrtaceae. Clus- 
tered or solitary crystals of calcium oxalate are 
commonly deposited in cells of the parenchy- 
matous tissue; raphides are present in Onagra- 
ceae and rarely in Lythraceae. Iridoids, polyacet- 
ylenes, juitery lact gl inol and 
benzylisoquinoline alkaloids are absent. Essen- 
tial oils are present in secretory cavities in Myr- 
taceae 

Chromosome numbers tend to be multiples of 
11 or especially 12 (Х = 12 is considered a likely 
primary basic number by Raven, 1975), but show 
a considerable range of variation particularly in 
Onagraceae, Lythraceae, and Melastomataceae. 

This description is valid for the Myrtales if 
restricted to the “core families": Onagraceae, 
Trapaceae, Lythraceae, Oliniaceae, Combreta- 
ceae, Alzateaceae, Penaeaceae, Rhynchocalyca- 
ceae, Crypteroniaceae, Memecylaceae, Melas- 
tomataceae, Psiloxylaceae, Heteropyxidaceae, 
and Myrtaceae. With this circumscription the 


Myrtales seem to be homogeneous, natural, and 
easily definable. If the order were expanded, as 
recommended by some taxonomists, to include 


TT 


modification in each case. These families, con- 
sidered by some as serious candidates for inclu- 
sion in Myrtales, will be discussed in more detail 
near the end of this paper. 
A NOTE ON THE CIRCUMSCRIPTION OF 
THE FAMILIES OF MYRTALES 


For the purpose of the following account on 
distribution of character states, the following 
notes may be adequate. 

The Onagraceae present no problems and are 
circumscribed and subdivided as by Raven 
(1979), comprising 17 genera of ca. 675 species 
distributed among seven tribes. 

Tra consist of the genus Trapa only. 

The family Lythraceae is more widely circum- 
scribed here than in most contemporary litera- 
ture. It includes Punicaceae, with the genus Puni- 


638 


ca (Levin, 1980, treats one of the species in the 
segregate genus Socotria), and Sonneratiaceae, 
with the probably rather distantly related genera 
Sonneratia and Duabanga. 

The Combretaceae here include Strephone- 
mataceae (Venkateswarlu & Prakasa Rao, 1971), 
which consist of the single genus Strephonema. 
With the inclusion of the genus Strephonema, 
the Combretaceae (syn. Terminaliaceae) are cir- 
cumscribed as in current works. The mangrove 
genera Lumnitzera and Laguncularia have prob- 
ably adapted to their mangrove life by conver- 
gence. 

Oliniaceae consist of the genus Olinia only. 

Alzatea and Rhynchocalyx, which were treated 
in Crypteroniaceae by van Beusekom-Osinga and 
van Beusekom (1975), have here been excluded 
from this family and proved to be so distinct that 
they are each given family rank (Graham, 1984; 
Johnson & Briggs, 1984). 

Penaeaceae (Dahlgren 1967a, 1967b, 1967c, 
1968, 1971) consist of seven genera, Endonema, 
Glischrocolla, Saltera, Sonderothamnus, Brach- 
ysiphon, Stylapterus, and Penaea. 

Crypteroniaceae, after the exclusion of A/zatea 
and RAynchocalyx, consist only of Crypteronia, 
Axinandra, and Dactylocladus. 

Memecyclaceae with some hesitation are here 
considered as distinct from Melastomataceae (by 
Dahlgren). It consists of six to eight genera, Mou- 
riri, Lijndenia, Memecylon, Votomita, Spathan- 
dra, and Warneckea. Pternandra is also includ- 
ed, whereas the position of Astronia is doubtful. 

Remaining are Psiloxylaceae ( Psiloxylon), 
Heteropyxidaceae (Heteropyxis, Stern & Bri- 
zicky, 1958), and Myrtaceae, which are undoubt- 
edly derivatives from the same ancestral Stock. 
(Thorne considers Heteropyxis and Psiloxylonto 
represent subfamilies of Myrtaceae.) 


DISTRIBUTION OF CERTAIN ATTRIBUTES 
IN THE FAMILIES OF MYRTALES 
AND SOME OTHER FAMILIES 


The attributes discussed below and outlined 
as to their distribution in the myrtalean families 
and some allied families were selected on the 
basis of the following criteria: 

(1) they are either characteristic of the order 
or part of the order and frequently mentioned as 
"key" attributes; 

(2) most are reasonably well documented, al- 
though a few are not: and 

(3) they do not exhibit complicated patterns 
in the order. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


Some of the attributes are often neglected to a 
great extent but deserve inclusion with the oth- 
ers. The selection is somewhat limited and can- 
not claim to include all the most essential items, 
but is thought to be representative in some de- 
gree, and to give an indication of: 

(1) distinctness of the order; 

(2) relationship among families of the order; 


n 
(3) degree of consistency of the attributes 
within families. 


WOOD ANATOMY 


As the wood anatomy is treated elsewhere in 
this symposium, by van Vliet and Baas, only a 
few remarks will be given here. 

The core families of Myrtales are all charac- 
terized by the combination of bicollateral bun- 


a combination which is otherwise very rare in 
angiosperms and restricted to Thymelaeaceae 
(excl. Gonystyloideae), certain Euphorbiaceae, L 
few families of Gentianales, part of Vochysi- 
aceae, and the genus Centopodium (— Emex pro 
parte) of Polygonaceae (van Vliet & Baas, 1984). 
Thymelaeaceae and Loganiaceae, which appear 
to some as closely allied to Myrtales, will be 
discussed later. For different reasons each family 
is considered by us as not directly related to Myr- 
tales 


From a purely wood-anatomical point of view 
it is obvious (van Vliet & Baas, 1984; Baas 
Zweypfenning, 1979) that Punica as well as 
Rhynchocalyx (treated here as Rhynchocalyca- 

) could well be included in Lythraceae, 
whereas Sonneratia and Duabanga, usually 
treated as the Sonneratiaceae, in different (and 
not always the same) wood-anatomical respects 
deviate somewhat more from Lythraceae. Thus 
the homogeneity of the former Sonneratiaceae 
must be reconsidered; Sonneratia and Duabanga 
diverge also in other respects (see p. 663). On 5 
collected evidence they are both included їп Ly- 
thraceae. 

Further, Crypteroniaceae and Memecylaceae? 
largely differ from Melastomataceae in having 
distinctly bordered pits and in lacking fiber и 
morphism, and Memecylaceae also for the mos 
part have solitary vessels and included сал 
which is пої the case іп Melastomataceae- es 
is taken to support treating Crypteroniaceae, " if 
lastomataceae, and Memecylaceae as distin 
amilies. 


о a ————————— — 


1984] DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 639 
Rhizophoraceae pee i oe те 
e send 
Haloragaceae с Combretaceae с 
Z Te. 
; i M. 
анали —Ó Oliniaceae N 
2 : 
ка Trapaceae Lythraceae Penaeaceae \ 
as 3 : 
p Onagraceae (Combretoideae) \ 
(Stréphonematoideae) : 


(Du Rhynchocalycaceae "i aceae \ 
em © 
~(Lythroideae) Alzateaceae \ 
"(Punicoideae) © 
ПА AT ELS ) О Стуріегопіасеае-(6*%) 
Heteropyxidaceae-() Psiloxylaceae \ 


Melastomataceae 


Lecyth 
T — INE Myrtaceae 
X 


| | 
/ | 
! Pe met | 
| A ; 
\ / / 
7 
wW A 
aU ^ и 
А WL P 1 
fus Ly ot Thymelaeaceae 
Rhizophoraceae ee n REL 
+ р = 
Haloragaceae „` Combretaceae о 
| Pd 2 
v 
d Oliniaceae  : 
се ee С X 
ip Tm h le 
p? re Trapaceae Lythraceae naeaceae 


\ 


Memecylaceae \ 


С Combretoideae) 
eo cort eae) 


^ Onagraceae 
33 nchocalycaceae 


A 


(Lythroideae) Alzateaceae 


~(Punicoideae) 


силине © Crypteroniaceae -(22::)) 


Heteropyxidaceae- Psiloxylaceae 


№ 

Lecythi : 
$ тен N Myrtaceae 

N 


Y 
| 
Ц 
Ц 
| 
\ 
X 
N 
В | 2 Е 
dmi c ai аа Thymelaeaceae 


í Ма ‘SURE 1. Distribution, in the myrtalean and some other families, of:—A. е vascular strands 
Опр). — В. diffuse (®) and terminal (О) sclereids, according to Rao & Das (1979). 


640 


Strephonema differs from other Combretaceae 
in certain wood-anatomical respects, and Psilox- 
ylon similarly differs from the Myrtaceae, sup- 
porting the treatment of these genera, which for 
other I | lai d to fc 
units, as separate families or, at least, as subfam- 
ilies. 

Alzatea also appears to be out of place in Ly- 
thraceae as well as in Crypt i 
appears it should be placed in a separate family 
(cf. Graham, 1984). This treatment is supported 
by various wood-anatomical details. 

These indications, all based largely on the data 
of van Vliet and Baas (1984), are important in 
the general considerations of rank, circumscrip- 
tion, and interrelationships. 

Some trends of evolution in wood anatomy 
are of significance in the order. An example is 
the reduction of pit borders and the limitation 
of pits to the radial walls in the fibers, i.e., the 
evolution from fiber-tracheids to libriform fi- 
bers. This has occurred in Lythraceae (incl. Puni- 
ca, Duabanga, and Sonneratia), and in Onagra- 
reas (tha 1 dhi 4 ix SE x 1 4 


separate 


andit now 


( 1 een the 
Lythraceae and Onagraceae), Oliniaceae, Melas- 
tomataceae, and Combretaceae, and in many 
Myrtaceae. In this respect these groups are thus 
specialized. 

On the whole, the differences between the Ly- 
thraceae (sensu stricto) and Onagraceae in wood 
anatomy appear to be conspicuously few. There 
als to be great d in wood anat- 
omy between Strephonematoideae and most 
Myrtaceae. Some of these similarities, as pointed 
out by van Vliet and Baas (1984), are, most like- 
ly, due to retention of primitive features and thus 
do not form a sound basis for phylogenetic con- 
clusions, but others are similarities of special- 
ization and therefore can be phylogenetically im- 
portant, although convergent evolution in some 
of these features has surely occurred. 


SLUTS LU 


SCLEREID IDIOBLASTS OR FOLIAR SCLEREIDS 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


branched and present in the blades, this being 
possibly of some significance in the consideration 
of the distinctness of A/zatea in relation to Ly- 
thraceae. The presence of leaf sclereids in Son- 
neratia and Duabanga may also be noted in this 
context. In Penaeaceae, leaf sclereids are present 
in all the genera and have been described by Rao 
(1965) as well as by Dahlgren (1971). 

Leaf sclereids are abundant and their shapes 
useful in the classification of species in Meme- 
cylaceae (Foster, 1946, 1947; Rao & Jacques- 
Félix, 1978; Bremer, 1979; Rao et al., 1980). 
Morley (1953) noted that the presence of ter- 
minal sclereids seems to be typical of this family, 
whereas their absence seems typical of Melas- 
tomataceae. Non-terminal sclereids do occur, 

owever, in various Melastomataceae, e.g. 
Plethiandra (Rao & Bhattacharya, 1977). 

In Crypteroniaceae, unbranched sclereids oc- 
cur in leaf petioles in Crypteronia and Dactylo- 
cladus, but not in Axinandra (van Vliet & Baas, 
1975). According to Keating (1982), Onagraceae 
lack foliar sclereids; their absence in the aquatic 
Trapaceae is expected. Within Myrtaceae, foliar 
sclereids are known to occur at least in Ango- 
phora, Eucalyptus, and Syzygium (Rao & Das, 
1979) 


Sclereids have not been recorded in Halora- 
gaceae but are known to occur in several genera 
of Rhizophoraceae and Thymelaeaceae. Scler- 
eids also occur in various taxa of Theales, per 
haps not in the Lecythidaceae, but in Bonneti- 
aceae, for example, and in several genera of 
Theaceae sensu stricto. Furthermore, in Primu- 
laceae, foliar sclereids are common, e.g., 1 Dion- 
ysia (Bokhari & Wendelbo, 1976, where sclereids 
are Classified). A 

The presence of sclereids and their variation 
must not be overemphasized as a taxonomic Cr 
terion. Considered at large (Rao & Das, 1979), 
they give a very scattered picture in the angio- 
sperm system. However, in isolated famlies к 
may be conspicuously plentiful or may be absent. 
and in such cases they may be of phylogenett 
interest. 


SIEVE-ELEMENT PLASTIDS 


As is shown by Behnke (1984), all Myrtales 
yet studied have sieve-tube plastids with — 
grains (S-type plastids) but without protein we 
talloids (P-type plastids). The fact that the р 
zophoraceae have protein crystalloids, whic 
numerous, rectangular or variously 4(0r 


1984] 


gled, and of variable sizes (type PVc, sensu 
Behnke, 1981) may be taken as an indication that 
this family is not myrtalean. However, in dicot- 
yledons a number of isolated families unexpect- 
edly have P-type plastids of various shapes 
(Rhabdodendraceae, Cyrillaceae, Erythroxyla- 
ceae, Oxalidaceae, Connaraceae, Gunneraceae, 
Vitaceae, Buxaceae), a feature which may not, 
alone, be sufficient evidence for excluding them 
from orders with S-type plastids. Of the enu- 
merated families, Erythroxylaceae are the family 
with the protein bodies most similar to those in 
Rhizophoraceae and Cyrillaceae, which should 
be considered in evaluating their phylogenetic 
relationships. 

The fact that Myrtaceae, but not other Myr- 
tales studied, contain crystalline protein in their 
sieve elements may indicate that they are some- 
what isolated in the order. 


PHYLLOTAXY 


расеае consist of decussate leaf pairs. 
Thymelaeaceae, often placed in Myrtales, have 
disperse ; 1 


DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 641 


prevailingly disperse, but sometimes opposite, 
leaves 


STIPULAR STRUCTURES 
(by F. Weberling, Ulm) 


In contradiction of the classical opinion, near- 
ly all families belonging to the Myrtales are char- 
acterized by the occurrence of stipules (Weber- 
ling, 1955, 1956, 1958, 1960, 1963, 1966, 1968). 
They seem to be lacking usually in the Melast- 
omataceae, and generally so in Memecylaceae, 
where they occur, however, in at least some taxa 
of Mouriri (Fig. 14B). 

In most cases the stipules are diminutive (**ru- 


families of the Myrtales stipules represent a rath- 
er constant vegetative characteristic, as in Ly- 


aceae, Penaeaceae, and Crypteroniaceae (and also 
in the possibly allied families Rhizophoraceae 
and Haloragaceae), whereas in the other families 
they are present in some genera only. In Ona- 
graceae, stipules are characteristic of five rela- 
tively primitive tribes, Jussiaeeae (Ludwigia), 

eae (Fuchsia), Lope- 


plays usual features in their development. They 
appear at a very early stage of the leaf develop- 
ment, forming lateral excrescences from the leaf- 
base (Fig. 2A, D, F). Their further growth shows 
a more or less pronounced prolepsis. Sometimes 
they grow so rapidly that they temporarily have 
nearly the length of the entire leaf (Fig. 2B) or 
they may even exceed the leaf in length (Fig. 2D). 
They also attain their final proportions a long 
time before the leaf-blade does. Thus stipules 
which are more or less flattened are able to serve 
as bud-scales, whereas stipules which function as 
glands contribute to bud-protection by covering 
the buds with their mucous secretions. 

Outside Myrtales as circumscribed here, stip- 
ules are present in Haloragaceae. In the pinnate 
leaves of Myriophyllum, more or less complete 
stipules at the very base of the leaf can be ob- 


642 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


NY 


SSP MMM 


MANN 


E IM I eI Ph 


SM enr 
NS SS 
~“ 


NL 
с) 


„== "ei 
й ~ 
- Bg 


ко a one in the Myrtales. A-C. Lopezia racemosa Cav. (Onagraceae).— A. growing point with to 
ои ~ : е larger one with primordia of stipules.—B. leaf primordium with stipules. —C. part оки 
ое g two leaf bases with stipules on the upper ends of ridges formed by the margins of decurrent рабин“ 
(Camb) Н + retiana L. (Onagraceae): leaf primordium with far developed stipules. —Е. Ludwigia cf. uruguay 
one sid рання part of a stem with lower part of foliage leaves and stipules. F-I. P. unica gram. 
ir 5 . Stages of leaf development.—H. base о young foliage leaf with decurrent wings cm 
auricles (a) and rudimentary stipules (st) — I. cataphyll and stipules. 


чип 


aids pis their insertion the formation of Jon), however, they form two or more minul® 
bna i d SH continues in a basipetal di- subulate, or club-shaped processes shifted so f 
ен sti what deeper into the leaf axil on either side 5 

У Stipules are situated one on either the leaf-base (Figs. 2H, 3A) or two groups 0 


side of the leaf axil. In this position they can be minute processes forming a transverse row 4 


observed in Lopezia (Fig. 2C), Ludwigia (Fig. the base of the petiole (Fig. 3F). The latter type 


2E), or in Crypteronia (Fig. 30), In many taxa has been reported for most genera of Lote 


of Myrtales (e.g., many Myrtaceae and Psiloxy- by Koehne (1884, 1893, 1903), though W! 


Де rede eee a 


1984] DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 643 


FIGURE 3. Stipules in myrtalean and some other families. A-B. Feijoa sellowiana Berg. (Myrtaceae).—A. 
-— · leaves with rudimentary stipules. —B. leaf bases in detail.—C. Crypt сва Jeptostachys Endl. (Cryp- 
D-F. Т, 


"ys iul ot tipul о. 


Md. cal dey oon D, 1.5 mm, in E, 3.5 mm, and in F, 10 mm long).— бен Myriophyllum pinnatum 
"tton (Haloragaceae); stages of leaf ге шы ызгы 'Н representing a nearly fully developed leaf. 


this family there are also taxa where leaves bear тапу Myrtaceae, and some Combretaceae (and 
Stipules in ‘normal’ position (e.g., Lagerstroemia also іп Lecythidaceae). Continuous morpholog- 
and Lawsonia). Intrapetiolar rows of stipular ical lines of intermediary forms (two- or three- 
ses also occur in Trapaceae, Penaeaceae, lobed stipules a.o.) between stipules in ‘normal’ 


644 


number and position, and intrapetiolar rows of 
stipular processes indicate that the two groups 
of processes composing an intrapetiolar row are 
equivalents of two stipules. The same becomes 
evident from the study of their ontogeny (Fig. 
3D-F). The dissection of the stipules may be а 
symptom of reduction. The displacement of stip- 
ular processes into the leaf axil probably is a 
result of an increased growth of the lower surface 
of the leaf-base. 

In some Myrtales (Punica granatum L., Fig. 

F-H, Lafoénsia microphylla Pohl, Lagerstroe- 
mia indica L., Penaea mucronata L.) and the 
lecythidaceous Napoleona talbotii E. G. Baker, 
the stems are winged, apparently by the leaf- 
bases being decurrent (Fig. 2F, G). These wings 
are prolonged at their upper ends into auricles 
situated on either side of the leaf-insertion, like 
stipules, whereas the true stipules are subulate 
processes located somewhat deeper in the leaf 
axil (Fig. 2H). 

In Rhizophoraceae, the Rhizophoroideae are 
characterized by large triangular to lanceolate in- 
terpetiolar stipules, whereas the genera of Ani- 
sophylleoideae differ by the alternate position of 
the leaves and the stipules being represented by 
a variable number of minute processes placed in 
the leaf axil. 

Habitually, in the myrtalean families, stipules 
are present in connection with all leaves except 
the cotyledons. But in Angophora and Eucalyp- 
tus, genera in which the foliage leaves of all or 
most species are destitute of stipules, Carr and 
Carr (1966) found that the cotyledons of many 
species have rudimentary stipules. Johnson and 
Briggs (1984) report on stipules at the cotyle- 
donary stage also in Arillastrum. The stipules can 
be two- or three-lobed or may be represented by 
several glandular processes situated on or near 
the margins of the leaf-base. The same is true for 


In many Myrtales stipules also Occur at the 
bases of the cataphylls (Fig. 21) and at the bases 
of bracts. This fact indicates that cataphylls and 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


bracts are of laminar origin (also confirmed by 
their venation). 


OTHER LEAF CHARACTERISTICS 


The leaves in Myrtales are normally simple 
and entire and have basically brochidodromous 
to eucamptodromous venation (Hickey, 1981; 
Hickey & Wolfe, 1975). In certain lines of evo- 
ution, i.e., most Melastomataceae and many 
Myrtaceae, there are several main secondary 
veins, which branch out from the base of the 
blade, with tertiary veins being transverse. The 
difference between the two families Memecyla- 
ceae and Melastomataceae is significant (but not 
altogether sharp), both types being probably sec- 
ondary to a typical brochidodromous type. Fur- 
ther trends of venation patterns are demonstrat- 
ed by Hickey (1981). 

s regards marginal teeth, these occur in cer- 
tain Onagraceae, viz., in the tribes Epilobieae 
and Onagreae, and also, although less conspic- 
uously so, in some Lythraceae (Hickey, 1981), 
being in these families conspicuously similar, and 
of a “Коѕоій” basic type with a broad, crater- 
like apical hollow: the ‘‘Fuchsioid” subtype. 
Another similarity (Hickey, 1981) is the presence 
on the leaf margins in taxa of the two families 
of short marginal hairs. Independent origin of 
both of these structures, the former of which 1s 
quite particular, seems to be unlikely, and thus 
we agree with Hickey that most likely they rep- 
resent original attributes in the order. 

In the Trapaceae (Trapa) the teeth have 7 
“unique double apex” (Hickey, 1981), which и 
quite different from that in the families men- 
tioned. Teeth also occur rarely in the genus So- 
nerila, Melastomataceae (e.g., in Sonerila sue 
folia Blume), where they may vary cone 
in length (Carlo Hansen, pers. comm.). in 
teeth do not seem to be of the same kind as! 
Onagraceae or Lythraceae; their filiform apex ™4Y 
represent a trichome. 2 | 

The phylogenetic significance о 
types pe alee by Hickey and Wolfe Bis 
who state that they often show great hae 
in families, orders, and larger groups and нв 
conclusions can be drawn from their geet 
tion. The Rosoid teeth in some Myrtales, ehe 
are a residual attribute, indicate a possible : 
nection with the Rosales and other و‎ 
sessing such teeth, such as Rhamnales, 
Sapindales, Cunoniales, Vitales, and r té 

The leaf teeth in Lecythidaceae аге 0 1% 
“Theoid” kind (Hickey & Wolfe, 1975) ап 


leaf-tooth 


-- 


1984] DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 645 


Rhizophoraceae Ir ae eee 
^ Combretaceae “~. 
Haloragaceae Zz O NE 
\ > =. 
` ~ 
» Oliniaceae ` 
. سے + سے‎ Ue 4 ЊУ 

Lythraceae Penaeaceae V 


" m, у 
= Trapaceae 


я (Combretoideae) \ 
(ређи ideae) \ 
Memecylaceae 


4 Onagraceae 
hynchocalyc aceae 


goideae). J: | 
“(Lythroideae) Alzateaceae | 


0 zm Punicoideae) 
(Sonneratioideae) Crypteroniaceae (5) \ 


Неѓегорухідасеае-{23) Psiloxylaceae Melastomataceae 
2 


1 
Thymelaeaceae 


Rhizophoraceae E E oe 
Haloragaceae ` Combretaceae oe ` 
\ 
٠. w 
Oliniaceae · 
ت‎ 
. a A umm h Р 
ТОО Тгарасеае Lyti — enaeaceae \ 


(Combretoideae) i 
(Stréphonematoideae e) 
R Memecylaceae\ 


ynchoc alyc aceae 


У: “а = 


hroideae) Alzateaceae 


v (L 
~(Punicoideae) 
(Sonneratioideae) Crypteroniaceae- ) 


Heteropyxidaceae-(.) Psiloxylaceae 


PN 
Lecythi 
чар N Myrtaceae 
N 


ы”: a an Г. Thymelaeaceae 


чы GURE 4. Distribution, in the myrtalean and some other families, of:—A. stipules, minute (dotting) or fairly 
пе (ћаксћпр). —В. tetramery of perianth (dotting). 


646 


1. Merous conditions in sepal and petal 
Muni in Myrtales and possibly related families. 


© d 16 & 52$ 
mery mery mery mery mery 
Onagraceae С). 9. Oe E) 
Trapaceae = = * = a 
Lythraceae = а T РА 
Oliniaceae ~ C ETT г ^ 
ombretaceae = - - T (F) 
е T n = + ~ 
еп "s E T ~ ux 
исму E =: = = a F 
Crypteroniaceae = за F t "3 
Memecylaceae = 4 Hs + = 
Melastomataceae rper. BN 
Psiloxylaceae — + ~ he AH) 
Heteropyxidaceae "um = => + т 
Myrtaceae = -a к 6) 
Thymelaeaceae ~ = » тоса) 
Haloragaceae С) G? h E = 
Rhizophoraceae БЕК + к. (7) 
Lecythidaceae -= ЖЫ eh G) 
Elaeagnaceae = ут ۴ = LT 


probably do not show connection with those in 
any myrtalean group. 


MEROUS CONDITIONS OF PERIANTH 


The merous conditions in sepal and petal 
whorls are shown in Table 1 and in Figure 4B. 


4-mery mostly being considered as secondary to 
5-mery. However, in the Myrtales 4- and 5- -mery 
are both very common. 

Merous conditions in perianth and androe- 
cium of the Myrtales have been discussed by 
Eyde (1977) in connection with the genus Lud- 
wigia. This genus, unlike the other, almost con- 
sistently 4-merous Onagraceae, has а 5- or 
6-merous perianth in a number of species. Eyde 
stated (1977: 653) that the “higher number of 
floral parts can occur in association with certain 
advanced features. For instance, in sect. Oocar- 
ies with 5-merous flowers, and in sect. Oligo- 

rmum, where 5-mery is the rule and 6- -mery 
occasional " ird numbers are linked with 


carp." Be- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


cause Ludwigia represents a phyletic line sepa- 
rated early from the rest of Onagraceae, 5-mery 
or more may not be derived in the Onagraceae, 
although the prevalence of 4- -mery in this family 
suggests that its i di 
had 4-merous flowers. 

Lythraceae are more or less evenly divided 
between genera with 4-merous and 6-merous 
flowers with respect to sepal, petal, and stamen 


tive in the family (provided ancestral Myrtales 
had isomerous floral whorls). Ado Zy- 
gomorphic genera are 6-merous, a further evi- 
dence that 6-mery is derived. Not all se 
genera, however, are 6-merous. The aquatic and 
marsh annuals, кален апа Tidit “ 
4-merous. Р 
in Decodon. There is variation in merous с 
ditions among populations within species in 
some genera, but the 4-merous or 6-merous state 
is clearly dominant in most instances (A. Gra- 
ham & S. Graham, pers. comm.). 

The merous conditions in myrtalean and some 
other families, somewhat generalized, are shown 
in Table 1. The commonest conditions are 4-mery 
and 5-mery. The great frequency of the former 
state is noteworthy since in most other dicoty- 
ledonous orders 5-mery is much more frequent. 
However, merous conditions are variable in 
Myrtales, and it is even rather typical in the larger 
(and some of the small) families that merous 
conditions vary from (2-)3 to 6 or more. 
outgroup comparison combined with an appre- 
ciation of the merous conditions in the order 
indicates that 5-mery is likely to be плови 

although 4-mery has arisen very early and pro 
ably, subsequently become dominant in seve’ 
evolutionary lines 


mong families often associated a 
on in Thymelaeace 


Босма dominant іп Haloraga 
Elaeagnaceae, and the only condition in 
petalanthaceae; whereas, in Lecythi pe - 
rare. Tetramery in floral parts has o 
consideration in regarding most of a n 
as related to the Myrtales or membe we 
order in spite of the fact that it is probably 
the ancestral state here. 


Dialy- 


es 
of the 


OVARY 
INFERIOR, SEMI-INFERIOR, OR SUPERIOR 


te 
In the Myrtales the floral tube is either sng 
to all or part of the ovary walls (epigyno 


| 


— 


1984] 


hemi-epigy tat pectively) or surrounds 
the ovary either tightly or loosely (perigynous 
states). The distribution of these states is shown 
in Table 2 and Figure 5A. 

Because hypogyny and perigyny are consid- 
ered to precede hemi-epigyny and epigyny and 
b l famili heterog in this 
respect, it is obvious that adnation between floral 
tube and ovary has occurred in several evolu- 
tionary lines. 

The floral tube (or hypanthium) is quite varied 
in length and may be short or long, and loose or 
tight around the ovary. Where it can be called a 
hypanthium, it bears on its edge sepals, petals, 
and frequently also one or two whorls of stamens 
огпштего 1 , althoug an also 
be borne on the inner side of the hypanthium, 
or near its base. 

In perigynous flowers of most Lythraceae, all 
the filaments are nearly or wholly free from the 
hypanthium. This condition may be considered 
either as an original state or asa separate, derived 
condition in relation to that where the filaments 
are inserted on the hypanthium edge. Exceptions 
are found in Lawsonia, where the stamens are 
inserted on the inner side of the hypanthium, 
and in Sonneratia, Duabanga, and some species 
of Cuphea, where they are inserted on or near 
lts rim. The first two genera, often referred to 
Sonneratiaceae, thus deviate from most other 
Lythraceae in having the stamens inserted on the 
Пт of the hypanthium. Also Rhynchocalyx 
(Rhynchocalycaceae), which is sometimes re- 
ferred to Lythraceae, has the stamens inserted 
on the rim of the hypanthium. 

In €pigynous flowers of Myrtales a hypan- 
thium continuing beyond the ovary is sometimes 
missing, as in Ludwigia (Onagraceae). 

_ Within Myrtales the perigynous flower, found 
In most Lythraceae, and in all Penaeaceae, Rhyn- 
chocalycaceae, Alzateaceae, Psiloxylaceae, Het- 
‘ropyxidaceae, Trapaceae, and in a great part of 
Melastomataceae but in very few Myrtaceae, is 
undoubtedly the ancestral condition. In Melas- 
'omataceae, there is a range of variation from 
Lo to epigyny, and in Combretaceae the 
ii are hemi-epigynous (Strephonema) or 
oo and the immediate ancestors of each 
amily must have had perigynous to hemi-epig- 
ynous flowers. Memecylaceae, Oliniaceae, Ona- 
i and most Myrtaceae have epigynous 

ers. In each of them the epigynous condition 
apparently evolved early, but the ancestors of 
each family presumably had perigynous flowers, 


h stamens 


DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 


647 


TABLE 2. Gynous conditions in Myrtales and pos- 
sibly related families. 


Нуро/ Hemi- 
perigyny epigyny Epigyny 


Onagraceae ~ - 4 
Trapaceae F (+) — 
Lythraceae * (+) 

Oliniaceae — — 
Combretaceae — — + 
Alzateaceae 


+++ 
| 
| 


Репаеасеае 
Rhynchocalycaceae 


"d 
g 
а 
© 

BZ 
os 
о 
e 
f 
® 
~ 
E 
~ 


Heteropyxidaceae 
Myrtaceae 


Thymelaeaceae + – 
Haloragacea 

Rhizophoraceae 
Lecythidaceae = E 
Elaeagnaceae 


+ 
| 
| 


because other families to which they are closely 
related have representatives with perigynous 
flowers. Lythraceae, in which perigynous flowers 


of other probable ancestral states, therefore take 
a central position in the order. 
А 1 £ d £t 


Zu 4 


/ g with Myr- 
tales, Elaeagnaceae and Thymelaeaceae have pe- 


22 LI © 
of variation from perigynous to epigynous flow- 
Ф 1 1 1 Ty J and 


ers, while D yp g 
Lecythidaceae have epigynous flowers. 


ONTOGENY OF FLORAL PARTS 
IN SOME MYRTALES 


In a study of the ontogeny of the flower in 
representatives of Lythraceae (incl. Punica), 
Onagraceae, and Myrtaceae, Mayr (1969) found 
the following features: 

The histogenesis of the organs of the flower 
shows different participation of cell layers, the 
relative number of cells in the basal level of the 
primordia being the critical factor. 

In Myrtaceae the sepals and petals are more 
or less simultaneous in ontogeny but in Lythra- 
ceae (also in Punica) and Onagraceae the petals 
develop considerably later than the sepals. 

The “epicalyx” found in many Lythraceae (see 


648 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


Rhizophoraceae а nt ee и 
. "- 
Haloragaceae - Combretaceae . 
\ . 


Ec | eer 


/ (Stréphonematoideae) ii 
/ (Dusban- Rhynchocalycaceae Метерујанни Я 
goideae 
[ a (Lythroideae) Ө Alzateaceae \ 
| 77 S" (Punicoideae) С) | 
\ (Sonneratioideae) О Crypteroniaceae-(_) \ 
~ - 


ME 
Psiloxylaceae Melastomataceae \ 
Z 


. 
... 
° 


Џ 
Thymelaeaceae 


Rhizophoraceae 


Haloragaceae P бв Combretaceae T ~ 
^ A ње 
А м, 
ја т Oliniaceae * x 
ET addline Bi 8 B eae V 
جر‎ тароо ythraceae enaeac 
Pd у \ 
Z Onagraceae O (Combretoideae) iens . 
74 i 3 (Strephonematoideae) Mosa = 
у (Duaban- Rhynchocalycaceae L ; 
/ asad’ У О \ 
| Š ^(Lythroideae) Alzateaceae . 
i / "(Punicoideae) С) \ 
(Sonneratioideae) i = Г 
b О Crypteroniaceae C) \ 


j Heteropyxidaceae-( ) Psilox laceae 
> E i 
Lecythidaceae N 


+ 
Y 
| 
Д 

! 
i 


Melastomatacese \ 


Myrtaceae 


Thymelaeaceae 


so 


M 


m 


— — 


1984] 
Fig. 8G) is i ted from the con- 
muitelly fused sepals (comparable to commis- 
sural stigmas). The position of Coridaceae, which 
is similar in this respect, is discussed on p 

In androecia with numerous, bandied sta- 
mens, the organogeny of the stamens within the 
bundles is centripetal in Myrtaceae but centri- 
fugal in Lagerstroemia and Punica of the Ly- 
thraceae. 

The androecium of all taxa with two whorls 
of stamens is actually diplostemonous. Where it 


size and secondary displacement in the course of 
growth. 

Some Onagraceae have commissural stigmas 
(which is also the case in Penaea and Stylapterus 
of the Penaeaceae; see under this family below, 
and Dahlgren, 1967a, 1968). 

Mayr (1969) concluded that, among the fam- 
ilies investigated, Myrtaceae stand apart from 
the other three in several important details. 


MERY AND DEVELOPMENTAL SUCCESSION 
IN ANDRO 


= the Myrtales, diplostemony is no doubt ba- 


pb stemony occurs in Trapaceae, Olini- 
àceae, Alzateaceae, Penaeaceae, and Rhyncho- 
calycaceae, and in disparate genera of Lythraceae 
and Melastomataceae, a few genera of Combre- 
laceae and Ona aceae, two genera (Crypteronia 
and Dactylocladus) of three in Crypteroniaceae, 
and (as a case of reduction in a polystemonous 
whorl) in at least Myrrhinium of Myrtaceae. In 
Combretaceae, the flowers in Meiostemon and 
Thiloa as well as in one species of Terminalia 
are regularly haplostemonous, one species of 

iloa having staminodia representing the sec- 
Опа whorl; in Conocarpus the androecium is 
sometimes reduced from ten stamens to varying 
Numbers down to five by abortion (Stace, pers. 
comm.). In Onagraceae, Circaea, Lopezia, some 
Species of Clarkia and Ludwigia, and one species 
of Camissonia have haplostemonous flowers 
(Eyde, 1977), all these cases being no doubt sec- 
ondary in relation to diplostemony. In Melas- 


DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 


649 


tomataceae, haplostemonous androecia are in the 
minority but are scatt ina | number of genera. 
Itisalso fairly obvious tl Lytl there 
have been both reduction and multiplication of 
stamen number from a diplostemonous condi- 
tion. Reduction has occurred either as loss of 
episepalous stamens (Orias, Lawsonia, Capu- 
ronia), or episepalous stamens (Tetrataxis, Di- 
plusodon, Galpinia, Pleurophora). Multiplica- 
den рак еса by i тооно 1 in the пева 
as? in 
episepalous stamens (Diplusodon). nmm à 
evolutionary relationships among the genera are 
not clear, it paes appear that me loss or qut of 
stamin al OIC 
than once in Lythraceae and both loss каг gain 
can occur within a single genus. An interesting 
staminal feature in Lythraceae is that stamens 
are often of two distinct lengths, with the epi- 
sepalous ones always longest. (All this according 
to A. Graham « 8 mm 


production, especially in large flowers. This does 
not mean that the original ancestors of the an- 
i ld have had an indefinit 


ber of stamens, which most likely were spirally 
arranged. 

Much emphasis has been laid on the devel- 
opmental sequence (initials or anthesis, accord- 
ing to authors) of stamens in polyandrous taxa, 
i.e., whether the groups of stamens develop сеп- 
trifugally or centripetally. Leins (1964) distin- 
guished three groups for their subdivision, but 
there must be many more than three evolution- 
ary lines for polymerous androecia. Cronquist 
(1968) and Takhtajan (1969) have laid much 
stress on whether orders have centripetal or cen- 
trifugal androecial development, and Merx 
miiller and Leins (1971) have further нении 
the occurrence and taxonomic эга» nce of 
these types. ave surely 
evolved secondarily in оен lines, ex- 
amples being the Capparales (Capparaceae), Car- 


„с. 
~ 

FIGURE Mee in tl i th — A. perigynous (blank), hemi-epigynous 
(donti (à ng) lowers —B. multistaminate sehen with centrifugal (hatching) and cen- 


tri 
petal Comte d successio 


650 


yophyllales (Aizoaceae, Cactaceae), Loasales 
(Loasaceae), Theales (several families), Thyme- 
laeales (Thymelaeaceae: Gonystylus), Malvales 
(several families, e.g., Tiliaceae, Sterculiaceae, 
Malvaceae), Violales (independently from the 
preceding?: various Flacourtiaceae, Begoniaceae, 
etc.) 1 lso (?) Rosales (CI bal 


Couepia), and Myrtales. In Rosales, the stamens 
are generally arranged in several whorls which 
tend to have stamens in a multiple number of 
that in the perianth whorls, and Chrysobalana- 
ceae may not belong here. Also in palms, the 
stamens, no doubt, have increased secondarily 
in number, with different developmental se- 
quences as a result (Uhl & Moore, 1980). A sim- 
ilar condition occurs in Vellozi ; and in Alis- 
mataceae a secondarily multistaminal condition 
develops from initials superposed on the primary 
fewer ones, resulting in numerous whorls of sta- 
mens (Sattler & Singh, 1978, and other papers). 

It seems that what is taxonomically important 
is not the developmental direction in itself but 
rather along which evolutionary lines these an- 
droecia evolved, i.e., whether the multistaminal 
condition in various Myrtales has evolved along 
the same lines or not. Within Myrtales there are 
families with multistaminal as well as diplo- and 
haplostemonous androecia, e.g., Lythraceae, 
Myrtaceae, Melastomataceae, and Combreta- 
ceae. There seems thus to be a general tendency, 
within the order, for reduction as well as mul- 
tiplication of stamens. 

There is some regularity in the distribution of 
these secondarily multistaminal androecia and 


r (1969, see 
above) observed that Punica and Lagerstroemia 


(1 vthraceaeYh 
VJ } 


g је ,asi 
most Lecythidaceae and various other Theales 
(see Fig. 5B). 

Within Melastomataceae, the genus Astroca- 
[ух may have up to ca. 65 stamens per flower, 
and in Plethiandra the stamens may be 20—30 
in number. The developmental sequence of the 
stamens in these genera has apparently not been 
studied. 

Diplostemony seems to be basic in Myrtales 
and wide-spread in the order, occurring in sev- 
eral of the larger families: Lythraceae, Combre- 
taceae, Melastomataceae, and Onagraceae. 


POLLEN FEATURES, PARTICULARLY 
OCCURRENCE OF PSEUDOCOLPI 


Pollen morphology of Myrtales and possible 
allied groups is described separately in this sym- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


posium by Patel et al. (1984); hence we restrict 
ourselves to some general comments. The pollen 
grains in the core families of this order seem to 
be basically 3-colporate, although two to more 
than five apertures have been reported. Further 
the pollen grains are basically tectate and fre- 
quently characterized by pseudocolpi (intercol- 
pate furrows or *rugae," sensu Erdtman, 1952 

The pseudocolpi are not actual apertures but 
conspicuously colpus-like thin parts of the exine. 
In their early ontogeny they differ from true ap- 


tetrads occur in some groups, especially in Ona- 
graceae, where another peculiarity, the occur- 
rence of viscin threads, is a characteristic feature. 
Pseudocolpi (Fig. 6) are recorded in the fam- 
ilies Lythraceae, Oliniaceae, Combretaceae, Pen- 
aeaceae, Rhynchocalycaceae, Crypteroniaceae, 
Memecylaceae, and Melastomataceae (incl. Me- 
mecyloideae) but are absent (or very indistinct) 
in many Lythraceae (see below, incl. the Puni- 
coideae, Sonneratioideae, and Duabangoideae), 
Trapaceae, Alzateaceae, Psiloxylaceae, Hetero- 
eae, and Onagraceae. More 


pollen grains connect the distinctly heterocolpate 
pollen grains with other types and make the fe 
ture somewhat vaguely defined. However, pres- 
ence of pseudocolpi is so significant in Мупа с 
and so rare outside the order, that we attach great 
phylogenetic significance to its distribution. bis 
significance of pseudocolpi in the Crypteronr 
aceae (as circumscribed by van Beusekom-Os- 
inga & van Beusekom, 1975), i.e., in the gener? 
Crypteronia, Dactylocladus, Axinandra, AM 
and RAynchocalyx, was elucidated, for examp 

by Muller (1975). He found Alzatea to differ fro" 
the others in lacking pseudocolpi, thus contr 


кш 1 of 
uting toward recognition of the heterogeneity 


ceae, however, shows great variation 1 al 
currence of pseudocolpi (see also Patel et 2» 
1984). Thus according to Erdtman (1952) yi 
pos (1964), and S. Graham (pers. comm.), РУ 
thraceae generally possess 3-colporate ре 

grains (іп Lafoénsia oracolpoidate, Са rdins 
1964). Nine genera have pseudocolpi, acco Me 
to S. Graham (pers. comm.). In Lythrum, " de 
there are three pseudocolpi alternating W! Gi- 
three apertures, but in Ammannia, Степе» ме 
noria, and Nesaea there are six ese 

seudocolpi being present between я 
eee iu EM other genera (according t° 


1984] 


DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 


651 


Rhizophoraceae OE ORE et m. 
à — 
Halorag ле "^ Compretecese oe 
» о 000 LIS ned 
j S NE 
FA Oliniaceae ` 
E. 4 AN 
ит? 
p i cis EENT Penaeaçeae\ 
PT о о АЕ \ 
/ hagraceae (Stréphonematoideae ) M \ 
: (Duaban Rhynchocalycaceae isi Nanas . 
y goideae) e etes 
| ^(Lythroideae) Alzateaceae 
; / ^(Punicoideae) 
X (Sonneratioideae) Crypteroniaceae- (577) 
х: Heteropyxidaceae-(_) Psiloxylaceae 


Lecythid à 
yt aceae A 


Myrtaceae 


Fic 
Ране i, att pPseudocolpi i 
apertures (hatching). 


ham, pers. comm. ), such as че Си- 
Phea, pones Galpinia, Lafoén 
St 


may have incipient (or rudi- 
mentary!) pseudocolpi: “R. ramosior marquerait 
le passag 
colpés” (Campos, 1964: 306). Here, as well as in 
the pollen grains of Lafoënsia, where the pseu- 
docolpi are very faint, these could be interpreted 
е аѕ incipient or reduced. A study of: the 
nay 
MA or faint) први seem to occur in 
спуед genera (A. Graham & S. Graham, pers. 
comm.). although this is not clear. In variation 
of Occurrence and number of pseudocolpi (rela- 
tive to apertures), Lythraceae are outstanding in 
the order, and it may be argued whether absence 
of Pseudocolpi represents an original or (by sec- 
ondary loss) an advanced state. 
нн апа Duabanga have Апфр!о-арег- 
jo 1969 
"ы Distinct peeudacolpi are lacking, but in 
"nératia intercolpate depressions resembling 


~“ 


Thymelaeaceae 


E 6. Distribution, in the myrtalean and some other families, of pollen grains without (blank) pseu- 
isomerous with apertures (dotting) and with pseudocolpi double the number of 


pseudocolpi may occur. According to Erdtman 
(1952) the pollen grains resemble those in Di- 
plusodon of the Lythraceae, and Muller (1981) 
reports a pollen type, Florschuetzia trilobata, from 


rarely 4-) colporate and likewise lack pseudo- 


olpi. 
Whether the very characteristic pollen grains 
ш: трк with three meridional crests of 


1 meeting at the poles rep- 


resent a heterocolpate туре ог rather a type with 
[ , needs to be 
verified. 


The heterocolpate pollen grain types thus do 
not represent a distinct category. They include 
very peculiar shapes, such as that i n | Oliniaceae, 


hers (Patel et al., 1984 ). 

Nevertheless, there is evidence from this at- 
tribute, as from others, that the families or 
subfamilies with clearly heterocolpate pollen 


652 


grains form a coherent group, along with some 
others, where pseudocolpi are absent or at least 
very indistinct (Lythraceae subfam. Punicoideae, 
Duabangoideae, and Sonneratioideae, Combre- 
taceae subfam. Strephonematoideae and Alza- 
teaceae) or where pseudocolpi are missing or 

oubled” in number (Lythraceae subfam. Ly- 


eae). 

Pseudocolpi, aside from Myrtales, are known 
only in Ehretioideae (Boraginaceae pro parte) and 
a few Fabaceae (Leguminosae) (Skvarla, pers. 
comm.), and the tendency to have pseudocolpi 
is not likely to have evolved independently in 
more than one line within Myrtales. 

Pseudocolpi are absent in Psiloxylaceae, Het- 
eropyxidaceae, Myrtaceae, and Onagraceae. The 
first three families are fairly homogenous. They 
have (2-)3(-4) apertures and аге mostly trian- 
gular, angulaperturate, very often syncolp(or)ate, 


syncolp(or)ate pollen grains of Psiloxylaceae as 
well as Heteropyxidaceae strongly resemble those 
in many Myrtaceae (Schmid, 1980). We agree 
with Johnson and Briggs (1984) that this strongly 
supports the assumption that syncolp(or)ate pol- 
len grains occurred in the common ancestor of 
these three families. 

The Onagraceae are palynologically very dis- 
tinct in the order. The pollen grains are note- 
worthy by the often triangular shape with three 
or more protruding, *'papillose" apertures, the 


1975), and the fine structure of the exine, in par- 
ticular the ektexine, which is granular, “beaded,” 
delicately branched, etc. (Skvarla et al., 1976), 
and especially by the constant presence of viscin 
threads (Skvarla et al., 


and Fabaceae. The relative number per pollen 
grain and the surface structure of these threads 
are variable in Onagraceae and supply some 
characters of interest for the division of the fam- 
ily. It can be claimed that the character-states 
associated with the pollen grains in Onagraceae 
along with many other distinctive features in- 
dicate that the family was differentiated early 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог, 71 


from ancestral Myrtales. At any rate, the exine 
structure as well as the pollen grain shape and 
apertures of the Onagraceae seem to have their 
closest resemblance in Myrtaceae (Nowicke, pers. 
comm.), Psiloxylaceae, and Heteropyxidaceae. 

Muller (1981) in his review of fossil pollen of 
angiosperms noted that probably myrtaceous 
pollen (Myrtaceidites) is known from Santonian 
and Maestrichtian (Cretaceous) of Gabon and 
Colombia, and that onagraceous pollen (cf. Epi- 
lobium type) are also known from the Maestrich- 
tian, whereas the earliest heterocolpate types so 
far known date from upper Eocene (Tertiary). 
The latter, Heterocolpites, are perhaps combre- 
taceous, although similar ones have been claimed 
to be melastomataceous. 

With due consideration given to the yet in- 
complete knowledge of fossil pollen and to M 
uncertainty of pollen identification, the a 
information тау indicate, an earlier diferent 
tion o 
than the heterocolpate ones (cf. the evolutionary 
discussion on pp. 68 

None of the families outside Myrtales, show- 
ing considerable similarities to them, possess 
pseudocolpi, but the tricolporate general pattem 
in Rhizophoraceae is of the basic type found in 
the Myrtales (Lythraceae pro parte, Alzateaceae), 
whereas the pollen grains in Lecythidaceae у 
from colpate to ср ров (via “colporoidate” 
transitions, Erdtm 952 

he porate wt и of Haloragaceae (see 
below) and Thymelaeaceae are different and in- 
dicate that these families are not allied with the 
Myrtales. 


EMBRYOLOGICAL FEATURES 


The main features of embryology of most ee 
the core families of Myrtales, with a num ber 0 
exceptions mentioned below, are rather er 
(Davis, 1966; Mauritzon, 1939; Schmid, 19 


Schnarf, 1931; Tobe & Raven, 1983a; iion d 


Table 1 in Schmid, 1984; Tobe & Raven, m 
The anthers are tetrasporangiate, the en 


BEES 


-— 


t 
GURE7. Distribution, in the myrtalean and some other families, of: — A. dry (®) and wet (О) stigm? s. 


acco cede to prm 


rrison & Shivanna (1977). 
to Corner (1976). 


— B. seed coats with fibrous exotegmen (hatc 


hing) according 


| 


а 


| 


Иос PÓ—M'— 


1984] DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 653 
Rhizophoraceae iit е unn 
; ا‎ 
Haloragaceae E Combretaceae "n 
. TO 
d i AN. 
SS ние = Oliniaceae 4 
ots pe iod Lythraceae и. 
== V / " 
A Onagraceae ч (Combretoideae) \ 
(Strephonematoideae) ў 
(Duaban- Rhynchocalycaceae Memecylaceae \ 
goideae) \ ‘ 
^(Lythroideae) Alzateaceae | 
v. ^(Punicoideae) 
(Sonneratioideae) Crypteroniaceae-(( 7) | 


Heterop xidaceae-( ) У 
: X ои Melastomataceae : 


NC 
Lecythid 
" завы ` Myrtaceae 
* 


N 
| | 
/ | 
| РА ја, 1 
\ ; 74 
K & 6 
d ‚ 
7 : > 
А Nas 6; а зва 
РЕНАН а Thymelaeaceae 
Rhizophoraceae p eem tea ыу. 
Haloragaceae m. Combretaceae e "s 
> P = 
— PE Oliniaceae ne 
<>»? i SE Br : 
: P 
55 à Trapaceae Lythraceae enaeaceae \ 
Pg ; (Combretoideae) X 
» Onagraceae (Stréphonematoideae) ob а 
T (Duaban- Rhynchocalycaceae y 4 
goideae) .' \ 
| ~(Lythroideae) Alzateaceae à 
: / "(Punicoideae) | 
\ (Sonneratioideae) О Crypteroniaceae-(_) \ 
э Heteropyxidaceae О Psiloxylaceae Melastomataceae \ 
Lecythi 7 
" седа > Myrtaceae \ 
ч ^ | 
| | 
| | 
1 и | 
! Let X 1 
i / i 
\ / / 
\ 
t * 
i ~ VE a. Z 
. * --— 2 a9 * 
B м. ~ ^ 
"о — Thymelaeaceae 


654 


cium develops fibrous thickenings, the tapetum 
is glandular, cytokinesis is simultaneous, and the 
pollen grains are bicellular when shed 

The ovules are anatropous, or in various taxa 
hemianatropous or campylotropous. They are 
nearly always bitegmic and always crassinucel- 
late. The micropyle is nearly always formed by 
both integuments. 

Mauritzon (1939) noted a peculiarity, namely 
that in some species of Combretumand in Trapa, 
one or both integuments ceased to grow in certain 
parts, being then replaced by chalazal tissue; this 
was also observed in Phaleria of Thymelaeaceae 
and also occurs in Myristicaceae. 

The integuments of most Myrtales are two- 
layered at the time of fertilization, but in Oli- 
niaceae, Trapaceae, some Combretaceae, some 
Onagraceae, and Cuphea and Punica of Lythra- 
ceae, the outer integument consists of more lay- 
ers. In contrast, both integuments of Lecythi- 

е 


f 
several cell layers (Mauritzon, 1939). Lecythi- 
daceae are also peculiar in that the two integu- 
ments gradually fuse into one. In Myrtaceae, there 
may be total fusion into one single integument 
in a couple of genera. 

A primary parietal cell is cut off from the ar- 
chesporial cell in probably all Myrtales, a differ- 
ence from the Lecythidaceae, where this is not 
the case. In addition, at the time of fertilization 
the nucellus is generally partly intact in the core 
families of Myrtales, whereas in the genera of 
Lecythidaceae and Rhizophoraceae studied, the 
whole nucellus between embryo sac and epider- 
mis is destroyed at this stage. The epidermis may 
or may not divide periclinally to form a nucellar 
cap. Embryo-sac formation, with important ex- 
ceptions (see below), conforms to the Polygo- 
num-type. The synergids are usually hooked, and 
the antipodals are mostly ephemeral [a fact that 
according to Tischler (1917) implies a weakening 
of the basal part of the embryo sac, and thus 
perhaps a first step leading to the Oenothera-type 
of embryo-sac formation found in Onagraceae, 
which lack antipodals]. Endosperm formation is 


The exceptions from the above pattern are no- 
table: 

Lythraceae conform well to the ordinal pattern 
of embryology. A uniseriate or, less commonly, 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


a multiseriate suspensor is present in the embryo | 
(Joshi & Venkateswarlu, 1935a, 1935b, 1936; 

Joshi, 1939). The occurrence of two nucelli with- 

in the same ovule has been reported in several 

cases (species of Cuphea, Lagerstroemia, and — 
Nesaea). The archesporium is multicellular as 
noted by Joshi and Venkateswarlu (1936). Mau- 
ritzon (1934, 1939) found Cuphea to deviate from 
the other genera in the structure of ovule and 
nucellus; also Lagerstroemia was found to be pe- 
ripheral; Mauritzon (1939) found Punica to be 
quite similar embryologically to Lagerstroemia. 
Also с РЕЈ 2 тұ L : +h i^ 


features to other Lythraceae (Venkateswarlu, 
1937; Mauritzon, 1939; Johri et al., 1967). The 
inner integument in Duabanga increases in 
thickness apically to form a considerable tissue, 
but this has not been reported in Sonneratia. 

Trapaceae (Ram, 1956; Trela-Sawicka, 1978) 
are peculiar in their embryology. The ovule has 
a long nucellar beak and thus no ordinary mi- 
cropyle. The endosperm may not be formed at 
all if the primary endosperm nucleus moves 10 
he base of the embryo sac and degenerates (Ram, 
1956), or it is very restricted if the primary еп" 
dosperm nucleus undergoes only one or two di- 
visions (Trela-Sawicka, 1978) to form a few free | 
endosperm nuclei, which degenerate before de- ' 
velopment of the embryo starts. The nutritive 
function of the endosperm of Trapa natans L. is 
taken over by the suspensor and nucellus, which 
in early stages consist of cells with dense cy! 
plasm; later, suspensor and nucellus cells undergo | 
endomitotic polyploidization (Trela-Sawick@, | 
1978). Embryogeny їп Trapa conforms 10 

а 


> 


+ 


suppressed, the other being fleshy and filled po 
starch grains (starchy embryos also occur, 
example, in some Myrtaceae). The anther - 
tum becomes irregularly two-layered and its vp 
become multinucleate with frequent nuclear 
sions 

Oliniaceae (Mauritzon, 1939; Rao & ri 
gren, 1969) have hemianatropous to сатру! 
ropous ovules but otherwise conform well wi 


are 
the myrtalean basic pattern, although data 
ical features- 
including 


у | 
the micropyles of the ovules and seem to supply | 


nutrients to the pollen tubes. Thus they ci 
as an obturator and correspond to the 0 


1984] 


of Thymelaeaceae. Mauritzon (1939) found tet- 
rasporic, 16-nucleate embryo sacs of the Peper- 
omia-type, rather similar to those of the Penaea- 
type (see below), in two species of Combretum, 
but the studies by Fagerlind (1941) on Quisqualis 
and by Venkateswarlu and Prakasa Rao (1972) 
on several genera, including Combretum, showed 
only monosporic embryo sacs, and it is thus 
doubtful that tetrasporic embryo sacs occur in 


DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 


655 


(1967) reported trinucleate pollen grains in most 
genera of the family, Tobe and Raven (1984c) 
report that the grains are strictly 2-celled when 
dispersed, as is the case in all other families of 
Myrtales. The placental epidermis may consist 
of palisade-like cells with a large amount of pro- 
toplasm (Subramanyam, 1948), which has also 
been observed in certain Lythraceae. Subraman- 
yam (1948) also observed that in mature seeds 
of Melastoma malabathricum L. the embryo was 


this family. Th d g that 
а re-examination would be desirable. 

Penaeaceae were studied by Stephens (1909) 
and consistently seem to have a 16-nucleate tet- 
rasporic embryo sac of the so-called Penaea-type. 
Most often four nuclei fuse in the center and after 
fertilization result in a 5-ploid endosperm nu- 
cleus. The family is rather poorly known em- 
bryologically and modern studies are thus very 
desirable. 


According to Tobe and Raven (1984a) the ge- 
nus Alzatea, composing Alzateaceae, agrees with 
other Myrtales in the main embryological fea- 
tures, but has a bisporic, АПит-туре, embryo 
sac. Like Rhynchocalyx (Rhynchocaly ) bu 
unlike other Myrtales, the micropyle is formed 
by the inner integument alone. RAynchocalyx 
(Tobe & Raven, 1984b) shows the Polygonum- 
type of embryo sac formation, differing in this 
characteristic from both Penaeaceae and Alza- 
teaceae. In this respect it exhibits а more basic 


em 


сторује formed by the inner integument alone 
see above), but it agrees with Lythraceae in hav- 
ng a multi-celled archesporium. 

Within the three, rather divergent, genera of 
Crypteroniaceae Axi rat far been stud 
led (Tobe & Raven, 1983b). In this genus the 
micropyle is formed by both integuments, the 
archesporium in the ovule is one-celled, and the 


yde & Teeri, 1967). The tapetal cells in these 
families are uninucleate. Although Brewbaker 


filled with starch grains, which is also the case 
with Trapaceae and some Myrtaceae. Otherwise, 
the ovular conditions conform well with the or- 
dinal account given above. 

M 


mbryological attributes (Mauritzon, 
1939, and later references). T i 


and fruit morphology between ‘Myrtineae’ and 
Lecythidaceae stated by, for example, Niedenzu 
(1893) was not supported by embryology, as Le- 
cythidaceae are very divergent embryologically 
(see below). Within Myrtaceae, the micropyle may 
be formed only by the inner integument (An- 
gophora, Darwinia, Thryptomene, Wehlia) (Da- 
vis, 1968, 1969; Prakash, 1969а, 1969b, 1969c), 
and unitegmic ovules occur in perhaps all species 
of Syzygium. The archesporial cell has rarely been 
observed to cut offa parietal cell, but Davis (1966; 
Prakash, 1969a) suspects that this happens so 
early that it has usually escaped observation. Ad- 
ventive embryogeny is reported in the family, 
and polyembryony is common. 

In Onagraceae (Johansen, 1929, 1934; Davis, 
1966) the embryo sac formation follows the Oe- 
nothera-type and is 4-nucleate, the single polar 
nucleus fusing with a male gamete into a diploid 
endosperm. In this peculiarity, which seems to 
be consistent in the family, Onagraceae are well 
characterized. 

Except for certain characteristic features oc- 
curring in particular families, of which the Pe- 
naea- and Oenothera-types of embryo-sac for- 
mation in Penaeaceae and Onagraceae 
respectively seem to be the most conspicuous, 
there is good conformity among the families of 
Myrtales in embryological ct teristi most 
aberrant member is 7rapa, which, however, 
seems adapted in its embryological syndrome 
characteristic of an aquatic life. 

Among the families with dubious affinity to 


656 


Myrtales, Rhizophoraceae do not deviate con- 
siderably from the Myrtales pattern. The antip- 
odals are not ephemeral as they usually are in 
Myrtales. Any specializations in embryo devel- 
opment (Corner, 1976) of the halophytic man- 
grove genera seem of little significance in dis- 
cussing phylogenetic relationships. 

Thymelaeaceae are very distinct from Myr- 

i bryological гезр (Fuchs, 1938; Da- 
vis, 1966; Corner, 1976; Tobe & Raven, 1983a). 
The pollen grains are tricellular when shed (a 
derived attribute found in Myrtales only in Ax- 
inandra, Tobe & Raven, 1984a). As in many 
Myrtales, however, a parietal cell is cut off from 
the archesporial cell and forms a parietal tissue, 
and also a nucellar cap is usually formed by peri- 
clinal divisions of the nucellus epidermis, which 
occurs in certain Myrtales. Unlike most Myrt- 
ales, however, the antipodals are persistent. An 
obturator of elongated cells from the base of the 
style is characteristic. Similar persistent and pro- 
liferated antipodals and a similar obturator occur 
in Combretaceae. 

As regards Haloragaceae (embryological sum- 
mary by Orchard, 1975), this family must be 
considered in the strict sense (i.e., excluding 
Gunnera and Hippuris). In this circumscription, 
the family yet deviates in embryological respect 
rom Myrtales in some important features. The 
anther wall formation in both Haloragis and 
Laurembergia has, for example, proved to be of 
the monocotyledonous type, although this may 
not be the case in Myriophyllum, and the pollen 
grains ofall tl g hed in the tricellular 
stage. Cellular endosperm formation is recorded 
in Haloragis (Nijalingappa, 1975) and one species 
of Myriophyllum but nuclear endosperm for- 
mation in another species of Myriophyllum and 
in Laurembergia. In all three genera mentioned, 
the embryogeny conforms to the Myriophyllum 
variation of the Caryophyllad type, which has 
not yet been found in Myrtales. The combination 
of attributes does not support the inclusion of 
Haloragaceae in Myrtales. 

Of other families occasionally referred to Myr- 
tales, Hippuridaceae by virtue of the unitegmic 
ovules with cellular endosperm formation fall 
out of the pattern. Even more so do Callitricha- 
ceae, which have unitegmic, tenuinucellate 
ovules, no parietal cell, cellular endosperm for- 
mation, and terminal endosperm haustoria (these 
are totally absent in Myrtales). 

Elaeagnaceae are surprisingly poorly known 


4 
ICSVCUL TE 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


embryologically, but the evidence known is in 
accord with the myrtalean pattern. 
Lecythidaceae (Venkateswarlu, 1952) deviate 
strongly from Myrtales, and the pollen grains are 
sometimes reported to be tricellular when dis- 
persed, which is rare in Myrtales. The ovule is 
tenuinucellate and no primary parietal cell is cut 
rom the archesporial cell, which is a differ- 


much earlier in the development. Some features, 
e.g., the ephemeral antipodials, agree with the 
myrtalean pattern. 

The 1 1 2 


1 VE ndi ES 


talean core families as related. The seven pri- 


plants, and in none ofthe other families that have 
been referred to Myrtales, with the possible ex- 
ception of Elaeagnaceae. 


SEED COAT STRUCTURES 


The seed coat structures in a great number of 
representatives of dicotyledons were studied by 
Corner (1976). In a chapter called “Criticism of 
the arrangement of dicotyledonous families into 
orders," Corner stressed that the families here 
considered the core families of Myrtales fall into 
two groups as follows (Fig. 7B): 

(1) seeds with a fibrous exotegmen composed 
of narrow pitted fibers or elongate tracheid fibers, 
often with sclerotic mesotesta: Combretaceae, 
Onagraceae, Lythraceae, Punicaceae, Sonnera- 
tiaceae (Punicaceae and Sonneratiaceae are here 
included in Lythraceae), Trapaceae, Legnotida- 
ceae; e 

(2) seeds with sclerotic mesotesta but withou 
a special exotegmen: Lecythidaceae, Meme 
laceae, Melastomataceae, Myrtaceae, Penae- 
aceae, Rhizophoraceae (excl. Legnotidaceae) а 

Halo 


to which also Callitrichaceae were referred = 
ever, a position for Callitrichaceae in OF 
Myrtales is out of the question). 
dimid (1976: 37) incorrectly stated e 
first group has tenuinucellate ovules; act i 
they are crassinucellate in all the families: ida- 
second group, with the exception of 5 
ceae, likewise has crassinucellate ovules par 
thidaceae being surely out of place 1n Myra 
Another difference between the groups о“ 


— 


1984] DAHLGREN & THORNE 


by Corner (1976) would be that in the first group 
the seeds are: *exalbuminous, exarillate and pro- 
vided with straight or slightly curved embryos. 
Punica with epidermal sarcotesta seems to pro- 
vide the least specialized and reduced seed.” 
Starch grains often occur in the embryos of Myr- 
taceae, but this is not a general feature of the 
second group. Besides, starch grains occur in the 
seeds of Trapaceae in the first group. Arils are 
also generally absent in the second group except 
for Lecythidaceae, lacking in all Melastomata- 
ceae, Myrtaceae, and Penaeaceae and in most 
but not all genera of Rhizophoraceae. Thus, this 
is not a difference. either. Also ihe жердеди of 


ffarance 


between ihe eroups. The sarcostesta in Punica is 
no doubt a specialization. 

Because the difference in seed coat structure 
was stressed by Corner as important and, to- 
gether with Corner's other arguments, was used 
by Briggs and Johnson (1979) as the basis for a 
distinction between ae and Myrtales, it 
needs some commen 

In group (1) there is ‚ош between taxa 
of the three subfamilies raat 
tioideae, and Punicoideae) of 


dle layers consisting of either a thin-walled me- 
sophyll or a densely sclerotic part (in Lawsonia 
and Lagerstroemia with crystals in the cells) or 
both, or by sclerotic cells only. The innermost 
layer of the outer integument may contain crys- 
tals. The inner integument consists of two layers 
only, an outer layer of narrow longitudinal tra- 
cheids or of narrow thick-walled fibers, and an 
Inner unspecialized layer with elongate thin- 
n cells. These observations support the gen- 

сопс] 1 1 4L kf °1 1 els 


related. 

Onagraceae have a non- -multiplicative outer 
integument ("testa") composed of large, often 
crushed cells, but rarely, as in Oenothera, of scle- 
otic cells. As in some members of the afore- 
mentioned families, the innermost layer of the 
Outer integument consists of crystal-cells. The 
md in Onagraceae, as in the previous fami- 
les, also remains two-layered. The outer layer 
Consists of a lignified fibers. Thus, it 
m Onagraceae belong to the first group of 

es, and in ato resemble some Ly- 
; in seed coat structure. 
Combretaceae may or may not have a multi- 


MYRTALES ¢ 


IIX1/ÀALIL 


657 


À AXZLN 


plicative outer ачен, fhe mesophyll con- 
sisting of thin-walled cell 

or tracheidal cells with more or less reticulate, 
in some cases spiral-annular, wall thickenings. 
The innermost layer of the outer integument is 
composed of sclerotic or tracheidal cells or is 
unspecialized. The inner integument consists of 
an outer layer of elongate, lignified fibers, while 
the other layers are unspecialized or crushed. 


much different. The outer integument is m 
plicative in the large seeds (Memecylaceae) but 
not in the smaller seeds studied (Melastomata- 
ceae). The outer epidermis varies much, from a 
palisade-like layer of radially elongate cells, as 
in some families of the former group, to a layer 
of cuboid cells with thickened outer walls. The 
mesophyll is thin-walled or there may be groups 
of sclerotic cells (as in the previous group). The 
innermost layer of the outer epidermis is unspe- 
cialized or (as in some members of the previous 
group) may consist of crystal-cells. The tegmen 
is not multiplicative and consists of two cell- 
layers. Unlike the families of the first group the 
outer layer of the tegmen in the studied taxa does 
not consist of fibers but is more or less crushed. 

In Myrtaceae, the outer integument in the seed 
may or may not be multiplicative and may or 
may not develop sclerotic tissue. The innermost 
layer may or may not consist of crystal-cells, the 
cell walls in this layer may be thin or thick an 
lignified, or may even be developed as radially 
elongate sclerotic cells at the micropylar end. As 
in group (1), the inner integument is not multi- 
plicative, but mostly unspecialized and crushed; 
however in Psidium the outer layer may have 
slight, unlignified thickenings. 

In the above variation Corner (1976) lays most 
stress on the occurrence of fibers or tracheids in 
the exotegmen, i.e., the outermost layer of the 
inner integument. However, tracheidal cells may 
be present in the endotesta, i.e., the innermost 
layer of the outer integument, as in Combreta- 
ceae, but not in Lythraceae studied. The presence 
of sclerotic cells to some extent seems to com- 
prise a typical feature in ‚мун The several- 


notable, as is its Ена ошег t 
An evaluation of these differences can e 
only in the light of a more complete uacua 
of the variation in each family. 

A division of Myrtales into two orders was 
suggested by Corner (1976), largely on the basis 


658 


of seed coat structure. The seed coat structures 
in Myrtales are so divergent, however, that these 
can hardly be the main basis of such a rearrange- 
ment, although the occurrence of a fibrous exo- 
tegmen is perhaps important for relating some 
families to each other and contributes a piece 
of evidence for including Sonneratiaceae and 


proved inaccurate or only partly true. To the 
former category belongs the statement that ten- 
uinucellate ovules characterize the Lythraceae 
group (see above). Development of stamens, oc- 
currence of starch in the embryos, etc., do not 
provide any differences between the suggested 
orders. Briggs and Johnson (1979), who accepted 
a division of Myrtales largely according to Cor- 
ner’s views, subsequently have abandoned this 
view. 


CHLOROPHYLLOUS/ACHLOROPHYLLOUS 
STATES OF EMBRYO IN SEED 


The occurrence of chlorophyllous embryos in 
seeds was presented by Yakovlev and Zhukova 
(1980) and discussed by Dahlgren (1980b). Chlo- 
rophyll formation in the embryo of seeds nor- 
mally seems to be dependent on availability of 
light to the embryo in the course of its devel- 
opment and thus is generally absent in seeds with 
copious endosperm and in seeds enclosed in a 
thick testa or pericarp. 

In Myrtales, the embryo is usually achloro- 
phyllous despite lack of endosperm. The records 
in the order are few, however. Chlorophyllous 
embryos were found in the mangrove genus La- 
guncularia of Combretaceae, in two species of 
Memecylon of Memecylaceae, in Sonneratia of 
Lythraceae, and in two species of *E ugenia" (— 
Syzygium) of Myrtaceae. The records of achlo- 
rophyllous embryos are distributed through the 
order and include all families investigated except 
Memecylaceae. No taxonomic conclusions can 
as yet be drawn on the basis of this feature. The 
few studied taxa of Haloragaceae and Thyme- 
laeaceae have achlorophyllous embryos, in which 
they agree with most Myrtales. 


CHROMOSOME NUMBERS 


Raven (1975) gives a summary of the chro- 
mosome numbers for the Myrtales. He concludes 
that as the base number is X — 12 in Trapaceae, 
Oliniaceae, and Combretaceae, and as this num- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


ber has also been reported for both Psiloxylaceae 
and Heteropyxidaceae (Johnson & Briggs, 1984), 
it is likely to be the original basic number for the 
order as a whole (or, less plausibly, X — 11, which 
Raven assumed to be the original base number 
in Myrtaceae and Onagraceae). 

Onagraceae (Raven, 1975) have X = 11, which 
is found in Fuchsieae and Circaeeae and in the 
more primitive taxa of Lopezieae and Onagreae. 

Trapa (Trapaceae) has X = 12. 

Within the Lythraceae, Lafoénsia has a chro- 
mosome number of n = 10, Lagerstroemia n = 
22-25, Lythrum n = 5, Heimia п = 8, Nesaea 
n = 30, Peplis n = 5, Rotala n = 16, Woodfordia 
n = 8, and Cuphea n = 6, 8, or 9, which suggests 
a basic number of the family of X — 8. This also 
seems to be the basic number in other genera not 
mentioned here (Graham, pers. comm. in Ra- 
ven, 1975). Punica, as most other Lythraceae, 
has л = 8, while Duabanga has X = 12 and Son- 
neratia X — 9 or 11 (Muller & Hou-Lin, 1966). 

Penaeaceae (Dahlgren, 1968, 1971) have n= 
10, as in Rhynchocalyx (Goldblatt, 1976). The 
chromosome numbers in Crypteroniaceae, 48 
circumscribed here, are not known. In Meme- 
cylaceae, Memecylon has X — 7 and Mouriri (one 
count only) п = 12, whereas several pipes 


, 


12, and 9. Oliniaceae and Combretaceae, which 
show some other similarities, both are report к 
to have the basic chromosome number oi А = 
12 

Thymelaeaceae have a probable base number 
of X = 9. Finally, Haloragaceae (excl. Gunnera 
and Hippuris) have X = 7, Rhizophoraceae п = 
32 (tribe Macarisieae) and n = 18 (tribe Rhizo- 
phoreae), suggesting base numbers of X т 8 and 
9; whereas, the base number of есуй н 
may be difficult to establish, п = 13, 16, 17, P. 
18 being some numbers reported in that family. 
Chrysobalanaceae have п = 10 or (more often) 
11. Finally, it may be mentioned that RS 
пасеае have a base number of Y= 12 9508 
11 in the tribe Colletieae (Raven, 1975). : 

The chromosome base numbers of the Му 
tales, as compared with those in other mA 
do not support inclusion of Lecythidaceae e ) 
order (rather Lecythidaceae fit with the Theales А 
though Rhamnaceae agree better (Х = 12 being, 
however, a base number in many complexes) 


CHEMICAL CHARACTERISTICS 
comprise : 
of chemical 
69, 1973). 


Myrtales, as circumscribed here, 
fairly homogenous complex in terms 
contents (Hegnauer, 1964, 1966, 19 


| 
[ 


— 


1984] DAHLGREN & THORNE 


Tannins. All families of Myrtales appear to 
contain tannin plants. In most of the families the 
tannins consist of the condensed type as well as 
of galli- and ellagi-tannins. Ellagic acid, accord- 
ing to Bate-Smith (1962), occurs in all studied 
taxa of Lythraceae (incl. Punicaceae), Combre- 
taceae, Melastomataceae, Myrtaceae, and Ona- 
graceae and, according to Lowry (1976), in Ly- 
thraceae subfam. Sonneratioideae; probably it is 
present in virtually all members of the Myrtales. 
Even a water plant like Trapa is known to be 
rich in tannins, the pericarp containing up to ten 
percent or more (Gnamm, 1949)! Species of 
Combretaceae, which are rich in gallyol- and el- 
lagi-tannins as well as condensed tannins, are 
used for tanning. 

Hegnauer (1969) concluded that “раіс and 
ellagic acids and tannins derived from these, as 
well as cond i tannins which are derived from 
flavon-3-oles and flavon-3,4-dioles, are char- 
acteristic of the order Myrtales." 

Tannins are also present in rich quantities in 
Rhizophoraceae. Bate-Smith (1962) recorded 
small quantities of ellagic acid in Cassipourea, 
but not in Rhizophora; whereas Lowry (1976) 
reported ellagic acid in species of Anisophyllea 
and Bruguiera as well as in Rhizophora. In Hal- 
oragaceae ellagic acid has been reported (Bate- 
Smith, 1962) for Haloragis as well as Myrio- 
phyllum, in Elaeagnaceae for Elaeagnus and 
Hippophaë, and in Lecythidaceae for Couropita, 
Eschweilera, and Lecythis. All these groups are 
tannin plants in the wide sense. Thymelaeaceae, 
however, consistently seem to lack ellagic acid 
and accumulate no tannins, an important differ- 
ence from all Myrtales. 

: The flavonoid profile (Bate- 
Smith, 1962; Gornall et al., 1979) in Myrtales 
" based mainly on common flavonols and 
their O-methyl derivatives (e.g., delphinidin, 
Cyanidin, pelargonidin, quercetin, kaempferol, 
O-methylated anthocyanins, and, quite 

Proanthocyanidins). The methylated and oxy- 

fl 


acid and quercetin. Glycoflavones are reported 
in at least single genera of each of the Lythraceae, 
Combretaceae, and Myrtaceae, and occur in all 
tribes except Onagreae and Epilobieae of the On- 
agraceae (Averett & Raven, 1983). In fact, gly- 
Coflavones may be widespread in Myrtales. Fla- 
vones are noticeably poor in the order. Caffeic 


MYRTAI FES 


AIIXI/AÀALILO 


659 


اا4 


acid is also rare in the order, except in Onagra- 
ceae (Bate-Smith, 1962). 

he flavonoid pattern for Thymelaeaceae 
(Gornall et al., 1979) is different from that in 
Myrtales. Methylated flavones, C-glycoflavones, 
and luteolin/apigenin are reported, whereas del- 
phinidin, cyanidin, pelargonidin, O-methylated 
anthocyanins, and myricetin are not recorded. 

Rhizophoraceae are known to possess cyani- 
din/pelargonidin, myricetin, quercetin/kaemp- 
ferol, and proanthocyanidins, and thus agree 
rather well with the myrtalean profile. Also Hal- 
oragaceae agree with Myrtales in flavonoid pro- 
file and, like Rhizophoraceae, seem to lack or be 
poor in flavones, as are Myrtales. In addition, 
Myrtales agree fairly well with Theales, Rosales, 
and other orders, such as Geraniales and Bal- 
saminales, in flavonoid contents. 

Essential oils. Myrtaceae are the only family 
in Myrtales with rich production of essential oils. 
The essential constituents of these (Penfold, 1948) 
in many cases are monoterpenes and, often to a 
considerable proportion, sesquiterpenes. Oils of 
phenyl-propane type are rarer. Characteristic of 
myrtaceous oils are phloroglusin derivatives of 
the baeckeol, eugenin, and tasmonol types. 

Essential oils are also present in flowers of 
Lawsonia (henna plant) of Lythraceae. 

Although Thymelaeaceae are not essential-oil 
plants, and lack ducts, the wood of some taxa 
contains essential oils. 

Triterpenes; triterpene saponins. Triterpenes 
are widely distributed throughout the order Myr- 
tales, and triterpene saponins are recorded from 
Combretaceae and Myrtaceae, although they are 
rare in the latter family. The occurrence of tri- 
terpene saponins in the other core families of 
Myrtales is uncertain or, at least, not common. 

It is noticeable that the saponin barringtogenol 
has been recorded in Combretaceae and Bar- 
ringtonia (of Lecythidaceae sensu lato) only, but 
the phylogenetic significance of this condition is 
uncertain. 

Triterpene saponins are also known to occur 
in Haloragis of Haloragaceae, and richly so in 
the fruits of Shepherdia of Elaeagnaceae, but also 
in some Thymelaeaceae. 

Cyanogenesis. Cyanogenic compounds oc- 
cur in several families of the Myrtales, viz., in 
Memecylaceae (Memecylon), Myrtaceae (Euca- 
lyptus), Lythraceae (Lawsonia), and Onagraceae 


Olinia (Oliniaceae) are reported to smell like 
“bitter almonds,” indicating cyanogenic com- 
pounds related to prunasin. 


660 


Cyanogenic compounds are also known in 
Haloragaceae (Haloragis and Myriophyllum). 

Alkaloids. Alkaloids are scattered in Муг- 
tales and are reported in the families Combre- 
taceae, Lythraceae (incl. Punica), Melastomata- 


their presence has not been confirmed and t 
report is most likely incorrect. 

Within Combretaceae the genus Quisqualis 
seems to contain a pyridin base. Lythraceae are 
richer in alkaloids and produce an interesting 
type of quinolizidine alkaloids not known from 
any other plants (Fujita et al., 1971; Seigler, 1977). 
Punica produces alkaloids similar to the better 
known tropane types, the chief being isopelle- 
trierin, N-methylisopelletrierin, and pseudopel- 
letrierin (Hegnauer, 1969), while others remain 
to be identified. Positive alkaloid reactions have 
been obtained for the genera Memecylon (Me- 
mecylaceae) and Clidemia and Sonerila (Melas- 
tomataceae), but these alkaloids have not been 
isolated. Alkaloids are rare in Myrtaceae, but 
alkaloid reactions have been obtained for a num- 
ber of genera; they await further analysis. 

Among other families associated with Myr- 
tales, Rhizophoraceae are characterized by their 

Ikaloids, which include hygrolintropine, and 
pyrrolizidin (necine) derivatives. Some of the al- 
kaloids contain sulfur 

aloragaceae seem to be alkaloid-free or al- 
most so (Orchard, 1975), while Elaeagnaceae 
contain tryptofan derivatives (Boit, 1961) such 
as elaeagnin and serotonin. Alkaloids are rare 
and little known in Thymelaeaceae. 

ere does not seem to be a consistent ten- 

dency in the alkaloid contents of the myrtalean 
and “possibly-myrtalean” families; the alkaloid 
contents in several families still largely remain 
to be analyzed. 

uinones. Napthaquinones are known to oc- 
cur in some taxa of Myrtales. The napthaquinone 
lawsone is known in Lawsonia of Lythraceae (also 
in Impatiens of Balsaminaceae). Lawsone ac- 
counts for the color in henna, which is used for 
dyeing hair and nails. Quinones (of unknown 
structure) are also known in Dichaetanthera of 
Melastomataceae (Hegnauer, 1969). 

Anthraquinones are KAONA in 1 Sonneratia (Ly- 
thraceae). The occurr us offers 
no taxonomically useful information. 

Aluminum accumulation. Aluminum accu- 
mulation (Chenery, 1948) is noticeable in 
Crypteroniaceae (Crypteronia) and especially in 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


Le Ps | A 9 1 ГА 


10,000 р.р. т. in several genera). Aluminum ac- 
cumulation occurs also іп Rhizophoraceae 
subfam. Anisophylleoideae (Anisophyllea, Com- 
bretocarpus, and Poga), but not in the other rhi- 
zophoraceous subfamilies (Chenery, 1948; Che- 
nery & Sporne, 1976). 

Mucilage. Mucilage cells characterize some 
families of Myrtales, viz., Combretaceae, Ly- 
thraceae, and Melastomataceae (quite often, 
Hegnauer, 1969). The mucilage contains sugars 
and is often acid in reaction. 

Storage substances in the seed. The seeds of 
myrtalean families mostly have a large and well- 
developed embryo, whereas the endosperm tis- 
sue is absorbed in the course of the seed devel- 
opment. Therefore, we are chiefly concerned here 
with the contents of the embryo. In most fami- 
lies, the embryo stores fatty oils and proteins, 
but it sometimes stores starch in Melastomata- 
ceae and Mice and always does in Trapa- 
ceae. Endosperm may be present or absent in 
Rhizophoraceae. If the latter, the embryo is large 
and stores fat and protein, which is also true in 
most Lecythidaceae, Thymelaeaceae, Elaeagna- 


195), in a somewhat resigned comment, sum- 
marizes: "One must frankly admit that so far 
chemistry cannot give a decisive contribution to 
the problem of the descent of the Myrtales. Sim- 
ilar polyphenolic and triterpene a occur in 
е Theales, Rosales, an Myrtales.” 
e families of Myrtales lack polyaceylenes 
ib substances, and benzylisoquino 
kaloids. The occurrence of such compounds in 
any taxon referred to the Myrtales indicates 
against inclusion of that group in the order. 
The presence of tannins, both galli- and ellagi- 
tannins and tannins of the condensed je 
typical of the order, and the flavonoid spect 
is characterized by the presence of flavonols A: 
cluding methylated flavonols), whereas. puc 
(except glycoflavones) are absent or near arly 50 3 
the families studied. Triterpenes are == 
istically present, ne saponins are t0 
in various representatives. Aikalóidé 


: nt à 
several families, but again does not t represe 


alu- 
typical attribute of the order. Considerable 


~ 


Е 


—— 


1984] 


minum accumulation occurs in Crypteroniaceae, 
Memecylaceae, and Melastomataceae and may 
indicate affinity among these families, but this 
affinity is better shown by other attributes. The 
seeds have but little endosperm and their em- 
bryos usually accumulate fat and ale 


mataceae and the Trapaceae which store starch; 
this character is obviously of little phylogenetic 
significance. Myrtaceae, Heteropyxidaceae, and 
Psiloxylaceae deviate from the other families in 
their rich contents of essential oils. 

The possession in Thymelaeaceae of poison- 
ous compounds, coumarins of the daphnetic and 
daphnoretin type, and the lack of tannins and 
ellagic acid t indicati that this family 


should not be associated with Myrtales, but that 
It may have close relationship with the Euphor- 
biaceae. 

Rhizophoraceae agree rather well with Myr- 
tales in the main chemical features, although the 
alkaloids present in subfam. Rhizophoroideae are 
absent from Myrtales. Otherwise the tannin con- 
lent (incl. ellagi-tannins), flavonoid spectrum, 
mucilage cells, aluminum accumulation, and oil- 
по Seeds аге in agreement with myrtalean fam- 
ilies, and Rhizophoraceae cannot be separated 
ftom this order on chemical grounds. 

Also Haloragaceae (excl. Gunnera and Hip- 
Puris) show a similar pattern; ellagic acid, quer- 
cetin, kaempferol, etc. are typical. Saponins and 


in Theales; hence, the position of the family does 
not become obvious from chemistry. 
Elaeagnaceae agree with the myrtalean fami- 
lies in general chemical features but the accu- 
mulation of L-quebrachite and the tendency for 
accumulation of indole bases and of sinapinic 
acid are not in accordance with Myrtales (Heg- 
паџег, 1966). 

By their possession of iridoids in at least some 
genera the families Escalloniaceae (or Escalloni- 
ideae of Saxifragaceae), Icacinaceae, Hippuri- 
daceae, Loganiaceae, and Callitrichaceae are 
deemed distantly related to Myrtales. 


THE CORE FAMILIES OF MYRTALES 


Myrtales, like Caryophyllales (or Chenopodi- 
ales), are one of the few larger orders that have 


DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 


661 


«€ 


a rather uncontroversial circumscription as re- 
nucleus" or *core" famili 


ese entities may 
not necessarily be entitled to familial status, but 
in essential points this does not make a great 
difference. (See p. 635 for the preferred classifi- 
cations of each of the two authors.) 


ONAGRACEAE A. L. DE JUSSIEU (1789) 


This family has 17 genera and ca. 675 species 
(Raven, 1964, 1976, 1979), ranging from the 
tropics to (especially in Epilobium) arctic-alpine 
habitats. Through the works of Munz, Raven, 
and associates, the family has become one of the 
most thoroughly investigated among the angio- 
sperms. Although most genera are herbaceous, 
some are woody, and the leaves are opposite, 
alternate or, more rarely, verticillate, and in some 
tribes have minute stipules (Fig. 2A—E). The leaf 
teeth are of the fuchsioid (a variant of rosoid) 
kind (Hickey, 1981). The vegetative parts are 
rich in oxalate raphides, which is another un- 
usual feature in the es. The flowers are 
epigynous, generally 4-merous, but 2-merous in 
Circaea and to 7-merous in species of Ludwigia, 

mery urring also within several genera 
(Eyde, 1977). The flowers are provided with a 
variably long hypanthium (lacking in Ludwigia, 
Lopezia, and sporadically in other genera). There 
are generally two staminal whorls or, by reduc- 
tion, a single whorl in the flowers. By dislocation 
in the bud, these often appear to be in an ob- 
diplostemonous position although the initials 
show a diplostemonous organization. Weak zyg- 
omorphy occurs in Epilobium (Chamaenerion), 
Clarkia, and Heterogaura, and strong zygomor- 
phy in Lopezia. The reproductive biology (Ra- 
ven, 1979) is varied, bird-pollination occurring 
in most species of Fuchsia and some species of 
Lopezia, Oenothera, and Epilobium. The pollen 


CA 
, 


1975) 

Ba AAA F YULIY Y ~ a ? 
and are generally conspicuously triangular and 
о- . Th ve various patterns of 


angulo-ape 

exine stratification (Skvarla et al., 1976). Most 
conspicuously they have viscin threads in all but 
one species (Circaea alpina L.; Skvarla et al., 
1978), the last mentioned feature matched only 
in certain Ericaceae and Fabaceae. Pseudocolpi 


662 


are lacking. The carpels (and locules) are gen- 
erally isomerous with the perianth whorls; in cer- 
tain taxa the septa are incomplete in the upper 
part of the ovary. The ovules are usually nu- 
merous, and in most features have a myrtalean 
embryological pattern, although they are con- 
spicuously distinct in having the monosporic, 
4-nucleate Oenothera-type embryo sac forma- 
tion. Antip s are lacking, and the endosperm 
is diploid. The fruit in most genera is a loculicidal 
capsule, but may be a berry (Fuchsia) or an in- 
dehiscent dry fruit (Circaea, Gaura, etc.) with a 
variable number of seeds. The seeds in the tribe 
Epilobieae are generally provided with a tuft of 
trichomes and have a taxonomically useful sur- 
face sculpture. The embryo lacks starch grains. 

Eyde (1981) provides strong evidence that 
epigyny has evolved separately in two lines with- 
in the onagraceous ancestors: in one line leading 
to Ludwigia, which has nectaries on the ovary 
summit, and one line leading to the other Ona- 
graceae, which have nectaries on the tube side 
of the gynoecium-tube junction. Differences in 
vasculature and other details support this con- 
clusion (Eyde, 1981). 

The Onagraceae are a very distinctive family, 
and differ from other Myrtales in several fea- 
tures. The similarities to Lythraceae in teeth 
structure and marginal ciliation of leaves pointed 
out by Hickey (1981), and the fibrous exotegmen 
of the seeds and the similar petal venation are 
some other conspicuous attributes which may 
indicate a quite close connection between the 
Onagraceae and Lythraceae. 


TRAPACEAE DUMORTIER (1829) 


This family consists only of the genus Trapa, 
which, excluding introductions, currently has a 
temperate to tropical Old World distribution. The 
number of species is perhaps three, although as 
many as 30 self-pollinating races have some- 
times been considered as species. The plants are 
floating aquatic herbs with decussate leaves, con- 
centrated in rosettes on the branch ends; the leaves 
are caducous and replaced on the submersed 
stems by chlorophyllous roots. The stems have 
bicollateral vascular bundles and the leaves ru- 
dimentary stipules, supporting a myrtalean affin- 
ity. The floating leaves have marginal teeth with 
a a unique double apex. The flowers are axillary, 


еріел rh 
£ynous, wi 


four valvate вера] lobes, four: ble petals, and 
four stamens alternating with the petals. The pol- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


len grains are triangular, and have three merid- 
ional ridges. They can be interpreted as possess- 
ing intercolpate depressions. The ovary is 
bilocular with one pendulous ovule in each loc- 
ule, but only one ovule develops into a seed. The 
family has a unique embryology: the embryo sac 
formation follows the normal type, but endo- 
sperm formation hardly takes place at all. The 
embryo sac becomes prolonged, and copious nu- 
trient tissue including starch grains are accu- 
mulated in the embryo, which has one large and 
one rudimentary cotyledon 
The family has often ва included іп Ona- 
graceae, but it lacks the viscin threads on the 
pollen grains, epigynous flowers, and the 4-nu- 
eae Oenothera-type embryo sac of that family. 
er, it seems more closely related to the Ly- 
аьа. although there is no obvious link be- 
tween the two families. 


LYTHRACEAE JAUME ST.-HILAIRE (1805) 


This family, with са. 29 genera and са. 585 
species (see Shaw, 1973; Schmid, 1980; Cron- 
quist, 1981) is here more widely circumscribed, 
including Punicaceae Horan. as well as Sonnera- 
tiaceae Engl. & Gilg. It is widespread and occurs 
in various climatic zones of the New and Old 
World, with a concentration in the tropical and 
subtropical regions. Its new circumscription 
makes it rather vaguely defined, the newly in- 
cluded genera having epigynous flowers and sta- 
mens attached on the inside of the hypanthium 
or on its rim. With various of its genera it pos- 
sesses a combination of features that are т 
as basic (plesiomorphic) in the order, їп whi ; 
it takes a central position. The amplitude of vari 
ation is considerable. «di 

The family includes herbs and shrubs as не 
as fairly large trees (Lagerstroemia, Таў 
Sonneratia, Duabanga). The leaves аге od 
more rarely disjunct-opposite, ог verticillate, " 
the leaves are entire or sometimes indistint 
dentate (“cryptic teeth”). The stipules show 
vancement through their dissection into e 
trichome-like structures displaced into the 
axil (see Diplusodon, Fig. 8С). 

Branched foliar sclereids are absent ii 
Lythraceae; they are reported to occur xp а s 
Sonneratia and Duabanga. vo sc 
eids occur rarely in other gen but in 

The flowers are usually P incite i 
Cuphea and Pleurophora are zy8° gus най 
Woodfordia approaches this condition. Р 


jn most 


— — — ~ 


663 


1984] 


nous or hemi-epigynous flowers occur in Sonne- 
ratia, Duabanga, and Punica, but not in the 
subfamily Lythroideae. The flowers in Lythra- 
ceae exhibit a variety of merous conditions: 4-, 
5-, or 6-mery being the most common (but to 
16-mery occurs in Lafoénsia, to 9-mery in La- 
gerstroemia, and to 8- чпегу.1 in | Punica and Son- 
neratia). Tl Ade- 
naria, Pehria, Pemphis, and Woodfordia. The 
calyx-lobes are valvate. One pecularity that oc- 
curs in a considerable number of genera, incl. 
Lythrum, Nesaea, Rotala, and Diplusodon (Fig. 
8G), is the presence of tooth- and spur-shaped 
structures isomerous and alternating with the 
often shorter calyx-lobes; these are nothing but 
extensions from the calyx-lobe base (and should 
not be confused with an outer whorl of perianth 
members), and no doubt can be regarded as a 
specialization (sometimes secondarily lost). The 
petals in Lythraceae have a peculiar, pinnate ve- 
nation, a feature which Chrtek (1969) regarded 
as a derived attribute, but еца has its coun- 
terpart in Onagraceae (and thus may be a syn- 
apomorphy for the two йй), Petals are 
sometimes absent through reduction and vary 
widely in relative size and in color (though being 
usually crimson, pink, or white). When present 
they are often а исте and may be reminis- 

t of petals in Malpighiaceae in the crinkled, 
undulate structures. 

Stamens more than double the number of se- 
pals are found in Punica and Sonneratia, but also 
in Lagerstroemia and species of Diplusodon, Gi- 
mee Неша, Heimia, Nesaea, and Physocalym- 


alternate with the sepals, as in Tetrataxis (Gra- 
& Lorence, 1978) and species of Nesaea 
(Graham, 1977), or may be opposite to them, as 
in other species of Nesaea and in species of Ro- 
‘ala, Peplis, Ammannia, and Lythrum. Two sta- 
mens or only one are found in species of Rotala 
and two or four stamens in Didiplis diandra 
Wood. Th £1 eR УК art : 4 (th 


long filaments in Lafoénsia inrolled) in bud, and 
are usually inserted on the inside of the receptacle 
between its base and middle, closer to the rim 
in Lawsonia, on the distal inner side of the hy- 
Panthium in Punica, and near or on the very rim 
in some advanced species of Cuphea and in Son- 
neratia and Duabanga. (The last condition is typ- 
ical of nearly all other Myrtales except some 
Combretaceae. ) The anthers generally lack strong 
Pecialization, and the connective is less devel- 
Oped than in Crypteroniaceae, Penaeaceae, Me- 


DAHLGREN & THORNE—MYRTALES 


МР 


mecylaceae, ог Melastomataceae, but have a 
broad connective in several woody genera (Ca- 
puronia, атша. Orias, and Tagen). 

Th y variable for 
the order and include heterocolpate types with 
pseudocolpi either isomerous to or double the 
number of the apertures as well as colporate or 
porate types without pseudocolpi. Porate pollen 
grains occur in Cuphea (Graham & Graham, 
1971) 

The common division of Lythraceae subfam. 
Lythroideae is according to whether the ovary is 
more or less completely septate (Nesaeeae) as is 
the case in subfam. Punicoideae and Sonnera- 
tioideae, or whether the septa are incomplete in 
the upper part of the ovary (Lythreae). The em- 
bryology of Lythraceae is of the common type 
compatible with the family’s basic position in 
the order. The fruit is capsular or baccate, the 
seed of Punica deviating by its sarcotesta. 

(Much of the above, detailed information has 
been received from A. Graham & S. Graham.) 

Punicaceae Horaninow (1834) has been in- 
cluded here, as a subfamily of the Lythraceae. It 
consists of Punica with two species, P. granatum 
in southern Europe and western Asia, and P. 
protopunica Balf. f. on Socotra [this latter species 
has been placed in the segregate genus Socotria 
by Levin (1980)]. The fairly large, bright red 
flowers are epigynous, 5-8-merous in calyx and 
corolla, and provided with numerous stamens, 
the filaments of which are attached to the inner 
side of the hypanthial tube. The stamens develop 
in centrifugal succession as in Lagerstroemia. The 
carpels are 7-15 and in P. granatum are situated 
on two levels, but in P. protopunica form an 
ordinary syncarpous ovary. The fruit has a leath- 
ery pericarp and the seeds are pulpy from the 
edible sarcotesta. Punica is technically easy to 
separate as a family, Punicaceae, and is usually 
treated on the family level. 

Also Sonneratia and Duabanga are generally 
ang together, as the family Sonneratiaceae 

. & Gilg, with perhaps ten species. Sonner- 
ia consists of mangrove trees, Duabanga of 
lowland forest trees. They differ from the Ly- 

having branched foliar sclereids, and 
the flowers are hemi-epigynous, relatively large, 
and have a carnose hypanthium and calyx. Un- 
like other Lythraceae with numerous stamens, 
those in Sonneratia seem to develop centrip- 
etally. The pollen grains (Muller, 1969) do not 
possess any distinct pseudocolpi (although their 
outline may approach a *heterocolpate" type); 


664 ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL 71 


Ке: 787 ШЕ 
uM go СУЯ 
(ud MSE ЭМ 


GURE 8. Diplusodon sigillatus Lourt. (Irwin et al. 12447 from Brazil).—A. branch.—B. leaf, upper am 
Nri side (left and right respectively). —C. leaf base нат: axillary stipules.—D. flower, pde t 
note that the petals are m on hypanthium rim n daxial “knee.” —E. $ ns in differ" 


views.— Е. ovary in longitudinal and transversal sect 


28, calyx іп fruiting stage, showing ing processes 
calyx lobe bases (see text). — Н. fruit.—I. seeds. (Ora. pe. E jose) 8 tag. 


Ми 


о 


1984] 


they are porate, as in some other Lythraceae, e.g., 
Diplusodon. 

The two genera differ from each other in a 
number of characters, and it seems questionable 
whether they are closely enough related to be 
treated together in the same subfamily. The dif- 
ference in wood anatomy, demonstrated by van 
Vliet and Baas (1984); the different chromosome 
number; the different inflorescence type and fruit, 
etc., indicate that they are not particularly closely 
allied and some of the similarities that have been 
used to justify the previous family, Sonnerati- 
aceae, are likely to depend on convergence. We 
suggest that each ofthem be treated as a subfamily 
(Sonneratioideae, Duabangoideae) under Ly- 
thraceae. 

Also the genus Rhynchocalyx, treated below 
in the family Rhynchocalycaceae (see below), is 
often included in Lythraceae. 


OLINIACEAE ARNOTT EX SONDER IN 
HARVEY & SONDER (1862) 


This family consists of a single genus, Olinia, 
with perhaps eight or ten species (Rao & Dahl- 
gren, 1969), of trees with opposite leaves, small 
supules (Weberling, 1963), and unicellular hairs. 
The inflorescence is paniculate, with the branch- 


is basally subtended by a short internode ending 

with some blunt teeth, a “‘calyculus,” which is a 

stem structure. The flowers are epigynous, 4-5- 

merous (Fig. 9E), and have a tubular hypanthium 

Mus des beyond the ovary. On the rim of this 
Danthinm = 


f ТАћес 


e four or gate white lobes, 

Which probably represent the calyx, and, inside 
these, and filling up most ofthe hypanthial mouth, 
p five thick, incurved, scale-like structures, 
which are best interpreted as petals. Below these, 
and inserted on the upper part of the hypanthial 
tube are the 4—5 isomerous stamens. The sta- 
Pein which are thus antepetalous, have a short 
lament and an anther with a carnose central 


" hemisphere of the pollen grain (Patel et al., 
е a The inferior ovary is 2-5-locular with ax- 
д р centae. The style is short, and in our ma- 
па] the stigma reaches the level of the anthers. 
Whether the flowers are self-pollinated or not 
ы Study. The embryology contributes no 
eptional details, and the embryo sac, contrary 


DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 


665 


to that in Penaeaceae, is monosporic and 8-nu- 


, in various respects, 
Combretaceae, Penaeaceae, Rhynchocalycaceae, 
Alzateaceae, and Lythraceae sensu lato, but is 
sufficiently different from all to be regarded as a 
distinct family. The interpretation ofthe "scales" 
as petals makes the flower correspond with Pen- 
aeaceae, where the stamens are alternisepalous, 
and Rhynchocalycaceae, where small petals al- 
ternate with the sepal lobes and are situated as 
hoods next to the stamens (in a fashion remi- 
niscent of certain Rhamnaceae). Oliniaceae re- 
semble the Combretaceae in chromosome num- 
ber (X — 12), epigyny, and certain other details 
(see p. 682). 


COMBRETACEAE R. BROWN (1810) 


This family of ca. 20 genera and 400 species, 
occurring both in the Old and the New World, 
and particularly common in subtropical and 
tropical Africa, consists of trees, shrubs, and lia- 
nas, including mangroves, with alternate, op- 
posite, or verticillate leaves lacking stipules or 
with minute stipules which are displaced into the 
leaf axils and dissected into multicellular glan- 
dular hairs (some species of Terminalia and 
Buchenavia). The stomata are anomocytic except 
in Laguncularia and Lumnitzera, where they are 
cyclocytic (Stace, pers. comm.). The trichomes 
consist of club-shaped or peltate glandular hairs 
and of nonglandular hairs which are of a dis- 
tinctive type (“combretaceous hairs" of Stace, 
1965, 1980). The inflorescences may be terminal 
on branchlets, as well as axillary, and consist of 
racemes, spikes, or heads with small or medium- 
sized, epigynous flowers with a usually fairly short 
hypanthium (sometimes absent or in Quisqualis 
to 8 cm long). This bears on its rim 4–5(–8) sepal 
lobes and equally many, mostly rather small pet- 
als, which are often lacking, as in Pteleopsis (Fig. 
10). There are one or two staminal whorls, the 
outer sometimes having two or three times the 
normal number of stamens. The filaments are 
often long and colored, as may also be the whole 
flowers, and are inflexed in bud; and the anthers 
only rarely (Thiloa) have a “massive,” fleshy 
connective. As in several related families, the 
pollen grains possess pseudocolpi (absent in 
Strephonema) and are tricolporate or triporate. 
A well-developed intrastaminal disc is very often 


666 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Уо. 71 


И 
К 


dios Ss alae 


FiGure 9. Olinia aequipetala (Delile 
et al. 532; B, J-K. Friis et al. 1228.—A. 


gitudinal section. – С. stamens, lateral and adaxial view. 4, B. Johnsen) 


- — —— = 
- — и нь 
> 


— — 


аа 


1984] 


present. The mostly inferior ovary is 2—5-car- 
pellate and unilocular, with 2(—6) pendulous 
ovules. An obturator tissue resembling that in 
Thymelaeaceae is sometimes present, which has 

n one reason for a suggested relationship 
between the two families. The embryology oth- 
erwise seems to be more or less of the basic myr- 
talean type [the occurrence of 4-sporic, 16-nu- 
cleate embryo sacs described by Mauritzon (1939) 
needs to be verified]. The fruit is generally one- 
seeded and indehiscent, rarely dehiscent; it is 
mostly leathery or drupaceous and often provid- 
ed with conspicuous wings or ribs. 

The family is dominated by the large genera 
Combretum and Terminalia; species of Lagun- 
cularia and Lumnitzera are mangrove trees; and 
Quisqualis species are creepers. The family is 
most closely related to those already described, 
but any close connections are not obvious. 

This account of Combretaceae does not in- 
clude Strephonema, which is a tropical, West 
African genus with three species. It was treated 
аз а separate family, Strephonemataceae, by 
Venkateswarlu and Prakasa Rao (1971) on the 
basis of morphological, embryological (Tobe & 
Raven, pers. comm.), and anatomical differences 
from the other Combretaceae, but it is better 
treated as a subfamily of Combretaceae. The 
Wood-anatomical differences include dimen- 
sions of vessels and fibers, the presence of fiber- 
tracheids, etc. (see also den Outer & Fundter, 

976, and van Vliet & Baas, 1984). The stomata 
are paracytic in Strephonema whereas they are 
зпотосунс or cyclocytic in other Combretaceae 
(Stace, pers, comm.), but its species have the 
‘ame type of characteristic (“combretaceous”) 
hairs as have other Combretaceae. The flowers 
are actinomorphic, 5-merous, bisexual, petalifer- 
005, and diplostemonous, and have a half-infe- 
пог Ovary (inferior in other Combretaceae). The 
ons grains lack pseudocolpi. The ovary is uni- 
Ocular and has two pendulous ovules as in other 
tod members. On the other hand, the mas- 
z ¢, hemispheric cotyledons in the seeds of Stre- 
WES TEMG pi ly with the folded, 
‘pirally twisted ones in other Combretaceae. 
i oe although fairly distinct, Strephonema is 
Onsidered a member of Combretaceae by 
ue taxonomists, e.g., by Exell (1930), Exell and 

lace (1966), and van Vliet (1979), who have a 
ciem, knowledge of the family. We agree with 
di authors that the genus should be placed in 
,' -Ombretaceae family as a separate subfam- 
ily, Strephonematoideae. 


DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 


667 


ALZATEACEAE S. GRAHAM (1983) 


Alzatea (Fig. 11) probably consists of two 
species. It was considered as lythraceous by 
Lourteig (1965), and was included in the widely 
circumscribed Crypteroniaceae by van Beuse- 
kom-Osinga and van Beusekom (1975). How- 
ever, A/zatea is unique in several features. Ac- 
cording to A. Graham and S. Graham, on whom 
we base part of this information, the species of 
Alzatea in Costa Rica “is almost epiphytic in 
habit, growing upwards via other trees in the 
cloud forests with only slender stem connections 
to the ground." It remains to be proven whether 
this is the case also with A. verticillata in South 
America. Baas (1979) and van Vliet and Baas 
(1975, 1984) in their anatomical evaluation found 
that A/zatea has different, trilacunar nodes, which 
they consider to be an ancestral rather than a 
derived feature (Baas, pers. comm.). In A/zatea, 
also, the arrangement of vascular tissue in petiole 
and midrib of leaves is different from that in 
Lythraceae, having a different ray type and pos- 
sessing branched foliar sclereids, which are un- 
known in Lythraceae. Like the Lythraceae, ru- 
dimentary stipules are present, however 
(Weberling, 1968). Pentamerous apetalous flow- 
ers in a branched panicle are rare in Lythraceae. 
Stamen, connective, and microsporangium fea- 
tures are also different from those in Lythraceae; 
whereas, the pollen grains (Muller, 1975) lack 
any ofthe specializations, e.g., pseudocolpi, found 


however. The placentation in A/zatea is parietal, 
thus differs from that in most Lythraceae. (Ат- 
mannia microcarpa DC., with parietal placen- 
tation, is aberrant within its genus and in Ly- 
thraceae; it exhibits reduced features, and does 
not approach Alzatea.) Al ding to Tobe 
and Raven (1984a) has a bisporic, A/lium-type, 
embryo sac; as in Rhynchocalyx (Rhynchocaly- 
caceae), but unlike all other Myrtales, the mi- 
cropyle of the ovules is formed by the inner in- 
tegument alone and the archesporium is 
multicellular. Also, according to S. Graham 
(1984; Tobe & Raven, 1984а), the seed shape 
and seed coat do not resemble those in Lythra- 


ceae. 
Thus, it would seem justified to place A/zatea 
in a separate family, Alzateaceae. The family is 
formally described by A. Graham and S. Graham 
(Graham, 1984). 


668 ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL. 71 


> јен fo. 


JURE 10. tap ones e from Tanzania; Кобен coll.—A. leafy branchlet. —B. flo one 
branchlet with male and fem n the same inflorescence.—C. inflorescence.—D. female flowers- 
same, longitudinal ата ‘tile x (ORE del B. Johnse ay 


1984) DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 669 


UN 
м 
* 


و 
?2 


= 


Priv ll. Alzatea verticillata Ruiz et Pav. (Alzateaceae), from Реги: A-H. Klug 3349, I-K. Woykowsksi 
96.—А. twig.—B. bud.— : of flower, interior.—E. interior of tepal.—F. disk.—G. stamen 
fruit.—J. transverse section of fruit.—K. seed. (From 


in : 
different Ме i transverse section of ovary. —1. 
5.) 


670 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


PENAEACEAE GUILLEMIN (1828) 


This is a fairly uniform family of ca. seven 
genera and 20 species restricted to the winter 
rainfall area of South Africa. The family consists 


small stipules dissected into rows of hair-like 
structures, which are usually glandular (but de- 
veloped as relatively long hairs in Stylapterus 
barbatus A. Juss., Dahlgren, 1967a). In this fea- 
ture the family agrees with certain Lythraceae. 
The inflorescences vary between branched pan- 
icles and racemes, or may consist of a solitary 
terminal flower (Sa/tera). The flowers are con- 


hypanthium is large 
and colored especially in Glischrocolla (Dahl- 
gren, 1967b), Endonema (Fig. 12; Dahlgren, 
1967c), and Saltera (Dahlgren, 1968), which are 
bird-pollinated. In Endonema, but not in the 
other genera, the stamens are inflexed in bud, in 
a way resembling that for Mouriri of Melasto- 
ee (Fig. = see also Мопеу, 1953). Тће 
у carnose, and 
the introrse microsporangia sometimes, as in 
Penaea and Stylapterus, are only about half its 
length. The pollen grains are generally squarish 
or rectangular, 3—6-colporate, and always pro- 
vided with pseudocolpi isomerous with the ap- 
ertures. The four carpels form a 4-locular pistil 
with a narrow filiform to fairly stout style pro- 
vided in Stylapterus and Penaea with four wings, 
in which case the stigmatic papillae are in com- 
missural position between the apical lobes of the 
stylar wings, an indisputably derived condition. 
Whereas, in Endonema each locule has two low- 
er pendulous and two upper ascending ovules, 
each locule in the other genera has only two as- 
cending ovules. The embryo sac formation is pe- 
culiar, conforming to the 4-sporic, 16-nucleate 
Penaea-type (Stephens, 1909). The fruit is cap- 
sular. 

Within Penaeaceae differentiation has taken 
place in two directions: (1) towards a large, rigid, 
and brightly colored hypanthium, in connection 
with ornithogamy, and (2) towards specializa- 


tions ofthe style, with four prominent wings, and 
commissural stigmas in flowers of mediocre size 
and with кет (- purplish) color. 

Penaeaceae show similarities to the Olini- 
aceae, к кос: Memecylaceae, Me- 
lastomataceae, and Lythraceae, most of which 
have perigynous flowers, minute stipular struc- 
tures in axillary rows, pollen grains with pseu- 
docolpi isomerous with the apertures, and prom- 
inently developed connectives. 

e ancestors of Penaeaceae could have had 
common origin with Rhynchocalycaceae, in 
which the petals are somewhat reduced, the sta- 
mens alternate with the calyx lobes and are lo- 
cated on the rim of a receptacle, the connectives 
are well developed, the pollen grains are hetero- 
colpate, the basic inflorescence type is panicu- 
late, d the geographic distribution is es. 
thoug 


in Sut Africa. There are avenue differences, 
however, e.g., the numerous ovules in the 2(-3)- 
mais pistil in Rhynchocalycaceae. 

Penaeaceae are distinct enough to warrant sep- 
arate familial status. 


4 
RHYNCHOCALYCACEAE JOHNSON & BRIGGS (198 ) 


This family consists of the genus Rhyncho- 
calyx Oliv., with the single species R. laws 
nioides Oliv., in the eastern parts of South Africa. 
Rhynchocalyx has previously been included in 
Lythraceae (Oliver, 1894; and several other e: 
thors) or Crypteroniaceae (van везени 
inga & уап Beusekom, 1 rd but is obviously 
out of place in both fat ilie n 

It is a tree (Strey & E 1968) Ms : 
cussate, opposite, entire leaves and fairly A: 
paniculate inflorescences (Fig. 13) with sm 
hexamerous flowers. These have an open hyper 


e 
and with a basifixed anther having а "e ati 
broadened connective (as in the fami! 


-het- 
tioned). The pollen grains are 3-colporate 


по РАВНА 


FiGure 12. 
Penaeaceae: A-J. Stokoe 
inflorescence (“flower”). 
baxial view.—I. pistil.—J. capsule.—K. seed. (Fr 


r 17.—A. bra 


Endonema Pr ge на fil.) Gilg, ап orthithogamous member of the ~ Afri 

214 пећ end with unifloral lateral infloresce 
ст е t lower, middle and upper pair in B. — F-H. 5 
om Dahlgren, 1967c.) 


can family 
re unifloral 
== lateral, and 


tamen; ie) 


G 


ف 


“= 


— 


671 


arivis 


ма 1 NASAL 


MYRTALES 


DAHLGREN & THORNE 


1984] 


VET een M 
Sener ORE 


672 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


du 
HANE 
HT е 
NA AMI | 
KE ANS ES 
25% LA SSA 
EH Vi 
AC A ee é ЈЕ | 
ОЧ о 


Wei 
SANE 


© = 
Rin On: ПЕРА 
АЗ AN ea 
A ESSE EI^ 
“es РА КУ РЕЗЕ VRA 


CS Ф 


is 
um 
ae 4 Гем 


8 YA E = 
"M. 2 

ONE 
РАХМ зу, 

DAES РАИ 
=з МОМ Ce у 

NA 
~“, S 


ے2 


а маама 


NK 
Ју 


LJ 
ж! 
iW 


4. 
FIGURE 13. Rhyn frica: A-H. Wood Ла | 
I-K. Strey 6539.—A ; i two petals and pr 
er n agp cnn rim.—F. petal, flattened out.—G. stamen. —H. ovary in longitudinal FACH from 
-—J. diagrammatic cross section of young frui і .—K. (MN 
Oliver, 1894; I-K from Strey & Leistner, 1968.) € IR Seine атны CLE 


| 


= 


1984] 


erocolpate, with three distinct pseudocolpi. The 
ovary 15 bi- (rarely tri-) carpellate and described 
by van Beusekom-Osinga and van Beusekom 
(1975) as unilocular, with two longitudinal pla- 
centae with numerous ovules, but it is partly 
bilocular. The style is simple and undivided. The 
fruit (Strey & Leistner, 1968) is a 2- (or 3-) locular 
capsule. It is cartilaginous, partly loculicidal, and 
contains 11—17 flat seeds per locule. 

Unlike the Penaeaceae, Rhynchocalyx has the 
Polygonum-type embryo sac formation; it is pe- 
culiar in having a micropyle formed by the inner 
integument alone instead of both integuments; 
the nucellus, as in Lythraceae, has a multicelled 
archesporium, but there are several differences 
between Rhynchocalyx and Lythraceae that ar- 
gue against a close relationship. (The embryo- 
logical information according to Tobe & Raven, 
1984b.) There are also emb yologi 
from Alzatea and Axinandra (Tobe & Raven, 
1983b, 1984b), which support treating Rhyn- 

e 


differences 


[Уйһгасеае. A link with Penaeaceae (see under 
is family) is likely, but embryology does not 


Support the inclusion of Rhynchocalyx in that 
family, 


CRYPTERONIACEAE A. DE CANDOLLE (1868) 


oua боса (Crypteronia, Fig. 14; Dac- 
of a and Axinandra with perhaps a total 
Dolls pecies; Shaw, 1973) are trees with op- 
ice T ci having a marked midrib and 
Which ar TOmous venation, the anastomoses of 
м" зый Close to the leaf margin. Small stipules 
bx Ma nt (note that such are seldom recorded 
pilis on] The inflorescences are 
olet ы: 9 poor racemules and the flowers small, 
eins: а 4—5-merous, and perigynous to 
Which ag and may lack or have small petals, 
Mid i. ess are connate apically (and 
mes u taneously as an umbrella). The sta- 

are alternisepalous and inserted on the 


DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 


673 


margin of the receptacle, inflexed in bud, and 
with a wide connective, which is conduplicate in 
Axinandra. The pollen grains are 2- or 3-col- 
porate, with apertures alternating with pseudo- 
colpi. The ovary is 2-6-locular and develops into 
a chartaceous or woody capsule. 

The embryology has been studied in Axinan- 
dra (Tobe & Raven, 1983b). It differs from all 
other Myrtales known in having an endothelium 
(i.e., integumentary tapetum). 

This family has recently been circumscribed 
and redefined by van Beusekom-Osinga and van 
Beusekom (1975), who, in addition to the three 
southeastern Asiatic genera, Crypteronia (Fig. 15), 
Dactylocladus, and Axinandra, which we here 
refer to the family, also included the Central and 
South American genus Alzatea and the South 
African genus RAynchocalyx, each with one 
species only. The two last-mentioned genera, ac- 
cording to these authors, make up Crypteroni- 
aceae subfam. Alzateoideae with paniculate in- 
florescences, superior bicarpellate ovaries, 

зс лул ес A chart + 


numerot p Iruits. 
However, they do not seem closely allied to the 
former genera, nor to each other, and are best 
treated as separate families, Alzateaceae and 
Rhynchocalycaceae. 

The Asiatic genera (van Beusekom-Osinga, 
1977) may form a monophyletic group, although 
even this is somewhat uncertain. Among them, 
Axinandra was considered by Meijer (1972) as 

Pe x. 4 ite & n 


particularly p 


Meijer to approach various other families, such 
as Lythraceae, Memecylaceae, and the tribe Ma- 
carisieae of Rhizophoraceae. 

Morley (1953) comments on the relationship 
between Axinandra and Dactylocladus (Crypte- 
roniaceae) and the genera of our Memecylaceae 
and Melastomataceae. He finds that the two gen- 
era differ from the Memecylaceae in lacking in- 
cluded phloem in the secondary xylem, in lacking 
terminal sclereids and anther glands, and in hav- 
ing anatropous rather than campylotropous 
ovules, antesepalous ovary locules, different flo- 


ral A fruit. Thus, these 
genera should not be included among the Me- 
mecylaceae, but would require a separate 
subfamily. We believe they can, provisionally, 


674 


kachand et al. 1554; D. Larsen 8695.—A. branch with spikes of male flo 


E 
с 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


3mm 


IGURE 14. Crypteronia paniculata Kurz. (Crypt i ) from coll 


of stem lists.—C. male flower.—D. female flower. (Orig., del. B. Johnsen.) 


wers. — B. branch tip showing 


Sang- 


PA iland: A-C. у 


а 


1984] 


be treated with Crypteronia in the family Cryp- 
teroniaceae. 


MEMECYLACEAE DE CANDOLLE (1828) 


Although there are still doubts about the dis- 
tinctness of this family, it is recognized here by 
one of us (Dahlgren) in accordance with the con- 
clusions by Johnson and Briggs (1984), the al- 
ternative being to treat it as a subfamily under 
Melastomataceae (Thorne). It consists of 6-8 
genera, the New World Моитт (Fig. 15) and 
Votomita, and the Old World Lijndenia (Bremer, 
1982), Memecylon, Spathandra, and Warne- 
ckea. The distinctness of Spathandra is still in 
dune, Pternandra is discussed below. 

ha 1 


Ix; 1 , не а 


Wy аге Mainly р B trees with 
opposite leaves having mostly pinnate venation 
with indistinct lateral and intramarginal veins. 
Stipules are probably generally absent; but Figure 
15B shows a species of Mouriri with a row of 
finger-like structures (dissected stipules), which 
agree with the stipules in various other families 
of Myrtales, e.g., Penaeaceae. 

Anatomically the family stands out as distinct 
(van Vliet, 1981: van Vliet et al., 1981; van Vliet 
& Baas, 1984) in having included phloem of the 
foraminate type (lacking in Melastomataceae), 
diffuse and mostly solitary vessels (frequently in 
multiples in Melastomataceae), the fibers have 
distinctly bordered pits (in Melastomataceae the 
a T$ are libriform). Fiber dimorphism occurs 

many Melastomataceae but not in Memecy- 
laceae, 

The indumentum is much less developed than 
E EO cen. The richness and variation 
ei Т SClereids (incl. terminal sclereids) is con- 

uous. Stomata have been found to be para- 
i (Memecylon) or occur in crypts (Mouriri). 


IN. tissues contain crystal druses (Baas, 


in 


E are generally small and less dif- 
йкы E in most members of Melasto- 
petils ub эщ stamens are twice as many as the 
bali ave a carnose, compact connective 
© он with a gland, and the anthers 
mee vem inally dehiscent. As in Melastoma- 
MENU OON and Penaeaceae, the 
Ovary is ab are consistently heterocolpate. The 
With eg erior and contains 1—5 locules, each 
largely co; 9 numerous ovules. The embryology 
except cor with that for Melastomataceae, 
becas К seeds are different. The fruit is 

large or (Pternandra) rather small 


DAHLGREN & THORNE—MYRTALES 


675 


KIF LION 


seeds, generally with extensive, folded cotyle- 
dons (Bremer, 1981). 

Morley (1953) defined this group by the pres- 
ence of included phloem in the dary xylem, 
pinnate leaf venation, occurrence of terminal 
sclereids on the vein endings in leaves and often 
in flowers, presence on the connectives of an el- 
liptic or circular depressed gland, antepetalous 
ovary locules (when locules are isomerous with 

e petals), campylotropous ovules, relatively 
few and large seeds, and characteristic floral vas- 
cularization, all characteristics which do not 
apply to Pternandra, however. Morley (1953) 
considered the closest relatives of Memecylaceae 
sensu stricto to be the tri ibessieae, in whic 
Pternandra (incl. Kibessia) has most of the me- 
mecylaceous features but leaf blades of the typ- 
ical parallel, melastomataceous type. Prernandra 
also lacks terminal sclereids, it lacks a gland on 
the connective, and has numerous anatropous 
ovules and small seeds, but yet is probably best 
placed in Memecylaceae. 


MELASTOMATACEAE A. L. DE JUSSIEU (1789) 


The Melastomataceae consist of perhaps 195 
genera and 3,500—4,000 species. These range from 
small, sometimes epiphytic herbs or shrublets to 
shrubs or, more rarely, lianas or trees. Nearly all 
have opposite leaves, which, characteristically, 
have 3-9(-19) main veins separate from the base 
of the blade. The leaves are entire in nearly all 
taxa, but have distinct, sometimes conspicuous 
teeth in Sonerila tenuifolia Bl., where the teeth 
seem to be an innovation and are different from 
those in Lythraceae and Onagraceae. Pellucid dots 
are generally absent, but occur in the genus Mi- 
crolicia, where their presence and nature de- 
serves attention. Stipules seem to be lacking. The 
nodes are unilacunar (van Vliet & Baas, 1984). 
Crystals occur as druses in all tribes except the 
Astronieae, where there are styloids instead; 
druses also occur in Memecylaceae and - 
teroniaceae where small styloids are also present 
(Baas, 1981). Interxylary (included) phloem ap- 
pears to be lacking; libriform fibers are charac- 
teristic, and the fibers are often septate, these 

liti p ting diff fi those in 
Memecylaceae (van Vliet & Baas, 1984). The 
stomata are generally anomocytic or polycytic 
(rarely diacytic, cyclocytic, or anisocytic), and 
the indumentum is extraordinarily differentiat- 
ed, the trichomes being generally large, multi- 


676 


ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL. 71 


B./Thsen. Фа 


buds | 


ch 20223.-* 
ranch, —B. bases of leaves showing axillary ‘Stipules as well as stem lists ending in ' p am 
petal.—F.5 


FIGURE 15. Mouriri chamissoniana Cogn., a Brazilian member of жешс. Hatschba 
uricles 


—D. flower in full т йе E etal.— 
note the difference in filament length within a flower. (Orig., del. B. Johnsen. 


1984] 


cellular, and scale-like. The flowers vary in size 
from small and nearly actinomorphic to large, 
conspicuous, and distinctly zygomorphic, and are 
generally wholly or partly epigynous, the ovary 
generally densely beset with complex hairs. The 
petals, as in much of the order, are commonly 
pink to crimson or violet. 

Stamens are in one or two whorls (diplo-, hap- 
lo-, and obhaplostemonous), with their filaments 
inflexed in bud and their connectives generally 
well developed, often prolonged or provided with 
appendages. The anthers are often poricidal but 
frequently open with longitudinal slits. The pol- 
len grains as far as known (Patel et al., 1984; 
Carlo Hansen, pers. comm.) are consistently het- 
торор, being supplied with pseudocolpi or 
with int 1 d i i with the 


usually three apertures. 

The gynoecium is generally 3—5-carpellate, and 
the ovary 3-5-locular, only rarely unilocular 
where the partitions are dissolved, with axile or 


Specializations, The fruit is baccate or capsular 

th seeds smaller than in most genera of Me- 
тесујасеае. Its embryo also has smaller and less 
folded cotyledons, which may be equal or un- 
equal (cf. Trapaceae). The seed coat lacks fibers 
in the exotegmen. 

With this circumscription Melastomataceae 
becomes a rather homogeneous family. The ge- 
nus Pternandra of Memecylaceae at least phe- 
netically shows some features of Melastomata- 
les. some of these may be plesiomorphies (lack 
d eee gland, lack of terminal sclereids, 
ion enda, others convergences (leaf vena- 
te t may be regarded as intermediate, which 
ni argument for including Memecylaceae as a 

amily in Melastomataceae, as preferred by 
one of us (Thorne) 


PSILOXYLACEAE CROIZAT (1961) 


У 15 closely allied to Myrtaceae and, 
Pto da road family concept, may well be in- 
me кы that family (Schmid, 1980). It is mono- 
Ma» onsisting of the genus Psiloxylon with the 
Maii · mauritianum (Hook. f.) Baill. on the 
жы Islands. The genus is a small tree with 
abro alternate (disjunct-opposite), stipulate, 
Магу us, and gland-dotted leaves and small, ax- 
и panicles. Divided myrtalean stipules are 

nt at least in young plants (Johnson & Briggs, 


DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 


677 


pers. comm.). The flowers are unisexual, 5(—6)- 
merous, and perigynous, with a nectariferous 
floral tube, free sepals and petals, and diploste- 
monous androecium. In the female and male 
flowers the stamen-like staminodia and a pistil- 
like pistillode, respectively, are present. The 
stamens are erect in bud, a rare feature in Myrta- 
ceae, but the pollen grai pi ly sim 
ilar to those in Myrtaceae. The tri- (bi-, quadri-) 
carpellate pistil is clearly superior and often has 
a (very) short stipe; it has an ext 1 
and the (2—)3(—4) stigma-lobes are flat and ге- 
flexed. In these characteristics Psiloxylon differs 
from nearly all Myrtaceae. The ovary is trilocular 
and has axillary placentas, each with numerous 
anatropous ovules. The fruit is a berry. (Infor- 
mation mainly from Schmid, 1980.) 

In anatomical respects (van Vliet & Baas, 1984), 
Psiloxylon shows a distinctive combination of 
features and has, for example, chambered, crys- 
talliferous fibers, lacking in the Myrtaceae. Psi- 
loxylon also has a cancellate testa, which is very 
rare in Myrtaceae. 

In the light of a number of distinctive features 
it seems justifiable to treat Psiloxylon as a dis- 
tinct family rather than as a member of Myrta- 
ceae as treated by Schmid (1980). The presence 
e 


1 d TRE, | 
УЗОР эу 


of Psiloxylaceae from the same ancestors as Муг- 
taceae and Heteropyxidaceae. With a broader 
i t the tl famili ld be treated 


Г. 
азыт 


1 

ily concept the 
as one (as preferred by Thorne). 
HETEROPY XIDACEAE ENGLER & GILG (1919) 


It is with doubt that this family is acknowl- 
edged here, by one of us (Dahlgren), in accor- 
dance with Johnson and Briggs (1984), the al- 
ternative being to include it in Myrtaceae either 
as a subfamily (as preferred by Thorne) or with- 
out discrimination at all (Schmid, 1980). 

The single genus Heteropyxis, with three species 
in southeastern Africa, consists of shrubs or small 
trees with disjunct-opposite (“alternate”), entire 
leaves with minute stipules. The leaves, as in 
Myrtaceae and Psiloxylaceae, are gland-dotted. 
The anatomy seems to agree with that in Myr- 
taceae, although the cork is not stratified, as is 
us the case in Myrtaceae; vasicentric tra- 
cheids are lacking (usually present in Myrtaceae) 
and axial parenchyma is lacking (rare in Myr- 


678 


tales) (data from Schmid, 1980). In some of these 
features Heteropyxidaceae agree with Psiloxy- 
he inflorescence is a small panicle of 


ous or pentamerous flowers. Sepals and petals 
are imbricate and free, and the androecium, usu- 
ally of (5-)8 stamens, are obdiplostemonous ог 
rarely obhaplostemonous. The stamens are erect 
in bud, the anthers longitudinally dehiscent, and 


Ка nila { 1 
the и iang ular 


similar to those in Myrtaceae, lacking pseudo- 
colpi. The pistil is generally bicarpellate, with 
sunken style, much longer than in Psiloxylaceae, 
and with capitate stigma. The fruit is a dry loc- 
ulicidal capsule with persistent style. The em- 
bryological information available is in accor- 
dance with the Myrtaceae. 

Similarities between Heteropyxidaceae and 
Psiloxylaceae are the spiral phyllotaxy, the sta- 
mens that are erect in bud stage, and the reduced 
carpel number. Both are primitive in having pe- 
rigynous flowers. On the other hand, Hetero- 
pyxidaceae differ from Psiloxylaceae as well as 
Myrtaceae in a number of respects (see Johnson 
& Briggs, 1984). 


MYRTACEAE A. L. DE JUSSIEU (1789) 


This is a large family of ca. 145 genera and 
more than 3,650 species (Schmid, 1980) with 
wide, chiefly tropical-subtropical distribution and 
a center in Australia, but also with many taxa in 
South America. As this family will be dealt with 
in more detail by other participants of this sym- 
posium, only a few remarks will be made here. 
Myrtaceae have generally been divided into two 
subfamilies, Myrtoideae and Leptospermoideae. 
Schmid (1980) reviewed the subfamilial history 
of the family and recognized two additional 

subfamilies: Chamaelaucioideae (formerly a tribe 
in Leptospermoideae) and Psiloxyloideae. For 
various reasons and in line with Johnson and 
Briggs’ treatment of Myrtaceae (1984), we have 
excluded Psiloxylon and Heteropyxis as separate 
families (or subfamilies, Thorne), and aban- 
doned the traditional division of Myrtaceae into 
(other) subfamilies. 

The family is a fairly distinct one, character- 
ized in particular by having gland-dotted leaves, 
stems, and floral parts (as do Psiloxylaceae and 
Heteropyxidaceae). In the presence of schizoly- 
signeous а с cavities в filled with casential 


iil 


derivatives of baeckerol, eugenin, and шато 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


types, etc.) Myrtaceae, Heteropyxidaceae, and 
Psiloxylaceae are distinctive in the order. The _ 
calyx and corolla are imbricate and the stamens _ 
are usually numerous, although very occasion- 

ally few. The inflorescences are basically panic- | 
ulate. The evolutionary trends within Myrtaceae | 
are presented in detail by Briggs and Johnson | 
(1979). The flowers are nearly always epigynous | 
and bisexual, nearly always actinomorphic, 4- or 
5-merous (other merous conditions are not rare), 
with a floral tube of variable length often pro- 
longed above the ovary, on the margin of which 
the sepals, petals, and normally numerous sta- 
mens are all inserted. The sepals or petals or both 
are occasionally fused, either into a cap (or oper- 
culu um) that is shed at anthesis, or else the fused 


cistaminal and then 
stemonous, obhaplostemonous, or haplostemo- 
nous. When the stamens are numerous they may | 


always opposite the petals. The developmental | 
succession of = polystemonous androecium is, | 

owever, centripetal. The connectives are only | 
rarely чыш although they usually pH 
or more apical secretory cavities (glands). | 
anthers dehisce by slits or (for example in certain 
cium-group) by pores. The pollen 
erally triangular, often colnet и 
pseudocolpi. Staminodia are rarely ргезе 
is great variation in number of loculi care | 
the pistil, which range from one to 16 per Hon" | 
three, four, five, and especially two being p | 
dominant (Schmid, 1980, tables з, 4). Тере | 


is usually numerous, occasionally 
ly one. One feature of note is that th мрак 
ел described as lacking a parietal рж calli 

(1966), however, suspects that the рапе | 
cut off so early that it has escaped een + | 


t in Pst 
visions in the nucellar epidermis (ехсер 
diu 


а ber 
The fruit i is, fleshy or. dry, respectively 
Or capst 


very осалдау. а ем great уай 
hiscent, nutlike structure, and there - th fruit and | 
ation in the shape of the embryo. Both 


1984] 


embryo are useful in the division of the family. 
Each fruit usually contains one to few, though 
very occasionally many, fertile seeds. The en- 
dosperm is initially nuclear and is usually lost at 
seed maturity, occasionally a scant amount of 
endosperm being present. The embryo some- 
times contains copious amounts of starch. 

Except for Psiloxylaceae and Heteropyxida- 
ceae, which Schmid (1980) included in Myrta- 
ceae, the family shows no obvious connections 
with the other families of the order. Punica, in 
its polymerous androecium, lack of pseudocolpi, 
etc., is reminiscent of Myrtaceae (convergence), 
but the relationship is probably not close. A phy- 
logenetic link with Lecythidaceae has been pro- 
posed but is not supported by detailed exami- 
nation. 


INTERRELATIONSHIPS OF FAMILIES AND 
EVOLUTION WITHIN MYRTALES 


To approach the interrelations between fam- 
ilies in Myrtales it mapa be ANY to deduce 
а probab 


tors. This can best be v le comparing the 
character states of the myrtalean families inter 
* and by examining those of probably related 
poss Rosales being chosen as the outgroup. 
bably woody 
,the mar- 
gins of which possibly had lateral teeth with a 
hollow, crater-like apex. Stipules were presum- 
ably present but minute, entire, and situated lat- 
erally. The stem had evolved bicollateral vas- 
сшаг strands and the vessel elements had 
alternate, vesti with entire 
Perforation or scalariform perforation with few 
bars. Furthe ermore, the ground tissue of the wood 
oceans of fiber-tracheids, the wood paren- 
ut Was paratracheal and apotracheally dif- 
se, sag the rays were heterogenous (van Vliet 
ө 1984). Crystals most likely occurred in 
" Axial pone and in the ray cells. The 


к 
Plants w ‚н i 


> арго bly tic, and no com- 
i Mithomes were developed. The flowers, 
ao paniculate inflorescences, were 
e E ic, perigynous, and diplostemo- 
-or 4-merous, and petaliferous. The pistil 

pie oe with axile placentation, a sim- 
itis yle, and a lobate or branched stigma. The 
к €ns did not have a particularly swollen or 
ini. ша differentiated connective. The anthers 
dular ongitudinally, the tapetum was glan- 
‚апа the pollen grains were binucleate at 


DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 


679 


anthesis and most likely 3-colporate, lacking 
pseudocolpi; viscin threads were lacking. The 
ovules were anatropous, bitegmic, and crassi- 
nucellate with a parietal cell cut off from the 
archesporial cell in the nucellus. The embryo sac 


protein and fat. The fruit was presumably cap- 
sular. In the seed coat, the exotegmen was prob- 
ably not fibrous, and the mesotestal layer prob- 
ably did not contain sclerotic cells. 

The immediately ancestral forms were tannin 
plants with a flavonoid spectrum based on fla- 
vonols of the commoner types. Ellagic acid and 
ellagi-tannins were synthesized. Triterpenes like- 
wise were presumably present, whereas triter- 
pene saponins may or may not have occurred. 

None of the extant families exhibits this com- 
bination of attributes, though the family ap- 
proaching most closely the ancestral form of 
Myrtales would have been fairly similar to cer- 
tain extant Lythraceae. In this family the leaves 
may have teeth of the kind mentioned above, 
although they are “cryptic,” and the leaf margin 
can be ciliate. Pellucid dots with essential oils 
are lacking. The flowers are also generally peri- 
gynous and generally petaliferous, diplostemo- 
nous, and perfect; the pistil is basically eusyn- 
carpous; and the embryology agrees closely with 
the general, unspecialized pattern in the order, 
with, for example, the Po/ygonum-type embryo 
sac formation. 

However, in Lythraceae, the wood does not 
have fiber-tracheids but libriform fibers, which 
are generally septate. The stipules quite often are 

and dissected, forming one or two 
groups of hair-like structures located in the leaf 
axils (Fig. 8c). The stamens are generally free 
this, 
generally at or near its base. This apa is 
dubiously primitive in the order, and m 
derived from the general condition анаи the 
stamens, like the petals, are inserted on the rim 
of the hypanthial tube. Furthermore, the pollen 
grains in at least nine of the 25 genera are het- 
erocolpate, the heterocolpate condition being 
probably ancestral in the family but derived 
within the order. Finally, the seed coat with its 
fibrous exotegmen represents a specialized type. 

Therefore, the Lythraceae should be excluded 
from consideration as wholly unspecialized. 
However, their position in the order is central, 


> 


680 


and they show close relationship with several of 
the families, including Penaeaceae, Rhynchoca- 
lycaceae, and Onagraceae. 

A number of the supposedly primitive states 


in Lythraceae, in Psiloxylaceae, Heteropyxida- 
ceae, Myrtaceae, and Strephonematoideae, al- 
though each of the taxa is specialized in various 


by Psiloxylon, which has retained the presum- 


ably р 
ers with a wholly superior ovary but has libri- 
form and septate fibers, which are presumably 
derived. Most Myrtaceae have numerous sta- 
mens and a more or less inferior ovary, but their 
wood is generally characterized by having fiber- 
tracheids. 

We have refrained from giving a cladistic pre- 
sentation of the probable evolution in Myrtales, 
as this is done elsewhere in this volume, by John- 
son and Briggs (1984), on the basis of the same 
data. However, we find it appropriate to discuss 
the probable or at least possible evolutionary 
courses that might have taken place in the order, 
as Our opinions may deviate in certain major as 
well as minor features from those of other au- 
thors. 

An evolutionary line that probably diverged 
very early from the myrtalean ancestors is rep- 
resented by Psiloxylaceae, Heteropyxidaceae, and 
Myrtaceae. These share some conspicuous fea- 
tures, such as the characteristic shape and ap- 
erture conditions (syncolpate) of the pollen grains 
(Schmid, 1980; Patel et al., 1984) and the pres- 
ence of schizolysigenous cavities with essential 
oils visible as pellucid dots on the green parts. 
The first representative of this evolutionary line 
doubtless had diplostemonous flowers with su- 
perior ovary such as in present day Psiloxylaceae, 
but the latter are specialized in having, for ex- 
ample, unisexual flowers with an extremely short 
style and reflexed, flat and carnose stigma lobes. 
The great concordance in pollen morphology 
among Psiloxylaceae, Heteropyxidaceae, and 
many Myrtaceae indicates that this rather pe- 
culiar type evolved very early from proto-myr- 
taceous ancestors and later in many Myrtaceae 
gave rise to superficially simpler kinds. The fact 
that this kind of pollen is known already in the 
Cretaceous (ca. 72 million years ago), before any 
other certain Myrtales, also indicates that this 
group of families was differentiated from the 
myrtalean ancestors very early 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


Also Onagraceae seem to deviate rather 
strongly from other Myrtales, and probably 
evolved as a lateral evolutionary line at an early 
stage. The evidence is somewhat contradictory 
in this respect. The family is an unusually distinct 
one in having the combination of epigynous 
flowers, pollen with viscin threads, Oenothera- 
type embryo sac formation, and tissues with 
calcium oxalate raphides. The latter three char- 
acteristics are absent from nearly all other Myr- 
tales, and it is likely that all these character states 
are derived ones. 

Thus, it is unlikely that other families, such as 
the Trapaceae, could have evolved from the ona- 
graceous evolutionary line after these attributes 
had been acquired. In pollen-grain shape and 
pollen-wall structure Onagraceae show some 
general similarity to Myrtaceae, Heteropyxida- 
ceae, and Psiloxylaceae (Nowicke, pers. comm.). 
But more conspicuous are a number of charac- 
teristics shared by Onagraceae and Lythraceae: 
wood with libriform and septate fibers; leaves 
with lateral teeth that have the same hollow and 
crater-like apex (*Fuchsioid" subtype, Hickey, 
pers. comm.), petals with similar, pinnate ve- 
nation (Chrtek, 1969); and seed coat with fibrous 
exotegmen (Corner, 1976). With the probable 
exception of the leaf teeth, these attributes seem 
to represent derived states, and should be so con- 
sidered. Convergent evolution of some of the 
derived states is not unlikely; though more likely 
is the alternative that Onagraceae diverged e 
proto-lythraceous ancestors after the wood 27 
seed-coat structures had already evolved. 

probable appearance of epigyny in tW ii 
dependent lines of evolution in the опаргасео : 
ancestors has been proposed by Eyde (1981) : 
the basis of the position of the пестапез on M 
posite sides of the ovary/hypanthium di 
In this feature the genus Ludwigia diflers 
all other Onagraceae. 


о in- 


rm 
The remaining families of the Myrtales form | 


a somewhat coherent group, most families being 
characterized by so-called **heterocolpa 
len grains, in which pseudocolpi are presen 
tween the true apertures. This eme 
tremely rare in angiosperms outside the M 

and it would be highly unlikely that 
evolved independently in several ph 
within the order. Accordingly, we P 
the genetic constitution for pseudoc 
expressed or not) evolved once in th 
ancestors of these families, but that 1t 
“become lost,” i.e., the attribute has 


e com 


is eX 


resume | 
olpi (whether 
mon 


te” por , 
t be- 


расодосо | 
yletic pe | 


| 


1984] 


to expression, in some lines. Thus, for example, 
in Lythraceae pseudocolpi occur in some but not 
in all genera (see above and in Patel et al., 1984); 
in some genera they are indistinct or inconsis- 
tently present. In Lythraceae at least Lythrum 
has pseudocolpi of the same number as the true 
apertures whereas in most lyth g with 
pseudocolpi these are twice as many as the ap- 
ertures, 

Pseudocolpi are absent (or very indistinct) in 
the pollen grains of Alzateaceae and Lythraceae 
subfam. Punicoideae, Sonneratioideae, and 
Duabangoideae, in Combretaceae subfam. 
Strephonematoideae, and in Trapaceae, where the 
intercolpate dey i dubiously correspond to 
pseudocolpi. The first five taxa, which are all few 
in species, show strong affinity, as expressed by 
similarities in various respects, to families or 
subfamilies where the pollen grains possess pseu- 
docolpi, and thus it is likely that their common 


great phylogenetic significance, and he suggested 
that this could serve as the basis for distinguish- 
ing а number of families from Myrtales sensu 
stricto as the order Lythrales. Although it is now 
obvious that this division would be unnatural, 
the fibrous exotegmen cannot be entirely ignored 
at the suprafamilial level. 


i Provided with lateral teeth which deviate from 
ове of other Myrtales in having a unique dou- 
s tay (Hickey, 1981). The tetramerous, hap- 
fruit iu flowers are nearly perigynous; the 
aterics; TY, indehiscent, and provided with char- 
"istic horns: the endosperm formation is ar- 


DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 


681 


rested in the initial stage (as in orchids); one of 
the cotyledons is reduced; and the embryo is filled 
with starch. In these features 7rapa has diverged 
strongly from other Myrtales and from any plau- 
sible ancestral type. The pollen morphology of 
Trapaceae may indicate affinity with the hetero- 
colpate condition if the intercolpate areas be- 
tween the meridional crests are homologous to 
intercolpate depressions and, hence, to pseudo- 
colpi, but this is far from settled. (Intercolpate 
depressions substitute for pseudocolpi, for ex- 
ample, in various Melastomataceae.) 

There is some variation within Lythraceae in 
the possession of sclereids. Thus, these are pres- 
ent in subfam. Sonneratioideae and Duabangoi- 
deae, whereas only few Lythroideae have un- 
branched sclereids restricted to the leaf petioles. 

fi bfamilies also deviate fi nearl 


all Lythroideae in having the stamens inserted 
on the rim of the hypanthial tube. Both these 


anthium. The flowers are 


. In the 
flowers of subfam. Sonneratioideae, Duabangoi- 
deae, and Punicoideae, the stamens are numer- 
ous. 
The different sequence of initiation of the an- 
droecium (centripetal in subfam 
deae and Duabangoideae 
u i tain genera of 
subfam. Lythroideae) suggests that the multi- 
staminate condition has evolved along several 
different lines in Lythraceae. Similarly, the hap- 
lo- and obhaplostemonous condition has cer- 
tainly evolved along several separate lines in the 
mily. 

Within subfam. Lythroideae the polymerous, 
large-flowered genera, such as Lafoénsia and 
Lagerstroemia have numerous stamens (in the 
former only diplostemony, however) and unspe- 
cialized pollen grains, lacking pseudocolpi. In 
these features they are generally considered to be 
primitive, a view that we wish to challenge. More 
likely, an increase in floral size has involved in- 
crease in number of sepals, petals, and carpels 
and especially has favored an increase in stamen 
number. Lack of pseudocolpi is found in about 
half of the lythraceous genera studied, and does 


682 


not seem to characterize natural groups of genera 
in subfam. Lythroideae (Graham & Graham, 
pers. comm.). The reasons for considering ab- 
sence of pseudocolpi as derived in the family are 
mentioned elsewhere in this article. In contrast 
to all other myrtalean families the pseudocolpi, 
when present, tend to be double the aperture 
number, a condition which should be considered 
another derived character state. 

How the first differentiation proceeded in the 
common ancestors of Lythraceae is perhaps im- 
possible to deduce. As the insertion of stamens 
on the hypanthial rim is the normal state outside 
Lythraceae (some Combretaceae excepted), we 
presume that this was the ancestral state, and 
that their insertion inside the hypanthium is an 
apomorphy that arose in the ancestor of subfam. 
Lythroideae and, perhaps, Punicoideae. Puni- 

id hould have diffe iated early from the 
latter line with its epigyny, increase in stamen 
number, indehiscence of fruit, acquisition of sar- 
cotesta, etc. Alternatively, epigyny could have 


etc. suggest that Duabanga and Sonneratia dif- 
ferentiated early from each other, Sonneratia 
having possibly arisen at a later stage from the 
common lythraceous line. 

A fibrous exotegmen is also found in the seeds 
of Combretaceae and, although not known in 
Strephonema, it is likely that it is the case in this 
genus, too. A considerable number of features 
are common to the subfamilies Combretoideae 
and Strephonematoideae, among them the com- 
bretaceous hair type (Stace, 196 5), the racemose 
inflorescence type, obdiplostemony, at least some 
degree of epigyny (only partial in Strephone- 
matoideae), and the unilocular ovary. Strepho- 
nema differs from other Combretaceae in the 
only hemi-epigynous flowers, in stomatal type 
and in several wood-anatomical features (van 
Vliet & Baas, 1984), which may justify separa- 
tion at family level (see Venkateswarlu & Prakasa 
Rao, 1971), but as they are so obviously related, 
subfamily rank may be sufficient 


pate pollen grains, have seeds without a fibrous 
exotegmen but often with sclerotic cells in the 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


mesotestal layer. Although Oliniaceae are un- 
known in the latter respect, they probably belong 


іп this group as is indicated by the number of _ 


features shared with Penaeaceae and Rhyncho- 


caceae, Penaeaceae, and Alzateaceae. Alzatea- 
ceae (Alzatea) probably belong to this group, 
although their pollen grains lack pseudocolpi. In 

th £ ilies the І havea fixed, opposite 
phyllotaxy, and the stamens are inserted on the 
hypanthial rim, both features of which may, 
however, be ancestral (plesiomorphies). The con- 
nective is also frequently enlarged in these fam- 
ilies. 

The two unigeneric families Alzateaceae and 
Rhynchocalycaceae share a number of wood-an- 
atomical characters (van Vliet & Baas, 1984), 
which makes it likely that they are closely allied, 
and in which they differ from especially Penae- 
aceae, which they otherwise resemble in floral 
characters. It is extraordinarily difficult to reveal 
whether wood-anatomical features have evolved 
by convergence here. Fiber-tracheids, which are 
considered primitive, are found in Penaeaceae, 

emecylaceae, and Crypteroniaceae, whereas li- 
briform and septate fibers have arisen in Melas- 
tomataceae and, probably independently, in Oli- 
niaceae, Rhynchocalycaceae, and Аре 
the last three families perhaps being rat 
allied. 

Whereas Memecylaceae have fiber-tracheids 
and solitary vessels, they are derived in having 
included phloem and also epigynous flowers, and. 
as a rule, large seeds with curved embryos. The 
Crypteroniaceae, here restricted to the - 
Asiatic genera Crypteronia, Dactylocladus, ы 
Axinandra, are a variable group which also ки 
retained primitive wood features but adop d 
diverse specializations in the flowers of each ge 
nus. Whether all three genera have an inte" 


her close 


mentary tapetum, as in Axinandra (Tobe & je 
ven, 1983b), is uncertain. Parallel — : 


Melastomatoideae which are specialize 
the wood with libriform and septate fibers s. 
aggregated vessels, in their more developed 
dumentum, and in their leaf venation. NU 
It is conspicuous that the mentam del 
families sl very few synapomorpht : 
may not be so series interrelated as has 8€? 
erally been presumed. : ws 
Penaeaceae, which have also retained à er 
tive wood anatomy, approaches the eee 4 
families, but are also closely connected "E а 
niaceae, Rhynchocalycaceae, and Alzatea 


1984] 


various floral characters, e.g., in the obhaplo- 
stemonous condition. The bisporic A//ium-type 
embryo sac in Alzateaceae (Alzatea) (Tobe & 
Raven, 1984a) may or may not be seen as a step 
in the direction toward the tetrasporic Penaea- 
type of Penaeaceae; at least the deviation from 
the Polygonum-type may have a common ge- 
netic basis. Both families have apetalous, peri- 
gynous flowers with prominent connectives. Al- 
zateaceae are, however, very isolated by having 
trilacunar nodes and a different arrangement of 
vascular tissue in petiole and midrib of leaves 
(van Vliet & Baas, 1984), pollen grains lacking 
pseudocolpi (Muller, 1975), which we consider 
à derived state in this case, and a bicarpellate 
unilocular ovary with parietal placentation. In 
all this it appears as a distinct and isolated taxon, 
and the close connection with Rhynchocalyx in- 
dicated by the bicarpellary ovary and other de- 
lails that caused the treatment of these genera in 
4 subfamily of Crypteroniaceae, earlier, may 
largely be due to convergence. 

Penaeaceae, Rhynchocalycaceae, and Olini- 
| ith African distribution, may be closely 
interrelated, the last two more advanced in wood 
anatomy. Penaeaceae and Rhynchocalycaceae in 
Particular resemble each other in the basically 

obhap- 


lostemonous flowers, the conspicuous connec- 

lives of the anthers, the heterocolpate pollen 

grains, and the basic chromosome number (Х = 

10), but the differences in wood anatomy, carpel 

= seed number, etc., still indicate some dis- 
ce. 


Oliniaceae and Penaeaceae each have a num- 
ber of characteristic features (autapomorphies) 
but the two have rather few of their own syn- 
apomorphies. 
age onider it very difficult to speculate about 

errelationships and evolutionary se- 
Quences for th ma 


| 
К 
5 
З 


2 ary courses in this part may 
Tongly change their evolutionary model. 


FAMILIES ALLEDGEDLY RELATED TO OR IN 
VARIOUS RESPECTS CONSPICUOUSLY 
SIMILAR TO MYRTALES 
oon families have traditionally been linked 
Ceae yrtales, viz., Haloragaceae, Rhizophora- 
' Lecythidaceae, Thymelaeaceae, and, less 


DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 


683 


often, Elaeagnaceae. In addition to these, there 
are a few families which have a combination of 
attributes similar enough to those of myrtalean 
families that they also deserve mention here. 
These include Elatinaceae, Coridaceae, and 
Chrysobalanaceae. 


THY MELAEACEAE 


Thymelaeaceae, with perhaps 500 species in 
50 genera (Shaw, 1973; Cronquist, 1981), are 
sometimes included in Myrtales (and are still so 
placed by Cronquist, 1968, 1981, 1984), and the 
family indeed possesses a number of myrtalean 
attributes. Some of these are evaluated here. 

The family consists mainly of shrubs (rarely 
trees, lianas, or herbs). Most, but not all genera 
(not the Gonystyloideae), agree with the myr- 
talean Ё iesin р ing intraxylary 
interxylary) phloem, vestured pits, and presence 
of elongate crystals in the wood (van Vliet & 
Baas, 1984). The phloem is permeated by a net- 
work of tough fibers. The leaves are alternate, 
opposite, or verticillate, entire, and have muci- 
laginous epidermal cells. They lack stipules, rep- 
resenting a difference from most Myrtales. The 
flowers are frequently 4-merous and perigynous 


:1 Kd f 
AOI Witwil 


ocated on a more or less well- 
developed, frequently cylindrical or campanu- 
late and brightly colored hypanthium. The petals 
are generally lacking or are small or reduced to 
entire or 2-cleft scales (cf. Oliniaceae). The pollen 
grains are pantoporate and crotonoid, reticulate 
or rarely with no sculptural pattern and whol- 
ly unlike those in the myrtalean families, without 
connection with wind pollination, and are dis- 
persed in the trinucleate stage, which is rarely 
the case in Myrtales. The pistil consists of two 
or rarely up to 12 carpels and may have as many 
locules, but it is generally unilocular, with a sin- 
gle, often excentric style (considered pseudo- 
monomerous), a condition not met with in Myr- 
tales, where the most nearly similar condition is 
that found in Combretaceae. Thymelaeaceae, like 
a few Combretaceae, also have an obturator de- 
scending from the base of the stylar canal to the 
ovules, and, as in the latter family, the ovules 
are pendulous. The embryological features differ 
to a considerable degree from the basic pattern 
in Myrtales (Tobe & Raven, 1983a). The fruit in 
Thymelaeaceae is generally indehiscent, rarely a 
loculicidal capsule. As in Myrtales, the seed gen- 
erally possesses little endosperm; its embryo is 
rich in fatty oils and, as in some Myrtales (e.g., 


684 


in Melastomataceae), has expanded, flat cotyle- 
dons. 

Whereas some of these attributes might indi- 
cate a position in Myrta 


this. Among the chemical features of Thymelae- 
aceae that may be mentioned are a lack of tan- 
nins, lack of ellagic acid, a different flavonoid 
spectrum (cyanidin, pelargonidin, delphinidin, 
methylated anthocyanidins, and myricetin all 
lacking), and presence of coumarins like daphnin 
and daphnetin. The lack of bicollateral vascular 
strands in the relatively primitive Gonystyloi- 
deae indicates that the thymelaeaceous ancestors 
did not have internal phloem. A number of tax- 
onomists believe that Thymelaeaceae approach 


Thymelaeaceae is totally distinct from that of 
any Myrtales and similar to that of most Eu- 
phorbiaceae. There is also similarity between 
Thymelaeaceae and Euphorbiaceae in seed wall 
structure (Corner, 1976), in which Thymelae- 
aceae differ from the myrtalean families. Both 
authors consider that Thymelaeaceae should be 
placed near Euphorbiaceae, and that these two 
families are related to Malvales. 

It seems important, in this context, to recon- 
sider the homogeneity of Thymelaeaceae. Some 
evidence suggests that the Gonystyloideae are 
out of place in this family, and may, moreover, 
not even be closely allied to it. If this is supported 
by further evidence, then some of the arguments, 


et 
chemical, embryological, pollen-morphological, 
and other evidence still argues strongly against 
placement of Thymelaeaceae in this order. On 
the basis of pollen, Gonystyloideae do resemble 
other Thymelaeaceae closely in their unique ex- 
ine, and the family is probably natural (Nowicke, 
pers. comm.). 


HALORAGACEAE 
This family has often been placed in Myrtales 


by virtue of its often Opposite leaves with minute 
supules, its 4-merous, basically diplostemonous 


Many vegetative features are in accordance 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


with those in Myrtales; however, internal phloem 
and vestured pitting are absent. According to 
Hickey and Wolfe (1975), who assigned Halo- 
ragaceae to Hippuridales, the leaf teeth are ofthe 
Rosoid type (similar teeth occur in some Ona- 
graceae and Lythraceae; Hickey, 1981). Stipules 
(see above) are present and of a vestigial kind, 
as in Myrtales. Inflorescence characteristics pro- 
vide little assistance in assigning Haloragaceae 


to any major complex. The floral anatomy of | 


Haloragaceae (Orchard, 1975) shows similarity 
to that in Cornales and Araliales rather than t0 
that in myrtalean families. Pollen morphology 
shows features connected with wind pollination, 
and comparisons with other groups (Orchard, 
1975) give no clear indications of phylogenetic 
affinity. The pollen grains are shed in the tricel- 
lular stage as in Araliales, but unlike Myrtales. 
The gynoecium lacks a single style, and the sty- 
lodial parts are either very short, or there are 
separate stylodial branches, as in Araliales. The 
fact that the anther wall formation in certain taxa 
of Haloragaceae is ofthe monocotyledonous type 
may not be very informative because the dicot- 
yledonous type also occurs in the family. More 
interesting, perhaps, is the fact that the endo- 
sperm formation in Haloragis and some species 


of Myriophyllum is of the possibly more e 
ra 


Polygonum-type, excluding any orig! 
within Onagraceae, and the embryogeny 15 of the 
Myriophyllum variant of the Caryophyllad (© 
in which the family differs from all Myrtales (К2- 
pil, 1962; Kapil & Ваја-Вама, 1968). The ж 
are often fairly rich in endosperm, which 15 nO 
so in Myrtales; but in Araliales the endosperm 
is even more copious and the embryo propor 
tionally smaller than in Haloragaceae. F 

ur conclusion is that Haloragaceae pe 
comprise a fairly isolated family. They ро i 
a number of myrtalean attributes vean 
counterbalanced by several din 915) 
of us (Dahlgren) cannot support Orchard ( 


est connection with Cornaceae, becau 
tegmic, tenuinucellate ovules, lack ^ 
common presence of iridoids, and ot! 


and Combretaceae, the latter of whic ud 
myrtalean. Thus Haloragaceae may ; 


| 


Í 


of tannins, | 
er details | 


1984] 


treated in an order separate from, but near Myr- 
tales. In accordance with Orchard’s findings, 
Haloragaceae should be separated from Gun- 
neraceae and Hippuridaceae. Its position is pos- 
sibly closer to Araliales (near which it was placed 
in Engler & Prantl’s “Die Natürlichen Pflanzen- 
familien") than to Cornales. However, one of us 
(Thorne) agrees with Orchard in placing Halo- 
ragaceae in Cornales, and considers Gunnera- 
ceae and Hippuridaceae (see below) as related 
families in the Haloragineae. 


RHIZOPHORACEAE 


The homogeneity of Rhizophoraceae needs 
careful study. Such segregates have been de- 


opposite or alternate leaves. The stipules in some 
mangrove genera (Rhizophoreae) are relatively 
large and entire, but in another generic group 
they are minute and even dissected into minute 
components situated in the leaf axils. Contrary 
lo the Myrtales (except A/zatea), the nodes are 
trilacunar. The vessel elements in some Rhizo- 
Phoraceae have scalariform or mixed scalari- 
form/simple perforation plates, which are 
rely known in Myrtales. The flowers show sim- 
llarities with those in myrtalean families (those 
In Macarisia, for example, with flowers as in 
Lythraceae). They vary from nearly hypogynous 
Or perigynous (e.g., Ceriops) to hemi-epigynous 
(Rhizophora) or epigynous, and have variable 
merous conditions, including the tetramerous (cf. 
Sonneratiaceae). A hypanthium extending be- 
Yond the ovary occurs in some genera with epig- 
ynous flowers. Also the basically diplostemonous 
flower lype is in agreement with Myrtales; in 
Kandelia the stamens are numerous (cf. La- 
ene in Lythraceae). An intrastaminal 
к. i dia disc is generally present in the flow- 
ES ombretaceae). The pollen grains are tri- 
s cd and comparable to the basic myrtalean 
i еге are two to six carpels forming a pistil 
with 45 many locules (rarely a single locule) and 
à simple style. The ovules are bitegmic and 
стазу писе аје although the integuments have 
ie layers than is usual in myrtalean fam- 
in Page the nucellus is destroyed much earlier 
с е opment (Mauritzon, 1939). The baccate 
capsular fruit contains one or few seeds, the 
ed coat of which Corner (1976) found to re- 
ble that in some myrtalean families as well 


DAHLGREN & THORNE—MYRTALES 


685 


KRIPLION 


as that in Lecythidaceae. The seeds of several 
genera contain more endosperm than is found in 
myrtalean families. 

Chemically there is hardly any conspicuous 
feature to distinguish Rhizophoraceae from 

yrtales, but the combination of chemical at- 
tributes is not unusual. To one of us (Dahlgren) 
the lack of iridoid compounds and the richness 
of tannins argue strongly against a position of 
Rhizophoraceae in the Cornales, which is further 
supported by the embryological features: biteg- 
mic, crassinucellate ovules, formation of parietal 
cells, and nuclear endosperm formation. The 
other of us (Thorne), however, prefers to place 
Rhizophoraceae in Rhizophorineae, near Hal- 
oragineae, in his Cornales (which constitute with 
Araliales his Corniflorae). He regards Corniflorae 
as having common ancestry with Rosiflorae and 
Myrtiflorae, and believes the probable common 
ancestors of these three superorders as being most 
nearly represented today by various members of 
the Saxifragaceae, in the broadest sense. 

It is our conclusion that Rhizopl 
be excluded from Myrtales, but that they possess 


а 


to have occurred in pre-myrtalean ancestors, 
which could well indicate a fairly close common 
origin. 


LECY THIDACEAE 


ceae, Barringtoniaceae, Foetidiaceae, and Na- 
poleonaceae; Prance & Mori, 1977, 1978) has 
frequently been placed in Myrtales, alternatives 
being its inclusion in Theales, as suggested in- 
dependently by both of the present authors 
(Dahlgren, 1975a, 1980a; Thorne, 1976, 1981), 
or its treatment in a separate order (Cronquist, 
1968, 1981). 

Lecythidaceae are mainly trees, which, con- 
trary to Myrtales, lack internal phloem and ves- 
tured pits. The vessels sometimes have scalari- 
form, although more often simple, perforation 
plates. The leaves are consistently alternate and 
entire, and in certain genera, at least, are pro- 
vided with minute stipules; for this last reason 
and other reasons the family is considered to be 
myrtalean by Weberling (pers. comm.). Stomata 

isocytic, diti ther rare in Myrtales 
(but known within Onagraceae and Melasto- 
mataceae). The flowers have variable merous 
conditions, and are commonly large. They are 
hemi-epigynous or epigynous, often with con- 


The family Lecythidaceae (incl. Asterantha- 
i N 


686 


nate sepals. The petals are broad and imbricate 
(rarely lacking). There are generally numerous 
stamens and staminodia, symmetrically or 
asymmetrically disposed and developing in cen- 
trifugal sequence, as in most Theales. The pollen 
grains, at least in certain genera, are trinucleate 
when dispersed, and the tapetum is reported to 
be amoeboid. In both of these features the family 
deviates strongly from the myrtalean pattern. The 
pollen grains are tricolpate, often syncolpate (the 
Planchonia-type; Erdtman, 1952) or tricolpo- 
roidate, whereas, the simply colpate condition is 

e Myrtales. The ovary is 2–6-саг- 
pellate, with as many locules, and has a simple 
style. Placentation is axile to basal, and the ovules 
bitegmic and tenuinucellate, with the integu- 
ments being modes ки ipte nucellus more rap- 

uring than is the 
case in myrtalean taxa a (Mauritzon, 1939), Axi- 
nandra excepted (Tobe & Raven, 1983b). A pa- 
rietal cell is not formed. In these latter attributes 
Lecythidaceae are thealean. The fruits are of var- 
ious kinds and often very large (Prance & Mori, 
1978), and also the seeds (as in Bertholletia) are 
sometimes conspicuously large. The endosperm 
is chiefly or entirely absorbed during seed de- 
velopment and the embryo is large and rich in 
fat, as in myrtalean families. 

The chemical contents of Lecythidaceae large- 
ly agree with those of myrtalean families (see 
above), but also agree with those in Theales. Lack 
of internal phloem, relatively more primitive 
vessels without vestured pitting, presence of 
wedge-shaped phloem- -rays, alternate leaf ar- 
rangement, polymerous, centrifugally develop- 
ing androecium, and tenuinucellate ovules all in- 
ek thealean affinity, as does the lack of 

ndosperm in the ripe seeds. A funicular aril, as 
ue in some Lecythidaceae, has its correspon- 
dence in the thealean Clusiaceae. We do not claim, 
here, that the position of Lecythidaceae in Theales 
is settled, but a position in that order, especially 
in its own suborder, seems most appropriate. 


idly 


ELATINACEAE 


The small aquatic family Elatinaceae is gen- 
erally considered to be thealean, but deviates from 
most Theales in some features, such as in having 
stipules and in having crassinucellate ovules. 

The family consists of Elatine and Bergia, 
which are herbaceous, with the exception of the 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


partly suffrutescent Bergia suffruticosa Fenzl. The 
leaves are opposite or verticillate and possess 
small interpetiolar stipules. Neither internal 
phloem nor vestured pitting has been reported. 
The small flowers are solitary or aggregated in 
cymes in the leaf axils and possess six or fewer 
(sometimes four) sepals and an equal number of 
petals, and are diplostemonous or haplostemo- 
nous. Hypanthial as well as disc structures are 
lacking. The pollen grains are tricolporate, bi- or 
trinucleate when dispersed, and the 2-5 carpels 
form a syncarpous, 2-5-locular ovary with bi- 
tegmic, crassinucellate ovules and nuclear en- 
dosperm formation. The seeds have little en- 
dosperm (see also Tobe & Raven, 1983a), and 
the embryo varies from nearly straight to strong- 
ly curved. It is filled with protein and fat. 
This little family exhibits a combination of 


ferent interpetiolar stipules, and the hypogynous 
rather than perigynous flower argue against à ро" 
sition in Myrtales. 


CORIDACEAE 


The monotypic family Coridaceae Me 
by one of us (Dahlgren) is normally conside 
a comfortable member of Primulales and the sin- 
gle genus, Coris, is most often treated in Er 
ulaceae. Sattler (1962) provoked new ideas ! 
finding similarities between Coris a d 
Lythraceae, for example in the diírenision d 
calyx. The following similarities between 1 D 
and Lythraceae were mentioned by Sattler: " 
descending initiation of the sepal primordia 
Coris, occurring also in Cuphea; (2) simi АЫ 
icalyx-like structures; (3) valvate aestiva 
calyx lobes in both groups; 9 eee с p^ 
floral apical meristem in Cori Cuphea; is 
the centrifugally initiated motes in ‘One ап 


raceous taxa, such as Diplusodon hexand 
7) carpel initiation, starting as an ann 


in Coris and in Cuphea; (8) strongly === n^ | 


ta in the ovary in certain Lythra 
of the condition in Coris, where ch ik 
central placental column; (9) журоор ie 
ers in Coris and, although weakly, їп as TE 
thraceae; (10) similar pale crimson pe А 

and (11) secretorial cavities in Corts and 


— — ———— ^ 


1984] 


The ovules in Coris are bitegmic and tenui- 
nucellate; in the latter respect they differ from 
those in Myrtales. In the genera of Lythraceae 
studied by Joshi and Venkateswarlu (1935a, 


: 19355, 1936) the ovules are crassinucellate and 


cut off a parietal cell, although in the smaller- 
flowered genera the nucelli tend to have fewer 
cells. The condition in Coris is at present being 
investigated by Bolt-Jorgensen (Copenhagen). It 
seems that many features of Lythraceae and Cor- 
is are held in common, and at the present point 
it not easy to establish whether these have mostly 
evolved by convergence, so that we can reject 
Airy-Shaw's and Sattler's hypothesis of an affin- 
ity. The overall pattern of placentation and em- 
bryology in Coris is primulaceous. Species of Ne- 
saea іп Lythraceae (Fernandes, 1978, 1980) are 
superficially quite similar to Coris. 

Among the differences between Coris and Ly- 
thraceae thus remaining to be explained are the 
alternate exstipulate leaves, the lack of internal 
phloem, the wholly free-central placentation, and 
the tenuinucellate ovules of Coris, all non-myr- 
talean features. 

Thus both ofthe authors reject (Thorne strong- 
ly so) placement of Coris in Myrtales. 


CHRYSOBALANACEAE 


The members of this family have alternate, 
simple, entire, and stipulate leaves, the stipules 
being small but not as minute as in myrtalean 
families. The stems lack internal phloem (Prance, 
Pers. comm.) and vestured pits in the vessel ele- 
ments. In flower construction Chrysobalanaceae 

h > 24 + о НА fam- 


W CO 


< which secondarily oligo- and 
multistaminate conditions have evolved. en 


* pollen grains are 3-colporate. 
against considering Chrysobalanaceae as rosa- 
0005, are, for example, the occurrence of foliar 
Sclereids and tl fale} 1 gy د‎ 
and generally pseudomonomerous) character of 
the gynoecium when this is 2- or 3-carpellate. A 
reduction of carpel number to one (i.e., a sec- 


DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 


687 


ondary, truly monomerous condition) no doubt 
also occurs in part ofthe family (cf. the discussion 
under Elaeagnaceae) The embryology of the 
family is very similar to that in families of Theales 
(Tobe & Raven, 1984d), which favors inclusion 
of Chrysobalanaceae in that order. 
Chrysobalanaceae contain ellagic acid and el- 
lagi-tannins (Hegnauer, 1973) as do Myrtales (and 
some Theales and Rosaceae, but not Amygda- 
laceae or Malaceae). The embryo contains pro- 
tein and fat, rarely (Couepia) some starch. In 
these features the family agrees with Myrtales. 
In the light of the several conspicuous differ- 
ences between Chrysobalanaceae and Rosales 
sensu stricto and similarities between Chryso- 
balanaceae and, for example, Ochnaceae of 
Theales, the family should not be considered as 
the link between Rosales and Myrtales as may 
be thought from some gross morphological fea- 
tures. Should there prove to be a connection be- 
tween the Myrtales and the Theales (see p. 688), 
then Chrysobalanaceae come into the picture. 


ELAEAGNACEAE 


Elaeagnaceae have occasionally, but rather 
rarely of late, been associated with Myrtales. Some 
vegetative features argue against a myrtalean re- 
ationship, as the alternate exstipulate leaves, lack 
of internal phloem, and lack of vestured pitting 
in the vessel elements. The anomocytic stomata 
and peltate hairs are found also in Combretaceae 
of Myrtales, and the vessel elements have simple 
perforation plates as in Myrtales. The flowers, 
which are mostly unisexual, agree in several re- 
spects with those in Myrtales, being often tetra- 
merous, the male flowers being haplo- or dip- 
1 a 1 й 1 + 


4 41 a 


provided with a hypanthium. Petals are missing. 
Foreign to Myrtales is the monocarpellate pistil 
with a single erect ovule, but embryological fea- 
tures and the exendospermous seed of Elaeag- 
naceae agree well with the conditions in Myr- 
tales. Chemically Elaeagnaceae agree also fairly 

НК EEN aithanahtheiralkalnid 


contents, tryptophane derivatives, are special. 
Eyde (1975) considers that Elaeagnaceae can- 
not be derived from Myrtales as it has a truly 
solitary carpel (which is evidently the case; Eyde, 
1975, fig. 2), but we see no reason why the carpel 
number could not be reduced in a syncarpous as 
well as in an apocarpous gynoecium. However, 


688 


there are other reasons why Elaeagnaceae cannot 
be considered of myrtalean origin, such as their 
lack of internal phloem. The pollen grains are 
tricolporate, being sometimes reminiscent of 
those in certain Myrtaceae. 

Both authors (Thorne, 1981; Dahlgren, 1980a) 
believe that Elaeagnaceae are closely related to 
Rhamnaceae, which was also proposed by 
Hutchinson (1959). This is supported by simi- 
larity of seed coat (Corner, 1976) and by par- 
asitizing fungi (Thorne, 1979). The position of 

oth of these families in relation to the Myrtales 
is assumed to be distant, with some similarities 
explained by convergence (see Rhamnaceae, be- 
low), but th imilarities clearl 
study. 


^^. 41 
J VVOVI YY LIU LIL! 


FAMILIES SOMETIMES ASSOCIATED WITH, BUT 
APPARENTLY DISTANTLY RELATED 
TO MYRTALES 


Rhamnaceae are among those families which 
only occasionally have been mentioned as pos- 
sibly related to myrtalean families, but which 
exhibit some interesting similarities. They are 
woody and have simple, often opposite leaves 
with (or rarely without) small or moderate-sized 
stipules, which may be present as a row of small 
hair-like structures. Intraxylary phloem is lack- 
ing, and the vessels have no vestured pitting al- 
though their perforation plates are simple as in 
Myrtales. The flowers are actinomorphic, with 
inferior to superior ovary, and generally have 
small petals opposite a single whorl of stamens. 
A hypanthium occurs in several genera (cf. 
Elaeagnaceae), and there is usually a prominent 
disc. The pollen grains are mostly tricolporate 
and two-celled. The carpels are 2-5, forming a 
syncarpous 2—5-1осшаг pistil with simple style, 
which agrees with myrtalean families, although 


the locules have but one ovule each. The em- 


are peculiar in the production of benzylisoquino- 
ine alkaloids, d ted i 1 


ral genera. An- 
thraquinones are common. Tannins are present, 
but ellagic acid or ellagi-tannins have not been 
recorded. 

The family cannot be considered seriously for 
membership in Myrtales, especially because of 
vegetative anatomy and chemistry, although 
technically there are a number of obvious sim- 
ilarities. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


Datiscaceae were recently thoroughly ге- 
viewed by Davidson (1973, 1976). Shaw (1973) 
suggested relationship with Haloragaceae, which 
are often placed in Myrtales. Therefore mention 
may be justified here. Datiscaceae consist of three 
genera, the herbaceous Datisca and the tree gen- 
era Octomeles and Tetrameles. The latter genera 
may represent the more nearly ancestral forms. 
Internal phloem is lacking in the stem. The leaves 
are alternate and exstipulate and bear multiseri- 
ate, peltate or glandular hairs. As in many Myr- 
tales, these genera possess branched sclereid id- 
ioblasts. The flowers are 4- to 8-merous in calyx 
and (when present) corolla, and the pollen grains 


which is rare in Myrtales. Davidson on the basis 
of an extensive survey of the family concluded 
that it was not allied to the Myrtales. Links to 
Flacourtiaceae and other families of Violales аге 
apparently most likely. 

Marcgraviaceae in their opposite leaves, flow- 
ers which may have numerous stamens, and the 
nearly exendospermous seeds show some super- 
ficial similarity to Myrtales. There is no internal 
phloem, no vestured pitting, stipules are lacking. 
androecial developmental sequence is centrifu- 
gal, and ovules are tenuinucellate and at least mn 
some taxa have cellular endosperm formation. 
These features are all lacking in Myrtales (cellular 
endosperm also in Theales). From the evidence 
available Marcgraviaceae seem best placed in 
Theales. 


n well 
as in several families of Myrtales, often are 


supplied with branched sclereid idioblasts. ape 
ules, internal phloem, and vestured РИШ И 
lacking. The flowers are mostly тоге open hy- 
in the Myrtales and lack the сопзрилир aa 
panthium of this order. They have from five d. 
liceria and other genera) to numerous "a 
These, however, tend to develop in centri зд 
succession. The anthers of a Camellia "d 
for example, also possess a laterally exp? 
connective reminiscent of that in some p 
lean members. The syncarpous pistil has à " 
style, and the ovules are anatropous and, 

the exception of their tenuinucellate Boy 
(and lack of development of parietal се | 
somewhat similar in their embryology " 

of Myrtales. Rarely are they unitegmic. The 


— 


———— 


1984) DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 


also lack endosperm. The alkaloid content in 
many Theaceae consists of purin bases. Other- 
wise Theaceae resemble the myrtalean families 
in containing ellagi-tannins. The similarities be- 
tween Theaceae (and other thealean families) and 
Myrtales are ambiguous but (in the view espe- 
cially of one of us, Thorne) do not indicate a 
close phylogenetic affinity at all. 

Clusiaceae (Hypericaceae) agree with Thea- 
ceae in showing certain similarities to Myrtales 
(see also above for Lecythidaceae), but do not 
have the internal phloem and usually lack stip- 
ules. The lack of hypanthium, the tenuinucellate 

a 


may superficially resemble Myrtaceae, but the 
secretory ducts contain great amounts of yellow 
lo red phenolic pigments consisting of anthra- 
quinone and xanthone derivatives and coumar- 
ins, which are not matched in Myrtaceae. A close 
relationship to Myrtales thus cannot be seriously 
Proposed. 

Myrsinaceae consist of woody plants with al- 
ternate or opposite leaves without stipules. In- 
ternal phloem is lacking. The vegetative parts 
have schizogenous ducts with resinous contents. 


her, and the ovules in addition are tenuinu- 
cellate. Finally, the seeds are rich in endosperm, 
which they are not in Myrtales. These conditions 
indicate that Myrsinaceae are rather closely al- 
led to Primulaceae rather than to families in 
Myrtales. 

Geissolomataceae (see Dahlgren & Rao, 1969; 
Carlquist, 1975) are a monotypic South African 
amily which has often been associated with Pen- 


= at all, see Fagerlind & Dunbar, 1973). In 
> the pollen grains lack pseudocolpi 
Ich Penaeaceae have), the stylodial branches 


689 


are free from each other, and the seeds have co- 
pi dos and a small embryo. Therefore, 
there are no reasons at all to include the genus 
in Myrtales. Rather, a position in or near Ha- 
mamelidales or in Cunoniales (proposed by 
Dahlgren) seems appropriate, which agrees well 
with the view of Thorne, who firmly believes that 
Geissolomataceae are closely related to Bruni- 
aceae and places these in the suborder Bruni- 
neae, along with Buxineae and Pittosporineae, 
in a widely circumscribed order, Pittosporales 
(Carlquist, 1975; Thorne, 1975, 1977, 1981). 
unneraceae, with the single genus Gunnera, 
are herbaceous plants with a habit different from 
5 


cellular endosperm formation, and seed with со- 
pious endosperm and a tiny embryo, comprise 
important diff fi Myrtales. This family 
also seems to have no close relationship to Hal- 
oragaceae, though one of us (Thorne) still prefers 
to retain Gunneraceae in his suborder Halora- 
gineae of Cornales. 


P A BAe DW. .1 » A 


I l'ULCGCCQOC 5119 W | 
to myrtalean families but lack internal phloem 
and have alternate leaves without stipules. The 
flowers are hypo- to perigynous and as in most 
Myrtales have a tetramerous perianth on a con- 
spicuous hypanthium. Pollen grains morpholog- 
ically have some resemblance to those in Ona- 
graceae (but no viscin threads and a very different 
exine structure) but hardly to those in other myr- 
talean families. The pistil is monocarpellate. The 
embryology agrees with that of Myrtales in most 
features, and the ripe seed is almost devoid of 
endosperm. The chemical characters are similar 
to those of Myrtales (tannins, flavonols, occa- 
sional aluminum accumulation, cyanogenic 
compounds) except that ellagic acid is not re- 
corded. Proteales are quite distinct from Myr- 
tales. 

Malpighiaceae resemble superficially Lythra- 
ceae in the often violet, unguiculate petals wit 
wavy margins. They lack internal phloem, but 
the vessels have vestured pits as in Myrtales and 
the perforation plates are simple. The leaves are 
simple, alternate or more often opposite, and 
may or may not have stipules. The 
stomata and branched “‘malpighian”’ hairs 
be, however, unusual in Myrtales, and papillae 
are frequently present on the lower surface of the 
leaves. The plane of symmetry of the flower, 
which is slightly zygomorphic, is oblique, the 
flowers are obdiplostemonous, and in contrast 


690 


to all Myrtales, the stylodial branches are often 
separate to their base. Each of the 3—5 locules 
has one pendulous, hemi-anatropous ovule with 
an embryology similar to that of Myrtales; the 
embryo sac, at least in some cases, is tetrasporic 
and reputed to resemble that in Penaeaceae. The 
seeds are exendospermous. The fruits vary but 
tend to be schizocarps, quite dissimilar to any 
found in Myrtales. Chemically, the family resem- 
bles various Myrtales in having triterpene sa- 
ponins, but ellagic acid is not reported and the 
tannins seem to be of the condensed type only. 

Malpighiaceae do not seem to be very close to 
Myrtales, but a number of similarities suggest 
that a set of attributes occurring in Polygalales 
(or Polygalineae of Geraniales) are held in com- 
mon with that in Myrtales. 

Pittosporaceae lack stipules and have schizo- 
genous secretory ducts with resinous contents. 
Their production of polyacetylenes, unitegmic, 
tenuinucellate ovules, and copious endosperm 
and very small embryo in the ripe seeds do not 
indicate myrtalean affinity. 

Escalloniaceae and Icacinaceae, whether 
closely related to each other or not, both differ 
from Myrtales in similar ways. They lack stipules 
and a hypanthium, and they have unitegmic and 


endosperm formation. In addition, they occa- 
sionally contain iridoids, which have not been 
found in Myrtales. 

Montiniaceae (Montinia, Grevea, and Kali- 
Phora) agree in morphology and especially in em- 
bryology with the majority of Cornales and also 
contain iridoids, which are quite common in this 
order. Griseliniaceae are probably related here 
too, along with Escalloniaceae, but need to be 
studied further. 

Columelliaceae in overall floral construction 
and embryology (unitegmic, tenuinucellate ovules 
with cellular endosperm formation and terminal 
endosperm haustoria) are typically cornalean and 
thus can safely be excluded from M les. 

Montinioideae, Griselinioideae, Escalloni- 
aceae, and Columellaceae are treated by one of 
us (Thorne) in the Saxifragineae of the order Ro- 
sales, which he id have i 
with the Cornales. 

Dialypetalanthaceae (Fig. 16), like Rubiaceae, 
have opposite leaves with interpetiolar stipules, 
but the petals are free, the stamens 8-12(-16), 
the ovules more numerous, and the seeds differ- 
ent. The pistil is bicarpellate, and the fruit, al- 
though capsule-like, opens up as a Schizocarp. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


The flat seeds are numerous, flat, winged, and 
apparently have evolved from unitegmic ovules. 
The position of this family although not yet firm- 
ly placed in Gentianales certainly does not seem 
to fit into Myrtales. The stomata (Н. Rasmussen, 
pers. comm.) are paracytic, indicating (albeit not 
definitively) affinity with the Rubiaceae. Dialy- 


IP. 4 
ofthe Rubiaceae or a relict family closely related 
to the Rubiaceae in the Gentianales. 

Loganiaceae and Rubiaceae are preferably 
placed in the same order, Gentianales, of sym- 
petalous angiosperms. Like Myrtales they have 
opposite leaves, vestured pits, and many Logani- 
aceae also have bicollateral vascular bundles. In- 
terpetiolar stipules of rubiaceous type are absent 
in typical Myrtales, and stipules are lacking in 
Loganiaceae. 

Loganiaceae and several other families in Gen- 
tianales show a combination of intraxylary 
phloem and vestured pits, as do Myrtales, 
Thymelaeaceae (or most of its taxa according 10 
its circumscription), part of Vochysiaceae, and 


one genus of Polygonaceae. Van Vliet and 
AG RUM i REN Myrtales 
and Gentianales, e.g., Loganiaceae sensu — 
the combination of intraxylary phloem, - pe 
i uide add di : f crystal ty 


tfl, 


r-tra 


Е 
e 


(including raphides and styloids) as shown si 
Mennega (1980). This calls for a general mer 
of other features. The embryology of Logan 


aceae [which in the sense of Leeuwenberg n 


generally provided with copious овде о 
Chemically, Gentianales show little име 
Myrtales (see Dahlgren et al., 1981), and им 
morphology the similarity may be supe Gen 
Thus, in spite of the fact that Myrtales and 


|- 
(1980a; Dahlgren et al., 1981), one of us (Dah 


gren) does not consider the two orders as i i 
is case that ! 
es have 


wood-anatomical and floral similarities ges gi 
been retained from common, proto- 
ancestors. 

Hippuridaceae (= Hippuris) from e 
(1969) chemical account, also according 


uer s 


le 


1984] DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 691 


ow 


E^ 
|| 


qM RE 16. Sarees fuscescens Kuhlm., forming the monotypic Brazilian Dialypetalanthaceae: A- 
В fiting b al. 8967. H-J. Prance et al. 6526. —A. most part о of i nflorescence and u uppe per leaf pairs o 
it Rede note the vari —C. flower just before opening, showing 
Pals and petals. — D. inner petals. —E. an outer petal.—F. flower in соф udi pre section, petals 
oe џ шы stigma in detail.—G. stamens; above: staminal tip in detail.—H. capsules ifferent views, 
right opening along carpel commissures.—I. placenta with seeds.—J. seeds. (Orig., del. В. сна п.) 


692 


gren (1975a), Jensen et al. (1975), and Wagenitz 
(1975), seem to be best removed far from Hal- 
oragaceae, and show no discernible relationships 
to Myrtales either. Yet Cronquist (1968) and 
Thorne (1976, 1981) on the basis of other sim- 
ilarities prefer to retain Hippuridaceae in the same 
order Haloragales or suborder, Haloragineae, with 
the Haloragaceae and Gunneraceae, though both 
agree that these families are not close relatives 
of Myrtales but probably have common ancestry 
with them and Rosales. The leaves are verticil- 
late, and the small, epigynous flowers are so re- 
duced as to give very little morphological indi- 
cation of relationships. However, the unitegmic, 
tenuinucellate ovules with cellular endosperm 
formation, and the chemical spectrum, including 
the biosynthesis of carbocyclic iridoids, indicate 
scrophularialean or, alternately, cornalean affin- 


ity. 

Callitrichaceae have now received an accept- 
able position near Verbenaceae and Lamiaceae 
on the basis of the 4-seeded schizocarps, uni- 
tegmic and tenuinucellate ovules, cellular en- 
dosperm formation, terminal endosperm haus- 
toria, and carbocyclic iridoids, all characteristics 
that are foreign to Myrtales. 


RELATIONSHIPS OF THE ORDER MYRTALES 


The position of the order Myrtales has varied 
in different classifications and is still a matter of 
divergent opinions. Cronquist (1981) and Takh- 
tajan (1980) in their recent classifications have 

en somewhat constrained by their division into 
the subclasses Dilleniidae and Rosidae of the 
majority o ipetal rd f dicotyled 
Myrtales in both classifications are placed in the 
Rosidae, where they form the main order in 
Takhtajan's superorder Myrtanae. It is generally 
agreed that the order is more or less related to 
Rosiflorae, including Rosales, Saxifragales, and 
Cunoniales, although other, quite small, orders 
occasionally treated with Myrtanae are consid- 
ered even more closely related, as Haloragales 
and Rhizophorales (and Lecythidales) when these 
are acknowledged. Other orders sometimes rec- 
ognized and often associated with Myrtales are 
Elaeagnales and Thymelaeales. Theales and pre- 
sumably closely related Primulales, being mem- 
bers of their Dilleniidae, have tended to be left 
out of comparison, although at one Occasion or 
another the similarity has been pointed out, e.g., 
by Hickey and Wolfe (1975). 

Several of these groups have been compared 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


on the previous pages with myrtalean families, 
notably those representing monofamilial orders 
in some classifications, or have even been in- 
cluded as components in a more widely circum- 
scribed Myrtales: Haloragaceae (Haloragales), 
Rhizophoraceae (Rhizophorales), Thymelae- 


es) and Elaeagnac 
generalities will be discussed, and other orders 
compared with Myrtales. 
T ma ix 4 had orant 


+ 1 ++ 


which g 
importance above are the occurrence of internal 
phloem, i.e., the presence of bicollateral vascular 
strands, and of vestured pitting in the vessel ele- 
ments. When the Myrtales are strictly circum- 
scribed, these characteristics become critical. 

nly one of the serious candidate families for 
myrtalean membership mentioned above pos- 
sesses both bicollateral vascular strands and ves- 
tured pits, viz., Thymelaeaceae (these features 
being shared also with some Euphorbiaceae). 
Cronquist (1968, 1981, 1984) includes Thyme- 
laeaceae in Myrtales, but, as pointed out previ- 
ously, this meets with serious objections, espe 
cially with regard to phytochemical an 
embryological evidence. 

nother order where opposite leaves аге сот" 
bined with internal phloem and vestured pits 1S 
Gentianales, within which especially Logani- 
aceae show some resemblance to Myrtales. Be- 
cause floral morphology, embryology (unites: 
mic, tenuinucellate ovules), and chemistry (lac 
ofellagic acid and tannins on the whole, en 
of iridoids and indole alkaloids) are vastly dif 
ferent, one of the authors (Dahlgren) does not 
consider the relationship between the L 

e 
Disregarding bicollateral vascular strands and 

vestured pitting, Haloragaceae, Rhizophorace "i 
Elaeagnaceae, and Chrysobalanaceae prov! : 
combinations of attributes which are not p 
ously different from the myrtalean, although kei 
ious peculiarities in each family would be à s 
rant or at least *untypical" in Myrtales. = й 
main phytochemical spectrum these um 
in good agreement with the myrtalean iem 
and vegetative as well as floral details, also. г< 
conspicuously similar in various respects uf. 
ever, it is important to remember that mor * 
the basic features of Myrtales are widesp n 
choripetalous dicotyledons. None of the re 
mentioned which lack internal phloem an ave 
tured pitting seems to relate (in compar? 
morphological terms) clearly to any of the 


~ = 


== 


————  OoO0"«c———— 


1984] 


families" of Myrtales. Thus it seems convenient 
and adequate to use the presence of these two 
attributes as significant diagnostic criteria for 
Myrtales. 


MYRTALEAN VERSUS ROSALEAN ATTRIBUTES 


One of the families mentioned above as par- 
ticularly similar to many Myrtales is Chryso- 
balanaceae. This has been alternately referred to 
Rosales and Fabales (where these orders are not 
united); whereas, its position in Myrtales has 
hardly ever been suggested. Disregarding the lack 
of internal phloem and vestured pitting, the fam- 
ily seems to agree nearly as well with myrtalean 
as with rosalean attributes, thus justifying a com- 
parison. Rosales sensu stricto normally include 
at least Rosaceae, Neuradaceae, Amygdalaceae, 
and Malaceae [all more often treated as subfam- 
ilies of Rosaceae sensu lato, whereas the Chry- 
sobalanaceae are often treated separately, in the 
Vicinity of Sapindaceae and Connaraceae (in 

pindales or Sapindineae of Rutales)]. 

| Vegetatively Rosales sensu stricto are diver- 
sified: they are basically woody plants, the vessels 
of which generally have simple perforation plates. 
Stomata are mostly anomocytic, mucilage cells 
are common, and glandular hairs are common. 
The leaves are generally alternate, quite often 
compound, and in many species have well-de- 
veloped stipules (never represented by rows of 
finger-like Projections in the leaf axils as in many 

yrtales). The leaf teeth in Rosales are of the 

08014 type (Hickey & Wolfe, 1975) and are 
‘lightly resembled by those in some genera of 
Onagraceae (Hickey, pers. comm.). The flowers 
аге basically actinomorphic and the inflores- 
cence determinate. A conspicuous similarity to 
the Myrtales is the prominently developed floral 
receptacle, which in several groups results in pe- 
"8yNous, urceolate types comparable to those in 
many Myrtales. A second trend, with elevated 
receptacle, has not evolved in the Myrtales. The 
letramerous condition is rare in Rosales, but 
EM (although, quite likely, secondary) in 
di Myrtales. The androecium of Rosales, al- 

ugh probably evolved from a diplostemonous 
M. has multiplied by the insertion of more 
Е 5 as well as by increase of initials in each 
h orl. A presumed primitive condition is the 
Pocarpy of many Rosales. A syncarpous pistil 
occurs only in a few Chrysobalanaceae and in 
*Pigynous Malaceae (= Rosaceae subfam. Maloi- 
deae). Rosales sensu stricto and Myrtales agree 
*ssentially in pollen morphology, embryology, 


DAHLGREN & THORNE—MYRTALES CIRCUMSCRIPTION 


693 


sparsity of endosperm in seed, and also in phy- 
tochemistry. Chrysobalanaceae deviate from the 
"typical" rosaceous pattern in several respects. 
In some of these, as syncarpy, single style, ur- 
ceolate receptacle, and mode of stamen multi- 
plication, they approach the Myrtales, although 
this may be by convergence. New embryological 
evidence (Tobe & Raven, 1984d) indicates great 
agreement with families of Theales, and Chry- 
sobalanaceae may best be treated as a member 
of this order. 


MYRTALEAN VERSUS CUNONIALEAN ATTRIBUTES 


Cunoniales (Dahlgren, 1980a) can be variously 
circumscribed, but their delimitation from Sax- 
ifragales contributes difficulties. In some respects 
this group of families is more specialized than 
Rosales sensu stricto, e.g., in having more often 
syncarpous pistils, but in other features it shows 
much less specialization, as in wood-anatomical 
characteristics and abundance of endosperm in 
the seed. Stipules with various degrees of devel- 
opment occur in the order, thus agreeing with 
Myrtales, where they are mostly present but mi- 
nute. The basically diplostemonous flowers, 
which are more often 5- than 4-merous, the gen- 
eral lack ofa hypanthium, a h pres- 
ence of a well-developed disc are only partly in 
agreement with the myrtalean pattern. The gy- 
noecium in Cunoniales ranges from nearly apo- 
carpous to syncarpous, and the mature seeds dif- 
fer from those in Myrtales by having, as a rule, 
copious endosperm, but embryological and phy- 
tochemical characteristics are not very different 
from those in Myrtales. As Cunoniales, which 
are dubiously homogeneous, show resemblance 
to Rosales and Saxifragales (Thorne treats all 
three as suborders of Rosales), they also ap- 
proach a hypothetical ancestral myrtalean type. 
However, the similarity between families of the 
orders is not particularly impressive to some 
phylogenists. 


MYRTALEAN VERSUS SAXIFRAGALEAN ATTRIBUTES 


Saxifragales sensu stricto (Dahlgren, 1980а), 
include Crassulaceae, Saxifragaceae sensu stric- 
to, and a few small families, e.g., Grossulariaceae 
(Saxifragaceae subfam. Ribesioideae), some often 
included in Saxifraceaeae sensu lato. The two 
principal families may not be as closely allied to 
each other as often stated. Each of them agrees 
in many respects with Myrtales, especially in flo- 

: т. Î partiy also in chemistry. Op- 


694 


posite leaves characterize many Crassulaceae, but 
stipules are lacking. The pentamerous or, espe- 
cially in Crassulaceae, often tetramerous flowers 
are obdiplostemonous, but the significance of the 
difference between this and the diplostemonous 
condition is obscure. In Crassulaceae, the carpels 
are isomerous with the other floral whorls, as in 
many Myrtales, and the seeds are also exendo- 
spermous; whereas, in Saxifragaceae the seeds 
have copious endosperm. The tubular flowers of 
many Crassulaceae, e.g., Kalanchoé, should not 
be confused with the similar ones in many Myr- 
tales, because in Myrtales the floral tube repre- 
sents a true hypanthium. In Crassulaceae, how- 
ever, it consists of the fused petals only 
(sympetaly!), to which the filaments are more or 
less adnate. The endosperm formation in Saxi- 
fragales is intermediate (helobial) or cellular, 
which is never the case in Myrtales. 

In Saxifragales, the Grossulariaceae (Ribes), no 
doubt by a combination of parallel and conver- 
gent evolution, have developed a number of fas- 
cinating similarities to Fuchsia (Onagraceae), and 
exhibit a combination of epigyny, a simple (or 
cleft) style, an urceolate to tubular hypanthium, 
often brightly colored like the calyx lobes, fre- 
quently reduced petals, and a baccate fruit (Ribes 
speciosum is called "California-Fuchsia"). The 
seeds are, however, enclosed by a carnose, juicy 
arillus, the endosperm is copious, and the em- 
bryo is minute. 

There are accordingly no close bonds between 
the Saxifragales sensu stricto and the Myrtales, 
although some basic features indicate that the 
groups may be derived from distant common 
ancestors. 


MYRTALEAN VERSUS RUTIFLOREAN ATTRIBUTES 


What has been said for the previous orders is 
partly valid also for various members of the or- 
ders Rutales sensu stricto, Sapindales, Gerania- 
les, and Polygalales, where the general level of 


ceae, may strongly resemble myrtalean families 
hint each Nibil Ai с. 


portant ашегепсеѕ from them 
and lacks internal phloem and a hypanthium. In 
both aforementioned families there are, for ex- 
ample, separate stylodial branches instead of a 
single style. There is, however, within the ruti- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


florean complex a basic morphological, embry- 
ological, and phytochemical pattern of charac- 
teristics which approaches that of the Rosiflorae 
as well as the Myrtiflorae. However, any rela- 
tionships between these groups must be fairly 
distant. 


MYRTALEAN VERSUS THEALEAN ATTRIBUTES 


The comparison between the orders Myrtales 
and Theales is justified because of certain shared 
attributes. Also, Lecythidaceae have quite often 
been included in Myrtales, and indeed some of 
their members are similar to such large-flowered, 
polyandrous tree genera as Sonneratia, Duaban- 
ga, Punica, and Lafoénsia within Myrtales. Also 
various details, such as the occurrence of minute 
stipules in some Lecythidaceae (Weberling, 1958) 
and the similar phytochemistry, could be taken 
to support the view that the Theales and Myrtales 
may be distantly related. 

The members of Theales are mostly woody. 
They lack the internal phloem and vestured pit- 
ting of the Myrtales and often have more prim- 
itive vessel types; but they resemble many Муг 
tales frequently in having foliar sclereids, although 
possession of the latter is usually a feature of low 
phylogenetic significance at this level (Rao & "e 
1979). The flowers vary in merous condition 
but are more rarely tetramerous and а typ! 
hypanthium is rare. The petals are normally e 
and imbricate. Typical of a great part of Th "i 
are the numerous stamens with соп ИН 
velopmental succession. Pollen morph 
above, under Lecythidaceae), bitegmic 0 d 
nuclear endosperm formation, and paf 
lack of endosperm in the ripe seed are d 
but not high level, agreement with ape 
Myrtales, but the ovules are generally ten ta 


1 es 
issimilar to those in M 
cellate and diss 


tales. Many taxonomists, on the ea i 
; і consider the 
differences mentioned, ‚ that they 


are placed in different subclasses, 11 in the 
Dilleniidae and Myrtales in the RM cul 
classifications of Takhtajan (1980) a 

quist (1981). 


¬ 


- 


~ 


= 


= 


a 


1984] 


MYRTALEAN VERSUS CORNALEAN ATTRIBUTES 


For Rhizophoraceae as well as Haloragaceae, 
alternative positions suggested in most literature 
are either in Myrtales or in Cornales. Therefore 
a short note on the differences between these two 
orders is justified. Crucial in this connection is 
the definition and circumscription of Cornales 
(see Huber, 1963). As defined by one of us (Dahl- 
gren) Cornales include a number of families 
(among others, Cornaceae, учганеасс, 
Montini naceae, Sy 
plocaceae, Adoxaceae, сано with var- 
iably opposite or alternate leaves, without inter- 
nal phloem, with vessel elements having simple 
or scalariform perforation plates, and lacking 
vestured pitting. The flowers are sympetalous, 
and embryologically the families are fairly well 
defined by the generally unitegmic, tenuinucel- 
late ovules and cellular endosperm formation 
(Philipson, 1974; Dahlgren, 1975b), which com- 

ine with the frequent occurrence of iridoid 
compounds (Jensen et al., 1975) but lack of ellagi- 
tannins. When so circumscribed, Dahlgren con- 
siders the order fairly homogeneous, and as hav- 
inga quite distant relationship with the Myrtales. 

In at least the wood-anatomical features, Hal- 


acteristics Dahlgren finds little to support such 

à relationship. 

e ond author, “о p a very dif- 
n for his Cor- 

nales, which permits inclusion of the above- 

mentioned two families in the order. 


erent 


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4 
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ophyll 


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| Lega Chlo- 


areview 


MYRTALES AND MYRTACEAE— 
A PHYLOGENETIC ANALYSIS! 


L. A. S. JOHNSON AND B. G. BRIGGS? 


ABSTRACT 
Phylogenetic analysis of 19 families or quasi-families of the Myrtales is carried out by CLAX, a 


new numerical t technique, as well as by: other Aeon the comparative merits of which are 
TI 


e discussed. 


particular Psiloxylaceae- Heteropyi ШШ 


and the Lythraceae sensu ‘lato (including Punk Duabanga, and Sonneratia). O 


eae are very 


aden but may have an early link with Trapaceae. Memecylaceae and Студио твом аге зерага! ted 
to, a family atk is recognized, and the new unigeneric family 


«йди антин: is described. The earlier suggestion 


Scenarios of phylogeny are given, with attention to phyiogeography; the order: seems to have origina ated 


a considerably ғ си picture. of tribal and generic relationships; the formerly 


е sensu stri icto) in West 
es 


su 
d. The subfamily Chamelaucioideae, as 


discarded by us, is shown to be a cde kon grade taxon, and cannot 


suballiance, much less as a subfam 


. Consideration is given to the status of Kjellbegiodendron the 


(possibly combined) uci eden Са Eucalyptus alliances, the Acmena alliance, and Osb 


1. INTRODUCTION 


Our task is twofold: to consider the place of 
Myrtaceae among other families, and to provide 
an analysis of the major subdivisions within the 
family. In this we adopt an explicitly phyloge- 
netic approach, attempting to present a recon- 
struction of ancestral conditions and a set of pos- 
sible scenarios of subsequent developments. An 
endeavor to view the Myrtaceae in context has 
required general consideration of the phylogeny 
ee Myrtales. Indeed, as thie study progressed, it 


+ 


general questions. This led to some overlap Sith 
the field covered in this symposium by Dahlgren 
and Thorne. 


аэ ы 


to 
' For helpful discussigns and the provision of unpublished information or specimens we are юма 
Guéh 


Graham, John Green n/Peter Wilson, Paul Gadek, 
Lassak, Helene Martin, E 

Trace ^ 

in или арын Rolf Dahlgren and Pieter Baas, for th 


The data on which our analyses have pes 
based were in part gathered independently 0 
those presented by Dahlgren and Thorne, but 
these authors drew our attention to the pe 
cance of some taxa (particularly Alzatea pe 
Rhynchocalyx) and enabled us to include a 
tional characters. Our conclusions and theirs now 
agree in most respects. 


2. METHOD OF PHYLOGENETIC ANALYSIS 


2.1 APPROACHES 

w, but in the 
ly promoted. 
schools 0 of 


Phylogenetic analysis is not ne 
last decade has been most vigorous 
especially in zoology, by the various 


Shirley 
ruce Knox, 


and, 
be, 
dgardo Romero, Rudi Schmid, Keith Taylor, Joy Thompson, Ниш 26 jum. 
y, John Waterhouse, and Elsa Zardini. We thank Peter Raven and | other contributors to tht 
al before p 


n various ways relating to methods of ph ylogenetic. analysis we are grateful to 


С hris Jo hnson, Louisa Murray, Peter Weston, and 


of the following —— 
Botanical Garden, St. Loui 
Western Australian Herbarium, ‘Pe 
assistance and drawing of diagrams. 
2 Royal Botanic па Sydney; imo 2000. 


ANN. Missouri Bor. GARD. 71: Oa 1984. 


Canberra; the Royal Preto 
; the E Срески Herbarium, Brisbane; the National Herbarium, 
rth. We also wish to thank Louisa Murray an 


and Don Fortescue for ог technic 


- 


- — 


~ 


а 


Мала ал ааа i V" 


1984] 


cladists. Unfortunately, this approach is becom- 
ing overwhelmed by methodological preoccu- 
pation. Hull (1979) gives a balanced account, 
which has been largely ignored by the enthu- 
siastic practitioners of what he has called “Cla- 

ism with a capital С," just as Johnson’s (1969, 
1970) and other criticisms of Adansonian phe- 
neticism were not refuted, but simply ignored, 
by its adherents. 

We reject all forms of phenetic analysis for 
purposes of phylogenetic reconstruction at higher 
taxonomic levels. Johnson (1969, 1970) gave an 
exhaustive criticism of the unsound, or indeed 
biologically almost nonexistent, theoretical 
foundations of phenetics in such applications. 
Phenetics is moribund among zoologists, al- 
though discerning students of evolution such as 
Ernst Mayr (1981) find it necessary to reiterate 
Its theoretical as well as practical deficiencies. In 
botany it lingers on, and new applications of hard- 
core phenetics (e.g., Barabé et al., 1982; Mac- 
arlane & Watson, 1982) continue to appear, with 
no indication to their readers either that the foun- 
dations have been challenged or that a different 
approach exists and flourishes. 


2.2 THE CLAX METHOD 


One of us has been involved in the develop- 
«ещ (Johnson & J ohnson, in prep.) ofa cladistic 
(“small с”) method, CLAX. Full exposition of 
this method must unfortunately await presen- 
lation elsewhere, but the results of hand-working 
data on Myrtales by CLAX and by the variant 
CLAXMIN are given and compared briefly with 
those from several other procedures. The CLAX 
results lead to several competing phylogenetic 


Fypotheses but several groupings are robust un- 
е 


stri i к : 
trict neo-Hennigian cladograms in laying stress 


^. length of internodes, including final branches 


character-states (see below, 3.1.2), as indeed can 
н other methods of numerical cladistic 
nalysis. These do not contribute to the topo- 


JOHNSON & BRIGGS—PHYLOGENETIC ANALYSIS 


701 


logical determination of generated trees, but do 
enable us to see something of the extent of evo- 
utionary change. [Eldredge and Cracraft (1980) 
distinguish “trees” from cladograms, using the 
ormer term more or less for what we call phy- 
ograms. The term “tree,” however, has an es- 
tablished meaning in graph theory. This math- 
ematical meaning embraces both cladograms and 
phylograms, as pointed out by Rohlf and Sokal 
(1981). Such diagrams, with an **ancestral" point 
specified, fall into the subclass of “directed trees." 
Herein, we shall use “tree” in general to signify 
“directed tree."] “Риге” cladograms can be ex- 
tracted from such phylograms, without change 
of topology. These phylograms in no way con- 
found cladistic procedure by mixing in 
ics," contrary to the 


— 


=“ ы 


Mayr's (and others’) “evolutionary” approach to 
phylogeny. 

CLAX is a much-refined development of a 
method of phylogenetic analysis outlined pre- 
viously (Johnson & Briggs, 1975). It is a “top- 
down” procedure, and the core of its algorithm 
unites in pairs (or larger sets) those taxa with the 
highest score of derived states (apomorphies in 
common), continuing the process at each de- 
creasing “advancement level.” An important 
feature is that equal possibilities of minimal and 
subminimal length can all be followed through 
at all stages. The method assumes that we can 
usually assign polarity to character-state changes 
(variations in the polarity assumed are treated 
separately) and also, in general, that the greater 
the number of apparently synapomorphous (de- 
rived in common) character-states of any two or 
more taxa the greater the confidence we can have 
in the common derivation of the characters on 
the stem concerned. 

In all methods of cladistic analysis, the user 
determines which characters to use, on the basis 
of the distribution of features in the taxa, his 
judgment as to what features are homologous, 
and what should be regarded as single characters 
or syndromes of several characters. In the same 
way it appears that there is a place for judgment 


In its basic form, CLAX does not generate re- 
versal of character-state changes, and conse- 
quently the position of the root of each tree is 
determined. The user may decide whether re- 
versal of a particular character is acceptable, as 
we have done in our analyses. Such reversal is 
by explicit rescoring in data matrices or in the 


702 


submatrices for parts of a tree. Additional com- 
putation is necessary, of course, where alterna- 
tives of this kind are invoked. 

For comparison, and for those who insist on 
methods that generate reversals unrestrainedly 
in the search for shorter trees, CLAXMIN—a 
development from CLAX —has also been used 
(2.4.1), as have some existing methods. In con- 
trast to CLAX, we do not recommend any such 
method as CLAXMIN as an approach to phy- 
logenetic analysis. 

CLAX acknowledges the methodological val- 
ue of parsimony (but not any principle of evo- 
lutionary parsimony as such; see the excellent 
critique by Crisci, 1982) though not at the ex- 
pense of accepting unrestrained reversals. Most 
cladistic procedures strive to obtain а “most par- 
simonious" solution, in the sense of a tree or 
"network" (— undirected tree) of minimal length 
for the characters and the scori sed. 
However, it should be remembered that (1) they 
frequently fail to find a shortest tree, (2) there 
may be very many shortest trees of which they 
find one or two at most, (3) there may be an even 
greater number of supraminimal trees longer by 
only one to two steps, (4) variants, whether min- 
imal or supraminimal, may differ greatly from 
each other in topology, (5) shortest trees in prac- 
tice tend to invol d often repeated 
reversals of character-state change, (6) shortest 


minimizing assumptions necessary for “ехрја- 
nation" in a wider context. 

CLAX was developed to avoid the pitfalls of 
(2) and (3) in a top-down method with user- 
control of character reversibility, as well as user- 
choice intervention at intermediate stages for 
large taxon- and character-sets where numbers 
of alternatives may be generated. 

A A a 


top р t necessarily find 
the shortest no-reversal trees, for reasons that 
will be detailed elsewhere (Johnson & Johnson, 
in prep.). In brief, in the n-dimensional lattice 


for preferred terminology) representing the 7 at- 
tributes used, the unions established at points 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL 71 


most distant from the origin (zero point for all 
co-ordinates) may channel the downward-de- 
veloping tree structure into paths that exclude 
the possibility of finding a shorter overall set of 
paths, such as could result (later in the procedure) 
from joining the taxa (including the generated 
hypothetical taxa) in a different order. So, by 


4 а 


g за g f 
additional equal or shorter ultimate trees may be 
ound by a catching-up process. Moreover, phy- 
lograms of greater than minimal length may be 
more believable on grounds external to the anal- 
ysis (i.e., more parsimonious in a broader frame- 
work), although they involve a higher degree of 
homoplasy (parallelism, or even convergence if 
the user fails to discriminate convergent сћаг- 
acters as “different” when scoring). 

To overcome this difficulty, the procedure al- 
lows also for supraminimal joining (and thus su- 
praminimal partial and eventual trees) in the 
computations, longer up to a fixed amount than 
the minimals (at each stage); the maximum value 
(P) of this extra length is preset as a user-deter- 
mined constant in the program. We find empir- 
ically, and can glimpse the foundations of 3 
mathematical demonstration, that the additional 
probability of finding shorter ultimate trees falls 
off very rapidly as the value of P increases. В 
CLAX analysis of Myrtales, with 19 taxa, Ps 
yielded some partial trees that caught up with 
minimals during the computation, but increasing 
the value to P = 2 generated no additional pe 
all competing minimal tree. At P — 2 we obtain 
one phylogram that returned to minimal length 
at a lower stage in the processing but aroa 
off to a supraminimal level again before “ШИ 
pletion. This parti tree corresponds WI 
CAMIN-SOKAL result mentioned at 2.3. 

Some supraminimal overall trees have ж 
worth considering in their own right. tee 
portant to recognize that marked ап 
topology, at any level, may characterize NO” 
competing minimals but also вир 
worthy of serious consideration as piss t 
hypotheses. Hence it should not be assume sal 
cladograms produced by methods with lim а 
and often non-minimal output poon d (a 
proximate 10 “most parsimonious rees, 
fortiori) to “true cladograms." 

Unlike those extreme Cladists wh 


e not only 


о divorce 


: in some 
f Many authors (e.g., Farris, 1970) designate shortest trees as “optimal;” this implies that they e p 
nse **best estimates" of the true phylogeny. We reject this implication: minimal, no more and no less, 
shortest trees are, in terms of the data and method used (including any user-set constraints). 


س 


~" 


1984] 


their approach from evolutionary consider- 
ations, we do suggest that the junctions (dichot- 
omous, trichotomous, or higher-order) may in 
acceptable trees represent an approximation to 
the relevant character-state sets of conceivable 
ancestors. If they merely represent some abstract 
set (see Hull, 1979; Mayr, 1981— but those au- 
thors report this notion, they do not espouse it), 
we cannot see that they are of any conceptual 
use to anyone. We do not, however, believe that 
it is valid to assign quantitative probability (per- 
haps more properly likelihood) values to such 
comparisons, nor can we see that assignment of 
numerical likelihood to character-state innova- 
tions (Felsenstein, 1981) is possible in any but a 
tiny minority of cases. 
Tha h d at 1 


d 4 h 


node of the tree are defined by their positions 
and by the character-state sets computed by the 
procedure. These sets should always be consid- 
ered, so far as possible, for acceptability by cri- 
teria external to the analytical procedure itself. 
We have attempted this in the Myrtales, and the 
intermediate ancestors considered plausible are 
discussed below (3.2:3:32 +. 3:29). 

_All CLAX computation for this study was car- 
ried out by hand, since the rather complex com- 
puter program in the language PASCAL (John- 
son & Johnson, in prep.), allowing supraminimals 
and user intervention at various points, was not 
complete at the time of writing. Results of ap- 
plying CLAX to the order Myrtales are given at 
3.2 (Figs. 3-7) 


. 


2.3 CAMIN-SOKAL METHOD 


Since it also assumes known polarity of char- 
acter-state changes, the algorithm of Camin and 
= (1965) may be compared with CLAX, 
‘hough it does not operate on the same principle. 
We used the CAMIN-SOKAL PARSIMONY 
ALGORITHM program of Felsenstein, part of 
E package for inferring phylogeny (Felsenstein, 

79, 1981). The single tree produced for Myr- 
= was one step longer than the shortest CLAX 
esults. This tree was, in fact, identical with one 
of the CLAX supraminimals (2.2). Thus this ap- 
Proach can yield a result included among those 
given by СІ АХ but is much less satisfactory in 
101 allowing for the multiplicity of competing 
rees. Moreover, it does not possess a systematic 
Procedure designed to give a high probability of 
capturing no-reversal minimals 


os Phylogram obtained is discussed below 


JOHNSON & BRIGGS—PHYLOGENETIC ANALYSIS 


703 


2.4 MINIMAL-LENGTH METHODS ALLOWING 
CHARACTER-STATE REVERSALS 


The results reported in this section were ob- 
tained from an earlier version of the data matrix 
lacking certain embryological characters (76 and 
77) included in Table 1. They have not been re- 
computed since we have rejected these methods 
for reasons that would not be affected by includ- 
ing the additional characters. The lengths of trees 
given are comparable with each other but would 
need adjustment for comparison with Figures 3, 
4, and 5. From inspection, it appears that the 
range of topologies would not be much affected 
and the lengths would increase by about five units. 
Figure 1, as presented, has been adjusted so that 
it is directly comparable with the CLAX phy- 
lograms. 

2.4.1 CLAXMIN. For comparison, we have 
processed the Myrtales data (again by hand, but 
taking some short cuts) by CLAXMIN. This al- 
lows partially or completely unrestrained rever- 
sal of character-state polarity both initially and 
internally. It achieves this by minimization of 

e whole data matrix, in effect rescoring char- 
acters (except any predetermined by the user as 
non-reversible) by assuming an **original" state 
such that each column-total is minimized. This 
replaces the overall origin (**ancestor"), on which 
the tree is to converge downwards, with what 
might be called a quasi-centroid in the lattice 
(“Manhattan”) metric with respect to the array 
of points representing the taxa in the n-dimen- 
sional character space. (By the nature of the met- 
ric and the existence only of points with integral 
or a limited set of fractional co-ordinates, such 
a quasi-centroid is not necessarily unique). Ex- 
cept in the no-restraint case, this is modified for 
the “reserved” characters in which reversal is not 
permitted; for these the original zero co-ordinate 
is retained in the dimension concerned. All equal 
emporary minimal, or allowed supraminimal, 
alternatives are held for later processing. 

Setting the origin at a lattice centroid will in 
general decrease tree length but will not guar- 
antee a shortest branching path convergent on 
the origin. The constellation of points may be 
such that /ocal reversals of direction will yield 


c 


the taxa and their differential characters on each 
forked-off portion of the tree, working upwards 


704 


fL 1 (NH \ ^ a s 4 11 а Ms Read +1 + 


satisfy a pre-set Р level (see 2.2), meanwhile соп- 
tinually readjusting the temporary new origin. 
This in effect seeks the local quasi-centroids for 
all parts of the trees but does not necessarily 
accept them since shorter overall trees may result 
from not doing so. Any tree or partial tree that 
exceeds the pre-set P level is discarded (note that 
if P is set at zero or too low, some eventual 
minimals are likely to be lost). The procedure is 


through fully, it should yield all minimals pro- 
vided that P is set high enough. For obvious 
combinatorial reasons, however, the computa- 
tional load will increase rapidly as the data-set 
grows, and may become impractically high. 

When, and only when, character-state reversal 
is completely unrestrained, each tree may be 
treated as undirected, i.e., as what Farris (1970) 
calls a network (wrongly, as pointed out by Rohlf 
& Sokal, 1981). These graphs may then be re- 
rooted at any chosen point to form directed trees, 
which are of equal length but involve different 
initial character-states. 

For such attachment of the root point, one 
must remember that we adopt the convention of 
writing the character-state innovations on each 
internode of a tree in the numerical order of their 
listing in the data matrix; nevertheless they can 
be rearranged in any order within any internode. 
We have attached roots in such a way as to min- 
imize the number of reversals from the “апсеѕ- 
tral” state as originally assumed in the matrix, 


ging y on each portion 
of the internode intercepted by the attachment. 
Such minimization of change from the initial 
assumptions is, of course, not obligatory, and a 
vast number of directed trees may be consistent 
with any undirected-tree graph—many or even 
all of them will of course represent absurd phy- 
logenetic hypotheses. 

The initial result of CLAXMIN on Myrtales 
data yielded no less than 64 trees of length 135 
(without the ancestor; equivalent to 142 if the 
stalk to the originally assumed ancestral state is 
included). 

2.4.2 WAGNER-78. For further compari- 
son we used the more conventionally cladistic 
and currently popular WAGNER-78 program of 
Farris. This is not fully documented in any pub- 
lication by its author, or in the program in its 
available form, but rests on the foundation ex- 
pounded by Farris (1970) and discussed by Jen- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


sen (1981). It is, we believe, an unacceptable 
method for all of the reasons given above (2.2), 
but especially because of point (5). Even if that 
is not considered relevant, the usual operation 
of WAGNER-78 results in failures on points (1) 
and (2). Jensen (1981) correctly points out the 
danger of relying on Farris’s WAGNER proce- 
dure for reasons (1), (2), and (4). The reason for 
failure on (1) is that channeling very often pre- 
cludes finding a minimum tree, even after the 
so-called optimizing procedure of the method is 
applied. Essentially the problem is similar to the 
one CLAX is designed to overcome (2.2), though 
the path-finding procedure and assumptions are 
different. It is a fundamental fault in WAGNER- 
78 and its predecessors. 

We applied the method both including and 
excluding the ancestor implied by the original 
scoring (treating this as another taxon repre- 
sented by a row of zeros in the data matrix). We 
used two different arrangements of the family 
sequence in the matrix in the without-ancestor 
case and five in the with-ancestor case. As Jensen 
(1981) points out, such rearrangements result in 
different seq of processing by the program: 
As with the CLAXMIN Myrtales results, we have 
examined those from WAGNER-78, mostly af- 
ter setting them out fully in a form comparable 
with the CLAX phylograms presented herein: 
They are not illustrated, but are all topologically 
different from the CLAXMIN trees and from 
each other, and differ also in numbers of reversals 
of direction in character-state changes (using ye 
attachment points as indicated above). WAO- 
NER-78 trees obtained had lengths of 138 : 
processed without ancestor, and 143, 144, pe 
145 with ancestor (equivalent to a range ве 
137 to 139 with the ancestor-stalk remov 


Characteristic examples of earlier CAE E 


the tree shown in Figure 1, or its variants, 243. 
by later application of CLAXMIN (see 243. 
although certain groups are robust (sce i 
3.2.6). Being in fact supraminimal, these ens 
are not illustrated. The aes ore 
Figure 1 does in fact have 18 inte 

њиве one multiple reversal (character 75, 
the Combretaceous stem). 

It will be seen that these ap | 
МЕЕ-78 failed to yield minimal trees at а", 
the results implied more character-sta 
than in shorter trees obtained by C 


plications of WAG- 


| 


— m 7 


— HH da  —— — MÀ 


1984] 


Moreover, they tended to give “chained” trees, 
with most taxa coming off one by one. We woul 
surmise that the frequency of such chained clado- 
grams in cladistic studies in recent literature is 
partly an artificial consequence of the use of Far- 
ris’s program. 

2.4.3 Other minimal methods and compari- 
sons. D. H. Colless (pers. comm.) has devel- 
oped two programs, SWAG and RWAG, that 
generate and compare large numbers of Wagner- 
type trees. Runs of our Myrtales data by SWAG 
yielded (without ancestor) two trees of length 135 
and (with ancestor) six trees of length 143. None 
was the same as either those obtained by WAG- 
NER-78 or the initial 64 trees of length 135 ob- 
tained by CLAXMIN as hand-computed. Sur- 
prisingly, RWAG, out of 1,000 trees, produced 
one of shorter length (134). 

Subsequent hand-reworking by an extended 
version of our original CLAXMIN yielded the 
same tree as the shortest RWAG tree, together 
with variations that in combination amount to 
30 or more different trees also of length 134! 
These had been missed because, to reduce com- 
putation in hand-working the data, insufficient 
Supraminimal partial trees had been considered. 
Some of these trees differ in topology, others only 
in length of internodes. We do not count the huge 
number of variants obtained by changing the root 
Point. One version (topologically different from 


; п of his 
н PARSIMONY ALGORITHM рго- 
м a tree of length 134, different in topology 

om any of the other clad id а 
Placing the Combret ш те 
= the Myrtacean line and the remainder 
= ч families. We did not obtain this tree from 
Sel and-working of CLAXMIN, but believe that 
А пе obtained by а complete computerized 
ме ‘cation of this method. The program does 
ni indicate the character-state changes but we 
ulis Worked these out from the matrix to fit the 
the T. process of considerable difficulty since 
of Ar aig gives no information on the lengths 

lernodes and the positions of reversals. 
lt is interesting that, from this limited sample, 


qu 
ACY 


JOHNSON & BRIGGS— PHYLOGENETIC ANALYSIS 


705 


the Felsenstein program for the Wagner proce- 
dure seems to have been far more efficient than 
WAGNER-78. Not only was an apparently min- 
imal tree produced from a single run (in contrast 
to longer trees from Farris’s WAGNER-78 and 
a single tree of similar length out of 2,000 pro- 
duced by runs of Colless’s SWAG and RWAG), 
but both chaining and internal character-state 
reversals were less than in all WAGNER-78 re- 
sults. This surprising result may be fortuitous, 
since, in analyses of Rutaceae tribe Boronieae (J. 
A. Armstrong, pers. comm.), the tree resulting 
from a single run of this Felsenstein procedure 
was longer than any of the trees of rather widely 
ranging length produced by WAGNER-78. 

All of this heightens our confidence in CLA X- 
MIN, especially against WAGNER-78 but also 
as against SWAG and RWAG, as a method of 
seeking unrestrained minimals. It emphatically 
underlines Jensen's warnings against accepting 
any single result of an application of such a pro- 
cedure as WAGNER-78 as a basis for phyloge- 
netic conclusions. The same applies, in part, to 
Felsenstein s WAGNER PARSIMONY AL- 
GORITHM, since it produces a single result 
without any warning that this is far from unique. 

However, we believe that unrestrained CLA X- 
MIN results are also unacceptable, because they 

An и а о. 1s. We 


would warn both phylogenists and formal tax- 
onomists against all such unrestrained-reversal 
approaches, which are insidiously misleading. 

In essence, CLAX-type procedures, with more- 
or-less set polarity of character-state change, treat 
homoplasy (repeated innovation of the “same 
or a similar character-state) as being more likely 
overall than evolutionary reversion. Unre- 
strained CLAXMIN, WAGNER-78, WAGNER 
PARSIMONY ALGORITHM, SWAG, and 
RWAG treat overall shortness of the tree as over- 
riding any objection to reversion. WAGNER-78 
seems to be particularly prone to yield multiple- 
reversal trees. 

A few groupings in the Myrtales are robust 
under all analyses and the phylograms generated 
by CLAX and CLAXMIN show considerable 
congruence (see 3.2.6). For the same data, these 
groupings would probably tend to show up sim- 
ilarly (though subject to confounding by counting 
symplesiomorphous **matches"), not only in any 
reasonable (which may not mean any) phenetic 
analysis, but also in an "intuitive" analysis. This 
merely goes to show that a very strong and dis- 
tinctive signal gets through a lot of noise! 


90L 


МЯачуо TVOINV.LOS ІҸПОЅЅІИ JHL ЧО STVNNV 


11 L= 139 (internal) 


IL 10A] 


= 


— 


- 


~ 3" 


Пи 


1984] 


We use the term “reversion” to indicate ап 
actual evolutionary change back to a previous 
condition. This is in contrast to “reversal” which 
refers merely to a formal change of sign in the 
trees generated. It has been put to us (Vicki Funk, 

comm.) that many reversals can be inter- 
preted as instances of neoteny, i.e., a later de- 
velopment in ontogeny may fail to occur. We 
would add that there are two aspects in plants: 
(1) such failure ofa stage in ontogeny ofthe whole 
plant (say retention of a juvenile leaf form or 
phyllotaxy into a reproductive phase; this x me 


ure of a stage i in organogeny (say in nn 
of a style). 

The expression of the character-state con- 
cerned is in both of these cases taken to have 
occurred regularly in ancestors but the devel- 
opment is suppressed or not realized (by any of 
a variety of mechanisms) in the taxon under con- 
sideration. 

Naturally we are on the watch for neoteny of 
either of these kinds and we agree that neotenic 
loss (just as with loss by conversion to another 
State) is itself an apomorphy. Funk suggests that 
because neoteny is the loss of a character [-state] 
We are left with congruence (agreement with oth- 
er characters) as “the only way we have of testing 
whether or not the absence of a character [-state] 
is a real absence (in the sense that it has never 
existed) and therefore plesiomorphic, or "a 
or reversal and therefore apomorphid.” Congru- 
ence tests of the kind suggested by Funk have 
been done (3.2.6, Figs. 6, 7) but do not appear 
lo bear Particularly on neoteny or the assessment 
of homology. 

Neoteny may be suspected, not on the basis 
of congruence between different cladograms, but 
On the basis of "agreement with other characters” 
аз stated above. The agreement of characters is 
indeed expressed in the shortness of trees when 


JOHNSON & BRIGGS— PHYLOGENETIC ANALYSIS 


707 


change of sign (unrestrained or somewhat re- 


appeals to parsimony, but excludes those aspects 
of parsimony external to the immediate scope of 
the analysis. 

It is surely not an authoritarian “‘prior-knowl- 
edge" approach to consider that one can some- 
Ed 41 221 ае. | ЛЕ | x + 


or otherwise) on the basis of information and 
experience that are not formally expressed in the 
data set used in tree-generation. Some combi- 
nations of attributes will work biologically either 
in relation to the external environment or to the 


syndrome depen 


ds. We have discussed this brief- 
ly in relation to infl in Myrtales (Brigg: 


versal (neotenous or *real"), and have indeed 
considered possible reversals in this way in the 
present study. A few are discussed in the text. 
To take one or two particular examples, Figure 
1 would require loss of leaf teeth to be followe 
by regaining of fully organized teeth of essentially 
rosoid form, reversion from a valvate to an im- 
bricate calyx aestivation and loss of the special- 
ized condition of fibrous seed exotegmen fol- 
lowed by its reappearance. Perhaps none of these 
is impossible but there seems no reason to prefer 
such hypotheses, with all that they imply devel- 
opmentally and adaptively, over repeated in- 


мн ы с 

~ 

i FIGURE 1, A phylogram generated by CLAXMIN; not accepted as the basis of our phylogenetic hypothese: 

y Figs. 3 and » ма length = 139; length with ba basal stalk = 149; (respective надан without characters 
some are 134 and 1 144). [TI th see text 


PSX “Ad 
Ivan " 
~ cement level is shown on the left. 


independent, involving combinations of memen in the regions ALZ-RHY- on) PNA and MRT-HTP- 


-state innovations are shown 
А”) is sho wn “= е superscripts 


direction 
"i fro om those in the ori 


ulated, as in the original sco 


iden by an ancestor of the group A' from an earlier ancestral condition (A) as 


708 


novation of various other character-states simply 
on the grounds of the shortness of the resulting 
tree. The trees are, in any case, necessarily in- 
complete and arbitrary to some degree in choice, 
matching, and scoring of characters (Johnson 
1969, 1970). The WAGNER-78 trees, as stated, 
involve more multiple reversals, and are not even 
minimal. 


3. PHYLOGENY OF MYRTALES 
3.1 THE DATA 


3.1.1 Thetaxa. The families included in this 
Study are those that formed the Myrtales and 
Lythrales of our previous account (Briggs & 
Johnson, 1979). Several families that have at 
times been placed in Myrtales by various authors 
were there considered to be of distant or doubtful 
affinity; our conclusions on their relevance to 
Myrtales are unchanged and are very similar to 
those of Dahlgren and Thorne (1984). Thyme- 
laeaceae are retained in Myrtales by Cronquist 
(1981, 1984), but would certainly separate below 
the “ancestral” base in our analysis. For the rea- 
sons given by Dahlgren and Thorne, we believe 
that the family’s affinities lie elsewhere. We can- 
not accept Elatinaceae as a member of Myrtales, 
despite some (not complete) embryological con- 
gruence of that family with the order (Tobe & 
Raven, 1983a). It would branch off below the 
ancestor in our phylograms by virtue of several 
characters, including the several-styled gynoe- 
cium. This is reinforced by the absence of in- 
traxylary phloem and vestured pits (Dahlgren & 
Thorne, 1984), which are fundamental charac- 
ters of Myrtales as here constituted. 

We withdraw our former suggestion of up- 
holding a distinct order Lythrales. The present 
Study supports the views of other authors (ëp. 
Schmid, 1980) in completely rejecting the Ly- 
thrales concept. It was based in part on the 
erroneous report of a tenuinucellate condition in 
so-called Lythrales (Corner, 1976), which is dis- 
cussed by Dahlgren and Thorne (1984). This error 
had been pointed out by Stafleu (1978) in a re- 
view that we overlooked; we erred also in not 
ourselves checking the standard embryological 
literature. In 1979 we also took into consider- 
ation seed-coat characters (see below), centrip- 
etal versus centrifugal development of the an- 
droecium, presence or absence of toothed leaves, 
and the chemical nature of seed reserves. 

We do not discount direction of androecial 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


development as a phylogenetic indicator as 
strongly as do Eyde (1975) and Schmid (1980), 
but now conclude, in agreement with Dahlgren 
and Thorne (1984), that polystemonous condi- 
tions are secondary in several distinct lines of 
the Myrtales and that the directions of stamen 
initiation in these are not significant for the oli- 


ge 
© 
РД 
[4"] 
3 
о 
5 
о 
= 
[^7] 
S 
2. 
QO 
ge 
Loe | 
[e] 
(= 
"3 
[^7] 
3 
+ 
m 
€ 
a 


to further studies by Hickey (1981), including 
the finding of cryptic teeth in some Lythraceae 
(e.g., Cuphea); these are in fact not difficult to 
observe once one knows about them. Our inter- 
pretation of the significance of leaf teeth and their 
loss is clear from our listing of characters and 
from the phylogenetic scenarios. The comments 
of Keating (1984) on leaf teeth in Onagraceae are 
also pertinent to the interpretation of this feature 
in Myrtales. 

We have now examined seeds of a scatter of 
Myrtaceae and, contrary to the impression given 
by the literature (Corner, 1976; Hegnauer, 1969), 
find oil (presumably fatty) to be the most fre- 
quent and widespread storage material (e.g. in 
species of Callistemon, Eucalyptus sensu stricto, 
the eucalypt segregates “Corymbia” and Sym- 
phyomyrtus, Fenzlia, Leptospermum, Lophos- 
temon, Psidium, and Rhodomyrtus). Two species 
of Austromyrtus differ: oil in A. tenuifolia (Sm) 
Burret, starch in A. bidwillii (Benth.) ee 
Starch was also found in species of Астепа per 
Syzygium and appears to be mostly a e gi 
feature in species with large storage cotyl a 
and cryptocotylar germination [cf. our earlier 
mark (Briggs & Johnson, 1979: 16 
starchy seeds of Trapa]. А 

ты онаа ае this analysis аге аай 
or *quasi-families." Wherever there seem 5 
be serious doubt about the placement a 
tinctiveness of a group we have treated 1t p 
rately; this does not imply any necessary " 
tance of family rank, and indeed we er 
sinking some commonly recognized "d p 
while elevating other groups not usually 
guished at family rank (see 3.3.2). _ 

Where brief reference to the taxa 15 П idi 
in the figures, we use the 3-letter app go 
(they are not acronyms as he states) : 
(1982). For groups not in his list we are! DU 
the following: Alzateaceae ALZ, Duabang RHY 


е 
Laguncularieae LAG, miye CMB | 


(which is 000 


4) on the 


is used for the tribe Combreteae 


1984] 


part of the traditional Combretaceae), MLS re- 
fers to Melastomataceae sensu stricto with Me- 
mecylaceae kept distinct, and SNN covers only 
the genus Sonneratia. 

3.1.2 The characters. The characters used in 
the phylogenetic analyses (Table 1) are those for 
which data are available to us and which present 
differences within the set of taxa. The state con- 
sidered ancestral within each taxon is scored; 
differences developed subsequently within the 
laxa are not relevant to comparisons between 
taxa. Whether conscious or unconscious, weight- 
ing of characters is inevitable. This is because (1) 
itis both theoretically and practically impossible 
to define, even in terms of the genetic code, such 
à concept as equivalent unit attributes (see John- 
son, 1969, 1970), and (2) "probability of evo- 
lutionary change" (a complex concept at best) is 
variable between as well as (temporally) within 
"characters" (serially transformable attribute 
sets), so that the methodological analyses of Fel- 
senstein (1981) serve more as warnings than as 
useful recipes. In some cases we have assigned 
two serial binary characters, because the change 
involved is clearly complex, even though only 
extreme conditions are present. These are shown 
by brackets in the score column of Table 1. One 
can argue ad infinitum on all such matters, and 
we have simply adopted what seemed to be rea- 
sonable weighting 

For ease of representation and because it is 


used but not presented here (e.g., programs de- 


hree states represented by the ordered pairs (0,0; 
1,0; 1,1). Ву changing the initial assumptions, 
any Опе of these states сап be taken as the starting 
Point and the sequence can be read forwards, 
backwards, or from the middle in two directions. 
However, since the st dered. one cannot 


$i z Do. 
'multaneously assume both extremes as initial 


hus the combination (0,1) is not admissible. 


codd partial reversal, —a and + b (i.e., middle 
with гы Primitive) or by complete reversal —a 
, 0, but +a with —b is inconsistent. 
Initial assumptions on the direction of char- 
ers are made on out-group comparison and 


JOHNSON & BRIGGS— PHYLOGENETIC ANALYSIS 


709 


, 


"general principles," which usually amount to 
much the same thing. Our interpretations and 


* a5. 1 


р р very generally with those 
of Dahlgren and Thorne (1984) and of van Vliet 
and Baas (1984), and will therefore not be jus- 
tified here, although our reasoning sometimes 
differs. In a few cases we have no strong convic- 
tion about the polarity and the CLAX analyses 
have been done with alternative assumptions; 
these are marked in Table 1. Some other meth- 
ods of analysis allow reversal of any character, 
and are rejected for that reason (see 2.4.3). 

The taxa often include more than one state of 
a character among their constituent members. 
Our character-state sets do not cover those in- 
ternal ranges, which are indicated broadly by 
Dahlgren and Thorne (1984). The state consid- 
ered to be ancestral within the group is the ap- 
propriate one for comparison with other taxa. 
This is not necessarily the commonest state with- 
in the group and may not even be present among 
living members; it may be a state that it is nec- 
essary to postulate in order to account for di- 
vergent conditions within the taxon (Johnson & 
Briggs, 1975: 95). A striking example is the pos- 
tulated superior ovary in the ancestor of Ona- 
graceae (see 3.3.2 and Eyde, 1981). Clearly such 
assignment of an ancestral condition creates dif- 
ficulties if character-state reversal is allowed in 


versal of polarity would not necessarily change 
the numerical score but would lead to different 
members of the taxon being considered as ex- 
emplifying the ancestral state. 
Within the Lythraceae, subsidiary colpi occur 
on the pollen grains of some genera. Our initial 
> ا‎ Ca P ars 


tUL 


scored 0 for characters 48 and 49. In phylograms 
B and C (3.2.4, 3.2.5) we invoke an alternative 
hypothesis that the first stage of this condition 
(character 48) was attained in forerunners of the 
Lythracean group, but was not primitively pres- 
ent in the Myrtales as a whole. It must therefore 
be scored as 1 for the Lythraceae and for the 
three allied taxa, with an additional (reversed) 
character (—48) scored as 0 for (ancestral) Ly- 
thraceae but as 1 (representing loss of incipient 
subsidiary colpi) for Duabanga, Sonneratia, and 
Punica, this appearing as a synapomorphy on 


\ 


710 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


о NO а s 


(Мог. 71 


TABLE 1. Characters used in phylogenetic analysis of Myrtales. P 
1. Herbaceous habit 
2. Aquatic herbs 
3: уема aggregation 
4. j pits (cl 
_ tracheids to libriform fibers) 
5. 
tracheids to libriform fibers) 
6. Loss of apotracheal parenchyma 
7. Crystalliferous septate fibers 
8. retory cavities (oil glands containing 
terpenoids) 
9. Secretory cavities (oil glands containing 
terpenoids) 
10. Loss of trilacunar nodes 
11. Loss of trilacunar nodes 
12. "Myrtaceous" hair-type 
13. "Psiloxylon-type" riesce 
(2-armed, thin-walled) 
14. Nescit ai hair-type 
15. Revolute dom 
16. Fixation of anm phyllotaxy 
17. Fixation of spiral phyllotaxy 
18. Loss of leaf teeth 
19. Loss of leaf teeth 
20. Leaf teeth “trapaceous” (bifid) 
21. Stomate type 
22. Well-defined blastotelic? (anauxotelic) inflo- 
resce 
23. Well-defined blastotelic* (anauxotelic) inflo- 
rescence 
24. о нен о to axillary monad on 
uxotelic* 
25. big of пи ђе (bracteoles) in inflorescence 
26. Increase in floral mery 
27. Reduction of floral mery 
28. Reduction of floral mery 


mM 
w N 
ом 


34. 
35. 
36. 
31 


Loss of calyx imbrication 
Loss of calyx imbrication 
Loss of petals 


Petals small and thick (“oliniaceous”) 
Petals hooded (Rhynchocalyx-type) 


Staminal insertion 
Staminal insertion 


Stamens “ob” 


Obhaplostemony 


0 = woody; 1 = herbaceous 


0 = not aquatic herb 


; 1 = aquatic herb 


= mostly solitary; 1 = mostly grouped 


0 = bordered; 1 = reduced at least to intermediate 


state 
0 = bordered or intermediate; 1 = simple 


0 = present; 1 = absent or scanty 


0 = absent; 1 = present 
0 = absent; 1 = present 


0 = absent; 1 = present 


0 = trilacunar (3 gaps, 3 traces); 1 = at least some 
uction> 


0 = trilacunar or intermediate; 1 = unilacunar 
(1 gap, 1 trace) 
0 = not **myrtaceous" type; 1 = present 


0 = absent; 1 = present 


0 = absent; 1 = present 


exible*; 1 = spiral 
0 = керур ae 1 = teeth reduced at least to 


Qu dh; oos teeth or vestiges; 1 — teeth absent 
0 = teeth simple (or lost); 1 = teeth bifid 


anomocytic; 1 = paracytic 
0 = anthotelic; 1 = blastotelic (anauxotelic) 


0 = anthotelic; 1 = blastotelic (anauxotelic) 


0 = not reduced in this way; 1 = reduced 


0 = prophylls present; 1 = abse 
0 


= mery not regularly Медун 1 = regularly 


>5- 


merous 


0 = not reduced; 1 = reduced at least to flexible 
4-5 


0 = not турй or flexible 4—5; 1 = 


not or mdr поа 


<5-m 
0 = тое 1 = 
0 = some degree of imbrication 
0 = petals pre 1 = petal 


0 = petals рак » | = petals hooded íi 
0 — stamens = below hypanthium* rim; 


below 


0=at c some stamens below rim; 1 = 


stamens on rim 
0 = not “ob” (i.e., diplostemonous ог ћар! 


; 1 = stame: 
its د‎ 
0 = not pe ino 


| 
ous 


1 


not all 


all 


ns obdiplostemonous OF 


obhaplostemono! 


1984] 


TABLE 1. 


Continued. 


JOHNSON & BRIGGS— PHYLOGENETIC ANALYSIS 


| 


à 


38. Haplostemony 

39. Loss of stamen inflexion 

40. Stamen proliferation (centripetal) in bundles 
41. Stamen proliferation (centripetal) in bundles 


42. Stamen amid рио 

43. Reduction of sta men 

44. Presence of die кш 

45. Enlargement of terpenoid-containing connec- 
tive gland (“‘myrtaceous”’ type) 

46. Pollen syncolporate 

47. Pollen syncolporate 

Subsidiary colpi on pollen? 

49. Subsidiary colpi on pollen* 


50. Pollen + oblate? 

51. Pollen with viscin threads 

52. Pollen with “onagraceous” ехіпе 

53. Epigyny (fusion of ovary with hypanthium) 
54. Epigyny (fusion of ovary with hypanthium) 
55. Epigyny mus of ovary with hypanthium) 
56. Ovary stipita 

57. Reduction im cn number 


58. Reduction of carpel number 

59. Ovary multicarpellate but unilocular (“сот- 
bretaceous”’) 

60. Ovary multicarpellate but unilocular (“сот- 
bretaceous") 

61. Carpels antepetalous 

62. Style reduction 


63. Style reduction 
64. Exaggerated stigmatic lobing 
65. Reduction in stigmatic lobing 


66. Style base not sunken?» 
67. Style base not sunken? 
Very early loss of endosperm 
69 Oenothera-type embryo sac 
70 Oenothera-type embryo sac 
41. 
12. 
A eo ime 

4. Outer пир multiplicative 
75. Fibrous seed e otegmen 

6. Loss of fibrous. development of anther 


endothec 
77. Anther endothecium ephemeral 


* Brac 


0 = not haplostemonous; 1 = haplostemonous 
0 = inflexed; 1 = straight 

0 = absent; 1 = present 

0 = absent; | = present 


0 = absent; 1 = present 

0 = not pes 1 = ае 

0 = absent; 1 = 

0= RC Med or Betis |. = well developed 


0 = not syncolporate; 1 = syncolporate 
0 = not i 1 = syncolporate 
0 = absent; 1 = present 
0 = absent, Sid developed or only at one pole; 
1 = well developed 
0 = prolate or cage ai 1 = +oblate 
bud = — quond ] = present 
:1= e 
0- dun ctiam 1 = at least slightly fused 
0 = free or slight fusion; 1 = considerable fusion 
0 = not complete epigyny; 1 = complete epigyny 
0 = sessile; 1 = stipitate 
0 = isomerous with perianth; 1 = reduced to 4 or 
3 or fewer 
0 = 3 or more carpels; 1 = reduced to 2 carpels 
0 = condition absent; 1 = present 


0 = condition absent; 1 = present 


talous 
little or no 


0 = antesepalous; 1 = antepe 

0 = long or ERN length; 1 — 
elongatio 

0 = at least some ne elongation; 1 = not at all 

elongated (stigma sessile) 

0 = lobing or division no more than moderate; 1 = 
pronounced lobing 

0 = lobing or division at least moderate; 1 = 
very little or no lobing 

0 = sunken; 1 = not sun 


resen lost 
0 = not Oenothera-type; 1 = Oenothera-type 
0 = not Oenothera-type; 1 = Oenothera-type 
0 = not Penaea-type; 1 = Penaea-type 
0 = not Penaea-type; 1 = Penaea-type 
0= ; 1 = one redu 
0 = ои е = к 
0 = absent; 1 = 
0 = present; 1 = деен 


0 = persistent; 1 = ephemeral 


kets as 
: * For explanation see 
Potentially schen аи 


keke or ОРА (e.g. 8, 9) characters (see text). 


712 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


TABLE 2. Data matrix (taxa and characters) used in analysis of Myrtales. Character-states are defined in 


Table 1. 
س ہے ر‎ 
1 48 °6 8 9 10 11 142 13.14: eee 
Myrtaceae МЕТ 0 лт 0. 9 1 1 1 1 1 0 0 0 0 
Heteropyxida- 
HTP 0-0 0 0 U 1 0 1 | 1 1 1 0.0 | | 
Psiloxylaceae PSX О I uU лу p 1 1 1 1 1 1 1 0 9 џ | 
Репаеа PNA, 0 0 0 00 1 0 соо 1 I 0: о n. Т. 
Alzateaceae ALZ 0 "0 1 1 1 1 о 0 0 D 0 0 «о UM um 
Oliniaceae OLI 0 0 roo o 1 KETE 0 1 I 0 0 о. | 
Rhynchocalyca- 
ceae ки о о T? FI 1 1 0 O0 |! 1 0 TOM н 
Punicaceae PUN о 3954 = gg: | 1 B о 1| T 907307020 | Te 
Sonneratia SNN 9 1 0:79 ык 0 BO 1 ад а ОВО e 
Duabanga DUA 0 1 1 1 0 0. өө 1 I 0 0 30 у T 
Lythraceae YT 0:990 1 дно) 02 9 99 0 1 1 ооо FÉ 
Strephonema STH 07: 0: ооо *Q 0. Q9. 9g 1 155-0: 909931 08 0 
Combrete. MB 0 "0 0 ry: 70) 0 0 0 1 1 о она dob 
ропсмшнеће EAG О 0 0 0 0 0 0 D 0 1 4 оро 0:3 
Crypteronia- 0 
ceae PL 0 142 09.09. Q цу 0 90 Qe у D : : i 
Memecylaceae MMC 0 О: rd 0 Gee 
Melastomata- 
ceae sensu 
F0 
stricto ns 0 0 FEF 45 Q- Q Q- 0 O0 1 0^ O а. : 
Onagraceae ONA 0- O0 HG 50 0.0. D го БИ огы 
Trapaceae IRA 1! 1 1? 000 0 1 1 0 0 LIV 


the common stem of those taxa in the phylo- 


ams. 

Our concept of the primitive states will be bet- 
ter understood by reference to 3.2.2, where a 
postulated ancestor of the order is described. 

We are interested not only in branching se- 
quence but also in some indication, however 
rough, of the differences accumulated along 
branches, i.e., in patristic change (cf. Mayr, 1981). 
Each terminal taxon is simply a point at which 
the tree is truncated. It could be extended into 
further branches by considering the constituent 
members of the taxa (which would then present 
many more autapomorphies, synapomorphies, 


terest in assessing the degrees of divergence, and 
ultimately perhaps the assignment of taxonomic 
rank (for which the use of such a criterion lies 
outside Hennigian cladistics in the strictest sense, 
where only branching sequence is significant). 
Accordingly, we include a number of characters 
for which the presumed apomorphous state oc- 


curs in only one terminal taxon (aute pomo 
Since these do not affect the hoc dd 
who does not like them can simply st 


Notwithstanding claims to the eem he 
procedure can really “таке allowance d nich 
ing data; CLAX requires a numerical eu ks 
may be zero, for every character for d ps 
A few characters are not recorded for pled 
and some taxa are not sufficiently well sam per 
for their most primitive character-state (0 " 
ent assumptions of polarity) to be Re 
reasonable certainty. Extrapolation has M 
necessary; for example the non-woody 
ceae have been scored similarly to Оп 


Baas (pers. comm.), while stating that rimitivê 
nodes are generally regarded as more к flexi- 
points out that there can be considera and be 
bility within genera in some families, 


диви 


1984] 


JOHNSON & BRIGGS—PHYLOGENETIC ANALYSIS 


713 


TABLE 2. Continued. (Table 2 continues оп pp. 714 апа 715.) 


ы Ер 
29 30: SL 32 33 34. 35. 36. 37 38 39 


[SE 00-9 d 0 0 0 0 D 0 о 8 | 1 1 0 O 0 
И 0 000 0 0 о 0.0.0 0G 0 8 о Ij J | Q0 0.4 
Hd бо + 00 9 O OC €: 0 ке со с L 1:0 O 01 
HEN D о о 9 о о: 4 1 к мн TOOT 1 t 10.0.0 
Hu 5 o 0o Db à ог о 0 Bà B L| D 8 је Lb t 1.0.90 
НО nO 5 Xx O 0:00 От OO b 1з о J^ O 1 153 1 0.0 
FS о 0 0 б те O0 уу 1| се 5» | 1] + к TT OO 
HUM Оо о об о о се wi. wo 5 Lr о а о 0 9 
E n 0 D бо o о о о LP boo b 5551 ) о.о Q0 
МО oue OO о о 0 h LI 5 O 6 | је 0 0.0 
HON M € бо боб o o o» à кс 0 о оо оо оо 
HEN D do 4o 1o бу 0 05 1) Ww D 9 b 0 о [| 0! 0 0.90 
Hg 0 OF 1 ле 0o 1» 0o w о p», 1 0 5 6074 OTE 0 0 O 
мл wu 1; л о n oO о о о ^ 0 5 50 1 5 1 о о à 
[ES о |: | о 5 ов о D | P O P TT 1.5.8 
m D О O 0 0 90 I 0 0. o 1 0 0 
INS о ооо ос 8 0) 0 | |) 60 оро о | | ооо 0 
0M O 0:0 озу бе OC 1 б b & 0o 0 к 1 0 O O.4A 
JU i о: о бе мн о м не = ___ 190 01.1 


lieves that the trilacunar nodes of Alzatea cannot 
be used in strong support of its isolated position. 
Intermediate conditions are described by van 
Vliet and Baas (1975) in the three genera of Cryp- 
leroniaceae sensu stricto and in a number of Me- 
lastomataceae (‘“Melastomatoideae’’). These have 
three leaf traces, the lateral traces of the pairs of 
leaves sharing common gaps or alternatively 
‘imply girdling the node, which then has only 
че gaps corresponding to the median traces. This 
Condition is possible only with opposite phyl- 
Otaxy. Since the general patterns in the order 
Suggest that early } d spiral phyl 
lotaxy at some stage in their individual life his- 
lories (see 3.2.2 " Protomyrtalis"), the girdling or 
‘ommon-gap condition could scarcely be plesio- 
morphous for the order. We therefore do not 
Pe reversal of characters 10 and 11 (such as 
waa in the CLAXMIN and WAGNER-78 
cunar cf. Fig. 1), even though completely trila- 
is nodes are recorded only in Alzatea. This 
of а! implies several independent losses 
the trilacunar condition, either to the “іпіег- 


mediate stage” or to completely unilacunar states. 
Since the second stage of this has pretty obvious- 
ly occurred in Melastomataceae, there seems no 
great difficulty in envisaging multiple acquisition 
of the unilacunar condition. Alternatively, tri- 
lacunar nodes in A/zatea may be a neotenous or 


ilies of the Rosiflorae, an out-group basis for our 
assumption. 

16, 17. Phyllotaxy. Although it is conceivable 
that opposite phyllotaxy was primitive for the 
order or its predecessors, we believe that actual 
patterns indicate that ontogenetic change in this 
character was the primitive condition for both 
the Myrtales and Myrtaceae, with fixation to 
either opposite or spiral phyllotaxy in some fam- 
ilies or parts of the families (see 4.1.3). Both 
opposite and disperse (spiral) conditions occur 
among the Rosiflorae. Lythraceae are taken here 
to have attained the fixed opposite condition; 


714 


TABLE 2. Continued. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


MS 
54 2 


Ag ај 42 41 44 45 465 47] 48 40 S30 51 55.33 
Myrtaceae MRT 1 1 0 0 1 1 1 0 0 1 0 1 0 00 
Heteropyxida- 
ceae HTP ог 0707 0 1 1 1 1 0“ 0 1 о 0- 0 0 DEM 
Psiloxylaceae PSX 0 0: Di | ] 9g 1 1 0 O t 0 0 2 MM Н 
епаеасеае РМА o: DS 0 1 0: 0 0. D 1 1 о 0. 0: 0 Оа : 
Alzateaceae ALZ 0 0 0 0 O O O O 0 o0 0 0 D D' MM : 
Oliniaceae OLI D O 0 1 Ü D O0 9 1 о 0. 0 0 po 
Rhynchocalyca- 
ceae RI 0 39 D o 0 0 CE D 1 1 0 0 8 0 ШОШ : 
Punicaceae ин 0 € | 09 O0 с о 0 OQ 0 0 о M MOM : Н 
Sonneratia SNN о 0^ 0 0: O0 0: O. OQ. ж O- 0: о D 15 p e 
Duabanga DUA 0 9 0 0 о O э ж 0 0 0 ^ D D e 
Lythraceae IYT 0 0 0. ж-о 0 о 0 O & o0 90 $$ M n 
Strephonema STH D O. D» 0 0 6 5 0 OQ. 0 0 0 M 3 a 
Combreteae CMB- D 0 0 5D е о 0. O 1 1 0. O QO 1 | 19 
Lagunculariesae LAG 0 0 0 0 0 0 оо 1 ] 0 0 о ин 
Crypteronia- 
ceae CPT 0: 0) 0" 0. 0. € 020 1 ic 0: O FE © : 
Memecylaceae MMC 0 0 0 ] 1 0 0 D l 
Melastomata- 
ceae sensu У 
ricto MS D о о p» 5 5» oO 5 ) Lp 90 5 M а : н н 
Onagraceae ONA 0 0. 0 OF: с 0 0 O0 O0. O | 1 15 i, 0—06 
Тгарасеае TRA 0 0 07 0 U U 0 2 80 9 нв II 


and C 


authors have stated that “alternate” arrangement 
Occurs in some genera, but we find this to be in 
fact disjunct-opposite (Briggs & Johnson, 1979) 
in Lagerstroemia and Lythrum, for example, not 
truly disperse (spiral). 

18-20. Leafteeth. Characters 18 and 19 apply 
to the fuchsioid teeth as found in various Ona- 
graceae and, in a reduced form, in some Lythra- 
ceae (3.2.3). Teeth of this kind are also inter- 
preted as forerunners of the specialized bifid teeth 
of Trapa (character 20) (Briggs & Johnson, 1979; 
Hickey, 1981). Unvascularized tooth-like “cilia” 
(marginal projections of the epidermis) found in 
ceae, such as Baeckea, are dif- 
ferent in nature. They are almost certainly sec- 
ondary developments, as are the variable teeth 
of some species of Sonerila (Melastomataceae). 
In the latter case, single vascular strands enter 
the teeth but these appear to have developed 
from the multicellular hairs characteristic of the 


advanced Myrta 


gans of this genus. 


as secon 


are not always strictly marginal, 
underlying vascular pattern from 
hair types (Dahlgren & Thorne, 19 
tures of Sonerila do not indicate any 
vergence from the rest of Melas 
out-group comparison with neighboring Ee 
therefore supports the interpretation of the 


ary. 

22, 23. Inflorescence. Inflorescences ! 
tales are discussed by Briggs and Johnson 
where the terminology used here 15 expl 
that paper we overlooked the pre 
phylls (**bracteoles") in Ludwigia of ei om 
ceae and in the tribe Laguncularieae они = 
bretaceae. Although the publish 
are not clear in this regard, we have 
these structures to be present also 1D : 
nema and in some members of the C 


а EM e LS 
sB 
a This score applies to some Lythraceae, others would be scored “1;” see text for relevance to phylogram 


84). The fea- 


early di- 


tomataceae, and 


n My 
(1979). 
In 


ed descr! 
ave now found 


n dd E 


| 


sence of PF , 


аван 


1984] 


TABLE 2. Continued. 


JOHNSON & BRIGGS— PHYLOGENETIC ANALYSIS 


TLS 


met esi e m 
602 03 04 65 0b 67 


63 б9 707 71 72; T$ 740 75. 76 TI 


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о-о о ~ 
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دت س س‎ o 
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келке су и 


=== O O O о س‎ 
oo of 2 ос = 
et о Oe. OI 
P m Oe © © © 
=> о Om oO о о о 
о © > ооо о 
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———————- 


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OOO Ooo о > 
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асеае sensu stricto. In the latter ару рго- 
Phyllar bracteoles occur in Axinandra an m 
Species only of Crypteronia. We have not sius 
pras in Dactylocladus. 

9, 30. Calyx inthrication: On general out- 
group comparison, we take imbricate aestivation 
Of the calyx as the original condition. We 
some of the families generally described as a 
ing valvate Bec to include some members 
that preserve a degree of imbrication. Cases are 

lg Strephonema, and the tribe La- 
&uncularieae of Combretaceae. 

‚ 35. Staminal insertion. We cannot form 
any definite opinion as to the polarity of change 
in this character. Developmental studies will 
Possibly shed some light upon it. We have re- 

verted to the term “hypanthium” rather than 
oe um” as used in Briggs and Johnson 
si ). The latter term is preferable in some ways, 
м eo may result from its continuing use 
quite different structure in the Cyperaceae, 


о 


in which it has priority of usage. Although “‘hy- 
" is etymologically misleading, its ap- 
plication seems now to be standardized. 

44. Connective gland. Glands on the connec- 
tive occur in some Melastomataceae and Me- 
mecylaceae but appear to be secondary acqui- 
sitions in these taxa. They do not appear to be 
of the same nature as the terpenoid-containing 
gland in the Myrtaceae, Heteropyxidaceae, and 
Psiloxylaceae. 

48-50. Subsidiary colpi and pollen shape. We 
have preferred the term “subsidiary colpi" to 
*pseudocolpi," following Muller (1981a), who 
gave an excellent discussion of the evolution and 
dynamics of pollen grains in relation to shape, 
colpi, and exine structure. From this, and from 
out-group comparisons, we conclude with him 
that the more or less prolate condition with rel- 
atively little exine thickening is primitive for the 
order. A complete reversion from well-devel- 
oped subsidiary colpi to their absence seems un- 


716 


likely, but reversion from an incipient or weakly 
developed condition to apparent absence is re- 
garded as a possible alternative (3.2.4). The effect 
of such an interpretation is mentioned under 
S45. 

66, 67. Style-base. We have assumed that the 
sunken style-base is plesiomorphous, perhaps as 
a relict state deriving from a former apocarpous 
condition with the styles more or less running 
down the adaxial edge of the carpels, as in some 
Rosales. However, if it is not primitive the to- 
pology of Figures 3 and 4 is not affected, although 
the characters 66 and 67 disappear from their 
present positions, while —67 and —66 appear on 
the stem leading to the Myrtacean group (if we 
assume that the condition is primitive within the 
latter); alternatively these characters disappear 
altogether (the sunken style-base being then con- 
sidered to have arisen independently in Psilox- 
ylaceae, Heteropyxidaceae, and within the Myr- 
taceae) or appear only on the possible 
Psiloxylaceae-Heteropyxidaceae stem. 

74, 75. Seed-coat structures. These are largely 
taken from Dahlgren and Thorne (1984), ignor- 
ing within-taxon (later) apomorphies. We have 
examined seeds of Rhynchocalyx and are in- 
debted to S. A. Graham (pers. comm.) for in- 
formation on Alzatea and confirmation of our 
observations on RAynchocalyx. Neither genus 
shows a fibrous exotegmen or a multiplicative 
outer integument. In both, the seed coat is very 
simple, of only two cell-layers, whereas a multi- 
layered seed coat is general in Lythraceae (Gra- 
ham, pers. comm.) 

76, 77. Embryological features. Information 
has been obtained from Tobe and Raven (pers. 
comm. and 1983a, 1983b, 1984a, 1984b). 

3.1.3 Chromosomal features. Karyological 
characters have not been used in the analyses, 
and chromosomal evolution will need to be con- 
sidered in relation to the various scenarios for 
the Myrtales and the different reliability of parts 


* We do not discuss in detail the supraminimal tree produced by both CLAX and the Felsenstein p 
based on the Camin and Sokal algorithm (see 2.3). Its terminal groupings, with comm A-SNN- 
G-CMB-STH-MMC, ALZ-RHY-PNA-OLI-CPT-MLS, DUA Cyr | 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


-5ТН and MMC join at level 5 with MRT-HTP-PS: 


(Мог. 71 


of these. Many details are still lacking. A base 
number of 12 seems quite likely, as suggested by 
Raven (1975), with dysploid reductions in var- 
ious lines and within several families; X = 11 is 
of frequent occurrence, but chiefly in what we 
would consider to be somewhat advanced mem- 


Some further support for a base number of 12 
comes from our finding of 2n = 24 in Psiloxylon 
(Fig. 2). [Psiloxyl iti (Hook. f.) Baill, 
cultivated Royal Botanic Gardens, Sydney, 
voucher Briggs 7233 (NSW); seed source: Le 
Grand Brülé, Réunion, Guého 14 June, 1979] 
This numbe 
Heteropyxis (Fernandes, 1971). 

uch a base number may, of course, itself be 
derived by reduction after tetraploidy, or by tet- 
raploidy after reduction from the often-suggested 
dicotyledonous base number of X = 7, but there 
is no particular evidence to support this. For 


Z 


descending dysploidy has happened frequently. 
His arguments rest on what he considers to be 
cytogenetically most likely, and are not absolute. 
Thus, in the light of correlations of chromosome 
number patterns and other features, we believe 
that polyploidy followed by decreasing dysploidy 
has in fact occurred in various orders and tam- 
ilies. For instance in the Proteaceae e : 
: : : a 
Briggs, 1975) James 5 contenu a es 


a very ип урой ee 
of the phylogenetic pattern in the family 


dicated by a mass of other evidence. 


3.2 THE HYPOTHESES : 
3.2.1 Competing hypotheses. Arising from 
our analyses, we discuss three phylograms ( 
including some minor variants) represe 
potheses as to the evolutionary relationships 
sequence of diversification. 


«m 
on stalks up to level 
б). MMC 
C and MLS attach at level 10 in this phy 


(characte 


characters being 10, 11, 18, 19, and 34). The 
29, 30, 66, 67). All of the character- 
see no reason 
Nevertheless, it does illustrate that 
stages. 


а multiple analysis of this kind points to uncertainty а 


c 
X (the commo 
el 4 (С да 


ашчет OI M and 
char states concerned are of multiple innovation in this and other үрен . 
10 regard this slightly longer phylogram as competing very seriously with those scussed 


di 
t the earlier ancestral 


r has previously been reported in | 
71 | 


| 


nting hy 


наска 


| 


1984] 


These аге founded respectively on: (1) our 
original scoring, i.e., our views of the likely prim- 
itive conditions, derived from internal and out- 


group comparisons (3.2.2, Fig. 3) — phylogram А, 


(2)a variant of the above, allowing for an internal 
reversal; it is assumed that some degree of de- 
velopment of subsidiary colpi on the pollen grains 
is gained and subsequently lost (not illustrated) 
(3.2.4)—phylogram B, and (3) a further variant, 
with reversal of the character of subsidiary colpi 
as in (2) but making a different assumption as to 
the ancestral level of insertion of the stamens 
on the hypanthium (3.2.5, Figs. 4, 5)—phylo- 
gram C 


The character-state changes made in variants 
(2) and (3) result in shorter (“тоге parsimoni- 
ous”) trees. Moreover, these are characters in 
which it seems that reversal (in these cases not 
necessarily equivalent to actual evolutionary re- 
version) is not contra-indicated by structural im- 
possibility. All these phylograms, and their mi- 
nor variants as shown by alternatives on the 
diagrams, are conceivable sets of evolutionary 
relationships, unlike various phylograms dis- 
cussed and rejected above (2.4). 

To clothe the bones with some flesh, we pre- 


acters taken as ancestral within each of the taxa 
adopted here as families or quasi-families, that 
IS, each of the end-points of the phylograms. 
General conclusions will be discussed below, and 
the order of presentation of the phylograms and 
discussion does not necessarily imply an order 
of preference. 
ue fossil record of the Lythraceae has been 
== wed by Graham and Graham (1971), and 
р erous additional records have been cited by 
Yde (1972). Eyde and Morgan (1973) give a 
= in! of the record for Onagraceae. In 
ا‎ however, the paleobotanical record for 
Mow er 15 extremely scanty (Muller, 1981b). 
a Th distribution patterns and their impli- 
‘ons therefore form the basis of the historical 
ч овғоргарінс suggestions. The techniques of 
Ма Ie biogeography as fervently advocated 
ben Ў Cladists as Nelson апа Platnick (1981) 
iiis tef us to be too formalistic and, equally 
€ intly, subject to the same computational 
ми as discussed above (2.2, 2.4). None 
ess, we suspect that they would tend to in- 


JOHNSON & BRIGGS—PHYLOGENETIC ANALYSIS 


URE 2. Mitotic chromosomes of Psiloxylon 
mauritianum. 2n = 24. 


dicate a general pattern similar to that put for- 
ward below, though we are less dismissive than 
such authors of allegedly **untestable" dispersal 
hypotheses, less committed to their narrow view 
of acceptable scientific method, and much less 
convinced that allopatric speciation is a sufficient 
model upon which to base a rigid procedure. 
Moreover, we are conscious that fossils turn up 
in surprising places, and of the importance of 
extinction. 

3.2.2 "Protomyrtalis." Trees, evergreen, 
leptocaul, with sylleptic growth, of mesic habi- 
tats under equable climate. Bark of trunk and 
limbs probably with a tendency to shed in plates 
or strips. Without oil glands (secretory cavities) 
or laticifers; producing trihydroxylated flavo- 
5 ер ТУ Ноо 


» 


sand у: 
not producing iridoids or benzyl isoquinoline al- 
kaloids. Endotrophic mycorrhiza probably pres- 
ent. Vascular bundles of primary stems and main 
bundles of leaves bicollateral and hence with in- 
traxylary phloem in woody stems. Wood-ana- 
tomical characters as given by van Vliet and Baas 
(1984) for their *Protomyrtales." Sieve-tubes of 
the phloem with S-type (starch-containing) plas- 
tids, P-type plastids (with crystalline protein) ab- 
sent (Behnke, 1984). Hairs unicellular and un- 
branched, just possibly some multicellular 
uniseriate hairs present, glandular hairs absent. 
Stomates anomocytic. Nodes trilacunar or po- 
tentially able to revert to trilacunar condition 
(e.g., by neoteny?). Phyllotaxy probably varying 
during ontogeny (opposite-decussate > spiral — 
opposite?). Stipules present, small, perhaps with 
a tendency to become divided. Leaves simple, 
petiolate but not articulate or pulvinate, mod- 
erately large, dorsiventral, hypostomatic, with 
pinnate-reticulate and + brochidodromous ve- 


718 


nation, margins with modified rosoid (*fuch- 
51018") teeth. Inflorescence fundamentally an- 
thotelic (determinate), paniculate (sensu Troll, 
1964), but development of individual shoots 
flexible and inflorescence not sharply demarcat- 
od from the vegetative region (asi in ythe pprimitive 
by Briggs 
& J ohnson, 1979), prophylls | present on ultimate 
branches but metaxyphylls probably absent. 
Flowers with a distinct anthopodium [i.e., a ped- 
icel above any “bracteoles” (= prophylls) or oth- 
er “bracts” present], bisexual, pentacyclic, pen- 
tamerous or flexibly 4—6-merous, somewhat 
perigynous, neither very large nor very small, 


least not highly colored petals; these + spreading 
at anthesis, probably + obovate and with stipule- 
like outgrowths at the base. Androecium diplo- 
stemonous; stamens perhaps borne somewhat 
below the rim of the hypanthium, filaments per- 
haps incurved in the bud. Anthers versatile, dor- 
sifixed, introrse, connective narrow without a 


с 

what prolate, isopolar, 3-colporate and not syn- 
colpate, lacking subsidiary colpi, 2-nucleate when 
shed, exine thin and probably with a granular 
vinee layer (Gadek & Martin, 1982), not 
y ornamented, without viscin threads. No 
жый demarcated disk present but inner sur- 
face of hypanthium + nectariferous. Gynoecium 
fully superior (quite free from the hypanthium), 
isomerous with the perianth, syncarpous (not 
coenocarpous). Style simple, only moderately 
elongated, base possibly + sunken into top of 
ovary. Stigma probably of the Dry type, some- 
what lobed. Ovary narrowed at base but not stip- 
itate, gh пате and as many as the 
arpels rhaps for a com- 
pitum below the style- base. Plated axile, 
the placentas only moderately protruding and 
with axile vascular supply. Ovules several or nu- 
merous per carpel, anatropous or perhaps vary- 


pf ll 2 have greater validity than t 


p (us he evidence warrants, such comments are inserted 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


ing 10 | it 
to position on the placenta (as frequently; in living 
Myrtaceae), crassinucellate and bitegmic, all po- 


(Мог. 71 


| 


tentially fertile (no ovulodes); embryo. sac of | 


Fruit superior осоне capsule, probably 
rather pis walled. Seeds several or numerous in 
each loculus, — without. either. à die 
entiated fi 

integument; endosperm disappearing during de- 
velopment, very scanty or absent in ripe seeds, 
embryogeny of Onagrad type; suspensor short 
and small; embryo probably straight or slightly 


} 


curved, storing fatty oil and aleurone, starch ab | 


sent; cotyledons relatively thin. Germination 
phanerocotylar, cotyledons becoming herba- 
ceous. Chromosome number perhaps 1 = 12. 
3.2.3 Diversification and geographic Mer 
the implications of phylogram A. Am g the 


итча е тан of the ае cuan Rp | 


» somewhere in west 


| 


Оаа" is not truly redundant 4 
sometimes claimed, but the shorter form is used 
here.], two lines may have arisen (Fig. 3). Ове 
(A1) differs‘ from the ancestor (phylogram C) in 
complete loss of teeth on the leaf margins 


: for 
fixation of insertion on the hypanthium nm | 


at least one whorl of stamens (assuming that all 


an- | 
stamens were inserted below the rim in the 


cestral state). These characters marked hes 
that gave rise to the three Myrtacean 
and the large central group of the phy e " 

The other line (A2), which became establis : 
in west Gondwana, showed grouping of ke 
in the wood, and complete loss of trilacunar n 
(with = on the condition of one Ee 
one gap). Also, calyx aestivation became il 
pletely ые the style-base сате to је 
on the ovary rather than sunken, and a : 
exotegmen was developed in the seed coat. xi 
was the line eue to the Onagracean 
Lythracean familie 

ideo division (sequence of divisio 


w 


re rite ‘and the surviving lines may, 2$ 


, B, or C) and stem number. p 
ogram C at several important early divisions. Lest the first scenario 


at the main poi? 


on differ 


ay have followed closely upon | 


the line — 


1984] 


be only a sample of various lines most of which 
did not survive to the present. This separation 
marked the formation of the Myrtacean line (A3) 
which eventually, but not simultaneously, de- 
veloped a substantial group of distinctive char- 
acters. These include: secretory cavities contain- 
ing terpenoid substances in leaves, stems, and 
floral parts; loss of the trilacunar node; stan- 
dardization of the myrtaceous hair-type; com- 
plete fixation of staminal insertion on the hy- 
panthium rim; development of the connective 
gland; and shortening of the polar axis of the 
pollen grains to an oblate condition, with de- 
velopment of the syncolpate or parasyncolpate 
pollen-type and probably more elaborate thick- 
ening of the pollen exine. We cannot specify the 
likely region of occurrence of these plants within 
Gondwana, but perhaps it was at first still in the 
west. 

Diverging from the Myrtacean line (not ap- 
plicable in C) was a group (A4) marked by fewer 
character-state acquisitions; reduction of stig- 
matic lobing to very slight and loss of the sunken 
style-base condition, neither being unique to this 
group 


A further division followed, with the separa- 
поп of the ancestors of the Penaeacean and Me- 
lastomatacean families from the Combretacean 
phylad. The first of these assemblages (A5) was 
marked by the fixation of opposite phyllotaxy 
throughout ontogeny, partial loss of calyx im- 
brication, and fixation of staminal insertion on 
the hypanthium rim (character-state changes dif- 
fer in phylogram C). The second assemblage sep- 
arating at this stage (A6) is a strongly marked 
line giving rise to Combretaceae sensu lato, with 
Ils unilacunar single-trace nodes, a characteristic 
hair-type, well-defined blastotelic anauxotelic in- 

Orescences of generally racemose form (prob- 
ably by reduction of lateral uniflorescences to 
monads, accompanied by anauxotely of conflo- 
rescence axes derived from portion of seasonal 
&'Owth units) (see Briggs & Johnson, 1979), loss 
of anthopodium and adnation of bracteoles (flo- 
ral prophylls) to the hypanthium, a shift in the 
levels of insertion of stamens in the mature bud 
50 that the antepetalous whorl came to be in- 
*erted higher than the antesepalous stamens (ap- 
Parent obdiplostemony), partial “fusion” or con- 
ünuity [Sattler (1978) gives arguments for 
Preferring the latter term] of the gynoecium with 
the hypanthium (1.е., incomplete epigyny), de- 
velopment of a unilocular but still multicarpel- 


JOHNSON & BRIGGS—PHYLOGENETIC ANALYSIS 


719 


late ovary (i.e., loss of septa, with accompanying 
change in placentation), possibly a change to As- 
terad type embryogeny (Tobe & Raven, 1983a), 
and development of a fibrous exotegmen in the 
seed. The last-mentioned and fairly distinctive 
feature occurs also in the Lythraceae-Onagraceae 
group but, on the present hypothesis, would have 
been independently attained in the two cases. 
Not all the attributes indicated on this or on any 
other branch of the phylogram were necessarily 
acquired in a short period or in the order given; 
they do not appear to constitute such an obvious 
functional syndrome that one must believe that 
their acquisition was correlated as a marked 
"punctuation of equilibrium," and there may 
have been other divergences to now extinct lines 
along the way. 

Also early in the history of the order, the Ly- 
thracean group of families diverged from the pos- 
tulated common ancestor of Onagraceae and 
Trapaceae (a supraminimal alternative of C dif- 
fers). The Lythraceans (A7) were marked by 
another, independent, fixation of opposite phyl- 
lotaxy (see 3.1.2) and a reduction ofleaf toothing 
to a cryptic dentat diti ickey, 1981) still 
shown by the vascularization and by retention 
of the apical gland, as in modern CuphAea, re- 
duction to little or no stigmatic lobing, and mul- 
tiplication of the cell layers of the outer integu- 
ment of the seed (Dahlgren & Thorne, 1984). 


LK 


\ 


This 


(A8) leading to Onagraceae and Trapaceae, de- 
spite the great differences between those families. 
At this stage they were still woody plants. This 
is supported by the wood anatomy of arborescent 
and shrubby members of the Onagraceae, which 
gives no evidence of an earlier herbaceous con- 
dition (Carlquist, 1975); similarities between the 
herbaceous aquatic Trapaceae and some herba- 
A Y + А ge t | 
The suggested common stem would have been 
marked by reduction of the inflorescence to ax- 
illary monads on auxotelic axes (a character not 
shown elsewhere in the Myrtales except in in- 
dividual genera in some families, e.g., in some 
Myrtaceae), possibly some reduction of floral 
mery to a flexible condition of 4- or 5-membered 
perianth and androecial whorls, fixation of the 
staminal insertion on the hypanthium rim, loss 
of staminal inflexion in the bud, and a tendency 
for the pollen grains to become oblate. The sep- 
aration of Trapaceae and Onagraceae is dis- 
cussed at 3.3.2. 


OTL 


RHY 
274 49" TRA 
71 agwPNA OLI 
= TU 72' 62" CMB 
24 
4 PSX ALZ 26' | 71' 55" 30% STH 
ва, |63' |11" [49 Ба 29'* 29'" 
62” f62” |1о" 31“ 53У LAG 25'* 27 
62% 31” 7" 428" 32’ 55" 21^ 
58 ө, 
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39” "m 42' 
1 7" am 7'" 
l 
197 3У 
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The distribution of their descendants suggests 
that all the divergent groups of Myrtales up to 
this point may have occurred in the parts of the 
west-Gondwanan region that formed Africa and/ 
or South America. 

Within the Myrtacean line, this analysis throws 
no light on the sequence of divergence, and Fig- 
ure 3 shows two possibilities. The major descen- 
dant group is the family Myrtaceae, which ex- 
hibits much greater fundamental diversity in the 
east-Gondwanan region than in America or Af- 
rica. It is the only substantial Myrtalian group 
with this pattern. The unigeneric families Het- 


eropyxidaceae and Psiloxylaceae are today found - 


respectively in south-east Africa and in the Mas- 
carene Islands of the Indian Ocean. The latter 
are volcanic and apparently not original Gond- 
wanan fragments, so the distribution of Psilox- 
ylaceae is probably secondary as well as relict. 
The existence of these two groups and their def- 
inite relationship with Myrtaceae indicate that 
the ultimate origins of the Myrtacean line may 
well have been west-Gondwanan also (at least in 
the African portion of that region), although the 
Myrtaceae themselves probably underwent their 
primary diversification in the Australasian re- 
gion. At later stages the Myrtaceae extended to 
South and Central America but many major 
groups of the family, including some lines that 
= have diverged early, are absent from that 
i 
Since Heteropyxis and Psiloxylon are е 
with the subgroups of Myrtaceae in the analys 
of the latter, Figure 9 also bears on the аа 
of each of the alternative hypotheses. The а 
ditional characters used in that case viden 
tree that is one step shorter for the Heteropyxi- 
uu" Psiloxylaceae grouping than for a Het- 
bisce. eae-Myrtaceae grouping. Although not 
usive, this favors the phylogeny shown by 
Solid lines in Figure 
Returning to the diverdficlitiok of the central 
&'oup of families, the next division on this E 
-— Was between the Penaeacean and M 
atacean assemblages (with аса. 


ЕЛДЕ ооо маин 


JOHNSON & BRIGGS— PHYLOGENETIC ANALYSIS 


721 


aceae included with the former in the minimal 
but with the latter in a supraminimal), at the time 
all still perhaps in the west-Gondwanan re- 
gion. The first of these lines was marked by com- 


over, the fibrous thickening of the anther endo- 
thecium was lost, with complete collapse at the 
time of dehiscence as a further development 
(Tobe & Raven, 1984b). The further diversifi- 
cation of this phylad was marked in a line leading 
to A/zatea and Rhynchocalyx by specializations 
of wood anatomy (loss of apotracheal paren- 
chyma, vessel aggregation, loss of bordered pits), 
reduction in the number of carpels, and loss of 
participation of the outer integument in forma- 
tion of the micropyle of the ovules. The last fea- 
ture was reported by Tobe and Raven (1984a, 
1984b), together with other embryological re- 
semblances between these two genera. It is not 
included in Table 1 or our analyses. 

Alzatea alone within the order has (retains?) 
fully trilacunar nodes; it is also distinguished by 
loss of petals and reduction of the style, as well 
as by a disporic A//ium-type embryo-sac (Tobe 
& Raven, 1984b). The last feature is unique in 
the order and if included in the analyses would 
lengthen the A/zatea branch by one unit, com- 
parably with the distinctive embryo-sac types in- 
cluded for Penaeaceae and Onagraceae. The sin- 
gle known species is a large shrub or small 
scrambling tree of cloud forests at middle ele- 
vations of the Cordillera in eastern Peru and Bo- 
livia (Dahlgren & Thorne, 1984), and more re- 
cently discovered (Tobe & Raven, 1984b) in 
Panama and Costa Rica. Rhynchocalyx, a now 
rare tree of moist closed forests in south-eastern 
Africa (Strey & Leistner, 1968) shows unilacunar 
nodes, hexamerous flowers, a distinctive petal 
form, and subsidiary colpi on the pollen grains. 
We find that both of these genera retain branched 
anthotelic inflorescences (Trollian panicles; Troll, 
1964), inadequately characterized by previous 
authors. 


~ 
FIGURE 3 


four division 


of chara Phylogram A, based on data in Table 1 without bg the primary version) any reversal of direction 
cter-state change. Method of representation as in с 
is by 


1. Reference in text to vite arising at the first 
s shown (with arrow). [Alternatives of equal length 


ends the аА. MRT-HTP-PS 
laceae (CPT) with Melastomataceae (MLS 


х апа DUA-SNN- PUN: a supraminimal (lighter broken | line) places Cryp- 
).] 


722 


If the origin of Crypteroniaceae was indeed as 
shown in the primary version of phylogram A 
(shown by solid lines in Fig. 3) then the next 
events would be the initial step in loss of trila- 
cunar nodes and some degree of development of 
subsidiary colpi on the pollen grains (an addi- 
tional variant occurs in phylogram C). This would 
be followed by separation of Crypteroniaceae, 
with its own peculiar characters. As well as the 
features just mentioned, Penaeaceae and Olini- 
aceae share loss of apotracheal parenchyma, 
complete attainment of unilacunar single-trace 
nodal anatomy, and reduction of stamen fila- 
ments. If Crypteroniaceae in fact arose from the 
Melastomatacean branch, as shown in a variant 
of this phylogram longer by only one unit, then 
the wood-parenchyma character-change would 
show on the common stem of PNA-OLI with 
the A/zatea line. 

Crypteroniaceae are discussed below; both of 
the other families are endemic in Africa. The 
Pe 1 phic shrubs of the South 
African fynbos heathlands on infertile soils; Oli- 
niaceae consist of one genus of shrubs and trees 
in forests of tropical and southern Africa. Fea- 
tures of Penaeaceae are the tetramerous flowers 
in which the sepals assume the function of the 
lost petals, the well-developed subsidiary colpi, 
and the unique type of embryo-sac (Stephens, 
1909). The Oliniaceae have grouped vessels, small 
thick petals of distinctive type, and completely 
epigynous flowers; the style is very short, al- 
though the stigma is not quite sessile; the ovules 
are campylotropous, with a thick, vascularized 
outer integument (Tobe & Raven, 1983a). 

e Melastomatacean line, as shown in the 
primary version (but also see below), is marked 
by acquisition of subsidiary colpi and modifi- 
cation of the presumedly ancestral trilacunar 
nodes. Three leaf-traces are retained, but the lat- 
eral traces of the two opposite leaves at the node 
share a common gap or, in some living members, 
a girdling trace replaces the lateral traces (van 
Vliet & Baas, 1975). A supraminimal variant of 
the tree shows Crypteroniaceae associated with 
Melastomataceae and Memecylaceae. In any case 
the possible synapomorphies linking these fam- 
ilies provide rather weak evidence of their as- 
sociation, since, as shown in Figure 3, the char- 
acters concerned must have arisen independently 
a number of times in Myrtales as a whole. They 
may well have arisen in parallel twice or thrice 
within this group also. 

Wherever the family Crypteroniaceae di- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


verged, it is quite strongly distinct. It is here 
taken to comprise only Crypteronia, Dactylocla- 
dus, and Axinandra, in agreement with Dahlgren 
and Thorne (1984) and van Vliet and Baas (1984); 
inclusion of A/zatea and Rhynchocalyx, as for 
example by van Beusekom-Osinga and van Beu- 
sekom (1975), is strongly contra-indicated by the 
character-states possessed. These include the 


1 Al E 1 
шах Аел у Ulosoliiilial 


hence more plesiomorphous in the last two gen- 
era, blastotelic-anauxotelic in Crypteroniaceae 
sensu stricto); none of the authors cited clarified 
or stressed these differences. 

Unlike van Vliet and Baas (1975, 1984), we 
are not wholly satisfied with the grouping CPT- 
MLS-MMC, nor are we convinced of the slightly 
shorter alternative shown, since the inflores- 
cences within the groups are quite different in 
both cases. The blastotelic, anauxotelic systems 
of Crypteroniaceae contrast with anthotelic in- 
florescences in the other taxa (Briggs & Johnson, 
1979: 181), but resemble those of Combretaceae 
(including Strephonemataceae). No phylograms 
that we accept show Crypteroniaceae linking Wi 
Combretaceae. Others were computed that do 
show that association but are either longer (CLAX 


are less acceptable in other respects. Striking as 
it is, inflorescence similarity must probably be 
put down to remote parallelism or conven 
since a Crypteroniaceae-Combretaceae line 1s 0 | 
supported by a majority of the characters con 
sidered. 


ini ion of Figure 3, the 
In the supraminimal versio Mei 
d by Baas 


ж # ightly before CHP" 
haracter in the phy- 
а Memecyla- 
Whether the 


and co-authors), separates sl 
teroniaceae d iti 


logram links Melastomataceae ап 
ceae in contrast to Crypteroniaceae. Y Mes 
additional feature of uninucleate cells in 


Ra- 
mataceae (Tobe & 
ther tapetum of Melasto ecylaceae » 


ndra of the 
Crypteroniaceae (Tobe & Raven, * es 
attainment of a fully valvate calyx 15 e with 
linking Melastomataceae sensu stricto from 
Crypteroniaceae, and differentiating ec sai 
Memecylaceae, but this is a weak indicat! i 


ee 


1984] 


teroniaceae and the second stage (complete col- 
lapse) has an additional innovation on the Cryp- 
teroniaceae stem, homoplastic with that on the 
stem leading to Alzateaceae, etc. 
Melastomataceae and Memecylaceae are 
widespread in the tropics and in the western 
Gondwanan continents, but appear to be only 
recent (Miocene or later?) and scanty immigrants 
into the Australian region. The former is a large 
family, ding Myrt i 


е Му number of species, 
although it does not dominate extensive vege- 
tational communities as do many members of 
the Myrtaceae. The three genera of Crypteroni- 
асеае are endemic in south-eastern Asia and Ma- 
lesia. This distribution is unique in the Myrtales, 
and may point to an early geographic separation 
of ancestors, unless it is a relict of a wider range. 
In the well-marked Combretacean line, both 
the Laguncularieae and Strephonema are notable 
in having prophylls (**bracteoles") and an im- 
bricate calyx. Both cases are probably retained 
тот the primitive condition in the Myrtales; 
reversion to possession of suc organs after com- 
plete disappearance seems unlikely. One branch 
5 marked by acquisition of well-developed sub- 
sidiary colpi and complete epigyny. On this 
branch no distinctive synapomorphies mark the 
Laguncularieae, which would thus consist of three 
Separate lines for the three genera, grouped only 
use of primitive features in common (sym- 
plesiomorphies, and therefore cladistically non- 
Significant); however, Stace (fide Dahlgren & 
Thorne, 1984) reported the unusual condition of 
cyclocytic stomata in Laguncularia and Lum- 
пигета. The more advanced Combreteae are fur- 
ther marked by loss of prophyllar bracteoles and 
attainment of valvate calyx aestivation. We do 
not know whether the Asterad type of embry- 
овепу recorded by Tobe and Raven (1983a) is 
basic to the whole Combretacean line, or is con- 
fined to Combreteae. 
The second branch leads only to Strephonema. 
This is characterized by fixation of spiral phyl- 


19656), Paracytic stomates, and floral тегу re- 
-— to the 4-5 flexible condition (the last fea- 
hos IS seen also in some Combreteae). It differs 
с m its associates іп several wood and bark 
я агасіегѕ not used in the analysis, but these аге 
°nsidered by van Vliet (1979) to be primitive 
on Patel et al. (1984) note that the pollen 
tá ен is distinctive in respects addi- 
to the characters we have scored. 


Strenha» 


азе 


т 


JOHNSON & BRIGGS— PHYLOGENETIC ANALYSIS 


723 


in tropical west Africa. The Combreteae are 
widespread, but best developed in the west- 
Gondwanan continents of Africa and South 
America. The Lag lari ist of thr ry 
distinct genera: Laguncularia and Lumnitzera 
are near-mangroves or mangroves, the former in 
tropical America and west Africa, the latter from 
east Africa to the Pacific. The dryland Macrop- 
teranthes is endemic in tropical Australia, but 
nothing postively suggests that it was a pre-Mio- 
cene inhabitant of that continent. Although con- 
sidered by Stace (1965a) to be close to Lum- 
nitzera, its characters point to ancestors different 
from living species of that (at present) more 
widespread mangrove genus. 

Within the Lythracean group various possi- 
bilities exist as to the sequence of events. The 
common ancestor of the genera retained in Ly- 
thraceae sensu stricto could also be the common 
ancestor of the other members of the group. The 
terminal taxa are discussed below (3.3.2), as is 
Rhynchocalyx, which has often been included in 
the Lythraceae but which does not take that po- 
sition in this analysis. 

3.2.4 A variant hypothesis (phylogram 
B). Two variant hypotheses deserve consider- 
ation, involving different tral diti d 
hence some character-state changes of reverse 
polarity from those in the scenario presented 
above. The relevant characters are 34 and 35 
(stamen insertion on the hypanthium rim) and 
48 (some degree of development of subsidiary 
pollen colpi). The effects of the respective re- 
scoring of these on the CLAX processing can be 
considered jointly or separately: it will be con- 
venient to consider the pollen feature first. 

In the suggested phylogeny that results from 
reversal of character 48, the branching sequence 
is not changed and there is the same variant su- 
praminimal position of Crypteroniaceae as in 
Figure 3. Character 48 appears as an innovation 
on the branch leading to the large middle group 
of taxa, before the separation of the Combreta- 
cean and Penaeacean lines. Reversals of the char- 
acter (expressed as —48) would be inserted on 
the final stalks leading to ALZ and STH. The 
phylogram is thus one unit shorter than phylo- 
gram A, in which character 48 appeared on four 
internodes within the group. 

Accordingly, the scenario changes only in that 


5 ч „соц 
are assumed to have taken place very early, in 
the ancestor of the middle group of families, and 
to have been secondarily lost within that group 


z RHY STH 
"1 -48/X TRA 
24 4 29 73 
234 68' 
224 PS 65" 
x 64 | A 
E HTP 6205 a 
= 657 || 58"56' | 38' 
T MRT 58"4|57'43" - ica 
di es" 53" 45" * 1 39" 13" - 25" { то’ 
vied 53“ | |41' 36” 177" т" | UY T 20' 6 9' 
2 45" | 6۷ 3۷ l -34 |1e" |б1" 
la t -35" | 2, 52, 
ارا‎ v 51' 
49 "n mm 
114 Lb. VT 504439” 
T зө! 27^ 
9 30l[24' 
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4 tem 29۷ 24 
12° 11“ 11 
x TIT جو‎ | 10" 10 
2. 
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4 © 
53 L = 161 (internal) 


CL 


NAUVO 'TVOINV.LOS8 PHOOSSIN JHL ЧО STVNNV 


IL 10A] 


1984] 


only in A/zatea and Strephonema. If we were to 
assume further that some development of sub- 
sidiary colpi took place in the ancestor of the 
Lythracean group of families, this would imply 
loss of overt expression of this character-state in 
some lines within Lythraceae sensu stricto and 
in the line leading to the other three constituents 
of the group (see 3.1.2). 

3.2.5 A further variant scenario (phylogram 
С). Phylogram C (Figs. 4, 5) also assumes in- 
ternal change of the pollen character (some de- 
velopment of subsidiary colpi), but postulates 
additionally that, in the ancestor of the whole 
order, the stamens were inserted on the rim of 
the hypanthium. The first variant of this does 
not assume that subsidiary colpi were developed 
in the ancestor of the Lythracean group. The 
shortest phylogram then continues to place the 
Lythraceans with the Onagracean line, but there 
1s à change at the base of the tree. The Myrtacean 
group (СІ) is now seen as diverging first from 
the rest of the order, rather than having a short 
common stem with the central group of families. 

The other important differences expressed in 
this tree are that (1) within the Lythracean group, 
the Lythraceae sensu stricto would be marked by 
а phylogenetic downward movement of the an- 
droecial insertion on the hypanthium, and there 
would be some parallel development in Punica 
(implying that Duabanga, Sonneratia, and Pu- 
nica would have a common ancestor more prim- 
Шуе in some respects than could be assumed for 
the Lythraceae sensu stricto), and (2) some sim- 
ilar phylogenetic movement away from the rim 
would have occurred independently in the Com- 
bretacean line. 

All versions of phylogram C imply the same 
alternative minimal and supraminimal positions 
of Crypteroniaceae as in A and B, as well as a 
third grouping in which Crypteroniaceae unite 


JOHNSON & BRIGGS—PHYLOGENETIC ANALYSIS 


725 


with the bined ALZ-RHY-PNA-OLI assem- 
blage. Figure 5 shows the character-state inno- 
vations for these alternatives. 

The situation within the Myrtacean line is un- 
changed from phylogram A. 

Allowing alternative interpretations of the di- 
rection of change for particular characters leads 
to substantial re-grouping of taxa, particularly 
toward the base of the tree. The number of vari- 
ant phylograms, one or two units longer than the 
minimum, is increased by combinations of these 
alternatives. 

(a) In the primary version of phylogram C, 


the only y I pny taoubie ) 8 
a putative common ancestor for the non-Myr- 
tacean part of the order (C2) is the complete loss 
of the sunken style-base condition. Thus, if our 
assumption about the base were reversed, taking 
the sunken style-base as apomorphous, there 
would be a trichotomy at the bottom of the phy- 
logram, with the reversed characters (—67 and 
—66) showing on the Myrtacean stem. (Their 
inclusion on that stem would, of course, imply 
that the sunken style-base was considered an an- 
cestral character in the Myrtacean group as a 
whole, and that it was subsequently secondarily 
lost in some members of the Myrtaceae. This is 
not the sole reasonable hypothesis; see 3.1.2, 
characters 66, 67.) In any event, the Myrtacean 
group remains highly distinctive. 

(b) If the presence of subsidiary pollen colpi 
is taken as ancestral for the Lythracean line, the 
shortest tree still keeps (C3) that group with the 
Onagraceans but a supraminimal tree, which is 
only one unit longer, places the Lythraceans with 
the central group (C4) of families; this is also 


(1984) (see 3.1.2, character 50), then this alter- 
native "catches-up" since character 50 disap- 


——— c ааа ам 


— 


; FiGURE 4. Phylogram C, based on data in Table 1 except for assumption of different ancestral staminal 


35 in Figure 1. [This t ана dition in characters 34 and 35 in which stamens were inserted 


= the hypanthium 
s leading to the “middle group" of taxa, bei 


atives as in phylogram A (Fig. 3) exist within MRT-HTP-PSX. or 
i i ve not generated in phylogram A), a supraminimal only 
rhararter.ctat, + 4 f +h +h i Pe " 


e same equal-length 
PT links with PNA-OLI or with the 


o bined grouping 
¢ unit longer, places CPT with MLS (dotted line). Th 


Liidi aU 
n: 


are sh їп Е А +h 


Slate innovations within the Lythracean group are identical in the two positions.] 


ANNALS OF THE MISSOURI BOTANICAL GARDEN [Уо1. 71 


pears from two stalks and character —50 comes 
in on the stalk to the Lythraceans and the central 


54" 
3 
1 

11 


group. 

(c) Dahlgren and Thorne (1984 and pers. 
comm.) mention the possibility that the depres- 
sions between the colpi in the pollen grains of 
Trapa may represent incipient or reduced sub- 
sidiary colpi. Any hypothesis that character 48 
was common to the ancestors of Trapaceae and 
other families, except for Onagraceae and the 
Myrtacean group, would lead to a phylogram 
several steps longer. The primary division in the 


77" 
37" 


branch with the Lythracean group. Assuming al- 


RH 


ternatively that character 48 occurred in the 
ancestor of Trapaceae, without any further as- 
sumption that it was common to that line and 
others, would yield a phylogram of intermediate 
length, identical in topology with Figure 4. In 
this case innovation of character 48 would be 
homoplastic, occurring in the ancestor of Tra- 
paceae after its separation from the Onagracean 
line. 

(d) There is another tree (not illustrated) only 
two units longer than the primary version of phy- 
logram C, in which Memecylaceae are associat 
with the Combretacean group and the combi- 
nation ONA-TRA links with MRT-HTP-PSX. 


We do not accept this, but it illustrates the con- 
5 ight re- 


- = 


Ту 


or — с" 


58^ 
57'* 


E 


bottom of the order. e 
(e) Placing the Lythracean and Wee 

groups together, as in the supraminimal | 
in which 


in Figure 4, implies an early Фени КЫ teeth 


10“! 


viously discussed. From the opposite-leave? e | 
the Lythracean group would be marked ia | 
quisition of vessel clustering, unilacunar Е M 
and the two specialized character-states рі 
е seeds. The first of these seed features, ™ i 
cation of the outer integument, is unique 


7 

6 

7 
6“ 
30 


FIGURE 5. Two equal-length and one supraminimal alternative positions of Crypteroniaceae in phylogram C (as in Fig. 4) showing character-state 


innovations. 


—  — gp an 


, 


1984] 


MRT HTP PSX ALZ RHY PNA OLI 


JOHNSON & BRIGGS— PHYLOGENETIC ANALYSIS 


727 


LAG CMB STH CPT MMC MLS DUA SNN PUN LYT TRA ONA 


FiGURE 6. Congruence cladogram, expressing grouping common to minimal versions of CLAX phylograms 
also the supraminimal CPT-MLS link (Fig. 3) but excluding supraminimal variant position of 


A, B, and C and 
Lythracean families (Fig. 4). 


Lythracean group, but this hypothesis requires 
the fibrous exotegmen to have been acquired 
separately three times (in the Lythracean, Com- 
bretacean, and Onagracean lines). The only com- 
mon feature marking off the Penaeacean-Melas- 
lomatacean group from the Lythraceans would 
be the loss of all traces of leaf teeth. 

3.2.6 A preferred hypothesis? The foregoing 
analyses pick out several competing preferred 
hypotheses from the very large number of the- 
oretically possible phylogenetic trees which for 
19 taxa could be of the order of 1022 (Felsenstein, 
1978). That astronomical number is less daunt- 
ing than it Seems, since the vast majority of the 
Possible trees are manifestly implausible, and 
many of the variants differ only slightly. 

What degree of confidence can we have in the 
Selected few? Clearly, the phylograms presented 
here have a great deal in common. This is partly 
а result of our assumptions as to the set of avail- 
able and useful characters, our assumptions about 
the direction of character-state change, and the 
Implicit or explicit weighting assigned. As dis- 
cussed above (2.4.1), we have rejected shorter 
trees with initial character-states that аде је 
to accept. Trees with : 1 reversals 
of character-states are also rejected (2.4.3). 

d Confidence in the phylogenies or parts of them 
Spends on (1) the total number of synapomor- 
phies Shared by terminal taxa (a fundamental 
M of the CLAX method); (2) the lengths 
| internodes (equivalent to stalks) in the phy- 
gram, which express both the number of syn- 


apomorphies grouping certain taxa and the pa- 
tristic separateness of one group from another; 
(3) the degree of homoplasy both across the whole 
tree and in particular comparisons; and (4) the 
robustness of grouping, i.e., the invariance be- 
tween trees. In accord with (1) and (2), our con- 
fidence in the topology is greater at high ad- 
vancement levels than low in the phylogram. 
Numerical or purportedly probabilistic mea- 
sures could be devised to deal with all of these, 
separately or in combination, but such measures 


leading, because of the false confidence it engen- 


ers. 

Nevertheless, we can say broadly that confi- 
dence increases with high levels of (1), (2), and 
(4) as expressed above, and decreases with high 
levels of (3). 

All phylogenetic hypotheses are subject to 
“probable falsification” (see 4.1.3, characters 35— 
37); conversely, all may be supported by addi- 
tional evidence. False rigor in these regards is 
undesirable, but these statements are still true in 
a general and useful sense (Hull, 1967; Johnson, 
1969, 1970). Until additional hard data become 
available for the whole set of taxa, one can some- 
times prefer or reject particular variants on 
grounds of biological or geographical likelihood 
or consistency. The danger of circularity can be 
offset by the usual process of reciprocal illumi- 


728 
MRT HTP PSX ALZ RHY PNA OLI 
53 58 ба 63 33 72 62 
41 је 62 62 26 31 55 
40 56 31 [т 28 Isa 25 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


LAG CMB STH CPT MMC MLS DUA 


SNN PUN LYT 


à . 1 5 
FiGURE 7. Congruence cladogram covering minimal CLAX phylograms A, B and С (including all e 
illustrated in Figs. 3 and 4) and also a CLAXMIN cladogram (Fig. 1). See text for explanatio 


numbers and limitations of the representation. 


nation, as well as by progressive accumulation 
of information. 

With respect to the scenarios given here, we 
have perceived no strong indications or contra- 
indications as to the probable functional success 
ofthe hypothesized ancestors. We hope that oth- 
er investigators may be able to do so, bearing in 
mind the probable physical and biotic conditions 
during the periods concerned. Such fossil evi- 
dence as exists is too scanty to help either in 
reconstruction or in timing of events. 

The extent of congruence between the CLAX 
phylograms Figures 3 and 4 (excluding the su- 
praminimal variant position of the Lythracean 
assemblage) is shown in Figure 6. If all illustrated 

i X 


7 The currently vexe 
tuated equilibrium or is graduali 
analysis, or the application of formal taxo 
ardent supporters of punctuated equilibrium with the 
fortuitous, as is the scientifically damagin 


confidence set to have comparable value, which 
may not be so, on other grounds. ker а 
changes common to all the hypotheses consi¢ 
ered may be written in on the internodes ме 
Fig. 7) but the sum of these does not Me 
length of the tree or represent all the changes p 
must be taken into account. There are no = 
stant characters on the stems immediately belo : 
Laguncularieae, Crypteroniaceae, and Ly ~ 
ceae. One can conceive the phylogenetic his 
in the form of scenarios only by considering S€P- 
arately at least the favored contenders am 
more fully resolved trees (= hypot — ond 
In the Myrtales, as in the Myrtaceae an e 
plant groups we have considered, the ње i 
are mostly short on the lower parts of t s E 
This means that the ancestors were Rm it 
very different through a sequence of e 
divergence, and possibly that many er pe 
small divergences took place early an pe 
relatively short period. It does not а 
eral theory of punctuated equilibrium ЧЫ ай 
We believe (with Grant, 1982) that ген 
continuous range of tempi and modes p 
tion and that the processes leading 10 SU 
tion and speciation are those by wh virout 
course of time and given app " 
stances, taxa of higher order—and £r 


| í seeds by pune 
question (and vexatiously polemical dispute) of whether evolution pr f ћујорепе 
ffect the st metho; aoc 


thods 
ue 


more extreme philosophy of Cladism is pes 
8 association of political outlooks with evolutionary 


ich, in the , 


-—— 


} 


1984] 
tion— have their roots. Arguments for a different 


given by van 
specious and illogical. This is in no way to 
that hierarchical control is a vital part of genetic 
systems or that a systems-analytical approach 
(Riedl, 1977, 1979) is of value in understanding 
evolution; nor is it to deny that in certain groups 


<< 


lution and fixation of new syndromes in small 
populations under circumstances of strongly se- 
lective environmental novelty (Stanley, 1979). It 
is to deny that this must a/ways be the case, and 
it is to suggest that recognition of “higher” taxa 
is often psychologically and pragmatically influ- 
enced by the extinction, over a long period, of 
many branches of the relevant phylogenetic tree. 
When there has not been *enough" such extinc- 
tion, the sitit dde sine Spe ancestors 
are often seen to differ in few characters and not 
in obvious highly набаве syndromes, which 
often came later. 
би mont robust assemblage to emerge is Myr- 
H All the 
diis (even the вани analyses rejected 
here) show this group as having a common stem 
of considerable length, made up of character- 
States showing few homoplasies, i.e., there is a 
high level of character-state congruence. More- 
Over, the group branches off before or soon after 
any other divergence. 

The grouping Onagraceae-Trapaceae is also 
Present in all phylograms presented, but is less 
Strong in both respects. Some supraminimal phy- 
lograms not considered here would place Tra- 
paceae elsewhere, though very weakly. More- 
Over, we have had to extrapolate to some extent 
in assigning characters to Trapaceae, in which 
there are no living woody members, though the 
common stem shown does not depend on ex- 
trapolations. Tobe and Raven (1983a) state that 

“Trapaceae are more distinctive in their em- 
bryology than any other member" of the order. 
= merely means that the family has autapo- 

morphic pecularities, which have no effect on 
cladistic grouping. Raven (pers. ies ) does NOE 
consider 
Tee, to be аа 

The Lythra robus tly, 


tacea 


о“ 


but like o teak k ` together with 
Which it may possibly constitute a holophyletic 
кы 15 not so clearly isolated as the Myrtacean 


The Combretacean threesome has a long stem 
with some unique characteristics, despite the 


JOHNSON & BRIGGS—PHYLOGENETIC ANALYSIS 


729 


strong divergence of Strephonema. It associates 
fairly consistently (Fig. 6 although not Fig. 7) 
with the remaining complex of families discussed 
below, but not with a very long common stem. 
We have at times suspected that Crypteroniaceae 
may be associated with this group, partly because 
we are impressed by the inflorescence similarity, 
but other characters suggest that the blastotelic 
inflorescence is a convergent development in the 
two cases (3.2. 

The remaining families are rather aed held 
together in most analyses (Fig. 6) by a common 
stem without unique pns. Variation 
in groupings leads to these appearing as six in- 
dependent lines from the base in the more in- 
clusive congruence cladogram (Fig. 7). Like the 
Lythracean and Combretacean groups (but with 
rare exceptions interpreted as secondary re- 
versals in at least some of the phylograms), they 
show a pollen type marked by more or less pro- 
late grains, primarily without a high degree of 
exine thickening or elaboration, and probably 
pre-adapted to the development of subsidiary 
colpi. However, Muller (1981b) considered this 
basic pollen type (without manifest subsidiary 
colpi) to be plesiomorphous for the order, and 
his reasons appear sound. Consequently, it is not 


see 3.1.2 and 3.2.5 for a contrary view). The 
Lythracean phylad, on the results of the analysis, 
associates almost as closely with this weakly 
linked group of families as with Onagraceae-Tra- 
paceae. We would regard the — of the 
Lythraceans as an open ques 

As already mentioned, "m с о. of Cryp- 
teroniaceae has been regarded as problematical. 
The analyses suggest that this family does not 
form a holophyletic group with Melastomata- 
ceae-Memecylaceae. Nevertheless, the latter pair 
separate only by a short string of markedly hom- 
oplastic characters from the Penaeaceae-Cryp- 
teroniaceae group. 

The Penaeacean assemblage hangs together in 
the analyses with a shortish common stalk. On 
our scoring, the group divided into two parts, 
Alzateaceae-Rhynchocalycaceae and Penae- 
aceae-Oliniaceae(-Crypteroniaceae) respective- 
ly; all families are themselves well marked. 

Thus we are not prepared to put forward any 
single more favored precise phylogeny; rather, 
we present several competing (but not highly dis- 
similar) hypotheses as a basis for thinking about 
the order Myrtales and its constituents, and for 
checking and refinement in the future. The in- 
dividual terminal taxa are discussed below. 


730 


3.3 SYSTEMATIC IMPLICATIONS 


3.3.1 Subordinal division. Because of the 
uncertainties at the base of the phylogenetic tree, 
it seems best not to recognize formal suborders, 
but one can refer informally to the Myrtacean, 
Lythracean, and other complexes if desired. 

3.3.2 The families. Dahlgren in Dahlgren 
and Thorne (1984), has adopted family delimi- 
tations that coincide almost entirely with those 
we have reached from consideration of this anal- 
ysis. The few cases where Thorne takes a more 
inclusive view are discussed below and also by 
those authors. 

It would not be altogether unreasonable to ac- 
cept as families all of the 19 terminal taxa of our 
analysis, especially if one took as a basis the tra- 
ditional recognition of Sonneratiaceae and Pun- 
icaceae as families distinct from Lythraceae. 
However, the analysis Suggests that these are 
“weak” families and their removal probably 
leaves Lythraceae as a paraphyletic taxon, and 
moreover that there is no particular reason to 
place Duabanga and Sonneratia together in a 
single segregate family, or indeed as a subfamily, 
although they are still so associated, without any 
clear justification, e.g., asa family by Backer and 
van Steenis (1951) and Cronquist (1981), or as 
a subfamily by Thorne (1976, 1981). Tobe and 
Raven (1983a) acknowledge that there may be 
little reason to associate Sonneratia and Dua- 
banga. We might then take these as a point of 


sufficient condition depends on point of view and th 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


pt d from point-set topology) embraces holophyly and 
epend on the definition of the £roup concerned alone, but on that of at least one a 
y 


ken as a necessary condition for recognition in phylogenetic systematics. m y 
t strenoth af fi i g era ji 


(Мог. 71 


from the early Lythraceous stock, although Tobe 


and Raven (1983a) draw attention to embryo- — 


logical differences between Punica and the rest 
of Lythraceae sensu lato. 


The second closely-linked group is the Com- - 


bretacean complex, with three terminal taxa as 
fed into our analysis. The three genera of La- 


guncularieae differ considerably from each other | 


and, being grouped chiefly by symplesiomorphy, 
may not constitute a clade. Some authors have 
recognized a family Strephonemataceae, despite 
its possession of a number of ““Combretaceous” 
characters. Strephonema is peculiar in many re 
spects and must have branched off early within 
the line. Pending the accumulation of more crit- 
ical data, Combretaceae could perhaps be ге 
tained sensu lato, to embrace all three groups, 
with the present division (Exell & Stace, 1966) 
into only two subfamilies. However, the analysis 
provides no objection to recognizing Strepho- 

t family, and this may well emerge 
as the preferable treatment. 


Crypteroniaceae have been discussed above | 


(3.2.3). Accordingly, we would neither include 
the family in a broadened Melastomataceae nor, 
of course, іп a very broad concept of Lythraceae 
as suggested at one time by Thorne (1976). 


parate 0 y 


Nu 
by a short string of markedly homoplastic e 
acters from the Penaeaceae-Crypteroniae i 
group. This last ge hangs toge e 
analyses with a shortish common stalk; ee 
scoring, it divides into two parts, — ee 
Rhynchocalycaceae and Penaeaceae- 


. its con- 
aceae(-Crypteroniaceae) respectively. ide 
a . 


stituent families are themselves well mi ой | 


cyloideae, cannot stand. As pointe (i9 
Vliet et al. (1981), and van Vliet and Baas 


unequiV- 
ofa taxon 


as worthy of individual recogn 


ition at the same rank as the paraphyletic residue. 


OHIZ’ 


| 


| 
| 
| 


| 
, 


1984] 


the tribe Astronieae belongs in the Melastoma- 
toideae whereas Pternandra (including Kibessia), 
constituting the tribe Kibessieae, is more closely 
related to Memecylon and its allies. Morley (1953) 
had indicated this affinity, mentioning also the 
antepetalous ovary locules as a difference from 
the Melastomatoideae. The feature of interxylary 
("included") phloem (as distinct from the com- 
mon Myrtalian feature of intraxylary phloem) in 
the Melastomatoideae, in its more recent cir- 
cumscription, is not shown in the phylogram be- 
cause it was difficult to assign a direction and 
therefore a primitive condition to the character 
in other families. It does stand as an important 
additional distinction between Melastomataceae 
and Memecylaceae. 

At first sight, Mouriri, Votomita (Corypha- 
denia) (Morley, 1953, 1963; not mentioned by 
van Vliet et al., 1981), and the greater part of 
Memecylon appear very distinct from Melasto- 
matoideae, by virtue of the absence of strongly 
acrodromous venation. However, this feature 
does appear in Pter d also in the genera 
Spathandra and Warneckea (Jacques-Félix, 
1978a, 1978b; Jacques-Félix et al., 1978) and in 
= “Nise re-segregated Lijndenia (Bremer, 


Jacques-Félix et al. (1978) present the view 
that acrodromous venation is fundamental in 
Memecylon, and presumably modified to a sec- 
ondarily brochidodromiform condition in most 
of the genus. From the data in their paper and 
our examination of specimens, and by compar- 
ison with transitions in Myrtaceae (see also Hick- 
€y, 1981), we are not convinced of this. It seems 
*qually possible on the internal evidence, and 
oe likely from out-group comparison, that the 
original condition is brochidodromous as in most 
of the Myrtales, and that acrodromy has had 
Separate origins in Lijndenia, Spathandra, War- 
neckea, and Pternandra, as well as in ancestral 
Melastomatoideae (becoming fixed throughout 
that group). Incidentally, van Vliet (1981) dis- 
misses out of hand the claims to generic rank of 
Spathandra and Warneckea, apparently because 
they do not show differences from Memecylon 
within his field of study. This dismissal unjustly 
®verlooks the sets of correlated characters care- 
fully Pointed out by Jacques-Félix, and segre- 
gation seems well justified for the genera recog- 
"ized by him and probably for Lijndenia. 

In discussion of the Melastomataceae, van Vliet 
(1981), van Vliet et al. (1981), ter Welle and 
Koek-Noorman (1981), Baas (1981), and van 


JOHNSON & BRIGGS—PHYLOGENETIC ANALYSIS 


731 


Vliet and Baas (1984), all propose a broadened 
concept of the family, comprising three tribes 
Melastomatoideae, Memecyloideae, and Cryp- 
teronioideae. Despite the number of papers cit- 
ed, the arguments are not cumulative. From the 
characters used in our analysis, and without strong 
contra-indication from others mentioned by these 
authors, there are no unique synapomorphies to 
indicate that the three groups mentioned form a 
holophyletic assemblage. Crypteroniaceae, which 


that migh 
allies together with Melastomataceae sensu stric- 
to do not appear to be ancestral in either group, 
or else are shared with other families. Conse- 
quently, it will cause less confusion and is more 
logical to regard Memecylaceae as a family, with 
the constitution indicated above. The congru- 
ence cladograms (Figs. 6, 7) emphasize the lack 
of association of these taxa vis-a-vis Crypte- 
roniaceae. Some of the character-states discussed 
in the papers cited are plesiomorphous and have 
no significance in phylogenetic grouping. Of 
course, it is possible that future evidence may 
change this picture. Strongly advocated taxo- 
nomic conclusions founded almost entirely on 
particular subdisciplines, such as wood anatomy, 
embryology, chemistry, or pollen morphology, 
are always suspect, whether conservative or rad- 
ical. It is no more of an upset of usage to rec- 
ognize Memecylaceae than to sink Crypteroni- 
aceae, and clarity will be served thereby. 
Among the remaining families, Trapaceae and 


Onagraceae fairly clearly comprise two early-di- 
vergent lines, namely Ludwigia on the one hand 
and the rest of the genera on the other. This is 
recognized by other authors in this symposium, 
and is discussed by Eyde (1981). We have taken 
the ancestral floral condition as perigynous and 
not epigynous on the basis of the nectary position 
and Eyde’s well-argued case. Our ancestral pic- 
ture of the Onagraceae is of woody plants con- 
siderably different from some of the familiar 
modern herbaceous members, but there is no 
doubt of the unity of the family. The line leading 
to Trapaceae has clearly undergone great change 
since the ancestors of the Trapaceae separated 
from the proto-Onagrads, or from elsewhere 
among early Myrtales. Additional autapomor- 
phic features characterizing Trapaceae are found 
in the embryology (Tobe & Raven, 1983a). 


#32 


Alzatea does not fit in with anything else in 
the order, a conclusion in agreement with the 
views of Dahlgren and Thorne (1984) and with 
the findings of Graham (1984), who describes 
the family Alzateaceae. It comes out on a com- 
mon stem with RAynchocalyx in our analyses 
and Graham (pers. comm.) finds that both have 
trans-septal vascular supply to the placenta. She 
points out also that the placentation types (de- 
scribed by earlier authors as axile in RAyncho- 
calyx but parietal in A/zatea) differ in breadth of 
the placenta but are not as dissimilar as these 
terms might appear to indicate. However, trans- 
septal vascularization occurs in diverse families 
in the order (Schmid, 1984) and in scattered 
groups in Myrtaceae (Schmid, 1972a, 1972b, and 
our observations); it must have arisen several 
times. Moreover, the two genera are very differ- 
ent in anatomy, palynology, and general floral 
morphology. They do show embryological sim- 
ilarities, at least some of which could be syn- 
apomorphies (3.2.3), as well as differences (Tobe 
& Raven, 1984a, 1984b). For general accounts 
see Graham (1984), Lourteig (1965), Dahlgren 
and Thorne (1984), and references therein. 

Rhynchocalyx was referred to Lythraceae when 
originally described (Oliver, 1894), a position 
upheld by Sprague and Metcalfe (1938), Baas and 
Zweypfenning (1979), and van Vliet and Baas 
(1984). None of our phylograms support this; 
they indicate that the common ancestors of 
Rhynchocalyx, Alzatea, and the Lythraceae would 

common ancestors of several other justly rec- 
ognized groups as well. 

Some ofthe characters shown on the path lead- 
ing to Rhynchocalyx аге, of course, shared by 
Lythraceae; others do not occur at the base of 
Lythraceae but are found in several taxa within 
that family. Insertion of stamens on the rim of 
the hypanthium is found in Duabanga and Son- 
neratia, which we regard as offshoots from a 
Lythraceous base. The obhaplostemonous con- 
dition, trans-septal vascularization, micropyle 
formed by the inner integument only, and seed- 
coat type distinguish it from other Lythraceans. 
It may be argued that the first three could easily 
be homoplastically attained. The simple seed- 
coat structure may possibly be secondary, i.e., 
derived from the characteristic Lythraceous con- 
dition by evolutionary reversion. While all of 
these suppositions are conceivable, they imply a 
longer phylogram than those presented. Conse- 
quently, on the principles adopted in this anal- 
ysis, to accept Rhynchocalyx as being on the 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


Lythracean line would require additional evi- 
dence or cogent argument beyond that consid- 
ered here. 

It is not logically sufficient to point to resem- 
blances with particular members of the Lythra- 
ceae that must, in part, be the results of homo- 
plasy or be symplesiomorphic. To do so leads us 
back to the fallacies of phenetics or to intuition. 
On the characters used in our phylograms, we 


that R} 


in the Lythraceae; this opinion is strengthened 
by th id tly available. Graham 
(1984) now supports this view. Raven and Tobe 
(1984a, 1984b) give embryological evidence, in- 
cluding the ephemeral anther endothecium, that 
Rhynchocalyx ought not be in Lythraceae. 

In the context of the other taxa recognized 
herein as families, it should have a family to itself 
and it is therefore desirable to establish one for- 
mall 


RHYNCHOCALYCACEAE L. Johnson & B. 
Briggs, fam. nov. TYPE: Rhynchocalyx Oliv. 


Arbores foliis integris decussato oppositis, inflores- 
centiis paniculatis (anthotelicis), floribus em 
perigynis, lobis calycis valvatis, petalis шнш 
cucullatis, staminibus in verticillo singulo ante] " 
in summo hypanthii insertis, primo nnn e 
theris bithecatis prope basin dorsifixis, granis po^ : 
eninacatis еы ва Бис os 


к к : у 1 4 аб 
pellato sed plus minusve uniloculari, stylo be Re 


centis axilibus duabus longitudinalibusque, micron 
x integumento interiore solo formato, fructibus 
culicide capsularibus multispermis. 

As indicated above (3.2.5), there is no o: 
ty as to the position of the Lythracean line те 
ative to the branch bearing Rhynchocalycacet 
in the phylograms, and the wide separa 
these lines is to some degree an artifact г i 
presentation in the phylograms. For insi 
one supraminimal tree the Lythracean line JO 
proximately with that leading to Репаса dots 
Rhynchocalycaceae, etc. Nevertheless, this 
not invalidate what has been said above. 

The Myrtacean assemblage remains. ee 
(Briggs & Johnson, 1979) we recognized фе 
ylaceae and placed that family near et ill 
ceae, but with some doubtas to its closest » 
Schmid (1980) has argued for its pen ў 
Myrtaceae. Scott (1980) recognized au and 
loxyleae within Myrtoideae, while pe aa 
Zweypfenning (1979) pointed out resem 
in wood anatomy to the Lythraceae. plants 
now seen better material and young living 


e 


| 


| 


h лы н  ЗР a o { 


1984] 


of Psiloxylon and, if our interpretation of its 
characters is correct, the analysis shows it as 
clearly related to Myrtaceae but differing in a 
considerable suite of characters. 

In our earlier paper we were impressed by the 
resemblances between Heteropyxis and some 
Myrtaceae and, in particular, interpreted the an- 
droecium of Heteropyxis as reduced from a con- 
dition of five staminal bundles (then considered 
by us to be primitive in the Myrtaceae). Reduc- 
tions of that kind appear to have taken place in 
a number of Myrtaceous genera. Subsequent ex- 
amination of better material, including living 
plants, indicates that there are fundamentally two 
whorls of stamens and that, unlike the condition 
in various oligostemonous Myrtaceae, the vas- 
cular traces of the stamens are separate, showing 
no indication of reduction from a fascicled con- 


that there were originally two whorls of staminal 
groups (see 4.1.3), but that the antesepalous whorl 
was lost early in most lines. There is no indi- 
cation in the Myrtales at large that a polyste- 
monous condition is an original character of the 
order; so it seems likely that this arose by dé- 
doublement in the primitive Myrtaceae, and that 
the androecia of all members we admit to that 
family can be derived from such a condition. 
Heteropyxis and Psiloxylon appear to have di- 
verged before this acquisition of staminal pro- 
liferation. Both genera, moreover, have a com- 
pletely superior ovary contracted at the base, 
unlike Myrtaceae proper in which there is always 
some degree of union between the broad-based 
Ovary and the hypanthium. 

Schmid (1980) has provided very useful in- 
огтапоп on these genera, which has been used 
п our analysis where relevant. We can now con- 
firm that Psiloxylon has anthotelic, though some- 
What reduced, inflorescences. 


€ as the Myrtaceae proper. The further anal- 
~ the Myrtaceae and these close allies (4.2) 
bits Уб former hypothesis, but only by one 
bus IS does not provide sufficient grounds for 
кы. Heteropyxis and Psiloxylon in a single 

Y, and we recognize both Heteropyxidaceae 
апа Psiloxwia : RR 2 2 


a 4 К, o = 
rated early from the Myrtalian line. At an earlier 


JOHNSON & BRIGGS—PHYLOGENETIC ANALYSIS 


733 


stage of the present study (Johnson & Briggs, 
1981b) we suggested that Heteropyxis might be 
treated as a subfamily of the Myrtaceae; more 
detailed analysis does not support the implied 
grouping. 

The Myrtaceae constitute a large and diverse 
family, but one that is very well defined; the 
division advocated by Kausel (1956) into Myr- 


drome and the distinctiveness of the other two 
families from each other and from Myrtaceae 


th | Ee a 
E ae о © 


proper, as well as р 
ic patterns. 


4. PHYLOGENETIC ANALYSIS OF MYRTACEAE 
4.1 THE METHOD AND ITS LIMITATIONS 


4.1.1 The taxa. Our earlier treatment of 
Myrtaceae (Briggs & Johnson, 1979) listed the 
genera and assigned them to an informal system 
of alliances and suballiances, which may be re- 
garded as roughly equivalent to tribes and sub- 
tribes in a formal system. 


2.4 


ER | 11 == = 11 
IGCally таке тап 


units as the taxa to be considered (ће OTUs in 
the terminology of some authors), down at least 
to the level of the suballiances, but should treat 
problematical genera individually. We have not 
yet been able to do this for all taxa. Table 3 
indicates the placement of taxa of the present 
analysis in the earlier system. Distributions are 
indicated and discussed, down to the suballiance 
level, in Johnson and Briggs (1981а) and given 
in more detail for the Australian members (John- 
son & Briggs, 1983b 

In dividing the family into taxa for this anal- 
ysis, our emphasis on problematical situations 
has led to units of unequal status. Three anom- 
alous genera of the Lophostemon suballiance are 
treated separately but the Myrcia, Myrtus, Cryp- 
torhiza, and Eugenia alliances are grouped into 
*Myrtoideae sensu stricto." The character-states 
scored for this group are those conditions that a 
common ancestor could have possessed consis- 
tently with the polarities assigned and the states 
in the constituent groups so far as we are able to 
determine them. This assumes that the group is 
monophyletic (= “convex,” see 3.3.2) in the con- 
text of the other alliances. It does not assume 
that it is holophyletic (Ashlock, 1971), although 
the analysis would indicate that it is so. 

We make similar assumptions at a lower taxo- 


734 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


TABLE 3. Relation between taxa of present and earlier treatments. 


Taxa of Present Analysi 
(and Names of. Individual Genera = 


Previous Treatment (Briggs & Johnson, 1979) 


Sub- 
family* Alliance Suballiance 


Psiloxylon: excluded from Myrtaceae 
Heteropyxis: excluded from Myrtaceae 


Excluded from Myrtaceae 
E Heteropyxis 


Metrosideros group (Basisperma, Kania, Lophostemon, E Metrosideros Kania 
e Ї Mearnsia, Metrosideros, Ristantia, Te- Metrosideros 
pualia, Welchiodendron, Xanthostemon) Xanthostemon 
Lophostemon 
ro 
Kjellbergiodendron E Metrosideros Lophostemon 
(pro parte) 
Whiteodendron L Metrosideros Lophostemon 
(pro parte) 
Lindsayomyrtus Е Metrosideros Lophostemon 
(pro parte 
Backhousia group (Backhousia, Choricarpia) L Backhousia 
Arillastrum group? (Allosyncarpia, Arillastrum, E ucalyptop- E Eucalyptopsis 
sis, gen. nov.) 
Angophora group” (Angophora, Corymbia) I Eucalyptus Angophora 
Symphyomyrtus group (Eudesmia, “Sebaria,” Symphy- I Eucalyptus Symphyomyrtus 
omyrtus) 
Eucalyptus group (Eucalyptus, * Idiogenes," *Gaubaea") T Eucalyptus Eucalyptus 
Leptospermum group uu e Callistemon, Lamarchea, E Leptospermum Leptospermum 
Leptospermum, Melaleuca, Phymatocarpus) Calothamnus 
Chamelaucium group esee Baeckea, Calytrix, x L Chamelaucium Baeckea 
calypta," Chamelaucium, Corynanthera, Malleostem Chamelaucium 
Micromyrtus, Pileanthus, Scholtzia, Thryptomene, est th 
ordia) 
"Myrtoideae sensu stricto" (Austromyrtus, Eugenia, Fenz- M Myrcia 


lia, Meteoromyrtus, Myrcia, Myrtella, Myrtus, Pilothe- 
cium, Psidium, Stereocaryum, Uromyrtus, Xanthomyrtus) 


Osbornia 
Acmena group (Syzygium, gen. nov.) 


yrtus 
Cryptorhiza 
Eugenia 
M Osbornia 
M 


Syzygium 
Acmena 


Acmena 


* L = Leptospermoideae; M = Myrtoidea 


° Some change in circumscription ни with earlier treatment. It is now clear that Arillastrum 


must be 
formal 


removed from the Angophora group to the affinity of agen н (see 4.4). Foreshadowing a mere 
to 


© Referred to as the Bett suballiance in Johnson & Briggs (1983b). 


nomic level for some ofthe other alliances, which 


Metrosideros, and X. anthostemon 
suballiances. together with the residue of the Lo- 
phostemon suballiance after the anomalous gen- 


d 
era жайынан putas он Whiteodendron, - 
sayom ve been removed. We 


to Lophostemon, some of them undescri 

ter G. Wilson, pers. comm; В. F. y tjon: 
pers. comm. ), that deserve special considera nits 
if only for the purpose of redefining the su le 
liances. As we pointed out previously, the 


v 


1984] 


phostemon suballiance may not be a very natural 
group, even with the exclusions noted above. We 
discuss the Chamelaucium alliance separately 
(4.3), but hope to carry out a detailed analysis 
on this group and also on the constituents of the 
Leptospermum alliance, in which the suballi- 
ances may not fall out quite as simply as sug- 
gested in our previous paper 

Psiloxylon and Heteropyxis, though recog- 
nized herein as constituting separate families 
(3.3.2), have been included in the analysis for 
comparison. 

Because of the deviations from our previous 
classification, we have designated each terminal 
taxon in the diagrams as a group (gr.) rather than 
asan alliance or suballiance, except for the genera 
treated individually and for **Myrtoideae sensu 
stricto." Taxonomic conclusions are discussed 
below (4.4). 


4.1.2 The method. Since the completed . 


CLAX program was not available for computer 
use, and hand processing of the data by the CLAX 
method was very time-consuming, we took some 
computational short-cuts for the analysis of Myr- 
laceae, in contrast to that for Myrtales. It is there- 
fore less certain that a minimal tree (without 
reversals and on the initial assumptions) has been 
obtained; this will affect chiefly the portions of 
short internode-length, which are in any case very 
subject to variation according to character selec- 
tion and scoring. We have not performe A 
NER-78 analyses or other procedures of that kind 
but, as discussed above (2.4), we do not find these 
practically useful in any case. More detailed stud- 
les are planned (but see 4.2.2). 

-1.3 The characters. The characters used 
(Table 4) include only those in which the prim- 
Шуе and derived states occur differentially as 
fundamental to taxa used in the analyses. Further 
derived States, and indeed further characters, are 
Important in the evolutionary diversification o 
the family at large and mark many genera and 
*Peciés-groups. We have previously referred to 
many of them when listing vegetative and inflo- 
rescence features or when discussing adaptive 
Syndromes (Briggs & Johnson, 1979); other fea- 
ures are mentioned by Schmid (1980). 
in contrast to the treatment for the Myrtales, 
neg some of the methods of analysis required 

. “TY Coding, we have retained our original se- 
nal multistate coding, thus reducing the number 
of designated characters. 

ё апу characters additional to those used for 
© order are significant at this level, but natu- 


JOHNSON & BRIGGS—PHYLOGENETIC ANALYSIS 


735 


rally the character-states taken to be ancestral for 
the Psiloxylon-Heteropyxis-Myrtaceae line are 
omitted. 

The characters cannot be discussed at length 
in this paper. We have used all characters for 
which reasonable information has been available 
to us and which showed variation within the 
group, assigning polarity on the same principles 
as for Myrtales. Information has been derived 
from many sources, including Briggs and John- 
son (1979), Carr and Carr (1969), Dawson (1970a, 
1970b, 1970c, 1972a, 1972b, 1972c, 1972d, 
1975a, 1975b, 1976, 1977, 1978a, 1978b), Gad- 
ek and Martin (1981), Gauba and Pryor (1958, 
1959, 1961), Green (1979, 1980, 1983, and pers. 
comm.), Hyland (1983), Ingle and Dadswell 
(1953), Johnson (1972, 1976), McVaugh (1968), 
McWhae (1957), Pike (1956), Pryor and Johnson 
(1971), Schmid (1980), Thompson (1983), Wil- 
son (1981), and Wilson and Waterhouse (1982, 
and pers. comm.), as well as our own observa- 
tions in many fields. Useful characters undoubt- 
edly exist in chemistry (e.g., Hegnauer, 1969; 
Hillis 1966, 1967a, 1967b, 1967c, 1967d, and 
pers. comm.; Lassak, pers. comm.) and bark 
anatomy (Bamber, 1962; Chattaway, 1953), and 
should ultimately be available from such fields 
as protein sequencing. Nothing could be incor- 
porated from these fields into the overall analysis 
because of insufficient coverage of the taxa. 
Nevertheless, terpenoid and flavonoid chemistry 
as well as periderm anatomy have contributed 
to our general thinking in some of the Australian 
roups 

A few characters call for comment at this point: 
Characters 1-12. Wood anatomy. Data are 
drawn largely from Ingle and Dadswell (1953) 
and our own observations, but van Vliet and 
Baas (1984) gave valuable suggestions as to di- 
rections of evolutionary change. 

22-28. Phyllotaxy and inflorescence. Vegeta- 
tive phyllotaxy and branching in the Myrtaceae 
were discussed by Briggs and Johnson (1979) but, 
as indicated above (3.1.2), it now seems probable 
that although the opposite-decussate condition 
occurred in some ontogenetic stages of primitive 
Myrtales and primitive Myrtaceae, it was part of 
an ontogenetic spectrum in which disperse (spiral 
or "alternate") g t also occurred. With- 
in the Myrtaceae, the ultimate branches of uni- 
florescences usually revert to opposite in those 
cases where adult vegetative stages and conflo- 
rescence axes have spiral phyllotaxy. The se- 
quences in the spectra are various; for instance, 


ge 


736 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


TABLE 4. Characters used in the phylogenetic analysis of Myrtaceae. Postulated primitive states with zero 


scores 


очо WR WN 


© 


10. 
Id. 
12. 
13: 
14. 
15. 
16. 


— 
N 


18. 


. Vessel aggregation 


Elongation of vessel-ray pits 
Elongation of vessel-ray pits 


. Vessel-ray pits 


Loss of bordered pits from fibers 


Loss of vasicentric tracheids 


. Loss of apotracheal parenchyma 


Loss of paratracheal parenchyma 


. Increase in paratracheal parenchyma 


Increase in ray heterogeneity 


Oil ducts (many small) in stem pith? 

Oil ducts (few ped n stem pith? 

Oil ducts in the pe 

Loss of ded d о hairs (at least 
from vegetative body) 


. "Psiloxylon-type" modification of standard 
hai 


air 
" Kjellbergiodendron-type" modification of hair 
gophoroid hairs" 


19. *Angophoroid hai 


N 
© 


ел 


37. 
38. 
. Loss of syncolporate condition 


. "*Arillastrum-type" hairs 


Bristle-glands 


. Reduction of accessory buds 
. Loss of stipules (excluding retention only at 


cotyledonary med 


. Intramarginal v 
. Fixation of vA vegetative phyllotaxy 


. Fixation of spiral vegetative phyllotaxy 


. Fixation и: opposite phyllotaxy in 


inflore 


nce 
. Fixation P spiral phyllotaxy in inflorescence 
9. Reduction of degree of inflorescence 
1 


branching 


. Loss of recaulescence in inflorescence 
. Reduction of anthopodia 
. Reduction of perianth mery 


. Petal fusion into a calyptra 
tals 


. Herbaceous peta 
. Androecium 


. Stamen proliferation 


Loss of stamen inflexion 
Well-developed connective gland 


0 = — solitary; 1 = mostly grouped 
0 = small + isodiametric; 1 = elongated 
0= ховала orm (rem elongated; 
Е = considerably elong 
0= А. 1 = large simple 
0= a present (i.e. uc 
1 = pits dicm (i.e., fibers libriform) 
0 = present; 1 = absent 
0 = present (often scanty); 1 = absent 
0 = present (sometimes scanty); 1 = absent 
0 = scanty; 1 = confluent or ban 
0 = type 1; 1 = n А Па 
зеп 


0 = absent; 1 = present 
0 = absent; 1 = present 
0 = present; 2 = absent 


0 = absent; 1 = present 


0 = absent; 1 = present 
0 = absent; 2 = present 
0 = absent; 2 = present 
0 = absent; 1 = incipient (papillate condition); 


2 sent 
0 = сЗа 1 = infrequent; 2 = 
0 = present (row of hair-like pure А = absent 


0 = absent; | = pre 

0 = +opposite, ЕН мани to spiral, 
1 = opposite о 
disjunct-opposite) 

0 = — switching ontogenetically to spiral; 
1 = spiral throughout 

0= „> 1 = fully fixed 


0 = +opposite; 1 = disperse 
0 = much branched: 1 = somewhat reduced; 2 = 
greater reduction; 3 = reduced to triads or 
monads (or single-flowered reduced botryoids) 
0 = present; 1 = absent 
0 = developed; 1 = reduced; 2 = absent 
0 us; 1 = 5-4-merous flexible; 2 = 


V apparently obdiplostemo 
nous; 2 — partial к, of Lance stamens, 
= obhaplostem 
0 = absent; 2 = prol dues to cluster; 3 = well- 
developed seed 
rai 


eloped; b = well developed 


dev 
0 = pollen syncolporate; 1 = apocolporalé ____ 


| 
| 


A- áÀ—À 


737 


1984] JOHNSON & BRIGGS—PHYLOGENETIC ANALYSIS 
TABLE 4. Continued. 
40 0 = absent; 1 = present 


. Pollen with very large polar island 
41. Reduction of carpel number 


42. Epigyny 

43. Stipitate ova 

44. Exaggerated later growth of free portion of 
ovary above attached portion 


45. Trans-septal ovary vascularization 
46. Style reduction 


50. Limitation of ovule attachment 


51. Reduction of ovule rows on placenta 


сл 
х 
& 
e 
= 
6 
Бе 
© 
З 
о 
= 
© 
2 
= 


e ber 

- Modification of anatropous condition 

55. Оушоде« 

. Loss of fruit dehiscence 

57. Hypanthium fleshiness in fruit 

58. Ovary-wall fleshiness in fruit 

39. Seeds fewer than ovules in multi-ovulate 
Ovaries 


un 
B 


wn 
см 


60. Seeds fewer than ovules in 2- or few-ovulate 
Ovaries 
: j · Well-organized crystalliferous layer in testa 
- Embryo with hypocotyl much exceeding 
ns 


63. Embryo folded 
4. Cotyledons folded 


e 


0 = isomerous with perianth; | = 4—3 carpels (1 or 
2 less than perianth mery); 2 — 2 carpels 

0 = gynoecium free; 1 = slightly adnate (broad- 
based); 2 — greater adnation; 3 — virtually 
completely adnate 

0 = not stipitate; 2 = stipitate 

0 = absent; | = present 


0 = axile; 1 = mixed; 2 = trans-septal 

0 = at least medium elongation; | = not at all 
elongated 

0 = slight ог no lobing; 1 = exaggerated lobing 

0 = at least moderate lobing; | = little or no lobing 

0 = sunken; | = not sunken 

0 = over most of axile area; ! = near base of 
loculus only 

0 = many-rowed; | = few-rowed; 2 = 2-rowed 

0 = not peltate; 1 = peltate; 2 = strongly peltate 

0 = ovules numerous; 2 = ovules few 

0 = anatropous; 2 = hemitropous or campylotropous 

0 = absent; 1 = present 

0 = dehiscent; | = tardily dehiscent; 2 = indehiscent 


0 = dry; | = fleshy 

0 = most ovules developing to seeds; 1 = seeds 
several but much fewer than ovules; 2 = 
seeds reduced to 1 or 2 

0 = most ovules developing; 1 = seeds fewer than 
ovules 

0 = absent; 2 = present 

0 = absent; 1 = present 


0 = straight; 1 = folded or coiled 
0 = flat; 1 = folded 


бај types of secondary xylem as in Ingle and Dadswell (1953). 
€cords for oil ducts include unpublished data from Peter С. Wilson (pers. comm.). 


* See Carr and Carr (1962) 


p pointed out by Wilson (1981), in the Xan- 
ор suballiance spiral phyllotaxy is char- 
uum of Juvenile plants but is followed in 
um ees by the opposite-decussate condi- 
Ung Lophostemon and Welchiodendron the 
Bs pattern is encountered while in Tristan- 
Ы and Ristantia the phyllotaxy is disperse 
б shout (Wilson & Waterhouse, 1982, un- 
inis sad with an error for Lophostemon adults 
as x Table 1). Fixation in different directions 

GN in various groups. D. Carr and S. 
on ib 81) and S. Carr and D. Carr (1981) point 
nds at there are many variations of spiral phyl- 
У in the Myrtaceae and attach great impor- 


tance to this. We (Johnson & Briggs, 1983a) would 
consider these as secondary to the essential on- 
togenetic sequence of opposite-decussate and 
spiral, in one or other of the usual Fibonacci- 
sequence arrangements. 

The scoring of characters 27 and 28 (fixation 
of phyllotaxy in inflorescence) refers to the most 
plesiomorphous condition of the ultimate inflo- 
rescences attributable to the ancestor in each 
group. It frequently applies only within uniflo- 
rescences, which may be greatly reduced. This 
can be understood by reference to the analyses 
of inflorescences presented by Briggs and John- 
son (1979). The many other changes and re- 


[VoL. 71 

1 0 0.0 038 
00072 00 0 0 D 
0 0:030 


10 11 12 13 14 15 16 17 18 19 20 21 22 
000000000799 


43): 34:5.5.5. 7.8.9 
1 


1 


23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 
Data matrix (taxa and characters) used in analysis of Myrtaceae. Character-states are defined in 
Do C9". 0.059 


TABLE 5. 
Table 3. 


Psiloxylon 

Eucalyptopsis “alliance” 
Angophora suballiance 
Symphyomyrtus suballiance 
Eucalyptus suballiance 
Whiteodendron 
Lindsayomyrtus 
Backhousia alliance 
Leptospermum alliance 
Chamelaucium alliance 
"Myrtoideae" sensu stricto 


738 


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=> oo соо о о соо соо Оо Оо осо осоо 


0 


© со T – о со еч еч со соо O со со с єч 


О +з р 

cOoocococoocoo—-—-oooocococ 228% ос Bee e ae dang redd ea 
COC ос оо Seo eee eo Sh]. T = 

У|сосо-ооо----=5-ооо- 
OO C4 C4 € NANNAN — C 6€ сч e e 
“NN OONN KH NSH NOH NS 

Э|ооооооооооооо- оо 
ч ا کا ا ا ر س ت کے ا کا صا س کا جت‎ 

VIPGNNNOGoo goo one о 
осооооосоос шо сес ا کے کے‎ 

©[ссоосодосооооооо=зо 
O = e e e — e — — — — — — — — سے‎ 

%|99——-—-чааачолчовоо 
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A|-"-oocoocoocooco--—-—-—-ooooc- 
SONNNNANANMAANANAN 

is пјоооооо- ч ооророоо ~ 

© сз сз c^ e e c6 сб) её) сту en e e e C A 

S| nooooonna--oaoonumq 
oocococoocococoqueoco-o 

a|[oo----ooooooocooo 
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г|јочачачаосеоосоосоолчоолчо 
ооочачач“есоосососооло 

E e a mm mm E gg mme 
оочооооч- чоо - = = 

іа чооооообооооооо 

а оооооо-оромчосмчоо чо 
~“ > ~" до ооовсесјокнсе 

Фјоооооооо-ооооо - о 
EC O a a O a a = ص‎ 

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ہے ہے ہے ہے ہے ہے ہے بس ہے ہے — — O ~ m= e‏ = 
جا اھا کا feo‏ ات کی ےک کک س و 

"il"ccocococoosoogocoooo 

E: 

ч 

+ 


© 
sO COCO OO OCC ==—0 
© 


=... Onn –оооомо 


0 


[^] 
E - : g 
D S о Ф 2 ^o = о 8 E 
— Г ав | о 
5258 ај u 2838 Ф = за 
88555 9 = ess dad 3 
. 08 73.8 = с 3.5.5 2 5.9 5.9 y sess 2 
пл та 488%5 5 agag gidan B 
ВАДЕ ЕЕ > ЕВЕ БЕЗНЕЕ , 
закас Кое з "o ee SE SRE Se aS 9 
2 = © S [~] : E a , 3 © 

7 S&S fo 5 БЕЛЕ У БАЗЕ 5 БЕ5ЉЗЕЗ б 
НЕЯ ТРТ 

-ò "= У Bo о = 
SSRESSFESTSSSSBVveES PSHSREDESOSSES SRE S 

M Eos Бобо Oo > = ок а о хе Sten So sae ee eo oS & Б 
5580 Мом = не“ ~ 525 SV SCS SSseyuyss=s 2) 
~ = ок CE SE ESS SS ™BeeSetytsee et 8 Б а = 

2585 = o soa ge 5 S 2 5 Ko Ss 00 R Sus © 
ص‎ a оу ~ & © Wie "- ~ я 
о ЧИМЕ ISAS: о учити: gsgios: 


i 


— зе 


Bn. ^d 


1984] 


peated trends in inflorescences there described 
је је Ed 11 4 LE ы d 41 AA 4 Ta ae 


ly at a finer level of analysis, as can be seen from 
Table 2 of that paper. 

16-21. Trichomes are also discussed by Briggs 
and Johnson (1979: 172). We have considered 
the thin-walled unicellular hairs of the “Сог- 
ymbia" group (equivalent to a genus) of eucalypts 
asa variant ofthe rather similar but multicellular 
hairs designated as **angophoroid." It is uncer- 
tain whether these are phylogenetically homol- 
ogous with the Arillastrum-type branched hairs, 
the branched hairs found in a very few members 
ofthe Acmena alliance, or indeed the thick-walled 
acute hairs arising in groups on glandular pro- 
tuberances in a minority of species of E ucalyptus 
sensu stricto (the assemblages incorrectly called 
"stellate hairs" by earlier authors and by Carr & 
Carr, 1980). Their differences and occurrence 
suggest that some of them at least are indepen- 
dent developments, and characters 19-21 are 
scored accordingly. S. Carr and D. Carr (1981) 
foreshadow further critical studies on Myrta- 
ceous trichomes, which will be useful. We hope 
also to comment further on trichomes; for the 
present we merely draw attention (characters 17, 
18) to what appear to be variants of the standard 
myrtaceous hairs in Psiloxylon (thin-walled, usu- 
ally Subacute, bulbous at the base or unequally 
2-armed) and Kjellbergiodendron (very short, 
subacute). 

Other variants, for example as described by 
Schmid (1972a) and observed by us in Eugenia 
SPP. and some other Myrtoideae sensu stricto, 
are not basic characters to the taxonomic units 
treated in this analysis. 

24. Intramarginal leaf vein. On the basis of 
°ut-group comparisons within and beyond the 
Myrtales, we have taken brochidodromy as the 
ancestral state. The strengthening of primary-lat- 


appears to have 
Oped from the brochidodromous condition 
Па number of lines, as it has in other Myrtales 


devel 


2/- The androecium. Our general inter- 
pretation of the fundamental conditions in the 


ыл. Proper, display a wide variety of an- 
?*cial conditions in mature flowers. Schmid 


JOHNSON & BRIGGS—PHYLOGENETIC ANALYSIS 


739 


(1980) has designated the staminal placement 
within the Myrtaceae in terms of diplostemony, 
haplostemony, obdiplostemony, and obhaplo- 
stemony, with considerable discussion. This is 
almost wholly descriptive of the condition in ma- 
ture flowers, rather than interpretative. If we are 
to consider phylogenetic relationships, we are 

nd to mal interp i і to reach 
at least some tentative conclusions on evolu- 
tionary changes and consequent equivalences and 
homologies. The dangers of partial circularity are 
obvious and have often been stressed. They may 
be averted or corrected by reciprocal illumina- 
tion, successive approximation, and tests that 
potentially allow what might be called “probable 
falsification,” as discussed by Hull (1967), John- 
son (1969, 1970), and Mayr (1981). 

We have formed an hypothesis of the se- 
quences of androecial evolution in the Myrtaceae 
(Fig. 8) but cannot develop it fully here. Accord- 
ing to this, the origin of the family more or less 
coincides with the proliferation of stamen initials 
within each of the ten primordia corresponding 
to an earlier ancestral 5-merous, 2-whorled con- 
dition. The evidence suggests that the original 
androecial condition in the Myrtales was dip- 
lostemonous, but that in a pre-Myrtaceous 
ancestor (perhaps common to Myrtaceae and 
Heteropyxidaceae, if a supraminimal tree were 
accepted, see 4.2.2), and indeed separately in 
some other Myrtalian families, this had given 
way to apparent obdiplostemony. This would be 
the result of a spatial shift in the levels of initi- 
ation at the rim of the hypanthium and/or dif- 
ferential early growth in this region of the hy- 
panthium, not to suppression of whorls, hence 
the qualifier "apparent." The order of develop- 
ment within the resulting staminal groups or fas- 
cicles is centripetal with respect to the flower as 
a whole, i.e., the first-developed and often (but 
not always) longest stamens are in the radially 
outer median part of the bundle. 

In accord with the studies of other authors 
(e.g., Mayr, 1969) and with the obvious condi- 
tion in many genera with fasciculate stamens, we 
had previously thought that there were originally 
only five antepetalous primordia, i.e., that the 
family was fundamentally obhaplostemonous 
with proliferation. In Ari/lastrum, we have since 
found П antesepalous i staminal fascicles 
to be present, though inconstantly; the additional 
fascicles were also described and illustrated by 
Dawson (1970a), though he made no comment 
on their significance. 

Even if this were a reversion (failure of a sup- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог, 71 


XX У 


f the 
FIGURE 8. Trends in androecial poanion in the Myrtacean phylad. А-В. character-states in ancestors 0 
My 


Myrtaceae; С-М. conditions in 


E. irregular ring of stamens with some vestige of fasciculate condition; — Е. 


e, J-M occur in the Baeckea suballiance.—A. 


diplostemonous with 10 


0 stamen fascicles, the antesepalous e small (as postulated 
اي‎ E Ey only;- 
of pius ng fused at 


w 
—H. stamens reduced to few or сура in fascicle; —1. fascicles developed пије long claws; d partial sup supp 


ase; 
sion of central stamens in pese — 


antesepalous fascicles; — 
stamen 


- irregularly spaced; — M. ап tesepalous stamens only. [The a 


shown as if only one- dies i in relation to the floral radius. In fact, the original м ri Sn 
staminate fascicles show proliferation radially, as well as laterally, and this condition persists various!y 


of the derived states. Thus the conditions shown in C, D, I. E. G 


pressive mechanism), it would indicate an earlier 
obdiplostemonous condition. Developmental 
studies are necessary in the related genera of the 
Arillastrum group, and indeed in other assem- 
blages such as the Acmena group and the four 
constituents of the Myrtoideae sensu stricto, to 


sive. It is clear that only the antepetalous whorl 
remains in many groups in the family, including 
Eudesmia and apparently in S ymphyomyrtus and 
Eucalyptus sensu stricto. In the absence of pos- 
itive evidence of the loss of the antesepalous 
staminal groups in Myrtoideae, Backhousia, and 
Osbornia, and in view of their persistence in Аг- 
illastrum, these three assemblages are conser- 


tesepalous (“‘episepalous”’) staminal- fascicle pri- 
mordia, developed somewhat later than the pet- 


al-stamen complexes, in Myrceugenella (©. 
Luma in the usage of McVaugh, 1968). As p 
says, "Somit leigt im Prinzip ein diplostemo 
Androecium vor, das in beiden Kreisen e lyan- 
drisch ausgebildet ist." At least some ан 
ideae, however, do show suppression of C 
tesepalous whorl in organogeny y Рис 
Mayr, 1969). Conditions in the mature Mer 
do not necessarily reveal the situation at i 
mordial stage = ч needs to be er 


r four 


0 
ilies. In some cases it is dear that five ( 


fascicle-primordia a are not found, and tha from à 


ring, which 


— 


1984] 


son & Briggs, 1983a) in the mature flower (D. 

Carr & S. Carr, 1981, as “‘staminophore’’). As 

discussed below, we see this as a derived con- 

dition, usually from five or four primordia, but 

just possibly in some cases from ten primordia 

in two whorls, as mentioned above. 
Th + Гол E 


deecrihed 


luriseriate 
or multiseriate (e.g., Bentham, 1867, as "several 
series”; О. Carr & S. Carr, 1981), but they do 
not usually form clearly defined separate series; 
rather, in these **multiseriate" cases the stamens 
are simply several deep on any radial sector. 

As we see it, there have been several lines of 
departure, sometimes seen in combination, from 
the 5- (or 4-)fascicled condition (Fig. 8D): 
(1) Lateral confluence of fascicle-bearing pri- 
mordia in early or later stages of develop- 
ment to give a more or less uniform ring of 
Stamens (Fig. 8E-G), as discussed above. 
Sometimes this is partial, so that the fila- 
ments are shorter opposite the sepals, giving 
à subfasciculate appearance. 

From ancestral stage direct, or from (1), re- 

duction in stamen number (e.g., in Myrrhi- 

nium), at the ultimate to as few as five or 
four, e.g., in S Vzygium pro parte (“ Тегтаеи- 

а? and **Aphanomyrtus") (Schmid, 
1972b) (Fig. 8H). The last case implies a path 
from Figure 8F to 8H, not shown in the fig- 
ure, 

(3) Radial elongation of the united region to form 
à pronounced claw dividing into separate fil- 
aments on its edges, summit, and sometimes 
adaxial surface (Fig. 81). 

(4) Reduction from (3) by loss of the claw and/ 

ог reduction in number of individual sta- 

mens (Fig. 8H, alternative route, e.g., in La- 
marchea sp.). 

Partial (Fig. 8J) or complete suppression of 

median stamens in each bundle, resulting, 

(a) as a penultimate stage, in apparently an- 

lesepalous bundles each of which is made up 

of two adjacent edges of antepetalous fasci- 
cles (Fig. 8K, e.g., Astartea), and (b) as an 
ultimate stage, in few rather irregularly spaced 

Stamens (Fig. 8L) or, in the extreme, in five 

apparently regular antesepalous stamens (Fig. 
> €.£., in Thryptomene spp.). 

aon as these, there are of course consid- 

pat ifferences in filament length and color, 

as in the attachment, shape, and dehis- 
сепсе of anthers. 

MT applied these interpretations in pos- 

8 original conditions in the taxa, but many 


~ 
N 
~ 


— 
cn 
~ 


JOHNSON & BRIGGS—PHYLOGENETIC ANALYSIS 


741 


of the developments discussed appear to be later 
than the origins of the groups shown in the phy- 
logram for the family. Hence, most of them do 
not appear in the character list for this level of 
analysis. Nevertheless, the androecial structures 
are vital to the interpretation of the family and 
to the groupings accepted by us. 


4.2 PHYLOGENY OF MYRTACEAE 


4.2.1 "Protomyrtacea." As with the Myr- 
tales, using out-group comparisons and general 
morphological principles, we postulate an an- 
cestral ~ Protomyrtacea." This would represent a 
stage after the divergence of Psiloxylon and Het- 
eropyxis. Some characters that are fundamental 
to the order, and appear in the “description” of 
" Protomyrtalis," are not mentioned again. 

Habit and bark as in **Protomyrtalis." Schizo- 
lysigenous secretory cavities present in stems, 
leaves, flowers, and fruits, containing terpenoid 
substances (especially monoterpenes and ses- 
quiterpenes) as essential oils. Habitat and wood- 
anatomical features much as in 


a 
calyx, unicellular, acute, rather thick-walled, with 
n and s h wall. Nodes unila- 


t 

site?). Stipu 
filiform. Leaves as in **Protomyrtalis" but entire, 
without vascularized teeth. Inflorescence as in 
* Protomyrtalis." Flowers with a distinct antho- 
podium, bisexual, entomophilous, essentially 
pentacyclic (but see androecium below), 5-mer- 
ous or flexibly 4- to 5-merous, perigynous, me- 
dium-sized or small, actinomorphic. Perianth 
members free; calyx and corolla as in “Proto- 
тупа.“ Androecium of two whorls, with the 
apparent outer and better-developed whorl an- 
tepetalous, each whorl consisting of staminal 
clusters developed by proliferation within the 
primordia. Stamen-clusters inserted on the hy- 
panthium rim (or the antesepalous ones some- 
what below the rim); filaments inflexed in bud. 
Anthers as in **Protomyrtalis" but with a well- 
developed terpenoid-containing connective 
gland. Pollen isopolar, oblate, syncolporate with 
three apertures, lacking subsidiary colpi and vis- 


742 


cin threads, the tectate exine moderately thick- 
ened but not highly ornamented. Gynoecium 
broad-based (slightly united with the hypan- 
thium), but otherwise gynoecium, placentation, 
ovules, fruit, seeds, and germination as in **Pro- 
tomyrtalis." Chromosome number л = 11. 
4.2.2 Hypothesis and scenario. The histori- 
cal picture that emerges if the phylogram? (Fig. 
9) is approximately correct, taken in conjunction 
with the distribution of these families and of the 
order as a whole, suggests an origin of the Myr- 
tacean line (see 3.2.3) in or near the African por- 
tion of west Gondwana. Psiloxylaceae probabl 
included members now extinct; Psiloxylon itself 
is on the verge of extinction, and many of its 
character-states may have been acquired well af- 
ter the initial divergence. As shown earlier, there 
is no reason to link Psiloxylon with the non- 
Myrtacean families. Of some 20 apomorphous 
features shown for it, seven are autapomorphous 
(i.e., unique to this line). The homoplasies of the 
other advanced states are widely scattered 
among the Myrtaceae. The shortest tree pro- 
duced by the analysis shows a branch leading to 
Heteropyxis and Psiloxylon, but a tree one step 
longer would associate Heteropyxis with the 
branch leading to Myrtaceae. In any case, Table 
5 and earlier discussion (3.3) show that Heter- 
opyxis and Psiloxylon differ very considerably 
from each other and must have diverged early. 
The most important new feature of the ances- 
tor of the Myrtaceae proper (4.2. 1) is the stam- 
inal proliferation (4.1.3), which is combined in 
this line with at least some degree of epigyny. 
We take the latter term (in agreement with 
Schmid, pers. comm.) as synonymous with ad- 
nation or continuity of the ovary wall with the 
hypanthium. Some authors have described the 
ovary in some Myrtaceous genera as fully su- 
perior. This is not the case; there is always con- 
siderable adnation, in contrast to the narrow- 
based ovary in the perigynous (but not at all 
epigynous) flowers of Psiloxylon and Hetero- 
pyxis. Differential growth during fruit develop- 
ment may modify the situation from that at the 
flowering stage. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


We shall not narrate the suggested phyloge- 
netic sequences here; they can be ascertained from 
Figure 9 and Table 5. The hypothesized ances- 
tors of all main lines are not very different from 
one another. Two early internodes represent non- 
unique changes in single character-states, so that 
the sequential branching hypotheses at these 
points are weak. We suggest that the early di- 
vergences must have taken place at least by the 
Paleocene, although the macrofossil record does 
not yet appear to be useful in this regard and the 
microfossils are still not clearly assignable to 
groups. Internal analysis within the alliances and 
suballiances shows that many of the features 
commonly regarded as characteristic of partic- 
ular group isiti and that 
parallelism and g 
applies to vegetative, floral, and fruit features. 

All the lines of Myrtaceae shown in the phy- 
logram are present in the Australasian region. 
Among them only Kjellbergiodendron and 
Whiteodendron are absent from the Australian 
continent, and the pollen of Kjellbergiodendron 
shows strong resemblance to the sporomorp 
Myrtaceidites mesonesos Cookson & Pike from 
the Oligocene of south-eastern Australia 
(McWhae, 1957). The distribution and pona 


РНУуСОоБСОвГар y of the aliia : 
alliances are discussed by Johnson and Briggs 
(1981a), although they are arranged therein un- 
der subfamily concepts to which we no longer 
adhere. 

The **Myrtoideae sensu stricto” are best rep- 
resented in South America, with a probably те 
cent extension to the warmer parts of North 
America; but only the Myrcia alliance is endemic 
in the New World, though the Eugenia and n: 
torhiza alliances appear to be centered there. Th 
Myrtus alliance is well represented by genera : 
the Old World (mainly in the Australasian re 
gion) as well as in the New. In contrast to "t 
earlier views (e.g., Andrews, 1913; Beadle, 19 
our character-state polarity assumptions : 
analysis do not indicate the “Myrtoideae E 
base group for the family. In view of the occ ш 
rence in the Australasian region of the other mal 


s with 
nsiderable 


چ 


f 


1984] JOHNSON & BRIGGS— PHYLOGENETIC ANALYSIS 743 


40 
ACMENA gr. ANGOPHORA gr. 
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BERGI YRTU gr. 
2)” DENDRON 53(2)" |32(1)“ 
+ we 5311] 1 
34 57" ere. 0)” јат 2(2) 
"n DENDRON " " 
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BACKHOUSIA gr.[s::)* [312^ |зе(з), {267 | 7" UCALYPTUS gr. 
> . . 
6 4v 29(3)" f18’ 24У 23“// Ld 35 (3): 
|. 26 63" 29(2)'" [13^ 16(2) "v [157 s” 33” 
59(2)' [29(1)" [12v 16(1)' [i177 3" 32(2)'" 
"MYRTOIDEAE вв.” 59(1)^ 1179 giv 10У 32(1)'* 
PSILOXYL — 
ih $*"CHAMELAUCIUM [?*(3" f° 45(2)/ эт 
58 63v 62’ gr. 8v 2 4 5(1) 24" 
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40, 5 4(2)” 49(2)'" 2517 
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29(1)" |52(2), se(1)'* 16(2)'" 
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| 
Ros. ч " Phylogram of relationships in Myrtaceae. Representation as in Figure | 1 but apie a 
ча f n фри 5. [If Myrtoideae, Backhousia, and Osbornia ors 
a ully Pa, plostemonous condition (character 35(3)), an equal alternative occurs with ty Meirosideros 
ж | ising at level 8, above the base of the left-hand fork from level 7. The alternatives shown among 
JPtus and its allies are discussed in the кез (4.4).] 


4 u at least some myrtoids with several  taceae from Australia appear to be from the 
dut E ог near-endemic genera, it seems likely Paleocene (Lange, 1982, and references therein). 
iy oh of the early diversification of the fam- Probable pd extensions from this region are 
tho Place in the east-Gondwanan region, al- listed and discussed by Johnson and Briggs 
ugh the earliest-known reliable fossils of Myr- (1981а). ey notably the South American 


744 


“Jeptospermoid” Tepualia'? and perhaps some 
southern amphi-Pacific members of the Myrtus 
alliance (represented by allied but now distinct 
genera in the east and west), may result from 
connections or propinquity until mid-Tertiary in 

tarctic region; ot , such as th t Asian 
outliers of the Myrtus and Acmena alliances and 
perhaps some “leptospermoids,” may date from 
the Miocene approximation of the Australian 
Plate to that region. Others are almost certainly 
the result of dispersal over considerable dis- 
tances, for instance, Metrosideros sensu stricto 
in much of the Pacific and perhaps the progenitor 
of “genus aff. Mearnsia" (“‘Crystalla’’) in south- 
ern Africa (Briggs & Johnson, 1979). Since 
“Crystalla” is much more closely related (by any 
criteria) to the west-Pacific Mearnsia, and indeed 
to the whole of the Metrosideros alliance, than 
Heteropyxis or Psiloxylon are to any Myrtaceae, 
it does not seem likely that the African-Austra- 
lian disjunction in this case is particularly an- 
cient. 

After the exclusion of the unrelated Syzygium 
and its allies (the Acmena alliance, see below), 
Eugenia still remains a huge genus centered in 
South America with a scattering of species from 
Africa to the Pacific. We take it to include Jos- 
sinia (Schmid, 1980; Briggs & Johnson, 1979), 
at times used for the Old World species, and are 
unconvinced that Scott (1980) is justified in rec- 
ognizing a small group of Mascarene species as 
a separate genus rather unfortunately named 
Monimiastrum. Eugenia needs a thorough re- 


the 
лм 4 


supposed 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


consideration, in the context of such South 
American taxa as Pilothecium (Briggs & John- 
son, 1979; Legrand, 1975). 

A few odd cases remain unexplained, such as 
the occurrence of Meteoromyrtus in peninsular 


India and Stereocaryum in New Caledonia; these | 


seem to belong to the Eugenia alliance, but Ster- 
eocaryum, at least, can hardly be a late derivative 
of Eugenia itself. The Acmena alliance is cen- 
tered in the Australasian-Malesian region, but à 
few members ofits largest genus, Syzygium, have 
reached Africa, perhaps through southern Asia 
(one species is still found in southern Arabia). 


The type genus of the family and order, Мутњ, | 
has one of the most atypical distributions, being 


the only representative of Myrtaceae in the ex 
tended Mediterranean region. Scott (1979) con- 
siders that the Australasian-New Caledonian 
Austromyrtus should be included in Myrtus, 
Byrnes (1982) makes a similar recommendation, 
on the logically insufficient ground that the species 
referred to Austromyrtus display considerable 
heterogeneity. We are not disposed to accept this 
without critical reassessment of the affinities of 
Myrtus sensu stricto vis-à-vis the American Psi- 
dium group of genera. * Austromyrtus" and 15 
western Pacific allies need critical phylogenetic 
re-evaluation; Byrnes’ studies will yield useful 
information but traditional (phenetic though nol 
numerical) approaches will not serve to clarify 
evolutionary taxonomy. 

Common and wide occurrence of taxa ы 
today is not necessary to the conclusion that t 


of 
"> Fossils (by courtesy of Edgardo Romero and Elsa Zardini) and photographs of fossils that we have see 


could conceivably belong among the more generalized members of Symphyomyrtus. Dr. Romero’ 


are simil 


tic. 
C E ucalyptus (sensu lato) from the Miocene of Patagonia (Frenguelli, 1953) are somewhat enigma 
The illustrations of fruits of Eucalyptus patagonica (“patagonicus”) Fr 


enguelli, if we interpret them со 


arin some | 


сарзшаг га 


DAT: r show a clearly ; vhet 
bud-like piece shows a calyptra (operculum) of eucalypt type. On the whole they do not appear to us 


to belong 
упојдеге. 


to the Eucalyptus alliance, and probably not to *Leptospermoideae," although they may perhaps be M renguelli 
a tly from th f ti ar F rich 


mparable with that of Gymnostoma (Casuarinaceae) of which a fossil occurrence CCo 
i nson & Wilson, 1981). Though they are un 


rosideros by Jarzen (1982) is ve 


m- 

s well as some lU 

that contin is conceivable that species ey have 

uth America through the Australia-Antarctica connection but, if $0, ituation 
ave i ndwana. The pata 


less 50 У 
ћ "Fossil 


familiar | 


А 


| 


1984] JOHNSON & BRIGGS— PHYLOGENETIC ANALYSIS 745 


ancestors of the lines concerned diverged early. 
It is often stated that “Eucalyptus” (referring in- 
discriminately to various members of the An- 
gophora, Symphyomyrtus, and Eucalyptus sub- 
alliances) appears scarcely if at all in the fossil 
record before the Oligocene and became domi- 
nant over wide areas as late as the Pleistocene. 
Nevertheless, Lange (1978, 1982) has described 
fruits that look like advanced members of this 
group as “probably of early Neogene age." Phy- 
logenetically it makes no sense to assert, as pa- 
leobotanists and paleogeographers are wont to 
do, that the eucalypts were a late development 
within "Leptospermoideae." Their characters аге 
inconsistent with such an origin. Neither is it 
necessary to assume that the earlier members o 
the various eucalypt lines dominated large areas 
of vegetation or that they were associated with 
very open forest or woodland conditions. On the 
contrary, their indicated affinities suggest that 
they were adapted to conditions marginal to rain- 
forest, intolerant certainly of suppression by 
shading, but possibly occupying quite small areas. 
The genus Gymnostoma in the Casuarinaceae, 
Which dates at least from the Eocene, provides 
àn ecological parallel (Johnson & Wilson, 1981; 
Johnson, 1982), expansion into more open hab- 
1415 in that family being chiefly associated with 
the more “advanced” genera Casuarina and Ál- 
locasuarina. 
The initial adaptational features marking the 
divergences, not only of the main lines shown, 
but of many genera of the family, will need fur- 
ther study and consideration. They have doubt- 
less predetermined the later directions taken in 
b. radiation of each group (see also Riedl, 1977, 
79). As a result, quite different habitats have 
‘emained characteristic of some genera, whereas 
bes се parallelism from similar structural 
paca eatures, or convergence from dissimilar 
Рас чта associated with the occupation of 
edi ra es. We have discussed a number of 
чек с" (Briggs & Johnson, 1979; John- 
riggs, 198 1a). 


4.3 THE CHAMELAUCIUM ALLIANCE 
a commenting on the systematic impli- 
a меч of the analysis within the family, we must 

urther at the Chamelaucium alliance. 


ha : 
"* recognized a subfamily Chamelaucioideae 


(usually misspelled as *Chamaelaucioideae" or 
even *Chamaelaucoideae"). We have pointed out 
(Briggs & Johnson, 1979) that this is untenable. 
More than a century ago, Bentham (1867), who 
treated the three subfamilies of such later authors 
as tribes, wrote, “The first two subtribes of Cha- 
maelaucieae have a peculiar habit . . . but some 
of the third subtribe (7hryptomeneae) pass so 
gradually into the Leptospermeae, as only to be 
distinguishable from Baeckea by the examina- 


. Green, 
pers. comm.) are well aware of the affinities and 
difficulties of distinction in this area. Our own 
studies show that the connections are multiple 
and involve considerable parallelism. 

Schmid (1980) retained Chamelaucioideae in 
the body of his paper. In the lengthy appendix, 
written after he had seen our treatment, he ad- 
vocated its retention, claiming that “the distinc- 
tiveness of Chamelaucioideae sensu Schmid... 
as well as differences in inflorescence, fruit, and 
embryo structure between this taxon and Baeck- 
einae . . . strongly argue against including the lat- 
ter in Chamelaucioideae sensu Schmid or ‘Cha- 
melaucium alliance’ sensu Briggs and Johnson.” 
He also stated that “other than their probably 
correct belief that the ‘Chamelaucium suballi- 
ance' is *an evolutionary grade' with its origins 
amongst early members of the Baeckea suballi- 
ance" we “р tionale for thi it 
el realignment.' 

In fact, the realignment is only formally novel, 
in that Bentham (1867) pointed out the lack of 
clear distinction. Bentham, of course, did not 
recognize a high-level distinction between his 
*Baeckeae" and what we call the Leptospermum 
alliance, and neither does Schmid. 

To deal with Schmid's points as cited: (1) there 
is no consistent difference in inflorescence be- 
tween our Chamelaucium alliance and quite a 
number of other “leptospermoids,” as will be 
evident from Table 3 of our cited paper; (2) in 
Scholtzia, which is clearly related to Baeckea, 
fruits of some species approach closely the in- 
dehiscent fruits of the so-called Chamelaucioi- 


observations) suggesting homoplastic develop- 
ment. The embryos in fact do not differ greatly 
in the Baeckea and Chamelaucium suballiances, 
and we now doubt that even the small difference 
as quoted in our earlier paper and by other au- 


746 


thors is consistent. All of these embryos do differ 
markedly, as indicated previously, from those in 
the Leptospermum alliance. 

Schmid (1980) refers also to the diversity of 
chromosome numbers, quoting us on the con- 
trast with the general stability in the family. As 
we had indicated, diversity in base numbers is 
in fact characteristic only of some genera within 
part of the so-called Chamelaucioideae, and is 
consequently cladistically irrelevant to the origins 
of the group as traditionally conceived. Smith- 
White (1959, and references therein) сона 
karyological suay of te group, and he 
stressed it edid aat 
it clear that die = 11, the prevailing number іп 
Myrtaceae as a whole, was general in Calytrix, 
Thryptomene, and their associated genera [i.e., 


Thryptome- 
neae")]. Moreover, it appears to be constant in 
Pileanthus, Chamelaucium, and section Cato- 
calypta ofthe possibly diphyletic Verticordia. Rye 
(1979) has extended karyological studies, finding 
some additional base numbers, including X — 10 
and X — 9 in individual species of Thryptomene, 
as well as X — 10 and X — 8 in Beaufortia and 
X — 20 in Phymatocarpus. The last two are un- 
doubted members of what we have called the 
Beaufortia infra-alliance (Johnson & Briggs, 
1983b) within the Leptospermum alliance (it is 
equivalent to the Calothamnus infra-alliance of 
Briggs & Johnson, 1979). 

Combining the karyological and morphologi- 
cal evidence, we conclude that there have been 
quite a number of descending dysploid series, 
including two in the Leptospermum alliance, one 
or two in Thryptomene, and several in various 
genera of the Chamelaucium group as narrowly 
interpreted (i.e., the Chamelauciinae or *Eucha- 
maelaucieae" in Bentham's sense). They appear 
to be associated with the mode of life of these 
habitally and reproductively very specialized 
genera. As stated, dysploidy gives no cladistic 
support to the concept of an integrated Cha- 
melaucioideae in the traditional sense upheld by 
Schmid. 

Schmid (1980) refers also to pollen morphol- 
ogy as differing markedly from that of the rest 
ofthe family, citing Pike (1956). In reading Pike's 
paper, one should refer to tables and text as well 
as illustrations, since these are not always con- 
sistent; but it is clear from her findings and even 
more so from the pollen we have ourselves ex- 
amined in the Chamelaucium alliance and else- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vo.. 71 


where in the family, that this also is not cladisti- | 


cally sustainable. We take it that a more ог less 
oblate syncolporate or parasyncolporate condi- 
tion is fundamental in the Myrtacean line, asa 
derived condition from the more or less prolate 


} 


and ера grains basic to the Myrtales | 


(3.1 

БИ the Myrtaceae, apocolporate (includ- 
ing "brevicolpate" and “‘longicolpate’’) grains are 
seen as a secondary development, and occur in 
genera scattered through several alliances. Cer- 
tainly, such conditions, and particularly Me 
colpate grains, are frequent in the Chame 


cium suballiance. But they are neither und | 


in the suballiance nor confined to it; they appear 
also in some members of the “Baeckea suballi- 
ance," and we have found series within some 
genera from syncolpate to brevicolpate. Again, 
the condition is not fundamental to the "cha- 
melaucioids," except perhaps in the “Chamelau- 
ciinae.” It must be seen as homoplastic within 


the group and is — irrelevant to its phy- | 


logenetic recognitio 


ees character discussed above, 


the consistent амер of Myra e 
from all veg nguis 
es the whole of our Chamelaucium alliance > from 
the Leptospermum alliance 

pert analysis (Fig. 9) would place the 
origin of the **Baeckea suballiance,” and that 0 
such genera as зен Р and its allies, alongside 


nsid- 
remainder requires additional internal со 


eration of the Chamelaucium alliance. 
4.3.2 Phylogeny within the Chamelaucium 


— 


| 


alliance. Our conclusions on probable pifio 


sum- 
eny within the Chamelaucium alliance are + 
marized in Figure 10. This is not a ripe 
merical phylogram, but expresses the same 


i bser- 
of thought. It is largely based on our ow? - 


м the literature 
9, 1980, 1983; 
Rye, 1979; Schmid, 1980); and unpublished s 
formation from workers on particular 
especially from J. W. Green 
Figure 10 does not меш to specify 

branching at all points but, although а 
characters exist that should be taken ! 
count, we believe that the main рћујове 
groups shown are realistic. The chief char? m 
used are indicated on the diagram or are : ge 
self-explanatory. The terms dichasium, bo 


dition 


into ac 


|| 


fy order a | 


епейс | 


( 
| 
| 


1984] 


x= 11 H 
CALYTHROPSIS RYLSTONEA 9 
CALYTRIX "CATOCALYPTA" 11 


JOHNSON & BRIGGS—PHYLOGENETIC ANALYSIS 


WEHLIA d "P 7,8,9,11 
HOMALOCALYX 
Es pee ae x = 11,10,9 
CORYNANTHERA es 
MALLEOSTEMON MICROMYRTUS THRYPTOMENE 
1-locular 
indehiscent SCHOLTZIA spp. monad | 
ovary 3- or 2- locular monad tbrevicolpate pollen AM 
fruit dehiscent ASTARTEA 
CHOLTZIA 
st. 1 row united at base oue 
ammer stamens 


monad ovules 207 


ovules 2 


leaves spiral 


BAECKEA 
stamens reduced vüles collat. 
e зә XY 
placentas subapical 


*brevicolpate pollen 
dichasium botryoid or dichasium 
monad 
monad 


——— opposite-decussate 


х= 11 
HYPOCALYMMA 


BALAUSTION 


opposite-decussate ——34 


EN 


това: еки lost 


арте ной 


Е IGURE 10. Sketch phylogram of relationships 1 in e O alliance (not a rigorous numerical phylo- 


mportant 
nad refers to inflorescences. [Baeckea is almost ce 


e." Chromo i num 
. st. = stamens; cots. = 
rtainly a ae group, as is the 


uired the — و‎ ary Vii the 
bers are shown, and som ой 
слу неро = эз Ы 

* Baeckea latte 


(below the transverse broken line), whilst the now abandoned “Слатеіаисіит ве аге“ above the line is 
c.] 


highly polyphyletic 


and monad are used in the sense of Briggs and 
Johnson (1979), where the structure of Myrta- 
ceous inflorescences and the significance of their 

ч are treated in some detail. 
Pi i А stamens” refers to а specialized 
муун which the filaments are strongly bent at 
ја рѕ and adnate to the connective of the an- 

ers; in the extreme condition the anthers open 
uae and may have more or less confluent 
бап om Stamens were mentioned by Ben- 

) as occurring in part of Scholtzia, 
nd J. W, Green (pers. comm.) pointed out to us 
Brig D found in several species formerly 
Бесна == icromyrtus, most of which are now 

1983), n the new genus Malleostemon (Green, 


"e 


We have closely examined most of the species 
mon »Ptomene Micromyrtus, and Malleoste- 
thes oa as the single species of Corynan- 

жш some species of Scholtzia. Publications 
have re Of these by Green (1979, 1980, 1983) 
ve been most helpful. We confirm his obser- 


vations, which are particularly useful in inter- 
pretation of the gynoecium. As yet, we have sam- 
pled the other genera much less intensively, and 
will need to pursue comparative studies. Some 
of the genera need redefinition. We have taken 
Baeckea in a broad sense, which will not hold. 
Baeckea sensu lato includes a variety of diver- 
gent lines with respect to androecial and gynoe- 
cial modification, and several states of inflo- 
rescence reduction, as well as some diversity in 
pollen type. We perceive Micromyrtus and 
Corynanthera as arising from a single line; this 
is not to deny tl grade leav 
ing a paraphyletic residue) of кош 
which is characterized by its highly modifi 
locular anthers (Green, 1979). These genera are 
evidently most closely related phylogenetically 
to a different portion of Baeckea from those por- 
tions to which 7Aryptomene and Astartea are 
respectively allied. Other groups within Baeckea 
may be equally worthy of distinction (Briggs & 
Johnson, 1979; M. E. Trudgeon, pers. comm.) 


748 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


and indeed were distinguished by the discerning 
nineteenth century botanist Schauer (1843). The 
T taxonomy of the Australian Myrtaceae, 

particular, has been largely fixed in the mold 
нн dn Bentham (1867) over a century 
ago. Subsequent authors have mostly simply used 
Bentham’s classification and ignored his sage re- 
marks; these indicate how tentative his decisions 
were in fact, as seen by himself. Bentham would 
probably do something quite different, in many 
cases, on today's evidence. 

We also tentatively recognize “‘Catocalypta”’ 
as a distinct entity from Verticordia, though there 
are remarkable parallel developments in these, 
and some species may not be satisfactorily placed 
in either group. 

Homoplasy must indeed be very widespread 
— пи ашина. Even ин a distinctive fea- 


di USL поо 
than once, since it occurs onlyi in part of Scholtzia 
and also in the two new genera, which would 
appear to have arisen near the base of Scholtzia. 
Doubtless the explanation lies in the prospec- 
tively adaptive previous condition of the anthers 
and in parallel evolution of pollination syn- 
dromes. 

Figure 10 shows six separate lines crossing the 
boundary between the so-called Baeckeinae and 
the traditional *Chamelaucioideae." This stage 
is marked by the reduction of the Ovary to a 
unilocular condition, developing into an inde- 
hiscent fruit. Each of these postulated phylads is 
supported not only by the characters shown on 
the diagram but by overall resemblance, much 
of which has been noted by previous authors. 
We have little doubt of the general affinities 
shown, although more detail will doubtless 
emerge. 

Thus the so-called subfamily *Chamelaucioi- 
deae" is a highly polyphyletic grade taxon resting 
on one limited character syndrome. As such, it 
is not only unacceptable as a subfamily but we 
would not now uphold our equivalently circum- 
scribed Chamelaucium suballiance (as distinct 
from our more inclusive Chamelaucium alli- 
ance); the situation calls for a new classification. 
Further comments are given below (4.4) 


4.4 SYSTEMATIC IMPLICATIONS IN MYRTACEAE 
The implications of this analysis for formal 
classification will be largely evident from Figures 


9 and 10. More detailed study, down to lower 
taxonomic levels, is being pursued. 


сессия апа Неїегорух ШШШ аге ed 
ognized as families for reasons already advanced. 
Within the Myrtaceae proper, phytoğéog 
and possible phytogeographic history have been 
briefly discussed (4.2.2; Johnson & Briggs, 19813). 
They should be considered in relation to the sug- 
EE phylogeny. 

It is clear from the analysis that our earlier 
ес of two of the traditional three 
subfamilies must be abandoned. We hinted at 
this at the time (Briggs & Johnson, 1979), but 
subsequent study of a wider range of features 
demonstrates that the Acmena group must have 


a separate origin from the remainder of the tra- | 


PM EH MH 


ditional Myrtoideae, and that the Arillastrum and | 


Eucalyptus groups are likewise remote from oth- 
er members ofthe traditional Leptospermoideae. 
These subfamilies have been recognized on the 
features of succulent and indehiscent versus dry 


f 


and dehiscent fruits. Supposedly supporting | 


characters show a correlation with these, as might 


indeed be expected since they often characterize | 


subgroups that are numerous in genera an or 
species. Statistics of numerical predominance, 
such as have been accumulated by Schmid (1980) 
may indeed show correlations with phylogeny, 
but they are not a logical basis for deducing itor 
for a systematic arrangement that attempts (0 
reflect phylogeny. This is obvious from 4 con- 
sideration of the evolutionary process. In fact 
the correlations in all these cases are impe ect 
as again we should expect. P 

A fuller rationale for a revised system within 
the Myrtaceae must await further investi 
and will have to be presented elsewhere, but 2 
characters indicated in Figure 9 аге among 
most significant, although many о 
not been used in formal taxonomy О 
up to the present. The internodes 0 


f Myrtaceae 
n the phy- 


the implications of such a tree form аге disc 


f them havê 


2.6). | 
under the Myrtales (3.2.6) б hypoth 


Consequently, clear-cut sister-grou 
eses cannot be put forward with great con - 
Such situations should not be in the least SU 
prising, and indeed seem to show up when "n 
large groups are investigated phylogene 
Polhill et al. (1981) give an excellent i 
of phenomena of this kind in the large ап The 
plex legume family (Fabaceae sensu lato). 
are very evident in Proteaceae (Johnson 
1975) 


a 
| : nom): 
Before discussion of the overall taxo 


fidence: — 


1984] 


few comments on the groups are necessary. We 
shall work from left to right across Figure 9. 

However it may be ranked, the group here 
called Myrtoideae sensu stricto does seem to hold 
together, though we would like to analyze it more 
critically and a great deal of detailed revision and 
gathering of I hol gi linfi ti r 
needed. Some of this is under way in North and 

uth America and elsewhere. The Myrtoideae 
branch is shown as coming off among groups 
traditionally treated as Leptospermoideae. The 
three suballiances included here can be main- 
tained for the present subject to the reservations 
we expressed in 1979, particularly in regard to 
the Cryptorhiza alliance. In the Myrtus alliance, 
which seems generally to be well defined, the 
Malesian and New Caledonian genus Xantho- 
myrtus shows some rather anomalous wood-an- 
atomical characters (Ingle & Dadswell, 1953) and 
its pollen is also rather unusual (Pike, 1956). 
Nevertheless, it seems to conform in other re- 
Spects with the alliance and we can, at present, 
see no other place where it might belong. Scott 
(1978) has united Fenz/ia and M. yrtella, but these 
seem clearly distinct, though closely related. Re- 
lention of both genera may require nomencla- 
lural conservation or a new name for Fenzlia. 
We have not accepted all his conclusions, but 
и 979) is certainly correct in pointing out 

omyrtus occurs on the Australian main- 

land, for which it was not recorded in our earlier 
ess Byrnes (1982) has since indicated that 

other Australian species is referable to Uro- 
myrtus. 


don PhYtogeographically enigmatic New Cale- 
шал ушн shows a peculiar condi- 
о. зи its tetramerous flowers, when open, 
мече Eo well-marked antesepalous 
Мека numerous stamens. In fact, this ap- 
Мы. o coy by splitting of the hypanthium 
“ы g" intersepaline sinuses, thus me- 
ы эдн viding the ormerly continuous 
ма. sni ring of stamens into four false 
Wis ee Pan the appearance of these conspic- 
йы ча is so like that of taxa with true fas- 
чы, т Arillastrum or E udesmia Spp., one 
чы. at the condition is an adaptive con- 
се. Osbornia is discussed below. 
№ = Chamelaucium alliance appears to have 
8115 at the base of the perhaps paraphyletic 


JOHNSON & BRIGGS—PHYLOGENETIC ANALYSIS 


749 


Baeckea is closely allied to Xanthostemon 
(Metrosideros alliance); convergence in one or 
two features seems more likely. As stated above 
(4.3.2) we do not now uphold the two suballi- 
ances within the Chamelaucium alliance, and a 
different break-up will have to be devised in line 
with the pattern shown in Figure 10. Polyphyletic 
grade taxa are not tolerable in any attempt at 
rational systematics. 

The Leptospermum alliance itself shows no 
common stalk separate from the Chamelaucium 
alliance, and we hope to give it further attention 
with a view to defining appropriate suprageneric 
taxa. It probably does not break up as clearly as 
we accepted in 1979 into the Leptospermum and 
Beaufortia suballiances (the latter equivalent to 
“Calothamnus suballiance") (Johnson & Briggs, 

83b) 


The Backhousia group needs no comment be- 
yond our remarks of 1979, but the position of 
the mangrove genus Osbornia is somewhat prob- 
lematical. Figure 9 shows it as clearly on the same 
stem as the Backhousia alliance, in contrast to 
our earlier suggested placement in an alliance in 
the Myrtoideae sensu lato. Nevertheless, Osbor- 
nia differs from Backhousia and its ally Chori- 
carpia in many respects, as pointed out also by 
Wilson (1981). Schmid (1980) discusses the po- 
sition of Osbornia in terms of Myrtoideae and 
Leptospermoideae in their traditional senses, 
which is now irrelevant, but he is probably cor- 
rect in disagreeing with our tentative placement 
in 1979. Its association with the Backhousia group 
is not as definitely established as the phylogram 
suggests, for some alternative trees, only slightly 
longer, tend to place it elsewhere. Its position is 
something of a mystery, but it is certainly very 
distinct. 

The Metrosideros alliance comes out as some- 
thing of a basal group, rather than as a well- 
defined sister-group to others in the family. Very 
useful studies by Dawson (1970b, 1970c, 1972a, 
1972b, 1972c, 1972d, 19752, 1 
1978b) tribute to our knowledge of it, but that 
author does not present his results in the context 
of phylogenetic analysis. Wilson (1981) and also 
Wilson and Waterhouse (1982) have studied some 
groups intensively, and Wilson is tinuing this 
work. As with all basal groups, classification by 
Hennigian principles is difficult and practically 
unusable, so one may need to compromise rather 
than insist on holophylesis as a necessary con- 
dition for taxonomic entities. This applies both 


- 


750 


internally and with regard to better-defined groups 
that can be seen, in a sense, as arising from within 
the Metrosideros basal complex. This would im- 
ply that the Metrosideros alliance is a paraphy- 
letic group in the sense of Ashlock (1971), though 
not necessarily in that of Nelson (1971). 

The suballiances within the Metrosideros group 
do need reconsideration, especially in the light 
of several new genera from the northeast Aus- 
tralian rainforests, — study by Wilson and 
Hyland (pers. com 

We still bri б likely that Basisperma be- 
longs phylogenetically with members ofthe Kaz- 
ia suballiance. Wilson and Waterhouse (1982) 
refer Basisperma to the affinity of Ristantia, a 
genus of very different facies that has been as- 
sociated with the Lophostemon suballiance sensu 
lato but is rather anomalous there. In the light 
of other character-states, we suspect that the sin- 
gle large seed and placentation are convergent in 
these otherwise dissimilar genera. Single large 
seeds seem to be adaptations to vertebrate dis- 
persal in tropical forest in diverse lines of the 
Myrtaceae. Wilson (1982) asserts simply that our 
placement of Basisperma with Kania and its al- 
lies “cannot be justified on morphological and 
anatomical grounds,” but offers no further evi- 
dence. 

We indicated in 1979 that the Lophostemon 
suballiance was unsatisfactory and tentative 
Wilson and Waterhouse (1982) make this clear- 
er, and possibly several suballiances should e 


indsayomyrtus as 
excluded from the Metrosideros group, where they 
were formerly tentatively placed in the Lophos- 
temon suballiance. They show relationships with 
the Acmena alliance, which is itself well defined. 
These three genera are not very close to each 
other and represent tag-ends that are barely sur- 
viving as phylads. The apparent former occur- 
rence of something very like Kjellbergiodendron 
in southeastern Australia has been mentioned 
(4.2.2; McWhae, 1957). Schmid (1980) discusses 
Kjellbergiodendron in relation to the traditional 
subfamilies, and again this is scarcely relevant. 
Kjellbergiodendron would not fit in the Myrt- 
oideae sensu stricto in inflorescence, phyllotaxis, 
indumentum, or floral details, including the 
staminal fascicles. 

Schmid (1980) states that fasciculate stamens 
occur in the Myrtoideae, citing Syzygium pro 
parte (Pareugenia) but, as he Says, those species 
have many fascicles showing no definite relation 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


to the petals; this seems to be a secondary con- 
dition. In any case, бен р: isa Wu of the 
Acmena alliance, ich we show a ewhat 
more closely ul was. to Keller 
dendron than to Myrtoideae proper. The 

fascicles of Stereocaryum, which does fit in ie 
Myrtoideae, have been mentioned above. 


| 


[VoL. 71 | 


mid points out that the staminal fascicles | 


Sc 
of Kjellbergiodendron are “quite different” from 
those of Whiteod 
sistently different, but no more so than within 
groups of the Lophostemonalliance, for example. 
We do not claim that Kjellbergiodendron and 
Whiteodendron are as close as suggested by van 
Steenis (1952); quite a lot of their resemblances 
are probably either symplesiomorphic or habital 
parallelism. But Schmid’s statement that “pal- 
ynologically Whiteodendron is clearly lepto- 


©“. 


spermoid,” in contrast to the supposedly “my! 


| 


endron. They are indeed con- | 


toid” pollen of Kjellbergiodendron, cannot be | 


sustained in d terms. The syncolporate pol- 
len condition shown in Kjellbergiodendron is 
probably а within the family (4.2.1) and 
is seen in some members of almost all alliances. 
Apocolporate conditions, as in Whiteodendron, 
must have been multiply derived and also ne? 
up in various groups. Again, use of weight 0 
numbers or “prevailing conditions” i a 


genetic 
the Go s of phylogenetic taxonomy. 
mena alliance needs further attention 

at the generic level. Waterhousea (No. 123" 
nus nov.” of Briggs & Johnson, 1979), by 
tinctiveness of which was pointed out to US 
J. T. Waterhouse (pers. comm.), has since 
described by Hyland (1983). It is not пон 
as we had thought. Syzygium itself may We 
clude two or three rather di lines. inm 
we agree that the forms with reduced flo рУ 
included in Syzygium by Schmid (197200 si 
not likely as such to have supportable ¢ claim 

eneric separation. : 
Т Тһе E picture and the mass of ev! 
dence, including wood-anatomical ang ized 
well as the unitegmic ovular condition in va 
ium (Tobe & Raven, 1983a), argue very $ 
against Schmid’s continued association = 
вета sensu stricto and Syzygium sensu la ue 

“тоге closely than distantly related gi 58 
ataceae.” Schmid (1980) himself justifies d 
definite statement with the words “my СО 
atism still demands [it]." We cannot Se 
conservatism weighs against evidence. EN 

Finally, we come to what we have pre 


of “Еи 


how 


| 


1984] 


called the Eucalyptopsis and Eucalyptus alli- 
ances. Further study and better material have 
convinced us that Arillastrum is not, as we pre- 
viously thought (Pryor & Johnson, 1971, 1981; 
Johnson, 1972, 1976; Briggs & Johnson, 1979; 
Johnson & Briggs, 1981а) a member of the An- 
gophora suballiance of the “Eucalyptus alli- 
ance.” Rather it agrees in many ways, namely in 
leaf venation and hair-type as well as in flower, 
fruit, and seed features, with the other three 
monotypic genera previously referred to the Eu- 
calyptopsis “alliance” (Johnson & Briggs, 19835). 

onetheless, Arillastrum and its allies are now 
showing a fairly definite relationship to the three 
suballiances that constitute “the eucalypts," i.e., 
Eucalyptus of botanical tradition together with 
Angophora, and may be best included with them 
as a fourth suballiance (eventually subtribe) 
(Johnson & Blaxell, in prep.). 

These eucalypt genera have been discussed 
elsewhere by one or both of us in the works cited 
above. We here reiterate that they fall into three 
groups, each ch = Р, LES | 1.1 1 1 + 
with some doubt as to the sequence of divergence 
of the groups themselves. 

Three alternatives are shown in the phylogram 
(Fig. 9). The shorter of these on our character 
scoring shows a primary divergence that asso- 
ciates two of the “eucalypt” groups with the Ar- 
lastrum group on the one hand, while the Eu- 
calyptus “suballiance” (consisting of Eucalyptus 
sensu stricto, **7diogenes," and **Gaubaedq") is its 
Sister-group. If this is correct then the “euca- 
lypts” (if one excludes the Arillastrum group from 
that category) are polyphyletic. This may indeed 
be the case and the hypothesis calls for testing. 
On the other hand, the other two alternatives 
(one of which also implies polyphylesis for the 
ao are longer by only one step. We may 
i ve given too much weight or the wrong po- 
arity, at least locally in this portion of the phy- 
ы” to the characters of ovular condition 
ме 5 a 54) and/or presence of crystalliferous 
Et testa (61). If these were altered, the 
кад engths would change and a further al- 
"à vel hypothesis would be favored in which 
т т group separates first from the 
the > from which the Е ucalyptus group is 
dis to diverge. On such variant scoring ad- 

Slightly longer trees exist, including those 


t 3^ 

dis three distinct subgenera of the psyllid G/y- 

а (see below) аге respectively specific to the 
Ymphyomyrtus and E ucalyptus groups, but this 


JOHNSON & BRIGGS—PHYLOGENETIC ANALYSIS 


With the topologies shown in Figure 9. Two of 


TM 


genus is not known to occur on members of the 
Angophora or Arillastrum groups. This might fa- 
vor the alternative that associates the Symphy- 
omyrtus and Eucalyptus groups, but one must 
bear in mind that the third subgenus of G/ycaspis 
occurs on a variety of Myrtaceous hosts taxo- 
nomically remote from the “eucalypts” (К. 
Moore, pers. comm.; К. Taylor, pers. comm .). 
The ten or eleven genera (segregating the dis- 
tinctive section Sebaria from Symphyomyrtus; 
and see under **Gaubaea," below) that we now 
gnize in principl g the “eucalypts” will 
be formally established elsewhere. They are more 
clearly distinguished than some traditional gen- 
era in the Myrtaceae, and indeed in other fam- 
ilies, that no one challenges. Only in one case do 
we believe that there may be some doubt as to 
assignment to a *'suballiance." The two species 
that we have placed in **Gaubaea," endemic in 
Queensland, definitely do not fit in the Ango- 
phora suballiance of the Symphyomyrtus sub- 
alliance. They are very different from Eudesmia, 
despite their association with that group by Carr 
and Carr (1968). However, we have placed 


к 
1 1 1 + 


have some features of that group. Supporting evi 
dence from host-group-specific insects, especial 
ly Glycaspis of the Psyllidae (Hemiptera), such 
as exists for members ofall other eucalypt genera, 
is as yet lacking for ““Gaubaea” (K. Moore, pers. 
comm.) although a less host-specific psyllid group 
is recorded from Symphyomyrtus, “Саиђаеа,” 
Callistemon, Melaleuca, and Leptospermum (K. 

aylor, pers. comm.). Nor is there chemical evi- 
dence from flavonoids (W. E. Hillis, pers. comm.) 
to give definite support or otherwise to its sug- 
gested position. The terpenoid essential oils also 
remain to be studied (E. Lassak, pers. comm.). 


(Moore, pers. comm.) and chemi 
(Hillis, pers. comm.) do support a closer rela- 
tionship of *Idiogenes" with Eucalyptus sensu 
stricto than with any other eucalypt genus. 

4.4.1 The failure of the subfamilies. Since 
both the traditional three subfamilies and our 
later two subfamily divisions in Myrtaceae are 
untenable, what can be done about infrafamilial 
classification? We hope to formalize a system of 
tribes and subtribes, more or less equivalent to 
our informal scheme of alliances and suballi- 
ances. Such a scheme will have to differ from 


792 


that put forward іп 1979 in several ways upon 
which we are not yet ready to decide. By the very 
nature of phylogenetic divergence, and the per- 
sistence of various tag-ends, as well as by the 
ever-remaining uncertainties, no such system can 
be unequivocal. Nature does not comply with 
our classificatory desires. 

It is doubtful that any new taxa at the level of 
subfamily will be satisfactory, and we strongly 
advocate the abandonment of the subfamilies 
hitherto recognized on the grounds that contin- 
ued reference to them is misleading in setting a 
phylogenetic context and is phytogeographically 
irrelevant 


5. CONCLUSION 


Phylogenetic analysis of the 19 taxa and 77 
Уа coded characters used for the study of 


Бе in еа ы used aR а 
he CLAX approach, though designed to di- 
aa such problems, does not yield a unique 
phylogenetic hypothesis in which we can have 
confidence. This is indeed to be expected. It does 
point up regions ог. comparative оно апа 
uncertainty es upon which 
reasonable alternative scenarios к о. hy- 
potheses in semi-narrative form) can be built. 
These scenarios provide a basis for more detailed 
nayiogeographig and iyd hypotheses, 
ich are not carried far her 
Loue dee and pri th must have been 
rife at all levels (and consequently all periods) in 
the history of Myrtales and Myrtaceae, and a few 
possible apparent evolutionary reversals (not 
) een brought 


necessarily g 
to attention. 

Formal taxonomic treatment is theoretically 
compatible with divergent phylogenetic tree 
structure, as indeed it is with any directed tree 
structure equivalent to an ultrametric (Rohlf & 
Sokal, 1981). In practice, the uncertainties of the 
tree structure, as well as the number of branching 
levels, render a complete formal hierarchic cor- 


"subfamily Chame- 
laucioideae" of the Myra but there are a 
number of others. 

We agree with Le е majori of contributors to 
th ofthe Myr- 
tales and agree on many of the trends and lines 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


of change and divergence. Efforts to resolve un- 
certainties have especially concerned Melasto- 
mataceae, Memecylaceae, Crypteroniaceae, Al- 
zatea, and Rhynchocalyx; they have been 
discussed in the body of this paper. 

We conclude that Myrtaceae form a coherent 
and holophyletic group, and that Heteropyxi- 
daceae and Psiloxylaceae diverged from the an- 
cestral lineage of Myrtaceae at an early stage. 
These relict groups can be reasonably treated as 
families. The family Myrtaceae sensu stricto is 
unique in the Myrtales in having its greatest fun- 
damental diversity in the Australasian region. 

Infrafamilial phylogeny in the Myrtaceae is be- 
coming clearer, but needs more detailed study. 
As seen here, it is decidedly inconsistent with 
recognition of the two traditional subfamilies 
Myrtoideae and Leptospermoideae, not to men- 
tion Chamelaucioideae. A formal system of tribes 
and subtribes may be desirable but will be dif- 
ficult to apply with both certainty and consisten- 
cy. For the time being we recommend use of our 
informal “alliances” and ‘‘suballiances” (Briggs 
& Johnson, 1979; Johnson & Briggs, 1983b), 
subject to the caveats and modifications in sec- 
tion 4. 

As гриџишељене and indeed general evolution- 
ary understanding improves, change in forma 
taxonomy is inevitable. The present analysis and 
proposals will not be the last word, probably even 

on our own part. 


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evolution бо “Acta Biotheor. 31: 3-28. 

WEBER, W. A. Mnemonic three-letter acro- 
nyms for the families of vascular plants: a device 
for more effective herbarium curation. Taxon 
74-88. 

WELLE, B. J. H. TER & J. KOEK-NOORMAN. 

Wood anatomy of the Пливи Melastomata- 
сеае. Blumea 27: 335—394. 

WILSON, PETER G. 1981. A taxonomic revision of the 
Metrosidereae. Ph.D. dissertation. University of 
New South Wales. (Unpublished.) 

1982. Additions to the genus Kania (Муг- 

taceae) in Malesia with notes on Cloezia. Blumea 

28: 177—180. 

. WATERHOUSE. 

genus Tristania R.Br. (My 

neous assemblage of five genera. Austral. 

30: 413-446. 


1982. A review of the 
rtaceae): a heteroge- 
1. J. Bot. 


ои 


—-— 3299 


ALZATEACEAE, A NEW FAMILY OF MYRTALES IN 
THE AMERICAN TROPICS! 


SHIRLEY A. GRAHAM? 


ABSTRACT 


The suggested affinities of the New World tropical genus A/zatea have included eight families in 
five orders since its discovery in the eighteenth century. Until recently, knowledge of the genus has 
been superficial, primarily limited to macromorphological features. No 1 
recently published and current research in anatomy, embry 
distics of Alzatea and closely related genera allows 


t n 
1 cestral position with respect to the pollen of close associates. 
Parietal placentation and transeptal vascular supply of the ovary and anatomically simple seed relate 
Alzatea to Di L |] гр 1 1 1 у 4 < . 


between Alzatea and Rhynchocalyx are deemed sufficient to justify establishment of the family Al- 
t ants of Alzatea with large, sessile leaves from Central America are recognized as А. 


zateaceae, 
verticillata subsp. amplifolia 8. A. Graham, subsp. 


Alzatea is an enigmatic genus of Central and 
South America whose suggested affinities, since 
15 discovery in the eighteenth century, have in- 
cluded eight families in five orders. The genus is 


г ; ар 
От particular families as arguments for cer- 


чо; of relationships. The past several years 


теу, there has been an increased in- 
tive ы the genus stimulated by the collabora- 
whack тен of the Myrtales, the order to 

zatea most certainly belongs. New ob- 


nov 


servations and data of diverse types for A/zatea 
and related families now allow an evaluation of 
the phylogenetic and taxonomic position of the 
genus in the Dicotyledoneae in a more complete 
way than was possible previously. The evidence 
for A/zatea's position as a monotypic family of 
the order Myrtales is assembled from personal 
observations and the extensive studies of several 
specialists, with much of the information gen- 
erated since the Myrtales symposium of the XIII 
Botanical Congress in 1981. Th 


cromorphology, palynology, embryology, anat- 
omy, and cladistics as the basis for recognizing 
the new family Alzateaceae. 


CHARACTERIZATION OF ALZATEA 


Macromorphology. Hemi-epiphytic shrubs 
or small trees, 2-20 m tall, with stout, gray, 
roughened trunks or sometimes trunks slender 
and reaching the forest upper story supported by 
adjacent trees; branches glabrous, opposite or 


? Hj . B . . . . 
Tae following individuals are gratefully acknowledged for information shared: Peter Raven, Hiroshi Tobe, 
às Croat, Gentry, Sandra Knapp, James Solomon, Alan Graham, and Barbara Timmerman. John 


t 
ae of Rhynchocalyx in Natal, and Joan Nowicke provided the scanning electron micrograph o 
frei àm also indebted to the curators of CR, MO, and F for loan of herbarium collections of A/zatea and 
1 nchocalyx for study. 
rtment of Biological Sciences, Kent State University, Kent, Ohio 44242. 


A 
NN. MISSOURI BOT. GARD. 71: 757-779. 1984. 


758 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 
TABLE 1. Systematic placement of Alzatea by selected authors. 

Year Author Classification 

1794 Ruiz & Pavón Santalaceae (Between genera of) 

1825 Candolle, A. P. de Celastraceae 

1826 Blume elastraceae, near 

1845  Planchon Lythraceae 

1862 Bentham & Hooker Celastraceae 

1868 Candolle, A. L. P. P. de Crypteroniaceae 

1872 Miers Rhamnaceae 

1892  Loesener Celastraceae, doubtfully 

1911  Hallier ythraceae sensu lato 

1918  Hallier Melastomataceae sensu lato 

1942  Loesener Flacourtiaceae 

1955 Willis Celastraceae 

1956 MacBride Rhamnaceae (or Clusiaceae or Icacinaceae) 

1965  Lourteig Lythraceae 

1966 Airy Shaw Lythracea 

1967 Hutchinson Flacourtiaceae 

1975 van Beusekom-Osinga & van Beusekom Crypteroniaceae 

1981  Cronquist Lythraceae, questionably 


ПН E 


verticillate, distinctively purple-red, peeling, be- 
coming red-brown with age; stems of the inflo- 
rescence distinctly 4-angled to narrowly winged, 
the young branches scarcely 4-angled, the mature 
branches round in cross section; nodes enlarged, 
especially knobby when branches are verticillate; 
leaf scars half-round to nearly circular, the base 
slightly raised, the bundles forming a crescent, 
U-shaped, or nearly closed-circular scar. Leaves 
mostly clustered at the ends of the branches, op- 
posite, less often verticillate, simple, entire, stip- 
ulate, the stipules axillary, 2 to a few in the axils 
at the base of the petiole, the stem wings of the 
inflorescence also extended at the nodes into stip- 
ule-like projections; petioles none or short, thick, 
deep purple-red, to 13 mm long; blades oblong- 
obovate, elliptical, or oblong-oval, thick, leath- 
ery, lustrous above, 50-145 mm long, 25—100 
mm wide, with blades of terminal leaves smallest 
and mostly about 70 mm long, 40 mm wide, the 
bases variable, attenuate to acute or rounding, 
commonly acute, the apices rounding, occasion- 
ally retuse, the veination brochidodromous, the 
secondary vein pairs 16-22, parallel, oriented at 


cyme subtended at the base by small fugaceous 
fertile bracts, i.e., the bracts themselves sub- 
tending buds. Flowers actinomorphic, 5(-6- 


merous, apetalous, bisexual, hemi-epigynous 


floral tube leathery, green to yellow, conical in 
bud, open-campanulate at anthesis, 4-6 mm long, 
4—7 mm wide, the thick, persistent, valvate lobes 
3 mm long, extending nearly to the base of the 
floral tube, the interior surface of the lobes Ir 
regularly thickened and fleshy; nectary-disc | p 
wide, lobed, extending from the ovary 10 t Е 
sinuses of the calyx lobes. Stamens 5, situat 


: ut- 
in the floral tube at the sinuses of the lobes. p" 


tending out of the calyx between the lobes. А 
simulating petals, the bisporangia PM 
horizontally along the broad terminal end о scing 
anther on each half of the connective, dehi rally 
longitudinally. Gynoecium slightly vil 
flattened, with a capitate stigma and stout, , ulaf. 
style 1 mm long: ovary bicarpellate, bilo’ 


К ч inating 
placentation parietal, the placentae term 


ing; ovules horizontally imbricate in 


== о 


mma gm 


Me 


"Y. 


o À—Á—— € 


GRAHAM—ALZATEACEAE 


759 


et ч 


FIGURES 1—7. Alzatea verticillata.— 1. Short-shrub (2-3 m) habit of A. verticillata subsp. amplifolia, Knapp & 


Kress 4336, on Cerro Tüte, Panama. Leafy 


branch in the lower right foreground belon 


ength, 8 
8331 (F). Actual diameter, 22 um.— 6. Branched sclereids of the leaf palisade tissue. Actual lengths, 


eptum (arrow) 


mm. — 5. Pollen of A. verticillata subsp. verticillata, 


um.— 7. Fertile seed with central embryo. Actual length, 2 mm 


vertical rows. Fruit an indurated, loculicidally 
dehiscent, reddish brown capsule, obcordate, 
M compressed-flattened, to 8 mm long, 
кы with raised horizontal venation ex- 
2 8 outward from the central septal vein on 
e Mn subtended by the persistent, erect to 
a Calyx lobes; remnants of the style per- 
Er „ај apex of each valve above the central 
e дан S numerous, crowded in the capsule, 
" ddish : per locule, thin, flat, the sterile seeds 
мей, ү" with roughened surface, the fertile 
Mi Ow-brown, obliquely oblong to lunate, 
tral p. 1-1.5 mm wide, the embryo cen- 
membra e гше seed, straight, encircled by the 
slightly Em wing, the cotyledons oblong to 

у spathulate, the stalk conical, directed to- 


ward the micropyle; endosperm not apparent. 
Figures 1–7; see also Dahlgren and Thorne (1984, 
Fig. 11), for general habit and floral and fruit 
morphology. 

Ovary morphology and anatomy. Ovary bi- 
carpellate, bilocular, and bilateral, at anthesis 3 
mm | wide, with suggestion of vena- 
tion apparent on outer walls, particularly in the 
center of each slightly compressed side. Venation 
consisting of a dorsal and ventral supply; dorsal 
bundle one per carpel, with a few short branches 
only and independent of the ventral supply; ven- 
tral bundles of opposing carpels distinct, posi- 
tioned laterally in the septum, two on each side 
of center in each half septum; ventral bundle 
branches traveling + horizontally through the 


5 


760 


. Septal plane, with 

split septum and basal septal hole.—c. Cross-section 

at mid to upper ovary level; paired ventral veins and 

dorsals represented by dark circles, placental regions 
tuated to indi positi i carpel wall 

d. Cross-section at level of basal opening. e-g. Dia- 


am 


Loculicidal plane.— f. Septal 
tum.—g. C 


septum to supply the ovules and carpel walls. 
Septum incomplete at the base due to the pres- 
ence of a central opening in the basal fourth of 
the septum, septal margins meeting above the 
opening, but free, not fused at anthesis. Placental 
region spreading laterally on the carpellary walls, 
broad, to 1.5 mm wide, terminating ca. | mm 
from the apex of the ovary. Ovules stacked hor- 
izontally in vertically staggered rows and super- 
posed in the locules. Figure 8a-d. 

The capsule of A/zatea has been described else- 
where as unilocular with a false septum devel- 
oping from the walls ofthe capsule inward as the 
fruit matures (Lourteig, 1965). The half septa 
with basal opening are, in fact, present in the 
young ovary, their free margins parallel and 
touching. They separate with dehiscence and 
subsequent opening of the capsule. 

Seed morphology. Seeds bilaterally com- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


pressed, horizontally layered in the capsule. Fer- 
tile seeds yellowish brown when dry, irregularly 
rectangular to lunate, frequently with a tail at the 
chalazal end, 2-3 mm long, 1-1.5 mm wide; em- 
bryo central in the seed and winged all around, 
straight with plane, oblong to spathulate coty- 
ledons, the stalk conical, 0.25—0.33 the length of 
the embryo, the raphe bundle ending at the chala- 
za. Outer integument (testa) two-layered, the cells 
reticulate-scalariform, the out layer of cells 
elongate with thin, undulating walls, composing 
most of the seed wing, the inner layer crushed. 
Inner integument (tegmen) two-layered, both 
layers crushed at seed maturity. Sterile seed (ca. 
Ъз of total seed) reddish brown when dry, pri- 
mar ily crescen t-shaped with curved tail, 2-3mm 
long, 1-1.5 mm wide, 0.5-1 mm thick on the 
convex side; raphe bundle on concave side, end- 
ing at the chalaza. Testa of densely packed, ra- 
dially elongate palisade cells with straight walls 
on the convex side, the remainder of seed coat 
composed of irregularly arranged, crowded, short, 
cuboidal or irregularly shaped cells. Central cav- 
ity present, no embryo development apparent. 
Figure 7. ; 

Pollen morphology. Pollen prolate-spheroi- 
dal, amb circular; tricolporate, colpi meridion- 
ally elongated, equatorially arranged, equidis- 
tant, straight, ca. 14 um long, extending within 
4—5 um of pole (PI 0.22), P/E 1.1, margins in- 
vaginated and slightly diffuse, tapering to acute 
apex with some sexine modification (gran 
tions) extending to poles, ektexine bridge Ee 
pore, pore circular, diam. 3-4 ит, sit 
midpoint of colpus; wall 1.5-2 um thick, psila 
bordering colpi, verrucate-areolate in elongat 
mesocolpal region suggesting faint вир ШЫ 
colpi; tectate; 18-22 um by 16-20 um. he 
scription was provided by Alan Grape 
partment of Biological Sciences, Kent State 
versity, Kent, Ohio. Figure 5. 

Tue above description is based on Klug i е 
(Е) and Woytkowski 8331 (F), both of e 
American origin with fully developed poe! wes 
functionally bisexual flowers. Pollen не 
both collections is 97%, based on a count pm i 
grains stained in cotton blue in lacto-phe! vei 
Central American plants pollen fertility 15 ar 
low and few grains are well-formed. bes 
tility does not exceed 3696 in the Costa y. No 
collections examined by Tobe (unpubl. data ams 
fertile pollen has been observed in the Pan 
collection of Knapp & Kress 4336 МЕ and 

Pollen of A/zatea has also been descr 


—————— 
ЦРНА  V— CC —— ———— € Ó 


| 
| 


-— 


1984] 


illustrated by Muller (1975) as part of a survey 
of the pollen of the Crypteroniaceae. 

Anatomy. The following account is con- 
densed from the detailed investigations of van 
Vliet (1975), Baas (1979), and Keating (1984). 
I f Qt ta ahavial nnb 11 


P 1 
VO Cally 


cyclocytic with subsidiary cells slightly sub- 
mersed below guard cells. In transverse section, 
blade dorsi-ventral, 380—440 um thick. Adaxial 
epidermal cells mainly square, larger than the 
abaxial ones. Adaxial, 1-2 layered hypodermis 
present, limited to each side of midrib or ex- 
tending over midrib. Palisade tissue 2-layered 
with abundant large, short-branched asteroscler- 
eids. Spongy mesophyll compact, mostly scleri- 
fied. Midrib a flattened cylinder with abaxial and 
adaxial plates and a central lacuna, secondary 
veins circular in outline, collateral. Scattered 
druses present in lower mesophyll and near the 
veins. Figure 6. Node: Trilacunar with three 
traces. Stem: Epidermal cells square. Cortex of 
parenchyma interspersed with stone cells and 1– 
4 more or less centric cortical bundles in each 
corner of the 4-angled twig. Cork arising next to 
perivascular sclerenchyma, the phellem cells in 
late stages forming alt ing layers of flat, thin- 
walled cells and square cells with unilateral wall 
thickenings. Primary phloem mostly sclerified in 
older material. Secondary phloem of sieve tubes, 
companion cells, chambered parenchyma and 
infrequent phloem fibers. Secondary xylem with 
faint growth rings. Vessels diffuse, 36/mm2, sol- 
lary and in radial multiples of 2-4. Vessel mem- 
bers (330-)530 and 570(-750) um long, mostly 
with long tails. Perforations simple in oblique 


ands. Vessel-ray pits 
large, simple, reticulate to scalariform. Thin- 
walled tyloses present in some vessels. Fibers 
(540-)960(-1240) um long, walls thin, minutely 
bordered to simple pits, septate and/or gelati- 
nous. Gelatinous fibers in tangential bands in 
young material. Parenchyma very scanty para- 
tracheal, Rays heterogeneous I-II type, 1-3 se- 
a usually with central portion of procumbent 
ene Primary xylem and internal phloem in a 
inuous ring. Pith of lignified parenchyma. 
ses abundant in chambered phloem paren- 
сћута. 
„>. Leaves of Alzatea contain ellagic 
„ flavonoid mono- and di-glycosides, in- 
М ing 3-OH flavonols. [Leaves of Hammel 6247 
O) were extracted using standard methods 


GRAHAM—ALZATEACEAE 


761 


outlined by Bate-Smith (1962). A chromato- 
graphic R, value of 0.32 was obtained in Forestal 
solvent, after ethyl acetate extraction. Additional 
leaf material extracted in 80% methanol was 


A 
HOAc-H,0; 3:1:1) and (2) 15% HOAc. The TLC 
patterns suggest the presence of flavonoid mono- 
and di-glycosides. Two-dimensional plates, de- 
veloped for the hydrolized material, showed the 
presence of 3-OL flavonoids. Contributed by B. 
Timmerman, Institute of Arid Land Studies, 


Myrtales, an order especially characterized by 
the presence of ellagic acid and tannins (Bate- 
Smith, 1962; Hegnauer, 1969). 


PROPOSED RELATIONSHIPS 


The relationships suggested for A/zatea en- 
compass eight families in five orders of two sub- 
classes (Table 2). Obviously this problematic ge- 
nus displays a number of floral and vegetative 
characteristics widespread within the dicotyle- 

ons, especially in the subclass Rosidae. Such a 


tures which supply limited or no useful infor- 
mation about its near relationships, or have fo- 
cused on one or two parallel or convergent 
specializations while ignoring a preponderance 
of dissimilarities. Most proposals of relationship 
were made prior to the availability of data from 
anatomical, palynological, embryological, and 
chemical information about A/zatea. When all 
current evidence is assembled, few taxa are se- 
rious contenders as close relatives of the genus. 


DISTANT RELATIONSHIPS AND 
NON-RELATED FAMILIES 


Placement of A/zatea in the Flacourtiaceae as 
a separate tribe or subfamily was first suggested 
by Loesener (1942), who excluded the genus from 
his monograph of the Celastraceae. Loesener's 
suggestion was followed by Hutchinson (1967) 
who established the monotypic tribe Alzateeae 
in the Flacourtiaceae to accommodate it. The 


in the Violales and are highly diversified (Cron- 
quist, 1981), so that several A/zatea features can 
be found within this diversity. However, these 
are attributes of wide occurrence in flowering 
plants and even collectively are useless as indi- 


762 


TABLE 2. Summary of family placement previously 
suggested for Alzatea, following Cronquist’s (1981) 
classification. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


Subclass Dillenidae 
Violales— Flacourtiaceae 
Theales— Clusiaceae 
Subclass Rosidae 
Celastrales — Celastraceae, Icacinaceae 
R nales— Rhamnaceae 
Myrtales— Crypteroniaceae, Lythraceae, 
Melastomataceae 


cators of close relationship. For example, in A/- 
zatea and the Flacourtiaceae there are trilacunar 
nodes, vessel elements with simple perforation 
plates, tricolporate pollen, parietal placentation 
(probably the character most influencing Hutch- 
inson's placement of Alzatea in the Flacourti- 
aceae), and bitegmic, crassinucellate ovules. On 
the other hand, the family lacks such important 
Alzatean (and Myrtalean) features as internal 
phloem, presence of ellagic acid and flavonols in 
the leaves, and in contrast to A/zatea primarily 
displays alternate leaves with paracytic stomates, 
imbricate sepals and petals, free styles and stig- 
mas, and seeds with abundant fleshy endosperm. 
No alliance of A/zatea and the Flacourtiaceae is 
acceptable by reason of these major morpholog- 
ical, anatomical, and chemical differences. 
Affinity to the Clusiaceae was postulated only 
because of similar vegetative morphology. Where 
Alzatea and Clusia grow side by side, as in Pan- 
ama, the similarity in leaf form and general habit 
is striking (S. Knapp, pers. comm.). The family 
Clusiaceae differs from Alzatea, however, in an 


not produce ellagic acid (Cronquist, 1981 ). They 
commonly have a 3-carpellate, unilocular ovary 


[Vor. 71 


with few unitegmic, tenuinuellar ovules, and a 
solitary seed with abundant endosperm, features 
absent from A/zatea. 

Alzatea was first associated with the Celastra- 
ceae by A. P. de Candolle (1825), followed by 
Bentham in Bentham and Hooker (1862), who 
chose to ignore Planchon’s view (1845) that the 
genus ought to be in the Lythraceae, not the Ce- 
lastraceae. In a later volume of the “Ргодгот- 
ous" (1868), A. L. P. P. de Candolle removed 
Alzatea to the Crypteroniaceae following Blume 
(1826—1827). Loesener (1892), regarded Alzatea 
of doubtful membership in the Celastraceae. In 
his later treatment of this family (1942), after 
reading Hallier's (1911) more extensive descrip- 
tions of the genus, he excluded Alzatea altogeth- 
er, suggesting instead that it be accommodated 
in the Flacourtiaceae, as a new subfamily or tribe. 
Besides lack of internal phloem, the Celastraceae 
have axile placentation, a major reason Loesener 
excluded Alzatea from the family. In addition, 
the sepals and petals are mostly imbricate, and 
the seeds are often arillate with abundant en- 
dosperm. Anatomically, the family differs from 
Alzatea in the presence of unilacunar nodes an 
secretory canals in the phloem. Even though the 
Celastraceae is a rather diversified family with 
several highly distinctive genera, it diverges from 
Alzatea in too many major characters to be con- 
sidered the appropriate family for the genus. 

Possible association of Alzatea with the Icac- 
inaceae was suggested by MacBride ( 1956), but 
no specific reason was given to support this view. 
As with the Celastraceae, the number of mor- 
phological and anatomical differences are чє 
great for the family to merit serious consider 
ation. е 

The family Rhamnaceae was thought а p 
able, if perhaps temporary, repository for pe s 
nus by Miers (1872) by virtue of its antepeta p 
stamen condition. Miers regarded alma А 
gether with Crypteronia, and possibly sie Me 
rataxis (Lythraceae) as a “peculiar group W - 
could be positioned in the Rhamnaceae as 4 П i 
tribe, the Crypteronieae. Floral morpho of 
the family exhibits some similarities to tha е 
Alzatea, e.g., 5-merous flowers in axillary e 
stamens alternating with sepals, the sepals 0 


i i i occurs 10 
' ‚ interior surface as 
with a raised, fleshy 


acking 


specialized features in which the family 


: the 
from Alzatea. Most distinctive of these are 


| 
| 


| 


— " ый НЕ —" — P nsn 


1984] 


Rhamnaceous ovary with its single, basal, erect 
ovule in each locule; drupaceous fruits; and wing- 
less seeds with stony, multiplicative walls. The 
family also lacks internal phloem and vestured 
pitting and produces no ellagic acid (Cronquist, 
1981). Similarities may be attributed to their 
common distant ancestry in the Rosidae and par- 
allel development of like structures in different 
lines of the subclass. Total evidence excludes A/- 
zatea from the Rhamnaceae. 


COMPARATIVE EVIDENCE FOR ORDINAL, 
FAMILY, AND GENERIC RELATIONSHIPS 


Among the several orders suggested for Al- 
zatea, the Myrtales offer the only comfortable fit. 
Two anatomical apomorphies of A/zatea, inter- 
nal phloem and vestured pitting, are major de- 
finitive features of the Myrtales (Dahlgren & 
Thorne, 1984). Other characteristics of A/zatea 
prevail in the order. These include vessel ele- 
ments with simple perforation plates, opposite 
and verticillate, simple, entire leaves with broch- 
Idodromous secondary venation, ellagic acid and 
flavonol glycoside leaf constituents, rudimentary 
axillary stipules (Weberling, 1968), anomocytic 
stomata, basically determinate inflorescences, 
floral tube with floral parts on the rim, bitegmic 
crassinucellar ovules, as well as several embry- 
ological features (Dahlgren & Thorne, 1984). 

At the familial level, Myrtalean families to 
Which Alzatea has been referred have been sub- 
Ject themselves to numerous interpretations, so 
that the varying familial placement of A/zatea in 
the order has depended in part on how the fam- 
ilies were defined. Hallier (1911), for example, 


(Punicaceae, traditionally). After an “angry” let- 
€ monographer ofthe Lythraceae, Emi 
e disputing Hallier's delineation of Ly- 
Чы. Hallier decided the same genera, ques- 
M у excluding Punica, were members of the 
|91 У о Чеае-Ме]азотатасеас (Hallier, 
Ке The change was due, not as much to 

пе 5 objection, since Hallier dismissed 
IIS argument as “pre-Darwinian,” as to 
ke pw awareness of the genera Dactylocladus 
V oe nl which he found overwhelmingly 
"i ю Crypteronia and Alzatea and which 

considered Melastomataceous by their au- 


GRAHAM—ALZATEACEAE 


763 


thors. Lourteig (1965), who regarded A/zatea as 
Lythraceous, extended her definition of Lythra- 
ceae to include Crypteronia. It has also been ar- 
gued since that A/zatea, Rhynchocalyx, Dacty- 
locladus, and Axinandra, with Crypteronia 
constitute a redefined Crypteroniaceae (van Beu- 
sekom-Osinga & van Beusekom, 1975). Most re- 
cently, A/zatea has been removed from that co- 
alition of genera, with the latter three genera 
repositioned as a new subfamily of the Melas- 
tomataceae (van Vliet, 1981) and Rhynchocalyx 
comprising the monotypic Rhynchocalycaceae 
(Johnson & Briggs, 1984). 

Several Alzatean characteristics occur repeat- 
edly throughout the order in more than one fam- 
ily and must be regarded as having originated 
early in the evolution of the group or as in- 
stances of convergent or parallel evolution. Ex- 
amples of the latter include foliar sclereids scat- 
tered throughout several families (Rao & Das, 
1979); hemi-epigynous flowers seen also in the 
Crypteroniaceae (van Beusekom-Osinga & van 
Beusekom, 1975), Melastomataceae, and Myr- 


some Onagraceae, Myrtaceae, Oliniace 
с 


with the widel 21 phic features 
of the order, have been used to infer relationship 
to the families Lythraceae and Crypteroniaceae 
(and the Melastomataceae via inclusion of Cryp- 
teroniaceae in that family). 

The most recent arguments for the disposition 
of A/zatea in the Lythraceae have rested on such 
common Myrtalean characteristics as quadrat 
branches, subcoriaceous decussate leaves, 5—6- 
merous flowers, and capsular, bilocular fruit with 
loculicidal dehiscence (Lourteig, 1965). Apo- 
morphic A t i 


tean fe ted to support place- 


ment in the family, e.g., obhaplostemonous sta- 
mens with enlarged connective and apetaly are 
now believed to have evolved more than once 
in the order (Johnson & Briggs, 1984). Although 
the parietal placentation of Ammannia micro- 
carpa DC. in Lythraceae has been cited in sup- 
port of A/zatea's placement in the family, the 
placentation is not homologous in these taxa. 
Ammannia microcarpa is a highly derived her- 
baceous species whose parietal placentation is 
unique in the Lythraceae. The species bears no 
other resemblance to Alzatea. Citation of this 
species as supporting evidence for inclusion of 


TABLE 3. Comparison of Alzatea and associated genera. 


Character Alzatea Rhynchocalyx Crypteronia Dactylocladus Axinandra 
No. of species 1 1 4 1 4 
Habit Small tree or shrub, Small tree Tree Tree Tree 
hemi-epiphyte 
Habitat et, submontane Moist, wooded, sub- Wet, submontane tropical Lowland peat swamps Wet, submontane 
tropical forest tropical ravines forests tropical forests 
Distribution Bolivia, Peru, Pana- Natal & Transkei, SE Asia, Phillippines, Ma- Borneo Malay Peninsula, 
ma, Costa Rica South Africa lay Peninsula to New Borneo, Sri Lanka 
Guinea, esp. Borneo 
Branches 
Arrangement Opposite or whorled Opposite or whorled pposite Opposite Opposite 
X-sect., young Quadrangular Terete to flattened Terete to quadrangular Flattened Quadrangular + 
Leaves 
Phyllotaxy Opposite or whorled Opposite or whorled Opposite Opposite Opposite 
Stipules Axillary, divided Axillary, divided Lateral, rudimentary 2 I 
Venation Brochidodromous Eucamptodromous Brochidodromous Brochidodromous, indis- Brochidodromous 
tinct 
Inflorescence 
ype Anthotelic, paniculate Anthotelic, paniculate Blastotelic, racemose Blastotelic, racemose Blastotelic, racemose 
Position Axillary, terminal Axillary, terminal Axillary, termina Axillary, terminal Axillary, terminal 
Flowers 
Sex Bisexual (& func. uni- Bisexual Bisexual & unisexual Bisexual Bisexual 
sexual?)- 
Insertion Hemi-epigynous, Hemi-epigynous, bare- — Perigynous Hemi-epigynous, strong- — Epigynous 
barely 1 ly 
Nectary-disc Present, broad Absent Absent Absent Absent 
Merosity 5(-6)-merous 6-merous 4—5(—6)-merou 5(—4)-merous 5(—4)-merous 
Floral bracts Minute, fugaceous Minute, fugaceous раја а (2) Solitary, caducous Three, persistent (?) 
Calyx 
Lobes Thick, adaxial surface Thin, membranous Thin, membranous Thin, membranous Thin, membranous 
raised, fleshy | 
uration Persistent Persistent Persistent Persistent Evanescent in fruit 
Aestivation Valvate Valvate Valvate Valvate alvate 


9L 


Nadav) ТУЭІМУІОЯ NINOSSIW IHL ЧО STVNNV 


IL 10A] 


i o а > и — > 
TABLE 3. Continued. 
Character Alzatea Rhynchocalyx Crypteronia Dactylocladus Axinandra 
Petals 
Number 0 6 0 
Shape — Hood-like, covering — Hood-like, covering sta- + Connate, broad- 
stamens in bud, mens in bud, clawed 
clawed 
Deciduousness ES Individually — Individually As cone-shaped unit 
Stamens 
umber 5 6 4-5 5 10 
Position Alternisepalous Alternisepalous Alternisepalous Alternisepalous Episepalous & epipet- 
Filaments Thick, short, flattened Thin, long, + flattened Thin, long, terete ? + flattened Thick, short, + flat- 
tened 
Connective Conduplicate Elliptical Orbicular or nearly condu- — Orbicular Conduplicate 
plicate 
Sporangia position Terminal Lateral Lateral to subterminal Lateral Terminal 
Pollen 
Aperatures Tricolpora Tricolporate Bisyncolporate Tricolpor: Tricolporate 
Shape Prolate- spheroidal Prolate-spheroidal Bilaterally flattened Prolate-spheroidal Prolate-spheroidal 
Subsidiary colpi 3, indistin istinct 2, indistinct 3, dist 3, distinct 
Exine Faintly to Faintly verrucate to Psilate Psilate 0 ا‎ ver- Psilate to finely ver- 
psilate psilate rucate rucate 
Nuclei at shedding 2 2 
Style 
Length Shorter than ovary, Shorter than ovary, Longer than ovary, filiform ^ Longer than ovary, fili- Longer than ovary 
stout stout form 
In fruit Base persistent Base persistent Entire style & stigma persis- Entire style & stigma Non-persistent 
tent persistent 
Stigma Capitate Capitate, narrow Punctate or capitate Capitate Punctate, minute 
Ovary 
Shape Bilateral, compressed Bilateral, compressed Bilateral & compressed or Globose Globose 
globose 
Carpel No. 2, 2 2 (3 or 4) (3)4 or 5 3 (2) 
Locule No. 2 2 2 (3 or 4) (3) 4 or 5 6 (4) 


[r861 


AIVIOVALVZIV~WNVHVIO 


S9L 


TABLE 3. Continued. 


Character Alzatea Rhynchocalyx Crypteronia Dactylocladus Axinandra 
Placentation Parietal Axiie Parietal or basal Basal Basal 
Septal Fusion Not fused Fused entirely Not fused or fused basally Not fused Fused slightly basally 
Q) Q) 


Many 6(-12) 
Horizontal in staggered ver- 
tical rows or + vertical & 


Ovule No./Capsule Ca. 40-60 Ca. 40 1215 6-12 
Ovule Position Horizontal in stag- Horizontal in single Vertical & basal Vertical & basal 


vertical rows 


99L 


Fruit 
Seed 
Shape 


Embryo Position 
Seed Wing 


Seed Coat Cells 


Testa Layers 
Tegmen Layers 


Embryology 


Anther Wall Forma- 
tion 


Anther Endothecium 
мон 
Sept 


ptu 
Ovule e FREE um 
Ovule Endothelium 
Micropyle Forma- 
tion 
Embryo Sac Forma- 


gered vertical rows 
Indurated capsule 
Irregularly LM to 
lunate, ened 
entra 
Encircling embryo 


Specialized cell types 
absent 


~ N 


Dicot Type 


Ephemeral 
Non-persistent 


Multi-celled 
Absent 
Inner integument 


only 
Bisporic, Allium-type 


Indurated capsule 


Obliquely ovate, flat- 
tened 


Apical 
At micropylar end 


Specialized cell types 
absent 


Basic Type 


Ephemeral 
Persistent 


Multi-celled 
Absent 
Inner integument only 


Monosporic, Polygo- 
num-type 


basal 
Indurated capsule 


Ovoid-ellipsoid, flattened 


Central 


At micropylar or chalazal 
end 


Indurated capsule 


Narrowly ellipsoid, flat- 
tened 


Central 
? 


Woody, greatly en- 
larged capsule 


Oblong, ellipsoid, 
flattened 

Basal 

At chalazal end 


Specialized cell types 
absent 

2 initially, becoming 
3 


Dicot Type 


Ephemeral 
Non-persistent 


One-celled 
resent 
Inner & Outer integu- 


ments 
Monosporic, Po/ygo- 
num-type 


N3G3VO 'TVOINV.LOS NINOSSIW JHL JO STVNNV 


1L 10۸] 


TABLE 3. Continued. 


Character Alzatea Rhynchocalyx Crypteronia Dactylocladus Axinandra 
Leaf Anatomy 
Cuticle Granular Smooth Granular Granular 
Stomate Anomocytic Anomocytic Paracytic Anomocytic Paracytic 
Petiole Bundle Cylinder, ab- & adax- Curved arc Cylinder, ab- & adaxial messe ab- & adaxial Curved arc 
ial portions with portions with middle la- portions with middle 
middle lacuna cuna lacu 
Sclereids Present, branched Present, unbranched Present, unbranched Rai unbranched Absent 
Nodes Trilacunar, 3 traces Unilacunar, | trace Common gap, | median Common gap, | median Complete girdling 


Stem Anatomy 
Cork Origin 
Vessel Aggregation 
Vessel Member 

ngt 
Vessel-Ray Pits 
Vesturing 
Septate Fibers 
Fiber Pitting 
Axial Parenchyma 


Rays 
Phloem Crystals 


Pericycle 
Mainly radial multi- 


ples 

530 & 570 um 

Reticulate-scalari- 
form, large 

Spreading, forming 
bands on vessel 
wall 

Present 

Simple-minutely bor- 
dered 

Very scanty paratra- 
cheal 

Heterogeneous I 


Clustered in cham- 
bered parenchyma 


Cortex 
Mainly solitary 
460 & 520 um 
Alternate, small 
Spreading, forming 
bands on vessel wall 
sent 
manie o. bor- 
dered 
Scanty paratracheal to 
vasicentric 


Heterogeneous I 
Solitary, prismatic in 
paren- 


bundle 


Pericy 
Mainly db multiples 


650-900 um 

Alternate, small 

Within pit chamber & on 
pit margins 

Absent 

Distinctly bordered 

Diffuse or scanty paratra- 
cheal to vasicentric 


Heterogeneous I 
Styloids in parenchyma 


bundle 


Subepidermal 
Mainly solitary 


950-1120 um 
Reticulate-scalariform, 


arge 
Within pit chamber only 


Absent 

Distinctly bordered 

Aliform to confluent 

Heterogeneous III 
tal sa 


Crystal sand & druses in 
parenchyma 


trace, 1 median 
bundle 


Pericycle 
Mainly solitary 
390—440 um 
Alternate, small 


Within pit chamber 
only 


Absent 
Distinctly bordered 
Aliform to confluent 


Heterogeneous I 
Styloids in paren- 
ma 


[r861 


dqV3OVA3.LVZTV — WVHV?IO 


L9L 


768 


Alzatea in Lythraceae (Lourteig, 1965) is an in- 
structive example of how one or a few phenetic 
similarities can be emphasized to justify rela- 
tionships of only remotely related or totally un- 
related taxa. The relationship of A/zatea to the 
Lythraceae is clearly of a general nature, based 
on characteristics widely dispersed in the family. 
No Lythraceous genus shares a sufficient suite of 
characteristics to be considered directly or closely 
related to A/zatea. 

Alzatea’s closest relationships appear to center 
around the genera of the Crypteroniaceae, Cryp- 
teronia, Dactylocladus, and Axinandra, and the 
genus Rhynchocalyx, by virtue of their posses- 
sion of more of the distinctive features which 
define A/zatea. Major similarities and differences 
among these genera, selected from recently pub- 
lished studies and personal observations of her- 
barium and fixed plant material, are compared 
in Table 3. Evidence of relationship based on 


In instances where variability occurs within the 
genus, as among the species of Crypteronia, the 
most common situation is recorded. The table 
is not meant to be all-inclusive; more complete 
characterizations may be found in the individual 
papers cited in the text. The reader is referred to 
these for further details not presented here. 
Macromorphological evidence. Among t 

most strikingly similar, advanced characteristics 
uniting Alzatea with Rhynchocalyx and Cryp- 
teronia pro parte are those of ovule and seed 
morphology. The three taxa display hemi-epig- 
ynous, bilaterally compressed, bicarpellate ova- 
ries in which numerous ovules are borne hori- 
zontally in one or more vertical rows. Placentation 
is parietal in A/zatea and Crypteronia (van Beu- 
sekom-Osinga & van Beusekom, 197 5) and axile 
in RAynci lyx (Sprague & Metcalfe, 1937; Strey 
& Leistner, 1968) but the solid central axis in 
Rhynchocalyx (Fig. 8e-g) is only slightly less 
evolved than the divided septum of A/zatea (Fig. 
8a-d) and Crypteronia. Additional ovarian fea- 
tures in RAynchocalyx, the narrow (ca. 0.5 mm 


cular system in Crypteronia is undescribed. 
However, free-hand sections of limited flower 
material of C. paniculata Planch. indicate that 
each fleshy half septum is free to the base and 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


has its own ventral vascular system which sup- 
plies the ovules and adjacent carpel wall as in 
Alzatea and Rhynchocalyx, although probably 
differs from them in the major ventral vascular 
supply of each half septum consisting of a single, 
rather than double, major bundle. The remaining 
Crypteroniaceae display quite different features, 
such as a 4-locular ovary with central conical 
placenta (other spp. of Crypteronia) or a nearly 
inferior, 4—6-locular ovary with ovules basal be- 
tween the septa (Dactylocladus and Axinandra). 

Transeptal bundles have been described for 
other members of the Myrtales and occur infre- 
quently in assorted families of other orders, e.g.. 
in Cornaceae, Rubiaceae, Araceae, Umbellifer- 
ae, and Oleaceae (Schmid, 1972, 1984; Eyde, 
1967, 1981; Puri, 1952). The condition is con- 
sidered derived from the common axile system 
and appears most frequently in families with in- 
ferior ovaries (Schmid, 1972; Eyde, 1981). In 
Myrtales, transeptal bundles are recorded in one 
or more genera of the Myrtaceae, Oliniaceae, 
Punicaceae, Onagraceae, and Тгарасеае, as well 
as in Alzatea and Rhynchocalyx (Schmid, 1984). 
The condition has most certainly arisen several 
times in the Myrtales and is not necessarily 1n- 
dicative of close phylogenetic relationship, al- 
though in A/zatea and Rhynchocalyx it 15 most 
parsimoniously considered to have been gam 
from their most recent common ancestor rather 
than independently evolved. 


persistent base of the style. Crypteront pi 
in retaining the entire style and stigma е 
hiscence of the capsule. A persistent style С 
acterizes Dactylocladus as well as Alzatea 
Crypteronia pro parte, but the fruit of the s 
differs in shape, placentation, and good ШЕ Al- 
Axinandra is even further differentiated des 
zatea by the epigynous, 6(—4)-locular ovary 
large, globose capsule with basal, erect 9 slat 
Compressed capsules and transeptal vase 
supply are unknown in the Lythraceae. hare 
In seed morphology, A/zatea appears 10 yp 
a simple, anatomically much reduced, о 
winged seed type with Rhynchocalyx pu = 
teroniaceae sensu stricto. Although the gis 
superficially similar, developmental gw 
differ in A/zatea, Rhynchocalyx, and mr 
the only genera studied to date, and thus f the 
be used to support a close relationship ^. 
genera (Tobe & Raven, 1983, 1984a, 


1984] 


The occurrence of a simplified seed in the Son- 
neratiaceae in Duabanga, but not in Sonneratia, 
indicates reduction in seed anatomy has occurred 
more than once within the Myrtales. The simple 
seed morphology of A/zatea is in marked con- 
trast to the multiple-layered seed coats of core 
families of the Myrtales which are further spe- 
cialized by the presence of fibrous and/or scle- 
rotic cell layers (Corner, 1976). Simplicity of seed 
structure in A/zatea is regarded as derived for 
reasons that the more complex seed coat is the 
common condition both in the Myrtales and in 
the Rosiflorae generally, and the simple seed is 
associated with advanced ovary characteristics 
of parietal placentation, transeptal vascular bun- 
dles, and bilateral symmetry. According to Cor- 
ner (1976), the main direction of seed evolution 
in Angiosperms has been toward reduction in 
complexity and size. 

Few other derived macromorphological states 
are shared by A/zatea and any of the other four 
genera. The unusual anther connectives with ter- 
minal or apically placed sporangia (Fig. 3) appear 
їп similar (homologous?) form in Axinandra but 
otherwise the genera hold no features incommon 
other than those widespread in the order. The 
expanded connective of Crypteronia anthers 
could be taken as an evolutionary intermediate 


lutionarily more advanced type in which the in- 
florescence axes are not terminated by a flower 
(Briggs & Johnson, 1979; Johnson & Briggs, 
1984). The well-developed nectary disc of Al- 
zatea is an apomorphy not noted in these other 
genera, 

Alzatea displays a total macromorphology 
Which places it at a distance from even those 
enera considered most closely related ог phe- 
netically most similar. The isolation is probably 
bes Pronounced than even macromorphology 
х = when one takes into account the likli- 


Ph 


bi n has very generalized features, being 
nucleate, prolate-spheroidal, and tricolporate, 


GRAHAM —ALZATEACEAE 


769 


with nearly psilate exine. Under the scanning 
electron microscope (SEM), mesocolpal depres- 
sions are apparent and have been interpreted as 
"incipient" subsidiary colpi (Muller, 1975, 1981). 
The presence of subsidiary colpi is a typical, al- 
though not constant, feature of Myrtalean pollen. 
It is the only pollen character of A/zatea which 
indicates relationship to the order, since other 
Alzatea pollen features appear in the dicotyle- 
dons in a number of unrelated families. There is 
no pollen characteristic of A/zatea which can be 
used to convincingly align A/zatea to any one 
Myrtalean family. It has been suggested that the 
pollen is comparable to that of Physocalymma 
in Lythraceae (van Campo in Lourteig, 1965). 
The characters they share, however, are gener- 
alized ones of shape, size, and possession of col- 
porate aperatures. They differ in sculpture pat- 
tern, Physocalymma having a rugulate-striate 
exine, A/zatea a psilate one. No case can be made 
for a close relationship to Physocalymma or any 
other Lythraceae based on pollen (Graham et al., 
unpubl. data). In contrast to pollen of A/zatea, 
pollen of RAynchocalyx, Dactylocladus, and 
Axinandra is tricolporate and distinctly 3-het- 
erocolpate, falling within the range of Melasto- 
mataceous and Lythraceous pollen types. Cryp- 
teronia pollen, on the other hand, stands totally 
apart from both A/zatea and the preceding taxa 
by its unusual bisyncolpate, bilateral condition. 
Although a hypothetical scheme for transition 
from A/zateato Crypteronia pollen has been pos- 
tulated, no transitional pollen type is known 
(Muller, 1975). The generalized features of Al- 
zatea pollen relegate the genus to an ancestral 
position with respect to the pollen ofother genera 
discussed but indicate no special relationship to 
any one of the families or specific genera in the 
Myrtales with which it has been aligned. 
Embryological evidence. Embryological 
comparisons confirm the Myrtalean position of 
Alzatea (Schmid, 1984; Tobe & Raven, 1984a). 
A comprehensive report of the embryology of 
the genus, from which this discussion is excerpt- 
ed, is presented by Tobe and Raven (1984a). Of 
the seven ordinal distinctions listed by them, A/- 
zatea differs only in one, i 


thraceous and Melastomataceous genera is 


Y 01535,8 7 


~ "d 
76 
мата 


PLANTS OF PERU 


URE 9. Aiz oien. Linde рај т subsp. verticillata, Vo 8331 (MO) from Peru. 


Fi 
с бесан Knapp & Kress 4336 (MO) from Cerro Tûte, Pana 


3°46°77 


TYPE LYTHRACEAE 


20 Mar, 1982 


9 10 
FIGURE 10. Alzatea verticillata subsp. amplifolia S. А. 


OLL 


N3QGIVO TVOINV.LO8 ІЧПОЅЅІИ JHL AO STVNNV 


IL 10А] 


, 


| 


1984] 


formed from both outer and inner integuments 
(Tobe & Raven, 1983). Unfortunately, compar- 
isons cannot be made with Crypteronia and Dac- 
tylocladus, which are unstudied embryologically. 
he most striking embryological feature of A/- 
zatea is the bisporic A//ium-type embryo sac, a 
type reported for no other Myrtalean taxa. The 
characteristic embryo sac type for the order is 
the monosporic Polygonum-type. Two excep- 
tions, besides A/zatea, are known, however, in 
Peneaceae and Onagraceae, each of which has its 
own peculiar embryo sac type. Rhynchocalyx 

conforms to the general Myrtalean condition. 
Alzatea is similar to Rhynchocalyx by virtue 
of the same micropylar formation and in having 

on 1 ү Ы пољ end | om 


а multicell 


dothelium development, and binucleate pollen. 
It differs in several ways, in addition to the em- 
bryo sac character. In Alzatea, anther wall for- 
mation is of the Dicotyledonous type with the 
wall four cell layers thick and the epidermal outer 
cell walls of the anther flat. The septum between 
microsporangia is non-persistent. Cells ofthe nu- 
cellus develop normally. In the seed, the embryo 
5 centrally positioned with straight cotyledons 
and the seed wing forms from the funiculus and 
outer integument. In Rhynchocalyx, anther wall 
formation is of the Basic type with wall layers 
five cells thick and epidermal outer cell walls of 
the anther papillate. The microsporangial septa 
persist after sporangial dehiscence. In the nucel- 
lus, subdermal cells elongate radially. In the seed 
the embryo is basally positioned with folded cot- 
yledons and the seed wing develops from the 
funiculus only. 

Axinandra, the only other putative close rel- 
ative investigated embryologically, is more dis- 
tantly separated from Alzatea than Rhynchoca- 
lyx by possession of two important distinctions: 
еле оуше archesporium with endothe- 
Ium present and the micropyle formed by outer 
and inner integuments. 
ea shares some generalized embryologi- 

atures with Lythraceae, but differs in many. 


toM 


f 
EE only. Tobe and Raven have concluded 
at, embryologically, Alzatea takes an isolated 


т which Lythraceae are also derived. 
natomical evidence. The recent series of an- 


GRAHAM —ALZATEACEAE 


771 


atomical studies in Myrtales offers a wealth of 
new information about A/zatea and associated 
taxa, as well as thorough assessments of rela- 
tionships based on anatomical data (van Vliet, 
1975, 1981; Baas & Zweypfennig, 1979; van Vliet 
& Baas, 1975, 1984; van Vliet et al., 1981; Keat- 
ing, 1984). Major anatomical distinctions of A/- 
zatea and the genera under discussion are ex- 
tracted from these works and listed in Table 3 
to facilitate comparison. 

Anatomical evidence clearly places A/zatea in 
the Myrtales. Familial and generic affinites, how- 
ever, are not clearly indicated by anatomical 
characters. A/zatea's leaf anatomy is particularly 

istinctive in the order. The combination of an- 
omocytic-cyclocytic stomates, midvein vascular 
system divided by a lacuna into abaxial and 
adaxial portions, abundant sclereids of two types, 
and small epidermal cells which are square in 
Cross section, are unlike any other genus inves- 
tigated in Myrtales (Keating, 1984). Other than 
the similar stomate condition shared by Rhyn- 
chocalyx and Dactylocladus, this synapomorphy 
isolates the genus in the order. 

Nodal anatomy additionally supports the ex- 
clusiveness of A/zatea in Myrtales. The trilacu- 
nar node with three traces is presently unknown 
elsewhere in Myrtales, where the unilacunar con- 
dition prevails. Trilacunar nodes, regarded as 
primitive in Angiosperms, may be ancestral in 
the Myrtales and ancestral to the common gap- 
median trace seen in some Melastomataceae and 
Crypteroniaceae (van Vliet & Baas, 1975). AI- 
ternatively, the possibility has been raised that 
the trilacunar node in A/zatea is a neotenous 
condition (Johnson & Briggs, 1984). In either 
case, the genus is unique within the order for this 
attribute. 

Wood anatomical details indicate A/zatea is 
linked in a general way to several Myrtalean fam- 
ilies but is not a close fit to any of them. Within 
the order there is a wide range of wood anatom- 
ical diversity and much overlap in the families 
tentatively associated with Alzatea, i.e., Cryp- 
teroniaceae sensu stricto, Lythraceae, and Me- 
lastomataceae. This heterogeneity restricts use of 
the anatomical data as an indicator of family 
placement for A/zatea. At the generic level, there 
are major anatomical distinctions between Al- 
zatea on the one hand and Crypteronia, Dactylo- 
cladus, Axinandra, and Rhynchocalyx on the 
other. A/zatea has branched foliar sclereids, tri- 
lacunar nodes with three traces, and clustered 
crystals in chambered phloem cells, character- 


772 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


n! 1 Cc S 


ис 4. Distribution of similar n genera and family associated with Alzatea. 


K — shared with A/zatea; — — not occurring: in the genus or dos ily; ( ) = rarely, occasionally, or in part 
occurring in the genus or family; ? = unknown; * = evolutionarily advanced feature in A/zatea. 


Presence of a Similar State in: 


cba Crypte- Dactylo- Axin-  Lythra- 


Selected Alzatea Characteristic alyx ronia cladus andra ceae 
Leaves opposite and whorled + + ce T (+) 
*Stipules axillary and divided + — = s + 
Inflorescence anthotelic (axes terminated by a flower) + а, ЕЕ E % 
*Flowers hemi-epigynous * * + d di 
*Nectary disc present F E E " (+) 
ers 5-merous E T * y (+) 
*Petals absent = T Е: = (+) 
*Calyx lobe pus beue within + T E x У 
жСајух е регѕ T T T F 2 
Stamen n modis ve E че = E (+) 
itimni short, thick um a © T E 
*Connective expanded with terminal sporangia “ + m T к 
Pollen tricolporate + У T T (+) 
*Subsidiary colpi indistinct, not prominent = * m m (+) 
Pollen нај + + + * Ы 
Ee: + E m E (+) 
Sty дне регѕіѕ * + + (+) 
S dh bilateral, а + (+) Y 
*Carpel num t (+) T ¢) 
*Ovary vasc i supply transeptal, lateral + (+) ? ? 
*Placentation parietal ad (+) is a 
*Ovules numerous, ca. 40 T (+) z i M 
Ovule position horizontal * (*) 3 Б Be 
Ovule archesporium multi-celled + 7 ? E : 
Ovule endothelium absen + ? ? Г : 
*Micropyle formed from inner integument only + » T7 T i 
*Embryo sac bisporic, A/lium-type — 7 2 x ү 
*Seed wing present + + F + (0 
*Seed testa 2-layered, unspecialized + F AR t 3 
*Seed tegmen 2-layered, unspecialized + + T T E 
es trilacunar with three traces — = 7 a ү 
Leaf stomates mainly anomocytic + T us ed | 
Petiole bundle a closed rin — + F z E 
Leaf sclereids pre + + T а: 3 
*Branched leaf sclereids prese - – = a : 
Wood vessels mainly in radial multiples – + a ae : 
*Vesturing forming surface + = m s ы 
*Vessel-Ray pits coarse, large = Е T Bs " 
*Septate fibers present + — = | s 
*Fiber pitting simple to minutely bordered T Т" 2 y у 
T parenchyma scanty paratracheal + (+) те " 1 
S heterogeneous I + d 


+ 
Pia birt crystals in chambered phloem parenchyma £ E | 


istics absent from the other genera. From Cryp-  Dactylocladus, in addition, it has pe o 
teronia and Axinandra, it also differs in having іріп of cork and less advanced heterogene 
anomocytic rather than paracytic stomata and II i ladus has а $ 

ray types, while Dactyloc 
septate fibers with simple pits rather than non- d d E T ous Шуй 
septate fibers with distinctly bordered pits. From 


There are extensive differences 


1984] GRAHAM—ALZATEACEAE 773 
TaBLE 5. Numerical summary of Table 4 listing of 43 characteristics of Alzatea shared with associates. 
No. Shared No. Shared No. Shared Total Wholly % Shared 
Genus Ancestral Derive in Part Unknown Shared With A/zatea 
Rhynchocalyx 10 17 0 0 JT 63 
Crypteronia 7 11 1 — Ancestral 4 18 45 
6— Derived 
Dactylocladus 7 7 0 5 14 33 
Axinandra 5 5 0 1 10 25 
Lythraceae 4 6 7—Ancestral 1 10 25 
8— Derived 


calyx in cuticle texture, mechanical support of 
the veins, petiole anatomy, and vessel-ray pit- 
ung. The coarse, large, reticulate-scalariform 
vessel-ray pitting contrasts particularly with the 
small alternate pitting in RAynchocalyx. The two 
genera are alike in having septate fibers with sim- 
ple fiber pits, scanty paratracheal parenchyma, 
and peculiar vesturing of inter-vessel pits which 
extends beyond the pits in superficial bands. 
However, only the vesture condition can be con- 
sidered highly derived; the other two features are 
typical of unspecialized “protolythraceous” wood 
(Baas, 1979), 

Although there are similarities with Lythra- 
eous anatomy, the trilacunar nodal condition, 
arrangement of vascular tissue of the petiole and 
midrib, and banded vesture type are not found 
9 the Lythraceae. Three major features of Al- 
bai. wood anatomy, scanty paratracheal paren- 
"T heterogeneous rays, and septate fibers 
мы pits recall unspecialized wood in Ly- 
mee There are also wood anatomical agree- 
Pic: о Alzatea with Melastomataceae (e.g., 
Оніо, сан vessel-ray pits), Sonneratiaceae and 
Ness E but no particularly close affinities to 
= them and no member of any of these 
Аш i а$ most of the characters of Alzatea. 
id € studies have led to the conclusion 
c etin is an isolated remnant of the an- 
wi ock which gave rise to Lythraceae and 

mataceae (van Vliet et al., 1981). 


ТАХО 
NOMIC AND PHYLOGENETIC RELATIONSHIPS 


acteristics are derived, 14 are regarded as ances- 
tral. The list underlines the dispersed nature of 
Alzatea attributes in putative relatives and the 
heterogeneity of the Crypteroniaceae sensu lato. 
Among th iated g Rhynchocalyx, wit 

27 similarities, shares the greatest number of fea- 
tures (Table 5; Figs. 11-14). Crypteronia, with a 
maximum of 24 shared features in C. paniculata, 
but only 18 shared with other species of the ge- 
nus, is less similar. Knowledge of the embryology 
of Crypteronia should contribute significantly to 
a more accurate assessment of relationships 


more distant, sharing, respectively, only 14 and 
ten of the 43 characteristics. Crypteroniaceae, as 
construed by van Beusekom-Osinga and van 
Beusekom (1975), thus groups a diverse assem- 
blage of genera, with A/zatea and Rhynchocalyx 
especially separated by significant gaps from the 
others. At least 25 characteristics of A/zatea can 
be found in one or more genera of the Lythraceae, 
but no single genus has many and hence none 
approach Alzatea phenetically. With respect to 
the relationship of A/zatea to its most similar 
associate, Rhynchocalyx, Alzatea differs from that 
genus in 16 of the 43 character states listed. At 
least four of these are apomorphies unique to 
Alzatea. It is this prominent degree of divergence 
of Alzatea from even its nearest taxonomic 
neighbor which supports establishment of a new 
family to accommodate this distinctive taxon. 
On the same basis, Rhynchocalyx is also isolated 
by a substantial suite of specialized characters 
and is best treated as a separate family. I earlier 
stated in personal communications with Dahl- 
gren, 1981 and Briggs, 1982 that the genus be- 
longed to the Lythraceae based on evidence then 
available. It had been regarded, since first de- 
scribed, as most similar to Lawsonia in Lythra- 
ceae, primarily due to their superficially similar, 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


NATAL 
NATALSE 


212 
<i; 
в = 
ac 
2 
a 
= 
2 
= 
Fi 
© 
© 
m 
= 


Gria Ret 


[VoL. 71 


| 


1984] 


floriferous, paniculate inflorescences of small 
white flowers (Strey & Leistner, 1968; Sprague 
& Metcalfe, 1937). Characters tying it to Ly- 
thraceae are now rightly regarded as ancestral 
ones shared by Melastomataceous and Lythra- 
ceous evolutionary lines. New contributions to 
our knowledge of the genus lead to the conclusion 
that Rhynchocalyx is another relic genus in the 
Myrtales, without close living relatives. This iso- 
lated position is best acknowledged by recogni- 
tion of the monotypic Rhynchocalycaceae (John- 
son & Briggs, 1984). 
A phylogenetic study of Myrtales (Johnson & 
Briggs, 1984), Including Alzatea, has recently been 
ds based on many 
of the same characters cited in Table 4. In the 
phylogeny preferred by the authors (their Fig. 3), 
three major evolutionary groups emerge, the Ly- 
thraceae sensu lato-Onagraceae- Trapaceae line, 
the Myrtaceae-Heteropyxis-Ps loxylon line, and 
àn assemblage now recognized as mem 
the Melastomataceae, Crypteroniaceae, Pene- 
асеае, Oliniaceae, and Rhynchocalyx and Alza- 
геа. Phylogenetic relationships among the mem- 
bers of this last group are uncertain and several 


dependent course over a long period of time, 
retaining some Pi ues ancestral features, as 


Rh ed from its nearest living relative, 
à 4 nchocalyx. Its distribution in the wet forests 
Topic Andean South America and in Central 


m s s 


GRAHAM—ALZATEACEAE 


775 


teroniaceae. Homoplasy in taxa of shared an- 
cestral lineage, especially with respect to 
macromorphological characters, has obscured the 
extensive divergence of A/zatea and is partly re- 
sponsible, together with the incorrectly placed 
emphasis on synplesiomorphy, for misdirected 
ideas of relationship and questionable taxonom- 
ic placement. Carefully considered phenetic 

pari d phylogenetic studi that 
Alzatea is an isolated genus within the Myrtales, 
derived from the same ancestral pool which gave 
rise to the modern Lythraceae, Crypteroniaceae, 
and Rhynchocalycaceae, but now distinctly sep- 
arated from them and consequently best treated 
as a monotypic family. 


TAXONOMIC TREATMENT 


ALZATEACEAE S. Graham, fam. nov. TYPE: 
Alzatea Ruiz & Pavón. 


Arbor gla idees ramis verticillatis purpurascen- 
tibus. Folia int sita et 


apeta 

cus one lobatus. Stamina 5, antepetala, margini 
disci 
connectivo late expansa ad basi et angustata usque ad 
is grana oblata-sphaeroidea, tricolpora- 


1 
ramene; ovulis in q oculo multis, horizontalis, 
ш ricatis . Fructus capsula indurata, lateraliter com: 


rie lunata, plana, circumcirca ala tenui cincta. xd 

This monotypic family ofthe New World trop- 
ics, represented by Alzatea verticillata, is distrib- 
uted along the lower slopes of the Andean Cor- 
dillera in Peru and Bolivia in humid forests of 
the upper Amazonian basin and disjunctly in 
cloud forests of Costa Rica and Panama. Figure 


Alzatea verticillata Ruiz & Pavón, Syst. Veg. Fl. 
Peruv. Chil. 1: 72. 1798. Fl. Peruv. 3: 20, 
pl. 141, fig. a. 1802. Type: Peru. Huanaco: 
nemoribus ad Chinchao praeruptum prope 
Mesapata praeditum (holotype, MA, pho- 


~ 


F 
TN IGURES 11—14. Rhynchocalyx lawsonioides Oliv., Natal, South Africa, closest living relative of Alzatea. — 


ing specimen, H.B. Nicholson 5. п. MO 
Uvongo Nature Reserve,— 13. T n hat 


-12. Tree i in bloom, edge of * rest adjoining Table Mountain, 
6mi 


eight; bark pale gray, Uvongo 
eaf length, 


25-15 m Reeve. —14. Inflorescence, flowers pierces in bud, actual bud ак 3—4 mm; actual 1 


776 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


84" 82° 


URE 13. 


= Subsp. | 
Distribution of Alzatea verticillata.—a. Subsp. amplifolia in Costa Rica and Panama. —b. 


Ес 
даа іп Peru and Bolivia. Dotted line represents the continental divide. 


tograph at F no. 91664!; 
1573979!, Е no. 843533). 


Alzalia mexicana F. G. Dietrich, Vollst. Lex. Gartn. 
1802. Nachtr. Vollst. ч алау » 199. 

1815. Neu. Nachtrg. Vollst. 187. 
vers TYPE: Based on A. one tia ас & Ра- 


la. Alzatea verticillata subsp. verticillata. 


Leaves elliptical or oblong-obovate, averagin 
66 mm long, 35 mm wide, basally attenuate; 


petioles 2—13 mm long. Peru and Bolivia. Figures 
9, 15a. 


Additional specimens (those not mapped in Fig. 14 
due to insufficient locality data are marked wi 


asterisk). BOLIVIA. Songo (= Zongo Valley), Nov. 1890. 
Bang 829 (K, MO!, МУ, US); PER 


mpa Alto Vaqueria, 2,200 m, 11 
Aug. 1967, ere 114 (Е 7), 21 Nov. 1967, Vas- 
quez А. 136 (Е! : Zepelacio, near M 

m, Oct. “Now 1933, Klug 3349 
K, МО!, 9). тон *Santa Ana, Pitabam- 
Nov 1866, Pearce s.n. (K); *Rio N gro, in th 
edi 1,000 m, 15 Jan. 1961, Woytkowski 6196 (MO!, 
P) 


1b. Alzatea verticillata T, amplifolia S. A. 

raham, subsp. nov. TYPE: Panama. Vera- 

guas: Cono Тое, 20 Маг. 1982, Кпарр & 
Kress 4336 (МО). 


Folia oblonga-ovalia, ad 145 mm longa, 100 mm 
lata, saepe ca. 90 mm longa, 65 mm lata, basi pleraque 


isotypes, F no. 


rotundata, sessilia vel Meses petioli 0-2 mm long. 
Costa Rica et Panama. Figures 1 


Additional specimens (those not mapped in i | 
due to insufficient locality data are ишке wl | 
asterisk). Costa RICA. CARTAGO: 0.5 km be oa x. pe 
1,200 m, 14 May 1967, Lent 966 (CRI, h Come 
1982, Poveda et al. 3264 (CR!), Oct. MES 4 
18728 (CR!); Moravia де Chirripó, 28 e d | 
veda & Sieng 1523 (CR!). PE Flo 1620-16 0 
teverde, cerro N of Pantano Chom os Ba 
m, 15 Jan. 1977, Dryer 1133 (CR!, p). er 
La Hondura, above Río Hondura, !, 400. da 566 
1967, Lent 1443 (CR!, Е!), 20 June c 1973, AM 
(C RJ), 24 Mar. 1977, Poveda 1564 (CR!). 

*La Palma, 1,500 m, 31 July 1936, 
*Quebrada Cuecha, 1,540-1,600 m 


e -— 


el 6247 (МО), 12 km N of Нотио, "T" 
io kaa & post 5532 (MO). Mee | 
Santa Fe, slopes and peaks of Cerro Ari poe + «йй. 
Tûte), 11 Sept. 1978, Hammel 4726 ( 
of Cerro Tite, 1,410 m, 5 June 1982, Knapp & & Dress — 
5392 (MO). 


Comparison of the South American and Cer 
tral American collections reveals two 7 sou 
differences consistent with geograp и = 
and significant enough to deserve fo 


Рапат | | 
nomic recognition. Costa Rican : a: y oblong | 
nian plants have ample, broad, he gu meric? 
to oval, sessile leaves and those e elliptic 


ican leaf specimens is 89 mm b si 
are sessile or subsessile with petio e 
or less. The mean size of South Am 


e E 


1984] 


is 66 mm by 35 mm; leaves are basally attenuate, 
petiolate to subsessile with petioles varying from 
(0-)2-13 mm long, averaging 6 mm. Leaves of 
the type collection from Peru average 91 mm by 
59 mm with petioles 10—12 mm long. On the 
Bolivian collection examined, leaves average only 
57 mm by 33 mm and are mostly sessile. No 
floral morphological differences separate the 
Central and South American collections and Baas 
(1979) found no striking anatomical differences 
between Peruvian and Costa Rican samples. As 
more collections of the genus are gathered, per- 
haps even from the intervening areas of Ecuador, 
Colombia, and the Darien, it may well become 
more difficult to apply subspecific names. Based 
on present collections, however, recognition of 
subspecies amplifolia serves to point up the ge- 
netic divergence now expressed in the disjunctly 
distributed Central and South American plants. 
Ht is possible that a discriminatory biological 
difference exists between Central and South 
American Alzatea. South American plants sur- 
veyed produce heterosexual flowers with pollen 
viability greater than 95%. In contrast, Central 
American plants appear to bear only functionally 
unisexual flowers. No fertile pollen has been found 
їп flowers from Cerro Tutte, Panama collections, 
although approximately 50% of the seed in each 
capsule appears fully formed. In Costa Rican col- 
lections Studied, no more than 36% of the pollen 
appeared normal (Tobe, pers. comm.; Graham, 
unpubl. data). Investigations are in progress to 
determine the nature of reproduction in the Pan- 
ama population (Raven, pers. comm.). 
Description of the habit and habitat of the 
senus are known primarily from collectors’ brief 
notations, mostly on herbarium labels. New ob- 
о however, are rapidly accumulating 
N з, American A/zatea аз а result of active 
бы by members of the Missouri Botanical 
= к currently working on the Central Amer- 
(1940) га. Alzatea is described in Ruiz’s journal 
ы | а$ а tall leafy tree with “а trunk divided 
E props that formed an arbor un- 
th. Disparately, it is described as a slen- 
= epiphyte reaching the crowns of 
"рыр img of the lower montane rain forest 
айы, са (К. Lawton, pers. comm.) or as 
re mall (ca. 7 m tall), much-branched trees 
оюну, E comm. to Raven). In Panama it 
rag ән -3m shrub of windswept elfin cloud 
MO), as eraguas Province (Knapp & Kress 4336, 
Pie о: а stream-side epiphytic shrub in Chi- 
оутсе (Hammel 6247, MO), and has 


GRAHAM—ALZATEACEAE 


til 


been observed also in Chiriqui Province growing 
epiphytically in tall trees of the forest (Knapp, 
pers. comm.). Height records vary from 2 m to 
20 m and it is apparent that habit varies consid- 
erably with site conditions. The typical form is 
probably a much-branched hemi-epiphytic tree 
of 6—12 m which is capable of climbing to greater 
heights with support of surrounding trees when 
it occurs in tall tree forests. Trunk diameter ranges 
from 5 cm in high-climbing specimens to 20 cm 
(to 80 cm in Costa Rica, fide Poveda) on free- 
standing trees. 

It occurs typically on steep slopes of the low 
montane rain forest at elevations of 1,000-2,200 
m either as isolated individuals or, in at least two 
instances, at Cerro Тше, Panama and Tapanti, 
Costa Rica, as a locally common component of 
the flora. In South America the genus appears on 


curs with and is easily mistaken for Clusia. The 
striking vegetative similarity between A/zatea and 
Clusia has led curators to file the unfamiliar A/- 
zatea with the Clusiaceae (Guttiferae); curators 
of Latin American collections are advised to check 
that family as well as the Celastraceae for un- 
detected specimens of A/zatea. 

Flowering of the genus in Peru occurs from 
August to October; mature capsules occur from 

ovember onward. The single collection from 


lected in March and in August, suggesting less 
seasonally restricted flowering. 

Production of nectar has not been observed 
(Knapp, pers. comm.) nor have insect visitors 
been reported. In the absence of petals, the showy 
pinkish white anthers may function to attract 
insects. The anthers are positioned, as petals 
would be, between the calyx lobes at anthesis 
and are sometimes mistaken by collectors for 
petals. The most recent observations of living 
plants have been on the Cerro Tûte, Panama, a 
windy site with frequent cloud cover where con- 
ditions are not often conducive to insect visita- 
tion. 

Seed containing embryos generally constitute 
less than half the seed produced. Lack of polli- 
nation may partially account for this, but in the 
Central American populations low pollen fertil- 
ity is certainly a factor. Studies of the reproduc- 


PS d 15 1 L 141 ~ oN 1 ++ 
tive отоору зпоша сас tO d осии Б 


778 


of how A/zatea has managed to retain its place 
in the flora of the New World tropics. 


LITERATURE CITED 


Airy SHAW, Н. К. 1966. A Dictionary of the Flow- 
ering Plants and Ferns. 7th edition. Cambridge 
Univ. Press, Cambridge. 

Baas, P. 1979, The anatomy of A/zatea id & Pav. 
(Myrtales). Acta Bot. Neerl. 28: 156-1 

WEYPFENNIG. ms Wood 

— of the Lythraceae. Acta Bot. Neerl. 28: 


-155. 
Влте-5мтти, E. С. 1962. Тће Phenolic ata grits 
of pl а 


$ос. , Bot, 58: 95-173. 
BENTHAM, С. & J. D. Hooker. 
Gen. Pl. 1(1): 362-363. 
BEUSEKOM-OSINGA, R. J. VAN & C. F. VAN BEUSEKOM. 
1975. Delimitation and subdivision of the Cryp- 
teroniaceae (Myrtales). Blumea 22: 255-266. 
ВИМЕ, C. L 26-1827. pibe tot de Flora van 
Nederlandsch Indié 17: 1067-1169. 

— B.Go& LAS mdr 1979. Evolution 

n the Myrtaceae—Evidence from inflorescence 

ц Proc. Linn. Soc. New South Wales 102: 
157-272. 

CANDOLLE, A. L. P. P. DE 
Prodr. 16: 677-679. 

CANDOLLE, A. P. DE 1825. Celastineae. In Prodr. 2: 
1-18. 

CORNER, A J. Н. 1976. The Seeds of Dicotyledons, 

mes. Cambridge Univ. Press, Cambri ridge. 

C бели А. 81. An Integrated System of Clas- 
sification of Flowering Plants. Columbia Univ. 
Press, New York. 

DAHLGREN, R. & R. F. THORNE. 1984 [1985]. The 
order Myrtales: circumscription, variation, and re- 
lationships. Ann. Missouri Bot. Gard. 71: 633 


1862. Alzatea. In 


. 1868. Crypteroniaceae. Jn 


Еуре, R. H. 1967 [1968]. The peculiar gynoecial vas- 

a of Cornaceae and its systematic signifi- 
cance. Phytomorphology 17: 172-182. 

1981. Reproductive structures and evolution 
in Ludwigia (Onagraceae). III. Vasculature, nec- 
taries, conclusions. Ann. Missouri Bot. Gard. 68: 
379-412. 


HALLIER, Н. 1911. Ueber Рћапег erogamen van unsi- 
cherer oder unrichtoger Stellung. Meded. Rijks- 
ege 1910: 1-40. 

18. Ueber Aublet’s Gattungen a 
oder а Stellung und über рћап enge- 
schichtliche Bezihungen zwischen ATE und 

: 1-33. 


hemotaxonomie der Pflanzen, 
е 5. Birkhauser Verl., Basel and Stuttgart. 
Mosel HINSON, J. 1967. The Genera of Flow wering 

Plants; Seen 2 Volumes. Clarendon 
Press, ord. 


isso 
R. 1984 [1985]. Leaf histology and its con- 
utio on to relationships in the Myrtales. Ann 

t. Gard. 71: 801-823. 


issouri 
LOESENER, L. E. T 1892. Celastraceae. Jn A. Engler 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


& K. Prantl, Nat. Pflanzenfam., 
— 


Ist Edition. 3(5); 


————. 19 Celastraceae. Jn Nat. Pflanzenfam., 2nd 
виа E 87-197. 
LOURTEIG, A. 1965. On the systematic position of 
Alzatea verticillata R. & P. Ann. Missouri Bot. 
ar 7 


MACBRIDE, J. F. . Rhamnaceae. In Flora of Peru. 
Publ. Field Mus. Nat. Hist., Bot. Ser. 13: 391- 


413. 
Miers, J. 1872. On the Hippocrateaceae of South 
erica. Trans. Linn. Soc. London 28: 319-432. 
MULLER, J. 1975. Note on the pollen morphology of 
Crypteroniaceae s.l. Blumea 22: 275-294. 
1981. Exine architecture and function in some 
Lythraceae and Sonneratiaceae. Rev. Palaeobot. 
3: 


1845. Sur les affinités des Genres 


Henslowia, “Wall. (Crypteronia? Blume. Quila- | 


grate Blanco.) Raleighia, Gardn. et Alzatea, Ruiz 
t Pav. London J. Bot. 4: 474-478. 

PO V. 1952. Placentation in angiosperms. Bot. Rev. 
(Lancaster) 18: 603—651. 

Rao, T. А. & S. Das. 1979. Leaf sclereids—occur- 
rence and distribution in the Angiosperms. Bot. 
Not. 132: —324. 

Ruiz, H. 1940. Travels of Ruiz, Pavón, and Dom 1 
in Peru and Chile (1777-1788). Translated 
E. Dahlgren. Publ. Field Mus. Nat. Hist., Bot. Ser. 
21: 1-37 m 


lensis гушаи Reprint. J. Cramer-Lehre, 


798. Systema Vegetabilium Flo- 
rae Peruvianae et Chilensis. 
& ———. 1802 


| 


| 


VON. 1794. Florae Peruvians ВИ 


Flora Peruviana et Chilensis | 


1972. A resolution of the Eugenia-$- 


3; 20: 
SCHMID, R. Bot. 59: 


zygium controversy (Myrtaceae). Amer. J. 
423-436. 


. Mi 

SPRAGUE, T. A. & C. ETCALFE. 
nomic position of Rhynchocalyx. K 
392-394. 

Strey, К. С. & О. A. LEISTNER. 
ery of Rhynchocalyx пе 


rican Bot. 34: 9-1 не сл 


1968. The гей9с07 
ides b J.S, AF 


Tose, H. & P. RAVEN. 1 83. 
inandra zeylanica Thw. (M 
tionship of the genus. Bot. Gaz. 
144: 42 
. 1984a [1985]. The споро e 
relationships of Alzatea = & Рау. ors Y 
Myrtales). Ann. Missouri Bot. 

& 1984b [1985]. he enna e 
relationships of АМ Ке ony 71; 836 
calycaceae). Ann. M ‚ Gard. 
843 


the rela- 


y of 
: tomy 
УЦЕТ, С. J. С. M. van. 1975. Wood ana 104 
Crypteroniaceae sensu lato. J. Microscop} 
65-82. 


Wood anatomy of palacotroicl N 
lastomataceae. Blumea 27: 39 ae omy o 
& Р. Baas. 1975. Comiti 


237. mese | 
ew Bull. 1937. | 


of AX | 


ave | 


| 


1984] GRAHAM —ALZATEACEAE 779 


the Crypteroniaceae sensu lato. Blumea 22: 173- 
195 


—— . 1984 [1985]. Wood anatomy and 
нЕ of the Myrtales. Ann. Missouri Bot. 
i EIN: 


—— J. K-NOORMAN & B. J. H. TER WELLE. 
1981. ‘Wood anatomy, —À dnd phylog- 
eny а 27: 463-473. 


Dh air F. 1968. Bemerkungen über das V 
kommen Rudimentárer Stipeln. I. Cyrillaceae =e 
die ition Cyrillopsis Kuhlm. II. A/zatea Ruiz 
& Pav. ин und Tristania К. Br. Acta Bot. 
Neerl. 17: 282—2 

МИР M C. 1955, dt Dictionary of the Flowering 

s and Ferns. 6th Edition. Cambridge Univ. 
din Cambridge 


A COMMENTARY ON THE DEFINITION OF THE 


ORDER MYRTALES 
ARTHUR CRONQUIST! 
ABSTRACT 


I concur in the delimitation of the order Myrtales proposed by Dahlgren and Thorne (this sym- 
posium), except for the position of the Thymelaeaceae, which they exclude. The Thymelaeaceae are 


how best to provide for the admitted differences within the framework of the taxonomic system. I 
find it more useful to retain the Thymelaeaceae in the 


Myrtales as a somewhat aberrant group than 


to establish a satellite order composed of a single family. 


It appears that among the participants in this 
symposium there is substantial agreement on the 
limits of the Myrtales, with the single exception 
of the family Thymelaeaceae. The Combreta- 
ceae, Crypteroniaceae, Lythraceae, Melastoma- 
taceae, Myrtaceae, Oliniaceae, Onagraceae, Pen- 

eaceae, Punicaceae, Sonneratiaceae, and 
Trapaceae, all of which have traditionally been 
referred to the Myrtales, are still kept there, al- 
though some of us would reduce some of these 
groups to less than familial status. The Cyno- 
moriaceae, Dialypetalanthaceae, Haloragaceae, 
Hippuridaceae, Lecythidaceae, Rhizophoraceae, 
Theligonaceae, and other families that have been 
included by some authors in the past are properly 
to be excluded. 

My esteemed colleague Academician Takh- 
tajan would add only three families, the Halora- 
gaceae, Lecythidaceae, and Rhizophoraceae, to 
the list of those included by Dahlgren and Thorne 
(1984). In his most recent system, Takhtajan 
(1980) puts each of these three families into a 
separate suborder, in contrast to the suborder 
Myrtinae for all the other families. Thus his sub- 
order Myrtinae is functionally equivalent to the 
order Myrtales as discussed here. 

It is interesting and perhaps significant that 
this degree of agreement has been achieved by 
several different individuals or groups working 
more or less independently of each other, al- 
though of course not in intellectual isolation. My 
own treatment was in the hands of the publisher 
before I saw the manuscript by Dahlgren and 
Thorne. As new information continues to ac- 
cumulate, the range of taxonomic schemes that 


' Herbarium, New York Botanical Garden, Bronx, New York 10458. 


ANN. Missouni Bor. GARD. 71: 780-782. 1984. 


can reasonably be defended is progressively nar- 
rowed. | 
It is also interesting that two of the characters 
which have played a large role in reshaping ! e 
definition of the Myrtales are anatomical: тег | 
nal phloem, and vestured pits in the vessels. it 
is only in the last several decades that enough 
information has become available about the | 
taxonomic distribution of these features both | 
within and without the Myrtales to permit any | 
reliance to be placed on them. We cannot claim | 
to be better taxonomists than our predecessore | 


but we do have more data to work with. | 


fully. The necessity to make a choice for pe | 
of a formal system magnifies the relatively 5 
disagreement between us. EE 
рна and Thorne (1984) present а ie | 
erable list of similarities between the T | 
aceae and typical Myrtales, including pi йв | 
presence of internal phloem. The vestis 1 The | 
of the vessels should be added to their pU of | 
evidently pseudomonomerous gyo% | 
typical Thymelaeaceae sets the family eee cae | 
the rest of the Myrtales, but it does no ^ | 
against a relationship. Rather it directs ow | 
for affinities (or at least for a plausible rae г than | 
to families with a compound pistil rathe | 
to families with simple pistils. 


1984] 


share some features, appear to have a simple 
pistil. Yet as Dahlgren and Thorne (1984) point 
out, there is no inherent reason why the number 
of carpels could not ultimately be reduced to one 
in a syncarpous as well as in an apocarpous gy- 
noecium. Indeed that very thing seems to have 
happened in the Cucurbitaceae. If the Thyme- 
laeaceae were to be associated with the Elaeag- 
naceae, then it would have to be assumed that 
the pistil of the Elaeagnaceae became monom- 
erous by reduction. The two families would then 
have to form an order of their own; collectively 
they would spoil any other order into which they 
were put. It is possible that future evidence will 
support such an association of these two families, 
but in my opinion the balance is now against it. 

The principal argument that Dahlgren and 
Thorne (1984) adduce against a position of the 
Thymelaeaceae in the Myrtales is chemical. There 
is no doubt that the Thymelaeaceae stand apart 
from the rest of the order in this regard. The 
question is what evolutionary and taxonomic 
Significance to attach to the difference. 

Unlike the other Myrtales, the Thymelaeaceae 


NC to lay great stress on such a single oc- 
s ге in an advanced genus of a family that 
chemically so diversified. Furthermore, the 
Euphorbiaceae, like the Myrtales, are commonly 
re and if this difference can be mini- 
ne a possible relationship to the 
ear, laceae, It can also be minimized in as- 
TR possible relationship to the Myrtales. 
wu ai several other chemical and morpho- 
Pi ada (e.g., phorbol-type diterpenoids, 
Pollen) that link some members of the 
ње to some members of the Eu- 
ically 597, but these similarities аге taxonom- 
А altered rather than being pervasive. 
EE to associate the Thymelaeaceae 
that these uphorbiaceae must confront the fact 
Миса ES families display different sets of 
ae eatures, suggesting only a fairly re- 
кей топ ancestry. Thus the Thymelae- 
aracteristically have internal phloem, 


CRONQUIST—COMMENTARY 


781 


vestured pits, daphnin, wedge-shaped phloem 
rays, more or less strongly perigynous, mostly 
perfect flowers, and well developed, often peta- 
loid sepals, all of which are unusual or wanting 
in the Euphorbiaceae. The Euphorbiaceae, on the 
other hand, tend to be laticiferous and have 
mostly unisexual, more or less strongly reduced 
flowers with an obturator of different nature from 
that in the Thymelaeaceae. The Euphorbiaceae 
are so highly diversified, especially in chemical 


can be found in particular features of particular 
genera. I don’t suppose that anyone wants to use 
the presence of mustard oils in Drypetes to war- 
rant the inclusion of the Euphorbiaceae in the 
Capparales. 

According to a hypothesis of chemical evo- 
lution that I proposed in 1977, the subclasses 
Hamamelidae, Dilleniidae, and Rosidae are all 
primitively tanniferous, producing ellagic acid 
and other tannins. Subsequent evolution within 
these subclasses and in the derived subclass As- 
teridae led to the substitution of other chemical 
repellents for tannins in many groups. A similar 
hypothesis was proposed at about the same time 
by Gardner (1977), who visualized a “gradual 
replacement of a defence based on tannins and 
crystals (primitive Rosidae) by defences based 

variety of toxic and repellent substances 
(advanced Asteridae)." Under this concept, the 


were tanniferous. Thus the chemical evidence 
alone does not preclude the origin of the Thy- 
melaeaceae from within the Myrtales. The taxo- 
nomic level at which the Thymelaeaceae should 
be recognized is debatable, but their ultimate 
attachment to a tanniferous group is inevitable. 

In a symposium concerned only with the limits 
of the Myrtales, I suppose it might be possible 
to exclude the Thymelaeaceae from the Myrtales 
as a discordant element. Being concerned with 
the general taxonomic system, I am not satisfied 
to exclude the Thymelaeaceae from the Myrtales 
unless I have a better place to put them. They 
would be an even more discordant element in 
any other order as presently constituted (at least 
in the Cronquist system, which is necessarily my 
frame of reference). The possibility of a future 
association with the Elaeagnaceae cannot be en- 
tirely discounted, but the Elaeagnaceae are just 
as strongly tanniferous as the Myrtales. Exclu- 
sion of the Thymelaeaceae from the Myrtales on 
chemical grounds would logically preclude as- 


782 


sociation of the Thymelaeaceae with the Elaeag- 
naceae 


Thus, if the Thymelaeaceae are to be excluded 
from the Myrtales, they must form an order of 
their own. I cannot really argue with anyone who 
chooses that alternative, as Takhtajan (1980) has 
done. It is a matter of lumping or splitting, in 
which there is no objective right or wrong. In- 
clusion of the Thymelaeaceae in the Myrtales 
does not complicate the distinction of the Myr- 
tales from other orders. Therefore I find it con- 
ceptually more useful to tolerate this somewhat 
discordant family in the Myrtales than to tolerate 
still another order consisting of a single family. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


LITERATURE CITED | 


ЖОШ, A. 1977. Оп the taxonomic oc | 
secondary 


Evol» Seoul. 1: 179-189. 

DAHLG M. T. & R. F. THORNE. 1984 [1985]. 
Theo order Myrtales: circumscription, variation, and | 

So ma E Ann. Missouri Bot. Gard. 71: 633- 

699. 


GARDNER, R. O. сы е distribution and 
ecological function of the secondary metabolites | 
of the Баа eos Biochem. Syst. Ecol. 5: | 


TAKHTAJAN, hie LES 
plants ern ophyta). Bot. 


1980. Outline of the ca E | 
а + 
(Енди) 46: 225—3 | 


WOOD ANATOMY AND CLASSIFICATION OF 
THE MYRTALES' 


GER J. C. M. VAN VLIET? 


AND PIETER BAAS? 


ABSTRACT 


wood anatomical diversity of the woody Myrtal 


es, comprising Combretaceae, Lythraceae (in- 


one Alzatea), Melastomataceae (including Crypteroniaceae), e, Oliniaceae, Onagraceae, 
Реп ае, е included in Lythraceae), Psiloxylaceae, Sonneratiaceae and also 
Thymelaeaceae, is summa ll these families share int 1 т апа vestured pits, апа 
their other wood anatomical чүн represent parts of continuous, sometimes divergent, often 
parallel, specialization series. orace Le ceae, Elati ae, Cor ae, Chrys- 
obalanaceae and Dia pealanthacea are exc uded cates око lack this €—— of characters 
The phylogenetic relationships wi , and pictured in a two-dimensional 


diagram (Figs. 2—8). 
of the vana are with Gentianales 


Features from vegetative anatomy such as bi- 
collateral bundles and vestured pits in the wood 
have entered discussions on the delimitation and 
classification of the order Myrtales for a long 
time. In this paper tl wood 
anatomy will be applied to these taxonomic as- 
pects. The knowledge of the wood anatomy of 
truly or putatively Myrtalean families has con- 
siderably increased in recent years (see references 
cited under the summarized wood anatomical 
descriptions) so that a discussion of its taxonom- 
їс implications can be meaningful. Our paper 
cannot, unfortunately, take wholly herbaceous 
families such as Haloragaceae and Trapaceae into 
consideration. For a survey of all families that 
have, from time to tim me, been assigned to the 
order Myrtales, the reader is referred to Dahlgren 
and Thorne (1984). 


DELIMITATION OF THE ORDER MYRTALES 


All families that have been and are currently 
regarded as indubitable members of the Myrtales 
are characterized by a combination of two ana- 
lomical features: vestures in the bordered pits of 
the secondary xylem, and bicollateral bundles in 
the primary stems (and leaves as far as major 
bundles are concerned), resulting in the presence 
of intraxylary or internal phloem in woody stems 
(not to be confused with interxylary or included 
л ОА 


Myrtales аге disc 
Most ilies | are са. des facis ү The der od anatomical affinities 


phloem, which occurs in a restricted number of 
genera and families of the order only). Several 
authors have also used one or both of these char- 
acters in their delimitation of the order. 

Vestured pits and intraxylary phloem are rath- 
er uncommon in the Dicotyledons, as can be seen 
in Figure 1, where the distribution of these char- 
acters is illustrated iret Dahlgren's (1980) dia- 
grammatic classification. The data are derived 
from Metcalfe and Chalk (1950), completed for 
recent records of vestured pits by Meylan and 
Butterfield (1974), Miller (1977), and Baas and 
Werker (1981). 

The combined occurrence of vestured pits and 
intraxylary phloem appears to be very rare. Out- 
side the Myrtales both features are found only 
in part of the Gentianiflorae (Apocynaceae, As- 

clepiadaceae, Loganiaceae pro parte) and in the 
Thymelacales (Thymelaeaceae only) of Dahl- 
gren's Malviflorae where the two characters are 
further only of very sporadic occurrence in the 
Euphorbiaceae, and then not even simultaneous- 
ly present in the same genera (Bailey, 1933; га 
calfe & Chalk, 1950). Other combined occu 
rences are limited to Vochysiaceae (Polygalaled) 
and the single genus Centropodium of the Poly- 
gonaceae (Polygonales). 

The sporadic occurrence of the two features 
outside the Myrtales as understood by us and 
Dahlgren and Thorne (1984), and their very con- 


. Prof. Dr. С. Kalkman i critically read the nosecript Mr. J. van Os prepared the drawings. In connection 


ec the research pro jec e wood anatomy of th 
the m 1 975-1977 faancially supported by the 


Myrtales, concluded with this paper, the first author was 
Netherlands Organisation for the Advancement of Pure 


2 
оче Botanicus, Nonnensteeg 3, 2311 VJ Leiden, The Netherlands. 
liksherbarium, Р.О. Box 9514, 2300 RA Leiden, The Netherlands. 


ANN. MISSOURI Bor. GARD. 71: 783-800. 1984. 


[ЕЛА 


POLYGONIFLORAE 


CARYOPHYLLIFLORAE 


w 


gore 


NYMPHAEIFLORAE 


Mia 


RANUNCULIFLORAE 


Í MAGNOLIIFLORAE 


MALVIFLORAE 


VIOLIFLORAE 


Г VESTURED PITS 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


Ln n 
CELASTRIFLORAE 


ARALIIFLORAE 


PRIMULIFLORAE 


S 
SS 


(Мог. 71 


2 ROSIFLORAE 
¢ en 
LOASIFLORAE 

ы” 


CORNIFLORAE 


BALANOPHORIFLORAE 


LAMIIFLORAE 


SOLANIFLORAE 
ASTERIFLORAE 


С mentam mor 


Distribution of vestured pits and intraxylary phloem in the Dicotyledons, projected on Dahlgren's 
1980 


classification system ( 
paper referred to Myrtales 


stant presence within the order, strengthen the 
value of these characters for the delimitation of 


alypetalanthus by Rizzini and Occhioni (1949) 
needs confirmation; in a wood sample we stud- 
ied, vesturing is not obvious, but SEM studies 
should be carried out to verify this. These fam- 
ilies also do not recall true Myrtales in other 
combinations of wood anatomical features (cf. 
van Vliet, 1976b, on Rhizophoraceae; Rizzini & 
Occhioni, 1949, 


> 


for other families). Thymelaeaceae, incorporated 
in Myrtales by Cronquist (1968, 1981) but treat- 
ed in Malviflorae or Malvaneae as a separate 


this 
). The cross-hatched part of the Malviflorae represents the Thymelaeaceae, in 


order by Takhtajan (1980) and Dahlgren a 
do share internal phloem and Ды. И wi 

с 
Myrtales and will later i in this paper MEC 
Combretaceae, Lythraceae (including Rhyncho- 
calyx and Alzatea), Melastomataceae (in ^ 
Crypteronia, Dactylocladus, and Ахіла 
Myrtaceae (including Негеторух:5), ош Е, 
Опаргасеае, Репаеасеае, Psiloxylaceae, d 
caceae (could also be included in L hrace e 4 
Thorne, 1976; Baas & Zweypfenning, 1979), 
Sonneratiaceae. 


Woop ANATOMICAL CHARACTERS 
OF THE МУЕТАГЕЗ 
should 


On the taxonomic level of the order d wood 
not expect to be able to provide a conci od аза 
anatomical diagnosis. Yet the major W 
tomical features will be reviewed in ог 
at least a sketchy portrait of the wood 


a ашна 


— 


"0 


1984] 


ONAGRACEAE 


OLINIACEAE 
PUNICACEAE 


VAN VLIET & BAAS—WOOD ANATOMY 


785 


PENAEACEAE 


THY MELAEACEAE 


PS I LOXYLACEAE 


LYTHRACEAE 


SONNERATI ACEAE 


LARGE AND SI 


m ill + А + 4 1 


VESSEL—RAY AND VESSEL—PARENCHYMA PITS 
MPLE 


COMBRETACEAE 


VESSEL— RAY AND VESSEL—PARENCHYMA PITS 
Z SIMPLE, BUT OF THE SAME SIZE AS THE 


INTER-VESSEL PITS, OR WITH REDUCED BORDERS 


FIGURE 2. ; 
м (Ттарасеае апа хоть not considered. Position of Thym 
of vessel-ray and iene Ere eee pits (white areas represent half-bordered pits). A = Alza 
а; Ep = Eucalyptopsis; Eu = Eucal M= 


T types 
СУ = званае D= Dua 


atterns in the woody Myrtales. Entirely herbaceous 
elaeaceae uncertain. Di yy rte sa 


calyptus pro parte; Me кынкы 


So = Sonner. тапа; St = Шашыла an Sy = Syzygium sensu lato; X = Xanthomyrtus. 


of the Myrtales. Thymelaeaceae will not be in- 
cluded in this survey. Constant for the whole 
order are vestured pits and intraxylary phloem 
as mentioned before. The other characters show 
Various degrees of diversity. 

Vessels. A number of Myrtales (most Myrta- 
cae, Penaeaceae, Memecyloideae of the Melas- 


mpl except ix very few Myrtaceae that have 
a ariform plates. Inter-vessel pitting is almost 
Ways alternate, and if deviating from this type 


elongated pits must be considered derived from 


the isodiametric alternate pits (van Vliet, 1981; 
Carlquist, 1975b). Vessel-ray and vessel-paren- 
chyma pits vary widely from half-bordered to 
large and simple. Vasicentric tracheids are typi- 
cal for most Myrtaceae, and some Combretaceae 
and Lythraceae show vascular tracheids and/or 
narrow vessels associated with the normal ves- 
sels. Fibers either have distinctly bordered pits 
and are non-septate (fiber-tracheids; see list of 
Myrtales with solitary vessels above) or more 
commonly are often septate and have simple to 
minutely bordered pits confined to the radial walls 
libriform fibers). Fiber dimorphism, presum- 
ably culminating in parenchyma development 
(i.e., phylogenetically, mot ontogenetically) oc- 
curs in many Melastomatoideae, some Lythra- 
ceae, and weakly in Punicaceae. Parenchyma is 
most typically scanty paratracheal (this type oc- 


ta, 


786 


MELASTOMATACEAE 


ONAGRACEAE 


OLINIACEAE 


PUNICACEAE 


LYTHRACEAE 


SONNERATIACEAE 


FIGURE 3. Distribution of various types of vestured 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


PS ILOXYLACEAE 


(Мог. 71 


PENAEACEAE 


THYME LAE ACEAE 


MYRTACEAE 


COMBRETACEAE 


pits according to van Vliet’s classification (1970 m 


À > or bo 
Myrtales. Families not studied are queried. See also legend to Figure 2; in the case of A/zatea, A stands 


the genus name and the type of vesturing. 


curs in all families); in addition, it may be apo- 
tracheally diffuse or in narrow, short to contin- 
uous broad bands i tati if 


I 1f more 
abundantly paratracheal it varies from vasicen- 
tric, aliform to confluent, to paratracheally band- 
ed; most families are heterogeneous with respect 
to parenchyma distribution. Rays also vary, and 
very often they do not fit into one of the types 
defined by Kribs (1968), but contain exclusively 
square to erect cells; in most taxa with hetero- 
geneous ray tissue the central cells are only weak- 
ly procumbent. Heterogeneous rays, type I-III 
and homogeneous rays occur in a minority of 
genera. The unique feature of radial vessels is 
entirely restricted to tribe Combreteae sensu van 
Vliet (1979). Included or interxylary phloem oc- 
curs in part of the Onagraceae, Combretaceae 
(Combreteae pro parte) and Melastomataceae (all 
Memecyloideae sensu van Vliet, 1981). Crystal 
types and distribution are quite diverse in the 
order and include some unusual forms, which 


may be highly diagnostic for some rean 
groups. Raphides occur in some One ШЫ 
one species of the Melastomataceae. d 
elongate to styloid-like crystals occur in pu 
Myrtaceae, Combretaceae and On 
megastyloids occur in one tribe of the Me di 
matoideae. Clustered crystals or druses are 


toma- 
d for some Combretaceae, ere 


boidal crystals in chambered fibers 1p» 
for a number of Lythraceae, Punicaceae = A 
loxylaceae. Many Myrtales completely d + 
tals in their wood. Silica grains аге ECC 
tirely restricted to part of the Мула а 
of very sporadic occurrence іп the CO 


besides 


o 


eae. и 
Carlquist and Debuhr (1977) include, 


—— 


1984] 


VAN VLIET & BAAS—WOOD ANATOMY 


PENAEACEAE 
MELASTOMATACEAE ITITEITI 
/ 1 | 1 | 1 \ THYMELAEACEAE 
t RUTAS | 
HH 
dou 
" << A a 
HAN = 
[s bd ПОР К 
ГТ HEITT Е 
| BENERE А 
N с 
1 
LIIELLI ка | 
MELLEL 
ONAGRACEAE St 8B 
сч 
a P OLINIACEAE 
РИМТСАСЕЛЕ (1114 ) C 
I—13—313 A 
+ ++ +4 
шш MYRTACEAE 
TI 
LE 
i-i 
ЕЕЕ 
HEA 
| [| PSI LOXYLACEAE A St 
CLE ls 
LYTHRACEAE . 
= 
as 
SONNERATIACEAE —7 
س‎ COMBRETACEAE 
eae 
ae 


LI 
у BRIFORM FIBRES 


Ш FIBRES SEPTATE 


FIGURE 4. Distribution of libriform septate fibers in Myrtales. See also legend to Figure 2. 


vestured pits and intraxylary phloem, the pres- 
boss of crystalliferous strands in axial xylem, in 
their definition of the order Myrtales. We cannot 
Support this, because so many genera entirely 
lack crystals, while in some taxa (e.g., Sonne- 
ratia) crystals are restricted to the ray system. 
°reover, one should not equate such diverse 


. Presence of amorphous contents 
ü so cited by Carlquist and Debuhr 
а typically Myrtalean feature is probably too 
азресіћс to be useful 


Su 
MMARIZED Woop ANATOMICAL DESCRIPTIONS 
OF THE FAMILIES 
(These do not include the common features 


5 
= as vestured pits, or statements on the ab- 
се of unusual features. Type of vesturing is 


left out, because of incompleteness of data, but 
will be discussed in a later section.) 


COMBRETACEAE 


The two subfamilies Combretoideae and Stre- 


р y very dif- 
ferent, necessitating separate descriptions. For 
the tribal delimitation of Combreteae as followed 
here see van Vliet (1979). His Combreteae cor- 
respond to the subtribe Combretineae in Exell 
and Stace’s classification (1966; van Vliet, 1976a, 
1979). 

Combretoideae. Included phloem of the fo- 
raminate type restricted to some genera of the 

tribe Combreteae. Vessels diffuse (wood rarely 

ring-porous or semi-ring-porous), solitary and/ 

or in radial multiples (in Combreteae the normal 

vessels are mixed with very narrow vessels and 


788 


MELASTOMATACEAE 


ONAGRACEAE 


OLINIACEAE 
PUNICACEAE 


LYTHRACEAE 


SONNERATIACEAE o9 


E INCLUDED PHLOEM 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


we 


PSI LOXYLACEAE 


Ш FIBRE-TRACHEIDS 


(Мог. 71 


PENAEACEAE 


[| 


Wi 


THYMELAEACEAE 


LA 


P^ МУЕТАСЕАЕ 


COMBRETACEAE 


rom mer 


* : = vascular 
FiGURES. Included (interxylary) phloem and various fiber features in Myrtales (cf. Fig. 4). c 
tracheids occasionally present; v.t. = vasicentric tracheids common. See also legend to Figure 2. 


vascular tracheids); average diameter 45-280 um, 
average vessel member length 200-650 um; per- 
forations simple; inter-vessel pits alternate; ves- 
sel-ray and vessel-parenchyma pits mostly half- 
bordered, but simple in a restricted number of 
species. Radial vessels (in rays) present in all 
Combreteae. Fibers 500-1,900 um long, walls 
with simple pits (libriform), frequently septate. 
Parenchyma often scanty paratracheal only, in 
part of the genera aliform, confluent or banded 
and infrequently marginal. Rays mostly unise- 
пате, sometimes 1-3(—more)-seriate, weakly het- 


and ray parenchyma; large rhomboidal com- 
pletely filling the cells or in enlarged idioblasts 
of rays and axial parenchyma; rarely styloids; 
large or small clusters (the latter in idioblasts); 


rarely in fibers; absent from some genera. Silica 
rains very rare. j 
: Strephonematoideae. Vessels diffuse, D: 
solitary; average diameter 250-270 um, per 
vessel member length 620—750 um; perfora 
simple; inter-vessel pits alternate; vessel ua 
vessel-parenchyma pits half-bordered. Gr 
tric/vascular tracheids very rare. Fibers dpi 
2,200 um long, walls with distinctly borde ks 
(fiber-tracheids). Parenchyma aliform pto 
fluent and in short apotracheal bands or jue 
Rays heterogeneous II-III. Crystals а 
Amorphous silica very rare. 


LYTHRACEAE 


ily de- 
Rhynchocalyx is included in the pee + 
scription. Alzatea, which has been pues a 
rypteroniaceae by van Beusekom-Os! d 
van Beusekom (1975) but can be accomm 


| 
| 


€——— 


VAN VLIET & BAAS—WOOD ANATOMY 


1984] 
PENAEACEAE 
THYME LAEACEAE 
MELASTOMATACEAE 
inm. 
26 3 
Eri 
) Тү 1 
Lf TTT TTD 
T TIS. 
Ir I L с 
LIT I j E! 
КЕТ m 
T ТЕ 
a H | : 
SED SED Sn d 1 
ONAGRACEAE T +: = 
Sy а. 
OLINIACEAE 444+? 
PUNICACEAE T E 
Eu = MYRTACEAE 
Ep 
PS I LOXYLACEAE 


LYTHRACEAE 


SONNERATIACEAE C8 


ЕЕЕ PARENCHYMA APOTRACHEALLY DIFFUSE TO 
DIFFUSE-IN-AGGREGATES 


COMBRETACEAE 


ППШ VESSELS MOSTLY SOLITARY (80% OR MORE) 


FIGURE 6. Distribution of primitive conditions of vessel grouping and parenchyma distribution in Myrtales. 


See also legend to Figure 2. 


in Lythraceae (Lourteig, 1965; Baas, 1979), pos- 
Sibly merits subfamily status, and its wood an- 
atomical characters are listed separately as far as 
they deviate from the remainder of the family 
5 & Zweypfenning, 1979; Baas, 1979). 
Vessels diffuse (wood rarely ring-porous o 
Semi-ring-porous), frequently in radial multiples; 
average diameter 30-220 a 1 


а simple and fairly large. Vascular tra- 
with very rare. Fibers 380–1,350 um long, walls 
t simple to minutely bordered pits, frequently 
tege In some genera dimorphous with alter- 
di 8 bands or areas of normal and paren- 
yma-like fibers. Parenchyma mostly scanty 
“ao only, rarely apotracheally diffuse, 
tiii ntric or aliform to confluent (and then de- 
via fiber-dimorphism). Rays mostly uni- 


seriate (rarely 2—3-seriate), heterogeneous II or 
composed of erect cells only; rarely homoge- 
neous. Crystals rhomboidal in chambered fibers 
or chambered axial parenchyma strands in part 
of the family, rarely in ray cells; often entirely 
absent. 

Alzatea. Average vessel member length 730 
um; vessel-ray pits large and simple; rays 1—3- 
seriate, heterogeneous I-II. 


MELASTOMATACEAE 


Three subfamilies with distinctive wood anat- 

ized: Melastomatoideae, Me- 
mecyloideae and Crypteronioideae. e tradi- 
tionally recognized subfamily Astronioideae has 
been abolished: Prternandra (including Kibessia) 
is transferred to Memecyloideae as a se te 
tribe; Astronieae (four genera) are transferred to 
the Melastomatoideae (see van Vliet, 1981). The 


790 


MELASTOMATACEAE 


.. 
SR. 


ONAGRACEAE 


OLINIACEAE 
PUNICACEAE 


LYTHRACEAE 


TTE 
SONNERATIACEAE 


ES LT 
LUCERE со 


FE. ] RAYS HETEROGENEOUS III 


Fi 
been modified to include woods 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


PSILOXYLACEAE 


(Мог. 71 


PENAEACEAE 


THYMELAEACEAE 


COMBRETACEAE 


NANT 
SQUARE CELLS PREDOM 
== RAYS HOMOGENEOUS ERECT AND SQ 


, 68) has 
IGURE 7. Distribution of variously specialized ray types in Myrtales. Krib's ray classifica au be 
exclusively uniseriate rays in his Heterogeneous III type. Whi 


with 
represent more strongly heterogeneous Pa heterocellular) rays. See also legend to Figure 2. 


Crypteronioideae include Axinandra, Cryptero- 
tylocladus (van Vliet, 1975, 1981; 

, 1981; ter Welle & Koek-Noor- 
man, 1979, 1981; ter Welle & Mennega, 1977). 

Melastomatoideae. Vessels diffuse, frequently 
in multiples; average diameter 50-340 um, av- 
erage vessel member length 200—1,000 um; per- 
forations simple; inter-vessel pits alternate, al- 
ternate plus elongate and curved, or scalariform 
(and then as a derivation from alternate!); vessel- 
ray and vessel-parenchyma pits mostly simple 
and large, often in a reticulate or scalariform pat- 
tern. Fibers 300-1,500 um long, walls with simple 
or very minutely bordered pits (libriform), fre- 
quently sep е., with paren- 
chyma-like fibers in narrow tangential arcs, or 
confluent and banded patterns Parenchyma 
mostly scanty paratracheal, or also apotracheally 
diffuse within the bands of parenchyma-like fi- 
bers; infrequently in continuous bands (and then 
presumably derived via fiber dimorphism). Rays 
often uniseriate (also 1—7-seriate), mostly com- 


posed of erect, square and weakly procul 
cells, rarely homogeneous (1.е., entirely me 
posed of procumbent cells). Crystals often " 
sent; raphides present in one species; Wem 
loids infrequent in one tribe; clustered crys er 
in са restricted to species with band 

a omniste Included phloem of йс 
raminate type present. Vessels diffuse зе ЖЩ 
itary; average tangential diameter 40- me 
average vessel member length 250-500 p sb й 
forations simple; inter-vessel pits (if oe pits 
ternate; vessel-ray and Vi рет 280-20 um 


uniseriate and ко: о 


1984] 


MELASTOMATACEAE 


OLINIACEAE 


PUNICACEAE 


.. 5 
و ی‎ a 
re .. 


LYTHRACEAE 


| „жаны. | 
ШШЩ ји SONNERATIACEAE 
WW 


П RAPHIDES 


Distrih 


An 4 


VAN VLIET & BAAS— WOOD ANATOMY 


PSILOXYLACEAE 


[i] снамвевер, CRYSTALLIFEROUS FIBRES 


791 


PENAEACEAE 


THYMELAEACEAE 


SOLITARY CRYSTALS, ALMOST COMPLETELY FILLING 
RAY CELLS 


gS QE 


Crypteronioideae. Vessels diffuse, solitary 
and/or in radial multiples; average diameter 80– 
170 um, average vessel member length 390-1,120 
4m; perforations simple; inter-vessel pits alter- 
nate; vessel-ray and vessel-parenchyma pits half- 
bordered, rarely also simple. Fibers 600–1,550 
^m long, walls with distinctly bordered pits (fi- 
ber-tracheids). Parenchyma diffuse in aggregates 
ог aliform to confluent. Rays uniseriate or 1-3- 
Serıate, heterogeneous I or III. Crystals absent. 


MYRTACEAE 

i Combined description of the two traditionally 
— subfamilies Myrtoideae and Lepto- 
e Schmid (1980) recognized two 
subfamilies: Chamaelaucioideae (for- 
For 1» Leptospermoideae) and Psiloxyloideae. 
Practical reasons the latter is still treated by 
ne а separate family: Psiloxylaceae (Ingle & 

dswell, 1953; Dadswell, 1972; Metcalfe & 
“a 1950; supplemented with original obser- 
tion) 5 On slides in the Rijksherbarium collec- 


Е ІС s t fA; dat s РА е UON ME . 
cells) in Myrtales. e — elongate crystals; m.s. — megastyloids. See also legend to Figure 2. 


1 
y ray or parenchyma 


Vessels diffuse, often forming oblique patterns 
(wo 1 
solitary, bu 
(Agonis, Angophora, Eucalyptopsis, Eucalyptus 
section Corymbosae sensu Dadswell, 1972; Lep- 
tospermum pro parte; Syzygium sensu lato sensu 
Schmid, 1972, i.e., an alliance of genera includ- 
ing Syzygium, Acmena, Cleistocalyx and Pilio- 
calyx, conforming to Ingle & Dadswell’s Eugenia 
*B' complex, 1953, or the Acmena-alliance sensu 
Briggs & Johnson, 1979; and Xanthomyrtus); av- 
erage diameter 30-250 um, average vessel mem- 
ber length 260-1,090 um (mostly 400—800 um); 
perforations simple, very rarely scalariform 
(Neomyrtus— Butterfield & Meylan, 1974, Mey- 
lan & Butterfield, 1978; Myrceugenia — Metcalfe 
& Chalk, 1950, Rudolf Schmid, unpubl. data; 
Luma —original observation, and Rudolf Schmid, 
unpubl. data; Ugni, Myrteola, and several other 
montane and cool temperate genera of Central 
and South America— Rudolf Schmid, unpubl. 
data; the record for Myrtus communis in Met- 
calfe & Chalk, 1950, is certainly incorrect); inter- 


792 


vessel pits (if present) alternate; vessel-ray and 
vessel-parenchyma pits half-bordered or simple 
(sometimes large). Vasicentric tracheids mostly 
present, but absent from Eucalyptopsis, Euca- 
lyptus pro parte, and Syzygium sensu lato (see 
above). Fibers 400—1,500 um long, mostly with 
distinctly bordered pits (fiber-tracheids), but with 
simple to minutely bordered pits d in 
Eucalyptopsis, Eucalpytus pro parte, Syzy 

sensu lato and Xanthomyrtus; very rarely чой 
(Metcalfe & Chalk, 1950; Meylan & Butterfield, 
1978; Moll & Janssonius, 1918). Parenchyma 
typically apotracheally diffuse or diffuse-in-ag- 
gregates, in addition scanty paratracheal to vasi- 
centric in many genera, more rarely confluent or 
even in wide or narrow paratracheal bands. Rays 
mostly 1—3-seriate, sometimes up to 8-seriate, 
rarely uniseriate; heterogeneous II in most Myr- 
toideae, more rely heterogeneous I in this 
subfamily; in I ys often more 
weakly кеша A to almost homogeneous 
(in Eucalyptus pro parte, Leptospermum pro 
parte, cf. Baas, 1977). Crystals if present, mostly 
small, rhomboidal in chambered axial paren- 
chyma cells in both subfamilies; rarely elongate 
in slightly enlarged cells; solitary crystals in en- 
larged idioblasts infrequent in some genera 
(Agonis, Calycorectes, E 78 рго parte, Feijoa, 
Leptospermum pro pro parte, 
Myrciaria, and Nothomyrcia); druses rare in Eu- 
genia (Chattaway, 1955). Crystals always absent 
from rays. Silica grains present in rays of at least 
12 genera of the Leptospermoideae (in addition 
to ten genera mentioned by Ingle & Dadswell 
(1953), also in COONS, original obser- 
vation, and X. ,Am 
1952, a gen. nov. according to Briggs & J был: 
1979), and rare in two genera (rays of Osbornia, 
parenchyma of Jambosa; cf. Amos, 1952) of the 
Myrtoideae. 

Note that within Myrtaceae, Syzygium sensu 
lato and Xanthomyrtus (Myrtoideae), together 
we Eucalyptopsis e  Fucabyptus pro parte 
(1 


t of their 
much higher level of xylem specialization: libri- 
form fibers, vessels in multiples, aliform to con- 
fluent parenchyma and large and simple vessel- 
ray and vessel-parenchyma pits all emphasize 
this (the two latter features also occur scattered 
in a few genera). Wood anatomical differences 
of this magnitude coincide in other Myrtalean 
families (Melastomataceae and Combretaceae) 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


with subfamily boundaries, also marked by mac- 
romorphological differences. 

Silica grains may appear to be of considerable 
taxonomic interest in the Leptospermoideae. 
They are present in all genera of the Metrosi- 
deros-alliance sensu Briggs and Johnson (1979) 
so far studied wood anatomically. The only ex- 
ception is Kjellbergiodendron. Interestingly 
enough this genus has been transferred to 
Myrtoideae by Schmid (1980) on the basis of 
both macromorphological and anatomical fea- 
tures. Outside the Metrosideros-alliance silica has 
only been found in one suballiance (Calotham- 
nus) of the Leptospermum-alliance. 


OLINIACEAE 


Vessels diffuse, frequently in multiples; aver- 
age diameter 50-70 um, average vessel member 
length 500—600 um; perforations simple; inter- 
vessel pits alternate; vessel-ray and vessel- 
parenchyma pits half- bordered. Fi ibers 900-1,000 


Cutler, 1974). 
ONAGRACEAE 


Combined description of the six tribes: Ер“ 
lobieae, Fuchsieae, Hauyeae, Јиѕѕіаееае, Lope- 
zieae and Onagreae (Metcalfe & Chalk, 1950; 
Carlquist, 1975b, 1977). 

Included phloem of the foraminate type often 


ul- 
present. Vessels diffuse, frequently in m 


ple; inter-vessel pits alternate, someti 
gate and curved (in Epilobieae, Fuchsieae, a 
pezieae, Onagreae pro parte); vessel-ray íi 
vessel-parenchyma pits Ме = 
sometimes with reduced borders 
820 um long; walls with simple pit 
often septate, or at least nucleate. 
mostly scantly paratracheal, apotra rach 
rare in Hauyeae, apotracheal par 
associated with included phloem. Rays Ш! 
ultiseriate, often predominantly of upright cel 


Fibers 
5 (libriform); 
Parenchym4 


а also 
- 10 


fiber- 
in axial parenchyma, rarely also in = йй! in 
like cells; sometimes rhomboidal to € bed 
non-chambered fibers, and in rays, OF 2 


| 


| 


О Т" чл 


= 


— 


1984] 


PENAEACEAE 


Vessels diffuse, predominantly solitary; aver- 
age diameter 20—55 um, average vessel member 
length 310-890 um; perforations simple; inter- 
vessel pits alternate when present; vessel—ray and 
vessel-parenchyma pits half-bordered. Fibers 
380-1,170 um long, walls 
dered pits (fiber-tracheids). Parenchyma scanty 
paratracheal and scanty apotracheally diffuse. 
Rays mostly uniseriate and composed of erect 
and square cells, or 1—3-seriate and heteroge- 
neous II. Crystals mostly absent, but present as 
druses or clusters in chambered parenchyma cells 
in one species, and as irregular aggregates in 
another (Carlquist & Debuhr, 1977). 


PSILOXYLACEAE 


Vessels diffuse, mostly in multiples; average 
diameter ca. 50 um, average vessel member length 
550-570 um; perforations simple; inter-vessel pits 
alternate; vessel-ray and vessel-parenchyma pits 
half-bordered. Fibers with minutely bordered pits 


see also Baas & Zweypfenning, 1979). 

Note that Schmid (1980) refers to distinctly 
bordered pits and apotracheal diffuse paren- 
chyma for Psiloxylon; in the material at our dis- 
Posal (Lorence 1488) the pit borders are very 
small (са. 1.5-2 um); apotracheal parenchyma 
has not been observed and can at most be very 
infrequent. Our observation of rhomboidal crys- 
tals in ray cells is new. 


PUNICACEAE 


This monotypic family could also be accom- 
Modated in Lythraceae (cf. Thorne, 1976; Baas 
19, Pfenning, 1979) (Bridgwater & Baas, 

Vessels diffuse, frequently in multiples; aver- 
hus Mer 40-70 um, average vessel member 
n ben i 250-330 um; perforations simple; inter- 

pits alternate; vessel-ray and vessel- 
oe pits half-bordered. Fibers 460-540 
‘ong, walls with simple pits (libriform), sep- 
ao” to fiber dimorphism observed in 
dieit samples. Parenchyma scanty paratra- 
9 virtually absent. Rays mostly uniseriate 


VAN VLIET & BAAS- WOOD ANATOMY 


793 


(rarely up to 3-seriate), composed of erect to 
weakly procumbent cells. Crystals rhomboidal, 
frequent in chambered fibers. 


SONNERATIACEAE 


Vessels diffuse, frequently in multiples; aver- 
age tangential diameter 120—160 um in Sonne- 
ratia, 120—230 um in Duabanga, average vessel 
member length 400—500 um in Sonneratia, 600— 
800 um in Duabanga; perforations simple; inter- 
vessel pits alternate; vessel-ray and vessel- 
parenchyma pits mostly half-bordered in Son- 
neratia, large and simple in Duabanga. Fibers 
700—1,000 um long in Sonneratia, 1,200—1,400 
um long in Duabanga; walls with simple pits 
(libriform); septate in Sonneratia only. Paren- 

} tin Sonneratia, aliform to confluent 
in Duabanga. Rays uni(—bi)-seriate, composed 
of weakly procumbent cells, with occasionally 
(e xs 2 4 ۹ 


( ) commonly ( га) за to 
erect marginal cells. Crystals rhomboidal; in 
Sonneratia large and almost completely filling 
the ray cells; in Duabanga smaller and some- 
times accompanied by minute crystals in axial 
parenchyma and ray cells (Metcalfe & Chalk, 
1950; Venkateswarlu & Rao, 1964, comple- 
mented with original observations). 

Note that the above data deviate to some ex- 
tent from those by Venkateswarlu and Rao 
(1964), which in our opinion is due to some er- 
roneous observations by these authors. Moll and 
Janssonius (1918) described some form of fiber- 
dimorphism: around some of the vessels the fi- 
bers are more thin-walled and have small inter- 
cellular spaces between them. This weak form of 
fiber dimorphism, presumably due to the effect 
of enlarging vessels on fiber differentiation, should 
not be identified with fiber dimorphism as occurs 
in Melastomataceae and some Lythraceae. 


THY MELAEACEAE 


Included phloem (of the foraminate or con- 
centric type) present in nine genera. Vessels dif- 
fuse, frequently in multiples, in part of the family 
in clusters or dendritic patterns; average diam- 
eter ca. 30—160 um, average vessel member length 
150—400 um; perforations simple; inter-vessel pits 
alternate; vessel-ray pits half-bordered. Tra- 
cheids (vasicentric and/or vascular) present in 
some genera with clustered or dendritically ar- 
ranged vessels. Fibers 300-900 um long, mostly 
with distinctly bordered pits mainly confined to 


794 


radial walls, but in some genera pits with strongly 
reduced to almost simple borders. Parenchyma 
scanty paratracheal to vasicentric, or aliform; 
sometimes also with apotracheal narrow bands 
or diffuse parenchyma. Rays 1-4(-9)-seriate, 
often almost or entirely homogeneous, some- 
times heterogeneous, composed of weakly pro- 
cumbent central cells and square to erect mar- 
ginal cells. Crystals often absent, if present small, 
solitary, diamond-shaped, or elongate in ray Cells 
and parenchyma cells; large styloids in included 
phloem of Aquilaria; crystalline masses or crystal 
sand doubtfully present in few genera (Metcalfe 
& Chalk, 1950; supplemented with original ob- 
servations on a limited number of genera). 


DISCUSSION 


Although the previous descriptive sections, 
partly pictured in Figures 2-8, show a consid- 
erable diversity, the order Myrtales as delimited 
by Dahlgren and Thorne (1984) and us is wood 
anatomically a fairly closely knit assemblage. The 
possible inclusion of Thymelaeaceae, the rela- 
tionship patterns within the order as evident from 
the wood anatomical variation patterns, and the 
wider affinities will be the subject of our further 
discussions. 


POSITION OF THYMELAEACEAE 


Although treated outside Myrtales by several 
authors (Takhtajan, 1980; Dahlgren, 1980; 
Dahlgren & Thorne, 1984), Cronquist (1968, 
1981) has advanced arguments to treat Thyme- 
laeaceae as an ordinary member of the order. 
Wood anatomy tends to support this opinion; 
apart from the shared intraxylary phloem and 
vestured pits, there are other similarities. In fact 
all wood anatomical characters of the Thyme- 
laeaceae can be retraced in the order Myrtales, 
albeit not in a single family (Figs. 2-8). The oc- 
currence of interxylary (included) phloem in a 
number of Thymelaeaceae as well as in anumber 
of Onagraceae, Combretaceae and Melastoma- 
taceae, is especially significant, because this fea- 
ture is rather uncommon in Dicotyledons as a 
whole. The fibers with distinctly bordered pits 
in Thymelaeaceae are a bit unlike the fiber-tra- 
cheids of Myrtaceae, Combretaceae pro parte, 
Penaeaceae and Melastomataceae pro parte, be- 
cause the pits are largely confined to the radial 
walls. The slightly elongate crystals of some 
Thymelaeaceae recall certain Combretaceae and 
Myrtaceae. In view of the somewhat reticulate 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


and faint wood anatomical affinities with the 
‘core’ families of the Myrtales, we would advo- 
cate a fairly isolated position, also in view of its 
other deviating attributes (cf. Dahlgren & Thorne, 
1984; Cronquist, 1981). The position of Thyme- 
laeaceae near Euphorbiales and Malvales in the 
Dilleniideae (Takhtajan, 1980) or Malviflorae 
(Dahlgren, 1980; Thorne, 1981; Tan, 1980), finds 
no support in wood anatomy. Vestured pits and 
included phloem never occur together in the oth- 
er families of this superorder: vestured pits occur 
in Dipterocarpaceae and some Cistaceae; their 
presence in Euphorbiaceae is restricted to Bri- 
delieae (two genera); intraxylary phloem occurs 
sporadically in some other Euphorbiaceae and 
would merit further study to establish whether 
it is really comparable to the type of internal 
phloem occurring in Myrtales. 


RELATIONSHIPS WITHIN THE MYRTALES 


Ideally one would like to construct a phylo- 
genetic system for the Myrtales, based on the 
occurrence of shared, uniquely derived special- 
izations, as was attempted for Lythraceae (Baas 
& Zweypfenning, 1979) and Neotropical Melas- 
tomataceae (ter Welle & Koek-Noorman, 1981). 
At the ordinal level, most wood anatomical char- 
acters are, however, unsuitable for such а cla- 
distic approach, because of the high probability 
of parallel specialization lines in individual fam- 
ilies. Thus the occurrence of homogeneous rays 
in some I ythraceae, N Telast taceae. and Com- 
bretaceae d t point to mutual affinity actos 
the family boundaries; likewise the specialization 
series from fiber-tracheids to libriform ripe 
probably occurred more than once in the о 
even within the family Myrtaceae the e 
of libriform fibers in the minority of bo" 
subfamilies probably represents parallel et 
ization. The same applies to specialized patte 
of parenchyma distribution. 


nal Bailey 
alization it 15 


f the 


: 0 
anatomy of the putative common ancestor 


Myrtales (cf. Carlquist, 1961, 1962, 19750 
summaries of and additions to these trends: =" 
Carlquist, 1980; Baas, 1973, 1982, mrs 
sion of possible reversions). Most р si 
acter states hypothesized for this o: of 
cestral stock are still represented in a n of 
extant Myrtales as well as in a fair num The 
Angiosperm families from other orders. 


| 


| 


1984] 


combination of ancestral characters can serve as 
a starting point to discuss the mutual affinities 
within the Myrtales, as well as the putative af- 
finities with other orders. A wood anatomical 
diagnosis of ‘Protomyrtales’ would read as fol- 
lows: 


Vessels mostly solitary, with scalariform per- 
forations (only retained in a few genera of the 
Myrtaceae) and alternate, vestured pits, half- 
bordered where in contact with rays and axial 
parenchyma. Vestures of uniform thickness 
attached to the entire roof of the pit chamber 
(van Vliet’s type A, 1978). Ground tissue of 
fiber-tracheids. Parenchyma scanty paratra- 
cheal and apotracheally diffuse. Rays hetero- 
geneous I. Crystals in axial parenchyma and/ 
or ray cells, probably of several types. Jntraxy- 
lary phloem present. 


The following specializations from this ancestral 
type are evident: 


l. Vessels tending to be arranged in (mostly 
short) radial multiples (most families; cf. Fig. 6 
all groups without vertical hatching). This com- 
mon specialization within the Dicotyledons has 

obably 1 several times within the order. 

2. Vessel-ray and vessel-parenchyma pits with 
reduced borders to simple, and ultimately large 
and mostly in a reticulate or scalariform pattern 
(Fig. 2). This specialization is most evident in 
Melastomataceae, Myrtaceae pro parte, A/zatea 
and Lagerstroemia of the Lythraceae, and Dua- 
banga of the Sonneratiaceae; probably at least 
Partly as a result of parallel development. 

3. Concentration of vestures around the pit 
apertures and development of trunk-like bases 
(van Vliet's series of types A, B1, B2, B3). This 
hypothetical specialization trend occurs within a 
number of families and is based on the fact that 
‘ype A mostly occurs in the representatives that 
have retained the highest number of primitive 
attributes in their wood (Strephonematoideae of 
Combretaceae: Sonneratia of Sonneratiaceae; 
Alzatea of Lythraceae; cf. Fig. 3). In Melasto- 
coe the vesturing is predominantly of type 

» and the slightly more specialized type ВІ is 
confined to a few Melastomatoideae—the wood 
мађ most specialized subfamily. In 
“= Ceae a range from types A-B2 has been 

untered, but too few representatives have 

i n studied submicroscopically to relate these 
Ypes to classification. 

4. Reduction of pit borders and limitation of 


VAN VLIET & BAAS— 


WOOD ANATOMY 795 


pits to radial walls in fibers (i.e., shift from fiber- 
tracheids to libriform fibers) followed by or con- 
comitant with septation of the fibers (Fig. 4). 
Lythraceae, Sonneratiaceae, Punicaceae, Psilo- 
xylaceae, Onagraceae, Oliniaceae and the largest 
subfamilies of Melastomataceae and Combre- 
taceae show this specialization; within Myrta- 
ceae it occurs isolated in the two major subfam- 
ilies. Fiber dimorphism represents a further 
specialization, and is limited to part of the Ly- 
thraceae, Melastomatoideae and Punicaceae. 

5. Parenchyma specialization (quite possibly 
reversible), presumably followed three different 
courses: a. Reduction leading to exclusively very 
scanty paratracheal parenchyma, or total ab- 

nce ofr hy ( t families, notably Me- 
lastomataceae, Lythraceae, Onagraceae, Puni- 
caceae, Psiloxylaceae, Oliniaceae, Sonneratia of 
Sonneratiaceae and Thymelaeaceae pro parte). 
b. Increase of paratracheal parenchyma (often 
paralleled by a decrease in apotracheal paren- 
chyma). This specialization is evident in part of 


ч 
о 


Тћутејаеасеае. с. The presumed development of 
banded parenchyma through fiber dimorphism in 
Lagerstroemia pro parte of the Lythraceae and 
some members of the Melastomatoideae. 

6. Ray specialization also occurred along di- 
verging lines: a. Towards a higher proportion of 
procumbent cells, and greater procumbency of the 
marginal cells (i.e., the classical specialization 
series according to Kribs, 1935, modified in 
1968): Heterogeneous I-II-III-Homogeneous. 
The homogeneous (or rather homocellular) end 
station is represented by few Myrtales only, least 


is especially common in Melastomataceae, O 
agraceae, Lythraceae and Punicaceae. Penae- 
aceae and Combretaceae also show this feature 
in some species but here it is not certain whether 
this should be ascribed to the truly juvenile na- 
ture of the material studied. In the former fam- 
ilies many species also never develop substantial 
amounts of wood, but some representatives at 
least do show the juvenilistic tendencies in their 


796 


rays at the periphery of thick trunks. Carlquist 
(1962) developed the hypothesis of paedomor- 


ber of woody plants such as 
giant lobelias and senecios that have probably 
evolved from a herbaceous ancestry. For the 
Myrtales involved, such ‘secondary woodiness' 
is not necessarily indicated—the perpetuation of 
juvenile characters throughout the development 
of secondary xylem may also be hypothesized 
for basically woody plants (cf. Baas, 1982). с 
v opes of ray width of the originally 1—4-se- 
rays to uniseriates (most families), or spo- 
jede phylogenetic increase in ray width (partly 
recapitulated in ontogeny) in e.g., some scandent 
Melastomataceae. 

7. Origin of interxylary (included) phloem in 
Memecyloideae, Combretoideae pro parte, On- 
agraceae pro parte and Thymelaeaceae pro parte 
probably independently of each other (Fig. 5). 

8. Miscellaneous specializations: a. Origin of 
radial vessels in the rays of one tribe of the Com- 
bretoideae. b. Development of vasicentric tra- 
cheids in Myrtaceae. This possibility might be 
questioned. In view of the numerous primitive 
wood attributes of the Myrtaceae one might also 
hypothesize that vasicentric tracheids belong to 
the set of ancestral characters of the Myrtales, 
and that this feature (like scalariform perforation 
plates) was lost in all families except one. c. De- 
velopment of vascular tracheids (reduction of very 
narrow vessels) in some Lythraceae, Combre- 
taceae and Thymelaeaceae (Fig. 5). d. Develop- 
ment of chambered crystalliferous fibers (Psilo- 
xylaceae, Lythraceae pro parte and Punicaceae) 
(Fig. 8). e. Development of megastyloids in some 
Melastomataceae, possibly from an ancestral type 
with rhomboidal to elongate crystals. It is very 
difficult to picture the other crystal types as prim- 
itive or specialized. Raphides, which represent a 
highly complex type of calcium oxalate deposi- 
tion, are OS in distribution i in the Dicot- 


cote raphides are more common. One can 
hardly imagine that in Onagraceae this feature 
evolved ‘de novo’ as a new specialization; it seems 
more likely that the expression of such a pre- 
sumably old character in derived families is still 
triggered by unaltered genotypical information. 
The lack of raphides does not imply that the 
information is absent but that perhaps it is in- 
complete or blocked by other genes; such a hy- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


pothesis would also be compatible with the ‘stray’ 
occurrence of raphides in one Bredia species of 
the Melastomataceae (van Vliet, 1981). By the 
same token, the haphazard occurrence of elon- 
gate crystals or druses (Fig. 8—rare features in 
the wood of Dicotyledons) might still witness 
(ancient?) links between the families sharing them 
in some of their species. 


The distribution of some of the primitive and 
‘ivari СЇ As к Ee T tha 


different families of the Myrtales is given in Fig- 
ures 2-8; in fact the arrangement of the families 
is the result of these wood anatomical distribu- 
tion patterns. There appears to be a high degree 


of correlation of primitive characters in some of 


the families or subfamilies and of derived char- 
acters in the remaining ones. Primitive charac- 
ters like solitary vessels, fiber-tracheids, and apo- 
tracheal parenchyma occur together in the 
majority of Myrtaceae, in Strephonematoideae 
ofthe Combretaceae, Memecyloideae, Cryptero- 
nioideae pro parte, and Penaeaceae. In al these 
groups, at least part of the species show hetero- 
geneous rays with a clear distinction between the 
procumbent, central cells and square to erect 
marginal cells in one to several rows. The most 
rimitive wood anatomical feature of the order, 
scalariform perforations (few Myrtaceae), coin- 
cides with these other primitive features. As 
as is known, the presumed primitive type of ves- 
turing also occurs relatively frequently in у 
taxa. Thymelaeaceae share primitive fibers, 47 
to some extent parenchyma distribution, but E 
generally more specialized in vessel grouping an 
ra ~ one 
A the common retention of prine 
features is not a sound basis for postulating Wc 
phylogenetic affinity, the above taxa still re a 
many of the ancestral бәрү, i de Myrtal 
nd evince at least common 
7 -ih the above it E пон e 
the opposed, specialized character states (v ү 
in multiples, libriform fibers (mostly septate 
duced or abundant paratracheal рагепс chy m је 
show a high degree of correlation in the yer 
ing taxa: Combretoideae of the Combre Olini- 
Sonneratiaceae, Lythraceae, aceae and Ме -— 
aceae, Psiloxylaceae, Onagraceae = 
matoideae of the Melastomatace : "il 0 
dence of specialized rays (heterogeneous inet 
homogeneous, and juvenilistic rays) 15 T€ 
high in these families, as is the occurrence gi 
more derived types of vesturing (yp шо, 
Within the Myrtaceae, Syzygium se 


these — 


| 


1984] 


Xanthomyrtus, Eucalyptopsis and Eucalyptus pro 
parte share the high specialization level of the 
above mentioned families. 

Of these wood anatomically specialized core 
families of the Myrtales, Psiloxylaceae, Olini- 
aceae, and some Lythraceae (notably A/zatea) 
have retained a low level of specialization in their 
rays (heterogeneous I) Especially the wood of 
Psiloxylon and Olinia (half-bordered vessel-ray 
pits) probably resembles that of the ancestor that 
gave rise to the diversely specialized types in this 
part of the order (the *Protolythraceae' type of 
Baas & Zweypfenning, 1979). Lythraceae and 
Punicaceae can be directly linked to this type, 
especially to Psiloxylon, through the shared crys- 
talliferous fibers. 

Of Sonneratiaceae, especially Sonneratia still 
retains many ancestral features but shows minor 
specializations in its uniseriate rays and (al- 
most?) total absence of axial parenchyma; Dua- 
banga diverged wood anatomically into another 
direction (aliform to confluent parenchyma, large 
and simple vessel-ray pits, homogeneous rays) 
and has a much higher specialization level. On- 
agraceae could also be derived from this type, 
but acquired (and/or retained) features that tend 
to underline a somewhat isolated position such 
as included phloem, rod-like crystals with one 
indented and i d end (Carlquist, 1975b), 


and raphides. 

For Combretoideae and Melastomatoideae the 
Story is more complex; these taxa belong to fam- 
ilies «assis. I ve ins 
Шуе Protomyrtalean wood anatomical syn- 
drome. If Combretaceae and Melastomataceae 
аге monophyletic families, this implies that the 
Specialized wood anatomies in the majority of 
their representatives arose independently from a 
more primitive type than that represented in the 
Protolythraceae type, and that the specialized 
Combretaceae and Melastomataceae are not so 
LAE related to, for instance Sonneratiaceae and 
du respectively, as their wood structure 
кы Еог Combretaceae this is quite 
Sore е, because the family does not resemble 

тапасеае so strongly. For Melastomata- 


Ceae and Lythraceae i 
Similarities are 
devel, 


many striking 
a result of parallel or convergent 
pits in 1 I ! ism; large vessel-ray 
ac Melastomatoideae and part of the 
"i NT gs in Alzatea and Lagerstroe- 
Ytlopm parte; Juvenilistic rays; etc.). Parallel de- 
= ents are more likely to occur in closely 

(i.e., genetically similar) groups; the sim- 


nm £1 
к 


f 
РУМ ЛОСТ 


VAN VLIET & BAAS—WOOD ANATOMY 


797 


ilarities in wood structure resulting from parallel 
or convergent evolution may thus still witness 
affinities: it seems therefore plausible to hypoth- 
esize a direct derivation of the ‘Protolythraceae’ 
type from the immediate precursor of Melasto- 
mataceae (which must have been very similar, 
if not identical, to the Protomyrtales type giving 
rise to Myrtaceae, Penaeaceae, and Combreta- 
ceae). 

The arrangement of Myrtalean families in the 


pe for Thymelaeaceae is not only a reflection 
of its presumed isolated position, but also of our 
more limited understanding of this family, sim- 
ply because we did not study enough represen- 
tatives in sufficient detail. The arrangement of 
the woody ‘core’ families is based on a combi- 
nation of phenetic and phylogenetic classifica- 
tion principles; more emphasis on phenetic sim- 
ilarities, e.g., the shared possession of interxylary 
phloem, would put Combretaceae, Melastoma- 
taceae and Onagraceae much closer to each oth- 
er, but, as explained above, the acquisition of 
this character presumably occurred more than 
once in the evolutionary history of the order. 
However, the great distance between Combre- 
taceae and Melastomataceae in our diagram is 
primarily the result of our priority to put Stre- 
phonematoideae near Myrtaceae and Combre- 
toid 5 i ; and not because we 


anatomy could support the splitting of each into 
two or three separate families. Likewise, the per- 
fect fit of Psiloxylon and Olinia wood with Ly- 
thraceae, has not resulted in the submerging of 
these genera in Lythraceae in view of evidence 
from other characters; e.g., the secretory cavities 
of Psiloxylon, which suggest Myrtaceae, as 
strongly advocated by Schmid (1980). 

The splitting of the order Myrtales sensu lato 
into Lythrales and Myrtales as suggested by Briggs 
and Johnson (1979) cannot be supported by wood 
anatomy, but has also been withdrawn by these 
authors and thus needs no further comments 
(Johnson & Briggs, 1984). 

We are aware that our arrangement of families 


798 


can be opposed if emphasis is put on other char- 
acter complexes, or if most known attributes are 
simultaneously employed (as attempted by 
Dahlgren & Thorne, 1984). In our opinion, any 
so-called conflicting evidence will only strength- 
en the tissue of intimate relationships between 
the core families of the Myrtales. If floral and 
leaf structure for instance point to a Myrtaceous 
nature of Psiloxylon, while the wood witnesses 
Lythraceous affinities, Psiloxylon only bridges a 
gap between Lythraceae and Myrtaceae; simi- 
larly presumed affinities of A/zatea with Cryp- 
teronia (van Beusekom-Osinga & van Beuse- 
kom, 1975) in combination with the Lythraceous 
wood anatomy of Alzatea, provides additional 
evidence of relationships between Melastoma- 
taceae and Lythraceae. The main conclusion can 
only be that whatever minor adjustments one 
wishes to make in the classification, the 10 core 
families of the Myrtales, possibly with the ad- 
dition of Thymelaeaceae, are a very natural as- 
semblage of closely related families. 


POSITION OF MYRTALES IN THE DICOTYLEDONS 


The hypothesized wood structure of Proto- 


phloem. Among the (super)orders suggested as 
related to Myrtales in recent systems of classi- 
fication (Dahlgren, 1980; Takhtajan, 1980; 
Thorne, 1976; Cronquist, 1981) these two fea- 
tures are absent or very rare and hardly ever 
occur in combination in Rosiflorae (Rosales, Cu- 
noniales), Corniflorae, Rutiflorae, Theiflorae as 
shown in Figure 1 (see Dahlgren & Thorne, 1984, 
for a review o 
of various attributes of these taxa with Myrtales). 
Of these only Vochysiaceae pro parte combine 
vestured pits and intraxylary phloem. This fam- 
ily is wood anatomically specialized (cf. Quirk, 
1980) and any affinities to Myrtales can at most 
be very remote. In Dahlgren’s (1980) and 
Thorne’s (1976) system the Myrtiflorae are po- 
sitioned next to Gentianiflorae in their pictorial 

“transverse sections through the phylogenetic 
shrub,” but these authors do not comment on 
mutual affinities between these orders. The an- 
atomical evidence would support a common der- 
ivation because the combination of vestured pits 
and intraxylary phloem is well represented in the 
order Gentianales. Moreover, primitive features 
like scalariform perforations occur sporadically 
in some representatives, fiber-tracheids also oc- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


cur, and even the diversity of crystal types in- 
cluding raphides and styloids is matched (cf. 
Metcalfe & Chalk, 1950); the single family Lo- 
ganiaceae, if taken in a broad sense, covers much 
of the wood anatomical diversity also encoun- 
tered in Myrtales (cf. Mennega, 1980). 

If less weight is attached to intraxylary phloem 
and vestured pits, the primitive Protomyrtalean 
wood anatomy could be used to argue in favor 
of affinities with a majority of the larger orders 
of Dicotyledons, because 1 in " ONE “ them there 
are at least 
perforations, fiber-tracheids snd Wes 
parenchyma distribution and ray type. In 
case the Rhizophoraceae would also be а can- 
didate for affinity (cf. van Vliet's reconstruction 
of Protorhizophoraceae wood), but it should be 
stressed here that Rhizophoraceae are not more 
similar to Myrtales than to many other, unre- 
lated woody Dicotyledons 

With these vague concha on the ordinal 
and supraordinal level we have stretched the pos- 
sibilities of systematic wood anatom 
abounding parallelisms partly directed 4 coun- 
teracted by ecological trends (cf. Baas, 1976, 1982; 
Carlquist, 1975c, 1980), further interpretation 


—— 


у. With | 


of | 


extant wood anatomical diversity patterns with 


a bearing on events, that must have taken ye 
in early Cretaceous times (cf. Muller, 1981, a 
the earliest pollen records of Myrtaceae), WO 
be indulging in very wild speculation indeed. 


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1975b. Wood anatomy of Onagraceae with 
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Ка Missouri 
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—— —. 1968. Commercial Foreign Woods on the 
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LouRrEIG, A. 1965. On the systematic position of 
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MENNEGA, A.M. W. 1980. Anatomy ofthe secondary 
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METCALFE, С. R. & L. CHALK. 1950. Anatomy of the 
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MEYLAN, B. A. & В. G. BUTTERFIELD. 1974. Occur- 
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New Zealand woods. New Zealand J. Bot. 12: 3- 
18 


& The structure of New Zealand 
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Мои, J. W. & H. H. JANSSONIUS. 1918. Mikrogra- 
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Muca, M. B. & D. Е. CUTLER. 1974. Taxonomic 
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SCHMID, R. 1972. A resolution of the Eugenia-Sy- 
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423-436. 


. 1980. Comparative os and morphol- 
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subfamilial and tribal a E of Myrtace 
595. 


TAKHTAJAN, A. L. 1980. Outline of the a 
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: 225-359. 


TAN, К. 1980. stirred in the ee I. Notes 
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he Angiospermae. Evol. Biol. 9: 35-10 
981. Phytochemistry and извели рћу- 
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D. S. Seigler (editors), Phytochemistry and Angio- 
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d J. & P. S. P. RAo. 1964. The wood 
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6-9. 


VLIET, С. r CM. VAN. 1975. Wood anatomy of the 
аа sensu lato. J. Microscopy 104: 
-82. 


—. 1976a. Radial vessels in rays. I.A. W.A. Bull. 
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800 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог, 71 


1981. Wood anatomy of the palaeotropical genus Miconia (Mel ). Acta Bot. Neer! 
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g 
Bull. 1977/2: 31-3 


— —n!ueÀ— € 


LEAF HISTOLOGY AND ITS CONTRIBUTION TO 
RELATIONSHIPS IN THE MYRTALES! 


RICHARD C. KEATING? 


ABSTRACT 


An examination of the leaf histology of a wide array of families thought at one time to be included 


e bound 
tissue ifierentiation also appears often to be a family characteristic. 


In most respects, plant families p gthe 
core of the Myrtales form a coherent group and 
the recognition of the order has not been partic- 
ularly controversial (Dahlgren & Thorne, 1984). 
At the same time, many of the included taxa pose 
problems as to their level of recognition as well 
as to which higher taxon they should be assigned 
within the order. In addition, more than 30 other 
families have been assigned to the Myrtales at 
some time in the recent past (Dahlgren & Thorne, 
1984) demonstrating insufficient knowledge of 
the boundaries of the order as well as its evo- 
lutionary background. 

A review of the general literature on the cir- 
cumscription of the order and the evidence used 
in its definition has been ably dealt with in the 
Other papers from this symposium from the 
standpoint of general systematic review (Dahl- 

gren & Thorne, 1984; Johnson & Briggs, 1984), 
Wood anatomy (van Vliet & Baas, 1984), leaf 
architecture (Hickey, 1981), pollen (Patel et al., 
9 and sieve element plastids (Behnke, 1984). 
we restrict my comments to the contribution 
а made by leaf histology, recognizing that а 
» T understanding will depend upon a synthesis 

m ч the above plus data yet als ~ rew 
when 
> to use features mei young vege- 
м E anatomy in a systematic investigation. First 
е insufficient number of studies of this sort 


Di т —— 


der as follows: Lythraceae, Rhyncho- 


e cells and 
ound tissue. The sharpness of 


to provide any reliable trends of specialization. 
Iam convinced, however, that leaf histology con- 
tains not only valuable diagnostic characters, but 
that these characters will eventually demonstrate 
great utility in evolutionary studies. Much of the 
value will be based on both an increasing number 
of systematic studies of leaf histology, as well as 
character correlation with studies of leaf archi- 
tecture (er Htm "e 1). Mar structure studies 
of both 
idly. Leaver are obviously the most easily ob- 
tained of all plant materials both from the field 
and from herbarium collections. While leaves 
respond readily to evolutionary pressures toward 
other modifications, their en- 


ground plan of the phylad to which they belong 
(Keating, 1984; Dickison, 1970). 
In this study a particular probl the 
interpretation of the data from my sample. The 
in that 176 species 
were е examined representing 55 genera from 19 
families. Actually, the specimens at hand amount 
to a very small sample of many of the families. 
Even th were veas t oose spec 
imens representing geographic and taxonomic 
diversity within each family, а the fam- 
ily samples most likely do not include the total 
spectrum of characters to be found in them. The 
absence of a character from one group does not 


This work was — y ied di National pee Foundation grants DEB 77-15571 to the author and 
. I am grate rved 


by DEB 78-23400 to 


*Pecimens and to Р. ү oon for M assistance in o 
* Department of Biol 


ANN. Missouri Вот. GARD. 71: 801-823. 1984. 


à from rea institutions for liquid preserv 
many 5 


petes 
ogical Sciences, Southern Illinois paneer Sawardeville, Illinois 62026. 


Selected histological features of leaf transections of families of Myrtales. 


TABLE 1. 
Histological Features 
Struc- Tri- 
ture chomes Cuticle Epidermis Stomata Chlorenchyma 
= v 
с 
Бо» 2 © 
" Wu E S a Е 3 
3 Е Е ESL. 2.4 
9 = a 8 m Е E E 9 
= a 8 moe ee 4 د‎ = 4 Б 84 
ы = 2 + x 5 = £ > 2 3 
den QUE pac О ww Bg a | a 
oe КЕ ЕЕ КЕЕ 55588 2 З 625 
ў = а а E = = 2 [55] © © © D ~ x ~ Ё 3 2 5 
5 E Е а 3 E 3 3 = 5 8 B 3 Ё Я Q4 
Б АОБ ЕИ X247 314344297 4 8 3. 
LYTHRACEAE 
Ammannia coccinia + + + + + + 1 50 6L. 3 
Cuphea spectabilis + + + + + + 1 30 Si 3 
Heimia salicifolia + + + + + 1 50 т S 
Lafoensia speciosa + + + + + + 1 25 SL NB 
Lagerstroemia speciosa + + + > + + 2 45 3:1. 3 
Lawsonia inermis + + + + + + 1(—2) 40 6:1. 3 
Lythrum i var. lanceolatum + + + + + + 1(-2) 50 SE 38 
Nesaea longipe. + + + + + + + 1 30 5-6:1 5 
Punica аы + + + sm + 2 50 i. 3 
Punica protopunica + + + + + + 2(-3) 40 5-8:1 5 
Duabanga moluccana + + + + + + + 2(-3) 50 5-6:1 4 
D. grandiflora * + + + + + 50 2:54 
D. grandiflora + + + + + + 2(-3) 50 5-6:1 9 
moluccana + + + + + + 2 50 4-5:1 4 
Sonneratia sp Dou + + + + + 3-4 30 scr i 
eta + + + + + + 3+3 . 60 3-4:1 6 
RYNCHOCALYCACEAE 
Rhynchocalyx lawsonioides + E + + + + + 2 60 a: 5 
TRAPACEAE 
Trapa sp. + + + + + + 2 50 4-1 8 
OLINIACEAE 
Olini i A + + + = + + а DS 50 BI EK 


<08 


N3QH VO TVOINV.LO8 INNOSSIN JHL 30 STVNNV 


IL 10A] 


TABLE 1. Continued. 
Histological Features 
Struc- Tri- 
ture chomes Cuticle Epidermis Stomata Chlorenchyma 
= > 
OED K E © 
ч 4455 E e £ Е 
E а 5 Е DEM 
Б 5 E y = У 
= a E a је а p mx 5 hs EM i 
б 2 8 . 5 є x @ = 5 2 23.3 
|- E = AO OR B $^ А м О © є £ g = d 
Б <= те 131332.,:31331131 341 3:25 
Па 5 а: | ЕЕ КЕКЕ $2 1 55 
nS 44g ee ed (444 ДАЉЕ. É I s 
COMBRETACEAE 
Anogeissus leiocarpus + + + + + + 1+1 50 E 5 
Buchenavia capitata + + + + + + 1 30 BEAJ 
Bucida buceras + + + + + + 1 50 5-10:1 5 
Combretum grandiflorum + + + + + + | 0 56401 5 
onocarpus erect > ш + + + + + + + 3-2 50 кї S 
Guiera senegalensis + + ds + + + + + 2 50 Ba 3 
Lumnitzera racemosa ate + + + + + 2+2 40 8:1 6 
Quisqualis indica + + + + + + + 1 30 3) I 3 
Strephonema pseudocola + + + + + + 1 25 12-15:1 9 
Terminalia sp. + + + + + + 1 45 5420517 
ALZATEACEAE 
Alzatea verticillata + + + ok +4 + + + 2 25 6:1 20 
PENAEACEAE 
Endonema lateriflora + + + + + + 2 30 61 3 
Penaea mucronata + + ++ + + 1 45 19:15 
MELASTOMATACEAE 
Tibouchina semidecandra + + + + + + + 1 60 —10-12-1 4 
Heterocentron subtriplinervum + + + + + + + + 1 30 art 6 
Memecylon blakeoides + + + + + + + 1(-2) 40 23:1 3 
M. guineense + + + + + + 2 15 1-2:1 4 
M. parviflorum + + + + + + + + 3-4 40 2-4:1 8 


ADO'IOLSIH AVA1—ONILVAN [p861 


£08 


Continued. 


TABLE 1. 


Histological Features 


Tri- 
chomes 


Struc- 


Chlorenchyma 


Stomata 


Epidermis 


Cuticle 


ture 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


SI3ÁV TJ A3uodg = 
oney чїрїд\/ц}8пәлт 


eurure o, әре$цед 


SIoÁ*'T әреѕцед # 


uijpodÁH 


Гегхеду эр [erxepy 
КиО [erxeqy 

AU [erxepy 

uoxung 

[олат 

ровлејич sio?) үегхеру 
Iexeqy < xg егхеру 
Terxeqy < [erxepy 
[eIxeqy = [erxepy 
рошошешо 

yloows 

PNL 

штроуј 

шц]. 

хәјашод 

ројзо-1 < Idus 
рођао- 1 зјаште 
[e121e[1qos] 


[eNUsAIsSIOg 


N 


— 


_ 


B * 


+ 


+ 


M. afzelii 


+ 


M. aylmeri 


M. lateriflorum 


M. sp. 


+ 4+2 


Mouriri sp. 


M. myrtilloides 
CRY PTERONIACEAE 


Axinandra zeylanica 


1(-2) 


Crypteronia paniculata 
PSILOXYLACEAE 


20 


Psiloxylon mauritianum 
MYRTACEAE 


Tristania laurina 
T. conferta 


Eucalyptus micranthra 


8-10:1 


Heteropyxis sp. 
ONAGRACEAE 


2-5:1 3-7 


15-25 


1-2 


(Мог. 71 


н —— | 


1984] 


preclude a relationship between the two groups 
being compared. In spite of this, samples of many 
families demonstrate unique combinations of 
characters which will be commented on, often 
as negating relationships between taxa. The 
available anatomical literature on each family 
was consulted in order to record the known struc- 
tural variability. 


MATERIALS AND METHODS 


All specimens available for this study were 
liquid preserved in either FAA or FPA at 50% 
alcoholic strength. Collection data follows each 


were removed for sectioning from the midrib and 
the margin, approximately equidistant between 
the lamina base and apex. The specimens were 
paraffin-embedded and sectioned at 10 um ona 
rotary microtome (Sass, 1958). Most prepara- 
tions were stained in Safranin-O, Fast Green FCF. 

After a preliminary survey of the genera, the 
features ^ dim below (cf. Table 1) were se- 
lected for th orough observation. Studies by 
Dickison (1970), Bócher (1979), Pyykkó (1966), 
and Dahlgren (1968) were useful guides for initial 
selection of characters. Numerous other useful 
characters exist which should be included when 


iag- 

nostic or systematically stable even though the 

evolutionary trends of specialization are as yet 
own for most of them. 


Lamina structure: Dorsiventral or isobilateral. 
ona r profile for t 

ial surfaces, Abe noted is the degree of abrupt- 
ness or discreteness of the lamina as it joins 
the midrib. In all illustrations, adaxial is up- 
Permost and all descriptive data are taken from 
that orientation 

Midvein and соиби veins: Shape or course 
in transection. Presence and configuration of 
internal or intraxylary phloem. This is often 

н in relation to extraxylary fibers. 
"is end or periphloic fibers: These often af- 
s € shape of the vein, especially secondary 

eins which may be transcurrent or round, etc., 

9n the basis of the shape of fiber patches or 
Sheaths 

аст. Features include relative thicknesses 
mr е adaxial and abaxial layers whether the 

aces are level or the cells papillose or other 

Unusual shape, whether the cells are enlarged 


KEATING—LEAF HISTOLOGY 


805 


and/or rounded internally causing the palisade 
с то undulate, and whether the cells have 
gu crystalline, or other contents. 
Cuticle Relative thickness, degree of ornamen- 
tation and whether the cuticle is flanged be- 
tween the epidermal anticlinal walls. Normal- 
ly, the adaxial epidermal cuticle is rated for 
thickness; the abaxial cuticle is usually thinner 


which they occur and whether they are level, 
sunken, or otherwise modified. 

Margin: There are a number of marginal shapes 
and modifications such as the type of marginal 
vasculature, thickenings, or gland types if pres- 

nt. Insufficient comparable data is at hand for 
this feature and it is therefore largely not taken 
into consideration in this report 

Hypodermis: Position and number of layers. 

Mesophyll: Chlorenchyma is noted as to number 
of cell layers of the palisade zone and its per- 
cent of the total mesophyll thickness. The 
length/width ratio of palisade cells is also not- 
ed as is the ma number of spongy 
layers. ТЇ 
constant for certain families. 

Sclereids: Type, position, and wall thickness are 
recorded. 

Secretory cells, ducts: Type and position and 
presence of epithelium are recorded. 

Cellular inclusions: Tannin cells are not usually 
noted since I have insufficient information as 
to the age of the specimens and its effect on 
tannin deposition. Crystal type, size, texture, 


ома isingly 


of calcium oxalate based on sha 
(Franceschi & Horner, 1980; Frcy-Wyesling 
1981) 


Arrangement ofthe obser the sys- 
tematic listing of Dahlgren and Thorne (1984). 
Individual genera are often noted separately if 
hey have been noted in the past as being con- 
troversial or anomalous. 


P$ у „2, | | 


OBSERVATIONS 
Lythraceae (Figs. 1-8, 10-15) 


The genera Duabanga, Sonneratia, and Puni- 
ca, often not included in the Lythraceae, are de- 
scribed separately below. In many species, one 
or both epidermal layers tend to be formed of 
large, rounded cells. Certain of them are con- 


806 


ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


@ 


€9 


coccinia.— 2 Сирт spectabilis.—3. Heimia запсуоћа. —4. t. Lagerstroemia speciosa. — —5. 5. Lafofns ium 
Lawsonia inermis.—7. Lythrum alatum var. lanceolatu —8. Nesaea longipes. —9. Ànchocay la or sl 
oides.— 10. Punica granatum.— 11. Sonneratia sp.—12. Sm apetala. Scale line = 1 m m. Legend 


figures: Hatching 


= xylem, stippling = phloem, solid black = extraxylary fibers. | 


KEATING—LEAF HISTOLOGY 807 


F "ne 
13 ‘CURES 13-18. Midrib transverse sections of Sonneratiaceae, Trapaceae, Oliniaceae, and Combretaceae. — 
emargi nga grandiflora.—14. Duabanga moluccana.—15. Duabanga moluccana.—16. Trapa sp.—17. Olinia 
пада. 


— 18. Terminalia sp. Scale line = 1 mm. 


808 


spicuously larger than the others and may often 
have mucilaginous contents. The midrib may be 
grooved, level, or slightly ridged adaxially and 
often prominently rounded-convex abaxially. The 
midrib is nearly immersed in Nesaea longipes 
(Fig. 8). The midveins vary from a complete cyl- 
inder to deeply semicircular to a fairly shallow 
arc. Most midveins are bicollateral, but others 
are apparently collateral. Secondary veins are 
generally collateral. In most genera, secondary 
veins are rounded except in Lagerstroemia spe- 
ciosa (Fig. 4) which has an adaxial transcurrent 
extension formed of parenchyma. Extraxylary fi- 
bers are generally absent. When present, they 
form an abaxial periphloic band on both the mid- 
vein and secondary veins [Lafoénsia speciosa (Fig. 
5) and Lagerstroemia speciosa]. Sclereids are ab- 
sent. Druses are common in the mesophyll and 
midrib ground tissue. Occasional prismatics are 
found in Lafoénsia. Lythrum alatum (Fig. 7) has 
a few epidermal cells containing radiating clus- 
ters of birefringent needle-like crystals. 
unica granatum (Fig. 10). The midrib is 
slightly and broadly grooved adaxially and is 
rounded abaxially. The midvein is a bicollateral 
short arc. Secondary veins are short arcs which 
are collateral and round in outline. Mesophyll 
tissue is developed in the midrib quite close to 
the lateral and adaxial sides of the midvein leav- 
ing most of the midrib ground tissue abaxial to 
the midvein. Extraxylary fibers and sclereids are 
absent. Very large prismatic crystals and some 
smaller ones occur in the palisade and spongy 
mesophyll. A few of the large crystals have cen- 
tral druse-like clusters around their equator. 
Duabanga (Figs. 13-15). Adaxial epidermal 
cells are flattened on the surface but are deeply 
rounded internally. Some of the larger ones con- 
tain mucilage. Abaxial epidermal cells on two of 
the three species are all deeply papillose with 
baculum-shaped knobbed extensions, each of 
which has an ornamented cuticle on its distal 
surface. The midrib is level or slightly convex 
adaxially and prominently convex-rounded or 


markedly idioblastic sclereids were not found. 
Druses vary by species from absent to large, coarse 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


and complex to medium-sized. They occur in | 
mid-mesophyll and around veins. | 
Sonneratia (Figs. 11, 12). Stomata are sur- 
rounded by guard cells which are partially en- 
closed by larger epidermal cells. The stomata are 
thus somewhat sunken. Тһе midrib is slightly | 
convex abaxially or on both surfaces. Both sam- | 
ples are or tend toward isobilateral structure. The _ 

midvein is a dorsiventrally flattened cylinder or 
an open flattened “U” shape. The vasculature is | 
bicollateral on the midvein and secondary veins. | 
Secondary veins are round and are nearly encir- | 
cled by phloem. Fibers are not present. Macro- | 
| 


and astro-sclereids are present in the mesophyll. | 
Many large mucilage cells are present subepi- 
dermally which may be of epidermal origin. 
Small, coarse druses are present in the mesophyll 
and around veins. | 


ham, Reveal et al. 4339 (MARY), Mod n | 

icifolia (H.B.K.) Link., Graham 141 , Mex- | 
E es 2 ne (L.) Pers., cult. MO 74248, | 
Brazil; Lafoensis speciosa (H.B.K.) DC. 


iss | 


cult. MO, H A v 
latum (Ell. Rothrock, Graham 460 (MICH), EO 
sippi; Nesaea longipes A. Gray, Turner 6163 (TEX) 
Mexico; Punica granatum L., Raven 26 cul 
s. loc.; P. protopunica Balf. f., Rudall s.n. (К), WC 
Duabanga grandiflora (Roxb. ex DC.) Walpers, of | 
s.n., India; Stone 12837, Malaya; D. тошосат АД 
Chai s.n., Borneo; Madani s.n., 3/5/77, байан ШШ 
neratia sp., Stone & Anderson 13165 (SAN), P А, 
apetala Buch.-Ham., Thanikaimoni s.n., 3/ 15/71, 
dia. 


Rhynchocalycaceae (Fig. 9) 


Rhynchocalyx lawsonioides. The | 
slightly concave or level adaxially and pro" 
nently rounded-protruding abaxially. The та 
vein is semicircular, somewhat V-shaped p 
ially with a tendency toward incurved — i 
reduced xylem development. Phloem 1$ и 
lateral. Secondary veins are similar 1n cong | 


ration only smaller than the midvein. Minor Be | 
are collateral with a circular patch of xylem 2 
an abaxial rounded patch of phloem. je 2 | 
scanty. Опе or two small patches аге we | 
the adaxial side of the midvein and secon. | 
veins. Minor veins have a transcurrent height › 
fiber patch which nearly doubles the Mec os | 
Sclereids are absent. Coarse-textured, ™ a | 
sized druses аге common in midmesophy к? | 
in midrib ground tissue. The large айах! | 


d 


1984] 


dermal cells are flat on the surface and rounded 
on the palisade side making the palisade zone 
appear to undulate. 


Specimen examined: Rhynchocalyx lawsonioides 
Oliv., Raven s.n., cult. MO 7442, South Africa 


Trapaceae (Fig. 16) 

Trapa. The midribisi d and centered 
within the zone of aerenchyma of this floating 
leaf. The small midvein has a rounded patch of 
xylem with an arc of phloem abaxial to it. A 
narrow zone of ground tissue (a bundle sheath) 
surrounds the vein and is in direct proximity to 
the palisade zone. The vein may be slightly bi- 
collateral. Secondary and minor veins are un- 
common. They appear to be bicollateral and are 
surrounded by a parenchymatous sheath. No fi- 
bers or sclereids are present. Druses are present 
around veins, in palisade, and in aerenchyma 
zones, 


pecimen examined: Trapa sp., Hellquist s.n. 6/77, 
Massachusetts. 


Oliniaceae (Fig. 17) 


s. adaxial portions. The adaxial portion may 
orm a transcurrent ridge. Diffuse sclereids were 
мы" Large or medium-sized, coarse-tex- 
ae Tuses are found mostly near veins with 
2 in mid-mesophyll. A large, dense mass of 
Th ses was found abaxial to the midvein fibers. 
d € leaf margin is slightly recurved and consists 
8 ered hypoderm-like tissue. 
Specimen exa 
соат! 1466 т oa н ox Ga AMG 


C 1 : 
ни (including Strephonema) (Figs. 18— 


ee: 1s often conspicuously circular in 
ally lea mina sectors commonly insert later- 
his ving a well-formed adaxial ridge. Com- 

т (Fig. 24) and Quisqualis (Fig. 23) have a 


KEATING—LEAF HISTOLOGY 


809 


midrib protruding prominently on the abaxial 
ide. The midvein is commonly cylindrical or a 
flattened cylinder. A pair of gaps are often pres- 
ent opposite the lamina insertion. Combretum 
has a three-quarter cylinder open adaxially. 
Quisqualis and Conocarpus (Fig. 25) have semi- 
circular or broad arc midveins. The midveins 
appear collateral with weak development of bi- 
collateral phloem in some specimens. Secondary 
and tertiary veins are quite variable and possibly 
diagnostic. While some are circular, most tend 
to be transcurrent with parenchymatous sheath 
extensas Buchenavia (Fig. 20) and Terminalia 


v, 


ing transcurrent veins. Other genera have fibers 
in sheaths, adaxial-abaxial patches, or in scanty 
patterns. Fibers also surround midveins. In 
Buchenavia, adaxial fibers form sheaths around 
prominent discrete patches of adaxial phloem. 
Sclereids are not common. In Bucida (Fig. 21), 
fibrous sclereids are well developed under the 
adaxial epidermis and attach to veins at trans- 
current extensions. Some occur isolated in the 
palisade region. Buchenavia also has vein exten- 

1 pou I. nouo d iie 


sions у р y fro 
the extensions. Strephonema (Fig. 27) has mac- 
rosclereids and trichosclereids common in the 
lamina in any orientation. Very large druses are 
common in enlarged cells of the mesophyll in all 
genera examined and some have styloid projec- 
tions. A few prismatics are found in Strepho- 
nema. 

Lumnitzera racemosa (Fig. 22). 
is thick, smooth, and flanged over 
er periclinal walls on both adaxial and abaxial 
epidermal layers. Outer palisade layers beneath 
both surfaces have dense, red-staining contents. 
The midrib is nearly immersed but the abaxial 
side shows a slight convex curvature. The mid- 
vein is a broad arc with collateral phloem. Fibers 
and sclereids are absent. Medium-sized, coarse 
druses are common and randomly placed in the 
mesophyll. 


The cuticle 


Specimens examined: Anogeissus leiocarpus (DC.) 
Guill. & Perr., Pilz 2088, Nigeria; Buchenavia оа 
p ) Eichler, ite 26623, cult. MO, s. loc.; 

ceras L., Raven 26618, cult. MO, Puerto Rico; iem 
чорда naire rum G. Don, cult. FTG X-2-328, s 
loc.; Con d erectus L., nares Ж син. МО, 


Риегїо Кїс 

5800, Nigeria Lumnitzera racemosa a Willd., cult. FTG 
64- рр dad Сои indica L., ‚ Raven 26572, 
cult. ; Strephonema ps . Chev 
Hall А Nabooh 46647, x Terminalia Sp., cult. 
FTG X-2-2700, s 


810 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


FIGURES 19-27. Midrib transver 
capitata. — 21. Bucida buceras. — 22. Lumnitz 
rum.— 25. Conocarpus erectus. —26. Guiera 


se sections of Combretaceae. — 19. Anogeissus leiocarpus. 


era racemosa. — 23. Quisqualis indica. —24. Combn e 1 mm. 
senegalensis.—27. Strephonema pseudocola. Scale line = 


(Мог. 71 


_ 20. Висћепаїй 
штапа) о 


1984] 


FIGURES 2 


KEATING—LEAF HISTOLOGY 811 


8-38. Midrib transverse sections of Alzateaceae, Penaeaceae, and Melastomataceae. — 28. Alzatea 
2. 


— 29. Penaea mucrona . Heterocentron subtriplinervum.— n: сее semidecandr ra.—3 
afzelii. — 33, Мен аујтет еп. —34. Ме балон parviflorum. — 35. mecylon lateriflorum. — 
mecylon guineense.—37. Memecylon oligoneurum.—38. Memecylon de "Scale line = 1 mm. 


812 


Alzateaceae (Fig. 28) 


Alzatea. Тһе midrib i d с 
both surfaces and not prominent. The midvein 
is a flattened cylinder with lacunae separating 
bicollateral adaxial and abaxial portions. Sec- 

ndary and minor veins are collateral and cir- 
cular in outline. Extraxylary fibers are absent, but 
large, thin-walled sclereids are abundant 
throughout the mesophyll. They have been called 
branched foliar sclereids by Dahlgren and Thorne 
(1984). The cells are actually the same shape as 
the armed spongy or palisade chlorenchyma in 
which they appear and they occur as lignified 
single cells or groups of cells. A 1–2 layered adax- 
ial hypoderm is present over the lamina which 
may become up to 7 layers deep over the midrib. 
Baas (1979) reported that the hypoderm is pres- 
ent only over the midrib in A. verticillata from 
Peru. Small druses are uncommon in the lower 
mesophyll and near the midvein and secondary 
veins. 


tel an 
J AVI 


Specimen examined: Alzatea verticillata Ruiz & Pa- 
von, Poveda s.n., Costa Rica. 


Penaeaceae (Fig. 29) 


The midrib is small, convex abaxially in En- 
donema, or totally immersed in Penaea. The par- 
tially bicollateral midvein is small, round to el- 
liptical, and with a short arc of xylem. Adaxially, 
phloem development is restricted to the lateral 
portions of the xylem. Sclereids are fibrous in 


branched astrosclereids with elongated arms are 
found throughout the mesophyll but are concen- 
trated in mid-mesophyll. Druses are large, coarse, 
and complex and are found beneath the epider- 
mis on the adaxial and abaxial sides of the me- 
sophyll. 


cimens examined: Endonema lateriflora (L. £) 


Spe 
Gilg, Rourke 1706, South Africa; Penaea mucronata 


L., Barker 332, cult. Kirstenbosch, South Africa. 


Melastomataceae (Figs. 30-41) 


p cells ptional in Het- 
erocentron (Fig. 30) in being large, flat on the 
surface and irregular and rounded on the palisade 
side. The midrib is large and rounded with lam- 
ina sectors inserted near the top of the adaxial 
side. Large, pyramidal, multicellular hairs may 


А Aawial P | 1 
4 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


be present on the midrib surface. The midvein 
is a semi-circle or three-quarter circle and may 


be small or large. The bicollateral phloem is - 


evenly dispersed on both sides of the xylem of 
the midvein and secondary veins. Minor veins 
are collateral with partially encircling abaxial 
oem. Fibers and sclereids are absent. Large 
coarse druses are found in the mesophyll and 
midrib often in large round cells. Small druses 
may also be present in the midvein area of Het- 
erocentron. 
emecyloideae, Memecylon. This genus 
forms midribs which are level or slightly grooved 
adaxially. Abaxially the midribs may be slightly 
convex, somewhat V-shaped or prominently 
rounded. The midveins vary from nearly cylin- 
drical, flattened or rounded adaxially, semicir- 


cular or form only a broad arc in those speci | 


| 
| 
| 


| 


— 


with the least prominent midribs. Midveins a | 
cylindrical with an adaxial groove in M. blake- | 


oides (Fig. 38), an incomplete cylinder with in- 
curved ends in M. guineense (Fig. 36), ог semi- 
circular or broad arcs in other species. The veins 
are bicollateral with the adaxial phloem often 
better developed than the abaxial in both mid- 
veins and secondary veins. Extraxylary fibers are 
not common. Memecylon aylmeri (Fig- 33) has 
well-developed fiber patches on the adaxial side 
of the midvein phloem and similar development 
y veins. The Memecylon sp. (Fig 

41) has a fiber cylinder bounding both outer and 
inner phloem of its nearly cylindrical midve! 
The secondary veins are also encircled. Phloem 
is often best developed closest to the proton 
Fiber-like sclereids are common subepiderma * 
and throughout the mesophyll. They are bc 
monly dispersed without relation to veins w 
some species they attach to vein sheath p 
They are variously seen to be without à e 
lumen, with a large lumen and thin walls, ro pé 
ed in outline, or irregular depending ОП cs 
species. Druses also vary by species. e 
and coarse druses are found in МЕНЕ = 
Smaller druses, more finely textured, occur as d 
some with a hollow-appearing non-bir 
center. They occur in the midrib ground be 
subepidermally in the lamina or in the m" 
sophyll. 

Memecyloideae, Mouriri (Figs. 39. 40). b 
midrib is grooved adaxially and is prO 
and somewhat flattened abaxially. 
lem is a flattened cylinder surrounded by P 
externally and internally. Large midve 
periphloic fibers forming a thin sheath 


Midvein X | 


both ёх | 


| 


1984] KEATING—LEAF HISTOLOGY 813 


F 3 . * 
> 39-46. Midrib transverse sections of Melastomataceae, Crypteroniaceae, Psiloxylaceae, and Муг- 
Nee Mouriri myrtilloides.—40. Mouriri sp.—41. Memecylon sp.—42. Crypteronia paniculata. —4 . AX- 
Jess а геујатса. —44. Psiloxylon таитпапит.—45. Астепа smithii.—46. Eucalyptus micrantha. Scale line = 


814 


ternally and internally. Secondary and minor 
veins are sheathed by fibers and the veins are 
bicollateral. Smaller leaves have no fibers. Dif- 
use sclereids are common in mid-mesophyll. 

ey may be branched or armed and may have 
a large lumen. Druses are common in mid-me- 
sophyll and are medium-sized and coarse-tex- 
tured. Phloem of secondary veins is best devel- 
oped on the adaxial side. Abaxial phloem is poorly 
formed or absent. 


mens examined: Heterocentron "ne 
vum so & Ot n & Bouch 38 


& Nabooh Е Ghana: M. ама BL., 

s.n., Borneo; M. parviflorum Thw., Leiden 2978, баз 

Bogor, s . loc.; Mouriri myrtilloides (Sw.) Poiret, s 

dack & Wurdack 2624, Jamaica; Mouriri sp., Madan 

s.n. 5/3/71 (SAN 81060), Sabah; Mouriri SP., ‚ Gentry 
: rt.) 


524, Peru; 
Cogn., Raven 26571, cult. MO, s. loc. | 


Crypteroniaceae (Figs. 42, 43) 


Crypteronia paniculata (Fig. 42). The midrib 
is nearly level adaxially and prominently round- 
ed-protruding abaxially. The overall shape is cir- 
cular with lamina inserted near the summit of 
the adaxial side. The midvein is circular with the 
xylem divided into abaxial and adaxial portions 
which are separated by lacunae opposite the po- 
sition of lamina insertion. The vasculature is bi- 
collateral. Extraxylary fibers form a well-devel- 
oped cylinder around the outer phloem as well 
as scattered patches in the center of the midvein. 
Sclereids are absent. Medium-sized druses, of 
medium texture, are common around veins and 
in mid-mesophyll. 

Axinandra zeylanica (Fig. 43). The midrib is 
slightly grooved adaxially and deeply rounded- 
convex abaxially. The midvein is deeply semi- 
circular with small incurved ends. The vein is 
uniformly bicollateral. Secondary veins are short 
collateral arcs. No sclereids or fibers were seen. 
Prismatic crystals appear in midrib ground tissue 
and many small druses occur in the mesophyll. 

pecimens examined: Axinandra zeylanica Thw., 


Faden 76/466, Sri Lanka; Crypteronia paniculata Bl., 
Stone 13280, Thailand. 


Psiloxylaceae (Fig. 44) 


Psiloxylon mauritianum. The thick adaxial 
epidermis has paradermal thickenings beneath 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 
the surface and is covered by a thick non-flanged | 
cuticle. The midrib is broad with the lamina | 
gradually increasing in thickness to a rounded | 
adaxial convex ridge. The midrib is only slightly 
convex or level abaxially. Midvein vasculature 
is a flattened cylinder with deep xylem devel- 
opment and bicollateral phloem. A prominent 
band of periphloic fibers surrounds the midvein 
and secondary veins. Minor veins have adaxial- 
abaxial phloem caps. The palisade mesophyll ex- 
tends prominently into the adaxial midrib ri 

Sclereids are absent. Secretory cavities lined R^ 
an epithelium are present subepidermally be- 
neath both surfaces. А few medium-sized druse | 
are found near veins. 


Specimen examined: Мени mauritianum Baill, , 
Gueho s.n. 12/1976, Mauritiu 


Myrtaceae (Figs. 45—50) 


c — M 


The midrib is adaxially grooved or ridged and | 
abaxially rounded and the midrib is generally no! 
prominent. The midvein is a broad arc or semi- 
circle in most species but approaches a flattened 
cylinder with one or more gaps in Eucalyptus 
(Fig. 46) and Tristania (Figs. 48, 49). The тій 
vein is collateral or bicollateral. Midveins may 
be bounded adaxially and abaxially by fiber lay- | 
ers. Secondary veins are circular or tending 10° , 
мага transcurrent. They may be aa by | 
а ring of fibers or ha | 
bundle caps. Мо sclereids were ичен = pi 
cavities are prominent beneath either € 

hey are surrounded by a single € 

piae nad layer. Irregularly shaped prn | 
crystals and druses of varying sizes and pe 
may be found in mesophyll and midrib gro : 
| 


u€ 


tissue. 
Heteropyxis (Fig. 50). Midrib vasculature 8 
a broad arc with well-developed xylem мр 
what similar to Tristaniaand Syzygium (Fig. | 
In the midrib, the palisade кари ge 


somewhat more than the spongy lay om the | 


differentiation of midrib ground dicil i 
mesophyll is also similar to the Мугіасеа 

secretory cavities аге also present. The sec 
veins have parenchymatous sheat 
which extend to both epidermal lay 


Merril 
Speci е examined: Acmena pe (P — Ev 


Schmid 1968-A2, cult. 


(1980) i = | 
& Perry | 
WP micrantha DC., Schmid eve cult LAM | 


1984] KEATING—LEAF HISTOLOGY ; 815 


(o. ү, 
AS 


Jw, 


а CURES 47-54. Midrib transverse sections of Myrtaceae and Onagraceae.—47. Syzygium paniculatum. — 
bol „плата conferta. —49. Tristania laurina.—50. Heteropyxis sp.—51. Ludwigia peruviana.—52. Fuchsia 
"ana.—53. Hauya heydeana.—54. Hauya elegans. Scale line = 1 mm. 


816 


Australia; Heteropyxis sp., cult. LAM, South Africa; 
Syzigium panicul G , Schmid 1969-41, cult. 
LAM, Australia; Syzigium sp., Faden 76/438B, Sri 
Lanka; Tristania conferta R. Brown, Ching s.n., 2/77, 
cult. LAM, s. loc.; 7. /aurina R. Brown, Hagen s.n., 
cult. Lam, s. loc. 


Onagraceae (Figs. 51—54) 


The midrib is grooved or ridged adaxially and 
prominently convex-rounded abaxially in the 
largest dorsiventral leaves. Isobilateral leaves 
often have a midrib which protrudes equally 
above both surfaces. Midribs may be sharply de- 
marcated from the lamina or may show a gradual 
decrease in thickness away from the midrib. 
Midveins vary from deeply semicircular to small 
arcs. Phloem may be bicollateral at the midvein 
but often the adaxial phloem is not closely and 
symmetrically disposed adjacent to the proto- 
xylem but instead occurs as patches separated 
from the xylem. The smallest midveins are col- 
lateral. Secondary veins are generally circular, 
collateral, and always without fibers. Periphloic 
fibers are noted in the midribs in a few species 
of Fuchsia (Fig. 52), Hauya (Figs. 53, 54), and 
Ludwigia (Fig. 51). Sclereids are not present. 
Raphides are present in all genera with druses 
and prismatics restricted to a few genera. 


Specimens examined: 125 species in 17 genera as 
listed in Keating (1982). 


DISCUSSION 


Lythraceae. Leafanatomy is made quite het- 
erogeneous with the addition of Duabanga and 
Sonneratia and the family is held to be a basal 
one in the Myrtales (Thorne, 1976; Cronquist, 
1981). One specimen of Lagerstoemia has the 
largest midvein, a complete cylinder with sub- 


stantial p E al 


cells are characteristically irregular in thickness 
with frequent large, rounded, mucilage-filled cells. 
Baas and Zweypfenning (1979) stated that Lager- 
stroemia is unambiguously advanced in wood 
characters while Graham and Graham (1971) 
held that it was primitive for the family. On the 
hypothesis that more complex leaf histology is 
primitive in leaves of Myrtales, Lagerstroemia 
has to be judged primitive. Bailey (1951), how- 
ever, stated clearly that different organs of the 
plant may evolve structurally at different rates. 

Ross and Suessenguth (1926) reported nine out 
of ten American Lafoénsia spp. have leaves with 
a hydathodal tip. The tip is very similar in struc- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


ture to the apical leaf hydathode in Punica (see 
below). The vascular supply is formed of a me- 
dian vein and two lateral veins which converge 
on the epithem tissue. 

Leaf histology of Punica as recorded here and 
in Metcalfe and Chalk (1950) fits well within the 
range of features recorded for Lythraceae. Baas 
and Zweypfenning (1979) noted similarities with 
Punica and the Lythraceae as well as the Myr- 
taceae. Leaf y offers no objection to merg- 
ing Punica with one of these families but this 
might be expected of any genus which has leaves 
as reduced as Punica's seem to be. Turner and 
Lersten (1983) have reported on the structure 
and function of the leaf tip in Punica granatum. 
The acute, mucronate tip is hydathodal with the 
foramen connected to the external environment 
by a number of stomata. The foramen is sub- 
tended by epithem tissue which, in turn, is distal 
to three converging veins. The median vein 1$ 
the largest as is true of all rosoid teeth (Hickey 
& Wolfe, 1975). Leaf tips in Lafoénsia (Ross & 
Suessenguth, 1926) differ in having a large schi- 
zenous or schizolysigenous cavity develop, lined 
with epithem and leading directly to the outside. 
Also, Lafoénsia may have heavily lignified tra- 
cheid development proximal to the epithem. 
Aside from these differences, Turner and Lersten 
(1983) note the obvious structural similarity be- 
tween the families Lythraceae and Punicaceae 0n 
this complex feature. Bridgewater and Baas (1 978) 
noted that wood anatomy of Punica is also spe 
cialized and that it shares derived status with 
several Lythraceae. ; 

The genera Duabanga and Sonneratia have 
among the most strikingly complex leaf anatomy 
in the Myrtales and the two genera also difier 
from each other in several ways. Baas f 
Zweypfenning (1979) noted the distinctness o 
the genera from each other and Dahlgren f 
Thorne (1984) stated that the homogeneity ee 
the Sonneratiaceae needs to be reconside еб 


nearly identical and the guard cells are тат i 
overarched by strongly cuticularized ране 
cells. Rao and Chakraborti (1982) have repo" i. 
on the structure of the apical knob of the er 
ginate leaf of Sonneratia caseolaris (L-) Engl. ues 
leaf has a highly dentritic, flared, vesci 4 
“pad” with veins ending in club-like aggregat! ne 
of brachytracheoids. An epithem seems ce det 
present, but the authors report finding по 0“ 


и 


_—— — ج — 


— = 9— 


— 


iis o Ra icc 


1984] 


to the surface. This apical knob is not rosoid nor 
does it seem to have any structural homologies 
with other teeth reported for the family. Dua- 
banga of the lowland forests of Indomalaya has 
dorsiventral leaves with either a thicker adaxial 
epidermis or with an abaxial epidermis which is 
strongly papillate. Sclereids are found in both 
genera which also serve to separate them from 
Lythraceae (Bannerjee & Rao, 1975; Rao & Das, 
1979). The question of whether the two genera 
are sufficiently closely related to be placed in the 
same subfamily is not easily answered. While the 
two are distinctive in my sample, there is con- 
siderable anatomical variation within each genus 
which must be assessed before venturing an 
opinion. Leaf venation architecture would be es- 
pecially instructive here. Muller (1981) noted that 
the pollen of Florschuetzia trilobata of the Oli- 
gocene and Miocene of Borneo seems to combine 
characteristics of Lythraceae and Sonnerati- 
aceae, supporting the hypothesis of a common 
evolutionary history. Venkateswarlu and Rao 
(1964) concluded on the basis of wood anatomy 
that Duabanga and Sonneratia should be in- 
cluded in the Lythraceae although Baas and 
Zweypfenning (1979) noted that this would cer- 
tainly extend the range of features in that family. 
If we follow Thorne (1976) and add the two gen- 
era to the Lythraceae, they would certainly need 
their own subfamily or subfamilies. 
| Rhynchocalycaceae. Rhynchocalyx lawson- 
loides with its enl ged adaxial epid is, midrib 
and midvein configuration, semi-transcurrent 
secondary veins, type and position of druses fits 
well within the Lythraceae. Most characteristic 
is the extension of palisade tissue from the lam- 
Ша into the midrib, adaxial to the midvein, a 
Pattern shown by nearly all leaves of Lythraceae. 
In short, the anatomy of Rhynchocalyx in no way 
extends the anatomical variation in leaf anatomy 
found in the Lythraceae. 
ei apaceae. Leaf anatomy of Trapa reflects 
=: floating habit of the genus. The 
ventral leaves have well-developed aeren- 
Уве in the abaxial two-thirds of the lamina 
te stomata are on the adaxial surface only. Met- 
€ and Chalk (1950) included Trapa in the 
= сеае and Airy-Shaw (1973) considered it 
(1980), relative of the Onagraceae. Takhtajan 
States that Trapaceae is related to the On- 
a especially to the genus Ludwigia. The 
ms т the more generalized species of Lud- 
eating, 1982) show no resemblance to 
"ара leaf anatomy. Even those Ludwigia species 


KEATING—LEAF HISTOLOGY 


817 


with floating leaves have not converged on the 
structure of Trapa leaves. The absence of raph- 
ides and its unusual histology distinguishes Tra- 
pa from Onagraceae and Lythraceae but leaves 
open the question of whether it might be closely 
related to them in spite of its ecological special- 
izations. The thin, monarch root anatomy о 

Trapa (Fahn, 1974) is probably unique in the 
Myrtales. Evidence linking 7rapa with any other 
family will not likely come from vegetative his- 
tological features. 

Oliniaceae. Mújica and Cutler (1974) found 
that leaf anatomy is very useful in Olinia for 
defining intra-generic subgroupings. Rao and Das 
(1976) and Mújica and Cutler (1974) have noted 
the presence of terminal sclereids in Olinia al- 
though these were not observed in my prepara- 
tions. As figured by Müjica and Cutler, the his- 
tological patterns of the leaf midrib and lamina 
are quite compatible with leaves of Lythraceae 
and Myrtaceae. Diffuse sclereids are not found. 
The adaxial patch of fibers at the midvein of 
Olinia emarginata is somewhat similar to the 

attern found in Memecylon aylmeri. Májica and 
Cutler (1974) noted that terminal sclereids sim- 
ilar to those of Oliniaceae occur in species of 
Memecylon and in Mouriri. They also noted the 
similarity of petiole structure in species of Me- 
mecylon and Olinia. Rao and Dahlgren (1968) 
noted similarities to leaf and wood anatomical 
features of the Rubiaceae although that family 
entirely lacks intraxylary phloem. 

Combretaceae. In contrast to the work on the 
leaf epidermis by Stace (1980, and references cit- 
ed therein), anatomy ofthe leaf d t produce 
a clear alignment according to the taxonomic 
tribes and subtribes of Exell and Stace (1966). 
The family has generally complex midrib vas- 
culature except in Conocarpus which has reduced 
leaves. Lumnitzera and Laguncularia, the man- 
grove genera, also show reduced and specialized 


large cells often occupying the entire height of 
the lamina in Anogeissus, and to a lesser extent 
in Bucida, Terminalia, and Guiera. In contrast 
to the finding of a number of unusual embryo- 
logical features in Guiera by Venkateswarlu and 
Rao (1972), I found no particularly distinctive 
vegetative features in that genus. Tobe and Ra- 
ven's (1983) conclusion, that Guiera's unusual 
embryological features are of secondary origin, 
is supported by vegetative anatomy. Overall, the 


818 


Combretaceae appear to have a coherent set of 
leaf anatomical features and one can agree with 
Dahlgren and Thorne (1984) that no particularly 
close connection with other families of the order 
is obvious. 

Strephonema seems clearly related to the 
Combretaceae with its midvein cylinder, and 
secondary veins with fiber caps. The large, coarse 

ruses and prismatic crystals, fiber-like and 
macrosclereids, and the characteristic length/ 
width ratio of the palisade cells are all clearly 
combretaceous. On the other hand, the midvein 
and secondary vasculature of Strephonema seem 
to be free of intraxylary phloem. This serves to 
isolate the genus somewhat but all of the Com- 
bretaceae I have observed have relatively weak 
intraxylary phloem development. Anomocytic 
stomata in Strephonema differ from the mostly 
parasitic members of the Combretaceae and the 
cyclocytic mangrove genera. Outer and Fundter 
(1976) felt that phloem, bark and wood char- 
acteristics plead for a less specialized and distinct 
subfamily of Combretaceae. However, the lack 
of intraxylary phloem would appear to be a sec- 
ondary loss if that character is regarded as basic 
for the Myrtales. 

Alzateaceae. Few specimens of the genus are 
known and we probably do not have a good cir- 


only. The isolation from other myrtalean fami- 
lies pointed out by Dahlgren and Thorne (1984) 
can be confirmed on the basis of leaf histology 
although the genus does seem clearly to belong 
to the order. Features which serve to isolate A/- 
zatea include the sclereids, which are simply lig- 
nified idioblastic cells of the same shape as spon- 
gy cells, the cyclocytic combined with anomocytic 
stomata, the three-trace, trilacunar node, the 
broken cylinder of midvein vasculature, and the 
particular form of small square epidermal cells 
as seen in transection. 

The structure of the mesophyll and of the veins 
is generally similar to several myrtalean families 
(Crypteroniaceae, Myrtaceae, and Lythraceae) but 
not a clear fit into any of them. Midrib and lam- 
ina structure is quite different from Rhyncho- 
calyx and does not support the contention of van 
Beusekom-Osinga and van Beusekom (1975) that 
they belong together in a subfamily of Cryptero- 
niaceae. Maintenance of the monogeneric Al- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


zateaceae is best supported on the basis of veg- 
etative anatomy. 

Penaeaceae. The seven, closely related gen- 
era have small coriaceous leaves, often with an 
ericoid habit (Airy-Shaw, 1973). Midveins and 
midribs are small and reduced in complexity 
which precludes useful systematic comparisons 
with those features. Dahlgren (1968) stated that 
leaf anatomy does not contribute much to dif- 
ferences between genera of the family. Dahlgren 
(1968) also noted that the families Geissoloma- 


all been considered closely allied on the basis of 
a variety of features. The array of diffuse and 
terminal sclereids reported by Rao and Das (1976) 
as well as the leaf axil bristles serve to isolate the 
family from all other Myrtales except possibly 
he Melast t M yloideae. Sclereids 
of the Memecyloideae recall those of Penaeaceae 
as does the specialized leaf margin consisting of 
a parenchymatous ridge as found in both Me- 
mecylon and Penaea. Large, coarse and complex 
druses are also found in both groups. — — 
Melastomataceae. The family is distinctive 
morphologically and anatomically. A compre 
hensive anatomical study of the young vegetative 
anatomy of the family would doubtless provide 
a number of diagnostic features and morpho 
clines (cf. Metcalfe & Chalk, 1950). By far the 
greatest number of leaf anatomical studies have 
been done of Mouriri and Memecylon of the ye 
mecyloideae. These works have demonstrat 
that sclereids of all types occur in these gener 
and that they are biogeographically and system- 
atically correlated (Foster, 1947; Subramani 
& Rao, 1949; Morley, 1953; Rao, 1957; Rao 


et al., 1980). Baas (1981) has called attention t0 
the systematically useful stomatal and ¢ "s 
types in the family. Midrib vasculature ph 
Melastomatoideae is much more diverse Ji 
implied by the sample included here and it узе pi 
be thoroughly studied. Reduction and simp m 
cation of midrib structure in both subfam 
suggest parallel trends of specialization. 
An interesting feature noted only 1n t 


phloem. 
intraxylary phloem of midveins and second# 
veins is usually better developed than thea re 
or collateral phloem. In secondary Mer 
abaxial phloem is often missing being TP 


T — 


1984] 


with robust development of the adaxial phloem. 
This tendency is especially pronounced in Me- 
mecylon. Relationships of the Melastomataceae 
to other myrtalean families are not readily sug- 
gested on the basis of leaf features. 

Crypteroniaceae. The delimitation of this 
family by van Beusekom-Osinga and van Beu- 
sekom (1975) included five genera and resulted 
in a diverse group from the standpoint of leaf 
histology. In spite of that diversity, van Vliet et 
al. (1981) included the genera as a subfamily 
within the Melastomataceae. Removal of A/za- 
tea and Rhynchocalyx improves the family (or 
subfamily) circumscription, although RAyncho- 
calyx does retain certain resemblances to Axi- 
nandra. These include the midrib shape, the 
midvein shape with the incurved ends of the 
semicircle. The Axinandra specimen examined 
here is probably somewhat immature and prob- 
ably will not bear extensive comparison. Cryp- 
teronia paniculata examined here has more 
prominent vasculature than most Lythraceae but 
it has several features similar to that family. The 
simple trichomes, palisade cell measurement ra- 
105, palisade percentage of the mesophyll, num- 
ber of spongy layers, and the shape of secondary 
veins with a convex xylem adjacent to normal 
collateral phloem are all similar. Among myr- 
talean families, Lythraceae show the greatest 
similarities to the Crypteroniaceae even though 
van Vliet and Baas (1975) found no resemblance 
Оп wood features. 

Psiloxylaceae. Psiloxylon mauritianum 
shows sufficiently distinct leaf histology to sup- 
port the concept of its belonging to a separate 
family as Dahlgren and Thorne (1984) conclude 
їп their review. The epithelium-lined secretory 
cavities found in Psiloxylon leaves are otherwise 
таге In the Myrtales except in the Myrtaceae. 
Midrib and midvein configuration in the genus 
are unique among reports known to me. On the 
Ps ya data from reproductive organs, Briggs 
hes ohnson (1979) state that “а conceivable 

mon ancestor of Psiloxylon and the Myrta- 
= would be decidedly un-Myrtaceous, in соп- 
in ng such an ancestor for the genera included 
е family ....” The array of leaf features 


et in the present study at least confirm 


(19 


is 80). There is insufficient information on the 


f anatomy of many genera of Myrtaceae to 


KEATING—LEAF HISTOLOGY 


819 


make a judgment on that basis either to include 
or exclude Psiloxylon from the Myrtaceae. 

ce Briggs and Johnson (1979; John- 
son & Briggs, 1984) have provided a list of char- 
acters, including a few leaf histological and ar- 
chitectural features, which may be reasonably 
inferred to be present in primitive Myrtaceae. 
The specimens which I examined were meso- 
morphic, dorsiventral, and lacking a hypoderm, 
all generalized features by the criteria listed by 
Briggs and Johnson. As noted by Metcalfe and 
Chalk (1950), Johnson (1980), and Erdtman and 
Metcalfe (1963), isobilateral leaves with a hy- 
poderm are common in the family. In leaf mid- 
vein vasculature patterns, one might hypothesize 
a trend of specialization which will have to be 
tested with much more data. A semicircular- 
shaped trace may have evolved in two directions: 
1) the trace has become reduced to a broad then 
narrow arc of tissue by simple reduction, and 2) 
has b i d adaxially and then 
flattened as noted in Eucalyptus obliqua L’Herit. 
(Metcalfe & Chalk, 1950) and Eucalyptus mi- 
crantha (Fig. 46) as illustrated in this study. Ac- 
mena smithii may represent an extreme form of 
an arc where adaxial xylem portions have been 
lost and only the adaxial periphloic fibers re- 
main. The trends noted by Briggs and Johnson 


ah + 


11101 


nation, suggest that discovery of many trends of 


1 
WY LAR 


vascular and other ! g p 
repay a comprehensive study of the family. 

Histological features of Heteropyxis leaves, in- 
cluding the midrib vasculature, mesophyll struc- 
ure, and the presence of the characteristic se- 
cretory cavities, are generally compatible with 
other myrtacean genera. These features plus those 
in the exhaustive list in Schmid's (1980) review, 
support the inclusion of the genus within the 
Myrtaceae. 

The family as presently circumscribed does 
not show obvious affinities with any other fam- 
ilies of the order except Psiloxylaceae. The in- 
clusion of Lecythidaceae in the family by Ben- 
tham and Hooker (1862) was shown to be 
unreasonable by Metcalfe and Chalk (1950) and 
it seems clear that Lecythidaceae should be ex- 
cluded from the order entirely. 

Onagraceae. This family, without doubt the 
best studied family of its size among the flow- 
ering plants, was recently thoroughly examined 
for its leaf architectural and anatomical features 


“+ 


820 


(Hickey, 1980; Keating, 1982). For leaf histol- 
ogy, 125 species representing all 17 genera were 
studied and only a brief summary of the conclu- 
sions will be repeated here. The family is a nat- 
ural coherent group and all of the genera share 
a number of features which also serve to isolate 
the family within the Myrtales. These include 
the presence of raphide crystals (Keating, 1982), 
the four-nucleate (Oenothera-type) embryo sac 
(Tobe & Raven, 1983), and viscin threads on the 
pollen (Skvarla et al., 1977). The genera of On- 
agraceae which show the best developed midrib 
vasculature (Ludwigia, Fuchsia, and Hauya, as 
figured here) show a unique arrangement of in- 
traxylary phloem compared to all other myrta- 
lean specimens that I have examined. The traces 
are not strictly bicollateral but instead the phloem 
on the adaxial side consists of individual strands 
in the midvein ground tissue often at some dis- 
tance from the midvein protoxylem. The adaxial 
phloem strands are not collectively oriented with 
respect to the shape of the midvein xylem. 

As the evolution of the family is presently 
understood (cf. Raven, 1979) the leaf anatomy 
trends of the family represent a reduction series 
in complexity of structure and developmental 
sequences. In their general conformation of leaf 
histology, the Onagraceae show their greatest 
similarity to the Lythraceae. Punicaceae leaves 


serve to link the family to other myrtalean fam- 
ilies. Leaf teeth are highly distinctive having a 
hydathodal apparatus including an apical fora- 
men, epithem tissue, and three converging veins. 
Named the “rosoid” tooth by Hickey and Wolfe 
(1975), it is only known from several saxifra- 
galean genera (Stern, 1974, 1978; Stern et al., 
1970; Styer & Stern, 1979a, 1979b), the Ona- 
graceae (Hickey, 1980; Keating, 1982, 1984), the 
Lythraceae (Hickey, 1981; Ross & Suessenguth, 
1926), and the Punicaceae (Turner & Lersten, 
1983). 


SUMMARY OF CROSS SECTIONAL LEAF HISTOLOGY 
FEATURES FOR THE ORDER MYRTALES 


The following ordinal description is based 
mostly on the species described above, which 
have more generalized anatomy. The inclusion 
of a large sample of more specialized species 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог, 71 


would have lengthened this treatment several 
fold, decreasing its utility. 

Leaf structure is mostly dorsiventral with iso- 
bilateral leaves occurring in several families. 
Adaxial and abaxial epidermal cells are of equal 
thickness or the adaxial cells may be up to 2-3 
times as thick as the abaxial. Epidermal cells may 
be convex or level on the surface or facing the 
mesophyll, and regular or irregular in shape. Mu- 
cilage cells may occur in epidermal cells in the 
Lythraceae. The cuticle is thick to thin or not 
visible. A hypoderm layer is rarely present in 
most families although it is fairly common in the 
Myrtaceae in genera with isobilateral leaves. The 
midrib in dorsiventral leaves may be grooved, 
level, or ridged on the adaxial side. It may be 
very large and rounded on the abaxial side, rang- 
ing to immersed or level. In isobilateral leaves, 
the midrib may be biconvex or circular, to level 
or immersed. The lamina may be abruptly dif- 
ferentiated from the midrib or it may taper grad- 
ually from a poorly defined midrib. Midveins 
normally consist of a single trace varying from 
a deep semicircle to a broad or short arc and at 
either collateral or bicollateral. Secondary veins 
are collateral or bicollateral with the phloem on 
the adaxial side occasionally the best developed. 
Extraxylary fibers are absent to scarce ог well 
developed when they form abaxial phloem caps 
or full sheaths. Fibers may form transcurrent ex 
tensions over the smaller veins. Sclereids, as 4 
trosclereids, macrosclereids, or trichosclereids, 
may be absent or rarely present to abundant. The 
mesophyll may be weakly or sharply а 
tiated into palisade and spongy layers. The = 
palisade layers have cells which vary from 2: | 
to 12:1 length/width ratios. Spongy mesophy 
cells may form а well organized аегепсћута да 
genera with floating leaves. Stomata аге mostly 
abaxial in dorsiventral leaves but are found 0? 
both surfaces on some dorsiventral leaves 
on all isobilateral leaves. Calcium oxalate “a 
tals are always present in one or more forms 
styloids, prismatics, raphides, druses, OF © di 
sand. They may be randomly dispersed 1n of 
mesophyll, restricted to upper or lower layers : 
the mesophyll, or occur only around verme эй 
gins are usually without unusual pem d 
but occasionally hypoderm or other lignifi p 
collenchymatous, non-mesophyll cells may 
a thickened edge. Marginal teeth, when P die 
are probably always rosoid and have а hy А 
thodal structure. Secretory cavities are rare 


| 
| 


~ 


ت 


1984] 


are present and epithelium-lined in some Myr- 
taceae 


COMMENTS ON FAMILIES OFTEN 
INCLUDED IN THE MYRTALES 


Thymelaeaceae. Leaf anatomical features of 
the family, minus Gonystylus are generally with- 
in the range as recorded for the core myrtalean 
families. Diverse anatomical features include a 
"ani 4 TA : 4 Sot ae за MS TERN PSP S 


of fibrous sclereid (Metcalfe & Chalk, 1950), a 
hypoderm, mucilaginous epidermal cells, and 
several crystal types including styloids, prismat- 
ics, druses, and crystal sand. Margins may be 
supported by “veins” which are actually scle- 
renchymat | ts (Metcalfe & Chalk, 1950). 
About half of the genera are recorded as having 
bicollateral vascular bundles. In most of my 
specimens, the midrib is small with an arc of 
vasculature with two exceptions. A small cylin- 
der is noted in Lethedon and Daphnopsis. 

The remaining genus, Gonystylus, is quite ex- 
ceptional for the family and it is certainly not 
myrtalean. Its midrib is very large, prominently 
protruding, and rounded abaxially. The vascu- 
lature consists of a broken cylinder in one species, 
and in the other, a broad cylinder of collateral 
bundles. The cylinder surrounds an inner 
U-shaped vein which in turn contains several 
smaller bundles. Each cycle of traces is capped 
by well-developed periphloic fibers. Gonystylus 
also contains epithelium-lined mucilage cavities 
Which occur in the palisade region. Cronquist 
(1981) includes Gonystylus in the family while 
Dahlgren and Thorne (1984) state that evidence 
Suggests that not only is Gonystylus questionably 
Included in the family, it may not even be close y 
allied to it. A thorough study of the anatomy of 
the family would need to consider the specialized 
Xeromorphic nature of many of the species. 

Haloragaceae. leaves of this family have re- 
калай, venation and generally simplified struc- 
m ith this data, it is impossible to affirm or 

eny affinities with practically any order. 
the p Phoraceae. This family fits poorly into 
lida yrtales on a number of grounds. The cy- 

папса! or incurved arc of midvein vasculature 


Show 


: vU у to J 
Rie The phloem commonly remains a con- 
"m us collateral band. A prominent hypoderm 

mmon which may be multilayered. The in- 
nermost layer is often comprised of large cells 


KEATING—LEAF HISTOLOGY 


821 


which extend separately down into the palisade 
zone in Rhizophora and Gynotroches. Some of 
these large cells may extend out to the adaxial 
epidermal surface. Laticifers, often articulated, 
are common in some species throughout the 
spongy and midrib zones. Complex midvein vas- 
culature is present in Carallia brachiata. The 
family needs more anatomical study both for 
better circumscription and for a better under- 
standing of its characters in light of its mangrove 
habit. The family is quite variable anatomically. 

Lecythidaceae (including Barringtoniace- 
ae). The family is distinctive in midrib shape 
and vasculature. Most specimens are convex 
adaxially and abaxially in various combinations 
of rounded and V-shaped profiles. The lamina 
sectors are horizontally or laterally inserted. The 
collateral midrib venation is highly complex. Le- 
cythis, Gustavia, and Couroupita have one large 
flattened cylinder toward the adaxial side of the 
midrib which is encircled abaxially by a series 
of smaller cortical bundles which often have 
centrically arranged xylem, i.e., have radial sym- 
metry with encircling phloem. A row of small 
bundles may also partially surround the main 
cylinder on the adaxial side. Each genus has a 
particular diagnostic arrangement of the bundles 
which in some cases are numerous. The genera 
Barringtonia, Careya, and Combretodendron, 
sometimes recognized as the Barringtoniaceae 
(Airy-Shaw, 1973) are distinguished as a group 
although they are comparable in complexity and 
clearly related to the Lecythidaceae sensu stricto. 
Those genera have an abaxially placed, deep 
U-shaped trace or flattened cylinder with an ar- 
ray of wing bundles pointing toward the laterally 
inserted lamina sectors. Adaxial or abaxial rows 
of accessory veins may be present. The palisade 
mesophyll extends into the midrib zone beneath 
nearly the entire adaxial surface but is not con- 
tinuous across the midrib. Trichomes, when 
present, have a multicellular buttressed base of 
complex and characteristic form. 

The closest pattern of midrib vasculature to 
this highly distinctive family appears to be among 
the Theales near the Guttiferae, Ochnaceae, 
Quiinaceae, and Theaceae as figured by Schofield 
(1968). The overall configuration of Lecythida- 
ceae leaf histology is strikingly similar to those 
families. 

Chrysobalanaceae. Species examined here ali 


ea ‘41‏ وء 
midvein vasculature with prom-‏ 


inent midribs. Parinari nonda shows the most 


822 


complex midrib venation described with xylem 
and phloem bands enclosed within the main vas- 
cular cylinder. Venation is collateral. What ap- 
pears to be internal phloem in some species may 
be due to loss of part of the included уннн 
The genera examined could fit into Myrtales 
terms of the configuration of characters јетри 
Elaeagnaceae. The peltate and multicellular 
stalked hairs are not matched by any other myr- 
talean families. Midveins and midrib configu- 
ration are compatible with the order but bicol- 
lateral phloem is absent. The raphides recorded 
throughout the leaf of Elaeagnus philippinensis 
are rare in the Myrtales. The Onagraceae, the 
only other family with raphides, otherwise shares 


which were never fused Уни ће midvein, leaf 
primordia fused 
phi owe glandular trichomes on the young 
y collateral oni a е form 
d within the 


a hi 


order. 


LITERATURE CITED 


ee HEX J. C. Willis' A Dictionary 
the Flowering Plants and Ferns, 8th edition. 

бнри Univ. Press, Cambridge 

Baas, P. 1979. The anatomy of Alzatea Ruiz & Pav. 
(Myrtales). Acta Bot. Neerl. 28: 158. 

te on stomatal t m and crystals 

in the leaves of Melastomataceae. Blumea 27: 475- 

479. 


V. J. ZWEYPFENNING. 1979. Wood 
anatomy of the Lythraceae. Acta Bot. Neerl. 28: 
117-155 


BAILEY, I. W. 1951. The use and abuse of anatomical 
data i in the study of phylogeny and classification. 
Phytomorphology 1: 67-79. 

"— B.C. . А. RAO. On foliar n 

a few species of Sonneratia. Curr. Sci. 
639-640. 

BEHNKE, H.-D. 1984 [1985]. Ultrastructure of sieve- 

element „plastids o Myrtales and ied groups. 


BENTHAM, G. & J. D. HOOKER. 1862. Genera Plan- 
tarum. Reeve & Co., London. 

Biro на GA, К. J. vAN & C. F. v VAN BEUSEKOM. 
1975. Delimitation and subdivi 


vision of the Cryp- 
teroniaceae (Myrtales). Blumea 22: 255-266. 
BócHrR, T. W. 197 79. Xeromorphic leaf types. Evo- 
lutionary 
por an ы Kongel Danske Vidensk. Selsk. Biol. Skr. 
(8): 1 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Уо1. 71 


BREMMER, K. . Taxonomy of Memecylon (Me- 
lastomataceae) i in Ceylon. Opera Bot. 50: 1-32. 
"TE ‚ S. D. & P. Baas. 1978. Wood anat- 
of the Punicaceae, IAWA Bull. 1978/1: 3-6. 

Bricos, B. G. & L. A. 8. Јонмзом. 1979. Evolution 
e Myrtaceae—evidence from inflorescence 

ны Proc. Linn. Soc. New South Wales 102(4): 


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Cuy 


ULTRASTRUCTURE OF SIEVE-ELEMENT PLASTIDS 
OF MYRTALES AND ALLIED GROUPS! 


H.-DIETMAR BEHNKE? 


ABSTRACT 
The core families of Myrtales (69 species investigated) contain S-type A plastids. In 


these, the presence of several 


medium-sized spherular starch grains is probably a 


ommon trend in 


the order. Among those Son ur ges coney associated or more or less meaty related, the great 
the sam 


majority also have S-type 
contrast to the close pie mE 


stids, s 


e, Gunne 
related families, have developed "ui ла That su PV- 


tids, which exclude all starch, 


btype PV-plast 
are igi in all tribes of Rhizophoraceae except Anisophylleae supports family recognition of the 
latte 


Sieve-element ch ters i ti d with the 
transmission electron microscope have repeat- 
edly contributed to the circumscription and clas- 
sification of higher taxa, e.g., Leguminosae 
(Behnke & Pop, 1981), Monocotyledoneae 
(Behnke, 1981b). Of these, the most intensively 
studied feature is the ultrastructure of sieve-ele- 
ment plastids. The great number of investigated 
angiosperms (some 2,000 species from nearly 400 
families—as of 1983-12-31) allow a оса фан 
of the plastids into P- and S-type, а ber of 
subtypes, and a great many of chaste forms 
by using both chemical and morphological com- 
position at the ultrastructural level (see Behnke, 
ide for more detail). The successful delimi- 
of the order Caryophyllales to the PIII 
ie families (Behnke, 1976; Mabry, 1977) and 
the use of sieve-element plastid data in separat- 
ing Vitidales from Rhamnales (Behnke, 1974; 
Dahlgren, 1980) and Buxaceae from Simmond- 
siaceae and Euphorbiaceae (Behnke, 1982a) 
stimulated, among others, the screening of all the 
core families of Myrtales and of those closely or 
more distantly related to the order, with the re- 
sults to be included in this symposium report. 


MATERIALS AND METHODS 


Preferentially young stem pieces of the plant 
species listed in Table 1 were cut into longitu- 


' For permitting collection of living material used in this study the author wishes to thank the 
-Dahlem 


ped of the Botanical Gardens in Berlin 


, Mainz, 
(Kirstenbosch), 1 Dorr (Kiel), D. M. C. Fourie (Pretoria), I. S. Gottsberger (Botucatu), A. Irvin 


uncosa (Petersham), K. Kubitzki (Hamburg 


5 
б Nicholson (St. Michaels-on-Sea, RSA), Н. Téhé (ORSTROM), R 


shipping living plant material, 
fixations, and А. Е. A. N 


A. P. Bennell (Ed 


dinal sections fixed in a formaldehyde-glutaral- 
dehyde mixture followed by 1% buffered 090, 
and dehydrated in acetone. Small pieces con 
taining phloem tissue were embedded and po- 
lymerized in epoxy resins, cut with an u!trami- 
crotome, and the final ultrathin sections viewed 
and photographed with a transmission electron 


| 


5 | 
microscope (for exact procedures see Behnk 


1982a). 
RESULTS AND DISCUSSION 
Sieve-elements of many of the myrtalean fam- 


ilies are extremely difficult to fixate in а close ' 


to-natural condition. There is less plasmatic 
content which is more labile and, during pre?” 
aration, sieve-element plastids burst more often 
than in the average dicotyledon family. bk 
theless, all of the 69 investigated species i 


е, 
core families of Myrtales (cf. Dahlgren & Thom ids | 


1984) could be shown to contain S-type P astı 
(cf. Table 1). Number, size, Figs 
starch grains in these plastids certainly MA c 
1-14), but some common trends may be d: 
nized. There are always several starch V "à 
one plastid— often six ог more (Figs „еб T of 
11), their size being variable (sometimes 

the same size) but never very large ап 

shape almost exclusively is a spherule. 
erably smaller starch grains are present in 


Cons 


o! 
Kew. 
ogor, Bonn, Copenhagen, Edinburgh. Hose Clark 
and Utrecht. I am particularly indebted to A. Assi (Abidjan), P. Berry ( el “Atherton, Оф), 
اوي‎ 
), Lee Ying Fah (Sandakan, Sabah), G. Merz (Неее), y 

y (Indooropilly) for [ping V 

and ici (Copenhagen) for he [lectors. | 

oel (Pietermaritzburg) and P. H. Raven (St Louis) for SE contact to berg). TH 

„Р тз. Р. Laupp (both Heidel 


Germ 
ANN. Missouri Bor. GARD. 71: 824-831, 1984. 


any. 


ts from the Deutsche Forschungsgemeinschaft. blic of 
2 Zellenlehre, Universitit Heidelberg, Im Neuenheimer Feld 230, D-6900 Heidelberg, Federal Repu 


1984] BEHNKE-—SIEVE-ELEMENT PLASTIDS 825 


-——! -8. Sieve-element plastids of the core families of Myrtales I. All plastids are S-type, with — 
асеае —4 Spaces е.—1. Schizocentron elegans.—2. Bertolonia macu кесе ч Medinilla magnifica, Pe 

3 , Rhynchocalycaceae. —6. Rh Е 
anga ае Plastids reproduced to cover 


е area, actual magnifications diverge around 20, 000: 


826 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


Мупасеа 
FIGURES 9-14. Sieve-element plastids of the core аг к Myrtales II. S-type рек from My 


- 
Trapa паа 
9. —— excelsa. — 10. listemon тет —11. ium littorale, Trapaceae. ies the same e area, 
Onagraceae. —13. Epilobium fleischerei.—14. Circaea y  Plastids reproduced to = 
actual mi diverge around 20, 00 


———— áo 


FIGURES 15-22. Sieve-element plastids of families often allied to Myrtales. S-type plastids in dev 4 
15. Haloragis етеста. — 16. Myriophyllum brasiliense, P- -type plastids in Rhizophoraceae. “11. Pise gui 
conjugata, S-type plastids in Thymelaeaceae.—18. Daphne mezereum, Lecythidaceae. —19. 


1984] BEHNKE- SIEVE-ELEMENT PLASTIDS 827 


ane. 

in t C ampi —20. Coris monspeliensis and Ch 

actual gnaceae. — 22. Elaeagnus angus. MM young si 
magnifications diverge around 20,000 x 


rysobalananceae. — 21. Chrysobalanus icaco, S,-plastids 
eve element. Plastids reproduced to cover the same area, 


828 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Vor 71 
TABLE 1. Sieve-element plastids in Myrtales and allied groups. 
Type of 
Family Species Source Plastids 
Melastomataceae ты cymosum (Schrad.) Naud. trecht 5 
и — e )D Edinburgh S 
B. d. Heidelberg S 
Bredia ан Day Ten Diels Edinbu S 
Calvoa orientalis T Copenhagen S 
Centradenia о Planch. Edinburg S 
Clidemia hirta (L.) D. Don nn S 
Dissotis rotundifolia (Sm.) Triana Copenhagen S 
Gravesia guttata (Hook.) Triana dinbur: S 
Heterocentron subtriplinervium (Link & Otto) R. Edinburgh 5 
Вг. 
Medinilla magnifica Lindl. Heidelberg 5 
оиы гомна D. Don Edinburgh S 
Метесу Utrecht 5 
ват humboldtianum Walp. Edinbur; 5 
Monolena primuliflora Hook. Copenhagen 5 
Pachycentria constricta Bl. ogor 5 
Sakersia africana Hook. Parc Nat. Comoé, 5 
Cóte d'Ivoire 
(Leg. Merz, Téhé 
& Assi) 
Schizocentron elegans (Schl.) Meissn. Edinbu 5 
Tibouchina semidecandra (Schrank & Mart.) Cogn. idel 5 
ососа guianensis Aubl. Heidelberg 5 
Triolena pustulata Triana Heidelberg 5 
T. scirpioides Naud Copenhagen 5 
Crypteroniaceae Crypteronia paniculata Bl. Bogor 
Penaeaceae Penaea mucronata L. Kirstenbosch (J. P. S 
Rourke) 
Saltera sarcocolla (L.) Bullock Cape Point Nature Re- 5 
serve (leg. D. Clark) 
Oliniaceae Olinia emarginata Burtt-Davy B. I. Pretoria (D. M. C. 5 
Fourie) 
Combretaceae Combretum racemosa Kew : 
C. quadrangulare Kurz Bogor 5 
С. sundaicum Miq Bogor 5 
Quisqualis indica L. Heidelberg 5 
Terminalia catappa L. Heidelberg 5 
Lythraceae 
subfam. Ly- Cuphea micropetala H.B.K. Berlin S 
throideae Lafoensia punicaefolia DC. Bogor 5 
Lagerstroemia indica L. Copenhagen 5 
Lawsonia inermis L. Copenhagen 
Lythrum salicaria L. ev Robert Heidelberg 3 
Rotala rotundifolia Buch.-Ham. ainz З 
subfam. Dua- Duabanga sonneratioides Buch.-Ham. Rio de Janeiro (leg. К. з 
bangoideae utitzki 
5 fam. Son- Sonneratia caseolaris (L.) Engl. Bogor 5 
neratioideae 
subfam. Puni- Punica granatum L. Heidelberg S 
coideae 
Rhynchocalyx lawsonioides Oliv. 5 


Natal (leg. H. B. Nich- 


НЕИН _ и 


н 


1984] 


BEHNKE-SIEVE-ELEMENT PLASTIDS 


TABLE 1. Continued. 


829 


Type of 
Family Species Source Plastids 
Myrtaceae Acca sellowiana Burret Heidelberg 5 
Agonis flexuosa (Willd.) Lindl. ew 5 
Angophora cordifolia Cav Kew 5 
Callistemon phoeniceus Lindl Heidelberg 5 
lothamnus rupestris Schau Mainz 5 
Eucalyptus diversifolius Вопр!. eidelberg 5 
Eugenia myrcianthes Niedenzu Copenhagen S 
Hexaclamys edulis Kausel ex D Mainz 5 
Kunzea ambigna (Sm.) Носћг. ew 5 
Leptospermum laevigatum Е. Muell. Heidelberg S 
Lophomyrtus obcordata (Raoul) Burret Utrecht 5 
Melaleuca acuminata Е. Mue Heidelberg S 
Metrosideros excelsa Soland ex Gaertn. Heidelberg S 
Myrceugenia luma Berg ainz S 
us commun Heidelberg S 
Pimenta racemosa (Mill. ) J. W. Morre Bonn S 
Psidium littorate Raddi Berlin 5 
Кћодатта cinerea Jack. Leila Forest, Запдакап, 5 
Sabah (leg. Behnke & 
Lee 83-07-22) 
Tristania conferta R. Br. Leiden 5 
Trapaceae Trapa natans L. Bonn 5 
Onagraceae Circaea cordata Royle Heidelberg 5 
C. x intermedia Ehrh. Zastler, Germany (leg. S 
Behnke & Cole 80- 
08-26/1 
Epilobium fleischeri Hochst. Heidelberg S 
Fuchsia arborescens Sims. Heidelberg S 
Godetia amoena G. Don ew S 
Oenothera biennis L. Heidelberg S 
O. missouriensis Sims. Heidelberg S 
Zauschneria californica Presl. Heidelberg S 
Families allegedly allied (after Dahlgren & Thorne, 1984) 

Haloragaceae Haloragis erecta (Banks & Murr) Eichl. Copenhagen S 
Myriophyllum brasiliense Cambess Bonn S 
Rhizophora. Bruguiera gymnorrhiza Lam. Berlin PVc 
ceae Carallia brachyata Brisbane, Australia (leg. PVc 
Cassipourea elliptica (Sw.) Poir. Finca La Selva PVc 

Costa Rica 
(Juncosa 26 VIII 74) 
C. cf. killipii Cuatrecasas Ch ombi PVc 
(Juncosa 2540) 
Ceriops tagal var. australis C. T. White Cape Ferguson, Queens- PVc 
land (leg. G. J. Mul- 
ler) 
Crossostylis biflora Forst. Edinbu PVc 
C. grandiflora Brongn. & Gris. Mt. Panié, New Caledo- PVc 
nia (Juncosa 20 IX 
81A) 
Kandelia rheedii Wight & Arn. Brisbane, Australia PVc 
(Leg. R. Tracey) 
Bonn PVc 


Rhizophora cf. conjugata 


830 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


TABLE 1. Continued. 


Family Species Source Plastids 
R. mangle L. Heidelberg PVc 
R. sexangula Copenhagen PVc 
R. stylosa Australia (leg. К. Tracey) PVc 
Sterigmapetalum heterodoxum Steyem. & Liesner Sierra de San Luis (Вег- Рус 


ry & Wingfielá 4304) 
Anisophyllea- ^ Anisophyllea trapezoidales Baill. Sepilol Forest Res., РУС 
сеае andakan, Sabah (leg. 
Behnke & Lee 83-7- 
21) 


Combretocarpus cf. motleyi Hook. f. Sri Aman, Sarawak 5 
(Leg. Othman Isma- 
wi) 


Thymelaeaceae Dais cotonifolia L. Mainz S 
phne mezereum L. Heidelberg S 
Passerina filiformis L. Bonn S 
Phaleria disperma Baill. Kew S 
Pimelea ка Labill. Bonn 5 
Wikstroe sp. Kew 5 
Lecythidaceae Pike acutangula (L.) Gaertn. ogor 5 
B. speciosa Forst. Copenhagen 5 
Chydenanthus excelsus (Bl.) Miers Bogor 5 
Couroupita guianensis Aubl. vene 5 
Gustavia angusta L. f. 5 
G. gracillinea Miers us ге Janeiro (К. Ku- 5 
bitzki) 
Napoleonaea е Веапу. 5 
Planchonia vallida Bogor 5 
Elatinaceae Elatine А он ще E: Berlin (S) 
Coridaceae Coris monspeliensis L. Berlin 5 
Chrysobalana- — Chrysobalanus icaco L. Berlin 5 
сеае Couepia grandiflora (Mart. & Zucc. ) Benth. ex Botucatu, Brazil (leg. I. 5 
Hook f. S. Gottsberger) 
Mois tomentosa 
Elaeagnaceae Elaeagnus <<" E Heidelberg $, 
Е. umbellata Heidelberg 5, 
Hippophae a E. Heidelberg So 


Families distantly related (all families mentioned under this heading by Dahlgren & Thorne (1984) contain 
S-type plastids except for:) 


Gunneraceae Gunnera magellanica Lam. Copenhagen : 
G. manicata Lindl. ex André d t Е 
С. tinctoria Mirbel Bon j 
Connaraceae Agelaea macrophylla С ) Leenh. А 
Connarus conchocarp Face “ie A E 
(leg. A. I 
C. oblongus Schellenb. Bogor 
C. suberosus Planch. Botucatu, Brazil (leg. 1. P 
S. Gottsberger) 
Rourea mimosoides (Val.) Planch. Bogor 
Roureopsis emarginata (Jack.) Merr. Bogor Р 


Rhabdodendra- Rhabdodendron amazonicum (Spruce ex Benth. ) Manaus, Brazil (leg. О. E 
e Hub. 


T. Prance P 
R. macrophyllum (Spruce ex Benth.) Hub. Manaus, Brazil (Prance 


———————— 7 c 2 — 


— nr 


— 


— > — 


= SS 


—-——— !7Zi.«-"-————— Q—A—AMv——————————— —e 


1984] 


dition (see e.g., Figs. 3, 8), and all grains may 
show a tendency to disintegrate at their periphery 
into tiny particles — most prominent, e.g., in Cal- 
listemon (Fig. 10), Epilobium (Fig. 13), and Cir- 
caea (Fig. 16). These features make the sieve- 
element plastics of the core families in Myrtales 
not very distinctive, but exclude at least some 
starch iiy like the one-large-grain, He iub: 
shaped, а: 

Most н the pia eater pes allies and the more 
or less distantly related families of Myrtales also 
contain S-type plastids (see Table 1), very few of 
which, however, fit the starch features described 
for the core families (e.g., Figs. 15, 18, 21; prob- 
ably also Fig. 19 but note very large grains). More 
informative is the absence of S-type plastids in 
some of the families. While its quantity is much 
decreased in Myriophyllum (Fi g. 16), starch is 
completely lost in E (Fig. 22) and 
probably also in Elatinaceae. Four families con- 
lain P-type sieve-element plastids — Rhizopho- 
raceae (Fig. 17) of the closer allies and Connara- 
ceae (Behnke, 1982c), Gunneraceae (see Behnke, 
1981а), and Rhabodendraceae (Behnke, 1976) 


e. (So-plastids) contain crystalline 

P(hloem)-protein bodies, another sieve-element 
character which among the myrtalean core fam- 
ilies is only found in Myrtaceae. However, the 

trastructural composition of the crystalline 

"Protein is unlike that of Myrtaceae, but comes 
Very close to crystalline P-protein in Proteaceae, 
Which is also among the distantly related group. 
However, Sieve-element plastids in Proteaceae 
are of S-type. 

The family Rhizophoraceae needs special 
Mention, since according to traditional treat- 
ments it incorporates both S- -type and P-type 
genera. While the 12 species examined from the 
tribes G Gynotrocheae, Macarisieae, and Rhizo- 
= reae (see Table 1) contain very specific sieve- 

ement plastids (Fig. 17) that include numerous 
aen crystals but no starch at all (subtype-PV; 

* only other пои recorded to have this sub- 
19828), E and Erythroxylaceae, Behnke, 
ораза апа Combretocarpus were 


BEHNKE-SIEVE-ELEMENT PLASTIDS 


831 


found to have S-type plastids. If further inves- 
ж on other penera and prier ees 
(e.g. fro tati 

chr romosome cytology) would corroborate the 
plastid diversity, a separation of the Anisophyl- 
leae as a distinct family, Anisophyllaceae, could 
be substantiated. 

Certainly sieve-element plastids cannot be used 
as a critical character to positively shape the or- 
der Myrtales, but are helpful in negating close 
relationships of some of the peripheral families. 


LITERATURE CITED 


BEHNKE, H.-D. 1974. P- und S-Typ Siebelement- 
Plastiden bei Rhamnales. Beitr. Biol. Pflanzen 50: 
457—464 

. Ultrastructure of sieve-element plas- 

tids in Caryophyllales Vontrspormae), ipn edid 

fort 

In T. J. Mabry & H.-D. Behnke ас). good 

lution of Centrospermous Families. Pl. Syst. Evol. 

126: 31-54. 


Sieve-element characters. Jn H.-D. 
Behnke (editor), Ultrastructure and Systematics of 
Seed Plants. Nord. J. Bot. 1: 381—400. 

Ib. Siebelement-Plastiden, Phloem-Pro- 
tein und Evolution der Blütenpflanzen: II. Mono- 
kotyledonen. Ber. Deutsch. Bot. Ges. 94: 647—662. 

1982a. Sieve-element plastids, exine sculp- 
turing and the systematic affinities of the Buxa- 
T Pl. Syst. Evol. 139: 257-266. 

b. Sieve-element plastids of Cyrillaceae, 
e hee vie and Rhizophoraceae. Presenta- 
tion and significance of subtype-PV plastids. Pl. 
Syst. Evol. 141: 31-39 

————. 1982c. Sieve-element plastids of Connara- 
ceae and Oxalidaceae. A contribution to the 
knowledge of P-type plastids in dicotyledons and 
their жо Bot. Jahrb. Syst. 103: 1-8. 

1981. Sieve-element еа and 

crystalline P(hloem)-protein in оѕае: mi- 

is to the cir- 


hie lee їп К. М. Polhill & Р. H. Raven > 
Адуап in І 


Lon cns 
DAHLGREN, R. M. T. 1980. A revised system of clas- 
sification of the angiosperms. Bot. J. Linn. Soc 
80: 91-124. 
DAHLGREN, R. I К Е THORNE. 
order scription, variation, ап 
71: sas. 


1984 [1985]. Ба 
5: circum 
rane бан phi Missouri Bot. Gard. 


6 
MABRY, T. J. 1977. The order Centrospermae. Ann. 
Missouri Bot. Gard. 64: 210-220. 


REPRODUCTIVE ANATOMY AND MORPHOLOGY OF 
MYRTALES IN RELATION TO SYSTEMATICS! 


RUDOLF SCHMID? 


Evidence from reproductive morphology and 
anatomy (excluding palynology) favors an inclu- 
sive M es of 11 core families (see below) over 
either a much broader Myrtales, as advocated, 
for example, by the Englerian school (most re- 
cently Melchior, 1964) or a narrower Myrtales 
and accompanying Lythrales, as advocated by 
Novak (1961, 1972) and more recently and in a 
rather different manner by Briggs and Johnson 
(1979), who, however, withdrew their concept in 
this symposium (Johnson & Briggs, 1984; see 
also argumentation in the appendix in Schmid, 
1980). Embryology provides the best evidence 
for a concept of core Myrtales consisting of Com- 
bretaceae, Crypteroniaceae, Lythraceae, Melas- 
tomataceae sensu lato, Myrtaceae (including 
Psiloxylaceae? and Heteropyxidaceae; Schmid, 
1980), Oliniaceae, Onagraceae, Penaeaceae, 
Punicaceae, Sonneratiaceae, and Trapaceae (fa- 
milial arrangement strictly alphabetical; see also 
Tobe & Raven, 1983a). 

The following embryological traits unite core 
Myrtales: anthers tetrasporangiate*, with con- 
spicuous endothecium*, glandular tapetum, si- 
multaneous cytokinesis; ovules anatropous*, bi- 
tegmic*, : llate; antipodals eph у 
absent*; endosperm писјеаг“; seeds exalbumi- 
nous*, The asterisks indicate that exceptions are 
known. Table 1 (pp. 834—835) lists such excep- 
tions, which in some cases are known for only 
one family or even only one species, for example, 
the trisporangiate anther of Corynanthera flava 
of Myrtaceae (Green, 1979). Other embryologi- 
cal features such as nuclear condition of pollen 
at time of shedding, persistence of anther epi- 
dermis, and types of anther wall development, 
embryo sac, and embryogeny vary appreciably 
(see Table 1). Significantly, Dahlgren and Thorne 


(1984) and Tobe and Raven (1983a) indepen- 
dently arrived at a very similar complex of em- 
bryological characters unifying core Myrtales. 
Reproductive anatomy, that is, histology and 
vasculature, gives no special aid in resolving the 
makeup of Myrtales. Features such as bicollater- 
al bundles (internal or intraxylary phloem) occur 
in peduncles, inflorescence axes, pedicels, flow- 
ers, and fruits of most myrtalean taxa (Schmi 
1972b, 1980, for Myrtaceae and Lythraceae, 
Schmid, unpubl. data and literature survey for 
other families). However, bicollateral bundles are 
1 нй mhed for veg- 
etative parts of Myrtales and other orders (Cron- 
quist, 1981; Dahlgren & Thorn, 1984; Metcalfe 
& Chalk, 1983; van Vliet & Baas, 1984) and then 
applied to their reproductive parts. The same 


pertains to vestured pits, which are unreported 
ut which 


с ME Tux P WR . ] 
теапу nistoiogica 


occur in Lythraceae, Melastomataceae, Myrta- 
ceae, Alzatea (Schmid, unpubl. data) 

ales, amphicribral bundles are common, а. 
cially іп androecia and placentae (Schmid, 1972b, 


ilies). However, amphicribral bundles seem Te 


alone Myrtaceae. An axile ovular supply jer di 
1972a) is most common and clearly le pa 
E" On- 
occurs variously in Myrtaceae, Oliniaceae, 
agraceae, Punicaceae, and Rhynchoca 
Myrtales (Eyde, 1981; Schmid, 1972a, a 
1980, unpubl. data and literature surv pe. 
as in Lecythidaceae sensu lato, Rhizop raceat 


d table 
; Text expanded somewhat from my symposium abstract (Schmid, 1981), with added references an (1984) 


and Thorne 


Supported 


ANN. Missouri Вот. GARD. 71: 832-835. 1984. 


ПИР | 7" 


= 


— 


1984] 


SCHMID—REPRODUCTIVE ANATOMY 


833 


sensu lato, and Thymelaeaceae, which were pre- 
viously attributed to Myrtales (see Dahlgren & 
Thorne, 1984). 

Various families can be fairly safely excluded 
from the aforecircumscribed core Myrtales on 
the basis of a combination of characters from 
both embryology and vegetative anatomy. For 
example, Rhizophoraceae sensu lato, Lecythi- 
daceae sensu lato, Theligonaceae, Cynomori- 
aceae, Hippuridaceae, among others, lack bicol- 
lateral bundles and vestured pits and in some 
cases (Rhizophoraceae, Lecythidaceae) also have 


1983; van Vliet & Baas, 1984), all of which are 
non-myrtalean attributes. And especially tenui- 
nucellate and/or unitegmic ovules, which occur 
variously in Lecythidaceae sensu lato, Hippuri- 
daceae, and Theligonaceae are significant in ex- 
cluding these families from core Myrtales. Thy- 


horne, 1984; Metcalfe & Chalk, 1983; van 
Vliet & Baas, 1984) and on the bes of wood 
anatomy (van Vliet & Baas, 1984), embryology 
(Table 1), and other aspects of reprod e anat- 
omy and morphology (Cronquist, 1981; Dahl- 


such an exclusion (Dahlgr 1984). 
There are, of course, jE esis est rel- 
evant to the aforenoted and other familial exclu- 
sions (see Dahlgren & Thorne, 1984; Orchard, 
1975; Tobe & Raven, 1983а). 


LITERATURE CITED 


Brisas, В, б. & L. А. S. Јонмзом, 1979. Evolution 
In the Myrtaceae—evidence from inflorescence 


Structure. Proc. Linn. Soc. New South Wales 102: 
157-256 


C : 
ORNER, E. J. Н. 1976. The Seeds of Dicotyledons. 
s An Integrated System of Clas- 
lication of Flowering Plants. Columbia Univ. 
D Press, New York. 
AHLGREN, В. & R. Е. THORNE. 1984 [1985]. The 
а Myrtale es: circumscription, variation, and re- 
Сени. Ann. Missouri Bot. Gard. 71: 633- 
D 
Avis, (0. І. 1966. — Embryology of the 
Ev osperms, John W Sons, New York. 
m H. 1981. Rencodaet ctive structures and evo- 
ution in Ludwigia (Onagraceae). Ш. Vasculature, 


оо CE re 


етар conclusions. Ann. Missouri Bot. Gard. 

68: 470-503. 

GREEN, Г W. Corynanthera, a new genus of 
Myrtaceae (Subfamily л» Tribe 
Chamelaucieae). Nuytsia 2: 368-374 

JOHNSON, L. A. S. & B. С. BRIGGS. 1984 [1985]. jos 
tales and Myrtaceae 

i Bot. Gard. 71: 700—756. 

MELCHIOR, Н. 1964. Reihe Myrtiflorae (Myrtales). 

p. 345-366, in H. Melchior (editor), A. Engler's 
Slats der duisi 12. Aufl. Bd. 2. Ge- 
brüder Borntraeger, Berlin-Nikolassee 

METCALFE, C. R. А L. CHALK. Anatomy of the 
eem 2ndedition. Vol. 2 Clarendon Press. 


МоуАк, F. A. 1961. Vyšší rostliny: Tracheophyta. 
Nakladatelství Československé Akademie Véd, 
Praha. 


„ 1972. Ms rostliny: N 2nd edi- 
. 2 Volumes. Academia Nakladatelstvi Ces- 

аА Akadem mie ved, Praha. 

А Тахопотіс revisions in the 


Gonocarpus. Bull. Auckland Inst. Mus. 10: i-iii, 
9. 


SCHMID, В. 1972a. A resolution of the Eugenia-Sy- 
zygium controversy (Myrtaceae). Amer. J. Bot. 59: 
423-436. 


2b. Floral anatomy of Myrtaceae. I. Sy- 
zygium. Bot. Jahrb. Syst. 92: 433-489. 
76. Lon S and anther dehis- 
cence. Bot. J. L aie 13: 303-315. 
19 Rep. end е anatomy of Actinidia 
chinensis Pinar anii Bot. Jahrb. Syst. 100: 
9-195. 


Comparative то and morphol- 

of Ps iloxylon and Heteropyxis, and the 
хиуа and tribal Е of Myrtaceae. 
Taxon 29: 559-595. 


: 198 Te Reproductive anatomy and morphol- 
ogy of Myrtales in relation to systematics. 13th 
Int. Bot. Cong., Sydney, Australia, 21-28 August 
1981, Abstracts, p. 131. 

1982. Descriptors used to indicate abun- 
dance and frequency in ecology and systematics. 
Taxon 31: 89-94. 

SMITH, B. B. & J. M. Herr, JR. 1971. Ovule devel- 
opment, megagametogenesis, and early embry- 
ogeny in Ammannia coccinea Rothb. J. Elisha 

Mitchell Sci. Soc. 87: 192-199 
Tose, H. & P. H. RAVEN. mbryological 
analysis of Myrtales: its definition and character- 
istics. Ann. Missouri Bot. Gard. 70: 7 н 

& 


Тһе embryol of Axi- 

nandra zeylanica Пар) and the rela- 
tionships of the genus. Bot. Gaz. 426-432. 

VENKATESWARLU, J. & P. S. PRAKASA Т 1972. Em- 
bryological урн in some Combretaceae. Bot. 
Not. 125: 161-179. 

VLIET, G. LEM. Е BAAS. 1984 [1985]. Wood 

anatomy and classification of the Myrtales. An 

Missouri Bot. Gard. 71: 783 


ТАМНЕ]. — 


834 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


TABLE 1. Some embryological features of core Myrtales and Thymelaeaceae.’ 


Cryp- 
Combreta € Lythrace Melastom? Myrtacea" 
Number genera/species 20/400 3/10 29/590 200/4,000+ 149/3,675 
Number sporangia/anther 4 4 4 4 4(3) 
Anther with conspicuous yes no yes по (yes)? yes 
endothecium at maturity 
Anther with glandular tape- уеѕ yes yes yes yes 
tum 
Anther with simultaneous yes yes yes yes yes* 
cytokinesis 
Ovules anatropous yes yes yes, very rare yes, very Occ. yes, OCC. other 
other‘ other‘ 
Ovules bitegmic yes yes yes yes yes, very OCC. 
uni 
Ovules crassinucellate yes yes yes^ yes yes 
Antipodals ephemeral, ephe- ephemeral ephemeral ephemeral 
persistent' meral 
Endosperm (initial) nuclear nu- nuclear nuclear nuclear 
clear 
Seeds exalbuminous yes yes yes yes yes, шы 
Anther epidermis persistent yes yes yes oce 
Type of MEN wall devel- Basic! Dicot Dicot irregular™ Basic” 
opmen 
Pollen at poet bi-, occ. trinuc binuc  binuc trinuc binuc 
Type of embryo sac Polygonum, Poly- Polygonum Polygonum Polygonum 
enaeaP gon- 
um D 
Type of embryogeny Asterad 72 Onagrad Onagrad (So- Onagrad (irreg) 
lanad)? 


ldem m 
* Embryological features considered as unifying the 11 families of core Myrtales (arrangement of T: 
strictly alphabetical; see also note b) are above the line; more variable embryological features are below MEC 


family 
Dahlgren & Thorne, 1984). Some conspicuous exceptions are elaborated below. Descriptors such as “rarely” 


therein and below, other recent taxonomic and anatomical literatu ure, and unpubl. pre on r d 
This table was compiled independently of Tobe no Raven (1983a), which appeared while the present 
was in press. These аз noted (pp. a "Thymelaeaceae gd from [core] Myrtales in possessing 


antipodal ёш that ола чй апа (4 s. ااا ا‎ these differences decisive n 
ruling out any direct аеру between Thymelaeaceae and core Myrtales. » Feature (1) 15 apparently сот 
to on к, but tits а giosperm ic unclear. Fea 5 (2) and (3) occur m 


ut are exceptional there (see Tobe & Raven and note i i below). The old literature Tobe ође 
ais Se feature (4) is not in agreement with кај newer conclusion of Corner (1976) given in note pe 
Raven did not cite Corner and also were unaware of the exception indicated i in note j. 1 thus am ma ae use 
than Tobe and Raven by the embryological срчана of TI tales, in рап J arè 
various families of the latter have peculiar em mbryological features. In other жун Tobe and Raven and 
in substantial agreement regarding the mulni features unifying core My 
Key: ation = etapa occ. = occasionally; trinuc = trinucleate; ? = information shouldbe verifi 
uation not known on basis of literature consulted and/or material examined. _ 1 
иконе including Memecylaceae fide Dahlgren and Thorne (1984). Мупасеве pris “А jo and 
ilox 


& 
в 
`@ 
х 

e 
5 

‚© 

e+ 
® 

> 
mi 
B 

g 
d 

= 
© 
8 

3 
у 
= 
AE 
о 
= 
EE 


known correspond precisely with those of core Myrtaceae (Schmid, 1980). 
: angiate only in Corynanthera flava (Green, 197 k even 
Endothecium poorly developed and lacking fibrous thickenings in Melastomatoideae, but conspicuous: 
with fibrous thickenings, in Memecyloideae (see Davis, 1966). 


| 


rrt RR tt 


aaa 


1984] SCHMID—REPRODUCTIVE ANATOMY 835 


TABLE 1. Continued. 


Oliniace Onagrace Penaeace Punicace Sonnerat Trapacea Thymelae 

1/10 17/670 5/25 1/2 2/7 1/3 50/500 

4 4 4 4 4 4 

yes yes 72 yes yes yes yes 

?yes yes 72 ?yes yes yes yes 

" yes 7 m yes yes yes 

no' yes yes yes yes yes yes, to other' 

yes yes yes yes yes yes yes 

yes yes yes yes yes yes 

ephemeral absent 2) ephemeral ephemeral ephemeral or persistent! 
absent 

nuclear nuclear nuclear nuclear nuclear ephemeral nuclear 
(nuclear) or 
absent 

yu yes yes yes yes yes yes, occ. no* 

оо Ie ааа 

n yes т? ?уеѕ уеѕ yes yes 

?Dicot 72 2 7: Dicot Dicot Basic, Mono- 

cot? 

? binuc 27 binuc binuc binuc trinuc 

Polygonum Oenothera Penaea Polygonum Polygonum Polygonum Polygonum 

? Onagrad Asterad 72 Onagrad Solanad Asterad 


о information in Davis (1966), but more recently VEL ee cytokinesis reported (Davis, 1968, 1969; 
Prakash 1969b, 1969c, 19694, 1969e—citations in Schmid, 1972b). 

E ue Oliniaceae hemitropous to campylotropous (Dahlgren & Thorne, 1984). Ovules of Lythraceae also 
ry rare amphitropous (Schmid, 1980), of Melastomataceae also very occasionally eens (Cron- 
quist, Te ; Other taxonomic literature), of M other— hemitropous 
amphitropous (Schmid, 1980), ог Thymelaeaceae anatropous to hemitropous (Cronquist, 1981; Owe, 1966). 
(1972a, 1972b), including some species 


۷ 


meti ue um under E ugenia (Davis, 1966). | 
of 


nnia 
NENET, DY оосо definitions this is crassinucellate ма at best, subcrassinucellate. 

" Guiera senegalensis (monotypic) of Combretaceae has pene rsistent, multiplicative antipodals (Davis, 1966; 
enkateswarlu & Prakasa Rao, 1972), the only known member of core Myrtales with this feature, and thus 


ipodals. 
sh ' Endospe rm occasionally scantily present according to Corner (1976), Petit (1908 —citation in Schmid, 1980), 
mid (1980). and taxonomic literature. 
* Endosperm < commonly absent from the seed or d to a trace, but copious in Lachnaea and Pimelea” 


(Corner, 1976: 27 0; see also Cronquist, 1981). See also note : 
' Anther development irregular, with only ddl Gui galensis (Davis, 1966; Venkateswarlu 
о, 1972). 


^” Anther development irregular and not characterized according to type by Davis (1966) or other workers. 
6ê, information in Davis (1966), but more recently anther development reported to be of Basic type (Davis, 
1969; Prakash, 1969b, 1969c, 1969d, 1969e—citations in Schmid, 1972b). 
SIC type in Wikstroemia canescens, Monocotyledonous type in Lasiosiphon eriocephalus (Davis, 1966). 
€ report of the tetrasporic Penaea type embryo sac for two species of Combretum needs confirmation (see 
& Thorne, 1984; Tobe & Raven 1983a; Venkateswarlu & Prakasa Rao, | 
Solanad embryogeny type in Melastoma malabathricum and Sonerila wallichii (Davis, 1 
1969. ular embryogeny in Darwinia fascicularis, D. micropetala, and Angophora Por (Prakash, 1969d, 
—citations in Schmid, 1972b). 


Р 


THE EMBRYOLOGY AND RELATIONSHIPS OF 
RHYNCHOCALYX OLIV. (RHYNCHOCALYCACEAE)! 


HIROSHI TOBE? AND PETER H. RAVEN? 


ABSTRACT 


era. Also, Rhynchocalyx, despite its shared distinctive multicelled archesporium, 
differs from Lythraceae in many attributes. Thus, evidence from embryo 
fi 


logy, combined with that 


rom other sources, supports the conclusion that RAynchocalyx is not directly related to Lythraceae, 
and is, therefore, best assigned to a family of its own, Rhynchocalycaceae. 


This paper reports the embryology of the rare 
monotypic South African genus Rhynchocalyx, 
and is the second concerning the unique genera 
of the order Myrtales. The first concerned Axi- 
nandra (Tobe & Raven, 1983b). The proper 
taxonomic assignment and relationships of 
Rhynchocalyx, like those of Axinandra, have 
often been disputed. Oliver (1895), who first de- 
scribed RAynchocalyx lawsonioides, classified the 
genus under Lythraceae. Later, Engler (1900) 
treated Rhynchocalyx as one of the “Gattungen 
der Lythraceen von unsicherer Stellung," and 
Koehne (1903) excluded it from Lythraceae. 
Sprague and Metcalfe (1937), however, returne 
it to Lythraceae, stating that Koehne's grounds 
for its exclusion from that family were not ten- 
able. Recently, van Beusekom-Osinga and van 
Beusekom (1975) proposed a broad definition of 
Crypteroniaceae that included Rhynchocalyx, 
together with Crypteronia, Dactylocladus, Axi- 
nandra, and Alzatea. Pollen morphology might 
or might not be taken to support a relationship 
of Rhynchocalyx with the other genera of Cryp- 
teroniaceae sensu lato (Muller, 1975): thus, 
Rhynchocalyx agrees with Dactylocladus and 
Axinandra in having heterocolpate pollen grains 


to Mr. 


zatea differ from the other three genera of 
Crypteroniaceae sensu lato in their wood anat- 
omy, and share many characteristics with Ly- 
th d Melast (van Vliet, 1975). 

On the other hand, leaf, twig, and nodal anat- 
omy suggests that Rhynchocalyx is closer to some 
Lythraceae, Oliniaceae, and Melastomatacea? 
than to the other members of Crypteroniaceae 
sensu lato (van Vliet & Baas, 1975). Neverthe- 
less, differences in floral structure and the pres 
ence of foliar sclereids in the petioles of Rhyn- 
chocalyx (Rao & Das, 1979) indicate that Ий 
not directly related to Lythraceae. In ae 
Rhynchocalyx may be distinguishable from Ly 
thraceae in not having nectaries in its aii 
although this feature needs to be reviewed 
Lythraceae. 

Жыкы. and Thorne (1984) pointed out а 
Rhynchocalyx stood apart from Lye 1 
having petals and stamens on the hypanthia 
and sclereids in its leaf petioles. Taki 


: | Me lysis, 
these facts into account in their cladistic апау ; 
at Rhyn 


family Rhynchocalycaceae for the ње a 
ily that is accepted both by Dahlgren and ‘bed à 
(1984) and by Graham (1984), who ye 
second new family, Alzateaceae, to acco 


teful 
' Grants to one of us (P. H. R.) from the National Science Foundation are acknowledged. We are also gra! his 


ths; 


H. B. Nicholson for the sustained and ample collection of material over a period of many ps! on this 


fine efforts made this study possible. We appreciate the comments of R. Dahlgren and L. A. S. Johnson 


problem. 


? Permanent address: Department of Biology, 
260, Japan 


3 1 0, 
Faculty of Science, Chiba University, 1-33 Yayoi-ch 


У Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166. 


ANN. MISSOURI Вот. GARD. 71: 836-843. 1984. 


| 


| 
| 


| 


ing all of | 


, 


Chiba 


1984] 


FIGURES 1-5 
(е), middle | 
Older anth 


between two mi 
of shedding. А 


ayers ( 


о 
.—4. Cross section of а dehisced anther. Note the persistent sep 
crosporangia on each side of the ant 0 Two-celled pollen gra 


TTOWS point out a nucleus of a generative f a vegetative cell. Bar = 10 


TOBE & RAVEN—EMBRYOLOGY OF RHYNCHOCALYX 


posee Bav Кан ы 


оо 26 
r 


ross section of a young anther. Its wall is formed by an epidermis (ep), an endothecium 
ti and a tapetum (7). mc: microspore mother cell. Bar = 10 um.— 2. Cross section of an 
the tapet T. Only the epidermis ( 


m.—3. Cross section of a mature anthe 


her. B 


аг = ит. 
cell and that о 


838 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Vor 71 


FIGURES 6- —6. 
functional archesporia cell is already divided into a f a young 0 
rest of the archesporial cell (arc) remains undivided. Bar = 10 ит.—7. Longitu dinal section of a уоште of 8 
with а young megaspore mother cell (тс) below parietal cells (pc). Bar = 10 џт.—8. Lo ngitudi 10 шт. 
i d megaspore mother cell (mc). Note the position y" a = an јал - 


Longitudinal section of an ovule primordium with а пуррае archesporium ; dd 
primary parietal cell т апа a sporogenous 


da 
Longitudinal section of a young ovule with a dyad composed of a smaller micropylar megaspore с) ап 


| 


| 


1984] 


date the equally unusual but not directly related 
Alzatea. 

Until we recently reported on the embryology 
of Axinandra (Tobe & Raven, 1983b), no em- 
bryological information was available on the 
genera that were relegated to Crypteroniaceae 
sensu lato by van Beusekom-Osinga and van 
Beusekom (1975). On the <a of available em- 
bryological information, however, we canno 
evaluate the proposed Siue of Axinandra in 
Crypteroniaceae together with Crypteronia and 
Dactylocladus, since the latter two genera are un- 

nown in this respect. The purpose of the present 
paper is to evaluate the relationship of RAyn- 
chocalyx to Axinandra, Lythraceae, and other 
Myrtales, and in the light of this information to 
comment upon its phylogenetic relationships and 
proper taxonomic placement 


e 


MATERIAL AND METHODS 


Flower buds and fruits of Rhynchocalyx law- 
sonioides Oliv. were collected and fixed in FAA 
(five parts stock formalin: five parts glacial acetic 
acid: 90 parts 70% ethanol) at Uvongo River, 
Natal, Republic of South Africa, by Mr. H. B. 
Nicholson. The voucher specimen is Nicholson 
s.n., in 1982 (MO). Preparations of microtome 
sections for the observation were made following 
the techniques discussed in a previous paper 
(Tobe & Raven, 1983b). 


OBSERVATIONS 


ANTHER AND MICROSPORES 


Bo a 


TOBE & RAVEN—EMBRYOLOGY OF RHYNCHOCALYX 


839 


whereas the endothecium and the two middle 
layers degenerate (Fig. 2). The tapetum is glan- 
dular and its cells become two-nucleate before 
degeneration. Thus a mature anther wall at the 
time of dehiscence is composed only of the per- 
sistent epidermis (Figs. 3, 4). The outer half of 
each epidermal cell forms a conspicuous papilla 
(Fig. 3). A septum between two microsporangia 
on each side of the anther remains intact even 
at the time of anther dehiscence (arrows, Fig. 4), 
a condition that is unusual in angiosperms. 

Meiosis i in a кинон шош cell is accom- 
panied by Shape of the 
dur microspore tetrads is, on the basis of 
the examination of 20 selected tetrads, “usually” 
(65%) tetrahedral and “often” (35%) decussate 
(expressions of the frequency follow Schmid, 
1982). Pollen grains are two-celled when they are 
shed (Fig. 5). 


MEGA TE AND NUCELLUS 


The ovule is anatropous and crassinucellate. 
The archesporium is hypodermal and is com- 
posed of three to five cells, only one of which 
further divides periclinally into two: i.e., the up- 
per primary parietal cell and the lower sporog- 
enous cell (Fig. 6). The primary parietal cell di- 
vides once anticlinally (Fig. 7) and both cells 
repeat periclinal divisions to form a massive pa- 
rietal tissue. The sporogenous cell develops into 
a megaspore mother cell (Fig. 7) and becomes 
enlarged by the time of meiosis (Fig. 8). In the 
enlarged megaspore mother cell a nucleus oc- 
cupies a position on the micropylar side (Fig. 8). 
Meiosis in the megaspore mother cell is accom- 
panied by successive cytokinesis. By the first 
meiotic division, the megaspore mother cell is 
partitioned into a dyad of megaspores in which 
the micropylar cell is much smaller than the cha- 
lazal cell (Fig. 9). The second meiotic division 
occurs earlier in the micropylar cell of the dyad 
than in the chalazal cell. The two daughter cells 
thus formed on the micropylar side are always 


Chalaza] 

Spores megaspore (c). Bar = 10 um.— 10. Longitudinal section of a young ovule with a linear tetrad of mega- 
bei (c). Note that the two micropylar megaspores are already crushed while the two chalazal megaspores are 
Пё formed. Bar 


= 10 um.— 11. Longitudinal section of a young o 
(second c боа. bottom). Note that subdermal cells of the oreas are radially — Bar = 10 


ovule with a functional chalazal megaspore 


am, 
13, Long ов виц inal section of a mature embryo sac with дерепега s (arrow). Bar = 10 um.— 

1 section of a ptioropviat part ‹ of a mature er ен E “two-layered structure of the inner (її) 
Ne the Outer (oi) i in eg: egg cell; sy: synergid 


10 um.— Ah esent section of a mature ovule to od the whole structure. Note the position M 


he funicular tissue. ii: inner integument; oi: outer integument; т: micropyle. Bar = 


100 u 


840 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Маг. 11 


ical cell ( 
FIGURES 15-21. —15. a two-celled proembryo composed of an apical ight-celle? 
basal cell (cb). The apical cell is dividi i B 10 um. 


ca) зк 


Longitudinal section of 


a ar = 10 um.— 16. Longitudinal section ipe \ 
proembryo. са: cells derived from the apical cell at the two-celled stage; cb: cells derived e apical cell les 
Bar = 10 um.— 17. Longitudi i der proembryo. Note that cells derived from lower rod. 

form a global part of the proembryo whereas those derived from the basal cell (cb) form the o (em). Arrow 
10 um.— 18. Longitudinal section of a young seed including a young dicotyledonous embryo свой еб 
indicate free endosperm nuclei. 5: suspensor. Bar = 100 um.— 19. Nearly mature seed with a m 


"A e 


| 
| 


| 


| 


1984] 


degenerating when the chalazal cell of the dyad 
is dividing (Fig. 10). A cell plate in the division 
of the chalazal cell of the dyad is also formed on 
the more or less micropylar side (Figs. 10, 11). 
Megaspore tetrads are always linear (Fig. 11) al- 


arrange iquely, and the lowest 
(chalazal) cell functions and thus develops into 
an eight-nucleate Polygonum-type embryo sac. 
Synergids are pyriform, and three antipodals are 
ephemeral; they degenerate without any sign of 
wall formation (arrow, Fig. 12). Consequently, 
an organized mature embryo sac just before fer- 
tilization comprises only five nuclei or cells— 
1.е., an egg, two synergids, and two polar nuclei. 

During megasporogenesis, subdermal cells of 
the nucellus elongate radially and form a jacket 


, around the enlarged megaspore mother cell or 


the megaspores (Figs. 8-11). This tissue, how- 
ever, gradually degenerates or is absorbed as the 
embryo sac enlarges in the later stages. 


INTEGUMENTS 


_ The ovule is bitegmic (Figs. 13, 14). Both the 
inner and the outer integument are initiated by 
periclinal divisions of dermal cells of the nucellus 
and grow only by divisions of the cells derived 
from the dermal initial cells, resulting in a two- 
yered structure. Neither of the integuments 
show any secondary multiplication in thickness 
(Figs. 1 3, 14). Cells of the outer epidermis of the 
> integument become tanniferous as early as 
© megaspore mother cell stage. 
E Inner integument exceeds the outer integ- 
mid in its degree of elongation (Figs. 13, 14); 
ae: € micropyle is always formed by the inner 
ument alone (Figs. 13, 14). 


FERTILIZATION, ENDOSPERM, AND EMBRYO 


Fertilization is porogamous. Endosperm for- 
олан is of the Nuclear type. The endosperm 
dp even at the free nuclear stage and 
ме E the process of seed development (ar- 
би 18); it does not show any particular 
oa ations of free nuclei on the micropylar 

n the chalazal side. Wall formation does not 
eur in free nuclei. We could not find cellular 


Ts oo 


TOBE & RAVEN—EMBRYOLOGY OF RHYNCHOCALYX 


841 


endosperm at any stage of seed development. 
The mature seeds completely lack endosperm 
(Figs. 20, 21). 

Embryogenesis conforms to the Onagrad type. 
The apical cell ofa two-celled p yo divides 
vertically, and the basal cell transversely (Fig. 
15). Cells derived from the apical cell contribute 
to the formation of a major part of the embryo, 
those derived from the basal cell only to a minor 
portion. The latter include the parts that are des- 
tined to form the root cap and cortex, as well as 
the suspensor (Figs. 16, 17). A young embryo has 
two equally developed cotyledons and a short 
and small suspensor (Fig. 18). The embryo in the 
mature seed is more or less flattened, its coty- 
ledons folded inside (Fig. 20). 


MATURE SEED AND SEED COAT 


The mature seed is depressed-ovoid in shape 
with a flat membranous wing on the micropylar 
side (Fig. 19). The wing is formed by divisions 
and elongation of cells of the funiculus (Figs. 14, 
19). No hypostase is formed throughout the de- 
velopment of ovule and seed. 

The mature seed coat is derived from the two- 
layered testa as well as from the two-layered 
tegmen. All of the constituent cells are highly 
elongated, particularly longitudinally. The outer 
surface of the outer epidermis of the testa is con- 
spicuously lignified. 

DISCUSSION 
The embryological characteristics of RAyncho- 


calyx lawsonioides may be summarized as fol- 
] . 


OWS: 

Anther tetrasporangiate; anther wall five layers 

thick, its formation of the Basic type; anther epi- 

dermis persistent, the outer half part of each cell 
. *11 224 z 


forming a p pap 1 
two middle layers ер} 1; tapetum glandular, 
its cells two-nucleate; septum between the two 
microsporangia on each side of the anther per- 
sistent. Cytokinesis in microspore mother cells 
simultaneous; microspore tetrads tetrahedral or 
decussate in shape; pollen grains two-celled when 
shed. 

Ovule anatropous, bitegmic, and crassinucel- 


~ 


2 em: embryo. Ваг = 
Side. w: wing. Bar = 100 


1 mm.—20. Cross section of a mature seed. Cotyledons (cor) of the embryo are folded 
—21. Longitudinal section of a mature seed. Both t 


he two-layered testa (ts) and 


the two-la m. 
yered tegmen (tg) constitute a mature seed coat. em: embryo. Bar = 100 um. 


842 


late, both integuments two-layered; subdermal 
cells of the nucellus elongated radially, forming 
a jacket around the megaspore mother cell or 
megaspores; micropyle formed by the inner in- 
tegument alone; chalaza without hypostase. 

Archesporium of ovule multicelled, compris- 
ing three to five cells, only one of them func- 
tioning and cutting off a parietal cell; cytokinesis 
at meiosis I resulting in a dyad composed of a 
smaller micropylar cell and a larger chalazal cell; 
the subsequent division of meiosis II earlier in 
the micropylar cell of the dyad than in the cha- 
lazal cell; tetrads of megaspores linear; chalazal 
megaspore functional, developing into an eight- 
nucleate Polygonum-type embryo sac; antipo- 
dals ephemeral. 

Fertilization porogamous; endosperm forma- 
tion of the Nuclear type; wall formation not oc- 
curring in free endosperm nuclei; embryogenesis 
conforming to the Onagrad type; embryo dicot- 
yledonous with a short and small suspensor; seed 
exalbumi ith a single flat branous wing 
on the micropylar side. Seed coat thin and fi- 
brous, consisting of elongate cells of the two- 
layered testa as well as ofthe two-layered tegmen. 


Rhynchocalyx shares six ofthe seven basic em- 
bryological criteria that define the order Myrtales 
(Tobe & Raven, 1983a): (1) anther tapetum glan- 
dular, (2) ovule crassinucellate, (3) inner integ- 
ument two-layered, (4) antipodals ephemeral, (5) 
endosperm formation the Nuclear type, and (6) 
mature seed exalbuminous (cf. Tobe & Raven, 
1983a). The only disagreement is that Rhyncho- 
calyx has a micropyle formed by the inner in- 
tegument alone instead of by both integuments, 
and this seems to be a feature subject to evolu- 
tionary modification within the group, indicating 
that the situation in Rhynchocalyx is a derived 
one. 

As regards the view of van Beusekom-Osinga 
and van Beusekom (1975) that Rhynchocalyx 
should be assigned to Crypteroniaceae sensu lato, 
we still have embryological information only 
concerning Axinandra, but lack it for the other 
constituent genera. Rhynchocalyx agrees with 
Axinandra in having an ephemeral endothecium 
(which is also characteristic of the Melastoma- 
taceae as a whole), but differs from Axinandra 
in many features. In Rhynchocalyx, the septum 
between two microsporangia on each side of the 
anther is persistent; the archesporium is multi- 
celled; the micropyle is formed by the inner in- 
tegument alone; the endothelium is not formed; 
the seed wing is formed on the micropylar side. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 | 
In contrast, in Axinandra the septum in the an- | 
ther is ephemeral; the arches is one-celled; | 
the micropyle is formed by both integuments, 
the endothelium is formed; the seed wing is | 
formed on the chalazal side. Evidence from tht 
embryology, as well as from vegetative anatomy | 
(van Vliet, 1975; van Vliet & Baas, 1975), in- i 
dicates the heterogeneity of Crypteroniaceae sen- 
su lato and virtually excludes the possibility that 
it would be desirable to retain both Rhyncho- | 
calyx апа Axinandra in the same family. 

As regards the alternative view that Rhyncho- } 
calyx should be (re-)placed in Lythraceae (van | 
Vliet, 1975; van Vliet & Baas, 1975), the pres | 
ence of the multicelled archesporium in an ovule | 
supports the view because this characteristic has 
been found only in Lythraceae (including Son- 
neratiaceae). Contradicting the view that Rh | 
chocalyx might be directly related to Lythraceae, 
however, are the facts that Rhynchocalyx has an 
ephemeral lotheci and a micropyle formed | 
by the inner integument alone, both features thal 
have not been reported in Lythraceae. In fact, in 
its ephemeral endothecium, Rhynchocalyx age? 
with Á : Ж Ro 5 S 4 


B 


with Lythraceae. The micropyle qi p | 
stitutes a distinct gap between Rhynchocalyx 


side of the anther is persistent; nucel же! 
mal cells elongate radially, forming pu | 
around the megaspores; the homotypic divis! | 
of meiosis occurs earlier in the micropylar © 
of the dyad than in the chalazal cell; starch 


on the other | 
hand, the septum in the anther probably o 
lapses, as is the case in most ango 
radially elongated nucellar subdermal cells 2 
not been observed; the homotypic e 
curs later in the micropylar cell of the dya 
in the chalazal cell; starch grains are ae te | 
the nucellus (Cuphea, Hubert, 1896); ere af 
endosperm commonly shows accumulati | 
free nuclei on the micropylar and/or the : ш | 
region of the embryo sac (Joshi & Venka 
lu, 1936) and may become cellular ( 
1934). | 
In view of all these points of di 
conclude that embryology provides stro 
port for the conclusion of Johnson 


Mauritzo? | 


ference, У 
ng sup | 


| 1984] 


(1984) that Rhynchocalyx should be assigned to 
a monotypic family not directly a to + 
thraceae 

archesporial characteristics with Lythraceae, but 
significant gaps between these two taxa are evi- 
dent in the characters of the anther wall, micro- 
pyle, nucellus, megasporogenesis, and endo- 
sperm. There is no strong evidence linking this 
remarkable South African relict genus directly 
with any other group, and it seems clear that it 
is best placed in a family of its own in order to 
emphasize its great distinctiveness. 


LITERATURE CITED 


BEUSEKOM-OsINGA, R. VAN & C. F. VAN BEUSEKOM. 
1975. Delimitation and subdivision of the Cryp- 
e (Myrtales). Blumea 22: 255-266. 

DAHLGREN, R. & R. F. THORNE. 1984 [1985]. The 
dE M es: circumscription, variation, and re- 


^ oma Ann. Missouri Bot. Gard. 71: 633- 


Davis, G. L. 1966. Systematic Embryology of the 
ngiosperms. John Wiley т Sons, New 

г & K. Prantl, Nat. 
Pflanzenfam. (Nachtr. 

GRAHAM, S. А. 1984 [1982]. pe ДАДА a new fam- 

y of Myrtales in the American tropics. Ann. Mis- 

uri Bot. Gard. 71: 757-779. 
Huser, М. Е. DE. 1896. кеш " Rcs sac em- 
Bot 


| ren 8. 100 — 
OHNSON, L. A. S. & B. О. BRIGGS. 1984 [1985]. Myr- 


TOBE & RAVEN — EMBRYOLOGY OF RHYNCHOCALYX 


843 


tales and Myrtaceae 
Missouri Bot. Gard. 71: 700—756. 
Јозн;, A. C. & J. VENKATESWARLU. 1936. Embryo- 
logical studies in the D uM Ш. Proc. Indian 
Acad. Sci. B, 3: 377-4 
03. duse In A. Engler, Pflan- 
72. 


` 1934. Zur Embryologie einiger Ly- 

thraceen. Acta Horti Gothob. 9: 1-21. 

MULLER, J. 1975. Note on the pollen morphology of 
Crypteroniaceae. Blumea 22: 275-295. 

ME D. 1895. Rhynchocalyx M =“ 
In W. J. Hooker, Icon. Pl. Ser. 4, 24(1): 2 

КАО: А. & S. Das. 1979. Leaf debi —occur- 
rence and distribution in the angiosperms. Bot. 
Not. 132: 319-324. 

SCHMID, R. 1982. Descriptors used to indicate abun- 
dance and frequency in ecology and systematics. 
Taxon 31: 

SPRAGUE, T. A. & C. R. METCALFE. 1937. The taxo- 
nomic position of Rhynchocalyx. Kew Bull. 1937: 
392-394. 

Tose, H. & P. H. RAVEN. 1983a. An embryological 
analysis of Myrtales: its definition and character- 
istics. Ann. Missouri Bot. Gard. 70: 7 

3b. The Сау of de 

nandra zeylanica (Crypteroniaceae) and the 

n meer Pie of the genus. Bot. Gaz. (Crawfordsville) 

144: 426-432. 

Mes GJ c M. VAN. 


dd Wood anatomy of 
J. Microscop. 104: 65- 


1975. Comparative anatomy of 
the Crypteroniaceae sensu lato. Blumea 22: 175— 
195. 


THE EMBRYOLOGY AND RELATIONSHIPS OF 
ALZATEA RUIZ & PAV. (ALZATEACEAE, MYRTALES)! 


HIROSHI TOBE? AND PETER H. RAVEN? 
ABSTRACT 


In this paper we present the first embryological studies of A/zatea, one of the genera of the order 
Myrtales whose placement has been most controversial. Although Alzatea agrees rather completely 


коюы coincide in their micropyle form, and both genera further 
-celled ovule archesporium, which is not known elsewhere in the 
order except in one of the small subfamilies of Lythraceae, Sonneratioideae. A totality of Kee 
Alzate: 
and suggests that Alzatea and Rhynchocalyx may be parallel descendants from a common ancestor, 
with which the modern Lythraceae possibly has a link. 


abes m‏ سے 


~ 


This paper deals with the embryology of the 
rare monotypic Central-South American genus, 
Alzatea, and is the third concerning the unique 
genera of the order Myrtales, following papers 
on Axinandra (Tobe & Raven, 1983b) and Rhyn- 
chocalyx (Tobe & Raven, 1984). As in the case 
of Axinandra and Rhynchocalyx, there has been 
a long history of arguments about the taxonomic 
position of A/zatea. According to Lourteig (1965), 
who gave a historical review up to that time, 
Alzatea has been placed in Celastraceae (De Can- 
dolle, 1825; Bentham & Hooker, 1862), Rham- 
naceae (Miers, 1872; Loesener, 1942: MacBride, 
1951), and Lythraceae (Planchon, 1845; Hallier, 
1911; Pilger, 1915). Lourteig (1965) herself con- 
cluded that A/zatea belonged in Lythraceae, based 
on its floral and vegetative characters as well as 
on anatomical and palynological characters. She 
considered the genus to be a member of subtribe 
Diplusodontinae of tribe Lythreae 

At other times in its history, A/zatea has been 
considered to have a close affinity with another 
unique genus, С rypteronia, regardless of the fam- 


' Grants to one of us (P. H. R.) from the Nati 


calyx. Muller (1975) suggested a possible 
relationship among these five genera based 0n 
their pollen morphology. But van Vliet (1975), | 
van Vliet and Baas (1975), and Baas (1979), on 
the basis of their studies of the wood, leaf, es 
and nodal anatomy, suggested not only ШМ A ) 
zatea and R 1 widely fror | 
three other genera of Crypteroniaceae sensu la ч 
but also that these two genera differed to а SU | 
stantial degree from each other. Dahlgren 4 | 
Thorne (1984) and Johnson and Briggs ( wd 
accepted the establishment by S. Graham (198% | 
of a monotypic family, Alzateaceae 
Results E our recent embryos Ee | 

have indicated that Axinandra and Qu kc | 
calyx are very different from each other, an | 
the former occupies a satellite position ү | 
lastomataceae (Tobe & Raven, 1983b, 1 «1 
Rynchocalyx is of less certain plac - 

probably deserves the family status N^ | 
accorded by Johnson and Briggs (1984). ЊЕ 
ried out the present study of the embryo ЖЕ 
Alzatea, which has hitherto been unknown: || 
contribution to determining its most appropri! | 
systematic position. 


MATERIALS AND METHODS LT ! 
mo 
e only species of what is probably a не | 
typic family, Alzatea verticillata Ruiz 


ledoed for financi 


support. We are also grateful to Miss Sandra koI and Sr. Luis Poveda for the collection of the fine 


on which our study is based. 
? Permanent address: De 
260, 


3 Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166. 
ANN. Missouri Bor. GARD. 71: 844-852. 1984. 


. ; |-сћо, 
partment of Biology, Faculty of Science, Chiba University, 1-33 Yayoi-¢ 


== 
Chis > 


1984] TOBE & RAVEN—EMBRYOLOGY OF ALZATEA 845 


"" ا 


® 


FIGUR 
acum yea -5. —1. Transverse section of a young anther. Its wall is formed by an epidermis (ep), an endo- 
кой а а D layer (ml ^ and а tapetum (/), inside the last of which microspore mother cells (mc) are 
ar — 10um section of an older anther. The epidermal cells (ep) are enlarged while the 


= ^C 
ofa — (et), the middle ces (ml) and the tapetum (1) are —€—X Bar = 10 um.—3. Cross section 


n arrow indi 
w indicates the degenerating septum between two M DM. gon = 100 um.— 5. Two-celled pollen 


Brai 
. Arrows point out nuclei of a generative and a vegetative cell. Bar = 10 um 


846 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Уо1. 71 


_ FIGURES 6-14, —6. Longitudinal section of an ovule primordium with a multicelled archesporium. rial cel 
indicate periclinal divisions of the dermal initial cells of the inner and the outer integument. АЕ al рой 
(arc). Ваг = 10 um.— 7. Longitudinal section of a young ovule with two growing integuments. ape 


the inner (ii) and the outer (oi) integument are two-layered in their original thickness. Only one ofthe gessi" “7 
cells functions to form parietal cells (p) and a single megaspore mother cell (тс). Bar = 10 um. —8. Long! | 


| 
| 


1984] 


was examined in this study. Most of our obser- 
vations were based on flower buds and fruits 
collected in Panama (voucher specimens: Knapp 
4336, 4087, MO; Knapp & Dressler 5392, MO), 
supplemented, particularly with respect to ma- 
ture seed morphology and anatomy, with ma- 
terial collected in Costa Rica (voucher specimen: 
Poveda 3264, MO). Both samples were fixed and 
preserved with FAA (five parts stock formalin: 
five parts glacial acetic acid: 90 parts 7096 eth- 
anol). Preparations of microtome sections were 
made following a technique described in a pre- 
vious paper (Tobe & Raven, 1983b). 

All of our flower samples from Panama (Knapp 
4336, 4087, Knapp & Dressler 5392) have pro- 
duced only sterile pollen sacs which have either 
crushed sporog ti or, at most, aberrant 
pollen grains. Therefore, a different herbarium 
specimen from Peru (Woytkowski 8331, MO) 
was used for the observation of the shape of mi- 
crospore tetrads and of the cell number of mature 
pollen grains. Pollen grains stained with 196 ace- 
tocarmine gave good results in counting the cell 
numbers in a few hours. 


OBSERVATIONS 
ANTHER AND MICROSPORES 


The anther is tetrasporangiate. The wall struc- 
ture prior to maturation comprises four layers, 
1.е., an epidermis, an endothecium, a middle lay- 
er, and a tapetum (Fig. 1). Since the endothecium 
and the middle layer have a common origin his- 
togenetically, the wall formation is regarded as 
conforming to the Dicotyledonous type (Davis 
1966: 10). During the process of maturation, the 
epidermal cells are enlarged while both the en- 

othecium and the middle layer degenerate (Fig. 
2). Consequently, the mature anther wall is com- 
posed only of the persistent epidermis, each of 
the epidermal cells being greatly enlarged (Fig. 
3), and the cells of the connective tissue adjacent 
to pollen sacs are radially elongated (Fig. 4). The 
tapetum is glandular, and its cells become two- 


EN o o 


TOBE & RAVEN —EMBRYOLOGY OF ALZATEA 


847 


nucleate before they degenerate. A septum be- 
tween two microsporangia on each side of the 
anther is broken down as is usual in angiosperms 
(arrow, Fig. 4). 

e shape of microspore tetrads, on the basis 
of the examination of 20 selected tetrads, is ^usu- 
ally" (65%) tetrahedral and “often” (3596) de- 
cussate (expressions for the frequency follow 
Schmid, 1982). Pollen grains are two-celled at 
the time of shedding (arrows, Fig. 5). 


) was 9796 stainable, that of a 
collection from Costa Rica (Dryer 941, CR) was 
only about 3196 stainable, and we have seen no 
fertile pollen in collections from Panama. These 
points clearly merit further investigation. 


MEGAGAMETOPHYTE AND NUCELLUS 


The ovule is anatropous and crassinucellate. 
An archesporium is hypodermal. Four to eight 

hesporial cells are differentiated from the oth- 
er somatic cells (Fig. 6). Only one ofthem divides 
further, periclinally into two: the upper pri- 
mary parietal cell and the lower sporogenous cell. 
The primary parietal cell divides once pericli- 
nally or anticlinally and both cells repeat peri- 
clinal and anticlinal divisions to form a massive 
parietal tissue (Fig. 7). The sporogenous cell de- 


megaspores (Fig. 9). The upper micropylar mega- 
spore of the dyad soon degenerates (arrow, Fig. 
10), while the lower chalazal megaspore func- 
tions (Fig. 10). This functional megaspore in- 
volves three successive nuclear divisions, re- 
sulting in two- (Fig. 11), four-, and eight-nucleate 
embryo sacs. Thus the embryo sac formation 
conforms to the bisporic A//ium-type. Synergids 
are pyriform (Figs. 12, 13), and antipodals are 
very ephemeral and disappear before fertiliza- 
tion. An organized mat bry just befi 
fertilization is composed of five nuclei or cells: 
an egg cell, two synergids, and two polar 


ретоге 


— 


ction of a young ovule with a single enlarged megaspore mother cell (mc). Bar = 10 шт.—9. Longitudinal 


udinal section of a mature ovule with an o 


young ovule showing a dyad of megaspores (c). Bar = 


Sac. N | 0 um.— 11. Longitudinal section of a young ovule witl i 

: Nucleus in the embryo sac (л). Ваг = 10 шт.—12, 13. Two successive longitudinal sections of a mature 

with an organized mature embryo sac. Egg cell (eg); synergid (sy); polar nucleus (pn). Bar = | 

is f s z i nized mature embryo. 
огтед by the inner integument (її) alone. Outer integument (oi). Bar = 


0 um.— 10. Longitudinal section of a young 


0 um.— 14, 
Note that the micropyle (at arrow) 
0 um. 


848 


nuclei (Figs. 12, 13). Both the nucleus and the 
nucleolus of the egg cell are much smaller than 
those of synergids (Fig. 12). 

During megasporogenesis and megagameto- 
genesis, the nucellar tissue does not show any 
particular differentiation. 


INTEGUMENTS 


The ovule is bitegmic. Both the inner and the 
outer integument are initiated by periclinal di- 
visions of dermal cells of the ovular primordium 
(arrows, Fig. 6); they grow only by divisions of 
the cells derived from the dermal initial cells. 
Th ing 1 integument i ist 


РТ £ two- 
layered and keeps its original thickness in the 
later stages as well. The outer integument also 
has a two-layered structure at the initiation stage 
but soon increases in thickness because of anti- 
clinal divisions of the constituent cells, resulting 
in a two- to four-layered structure (Fig. 7). This 
multiplication is most conspicuous in those por- 
tions of the integument along the equatorial line 
of the ovules, which are horizontally placed in 
an ovarian locule, and represents the first sign of 
the formation of the seed wing. 

The inner integument elongates more than the 
outer one. As a result, the micropyle is formed 
by the inner integument alone (Fig. 14). 


- 


EMBRYO AND ENDOSPERM 


Since we could not locate the remnants of pol- 
len tubes in microtome sections of fruit samples 
from Panama (Knapp & Dressler 5392), we are 
not certain whether the egg cell was actually fer- 
tilized in these samples or not. We did, however, 
encounter a fair number of proembryos in this 
collection. Based on our studies of these proem- 
bryos, embryogenesis apparently occurred nor- 
mally until at least the globular proembryonal 
stage, and conforms to the Onagrad type. The 
apical cell ofa two-celled proembryo divides ver- 
tically, and the basal cell transversely (Fig. 15). 
In an older proembryo, the upper globular por- 
tion is formed by cells derived from the apical 
cell at the two-celled proembryonal stage, while 
the lower part including the suspensor is formed 
by cells derived from the basal cell (Fig. 16). An 
embryo in a mature seed (from the sample col- 
lected in Costa Rica) has two equally developed 
cotyledons and a short and small suspensor. The 
cotyledons are not folded (Fig. 19). 

Endosperm formation is of the Nuclear type 
(Fig. 16), although, as mentioned above, there is 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


some doubt that fertilization actually occurred 
in these samples. The endosperm is very scanty 
throughout the seed development. Only about 
ten nuclei are observed even at the four-celled 
proembryonal stage. The endosperm does not 
show any accumulation of free nuclei in the cha- 
lazal region or in the micropylar region. Probably 
wall formation does not occur in free endosperm 
nuclei. The mature seed completely lacks en- 
dosperm (Fig. 17). 


MATURE SEED AND SEED COAT 


The mature seed has a membranous wing with 
the embryo centered (Figs. 18, 19). Its shape and 
size are diverse, depending on the degree of de- 
velopment of the wing. The wing is formed by 
tissues of both the funiculus and the outer 1n- 
tegument along the horizontal line of the seed, 
and is composed mostly of undulating epidermal 
cells (Fig. 20). A hypostase is formed by the time 
the embryo sac is mature, but it does not become 
conspicuous even in the mature seed (Fig. 18). 

The mature seed coat is thin except for a рап 
of the wing, and it is made up mainly from the 
elongate outer epidermal cells of the testa. The 
inner epidermis and, if present, the mesophyll of 
the testa, as well as the inner and the outer ері" 
dermis of the tegmen, completely collapse, leav- 
ing only their cell walls when the seed is mature 
(Fig. 17). 


DISCUSSION 


type; anther epidermis persistent; bot ( 
cium and middle layer ephemeral; tapetum glan 
dular, its cells two-nucleate; septum between p. 
microsporangia on each side of the anther cO 

lapsed; microspore tetrads tetrahedral or decus- 
sate; pollen grains two-celled when shed. e 

anatropous, bitegmic, and crass 

late; both integuments initially two 
later the outer integument two to four 
micropyle formed by the inner integum 


linear dyad of megaspores; micropy 
spore of the dyad degenerating; the 


~ 


- 


1984] TOBE & RAVEN—EMBRYOLOGY OF ALZATEA 849 


FIGURES 15-20, —15. Longitudinal section of a four-celled proembryo. Cells derived from an apical cell at 
the two-celled proembryonal stage (ca); cells derived from a basal cell (cb). Bar = 10 um.— 16. Longitudinal 
Section of a globular proembryo. Cells derived from the apical cell at the antares proembryonal stage (ca); 
cells derived from the basal cell (ch); free endosperm nucleus (fe). Bar = 10 um.— 17. Cross section of a mature 
tes ndosperm is absent. Note that a mature seed coat is composed of dansi outer epidermal cells of the 
r as well as of walls of crushed cells of the other layers. Embryo (em). Ваг = 1 um.— 18. Mature seed with 
M Wembranous wing (w). Embryo (em); hypostase (лур). Bar = 200 um.— 19. Longitudinal section ofa mature 
ng (м); embryo (em). Ваг = 200 um.— 20. Part of the wing. Note the dati epidermal cells con- 

mining the wing. Bar = 100 um 


850 


megaspore developing into a bisporic eight-nu- 
cleate Allium-type embryo sac; antipodals 
ephemeral. 

Endosperm formation Nuclear type; free en- 
dosperm scanty throughout seed development; 
mature seed exalbuminous; embryogenesis con- 
forming to the Onagrad type; embryo dicotyle- 
donous with a short and small suspensor; mature 
seed with a flat membranous wing along the hor- 
izontal line of the seed; wing formed by tissues 
of both the funiculus and the outer integument; 
mature seed coat thin except for a part of the 
wing, consisting only of elongate cells of the outer 
epidermis of the testa and of walls of the other 
collapsed cells of the testa and tegmen. 


Alzatea has six of the seven ordinal charac- 
teristics which we gave for the Myrtales (cf. Tobe 
& Raven, 1983a): (1) anther tapetum glandular, 
(2) ovule crassinucellate, (3) inner integument 
two-layered, (4) antipodals ephemeral, (5) en- 
dosperm formation of the Nuclear type, and (6) 
mature seed exalbuminous. The only disagree- 
ment is that Alzatea, like Rhynchocalyx (Tobe 
& Raven, 1984), has a micropyle formed by the 
inner integument alone instead of by both integ- 
uments. A/zatea is an exceptional member of the 
Myrtales in this respect. 

Alzatea is also characterized by having a bi- 
sporic A//ium-type embryo sac, a feature that is 
unknown elsewhere in Myrtales. Among other 
Myrtales, Penaeaceae and Onagraceae are char- 
acterized by unique embryo sac types, namely 
Penaea-type and Oenothera-type (cf. Tobe & Ra- 
ven, 1983a, for review). All other Myrtales in- 
cluding not only Axinandra and Rhynchocalyx 
(which have been relegated to Crypteroniaceae 
together with A/zatea) but also Lythraceae (which 
may be related to A/zatea), have a monosporic 
Polygonum-type embryo sac (Tobe & Raven, 
1983a, 1983b, 1984). Possession of an embryo 
sac type unknown elsewhere in the order seems 
strongly to suggest an isolated position of A/zatea 
within Myrtales. Embryological comparisons be- 
tween Alzatea and other possibly related Myr- 
tales are presented below using other features. 


4 g р y dip Witr 
Axinandra, with which Alzatea has been includ- 
ed as a member of an enlarged Crypteroniaceae 
(van Beusekom-Osinga & van Beusekom, 1975), 
Alzatea agrees with Axinandra in having a per- 
sistent anther epidermis and an ephemeral en- 
dothecium but differs from it in many other char- 
acters. In Alzatea, the ovule archesporium is 
multicelled; an endothelium is not formed; and 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


the micropyle is formed by the inner integument 
alone. In contrast, in Axinandra the ovule ar- 
chesporium is one-celled; a distinctive endothe- 
lium is formed; and the micropyle is formed by 
both integuments (Tobe & Raven, 1983b). In 
addition, the following point of difference may 
be mentioned: the seed wing is formed by tissues 
of both the funiculus and the outer integument 
in Alzatea, but it is formed by tissues of the 
funiculus alone in Axinandra (Tobe & Raven, 
1983b). This, especially taken together with the 
fact that the embryo is situated centrally in the 
wing in Alzatea, basally in Axinandra, strongly 
suggests that the wings on the seeds of Alzatea 
and Axi l tł logous and that this 
feature should not be used to link the two genera. 
n summary, too many dissimilarities to accept 
a mutual close relationship lie between Alzatea 
and Axinandra. 
As regards a relationship with Rhynchocalyx, 
Alzatea agrees much more closely in its embry- 
ological features with this genus than with any 


istics include: anther epidermis persistent; en- 
dothecium ephemeral; ovule archesporium mul- 
ticelled; micropyle formed by the HE 
integument alone; free endosperm nuclei scanty; 
and, finally, embryogenesis of the Onagrad type 
Tobe & Raven, 1984). Alzatea differs from 
Rhynchocalyx, however, in the following 1€ 
spects: the septum between two microsporang? 
degenerates in Alzatea but is persistent 1n We 
chocalyx; the radial elongation of nucellar su j 
dermal cells surrounding megaspores does " 
occur in Alzatea but is characteristic of wo 
chocalyx; a hypostase is present in Alzatea 
absent in RAynchocalyx; the seed wing 15 e 
by tissues of both the funiculus and the Ne 
integument in Alzatea but it is formed by SS a 
of the funiculus alone in Rhynchocalyx e 
Raven, 1984). Once again this suggests ~~“ 
seed wing in A/zatea may not be пои хі 
with that іп Rhynchocalyx, and should ga је: 
used as evidence of relationship betwee? a 
genera. Moreover, as we have seen, the сто“ 
is situated centrally in its wing 11 - 
Rhynchocalyx, it is situated apically ^ 


however, suggests that A/zatea is шош c 
related to RAynchocalyx than to eio d 
though A/zatea is still very distinct wee 
almost certainly not directly related 10 
chocalyx. : i 
As regards a possible relationship 10 Lyth 


| 


| 


| 


-— - 


— 


1984] 


ceae, Alzatea agrees with this family in having a 
multicelled ovule archesporium but differs from 
itin many respects. The anther epidermis is per- 
sistent in A/zatea but probably not in Lythraceae; 
the endothecium is ephemeral in A/zatea but 
seems to develop into fibrous thickenings in Ly- 
thraceae; starch grains are absent in the nucellus 
in Alzatea but present in Lythraceae (Cuphea, 
Hubert, 1896); the micropyle is formed by the 
inner integument alone in Alzatea but by both 
integuments in Lythraceae; the endosperm is 
scanty throughout seed development in A/zatea, 
much more abundant in Lythraceae (cf. Tobe & 
Raven, 1983a). Although we do not have com- 
plete enough information on the mature seed 
morphology and anatomy of Lythraceae to char- 
acterize the family fully, the points of difference 


TOBE & RAVEN—EMBRYOLOGY OF ALZATEA 


851 


considerable number of embryological charac- 
teristics in each case. These relationships strong- 
ly favor the establishment of a monotypic family 
Alzateaceae, standing apart from both Cryptero- 
niaceae in a restricted sense and from Lythra- 
ceae, a treatment which is here proposed by Gra- 
ham (1984), with support from Dahlgren and 
Thorne (1984) and from Johnson and Briggs 
(1984). 

When compared embryologically with other 
Myrtales, A/zatea shares many more character- 
istics with Rhynchocalyx than with any other 
genus. Similarities with Rhynchocalyx are shown 
by the vegetative characters (such as stomatal 
type and overall wood anatomy), too, although 
a considerable number of points of difference 
with Rhynchocalyx in other vegetative features 
(such as cuticular texture, petiole anatomy, an 
vessel hology) al іп (van Vliet, 1975; 


ичи 


zatea in Lythraceae on embryological grounds 
alone, thus Supporting the conclusions of Gra- 
ham (1 984). 

As regards the possibility of a relationship to 
Melastomataceae, which has recently been sug- 
gested on the basis of vegetative anatomy (van 
Vliet, 1975; van Vliet & Baas, 1975), Alzatea 
agrees with this family (only with the subfamily 
Melastomatoideae) in having a persistent anther 
epidermis and an ephemeral endothecium but 
differs from it in the following respects. Anther 
'apetal cells are two-nucleate in Alzatea, one- 
nucleate in Melastomataceae; the ovule arche- 
Sporium is multicelled in A/zatea, one-celled in 
Melastomataceae; the micropyle is formed by the 
inner integument alone in Alzatea, by both in- 
leguments іп Melastomataceae (cf. Tobe & Ra- 
es 1983a). Thus embryological similarities be- 
e is ni and Melastomataceae are limited 
i er wall characters alone whereas the dis- 

arities include embryological features of 
Many different kinds. Alzatea seems clearly to 
á much more distinct from Melastomataceae 
an from Rhynchocalyx. 
a evidence from the embryology 
си as well as from that of Rhynchocalyx 
dns Raven, 1984), clearly contradicts the 
bilo efinition of Crypteroniaceae to include 
zatea and Rhynchocalyx proposed by van 
она and van Beusekom (1975). 
че здө distinct from all other Myrtales in hav- 
dition ISporic Allium-type embryo sac. In ad- 
d Alzatea differs from Axinandra, Rhyn- 
ocalyx, Lythraceae, and Melastomataceae in a 


van Vliet & Baas, 1975). A relationship between 
Alzatea and Rhynchocalyx was likewise implied 
by their grouping as the only members of Cryp- 
teroniaceae subfamily Alzateoideae by van Beu- 
sekom-Osinga and van Beusekom (1975). Rhyn- 
chocalyx tends increasingly to be included in 
Lythraceae (van Vliet & Baas, 1975; Dahlgren & 
Thorne, 1984; Graham, 1984). Our recent study 
of the embryology of Rhynchocalyx suggests, 
however, that Rhynchocalyx is more distantly 
related to Lythraceae than might have been ex- 
pected (Tobe & Raven, 1984). The fact that A/- 
zatea has more similarities with Rhynchocalyx 
than with other Myrtales suggests that A/zatea 
and Rhynchocalyx are parallel descendants from 
a common ancestor, with which the modern Ly- 
thraceae possibly have a direct link. Our conclu- 
sion here agrees with that of Johnson and Briggs 
(1984), who, on the basis of their cladistic anal- 
ysis, concluded that RAynchocalyx was not di- 
rectly related to Lythraceae but deserved to be 
assigned to a family of its own. We believe on 
the basis of the accumulating evidence that the 
similarities between A/zatea, Rhynchocalyx, Ly- 
thraceae (including Sonneratiaceae), and pre- 
sumably Crypteroniaceae sensu stricto also are 
based on generalized ancestral features, not on 
8 с а акыр. Th 


A 11 


de p e 
unambiguous conclusion seems to be that if any 
one of these groups deserves recognition at the 
family level, each of them does. The only dis- 


inct e yologi on to 
Alzatea, Rhynchocalyx, and Lythraceae is the 
possession of the multicelled ovule archespori- 
um, which is unknown elsewhere in the order 


852 


except in one of the subfamilies of Lythraceae, 
Sonneratioideae (Tobe & Raven, 1983a). This 
shared characteristic seems to be suggestive of a 
relationship between these groups, although we 
still cannot evaluate the systematic significance 
of such an embryological character. 

From the viewpoint of vegetative anatomy, 
Alzatea is the only Myrtalean genus that has a 
trilacunar nodal type, which is considered an 
cestral rather than a derived feature (Baas, pers. 
comm. in Dahlgren & Thorne, 1984). The tri- 
colporate pollen grains of A/zatea clearly are also 
an unspecialized, ancestral feature, thus contrast- 
ing with the undoubtedly derived heterocolpate 
grains of Axinandra, Dactylocladus, Rhyncho- 
calyx, and many other Myrtales and the spe- 
cialized and very unusual bilaterally flattened bi- 
syncolporate grains of Crypteronia (Muller, 1975). 
But the persistent anther epidermis, the ephem- 
eral (or non-fibrous) endothecium, and the bi- 
sporic A/lium-type embryo sac, all of which аге 
characteristic of A/zatea, are undoubtedly de- 
rived features. They do not suggest a direct re- 
lationship of A/zatea with any other group, how- 
ever, and thus do not contradict the notion that 
it may have had a long, independent evolution- 
ary history of its own. 

We believe that the studies we have reported 
here underscore the utility of embryological fea- 
tures in elucidating the pathways of evolution 
within Myrtales. In order to fix the exact position 
of unique genera such as A/zatea and Rhyncho- 
calyx better, comprehensive embryological stud- 
ies will be required not only of Lythraceae and 
Melastomataceae (both of which have been 
studied only to a limited degree), but also of 
other genera, especially Crypteronia and Dac- 
tylocladus, which are unknown embryologically. 

Waren these dps Am available, embryological 


11 
J str Vos 


contribution to our aea с>. of this very 
distinct austral order of angiosperms, and to help 
to illuminate the relationships between its an- 
cient evolutionary lineages 


an- 


LITERATURE CITED 


Baas, P. 1979. The anatomy of ae Ruiz & Pav. 
ER Acta Вог. Neerl. 28: 156-158. 
BENTHAM, G. & J. D. HOOKER 
PL 108973711. 


eg Celastrineae. 
In Gen 
BEUSEKOM-OSINGA, R. vAN & C. F. vAN BEUSEKOM. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


975. Delimitation and subdivision of the Cryp- 
teroniaceae (Myrtales). Blumea 22: 255-266. 
CANDOLLE, А. P. De. 1825. Celastrineae. In Prodr. 
2: 2-1 


DAHLGREN, R. & R. F. THORNE. pes [1985]. The 
order Myrtales: circumscription, variation, and re- 
vi gidi ide Ann. Missouri a Gard. 71: 633- 
699. 
Davis, G. L. 1966. Systematic Embryology of the 
ngiosperms. John Wiley & Soris, New York 
GRAHAM, S. A. 1984 [1985]. Alzateaceae, a new fam- 
ily of Myrtales in the American tropics. Ann. Mis- 


HALLER, Н. 1911. Uber Phan erogamen von unsi- 
cherer oder cola Stellung. Meded. Rijks- 
Her. 1910: 1—40. 

Husert, M. E. De. 1896. Recherches sur le sac em- 
bryonaire des plantes grasses. Ann. Sci. Nat. Bot., 
Sér. 8, 2: 37-128. 

JOHNSON, L. A. S. 2n. Q; Briccs. 1984 [1985]. My: 

es and M —a phylogenetic analysis. 
Missouri Bot. Gard. 71: 700-756. 

LoESENER, T. 1942. Celastraceae. ПА. E Engler & K. 
Prantl, Nat. Pflanzenfam. 2nd edition. 20b: 87- 
197. 


LouRrEIG, A. 1965. On the systematic position i 
Alzatea R. & P. Ann. Missouri Bot. Gard. 52: 371- 
37 


8. 
MACBRIDE, P Rhamnaceae. /n Flora of Peru. 


. London 28 
5. Note on the pollen morphology of 
Crypteroniaceae. Blumea Mene 

PILGER, В. 1915. Celastraceae. In A. E 
Prantl, Nat. Pflanzenfam. (Маск) 404 
202. 


тегіса 
MULLER, J. 1 
): 198- 


PLANCHON, J. Е. 1845. Sur le affinites des oul 
Henslowia Wall. (Crypteronia ?) Blume, ac 
mum ? Blanco, висе Сап. et Alzatea 
Pav. London J. Bot. 

SCHMID, R. 1982. шн а used to indicate ШИШ 
dance and frequency in ecology and syste 
Taxon 31: 89-94. 

Tose, Н. & Р. Н. RAVEN. 1983a. Ane embryologe 
analysis of the Myrtales: its definition a ri 
acteristics. Ann. Missouri Bot. ae dais of Att 

& 1983b. The етогу and the reli 
rawfordsville) 


1984 [1985]. The — 
relationships of Клупсћоса у С \ у. 
calycaceae). Ann. Missouri Во 


nandra zeylanica (Сорас 
tionship of the genus. Bot. Gaz 
144: 426 


of 
VLIET, Ө: gu M 1975. Wood ana 04:65- 
айыра» sensu ;u lato. J. MicroscoP- 

82. 


75. Comparative et пуй 
the Crypteroniaceae Lae lato. Bl lumea 2 
195. 


| 


| 


| 


FLAVONOIDS OF RHYNCHOCALYCACEAE (MYRTALES) 


JOHN E. AVERETT! AND SHIRLEY A. GRAHAM? 


ABSTRACT 


chocalycaceae is a monotypic pod represented by the rare e lawsonioides from 
rtalea with closest a 


South Africa. Although unquestionably m 


an, it is isolated in the ord 


nity to 


oo verticillata i in the monotypic Alzateaceae. Foliar flavonoids of ahea are reported for 


osides, present in approximately 


the first time. Th 


yco 
equal тесе These г are quercetin 3- O-glucoside, 3- О ова, 3-O-rhamnoside, 3-O-xy- 


loside, and 3-O-galactoside. Querc etin 3-O-gluco 
Alzatea. The pattern agrees wi 
and flavones are rare. It differs in absence o 
more specific relat 
and widespread occurrence of the compound 


Rhynchocalycaceae is a newly recognized 
monotypic family based on the rare RAyncho- 
calyx lawsonioides Oliv. from Natal, South Af- 
rica. It has been regarded generally as a genus of 
the Lythraceae, related to Lawsonia in subtribe 
Lagerstromiinae (Oliver, 1895; Sprague & Met- 
calfe, 1937) although that position was rejected 
by the monographer of the family (Koehne, о. 
Recently, it was included in a remodeled Cry 


Ana- 
tomical, embryological, and morphological data 
now support the relationship of Rhynchocalyx 
to the unigeneric Alzateaceae but reflect a degree 
of isolation that merits its recognition as а sep- 
imo (Johnson & Briggs, 1984; Graham, 


Chemistry of Rhynchocalyx has not been pre- 
viously reported. In this study, foliar flavonoids 
are isolated, identified, and compared to the gen- 
eral myrtalean flavonoid pattern. 


MATERIALS AND METHODS 


Fac leaf material of one population of Rhyn- 
“a a ten lawsonioides was examined (South Af- 
Voucher specimen is deposited at MO. 
Techniques for chromatographic and spectral 
Nea of flavonoids follow those presented by 
Noni bry et al. (1 970). Briefly, the flavonoids were 
Tacted overnight from the leaves with 85% 
e The resulting extract was applied to 
tman 3MM chromatographic paper both di- 
Been 
‚ Department of Biology, University of Missouri-St. 


with typical profile of the 


de and quercetin 3- O-diglucoside also occur in 


ationships are possible based о on these flavonoid data due to the generalized nature 


rectly and after concentration on a rotary evap- 
orator. Solvent systems of t-butanol, glacial ace- 
tic acid, and water (3: 1:1 v/v) and 15% glacial 
acetic acid in water were sig to develop two- 
dimensional chromatograms. The chromato- 
grams were observed over ЧА light and 
in the presence of ammonia vapor to detect color 
characteristics of the various compounds pres- 
ent. The procedure presented by Mabry et al. for 
the isolation and spectral analyses of the com- 

d with tl that fused 
soditinn acetate was used for determining the 
spectral curve for that reagent. 

Acid and enzyme hydrolyses were carried out 
routinely for glycosidic characterization and to 

obtain the aglycone for positive identification. 
Acid hydrolyses were carried out in 5% НСІ at 
70°C for about 1 hour. Normally this treatment 
is sufficient to remove O-glycosides from the fla- 
vonoid skeleton. Enzyme hydrolyses were ac- 
complished at 27°C in water. These techniques 
as well as other pertinent data concerning the 
characterization of phenolic glycosides are dis- 
cussed by Harborne (1965). 

B-p-glucosidase was regularly employed be- 
cause this enzyme is reliable for detecting the 
presence of glucose. The flavonoid glycosides on 
which enzyme hydrolysis was not effective were 
hydrolyzed in acid as outlined above. The re- 
sulting sugar was then taken up in water and 
spotted on cellulose thin-layer plates along with 
standard sugars for comparison. Circular thin- 
layer chromatograms were developed in ethyl 
acetate, pyridine, and water (6: 3: 2 v/v) as de- 

scribed by Exner et al. (1977). After drying, the 


Louis, St. Louis, Missouri 63121. 


` Department of Biological Sciences, Kent State rar air ey Ohio 44242. 


ANN. Missouri Bor. Garp. 71: 853-854. 1984. 


854 


TLC plates were sprayed with a 0.1 M solution 
of p-anisidine and pthalic acid in 96% ethanol 
and placed in an oven at 130°C for ten minutes. 
The sugars were then visible as dark brown, red, 
or green bands. The aglycones also were run, 
along with authentic reference compounds, by 
circular thin-layer chromatography. 


RESULTS 


Five flavonol glycosides, all based on quer- 
cetin, were present in the population of Rhyn- 
chocalyx examined: (1) quercetin 3-O-xyloside, 
(2) quercetin 3-O-galactoside, (3) quercetin 3-O- 
rhamnoside, (4) quercetin 3-O-diglucoside, and 
(5) quercetin 3-O-glucoside. Each of the com- 
pounds was present in approximately equal con- 
centrations. Compounds (2) and (5) were insep- 
arable by the methods utilized but both sugars 
were noted in the hydrolysates. Rf values were 
consistent with the respective monoglycosides 
and not with that of a diglycoside. 


CONCLUSIONS 


The flavonoid pattern in Rhynchocalyx con- 
sists of a range of flavonol monoglycosides. The 
emphasis on flavonols in the genus is consistent 
with its classification in the Myrtales where com- 
mon flavonols are the most frequent constituents 
(Bate-Smith, 1962; Gornall et al., 1979). Both 
quercetin 3-O-glucoside and quercetin 3-O-di- 
glucoside are also found in Alzatea (Graham & 
Averett, 1984). Their wide dispersal in the an- 
giosperms, however, precludes any taxonomic 
implication. Myricetin, typical of the order, is 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Уо1. 71 


absent in both Rhynchocalyx and Alzatea. Fla- 
vonoid data support placement of Rhynchocalyx 
in the Myrtales but offer no further indication of 
phylogenetic relationship. 


LITERATURE CITED 
оиа Е. С. 1962. Тће Phenolic com 


ка Bot. 58: 95-173. 
BEUSEKOM-OSINGA, R. J. vAN & C. F. VAN BEUSEKOM. 
1975. Delimitation and subdivision of the Cryp- 


. AVERETT & H. BECKE 
hy: a convenient method for phy- 
tochemical analyses. Phytochem. Bull. 10: 36-41. 
GORNALL, R. J., B. . DAHLGREN. 1979. 
The distribution of flavonoids i in the angiosperms. 
Bot. pe 
GRAHAM " м 1984 [1985]. Alzateaceae, а new 
ily of Myrtales in the American tropics. Ann. Mis- 
souri Bot. Gard. 71: 757-779. í 
VERETT. 1984 [1985]. Flavonoids 0 
s). Ann. Missouri Bot. Gard. 


HARBORNE, J. 965. Plant polyphenols—XIV, 

НЕ of flavonoid glycosides by е 
d enzymatic hydrolyses. Phytochemistry 4: 1 
120. 

JOHNSON, L. A. S. & B. О. Bris. 1984 [1985]. po 

tales and Myrtaceae—a ар вале analysis. Ann. 
uri Bot. Gard. 71: 700-75 

Кее ЈЕ. 1903. Lythraceae. In A. Engler, Pan 
zenr. 17(IV, 216): 272. 

MABRY, T. J., К. MARKHAM & M. THOMAS. -= 
The Systematic eni of „КИШИ 
Springer-Verla, York Inc 

Olive D. 1895. RAynchocal | awsome Oliv. 

n W. J. Hooker, Icon. РЇ; pee rm 48. 

зина Т: А. . METCALFE. ull 1 n 

omic position of Rhynchocalyx. ees B 
392- 394. 


c——— o! J]— o 


FLAVONOIDS OF ALZATEACEAE (MYRTALES) 


SHIRLEY A. GRAHAM! AND JOHN E. AVERETT? 


ABSTRACT 


Three leaf flavonoids are reported from the Alzateaceae, a monotypic family of the New World 
tropics. Two are flavonol 3-O-glycosides: quercetin 3-O-glucoside and quercetin 3-O-diglucoside. The 


third is tentatively identified as 5,4'dihydro 


oxy flavone. The presence of these flavonols is consistent 


with the position of A/zatea in the Myrtales. The profile differs from the common pattern of the order 
in absence of myricetin and is further distinguished by absence of C-glycoflavones and the presence 
of a flavone, supporting the segregation of Alzatea as a distinct family within the Myrtales. More 
specific relationships with taxa in the order cannot be аан on this biochemical evidence because 
of the widespread occurrence of flavonols in the Myrtales 


Alzateaceae is a monotypic family of the New 
World tropics, long known from Peru and Bo- 
livia, and more recently discovered in the low 
montane rain forests of Panama and Costa Rica. 
The single species, Alzatea verticillata Ruiz & 
Pavón was first бега from. Peru in 1798. 

nine fam- 
ilies in five orders (Graham, 1984). In recent 
years the genus has been considered either a 
member of the Lythraceae (Lourteig, 1965) or 
the Crypteroniaceae in the order Myrtales (van 
Beusekom-Osinga & van Beusekom, 1975). It 
ly associated with the African 
genus Rhynchocalyx, M of uncertain affinities. 
Classification and relationships of these infre- 
quently collected genera have been restricted to 
comparison of macromorphological characters. 

On the basis of newly accumulated — 
much of it presented in this volume, the m 
talean position of Alzatea is confirmed. Mum 
ical studies demonstrate the presence of the in- 
ternal phloem and vestured pitting definitive of 
Myrtales (van Vliet, 1975). Embryologically, six 

t (Tobe 


МЗ Y 


а t Raven 1984). Presence of ellagic acid in the 
“aves (Graham, 1984) is consistent with the 
Nora an order especially characterized by 
hs a (Bate-Smith, 1962). Within the or- 
zatea takes an isolated position. It retains 
le Bes seemingly ancestral features, such as tri- 
bá те nodes and generalized pollen features, 
dx are associated with a number of unique 
Mi Orphic attributes. Phylogenetically, A/za- 
E separated from its nearest relative, RAyn- 
осајух, by a substantial suite of specialized 
TS Ahi c recognition of the mono- 

Pic Alzateaceae 

hue. s S MCN 


Chemical characteristics, whose usefulness in 
suggesting phylogenies and taxonomic classifi- 
cation is widely accepted (Stuessy & Crawford, 
1983), are not well known for Alzatea. Ellagic 
acid and flavonoid mono- and diglycosides, in- 
cluding 3-OH-flavonols, are reported but have 
not been specifically identified (Graham, 1984). 
In this study the foliar flavonoids are isolated 
and identified, and comparison made to the gen- 
eralized myrtalean flavonoid profile. 


MATERIALS AND METHODS 


Dried leaf material of two populations of A/- 
zatea was examined for flavonoids. Voucher 
specimens are deposited at MO (Costa Rica: Car- 
tago, Gómez 18725, 18728; Panama: Chiriquí, 
Knapp & Vodicka 5532). 

Techniques for chromatographic and spectral 
analyses of the flavonoids follow those presented 
by Mabry et al. (1970). Briefly, the flavonoids 
were extracted overnight from leaves with 8596 
methanol. The resulting extract was applied to 
Whatman 3MM botl 


both di- 
rectly and after concentration on a rotary evap- 
orator. Solvent systems of t-butanol, glacial ace- 
tic acid, and water (3:1:1 v/v) and 1596 glacial 
acetic acid in water were used to develop two- 
dimensional chromatograms. The chromato- 
ms were observed over ultraviolet light and 

in the presence of ammonia vapor to detect color 
characteristics of the compounds present. The 
procedure presented by Mabry et al. (1970) for 
the isolation and spectral analyses of the com- 
t fused 


1 
pullo 


sodium acetate was used for determining the 
spectral curve for that reagent. 


‚ Department of Biological Sciences, Kent State University, Kent, Ohio 44242 
* Department of of Biology, University of Missouri-St. Louis, St. Louis, Missouri 63122. 


ANN. MISSOURI Bor. Garb. 71: 855-857. 1984. 


856 


ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL 71 
TABLE 1. Absorption maxima for compound three (max™™). 
MEOH NaOMe AICI, АІСІ,/НСІ NaOAc H,BO, 
2717327 273, 388 280, 305, 346 282, 306, 345 275; 328 328 
Acid and enzyme hydrolyses were carried out DISCUSSION 


routinely for glycosidic characterization and to 
obtain the aglycone for positive identification. 
Acid hydrolyses were carried out in 5% НСІ at 
70°C for about one hour. Normally this treat- 
ment is sufficient to remove O-glycosides from 
the flavonoid skeleton. Enzyme hydrolyses were 
accomplished at 27°C in water. These techniques 
as well as other pertinent data concerning the 
characterization of phenolic glycosides are dis- 
cussed by Harborne (1965). 

6-D-Glucosidase was regularly employed be- 
cause this enzyme is reliable for detecting the 
presence of glucose. The flavonoid glycosides on 
which enzyme hydrolysis was not effective were 
hydrolyzed in acid as outlined above. The re- 
sulting sugar was then taken up in water and 
spotted on cellulose thin-layer plates along with 
standard sugars for comparison. Circular thin- 
layer chromatograms were developed in ethyl 
acetate, pyridine, and water (6:3:2 v/v) as de- 
scribed by Exner et al. (1977). After drying, the 
TLC plates were sprayed with a 0.1 M solution 
of p-anisidine and pthalic acid in 96% ethanol 
and placed in an oven at 130°C for ten minutes. 
The sugars were visible as dark brown, red, or 
green bands. The aglycones also were run, along 
with authentic reference compounds, by circular 
thin-layer chromatography. 


RESULTS 


Three flavonoids were present in the two pop- 
ulations of A/zatea examined. Two of the com- 
pounds were flavonol 3-O-glycosides: quercetin 
3-O-glucoside and quercetin 3-O-diglucoside. 
The third was tentatively identified as a 
5,4'dihydroxy flavone. The latter compound is 
similar to apigenin in Rf values (0.86, TBA and 
0.06, HOAc) and in color (purple in UV). Spec- 
tral data for the two compounds, however, differ 
significantly (Table 1). The data indicate fewer 
hydroxyls than apigenin and the absence of a 7 
hydroxyl. Thus, while the identification of the 
third compound is less than certain, there are 
few other possibilities compatible with these data. 


The emphasis on flavonols in Alzatea is con- 
sistent with its taxonomic placement in the Myr- 
tales where the flavonoid profile of the order con- 
sists of common flavonols and their O-methyl 
derivatives (Bate-Smith, 1962). The same fla- 
vonol glycosides are also found in the related — 
genus Rhynchocalyx (Averett & Graham, 1984) 
and are nearly ubiquitous in the woody angio- 
sperms (Gottlieb, 1975). Alzatea is distinctive m 
the absence of myricetin, which is otherwise com- 
mon in the order, and in the absence of C-ly- 
coflavones reported from Lythraceae, Combre- 
taceae, Onagraceae, and Myrtaceae (Gornall et 
al., 1979). The presence of a flavone is unusual 
for Myrtales, where flavones are very rare (Gor- 
nall et al., 1979). In lack of myricetin and pres 
ence of a flavone, Alzatea flavonoids are more 
similar to those of Rosales than Myrtales. The 
two orders are believed to share a common e | 
ancestor (Dahlgren & Thorne, 1984) and the 4" 
zatea pattern could reflect that putative eo 
ship. Further evaluation of the presence 0 8 
flavone and the limited flavonoid profile e 
ited are not feasible since Alzateaceae WR 


ly evolutionary or later reduced con y 
flavonoid data are consistent with other ge 
atic information; viz. A/zatea has many € 
features of the Myrtales, but also sufficient ©) 
ferences to justify recognition as its own 

in the order. 


LITERATURE CITED » 
Averett, J. E. & S. A. GRAHAM. 1984 je не 
vonoids of Rhynchocalycaceae (M 


Missouri Bot. Gard. 71: e constituents 
cance. J. Linn. 


опо 


1984] 


lationships. Ann. Missouri Bot. Gard. 71: 633- 


Exner, J., J. E. AVERETT & H. BECKER. 1977. Circular 
chromatography: a convenient method for p 
tochemical dabis. Phytochem. Bull. 10: 36- 41. 

GORNALL, R. . BoHM & HLGREN. 1979. 
6 distribution of б ысы: in the angiosperms. 

Bot. Not. 132: 1-30. 

GOTTLIEB, О. К. 1975. Flavonols. Chapter 7 in J. B. 
Harborne, T. J. Mabry * Helga Mabry (editors), 
The Flavonoids. о demic Press, New York. 

GRAHAM, S. A. 1984 [1985]. АБ ма a new fam- 

e in the American tropics. Ann. Mis- 
Bot. Gard. 71: 757-779. 

Мен J. B. 1965. Plant Polyphenols— XIV, 
characterization of flavonoid glycosides by acidic 
T: enzymatic hydrolyses. Phytochemistry 4: 107- 


GRAHAM & AVERETT—ALZATEACEAE— FLAVONOIDS 


857 


LOURTEIG, А. 1965. 
Alzatea verticillata R. 
Gard. 52: 371-378 

MABRY, T. J., К. MARKHAM & M. Tuomas. 1970. 
The Systematic Identification of Flavonoids. 
Springer-Verlag New York Inc., New York. 

Stugssy, T. Е. & D. J. CRAWFORD. 1983. Flavonoids 
and phylogenetic reconstruction. Pl. Syst. Evol. 
143: 83-107. 

TOBE, Н. & P. RAVEN. 1984 [1985]. The Борбу 
and relationships of Alzatea Ruiz & Pavon (А!- 
zateaceae, Myrtales). Ann. Missouri E ска. 
71: 844-852. 

VLIET, С. J. C. M. VAN. 1975. Wood anatomy of 
Crypteroniaceae sensu lato. J. Microscopy 104: 
65-82. 


On the systematic position of 
P. Ann. Missouri Bot. 


POLLEN CHARACTERS IN RELATION TO 
THE DELIMITATION OF MYRTALES! 


VARSHA C. PATEL,? JOHN J. SKVARLA? AND PETER Н. RAVEN? 


ABSTRACT 


Pollen grains representative of the Lythraceae (including subfamilies Punicoideae, Sonneratioideae, 
and Duabangoideae), Trapaceae, Oliniaceae, Combretaceae, Alza eaceae, Rhynchocalycaceae, Pen- 
aeaceae, Crypteroniaceae, Melastomataceae, Myrtaceae (including Psiloxylaceae and Heteropyxida- 
ceae), and Onagraceae, the 11 families constituting the order Myrtales, were examined with scanning 
(SEM) and transmission (TEM) electron microscopy. With omission of the Trapaceae, Myrtaceae, 
and Onaeraceae. th ining familiec | MS у ы т 4 1 1 Жи. 


former two subfamilies and weakly defined in the latter. Meridional ridges are also present in some 
Lythraceae lacking subsidiary colpi. 

Exine sculpturing in the mesocolpia is variable throughout the order with Crypteroniaceae, Alza- 
teaceae, Oliniaceae, and Penaeaceae basically psilate; Melastomataceae basically striate and rugulate; 
Combretaceae echinate, reticulate, rugulate, striate, and psilate; Lythraceae subfam. Lythroideae es 
psilate, verrucate, and granular; Lythraceae subfam. Punicoideae basi lly granular-microrugulate; an 
Lythraceae subfam. S tioid d Duab ideae basically verrucate-rugulate. Commonly, eo 


Ud 
ГО ЧУ Н {. Ек x. Al 
МОЈЕ. а 


ry colpi ( Ip ities) and col р g he mene 
regions. Exine structure is essentially of the post and ва construction with the fundamental ektexine 
and endexine stratification layers. In all Combretaceae and some Melastomataceae the foot layer 15 
strikingly delineated as domes, whereas in Alzateaceae the columellae layer follows a zig-zag course. 
The Oliniaceae and Penaeaceae are distinct throughout the order with remarkably thickened tectum 


lv 


Onagraceae. Myrtaceae, with pollen oblate-elliptic in lateral view and triangular in polar view, 
also without a counterpart in Myrtales. Based on the nature of the colpi, three distinctive pollen groups 
are evident: (1) longicolpate, (2) syncolpate and parasyncolpate with and without int 

ities, and (3) brevicolpate and brevissimicolpate. Myrtus communis and Psidium littorale m: 


( eae). 
genera of questionable taxonomic placement, suggests that they fit within the Myrtaceae. T 
family, Onagraceae, is also very distinctive in Myrtales. The viscin threads, tetrads and 


esed grateful to the many individuals, worldwide i 
eip our work would have been severely restricted. Th i i i tly appreciated 
Chissoe, S. Nelson, and P. Hoch. отел ука эз is work 
2 partment of Botany and Microbiology, University of Oklahoma, Norman, Oklahoma 13019, И 
was originally part of a Ph.D. dissertation at the University of Oklahoma. 
Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166. 


ANN. Missouri Вот. GARD. 71: 858-969. 1984. 


1984] 


PATEL ET AL.—POLLEN CHARACTERS 


859 


exceptionally thick endexine, essentially spongy-paracrystalline ektexine with columellae absent or 
1 1 1 4 4 + 1 + 2: at and 2-apertur 


ate grains (in Fuchsia) distinguish 


greatly re ^| yer,p gap , gra 
this family, which with a few superficial similarities to Trapaceae and Penaeaceae differs from all 


others in Myrtales. 


Pollen morphology in the core families of the 
Myrtales as recognized by Dahlgren and Thorne 
(1984) has received surprisingly little study. The 
very extensive reference citations given in the 
four monumental pollen bibliographic indices of 
Thanikaimoni (1972, 1973, 1976, 1980) for these 
families include a// studies in which pollen mor- 
phology is mentioned (e.g., atlases; regional and 
local floras; anatomical and embryological re- 
ports; horticultural, agricultural and geological 
records; chemical systematics, etc.), but relative- 
ly few of them are actually based on compre- 
hensive pollen investigative research. Of those 
emphasizing pollen morphology, about 9096 are 
confined to light microscopy Scanning 
electron microscopy (SEM) was utilized to a lim- 
ited degree and, remarkably, structural data from 
transmission electron microscopy (TEM) (with 
the exception of Muller, 1973, 1975, 1978a, 1981; 
Lugardon & van Campo, 1978; Gadek & Mar- 
їп, 1981, 1982; Skvarla et аі, 1975, 1976; 
Skvarla et al., 1978) are virtually non-existent in 
the order, Furthermore, there are noticeably few 

odern studies in the three largest families, Me- 
lastomataceae, Combretaceae, and Myrtaceae, 
ы though the latter is currently under intensive 
examination by Gadek and Martin (1981, 1982, 
Pers. comm.). 

In this report we have attempted to provide a 
pa morphologic overview of the major taxa 
nii core families (i.e., Lythraceae, including 

amilies Punicoideae, Sonneratioideae, and 


ues уай characters as revealed by SEM, 
wo this is supplemented in large part by 
Сга! information obtained by TEM. 


MATERIALS AND METHODS 


--— Pollen was treated by the acetolysis 
KOH t of Erdtman (1960). In some samples 596 
mes reatment followed acetolysis. For SEM, 
e ux. pollen was either critical point dried 
"id ried from 9596 ethanol, sputter coated 

8014, and examined with an ISI Super II 


SEM. For TEM, acetolyzed pollen was processed 
according to previously described methods 
(Skvarla, 1966) and examined with a Philips 
model 200 TEM. Some Onagraceae pollen was 
examined by TEM without acetolysis, that is, 
either freshly collected in 2.596 glutaraldehyde in 
0.1 M cacodylate buffer at pH 7.2, or after re- 
hydration from herbarium sheets. In both, sub- 
sequent processing basically followed earlier 
techniques (Skvarla, 1973). Pollen was examined 
with LM primarily to determine the nature of 
colpi and endoapertures. 

Table 1 lists taxa examined, collecting infor- 
mation, ubiquity of subsidiary colpi, figure ref- 
erences, and select morphologic data. 

The organization of this report is such that the 
core families are given individual discussion to 
include (1) general palynology, (2) specific mor- 
phology for taxa listed in Table 1, (3) a brief 
review of previous studies when relevant, and 
(4) significant morphological correlations with 
other core families. Following this treatment of 
the core families an attempt is made to sum- 
marize as well as synthesize the data for the entire 
order. Plate legends, in addition to being descrip- 
tive, frequently cite other reports in order to pro- 
vide as complete a background as possible. 


TERMINOLOGY 


The terms used in this study to describe pollen 
grain morphology are essentially those of Erdt- 
man (1971) for exomorphology and Faegri and 
Iversen (1975) for endomorphology. Although 
most are standard palynological jargon and 
therefore not in need of clarification, a few are 
particularly crucial to describing Myrtales pollen 
and are therefore discussed below. 

1. Subsidiary colpi (pseudocolpi). According 
to Faegri and Iversen (1964: 225) a “Pseudo- 
colpus (pseudopore): differs from a normal fur- 
row (pore) in that it is not an exit for the pollen 
tube," while the definition of Erdtman (1971: 
467) is “Colpoid streaks not functioning as ap- 
ertures." Muller (1981) considers the term to be 
a misnomer because pseudocolpi function in vol- 
ume changes ofthe pollen grain during expansi 
and contraction in response to moisture content 
(i.e., harmomegathy of Wodehouse, 1935), 


El. Pollen examined. (The parentheses ( ) in the column for subsidiary colpi mean that intercolpar concavities are recognized. Unless stated otherwise, 
all pollen grains are tricolporate.) 


Sub- 
sidiary 
Taxon Locality Collector Herbarium Colpi SEM-TEM Figure No. Remarks 
LYTHRACEAE 
subfam. Lythroideae 
Ammannia coccinea Rottb. California, USA Twisselman 7983 KE 6 TEM 
A. robusta Keer & Regel Oklahoma, USA Waterfall 3027 OKL 6 SEM, TEM 2A,B, 5A 
Crenea surinamensis L. Guyana de la Cruz 3301 MO 6 SEM IF Meridional ridge 
Cuphea carthagenensis Guatemala Aguilar 104 OKL 0 SEM С Tectal ridges 
(Jacq.) MacBr 
C. nitidula HBK. Mexico Graham 614 KE 0 TEM 5D Tectal ridges 
C. petiolata (L.) Koehne Arkansas, USA Demaree 40737 OKL 0 SEM 2D-F Variable striate sculp- 
ture 
C. racemosa (L.f.) Spreng. Veracruz, Mexico Graham 689 KE 0 TEM 
Diplusodon villosus Pohl Brazil Irwin et al. 26402 MO 0 SEM, ТЕМ 3A, B, 6E Tricolpoidorate, colpus 
Heimia salicifolia (HBK.) ^ Mexico Graham 141 KE 0 TEM 5G 
Link 
H. salicifolia (HBK.) Link Mexico Ventura 2430 MO SEM 1С-Е gtd oe and 
colpa 
Lafoénsia punicifolia DC. Chiapas, Mexico Breedlove 40657 MO 0 SEM, TEM 3D-F, 5Е, F, Meridional PX 
: 6A ural fields and 
Lagerstroemia speciosa (L. Honduras, cultivated Lent 4 OKL 0 SEM 3C Meridional ridges 
ers. 
Nesaea schinzii Koehne Bulawayo Distr., Rhode- Best 395 MO 6 SEM 1A,B 
subfam. Punicoideae 
Punica granatum L. Iran Antonio s.n. OKL 0 — — 
P. granatum L. Iran Grant 15704 MO 0 $ЕМ, ТЕМ 7А,В,8А Weak meridional 
ridges 
Р. protopunica Yemen, Socotra K 0 SEM, TEM 7C-G, 8B, С Meridional ridges 


Smith & Lavranos 
730 


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TABLE 1. Continued. 
Sub- 
sidiary 
Taxon Locality Collector Herbarium Colpi SEM-TEM Figure No. Remarks 
subfam. Duabangoideae 
Duabanga moluccana ВІ. Los Banos, Philippines Elmer 18275 MO 0 SEM 4F Triporate, meridional 
ridges, apertural 
fields, polar caps 
subfam. Sonneratioideae 
Sonneratia caseolaris Mahe Island, Seychelles Sauer 3808 MO 0 SEM 4E Triporate, meridional 
D ridges, apertural 
fields, polar caps 
TRAPACEAE 
Trapa japonica Flerov Japan Boufford et al. 19962 MO 0 SEM, TEM 10A-D, 11D Meridional ridges over 
apertures 
T. natans L. unknown Reverchon herbarium MO SEM 10E Meridional ridges over 
2532983 ertures 
T. natans L. Germany Engelmann s.n. MO SEM, TEM 9A, B, IOF, ПА Meridional ridges over 
apertures 
T. natans L. New York, USA House 21708 MO 0 SEM, TEM 9C-F,11B,C Meridional ridges over 
apertures; polyads 
OLINIACEAE 
Olinia — Burtt Natal, South Africa Hillard & Burtt 8691 MO 3(%) SEM, TEM 13A-D, 14E Asymmetric colpi, half 
Dav subsidiary colpi 
O. тайа Hofmeyr & Zululand Wylie 8822 K 3 (2) SEM 12А-С Asymmetric oe. half 
subsidiary colpi 
О. ees A. Juss. Malawi Chapman 996 MO 3 (0) SEM, TEM 12D-F, 14А Asymmetric colpi, half 
subsidiary colpi 
O. rochetiana A. Juss. Mt. Meru, Tanzania Greenway & Fitzger- MO 3(%) TEM 14D Asymmetric colpi, half 
а 14970 subsidiary 
O. vanguerioides E. G. Rhodesia Chase 6774 K 3(5) — Asymmetric colpi, half 
Baker subsidiary colpi 
O. ventosa (L.) Cufod. Cape Province, South Fries et al. 660 MO 3(%2) SEM, TEM 13E, Е, 14B, C Asymmetric colpi, half 
Africa 


subsidiary colpi 


SWAIOVVHO NA3TIOd-— "IV ІЯ TALVd [#861 


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—— 


TABLE 1. Continued. 
Sub- 
sidiary 
Taxon Locality Collector Herbarium Colpi ЅЕМ-ТЕМ Figure No. Remarks 
COMBRETACEAE 
Anogeissus acuminata Burma Po Chin 6100 MO 3 SEM 18D, F Echinate surface 
Wall. 
Buchenavia suaveolens Ei- Amazonas, Brazil Gentry & Ramos MO 0 SEM 18A-C Echinate surface 
hler 
Hs macrostachya Chiapas, Mexico Breedlove 25160 MO 3 SEM, ТЕМ 17A, 21B 
andl. 
Los. floribunda Mysore, India Saldanha 16363 MO 3 SEM 15G 
(Roxb.) Poir. 
Combretum cacoucia Exell Stann Creek Distr., Be- Dwyer et al. 552 MO 3 SEM 15A-C 
lize 
C. farinosum HBK. Sinaloa, Mexico Boke & Florantos 1 OKL 3 SEM, TEM 16D, 20B, C 
C. laxum Jacq. Loma Tequerre, Brazil Duke 10994 (3) MO 3 SEM, TEM 16E, G, 20A 
C. trifolium Vent. Vietnam Squires 792 MO 3 SEM 16F 
Conocarpus erecta L. Sinaloa, Mexico Waterfall 16249 OKL 3 SEM, TEM 17B, 20E 
Guiera senegalensis Lam. Cameroun Leeuwenberg 7485 MO 3 SEM 18E 
Laguncularia racemosa Costa Rica Croat 593 A MO 0 SEM 19E, F 
(L.) Gaertn 
Lumnitzera racemosa Eastern Province, Sri Davidse 7545 MO 3 SEM, TEM 19D, 21C 
Willd Lanka 
Poivrea coccinea DC. Tulear Prov., Madagas- Croat 31768 MO 3 SEM 19C 
Pteleopsis myrtifolia Wankie Distr., Zim- Raymond 130 MO 3 SEM 176 
(Laws.) Engl. & Diels abwe 
Quisqualis indica L. Laguna, Philippines С Q-2160 OKL 3 SEM 15F 
О. parviflora (Ridl.) Exell. Malaya Stone MO 3 SEM 16H, I 
Я. Pellesriniana (Exell.) Zaire Grant E MO 3 TEM 21D 
во argentea Venezuela Maguire et al. 41879 MO 3 SEM 17E, G 
Kun 
ee pseudocola Tchien Distr., Liberia Baldwin 8007 MO 0 SEM, TEM 19A,B,21A Reticulate surface 
ай catappa L. Croat 30941 MO 3 SEM 17F 


Tulear Prov., Madagas- 
car 


T98 


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Dahlgren & Strid 
3764 


TABLE 1. Continued. 
Sub- 
sidiary 
Taxon Locality Collector Herbarium Colpi SEM-TEM Figure No. Remarks 
T. edulis Blanco Luzon, Philippines Bernardo 23688 MO 3 TEM 20D 
T. edulis Blanco Laguna, Philippines Quisumbing 2156 OKL 3 SEM 17D 
T. oblonga (R. & P.) Pois. Colombia Renteria-Arriaga et MO 3 SEM 16A-C 
al. 1889 
Thiola inundata Ducke Amazonas, Brazil Ducke 644 MO 3 SEM 15р, E Echinate surface 
RHYNCHOCALYCACEAE 
Rhynchocalyx lawsonioides Natal, South Africa Nicholson s.n. MO 3 SEM, TEM 4A,C, 6D 
Oliv. 
ALZATEACEAE 
Alzatea verticillata Ruiz & Mendoza, Peru Woytkowski 8331 MO 0 SEM, TEM 4B, Р”, 6B, С 
PENAEACEAE 
Brachysiphon acutus South Africa Dahlgren & Strid LD — ТЕМ 27В 
(Thunb.) A. Juss. 3387 
B. fucatus (L.) Gilg. South Africa Dahlgren & Strid LD 3 SEM 24A, B Some tetracolporate 
2012 
Е a lateriflora (L. f.) South Africa Dahlgren & Strid LD 3 SEM 25A-C 
4979 
Do n4 formosa South Africa Kerfoot 5723 LD 5 SEM, TEM 23A,C,E,27A Some tetracolporate 
(Thunb.) R. Dahlgren 
Penaea cneorum Merrb. South Afríca Dahlgren & Strid LD 4 SEM 23D D F Tetracolporate 
subsp. cneorum 2982 
P. cneorum Meerb. subsp. South Africa Dahlgren & Strid LD — ТЕМ 27Е 
ruscifolia R. Dahlgren 2090 
P. mucronata L. South Africa Grant 2630 О 4 $ЕМ, ТЕМ 22А-С, 26А Tetracolporate 
Saltera sarcocolla (L.) Bul- South Africa p" & Strid LD 3 SEM, TEM 24C-E,27C, D Some 6-colporate 
oc 389 
S. sarcocolla (L.) Bullock South Africa ballo & Strid LD — 
4988 
Sonderothamnus petraeus South Africa Dahlgren & Strid LD 3 SEM, TEM 25E, Е, 26B, С 
Sond.) R. Dahlgren 3654 
5. speciosus (Sond.) R. South Africa LD 3 SEM, TEM 23G, 24F, 26D Some tetracolporate 
Dahlgren 


SH31O0V3HIVHO N3TIOd — "IV ІЯ TALVd [7861 


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TABLE 1. Continued. 
Sub- 
sidiary 
Taxon Locality Collector Herbarium Colpi SEM-TEM Figure No. Remarks 
Stylapterus ericoides A. South Africa Dahlgren & Strid LD 4 SEM, TEM 22D-F, 27E Tetracolporate 
Juss. subsp. pallidus R. 3365 
Dahlgren 
CRYPTERONIACEAE 
Axinandra zeylanica Thw. — Ratnapura Distr., Sri Waas 1210 MO 
Lanka 
A. zeylanica Thw. Sri Lanka Gunatilleke & Guna- MO 3 SEM, TEM 288, D, 30C 
tilleke 582 
Є rypteronia a Philippines Ramos 1478 MO TEM 30A 
С кыен. culat Thailand Niyomdham s.n. MO 2 SEM, TEM 30B,3IB, D Dicolporate syncolpate 
C Sp. urma Dickason 6680 MO 2 SEM ЗА Dicolporate syncolpate 
Dactylocladus stenostachys North Borneo Hassan 732 (A) A 3 SEM 28E Some tetracolporate 
D. stenostachys Oliv. Sarawak Chai 39708 MO TEM 29B 
D. stenostachys Oliv. Sarawak SPH. 3975 MO 3 SEM, TEM 28А, Е, 29C Some tetracolporate 
D. stenostachys Oliv. Sarawak Chai 1982 MO 3 SEM, TEM 28C, С, 29A 
MELASTOMATACEAE 
Acanthella sprucei Hook. f. Amazonas, Venezuela Davidse 2793 MO d SEM, TEM 33E,38D 
Adelobotrys tessmannii Huanuco, Peru Woytkowski 7850 MO (3) SEM, TEM 34A-C, 39А, В Some grains were сиђе 
Marhgraf haped with 4 colpi 
and 8 subsidiary col- 
pi on its edges 
Allomorphia caudata Yunnan, China Henry 10761 MO (3) SEM 34D 
(Diels) Li 
Astronia cumingiana Vidal Sarawak James et al. 5.34401 MO (3) SEM, TEM 34E, 39C 
Bredia hirsuta Bl. Tokunoshima, Japan Iwatsuki 523 MO (3) SEM, TEM 34F,39F 
Comolia stenodon (Naud.) razil King & Almeda 8370 CAS 3 SEM 36H 
Triana 
Dissochaeta celebica B\. Johore, Malaya pitis 2667 MO 3 SEM, TEM 33F, 38B 
Dissotis brazzae Cogn. ala, Zaire w & Musumba MO 3 SEM, TEM 33C. D. 38C 
p 
Marumia nervosa B\. Selangor, Malaya Ahmad S.A. 1080 MO 3 SEM, TEM 33A, B, 38A 


t98 


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TABLE 1. Continued. $ 
Sub- 
sidiary 
Taxon Locality Collector Herbarium Colpi SEM-TEM Figure No. Remarks 
Memecylon normandii Ghana Hall & Abbiw s.n. MO 3 SEM ЭТЕ 
Jacques-Felix 
Miconia alypifolia Naud. Peru Ochoa 11675 CAS 3 SEM 36A-C Some 6-colporate with 
colpi and intercolpar 
concavities 
M. caesia Cogn. & Gleason Colombia Barclay et al. 3352 US 3 SEM 36D 
ex Gleaso 
M. hondurensis Donn. Sm. Costa Rica Almeda & Nakar CAS 3 SEM 35D, E Some dicolporate, syn- 5 
colpate with inter- = 
colpar concavities “ 
М. melanotricha (Triana) | Panama Wilbur & Luteyn CAS (3) SEM 35A-C M 
1 otricha 19393 Ё, 
Mouriri cf. glazioviana Minas Gerais, Brazil Anderson 8895 MO 3 SEM 31F | 
Сорп. 5 
Osbeckia polycephala Matale Distr., Sri Lanka Lazarides 7219 MO 3 SEM, TEM 32B, 37D,E - 
Naud. 3 
Oxyspora paniculata DC. Yunnan, China Henry 90104 MO (3) SEM 34G, H, 39D, E 5 
Tibouchina candolleana Minas Gerais, Brazil Williams & Assis OKL 3 TEM 376 T 
(DC.) Cogn. 8044 Е 
T. urvilleana (DC.) Cogn. Сий. UC-Berkeley; na- Schmid 1980-12 MO 3 SEM 32С 9 
tive, Brazil = 
Tococa broadwayi Urban Venezuela Steyermark 94999 US 3 SEM 36F T 
T. formicaria Ma Ratter 3253 CAS 0 SEM 36G 
T. spadiciflora Triana Carretera, Colombia .Forero et al. 5703 MO 2 SEM, TEM 36E, 40A Polyads 
T. spadiciflora Triana Colombia Archer 1976 US ? 35F-I 
T. stephanotricha Naud Marischal Prov., Peru Schunke 8106 MO 0 SEM, TEM 36E, 40B, C Triporate 
Trembleya phlogiformis Minas Gerais, Brazil Irwin et al. 19723 MO 3 SEM, TEM 32A, 37B 
DC. 
Tristemma littorale Benth. Lagos State, Nigeria Brown 938a MO 3 SEM, TEM 32D,37A 
Votomita monadelpha Brazil Ducke 18494 K 4 SEM 32E, F Tetracolporate 
(Ducke) Morley 
MYRTACEAE 
Acmena smithii (Poir.) Victoria, Australia Beauglehole & Finck NSW (3) SEM 47B en 
Merrill & Perry ACB 32281 ^ 


TABLE 1. Continued. 
Sub- 
sidiary 
Taxon Locality Collector Herbarium Colpi SEM-TEM Figure No. Remarks 
Austromyrtus bidwillii New South Wales, Aus- W. Bauerlen 584 NSW 0 SEM 48F 
Benth.) Burret tralia 
Baeckea virgata Andrews Cult. UC-Berkeley; na- Schmid 1980-13 0 SEM 44A 
tive, Australia, New 
Caledonia 
Balaustion microphyllum Western Australia A. M. Ashby 312 NSW 0 SEM 44C 
С. A. Gardner 
Callistemon citrinus (Cur- Cult. UC-Berkeley; na- Schmid 1980-11 UC (3) SEM 43B, D 
is) Stap tive, Australia 
C. teretifolius F. Muell. Cult. UC-Berkeley; na- Schmid 1978-198 UC (3) SEM 43A, C 
tive, Australia 
сае validus S. L. Cult. UC-Berkeley; na- Schmid 1980-14 UE (3) SEM 43E Some tetracolporate 
Moo tive, Australia 
Chamaelaucium uncina- Western Australia Webster 18570 NSW 0 SEM 44F, Н Some dicolporate 
um Schau 
сайх У Darwin, Australia Byrnes 2786 NSW (32 SEM 47A 
(Roxb.) Merrill & Perry 
Eremaea pauciflora Domin Western Australia Coveny 8073 NSW 0 SEM 43F 
Eucalyptus ficifolia F. Cult. UC-Berkeley; na- Schmid 1980-10 De (3) SEM 42C-E 
Muell. tive, Australia 
E. robusta Michoacan, Mexico Cutler 4044 OKL (3) SEM 42F 
Eugenia cp „5 & Cayo Distr., Belize Croat 23525 OKL 0 SEM 47C 
am rg. 
E elliptifolia Merrill Leyte, Philippines Wenzel 1248 MO (3) SEM 47D 
Heteropyxis natalensis Natal, South Africa Davidson 2642 MO (3) SEM 42A, B 
Harv. 
Homoranthus wilhelmii Northern Eyre Peninsu- Alcock 4038 NSW 0 SEM 44B 
Cheel la, Australia 
Hypocalymna angustifol- Western Australia Coveny 8063 NSW 0 SEM 44E, G 
ium Schau. 
Luma ни (Molina) A. Cult. cem na- Schmid 1978-194A C 0 SEM 47E 
live, 
Cult. UC-Berkeley; na- Schmid 1980-9 UC о SEM 45C 


мааа decussata R. 
Brown 


tve, Australi 


ieee Sa) a 


998 


Мачу о 'IVOINV.LOH PIOOSSIN JHL ЧО STVNNV 


IL 10A] 


TABLE 1. Continued. Б 
и 
sidiary 
Taxon Collector Herbarium Colpi SEM-TEM Figure No. Remarks 
M. hypericifolia Smith С ult. ретеу: na- Schmid 1978-195 UC (3) SEM 45A, B 
M. preissiana Schau. Cult. UC- “Berkeley na- Schmid 1978-196 UC 0 $ЕМ 45D 
M. pulchella R. Brown TN UC- A. na- Schmid 1980-15 UC 0 SEM 45G Some tetracolporate 
ralia 
M. rhaphiophylla Schau. Ко River, West Earle 70 OKL (3) SEM 45E : 
A lia » 
Metrosideros Го С. Lord Howe Is., Australia s. col. NSW (3? SEM 41B z 
оо à 108602 ш 
M. polymorpha = Oahu, Hawaii, USA Chambers 3005 OKL (3)? SEM 41A "a 
Myrceugenella apiculata Pucara Peninsula, Ar- Dawson & Schwabe OKL 0 SEM 47F D 
DC. i 203A L 
Myrtus communis L. Cult. UC-Berkeley; na- Schmid 1980-18 UC 0 SEM, TEM 48B-D,49A-D Some tetrahedral tet- e 
ope rads > 
ч octodonta F. Idlers Bay, Papua New Womersley NGF NSW 0 SEM 46G 2 
че Сип 14065 T 
Радоша glabrum Виг- pis dag Wales, Aus- Brown 1900 NSW 0 SEM 46F © 
ы littorale Raddi Cutt Uc: € na- Schmid 1980-8 0 SEM 46А-С Some tetracolporate, = 
ica some tetrahedral tet- 24 
rads 
Psiloxylon mauritianum Gueho s.n. MAU 0 SEM 4SF Some tetracolporate 
Baill 14976 
Rhodamnia argentea New South Wales, Aus- Maiden & Boorman | NSW 0 SEM 48E 
Benth. tralia 
Temu divaricatum Berg chtien s.n. NSW 0 SEM 48A 
Thryptomene calycina J. Grampians, Victoria Beauglehole ACB NSW 0 SEM 44D 
. Black 28154 
Tristania conferta R. Cult. И шк; na- Schmid 1980-7 UC (3) SEM 41C,D 
Brow i li 
T. lactiflua F. Muell. Western teu Papua Henty & Foreman MO (3) SEM 41F 


2, 
S 
A 
z 
~ 
198 


ша 


а 


TABLE 1. Continued. 
Sub- 
sidiary 
Taxon Locality Collector Herbarium Colpi SEM-TEM Figure No. Remarks 
T. nereifolia R. Brown pd LS Wales Aus- Constable 5566 K 0 SEM 41E Triporate? 
Ugni molinae Turcz Ek DOUG; na- Schmid 1980-17 UC 0 SEM 46D, E Some di- or tetracol- 
tive, Central and porate 
South America 
ONAGRACEAE 
emen densiflora Washington, USA Piper s.n. MO 0 SEM S8B,E 
Wats 

B. deir (Lindl. ys Oregon, USA Thompson 5099 MO 0 SEM 58C 
B. desir (Lindl.) S. California, USA Abrams 6675 DS 0 TEM 63C 
B. ese Heller Oregon, USA Heller 12920 MO 0 TEM 63A-C 
B. stricta (A. Gray) Greene California, USA ones s.n. MO 0 SEM 58А 
Calylophus berlandieri Oklahoma, USA Towner 139 DS 0 TEM 61E, F 

Spach subsp. berlandieri 
C. toumeyi (Small) Towner Arizona, USA Towner 107 DS 0 ЗЕМ 55А-р 
Сатіѕѕопіа e (A. California, USA Parish & Parish 254 MO 0 SEM 57A, B 

Nels.) Rav 
C. arenaria ei Nels.) Ra- Arizona, USA Nelson 10140a MO 0 SEM, TEM 57D, F, 61A 
G: ен (Тогг.) Ra- Arroyo Malurino Moran & Reveal MO? 0 SEM 57H 

subsp. cedrosensis 19868 

(Greene) Raven 
C. robusta (Raven) Raven California, USA Gould 978 MO 0 SEM 57E, G 
C. tanacetifolia (Torr. & Cult. UC-Berkeley; na- UCB 69.1097 YC 0 SEM 576 

Gray) Raven subsp. tanace- tive, western МА 

tifolia 
Ci ircaea alpina L. subsp. China, Xizang (Tibet) Monbeig s.n. MO 0 SEM 50D 

moina з & Марп.) 
eges 
С. alae Royle Oslo, Norway MO 0 SEM 50C 


Cult. Missouri Bot. 
Gard. 


У coa Ese Жун ње давна 


898 


Nadav) 'TVOINV.LOS8 INNOSSIN JHL 30 STVNNV 


IL 10A] 


TABLE 1. Continued. $ 
Sub- 
sidiary 
Taxon Locality Collector Herbarium Colpi SEM-TEM Figure No. Remarks 

C. mollis Sieb. & Zucc. Kerita, Honshu, Japan Togasi 1797 MO 0 TEM 60D, F 
Clarkia breweri Greene California, USA Carter 1166 LA 0 TEM 62D 
C. speciosa Lewis & Lewis California, USA UCB 65.1421 Uc 0 SEM 52A,C 

subsp. speciosa 
C. unguiculata Lindl. Cult. UC-Berkeley; na- UCB 59.1244 UC 0 SEM 52B, D, F 

tive, western North 
America 

Epilobium collinum C. C. Sortavala, Finland Lindberg s.n. MO 0 TEM 63G - 

Gmelin > 
E. cylindricum D. Don. Gulmarg, Kashmir Stewart 10353 MO TEM 63F m 
E. glaberrimum Barbey California, USA MacMillan 14618 MO 0 SEM 59H 3 
E. hectorii Hausskn. New Zealand s. col. CH SEM 591 > 

202446 Д 

E. hirsutum L. Pyrenees, France Gautier 489863 DS 0 ТЕМ 63D,E 5 
E. brachycarpum Presl on, U Sheldon S11070 MO 0 SEM 59A-D E 
E. brachycarpum Presl California, USA Greene, 1876 MO 0 SEM 59Е-С Ы 
E. rigidum Hausskn. egon, U Kline M561 MO 0 SEM 591 e 
Fuchsia cylindracea Lindl. Todos Santos, Mexico Linderman 2030 MO 0 TEM 60A x 
F. garleppiana Kuntze & Dept. Cochábamba, Bo- Melhus & Goodman OKL 0 SEM 50B e 

Wittmark liva 3618 9 
F. thymifolia HBK. subsp. Michoacan, Mexico Waterfall 16474 OKL 0 SEM 50А m 

thymifolia م‎ 
Gaura calicola Raven & Texas, USA Henrickson 11334 Us 0 SEM 53A 

Greg. 
G. coccinea Pursh Texas, USA Reverchon 3844 0 TEM 62A, B 
G. demareei Raven & Arkansas, USA Demaree 62683 US 0 SEM 53D 

Greg. 
G. lindheimeri Engelm. & Cult. UC-Los Angeles: Raven, 1971 LA 0 SEM 52Е 

гау native, central USA 

G. mutabilis Cav. Chihuahua, Mexico Jones, 1903 DS 0 SEM 52G. H 
G. neomexicana Wooton New Mexico, USA Towner 109 US 0 SEM 34B. C 

subsp. neomexicana 
Gayophytum micranthum Prov. Coquimbo, Chile — Werdermann 200 MO 0 SEM 53F, H 

Hook, & Arn. 


698 


TABLE 1. Continued. 
oo 
u o 
sidiary 
Taxon Locality Collector Herbarium Colpi SEM-TEM Figure No. Remarks 
G. micranthum Hook. & Prov. Coquimbo, Chile Moore 216 LA 0 TEM 61D 
Arn. 
G. ramosissimum Torr. & Wyoming, USA Gooding 510 MO 0 SEM ЗЗЕ О I 
Gray 
Gongylocarpus fruitculosus Baja California, Mexico Moran 3529 DS 0 SEM 56Е 
(Benth.) Т. S. Brandegee 
subsp. glaber (J. Н 2 
Thomas) Carlquist & 
Raven 2 
G. rubricaulis Schlecht. & Mexico Davidse 9790 MO 0 ТЕМ 61G,H z 
am. = 
G. rubricaulis Schlecht. & Veracruz, Mexico Sharp 44846 MO 0 SEM 56D = 
Cham. - 
Hauya elegans DC. subsp. Chiapas, Mexico Breedlove 10229 MO 0 SEM 50G > 
barcenae (Hemsl.) 8 
Breedlove & Raven = 
Н. PM DC. subsp. ele- San Luis Potosi, Mexico Moran 13387 MO 0 SEM 50Е S 
е) 
— 
Н. ‘elegans DC. subsp. ele- Queretaro, Mexico Rzedowski 9294 DS 0 SEM 50F >, 
^ 
H. ЗӨ ens Donn. Sm. Chiapas, Mexico Breedlove 15653 DS 0 TEM 60C, E > 
Heterogaura heterandra California, USA Raven 20238 MO 0 SEM 54А-С © 
(Torr.) Cov. | 
Н. heterandra (Torr.) Cov. California, USA Bacigalupi 2341 DS 0 TEM 62C g 
Lopezia grandiflora Zucc. Jalisco, Mexico Breedlove 8066 DS 0 TEM 61B 2 
L. longifolia (Decne.) Plit- Morelos, Mexico Breedlove 8044 DS 0 SEM 510-6 
mann, Raven & Breed- 
love 
L. racemosa Cav. subsp. Jalisco, Mexico Breedlove 25800 CAS 0 SEM 51A-C 
racemosa 
Ludwigia alternifolia L. North Carolina, USA Peng 3738 MO 0 SEM 58F 
L. brevipes Eames South Carolina, USA Godfrey & Tryon MO о ТЕМ 60B 
1237 
Ramamoorthy 652 SEM 580, С Б 


L. goiasensis T. P. Rama- Brasilia, Brazil 


aeaiia is 


ан ы А Дејва Уа‏ ر 


1984] PATEL ET AL.—POLLEN CHARACTERS 871 


therefore, he recommends the term “subsidiary 
colpi" and we are in complete accord (Patel et 
al., 1983b). Subsidi 
ner ektexine than the surrounding | mesocolpial 
areas but in contrast to the colpi, all exine layers 
are usually represented. Frequently, the thinning 
of the ektexine is gradual and thus the subsidiary 
colpi often are not as clearly delimited as the 
colpi, although th d in thick- 
° ness just as in the colpi. Further, the surface 

sculpture in the subsidiary colpi is often different 
from that of the colpi. In the present study sub- 
sidiary colpi have been observed in Lythraceae, 
Combretaceae, Melastomataceae, Rhynchoca- 
lycaceae, Oliniaceae, Penaeaceae, and Cryptero- 
niaceae, cl the 
latter four families. Other families in which they 
have been observed are the Acanthaceae, Borag- 
inaceae, Hydrophyllaceae, Leguminosae, and 
Verbenaceae (Erdtman, 1971; Nowicke & Skvar- 
la, 1974; Faegri & Iversen, 1975; Ferguson » 
Skvarla, 1981, 1983; Raj, 1983). Sub у со 
are either equal to the number of colpi (= iso- 
merous) and alternating with them or there can 
be additional subsidiary colpi, as particularly 
noted in the Lythraceae. 

2. Intercolpar concavities. As originally de- 

ned by Wodehouse (1928: 453) for pollen in 
the Compositae tribe Mutisieae “These two 
species ... аге unique in the possession of three 


Remarks 


Figure No. 
62E 
56С, E 
SSE, Е 
62F 


SEM-TEM 
SEM,TEM 54D-F, 61C 


TEM 
SEM 
SEM 
TEM 


sidiary 


Sub- 
Herbarium Colpi 


MO 
MO 
MO 
MO 
M 

MO 


Collector 


Venturi 2873 


Anderson 5207 Cult. 
Stanford Univ. 

Breedlove s.n. 

Parnell s.n. 

Raven 26384 

Raven 26554 

Verity et al. 032 


one could make with the thumb i in a ball of soft 
dough. Since these impressions are between the 
furrows, I shall call them intercolpar concavities, 
and their position on the equator suggests = 


consider them to be structurally and Eun 
similar to subsidiary colpi, distinguished only in 
that they are markedly larger. In this study in- 
tercolpar concavities are found in some Melas- 
tomataceae, Penaeaceae, and Myrtaceae. They 
— also be present in Lythraceae as they appear 

be in light photomicrographs of Peplis portula 
sd Guers (1970). In Crypteronia large concavities 
in the mesocolpia have been considered by Mul- 
ler (1975) as pseudocolpoid depressions. Inter- 
colpar concavities have also been described in 
Calyceraceae (Skvarla et al., 1977) and, if our 
interpretations of Erdtman (1971) and Raj (1983) 
are correct, perhaps in Hoplestigmataceae, Ver- 
benaceae, and Olacaceae. Like subsidiary colpi, 
it will be of considerable interest to learn of their 

in other angiosperm groups. 


Locality 
Tucuman, Argentina 
Durango, Mexico 
Durango, Mexico 
Texas, USA 
Kansas, USA 
Kansas, USA 
Baja California, Mexico 


Continued. 


Taxon 
L. longifolia (DC.) Hara 
Smith & Rose subsp. 
wigginsii Munz 


(Nutt.) Heynh. 
S. linifolius (Nutt.) Heynh. 


Xylonagra arborea Donn. 


Gray 
О. таузшези Munz 


пе! 
Stenosiphon linifolius 


Oenothera brachycarpa A. 
О. texensis Raven & Par- 


Та 1. 


872 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Vo.. 71 | 


ас 


The 


‚ А, B. Nesaea : 
subsidiary COIP! 
s 5 


E dye RE Ls Scanning electron micrographs of Lythraceae subfam. Lythroideae pollen 
A. Lateral view i ane colpus with circular endoaperture (at center) and two su 

€. — B. Polar view. Each of the three colpi i bsidiary С irot ' 
Моје - : 1 pi alternates with two subsıdıa1) о elect 
Note that all of the nine mesocolpia are equal in size. Comparison should be made with the scanning di 
prs rograph of N. longipes (Graham, 1977, figs. 4—6) in which the three mesocolpia that are flanked by 5 430. 
colpi are ont £ Е ase tied Moe а 24397. 
co pı are prominent and larger than the remaining six mesocolpia. C-E. Heimia salicifolia C idi ry colpi 9f 


ae үнер. Polar view.—E. Surface detail. The three colpi have a granular surface. ien n wit y 

nisus di ч Pena cg yonmas of elongated, branched, often overlapping elements. i бн surfat 

: electron micrograph of Graham (1977. f 29) indi j ifferent sculptu Тк 
( 7, figs. 1-3) indicates a somewhat differ rrowh 5) 


1984] 


3. Heterocolpate. This term signifies the pres- 
ence of subsidiary colpi or intercolpar concavi- 
ties in addition to colpi and was originally de- 
fined by Faegri and Iversen (1950: 129) “Some 
furrows with, others without pores, free pores 
absent.” 


RESULTS AND DISCUSSION 
LYTHRACEAE 


Subfamily Lythroideae 


Dall Z5 1 " f 1 1 4 077 
р ( р у 
either three or six subsidiary colpi), radially sym- 
metrical, and isopolar. Great variability exists in 
shape, surface sculpture, aperture system, and to 
а lesser extent, exine structure. Apart from Ne- 
ѕаеа (Fig. ТА, B) and Ammannia (Fig. 2A, B) 
which are similar, each genus we examined has 
à distinct morphology and is described below. 
Ammannia: A. robusta (Fig. 2A, B) is hetero- 
colpate with six subsidiary colpi, subprolate in 
lateral view, circular in polar view. The surface 
5 striate. Colpi are long with obtuse ends and 
With a smooth, slightly granular surface. The en- 
doapertures are circular to slightly elliptic-lalon- 
gate. Subsidiary colpi are short with a slightly 
granular surface. 4mmannia coccinea, which also 
has a striate surface and six subsidiary colpi, was 
examined along with А. robusta in TEM (Fig. 
5A, B). The endexine is as thick or slightly thin- 
ner than the ektexine in the mesocolpial area. 
The foot layer is thick and often shows irregular 
o" near its lower margin, columellae are 
Me PR and simple and the tectum is very 
pes an imperforate. In cross section, the striae 
сш the tectum appear deeply grooved and 
nia и а! the base. In the colpal and subsid- 
sights am regions, the endexine is as thick or 
e ч icker than in mesocolpial regions and 
thin $i ayer appears to be continuous as a very 
i m. Near the endoaperture, the endexine 
granular and continues as a very thin layer 
Over the pore. 
ne ње С. surinamensis (Fig. IF) was exam- 
Rec with SEM. The pollen is spheroidal to 
ie: € in lateral view, while in polar view 
ightly collapsed grains are triangular with 


жо cou 


PATEL ET AL. —POLLEN CHARACTERS 


873 


meridional ridges f: ing obt corners. Pollen 
is heterocolpate with six subsidiary colpi, the me- 
socolpia between each pair of subsidiary colpi 
are wide and thick, forming three meridional 
ridges. Colpi are long and indistinct; subsidiary 
colpi are shorter than the colpi and also indis- 
tinct. Endoapertures are circular and raised. The 
surface is verrucate-rugulate. 

Cuphea: Both C. carthagenensis (Fig. 2C) and 
C. petiolata (Fig. 2D—F) are tricolporate-syncol- 
pate, oblate-suboblate in lateral view, triangular 
(sub-triangular to circular in C. petiolata) in po- 
lar view, and goniotreme (i.e., angulaperturate). 
In C. carthagenensis, the surface is psilate with 
meridional folds or ridges on the mesocolpia to- 
ward the pores. Colpi are very narrow and united 
at the poles. The pores are aspidote, like a cylin- 
drical extension, and open by a vertical splitting 
of the cylinder. In C. petiolata, the corners are 
obtuse, the surface is basically striate, but on the 
equator on each side of the colpus two elliptic 
areas are delineated in some grains. The size and 
the sculpture of these areas are highly variable 
and range from striate-spinulate to rugulate- 
striate in grains from the same collection. Colpi 
have a granular surface and the endoapertures 
are lalongate. 

Cuphea nitidula (Fig. 5D) and C. racemosa 
(Fig. 5C) were examined with TEM. The former 
is oblate-triangular with protruding pores (SEM 
not included here). It has a uniform endexine 
which is thickened at the base of the pores. The 
foot layer is thin, columellae are simple and ex- 
tremely short. The tectum is thin and tectal per- 
forations are rare. Tectal ridges are solid. The 
protruding pore (not illustrated in plate figures) 
has a thin granular endexine, a fragmented and 
thin foot layer, short columellae, and a very thin 


mellae are short, and the tectum is thin with 
some perforations. However, the endexine is very 
thick below the colpi and granular near the en- 
doapertures (not illustrated). 

iplusodon: D. villosus was examined with 
SEM and TEM (Figs. 3A, B, 6E). The tricolpoi- 


~ 


m : гах ; А 
*socolpium (open arrow) between the subsidiary colpi is wide and forms a meridional ridge. The exine surface 


is y 
7 па Slate. This pollen grain (see also 
Subsidiary co 


scanning electron micrograph of Muller, 1981, Pi. 1, figs. 1, 2) 
contrast to other grains with six subsidiary colpi (viz. Figs. 1A, B, 2A) in that adjacent colpi and 
lpi are not all equidistant. Scales equal 1 um. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


FIGURE 2. Scanning electron micrographs of oe bia subfam. Lythroideae polle en. A, B. Am 
ch c xine surface 15 
С. Cuphea 


ilate with large ridges (see transmission electron 
Те) пдот ly опе 


2: Late i view with ra 


up 
view showing syncolpate apertur of open 
crograph dc. pue iis of aê species O 


aperture > region. —E. Polar endoaperture а 
striate surface. See also transmission зар ті f Cup hea 


et al., 1968, figs. 4, 5, 8). Scales equal 1 


1984] 


dorate grains are subprolate in lateral view. En- 
doapertures are circular. The surface is verru- 
cate-rugulate with tightly packed verrucae as well 
as with elongated, convoluted rugulate elements. 
Colpi are very short and have large spherica 
elements on the surface. In section, the verru- 

late surf: ] pear to be com- 


E ж-а 


posed of a thick tectum which is supported by 
several thin columellae. A foot layer is absent. 
The endexine is thick and uniform, near the pore 
it increases in thickness and is granular. 

Heimia: H. salicifolia was examined with both 
SEM and TEM. Tricolporate pollen grains are 
spheroidal in lateral view and circular in polar 
view (Fig. 1C-E). The surface has irregularly 
shaped elements with overlapping fingerlike 
branches and irregular gaps between them (Fig. 
IE). Blunt spinules are also scattered on the sur- 
face. Colpi are long, with obtuse ends and a gran- 
ular surface. Endoapertures are lalongate. Thin 
section (Fig. 5G) shows a thick endexine, a foot 
layer which is either as thick as or thinner than 
the endexine, and simple or branched columellae 
which are erect and tall but becoming shorter 
toward the colpi. The lower margin of the tectum 
Is more or less straight while the upper margin 
's regular. Tectal perforations are numerous and 
often large. The endexine is very thick below the 
colpi; near the endoaperture, its lower margin is 
granular. The membrane over the endoaperture 
Consists of very thin granular endexine. The 
granules on the colpi surface (not illustrated in 
n figures) appear to be solid and constricted 
de base or rarely with fine columellae under 
ei L. punicifolia was examined with 
САЎ (Fig. 3D-F) and TEM (Figs. SE-F, 
Ne e tricolpoidorate grains are subprolate in 

view, and triangular-pl with ob 
‘use corners and straight sides in polar view. The 
ree protruding pores are situated midway be- 


nd ies elliptic, apertural fields (Muller, 1981). 
vends ace of the apertural fields is granular- 
тет te-rugulate; the surface of the ridges and 
o of the apertural fields near the apo- 

are rugulate but coarser than the rest of 
4pertural fields. The apocolpia have a psilate 


‚ the membrane over them is similar 


lo an : А 
d continuous with the surrounding area. In 


PATEL ET AL.—POLLEN CHARACTERS 


875 


TEM (Figs. 5E, F, 6A) the ektexine is thick in 
the ridge areas and thin in the apertural fields 
and at the poles. In the ridge areas, the foot layer 
is thick, with the upper margin often irregular or 
raised into domes, columellae are tall, erect and 
simple, and the tectum is thick, but discontin- 
uous due to the rugulate surface. In the apertural 
fields (Fig. 6A), the columellae are shorter, the 
foot layer is thinner, and the tectum irregular in 
thickness and discontinuous but with tightly 
packed verrucate units. The endexine in the ridge 
and aperture fields is thick and uniform (Figs. 
5E, 6A). At the poles (Figs. 5F, 6A) the entire 
exine is thinner. Here the endexine is very thin, 
and the foot layer and tectum are thicker than 
the endexine. The tectum is continuous and has 
a smooth upper margin and an irregular lower 
margin; the very short columellae are wider at 
their distal ends and appear to be finely branched 
Fig. 5 


g. 5 
Lagerstroemia: L. speciosa was examined only 
ith SEM. Tricolporate grains are subprolate in 


the mesocolpia, a poorly developed meridional 
ridge with two slightly depressed parallel areas 
on each side is discernible. Colpi are long with 
obtuse ends and a granular surface. Endoaper- 

ircul ith a slightly raised membrane 


2 


over them. 

Nesaea: N. schinzii was examined only with 
SEM (Fig. 1A, B). The tricolporate grains are 
heterocolpate with six subsidiary colpi. They are 
subprolate in lateral view and circular in polar 
view. The surface is striate. Colpi are long with 
acute ends and a granular surface. Subsidiary col- 
pi are shorter than the colpi and have a granular 
surface. 


Subfamily Punicoideae 


Punica protopunica and P. granatum, the only 
two species in the subfamily, were examined with 
SEM and TEM (Figs. 7, 8). The pollen is tricol- 
porate, radially symmetrical, isopolar, subpro- 
late in lateral view, and circular in polar view 
with slightly angular mesocolpia. In P. proto- 
punica the meridional ridges, polar caps, and 
ovoid apertural fields are weakly developed (Fig. 
7D). The surface of the polar caps is smooth- 
punctate with fine channels, that of the meridio- 
nal ridges is coarsely rugulate. In the apertural 


876 ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL 11 | 


fields, two faint subsidiary colpi with a rugulate row and discontinuous (Fig. 8A, B), although in 
surface (Fig. 7E) are present on the sides of each the polar caps of P. protopunica it is continuous | 
meridional ridge. In P. granatum only three (Fig. 8C). The columellae are very short, thick, 
weakly developed meridional ridges with rugu- and numerous. They are branched where theer | 
late surfaces were clearly observed in the center іпе is most thickened. The tectum is thick. The | 
of the mesocolpia (Fig. 7A). Exclusive of ridges, prominent endexine increases in thickness in the 
the surface is granular-rugulate (Fig. 7B). In both colpal regions and decreases at the polar caps. | 
species, colpi are long, with acute ends and with Near the endoapertures the endexine is granular. | 
a granular surface. Endoapertures appear to be — Punicoideae pollen is comparable to some Ly- 
circular to slightly oblong and lalongate. throideae although apertural fields, meridional , 
Thin sections show that the foot layer is nar- ridges and polar caps are not as well developed. | 


| 


25 


FiGURE 3. Scanning electron micrographs of Lythraceae subfam. Lythroideae pollen. A, B. Diplusodon | 
villosus.—A. Lateral view. The aperture system consists of a short colpus and circular endoaperture.—B. А | 


агго 
Muller (1981, Pl. 7, figs. 1, 2). Scales equal 1 um. l 
FIGURE 4. Scanning electron micrographs of pollen from Rhynchocalycaceae (A, C), Alzateaceae (B, D), and | 
Гу bfams. S tioideae (E) and Duabangoideae (F). A, C. RAynchocalyx lawsonioides.—A. | 
view.—C. Polar view. Subsidiary colpi appear to be united (i.e., they are *synpseudocolpate") (arrow) а | 


pole. See also scanning electron micrograph of Muller (1975, Pl. V, figs. 7-11). B, D. Alzatea verticillata.—B. | 


rugulate. The meridional rid 
polar caps and idional rid 
l um. 


the adjacent apertural fields. The endexine is well developed: under the meridional ridge it is nea y | 
thickness to the ektexine, toward the pores it bec lar as well as i ing in thickness. T section) | 
section is in contrast to Figure 6A which rer соп parallel to the polar axis (i.e., a longitu ted i? E 
and includes part of the polar cap and apertural field. These two different sectioning planes represen Iv) fo , 
and Figure 6A explain the disparity in respective endexine thicknesses. See also Muller qd | 


an А | 
; ; . i 
particularly the smooth, solid tectum, and the thick and branched columellae. The uniform salone of Mull 

| ection is directly comparable to the transmission electron micr kr | 
(1981, РІ. IX, fig. 3).—G. Heimia salicifolia (Graham 141). Section of a mesocolpium. Scales сла | 


2, 
| 
a 
ра 
< 
O 
4 
< 
= 
Z 
< 
~ 
Q 
& 
e 
к 
О 
un 
| 
> 
" 
L 
E 
i 
о 
n 
a 
< 
e 
Z 
< 


1984] 


PATEL ET AL.—POLLEN CHARACTERS 


879 


880 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 
Subfamily Sonneratioideae and the large, triangular polar caps have a psilate 
surface with a few punctae scattered over them. 

Sonnera tia lari. examined with SEM In a light microscope study, Muller (1969) de- 


(Fig. 4E, F). The pollen is triporate, radially sym- scribed the pollen morphology for five species 
metrical, and isopolar. Sonneratia grains are апа two interspecific hybrids of Sonneratia. Ma- 
prolate, cylindrical in lateral view, and triangu- јог conclusions from his study were: (1) that 5. 
lar-hexagonal in polar view, and three well-de- alba and S. caseolaris pollen showed great intra- 
veloped, meridional ridges alternating with three, specific variability that is geographically related 
oblong apertural (pore) fields are present. The and considered as genotypic, and (2) the domi- 
surface is verrucate in the apertural fields and nant pollen morphology of one parent of the two 
verrucate-rugulate on the ridges. Each apertural intraspecific hybrids suggested introgressive hy- 
field has a protruding pore at its center. Тһе sur- bridization. Later, pollen of S. alba and S. ca- 
face of the pore membrane is similar to that of — seolaris was examined by SEM and TEM (Mul- 
the surrounding field. In addition to the three ler, 1978a) in order to supplement the 
large ridges, six smaller ridges are present, two morphological data of earlier studies (Muller, 
in each apertural field. They are parallel to the 1969). Since our study did not include TEM ob- 
larger ridges and have a rugulate surface. The servations, the pollen ultrastructure of Sonnera- 
pore is located between the two smaller ridges, tia is summarized from Muller's work as follows: 


BENE 
a 


FiGURE 6. Transmission electron Rei cipis of pollen from Lythraceae subfam. rie (A, et р 
zateaceae (B, C), and Rhynchocalycaceae (D) Lafoénsia punicifolia. Section through th cap (left o 
) and apertural field. In the apertural T the verrucae (v) are composed of a quem D ‘and shot 


d than the ektexine. Toward the polar cap ia tis tectum is 
ier has a Гаје e posce теги below it. . The columellae are shorter and the foot layer is thicker 
apertural field. The endexine decreases in thickness from right to left (i.e., toward the polar сар. 63 


than in 
additional 
a portion of 
the mesocolpium. At the extreme right is the colpus. The foot layer is highly irregular and ori "pills (double 
arrow) and "valleys." The thickness and shape of the tectum be in direct correspondence with 
— ar the colpus, the tectum is thin, the co 

are short, and the foot layer is extremely thin. The endexine, goers is relatively thin in the mesocolpium, = 
5 thick i in the colpus .—C.A continuation c of the section in B to show the middle portion of ther men m 


tectum. The t layer is either absent or present only as thickened bases of columellae. The ; 


The section is near the end of a colpus or subsidiary colpus and includes portions of two m mesocolpia. 1-3).-E 
indicates — y the ir inner Lest margin of the tectum (see also Muller, 1975, Pl. УП, figs. 1— 
Diplusodon f the adjacent mesocolpia. The Y foot Шу 


FiGURE 7. Scanning oa micro; h f Lyth Hen A, B. Punica granatu 
( бан 7 5204 СА Lateral Hew А prap 50 yt гасеае subfam. Punicoideae pol “в он aru | 


surface of mesocolpia near a pe of a colpus. C-G. Punica protopunica.—C. Scanning electron mi ules belo" 
a fractured exine near the pole. Note the inner surface which is smooth toward the pole. The ge present: 07 


distinct.—E. Lateral view г the rugulate surface of the ridge (center) лак the pe colpi.— 
e. Scale 


Ficu Transmission electron micro —A. Punic 
graphs of Lythraceae subfam. писа pollen. section 
natum (Grant 15704). Transverse section of a a mesocolpium. B, C. Punica protopunica.—B. Transverst ө 
"d a mesocolpium. Note the **white line" separating the discontinuous foot layer 4 the ирет € ae 
2 pen pore. Note the thinning of the endexine at les ( 
contrast to other areas, the foot layer at the poles is thick and continuous. Scales equal 1 si 


————————— РОНЕ 


1984] 


PATEL ET AL.—POLLEN CHARACTERS 


у 7e 


pU. *“ Ф ذ‎ 


Retry 


1984] 


PATEL ET AL.—POLLEN CHARACTERS 


884 


the endexine is thin on the polar caps and thick 
in the equatorial zone. It is granular around the 
pores. The sole (= foot layer) on the other hand, 
is thick on the polar caps and thinner in the 
equatorial zone. In the porate fields of the equa- 
torial zone, short columellae connect the ver- 
rucae to the sole. In the meridional ridge areas 
in S. alba, the columellae are longer and rather 
widely spaced, and support a tectum. At the polar 
caps, distinct columellae grade into areolate pro- 
trusions of the sole. The tectum is continuous on 
the polar caps, partially broken on the ridges (in 
S. alba) and occurs as separate verrucae over the 
porate fields. A granulate layer completely or 
partially fills the infractectal cavities. Muller em- 
phasized that in S. alba well formed meridional 
ridges united with polar caps which markedly 
delineated apertural or porate fields, while in some 
grains of S. caseolaris the lack of meridional ridges 
did not confine the pores to fields, and in other 
grains, indistinct meridional ridges were found. 
The conclusion was that pollen of 5. alba was 
more advanced in “. . . controlled harmomega- 
thy than that of S. caseolaris and it is significant 
in this connection that the latter species has been 
proven to be phylogenetically older” (Muller, 
1978a: 287-289). 

Recognizing the taxonomic problems associ- 
ated with distinguishing pollen of S. caseolaris 
from S. alba (Muller, 1969, 1978a), our SEM 
results show that at least superficially, S. caseo- 
laris (Fig. 4E) appears more similar to Muller’s 
SEM of S. alba (Muller, 1978a, PI. II, fig. 1, 1981, 
Pl. VI, fig. 2) than to his SEM of S. caseolaris 
(Muller, 1978a, Pl. 1, figs. 1, 2, 1981, Pl. VII, fig. 
3). The similarity is seen in the well-developed 
meridional ridges and apertural fields in our 5. 
caseolaris and Muller's S. alba. 


Subfamily Duabangoideae 


Duabanga molucanna was examined with SEM 
(Fig. 4F). The pollen is triporate, radially sym- 
metrical, and isopolar, and the shape is subpro- 
late, elliptic in lateral view, and triangular-hex- 
agonal in polar view. As in Sonneratia, three 
well-developed, meridional ridges alternating 
with three, obl 1( ) field 


ent, although the ridges are less pronounced in 
Duabanga. The surface is verrucate in the aper- 
tural fields and verrucate-rugulate on the ridges. 
Each apertural field has a protruding pore at its 
center. The surface of the pore membrane is sim- 
ilar to that of the surrounding field. The large, 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


triangular polar caps have a psilate surface with 
a few punctae scattered over them. 


Discussion 

This report is in agreement with others which 
indicate that Lythraceae have the most diverse 
pollen morphology of the Myrtales. Much of this 
diversity centers on the apertural systems, for 
example, tricolporate grains are documented in 
Physocalymma (Cos Campos, 1964), Pemphis, 
Rotala (Guers, 1970), Heimia (Graham, 1977), 
Adenaria, Pleurophora, Galpinia, Woodfordia 
(Erdtman, 1971), and Diplusodon (Muller, 1981) 
heterocolpate grains with isomerous subsidiary 
colpi are present in Lythrum (Cos Campos, 1964; 
Guers, 1970; Heusser, 1971), Rotala (Guers, 
1970), and Peplis (Heusser, 1971); grains with 
six subsidiary colpi occur in Nesaea, Ammannia 
(Erdtman, 1971; Cos Campos, 1964; Guers, 1970; 
Graham, 1977; Lobreau et al., 1969), Crenea 
(Erdtman, 1971; Muller, 1981), and Lawson 
(Muller, 1981), and grains with three meridional 
ridges that alternate with apertural fields are 
present in Lafoénsia, Crenea, and Lagerstroemia 


phology with pollen ranging from bast : 
porate-spheroidal to tricolporate-syncolpate-o 

late triangular (Erdtman, 1971; Cos Campo 
1964; Graham et al., 1968; Graham & Gram 
1971; Guers, 1970. Graham et al. (1968) је 
amined the pollen of 153 species of Сирћеа 1 


: 4 1 ong |— 
order to determine the extent of diversity amo 


species as well as the potential use of pollen ! 
the systematics of the genus. Starting W1 n 
oblate, tricolporate, striate, tectate grain, Сир! 

was shown to be remarkably eurypalynou pedi 
great variation at sectional, subsectional, a a 
ic, and varietal levels. Twelve morpholog! sub- 
egories representing eight sections and nine p 
sections were established. Of particular COn ti 

was the great number of pollen types ier 
bud clusters, buds, and individual anthers 2 је 
len of C. crassiflora, С. koehneana, and с the 
rullensis. These authors felt it was crucial mine 
interpretation of the pollen data to ge het- 
whether the pollen polymorphism — th se 


| 


| 


th a basic | 


ifa «i ic pollen type 
erostyly or if a single basic po discussed by | 


eral variations was produced. As pr 
them (Graham et al., 1968: 1087-1088): 


The term “polymorphisme” has bee? 


ww www ww 


| 


|| 


1984] 


to describe the multiple pollen types produced 
by individual plants or anthers in Cuphea (Cos 
Campos, 1964), but in our opinion use of the 
term has been preempted by a different situ- 
ation existing in certain species of Primula, 
Lythrum, and other genera. As early as 1841, 
Vaucher noted three floral forms in Lythrum, 
and Darwin (1865) made a study of trimor- 
phism in L. salicaria L. According to S. Gra- 
ham (1964), ‘In this species there are three 
style lengths and three sets of stamens of lengths 
corresponding to those of the styles. The forms 
are termed long-, mid-, or short-styled, de- 
pending on whether the style exceeds, lies be- 
tween, or is shorter than the two whorls of 
Stamens. Pollen differs in color, size and 
amount of stored starch in each of the three 
stamen lengths. The longest stamens have the 
largest grains, the anthers are green, and the 
pollen is filled with starch. The two shorter 
stamen lengths have yellow anthers and cor- 
respondingly smaller pollen containing less 
starch.” Thus Lythrum salicaria produces three 
morphologically distinct kinds of pollen and 
each is consistently associated with another 
feature of floral structure, viz., stamen length. 
In Cuphea the multiplicity of pollen types is 
greater (up to 12 in C. strigulosa, fide Cos 
Campos, 1964, p. 332), occurs within a single 
anther, and is not correlated with any other 
feature of the plant. 


би in order to determine the nature of 
isi: tiple pollen types in Сирћеа, size studies 
od e Rer lactic acid preparations were con- 
= ( гаћат et al., 1968). The statistical data 

ег definitively gave support to the idea of 


n her 
“= Pollen variations rather than to hetero- 
у 


We comprehensive light microscope study 
VU 979) included 26 genera and 62 species 
cathe e pollen. Great emphasis was placed 
is. umber of subsidiary colpi and three major 
Pi 8roups were established: (1) three-pseu- 
ma run Pemphis, Peplis, Physoca- 
(ий CA: (2) sin-paeudoeolpate 
tia, 
man 08, and (3) non-pseudocolpate (Ad- 
ip ii zatea, С uphea, Decodon, Didiplis, 
sia Pen Galpinia, Grislea, Heimia, Lafoén- 
“= ga Based on number of subsidiary colpi 
(L Y did not support the tribal classification 
Faceae (Koehne, 1903) into Lythreae and 


PATEL ET AL. — POLLEN CHARACTERS 


885 


Nesaeae and their respective subdivisions. All 
had a mixture of the above three pollen groups. 
It was also concluded that, based on its non- 
subsidiary colpate pollen, A/zatea, which was 
originally placed near to Physocalymma and Di- 
plusodon (Lourteig, 1965), is better assigned near 
to Grislea or Adenaria. Also, the placement of 
Rhynchocalyx near Lawsonia (Sprague & Met- 
calfe, 1937) was disputed on the basis of three 
subsidiary colpi and indistinct pores in the for- 
mer and six subsidiary colpi and distinct pores 
in the latter. Both A/zatea (Graham, 1984) and 
Rhynchocalyx (Johnson & Briggs, 1984) are now 
regarded as separate monotypic families. 

In the most recent study of Lythraceae, pollen 
of Crenea, Diplusodon, Lafoénsia, and Lager- 
stroemia, as well as Sonneratia (subfam. Son- 
neratioideae), were compared from a harmome- 
gathic functional standpoint, and several 
structural pollen types were established (Muller, 
1981). Starting with a tricolporate, longiax pro- 
totype, Muller (1981) postulated that the rela- 
tionship between pollen form and function was 
indicative of adaptive radiation in the following 
directions or series: (1) in the first series there is 
a trend toward increasing the number of colpi 
(i.e., subsidiary colpi), (2) in the second series 
harmomegathic functions are transferred from 
individual colpi to flexible apertural fields alter- 
nating with meridional ridges, (3) in the third 
series harmomegathic functioning is transferred 
to prominent pores, and (4) in the last series 
harmomegathic functioning is lost in the ecto- 
and endoapertures. 

The usefulness of pollen morphology in the 
taxonomy of Lythraceae is summarized by Mul- 
ler (1981: 121-122) whereby he emphasizes the 
need: 


. . . for ecologic interpretations of function 
and for detailed ultrastructural studies to un- 
cover those characters which reflect ancient 
phylogenetic links. This can perhaps best be 
illustrated by a discussion of possible affinities 
between the genera Lafoénsia, Lagerstroemia, 
and Sonneratia, assuming that it is decided to 
place the latter in the Lythraceae. If conver- 


Lafoénsia would be considered closely related, 
but the differences in ultrastructure and the 
heterocolpate nature in some pollen types of 
this genus would argue against affinity with 
Sonneratia. If fossil evidence is taken into ac- 
count, the genus Lagerstroemia appears a much 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


FIGURE 9. icum electron ови рака of Trapaceae pollen. A-F. Trapa natans.—A. (Eng 
ridges. The у vertically cracked area of the dome; in the pam 


e cole ae DE s.n.). Polar view. The um АЕ 


three protruding domes (arro 


meridional ridges, which in turn, are united at the pole. — C. (House 21708). та view of the area pe 


two meridional ridges. Note that the ridges are continu two-part natur 


ous over the domed areas. The 


mann $” 


1984] 


stronger candidate, although its present-day 
types show less similarity with living Sonnera- 
tia types, having diverged rather strongly from 
a postulated common ancestral matrix, al- 
though the peculiar granular deposits in the 
intercolumellar space appear to be present both 
in Lagerstroemia and Sonneratia. 


In a more general sense and concerning the 
taxa examined in this study (Table 1), Lafoénsia 
is similar to Sonneratia of subfam. Sonneratioi- 
deae (Muller, 1969, 1978a, 1981, Fig. 4E); Di- 
plusodonis similar to Duabanga of subfam. Dua- 
bangoideae (Muller, 1981; Fig. 4F); and 
Lagerstroemia bears resemblance to Punica 
(subfam. Punicoideae, Fig. 7D, F). These simi- 
larities strongly support the view of Dahlgren and 
Thorne (1984) that Sonneratia, Duabanga, and 
Punica should be regarded as separate subfam- 
ilies independently related to Lythraceae. 


TRAPACEAE 


Trapa Japonica and T. natans were examined 
with SEM and TEM. Pollen from both species 
are basically similar. They are tricolpate, radially 
symmetrical, isopolar, spheroidal in lateral view; 
and triangular, goniotreme with obtuse corners, 
and straight to convex sides in the polar view 
(Figs. 9, 10). There are three meridional ridges 
9n the grains. The surface is granular. The three 
apertures are protruding and swollen as elongat- 
ed domes. In Т. japonica these domes are better 
developed than in 7. natans. Within them there 
is an elongated lens-shaped opening or colpus 
(Erdtman, 1943: 104-105, figs. 221-223) which 
is not Visible in scanning electron micrographs 
a it is covered by the meridional ridge. The 
meridional ridges are formed by the folding of 
P. ektexine and they are united at both poles 

ere their fused triangular base is greatly en- 
larged (Figs, 9p, 10B). The ridges are taller at the 
ae they extend toward the equator in a 
undulating manner their height de- 

ie The surface at the upper portion of the 

&* near the poles is smooth with many chan- 


в 


PATEL ET AL.—POLLEN CHARACTERS 


887 


nels. The lower portion shows a granular-ver- 
rucate surface (Fig. 9C). Toward the equator, the 
upper portion of the ridge is more rugulate-ver- 
rucate. Over the colpi, the upper portion of the 
ridge continues as a wide and not very tall, ver- 
rucate-granular band. The lower portion spreads 
over the swollen domes and is continuous with 
the surrounding interapertural areas (Fig. 10C— 
E). The surface of the domes is granular like that 
on the mesocolpia. It is not clear how the colpi 
open, but they appear to do so m an irregular 
splitting of the exine (Figs. 9A, 10D, F). 

One sample of Trapa natans LH ose 21708) 
showed clumps of grains (polyads?) along with 
free monad grains. Exinous connections between 
the members of these **polyads" are present (Fig. 
90-Р). However, there is no discernible specific 
arrangement of the polyad members, and the 
bridges connect different parts of the adjacent 
grains. This phenomenon is not yet clearly 
understood. 

In 7. natans the fine, granular surface of the 
grain is due to the tightly packed clavate and 
rod-shaped elements that form a very thin layer 
as seen in the thin sections (Fig. 11 A-C). These 
clavae are either solid in their entire length, or 
show a fine, fuzzy granular layer below them. 
The exine structure of 7. japonica (Fig. 11D) is 

similar to 7. natans but the fuzzy layer is not 
evident. When cut obliquely, the clavate layer 
appears to be beaded and spongy. The thick, more 
or less solid layer below the fuzzy layer appears 
to be the endexine which becomes granular near 
the pores. The foot layer is difficult to recognize 
but it is perhaps present as a very thin layer 
between the fuzzy layer and the solid endexine. 
On the granular е near the pores, such a 
layer is clearly visi 

Sections passing na the ridge show that 
it encloses a cavity (star in Fig. 11A). The clavate 
layer (CL in Fig. 11A), along with the fuzzy gran- 
ular layer (G in Fig. 11A), lifts to form the ridge 
wall. It continues as such for a short distance 
(i.e., the granular lower portion of the ridge as 
seen from the outside and designated by a solid 


~ 


es.—F. UH 


use 21 708). Extexinous bridges 


mee i I$ indicated by the stars: the open edis shows the upper part which is highly folded, the solid star sat 


us fused gra ns 


Pollen oy Аеш: hi ae лет a bridge connecting the "вон ма tas of two seri grains. и 


equal | 


888 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


star in Fig. 9C) and then becomes а more or less ognized by Erdtman (1971), who examined three 
discontinuous, solid layer (the psilate upper por- species and felt that the genus merited family 
tion of the ridge seen from the outside, the open status. Trapa pollen shows a distant resemblance 
star in Fig. 9C). The inner margin of this solid to Onagraceae pollen in surface sculpture and in 
layer is highly irregular. Clavae at the base ofthe the nature of the protruding apertures (see Figs. 
ridge cavity are large and often appear to be 50-53 of Onagraceae pollen below). Similarities 
branched. Just above these clavae, the cavity is to Onagraceae are further evident in the very 
filled with circular or elongate ektexinous ele- thick endexine and indistinguishable, or at least, 
ments. very thin, foot layer (compare Figs. 11 and 60- 
63). 


Discussion 


Structurally, the meridional ridge of 7 rapa is CONIA 


different from that found elsewhere in the order. _ Olinia emarginata, О. radiata, О. rochetiana, 
It is formed by the uplifting and folding of the О. vanguerioides, and О. ventosa, which com- 
ektexine and encloses a cavity. In contrast, the prise all species of the family, were examined 
ridge found in Lythraceae (Lagerstroemia, see with SEM and TEM. Pollen from all of the species 
also van Campo, 1966; and Punica) and Ona- is remarkably similar, both at the exomorpho- 
graceae (Ludwigia) is formed by the increased logical and the endomorphological levels. 


thickness ofthe exine. Moreover, the ridge passes Pollen is tricolporate, radially symmetrical, 
over the colpi in Trapa, whereas it alternates ovoidal to subovoidal in lateral view (Muller, 
with the colpi in the other groups. 1978b) and circular to triangular in polar view 


The distinctiveness of Trapa pollen was rec- (Figs. 12, 13). It is heteropolar because the plane 


2 А O 
— 


FIGURE 10. Scanning electron micrographs of Trapaceae pollen. A-D. Trapa japonica.— A. Lateral view ч 
a domed area (arrow) and a meridional ridge that passes over it (in this grain the ridge is discontinuous и“ 
equator). The maximum height of the ridge is at the poles. An elongated lens-shaped colpus is enclosed wi 


Close-up of domed area (arrow) which is less prominent than in T. japonica (see А, С, | д доте 
of verrucate, granular elements. — Е. (Engelmann s.n.). View showing irregular splitting of the ridge in the 
area. Scales equal 1 um. 


FIGURE 1 1. Transmission electron micrographs of Trapaceae pollen. A-C. Trapa natans.—A. (En ridge 
5.n.). Section of the meridional ridge with cavity (star) and surroundin The upper portion of the ~“ 


(within hracket) 


granular layer (arrow).—C. (House 21708). Two sections of the mesocolpium. The ektexine is thin e 
of tightly packed clavae with a fuzzy basal layer (arrowhead). The foot layer cannot be readily dis jum. 
and the endexine is thick (significantly thicker than the ektexine).—D. Trapa japonica. Section ofa m€ if апу, 
In all transmission electron micrograph preparations of T; rapa pollen, i : :< exine laye" 
diflerence in electron density from the ektexine. Studies with fresh pollen should help to clarify this exine 
as well as the presence or absence of the foot layer. Scales equal 1 um. 
FIGURE 12. Scanning electron micrographs of Oliniaceae pollen. A-C. Olinia radiata. — А. Polar view segment 
the polar face without subsidiary colpi.—B. Lateral view. The colpus is asymmetrical with the long tending 
extending into the polar face that lacks subsidiary colpi (lower half in this figure) and the short segment јр 
into the polar face that has the subsidiary colpi (a subsidiary colpus is indicated between arrows). rie three 
-— "Pera m ane.— C. Polar view showing the polar face tn 990)-— : 
subsidiary colpi alternating with the short segments of the colpi. D-F. Olinia rochetiana (Chapman Ірі with û 
rugulate-granular surface alternate with short segments of і. iew of the polar face 
not have subsidiary colpi. Scales equal | um. ne cM dis 


| 


m 


i 


| 


partially visible subsidiary colpus.—E. Polar view. Subsidiary СО that does 


PATEL ET AL.—POLLEN CHARACTERS 


ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL. 71 | 


ји رد‎ kde Pu ы 


Tw 


PATEL ET AL.—POLLEN CHARACTERS 891 


1984] 


892 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


that is perpendicular to the polar axis and situ- do not extend into both polar faces of the grain. 
ated at the greatest width of the grain divides it They are present on the polar face that has the 
into two unequal polar faces. This is referred to short segments of the colpi. Their surface is ru- 
as the modal plane (Muller, 1978b). The surface gulate, with irregular, branched channels (Figs. 
is usually psilate, or rarely psilate-punctate as in 12C-E, 13A, р-Б). They are often wide and 
O. radiata (Fig. 12B, C). therefore tend to resemble intercolpar concavi- 
The aperture system in Olinia is unusual in ties. This type of aperture system can also ас- 
that the pollen grains have asymmetrical colpi count for the grains being heteropolar. However, 
and half subsidiary colpi (Patel et al., 1983b). іп some grains a size difference between the two 
Each colpus consists of a long segment and a polar faces is not evident and such grains are 
short segment. Thelongsegmentsareonthelarg-  spheroidal in lateral view. Rarely, the subsidiary 
er polar face of the grain (Fig. 12A, F) and they colpi extend slightly beyond the equator into the 
are slightly wider than the short segments (Fig. opposite polar face. 
13A, F). The surface of the colpi is smooth or The ektexine in the mesocolpia consists of à 
ular and the ends are acute. An elliptic, la- very thick foot layer (Fig. 14) which becomes 
longate endoaperture is present on the modal extremely thick toward the colpi (Fig. 14D, E). 
plane where the t gments ofthe colp t rom the foot layer arise the thick and short, 
The endoapertures are covered by extensions of often prostrate or irregular-mound-like colu- 
the mesocolpia. mellae which are usually narrower at their distal 
The second unusual character of Olinia pollen ends where they form an infratectal granular lay- 
is the presence of three half subsidiary colpi which ег (Fig. 14C). The tectum is thick, uniform and 


een emer 
- 


polar face. The upper polar face has the long segment (L) of the colpus and no subsidiary col Su i 
view showing the polar face that lacks subsidiary colpi. The long segments of the three colpi are visible (arro 
heads) tails of part of the colpus of A.—D. Details of a subsidiary colpus showing te 


exine surface with irregularly branched channels. E, F. Olinia ventosa.—E. View of a subsidiary colpus with а 
rugulate surface.—F. Lateral view showing two subsidiary colpi, asymmetrical colpus, and psilate ехше surface. 
Scales equal 1 um. 


FIGURE 14. Transmission electron micrographs of Oliniaceae pollen.— A. Olinia rochetiana (Cr ~ 

Section of a subsidiary colpus. The rugulate surface elements described in scanning electron micrograP дё 

12Е) appear in transmission elect : grapl dome-shaped tect below which is an infratect 

layer. Columellae are absent and the foot layer (arrowhead) is narrow but consistent over the subsidi 
BC ne : 


ary colpus 
um 


FIGURE 15. Scanning electron micrographs of Combretaceae pollen. A-C. Combretum cacoucia. A Pg 
view showing three colpi with extensions of mesocolpia over the endoapertures and three subsidiary COP... 
Lateral view. The endoaperture appears as a wide elliptic shadow. The colpus membrane 15 #1 The exin? 
surface consists of echinate plate-like areas that are delimited by channels and punctae. The colpus wr ud: 

ver the endoaperture (arrow).—E. Subpolar view showing three apertures and three орну E 

с | three subsidiary colpi are wide and appear to be more like 10%? 5 pith 
concavities.—G. Calycopteris floribunda. Sublateral view showing a subsidiary colpus (center) an 
colpi. The exine surface is rugulate. Scales equal 1 um. 


ааа анана АШ‏ و gg‏ س 


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ANNALS OF THE MISSOURI BOTANICAL GARDEN 


ГАА. 


[Уо1. 71 


un 
24 
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1984] 


without perforations (except in O. radiata). The 
upper margin of the tectum is smooth. The end- 
exine is thin but becomes markedly thickened in 
the colpi and subsidiary colpi regions. The sub- 
sidiary colpi show a thinner, undulating, often 

ome-shaped tectum (Fig. 14A). The infratectal 
granular layer is continuous here. The columellae 
appear as short connections between it and the 
very thin, discontinuous foot layer. 

In the area of the endoapertures (Fig. 14D, E), 
the endexine is granular. The extensions of the 
mesocolpia show a disrupted thin foot layer, and 
a thin infractectal granular layer below a slightly 
thinner tectum. 


Discussion 


Oliniaceae pollen grains differ from all other 
groups in their unusual aperture system, i.e., the 
asymmetrical colpi and the half subsidiary colpi 
(Patel et al., 1983b). All species examined are very 
similar in exo- and endomorphology and are dif- 
ficut or impossible to distinguish. Erdtman 
(1971) reported three subsidiary colpi in O. cy- 
mosa (= O. ventosa) and that subsidiary colpi 
were absent in O. volkensii (= O. rochetiana). 
Samples of O. rochetiana examined in this study 
show half subsidiary colpi and asymmetric colpi, 
similar to the other species of Olinia. Since half 
subsidiary colpi occupy small areas on only one 
polar face and differ only slightly in surface sculp- 
turing from the surrounding exine, it is not sur- 
prising that their true nature is difficult to reveal 
ee the light microscope. However, in the light 
(197, сые of O. rochetiana by Archangelsky 

l, fig. 1, PI. 20), three half subsidiary colpi 
are clearly visible. 


— e 


PATEL ET AL.—POLLEN CHARACTERS 


897 


very thick foot layer and tectum, and a thin col- 
umellae layer with an infratectal granular layer 
extending over the subsidiary colpi (compare Fig. 
14 to Fig. 26). 


COMBRETACEAE 


Pollen is tricolporate (rarely tetracolporate in 
Quisqualis parviflora and Terminalia oblonga), 
mostly heterocolpate (except in Buchenavia, La- 
guncularia, and Strephonema), radially sym- 
metrical, and isopolar. The shape of the grains 
is spheroidal to subprolate in lateral view and 
circular to hexagonal in polar view. In the het- 
erocolpate species, the colpi are long, with acute 
ends, and with a granular surface. Syncolpate 
grains are present in Combretum farinosum (Fig. 
16D) and in T. oblonga (Fig. 16A) where the 
syncolpus is undulating like the line on a tennis 
ball. Endoapertures are lalongate and elliptic in 
Combretum cacoucia (Fig. 15B), C. laxum (Fig. 
16E), and Lumnitzera racemosa (Fig. 19D), cir- 
cular in Poivrea coccinea (Fig. 19C) and Ano- 
geissus acuminata (Fig. 18D), and circular to el- 
liptic in Bucida macrostachya (Fig. 17A), C. 
farinosum (Fig. 16D), Q. parviflora (Fig. 16H), 
and 7. oblonga (Fig. 16A, С). Subsidiary colpi 
are wide and often united at the poles in Ra- 
matuella argentea (Fig. 17E), Terminalia catap- 
pa, T. oblonga (Fig. 16A), and Guiera senegal- 
ensis (Fig. 18E). 

Diverse surface sculpture patterns are present 
in the family. The surface is striate in Combre- 
tum laxum, Guiera, and Poivrea. In C. laxum 
(Fig. 16E, G), thick striae are separated by short, 
punctate channels while the surface of the sub- 
sidiary colpi is striate-rugulate. In Guiera (Fig. 
18E), small groups of short striae cross, and the 
subsidiary colpi appear to have a finer, granular, 
striate surface. Poivrea (Fig. 19C) shows bands 
of fine, long striae while the subsidiary colpi are 
striate-rugulate. 


— 


F : CEN 
..'GURE 16. Scanning electron micrographs of Combretaceae pollen. A-C. Terminalia oblonga. — A. Lateral 


View of 


à tetracolporate, syncolpate grain. The subsi 


diary colpi are also united. Note that the two visible 


ures (arrows) are situated at two different horizontal planes of the grain.— B. Finely — Ma 
х de à 


in 
Mes, bsi colpus.—C. Lateral view of a tric 
G. porate, syncolpate grain. E, С. Combretum 1 
па тешт t 


half). The rugulate-punctate surface becomes finer 
m 


Bain » 4 | 
n. Compare with Figure 23B. Unless otherwise indicated, scales equal 1 um. 


898 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Уо 71 


Кыз. : 2 a electron петак of Combretaceae pollen.—A. Bucida macion Lateral i pial 
penis: Р center) and two subsidiary colpi.—B. Conocarpus erecta. Polar У m with’ 
> ons Over the apertures. Also note three subsidia lpi.— teleopsis e 4 ew 
colpus (at center) and two subsidiary colpi.—D. Terminalia edulis (Quisumbin ( Lateral vie" н 
colpus (at center) and two subsidiary colpi. E, G. R tuella argente ч view with а sub уой 
си colpi two colpi.— urface detail of a ru ulate subsidiary —F. Terminalia саіарр . the 
esocolpium near colpus иза T (triangle). Elongate, rE interwoven element ts form 


PATEL ET AL.—POLLEN CHARACTERS 


<i ФРУ ш 
pei [у 
Wye жы 


aM 


uut st 
к. к 


„Кои ЖЕ 18. даш, electron micrographs of + pollen. A-C. Buchenavia suaveolens. — A. Polar 


narrow (subsidiary colpi are absent) and the surface is echinate. — B. Lateral view.— C. Details 
PT surface. Note similar surface in T. inundata (Fig. 1 5E). D, Е. Anogeissus acuminata. — 
a wide and кл, келат colpus (at center). Two colpi are also Armaan The 
is ей LF. Polar view showing colpi alternating with subsidiary colpi. — E era ote ppi 
view with a colpus at center and PN вену colpi. The exine surface is striate. Scales equal 1 р 


p 


1984] 


In Combretum trifolium (Fig. 16F), Quisqualis 
indica (Fig. 15F), Ramatuella (Fig. 17E, G), Ter- 
minalia edulis (Fig. 17D), and 7. catappa (Fig. 
17F) narrow, elongated, and branched muri ap- 
pear tightly interwoven. Punctae are present in 
the channels separating the muri. The pattern is 
finer at the margins of the mesocolpia and less 
so at the poles where it appears to be punctate 
in Q. indica. The surface of the subsidiary colpi 
is rugulate-granular in Ramatuella (Fig. 17G), 
and C. trifolium. In О. indica (Fig. 15F), the 
subsidiary colpi are wider than in the other taxa 
examined and their surface appears to be similar 
to the surface on the meso- and apocolpia. In О. 
parviflora the surface is psilate (Fig. 16H, 1). 

In Combretum farinosum, Bucida (Fig. 17A), 
Pteleopsis myrtifolia (Fig. 17C), and Conocarpus 
erecta (Fig. 17B), the surface is more or less 
smooth to finely rugulate with punctae and short 
channels that are more pronounced at the mar- 
gins of mesocolpia. In Combretum cacoucia (Fig. 
|БА-С) and Terminalia oblonga (Fig. 16A-C) 
the surface is finely rugulate. The subsidiary colpi 
in С. farinosum, С. cacoucia, Bucida, T. oblon- 
84, and Conocarpus show a coarse, granular-ver- 
rucate surface. 
| a rugulate surface is present in Lumnitzera 
di ue (Fig. 19D) and Calycopteris floribunda 
i: 50). In Lumnitzera the surface of the sub- 
Сы | colpi appears to be granular, whereas in 
a Кз а It 15 rugulate-verrucate with slightly 
m *r rugulate elements than on the mesocol- 


е acuminata (Fig. 180, Е) and Thiola 
э а (Fig. 15D, E) have an echinate surface 
zl Pinules. In Anogeissus, scattered spinules 
"мы оп a smooth surface. They become 
the = and more numerous at the margins of 
idi €socolpia. They are also present on the sub- 
lary colpus and the colpus membrane over 
"эми ОО In Thiola, in addition to the 
tels tha » Mere are large punctae and deep chan- 
talso have punctae. Due to the channels, 

fu Mrs appears to consist of more or less 
Plates or islands" (Fig. 15D). The surface 


in 


тз BM OO 


PATEL ET AL.—POLLEN CHARACTERS 


901 


of the subsidiary colpi also has spinules and 
punctae. Longer spinules are present on the col- 

pus membrane over the endoapertures. 
Buchenavia suaveolens, Laguncularia race- 
mosa, and Strephonema pseudocola are without 
subsidiary colpi. In Buchenavia (Fig. 18A-C), 
grains are spheroidal in lateral view and trian- 
gular in polar view. The surface is echinate, like 
that in Thiola, with spinules, punctae, and deep 
channels forming "plates." Colpi are long and 
narrow. Endoapertures are lalongate. In Lagun- 
cularia (Fig. 19E, F), grains are subprolate in 
lateral view and circular to triangular in polar 
view. The surface is smooth with minute punc- 
tae. Colpi are medium length and have a granular 
surface f lpi p tove 
the lalongate endoapertures. Strephonema (Fig. 
19A, B) is subprolate in lateral view and circular 
to triangular in polar view. The surface is retic- 
ulate with large lumina which gradually decrease 
in size toward the margins of the mesocolpia. 
The large lumina are filled with rod-like, short 
elements, some of which are free standing while 
others extend diagonally and fuse with the muri. 
Colpi are long and wide with obtuse ends and a 
ular surface. Endoapertures are lalongate and 

elliptic. 
Bucida (Fig. 21B), Combretum laxum (Fig. 
0A), C. farinosum (Fig. 20B, C), Conocarpus 
erecta (Fig. 20E), Lumnitzera (Fig. 21C), Quis- 
lis pellegriniana (Fig. 21D), Strep/ (Fi 


Bert. 


21A), and Terminalia edulis (Fig. 20D) were ex- 
amined with TEM. In general, the tectum is thick 
and the columellae are short, erect and simple. 
In Q. pellegriniana, some columellae appear to 
ramify into two or three straight, fine, very short 
segments just below the tectum. A well-devel- 

pedi fratectal р; lar layer is present in Lum- 
nitzera. The foot layer is well developed in all 
taxa. It is either uniform in thickness (C. fari- 
nosum, Strephonema, Lumnitzera) or dome- 
shaped with the lower margin straight and the 
upper margin convex (Bucida, T. edulis, C. lax- 
um). In Conocarpus, in some areas the foot layer 
is dome-shaped and in others it is thin and 


~ 


„== Poivrea coccinea. Sublateral view. The circular endoaperture (dark area) is clearly evident through 
is striate (cf. with striate 


. Th 
Масе of G. senegalensis, Fig. 18E).—D 


“шге and two subsidiary colpi. The surface is rugulate. E, F. Laguncularia racemosa.—E. 


lar. The surface is 5 


C 
lpi are narrow with a granular surface (subsidiary colpi are absent). — F. Surface detail near an open endoap- 
ual ] um. 


: The surface is punctate. Scales eq 


902 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 | 


{ 


1984] PATEL ET AL.—POLLEN CHARACTERS 903 


" те 


О.» 
^ 


FIGURE 21. Transmission electron micrographs of Combretaceae pollen. — A. Strephonema pseudocola. Sec- 
bl nesocolpium. The thinning of endexine on both ends indicates the presence of endoapertures. The 
ack outline of the ektexine is due to the precipitation of osmium.—B. Bucida macrostachys. Section of a 
TD between a colpus and a subsidiary colpus.—C. Lumnitzera racemosa. Section passing through 
0 mesocolpia and an end of a subsidiary colpus (arrow). Note a thick infratectal granular layer.— D. Quisqualis 
Pellegriniana. Section of a col d adj t Ipi the fine g lar layer that the ektexi 
Processes on the colpus and extends into the intercolumellar spaces of the mesocolpia. Scales equal 1 um. 


~ 


es 20. Transmission electron micrographs of Combretaceae pollen.— A. Combretum laxum. Section of 
Ver | AR mesocolpia and a colpus or subsidiary colpus between them. Note the thick, dome-shaped foot 
farin, е endexine is thicker below the colpus (or subsidiary colpus) than below the тевосо!рла. B, С . Combretum 

osum. Section through a portion of a mesocolpium (on the right) and a portion of a subsidiary colpus (on 


d : : : н 
“= ous and the endexine (en) is greatly thickened. At the mesocolpial margin the thick foot layer (8) 
"S toward the subsidiary colpus.—C. Aperture region showing a thick, granular matrix covered by a fine 


904 


straight. The endexine is very thin in the me- 
socolpia, and thick at the colpi and subsidiary 
colpi. In Strephonema, it is either uniform or 
thin at the middle of the mesocolpia. At the mar- 
gins of the mesocolpia near the subsidiary colpi, 
the foot layer usually terminates but sometimes 
appears to continue as a very fine layer over the 
endexine of the subsidiary colpi. In T. edulis, C. 
laxum, Conocarpus, and Q. pellegriniana, finer 
and shorter columellae and a thinner tectum are 
present in the subsidiary colpi region. In С. Јах- 
um, the endexine is granular near the endoap- 
erture and granular-lamellate in Conocarpus and 
T. edulis. 

Combretum farinosum (Fig. 20B, C) differs 
from the other three taxa examined with TEM 
in having a very fine granular matrix in the col- 
umellae layer. This matrix fills the spaces be- 
tween the columellae and is also continuous in 
the subsidiary colpi region. Here, the columellae 
are shorter, the tectum is slightly thinner and 
often discontinuous as domes forming the gran- 
ular and rugulate units on the exine surface. The 
granular matrix is also continuous in the colpi. 
The columellae are embedded in it with their 
protruding distal ends forming the granules of 
the colpus surface. The tectum appears as a thin 
film on the matrix (Fig. 20C). Irregular, broken 
lamellae of ektexinous material (foot layer?) are 
also present. The thick endexine also appears 
granular in the vicinity of the endoaperture and 
is difficult to distinguish from the granular ma- 
trix. In Q. pellegriniana (Fig. 21D) such a gran- 
ular matrix is present over the thick endexine of 
the colpus. It extends into the intercolumellar 
spaces of the adjacent mesocolpia for a short 
distance, but is not as well developed as in C. 
farinosum. 


Discussion 


Apparently, there are no modern detailed 
studies of Combretaceae pollen (see Thanikai- 
moni, 1984). The following, therefore, is pre- 
sented as a brief background of the basic mor- 
phology. Erdtman (1971) described Quisqualis 
indica as having colpi alternating with “‘pseu- 
docolpoid thin walled areas" and made favorable 
comparisons with Cacoucia, Combretum, and 
Terminalia. He also described Laguncularia ra- 
cemosa but did not mention the presence or ab- 
sence of subsidiary colpi. Quisqualis latialata was 
described as having three pseudocolpi by Lo- 
breau et al. (1969). Sowunmi (1973) described 
pollen of Combretum glutinosum, Terminalia 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


avicennioides, T. glaucescens, T. macroptera, and 
T. superba in general as resembling each other 
and possessing a characteristic shape, aperture 
system, and exine. All grains were noted to have - 
**colpoid streaks" (= subsidiary colpi) alternating 
with colpi. Lastly, Guers (1974) and Guers etal. 
(1971) also showed a fundamental similarity in 
the pollen of Combretum aculeatum, C. gran- | 
diflorum, C. lokele, C. micranthum, C. platyp- 
erum, C. smeathnianni, Conocarpus erectus, 
Pteleopsis diptera, Terminalia glaucescens, T. 
laxiflora, and T. superba. All had colpi alternat- 
ing with subsidiary colpi. The one SEM illus | 
trated, that of Combretum aculeatum, is similar 
to С. cacoucia (Fig. 15A-C). | 

From a comparative point of view, Erdtman 
(1971: 117) felt that “Pollen grains + similar to 
those in Combretaceae occur in Melastomala- | 
ceae (cf. also Lythraceae and Penaeaceae). The | 
grains in Haloragaceae, Hernandiaceae, Myrta- | 
ceae, Punicaceae, Sonneratiaceae, etc. are = dif | 
ferent.” 

Our SEM observations indicate several rather | 
distinctive groups. Combretum (Figs. 15А-С, | 
16D-G), Quisqualis (Figs. 15Е, 16H, D, Bucida | 
(Fig. 17A), Conocarpus (Fig. 178), Pteleopsis (Fig, 
17C), Terminalia (Figs. 16A-C, 17D, F), M | 
matuella (Fig. 17E, С), Guiera (Fig. 18E), Pe | 
vrea (Fig. 19C), and Lumnitzera (Fig. 19D) с | 
prise the first group and are similar in és 
colpi alternating with subsidiary colpi. Vari 4 
surface patterns are repersented in this group. d | 
second group, characterized by the presence | 
an echinate surface and subsidiary colp! wo | 
resented by Thiola (Fig. 15D, E) and Ano aly of | 
(Fig. 18D, F). A third group, consisting 0 | 
Buchenavia (Fig. 18A-C) has an echinate 5 | 
but lacks subsidiary colpi. A fourth group Fe 
consisting of just one taxon, Laguncularia ^7 
19E, F), has a punctate surface and ! 


structural similarities. However, these b] 
limited at present. Strephonema is 50 "m 
from all other members of Combretacea® spat 
might best be considered to constitute à " 
subfamily Strephonematoideae, aS -— 
Dahlgren and Thorne (1984) and othe 


| 
| 


| 
| 


! 


1984] PATEL ЕТ AL.— POLLEN CHARACTERS 905 


Generalized comparisons with pollen from the 
core families essentially agree with Erdtman's 
(1971) suggestions given above. The pollen in- 
cluded in our first group shows broad resem- 
blances to some Penaeaceae, some Melastoma- 
taceae, and some Crypteroniaceae. Genera of 
Penaeaceae with these resemblances are: Endo- 
nema (Fig. 25A, C), Brachysiphon (Figs. 24A, B, 
25D), and Sonderothamnus (Fig. 25E). Genera 
of Melastomataceae that show these resem- 
blances are: Memecylon (Fig. 31E), Mouriri (Fig. 
31F), Trembleya (Fig. 32A), Osbeckia (Fig. 32B), 
Tibouchina (Fig. 32C), Tristemma (Fig. 32D), 
Votomita (Fig. 32E), Marumia (Fig. 33A), Dis- 
sotis (Fig. 33C, D), Acanthella (Fig. 33E), and 
Dissochaeta (Fig. 33F). Genera of Crypteroni- 
aceae that show these resemblances are Axinan- 


compares favorably with that in Penaeaceae 
(Glischrocolla, Fig. 274). 


ALZATEACEAE 


E. ао. verticillata, the only member of this 
өш family, pollen is tricolporate, radially 
in iino. 1sopolar, spheroidal to subprolate 
ten. Ee hexagonal to triangular (goni- 
pol ike obtuse corners and straight sides) in 
except ки. 4В, D). The surface is psilate 
Mesocolp; s elliptical areas at the middle of the 
áreas Pla where it is psilate-punctate; these 

are slightly depressed and possibly repre- 


-olpi : 
P! are long, with obtuse ends, and a smoot 


surfa А О, 
ce. A wide, coarse margin is present around 


apertures. 

aa the sides of the mesocolpia (i.e., around 

а > elliptic areas) the foot layer is well 

ы er the form of continous “hills” or 
es (Fig. 6B). The thick tectum has a 


lower 


foot layer, resulting in an undulated or a zig-zag 
columellae layer between the tectum and the foot 
layer. The short, erect columellae are un- 
branched. The endexine is relatively thin. At the 
middle of the mesocolpia (Fig. 6C), where the 
surface is punctate, the exine becomes thinner: 
the foot layer at first becomes thinner and then 
is present only as wide bases of the columellae; 
the columellae slightly increase in height and be- 
come branched; and the thin tectum has large 
perforati d an infratectal granular layer. The 
endexine increases in thickness as it does in taxa 
with subsidiary colpi. 

Near the colpi, the endexine is very thick and 
the foot layer tapers and is present either as a 
thin layer or is absent. At the margins of the 
mesocolpia, the very short columellae and the 
thin tectum with an infratectal granular layer are 
present on this thick endexine. The endexine is 
granular in the vicinity of the endoapertures. 


Discussion 


The punctate areas at the middle of the me- 
socolpia in Alzatea are suggested as being incip- 
ient subsidiary colpi by Muller (1975). The exine 
indeed is thinner in this area as is shown in the 
TEM (Fig. 6C). As mentioned by Muller, A/zatea 
pollen is comparable with that of those species 
of Rotala that show indistinct subsidiary colpi 
(Guers, 1970). Pollen ofthis genus has been char- 
acterized as (1) three colporate, (2) three colpor- 
ate with indistinct subsidiary colpi, and (3) three 
colporate with distinct subsidiary colpi (Guers, 
1970). Further, a spectrum of heterocolpateness 
also occurs within a single species (Cos Campos, 

964). Alzat 11 Iso b d wit! 


1 


Physocalymma (Cos Campos, 1964; van Campo 
in Lourteig, 1965). A detailed examination in- 
volving electron microscopy of these two lythra- 
ceous genera (i.e., Rotala and Physocalymma) 
should be instructive. 

Alzatea has been treated in several taxonomic 
systems (see Dahlgren & Thorne, 1984). Muller 
(1975) treated it in Crypteroniaceae following the 
system of van Beusekom-Osinga and van Beu- 
sekom (1975), as an ancestral tricolporate type, 
deriving from it the bisyncolporate bilateral 
Crypteronia type and the heterocolporate trira- 
diate Dactylocladus type. In a sense, he consid- 
ered Alzatea to have the relatively unspecialized 
pollen common in some angiosperm families, 
particularly in Lecythidaceae, Rhizophoraceae, 
Combretaceae, and Lythraceae (including Pun- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


A. Lateral vit? 


pe lef 
e. The subsidi" 


1984] 


icoideae, and in Lythroideae particularly Aden- 
aria, Pemphis, Pehria, Pleurophora, Physoca- 
lymma, Woodfordia, and some Rotala). 

Although the pollen of Alzatea is generalized, 
we feel that it is very similar to that of Chryso- 
balanaceae (Patel et al., 1983a) in shape as well 

in surface feat End p lly, it is sim- 
ilar to Dactylocladus, Axinandra, and Chryso- 
balanaceae (see also Corynocarpaceae, Nowicke 
& Skvarla, 1983) in having a zigzag columellae 
ayer. 


a 


RHYNCHOCALYCACEAE 


Rhynchocalyx lawsonioides examined wit 
both SEM (Fig. 4A, C) and TEM (Fig. 6D). Pollen 
is tricolporate, heterocolpate with three subsid- 
lary colpi, radially symmetrical and isopolar, 
spheroidal in lateral view and triangular-hexag- 
onal in polar view. The surface is coarse, with 
many punctae and irregular channels. Colpi are 
long, narrow with acut di, and have a granular 
surface. Endoapertures are lalongate. Mesocol- 
pial extensions are present over the endoaper- 
tures. Subsidiary colpi are wide and in some grains 
they appear to be united at the poles. Their sur- 
face 1$ similar to that of the mesocolpia. Thin 
section (Fig. 6D) shows the foot layer to be well 
developed in the mesocolpial regions; columellae 
нь numerous, erect, and branched distally, often 
m an infratectal granular layer (see Muller, 
5). The tectum is thick, perforate, with an 
me s upper margin that is locally discon- 
. uous and separated into domes. The endexine 


IS very thin and has an irregular lower margin. 
At the col 
thi 


the shots granular, the foot layer is tapered and 
rectly og ii columellae and thin tectum lie di- 
nedi Рем епдехте. Additional comments ге- 
di e ynchocalyx pollen can be found in the 
10n of Lythraceae and Crypteroniaceae. 


PENAEACEAE 


Р : у 
me grains are tricolporate in Brachysiphon 
“езі (Fig. 25D), В. fucatus (Fig. 24B), En- 


PATEL ET AL.—POLLEN CHARACTERS 


907 


donema laterifolia (Fig. 25A, С), Sonderotham- 
nus petraeus (Fig. 25E), S. speciosus (Fig. 24F), 
and Saltera sarcocolla (Fig. 24C, D). They are 
tetracolporate in Penaea cneorum (Fig. 23B, D), 
P. mucronata (Fig. 22A—C), and Stylapterus eri- 
coides (Fig. 22D—F), and 5-colporate in Gli- 
schrocolla formosa (Fig. 23A, C). Some tetra- 


fucatus (Fig. 24A), Glischrocolla, and Sondero- 
thamnus speciosus, whereas 6-colporate grains 
were observed in Saltera (Fig. 24E). Pollen of 
these taxa are heterocolpate with isomerous sub- 
sidiary colpi ог intercolpar concavities (in Sal- 
tera and Glischrocolla) alternating with colpi. 
They are radially symmetrical, isopolar (except 
some in Penaea, Saltera, and Stylapterus, see 
below), spheroidal to subprolate in lateral view, 
and circular to hexagonal (in tricolporate species) 
or circular to octag (in tet Iporate species) 
in polar view. The surface is psilate in Penaea, 
Brachysiphon, Saltera, Glischrocolla, Sondero- 
thamnus, and Stylapterus, with few pits and 
punctae. In Endonema it is rugulate with punc- 
t 


Colpi are long, with acute (Brachysiphon ru- 
pestris, Penaea, Saltera, and Stylapterus) or ob- 
tuse (Endonema, B. fucatus, Glischrocolla, Son- 
derothamnus) ends, the pollen surface is granular 
with the exception of Brachysiphon rupestris, 
Sonderothamnus speciosus, and Saltera, where 
it is smooth. Asymmetric colpi similar to those 
in Olinia were common in Glischrocolla (Fig. 
23C), Saltera (Fig. 24D), and Sonderothamnus 
(Fig. 24F). Endoapertures in such grains are lo- 
cated either on the equator, or on one polar face. 
The shape of these grains is spherical except in 

h also h idal, heteropolar 


L’ 


grains. Endoapertures are circular in Penaea and 
Stylapterus, and lalongate-elliptic with two lat- 
eral extensions in Endonema (Fig. 25B) and 
Brachysiphon. In Endonema, extensions of the 
mesocolpia are present over the endoapertures. 
They are either very small or absent in Brachy- 
siphon and are absent in the remaining taxa. In 
Sonderothamnus and Saltera, the endoapertures 
are slightly elliptic-lalongate and in Sondero- 
thamnus petraeus (Fig. 25F) the colpus mem- 
brane often persists as a horizontal bar over the 


e ТҮҮР p RP a S H *11 4 E | 


Colpi reese —E,F. Po 
su 9 The Subsidiary colpi are united at the poles in various combi 


lar views. 1р1 al e wit | 
nations. For example, in E the two opposite 


Scales Colpi are united while in F all four are united. The exine is smooth with few punctae and channels. 
qual 1 um. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


"d URE 23. Scanning electron micrographs of pengues pollen. A, C, E. Glischrocolla formosa. = 


‚рош 
сопсауїй® 
vi . Lateral view. Note the difference in the size and position n of the two visible intercolpar Sing rugis 
ane The central colpus is slightly asymmetric. LE Details of an окне COMMUN me ng 
с=з апа — center. B, D, F. Pe 1 1 orum. — В. Polar view. Compa: 
D.—D. Sub , L ; ч "ie d the cadena ар 
меч operculum erot osus. Rug p З т. 
а sibsidiary come Compare with чайн (Fig. 13D). Dales otherwise indicated, alee equal ^ А 


1984] 


open endoapertures. Round opercula were ob- 
served in Penaea cneorum (Fig. 23F), Brachy- 
siphon fucatus (Fig. 24A), Saltera, and Stylap- 


terus. 

The subsidiary colpi are long and have a 
smooth to granular surface except in Endonema 
(granular-verrucate) and Sonderothamnus (ru- 
gulate and similar to Olinia). The intercolpar 
concavities of Saltera and Glischrocolla have a 
rugulate surface on the margin and become gran- 
ular toward the center. Subsidiary colpi are often 
united in Brachysiphon and Sonderothamnus. 
Heteropolar grains with colpi or subsidiary colpi 
or intercolpar concavities united in various con- 
figurations were observed in Penaea (Figs. 22C, 
23D), B. fucatus (Fig. 24A), Saltera, and Stylap- 
terus (Fig. 22E, Р). In Saltera, 6-colporate grains 
with five intercolpar concavities and three very 
small, rudimentary or incipient (?) colpi were 
observed (Fig. 24E). In Sonderothamnus specio- 
Sus some grains appear to be fused in random 
configurations. 

In TEM (Figs. 26, 27), the tectum along the 
mesocolpia is very thick and without perfora- 
tions ш all taxa except Glischrocolla (Fig. 27A). 
A thin infratectal granular layer is present in all 
laxa except Penaea (Figs. 26A, 27F). The foot 
layer is also prominent, usually thicker than the 
tectum and dome-shaped. The upper margin of 
the foot layer is irregular. Between it and the 
bes Problematical columellae are usually 
“istinguishable. They are thick, very short and 
"regular and often surrounded by the infratectal 
uos layer. This columellae layer is undulat- 
ngor zig-zag in Saltera (Fig. 27C, D), and slight- 
i Br achysiphon acutus and Sonderotham- 
й 18. 26B); in Penaea (Figs. 26А, 27Р), it is 

Presented by a very thin, undulating gap be- 
Ween the tectum and foot layer. 

„о the colpi and subsidiary со1рї or in- 
hie concavities, the endexine increases in 
ess while the foot layer and tectum de- 

Phi the subsidiary colpus region in Son- 
tus (Fi mnus (Fig. 26C) and Brachysiphon acu- 
мора br 27B), a fragmented, thin foot layer 
Fui: E elaborate granular, spongy layer. This 
ye of I isa continuation ofthe infractectal 
better d € mesocolpia but is much wider and 
“С M d here. The intercolpar concavity 
ny rocolla and Saltera also has such a layer 
is 5 not as thick as in the above two taxa. 
Зан. Pongy granular layer is covered by a thin 
m. In Stylapterus and Penaea, the tectum, 
ular layer, and foot layer are all very thin in 


PATEL ET AL.—POLLEN CHARACTERS 


909 


the subsidiary colpi. The endexine is very thick 
and granular near the endoaperture. 


Discussion 


Pollen of the seven genera constituting Pen- 
aeaceae are best known through the light micro- 
scope studies of Dahlgren (1967a, 1967b, 1967c, 
1968, 1971) as part of his comprehensive study 
of the family. While variations in pollen size and 
shape are common the pollen is fairly uniform 
and is characterized by colpi alternating with 
subsidiary colpi. The only major difference is in 
the number of apertures which seem to be the 
most variable in Penaea and Saltera (Dahlgren, 
1968, 1971). These observations are also sup- 
ported in other studies (1.е., Erdtman, 1971; 
Archangelsky, 1971). 

Our results indicate that phically, Pen- 
aeaceae pollen resembles that of Oliniaceae (see 
Oliniaceae discussion), Melastomataceae (com- 
pare Endonema, Fig. 25A, C, with Tristemma, 
Fig. 32D, and Dissotis, Fig. 33C, D) and Com- 
bretaceae (compare Brachysiphon, Fig. 25D, with 
Combretum, Fig. 15B, and Quisqualis, Fig. 161, 
with Penaea, Fig. 23B). Endomorphically, the 
exine structure in the mesocolpium is similar to 
that of Oliniaceae (Fig. 14В—Е) while the subsid- 
iary colpal areas show a somewhat distant sim- 
ilarity to Onagraceae pollen (compare Sondero- 
thamnus, Fig. 26C, with Figs. 60-63). 


CRYPTERONIACEAE 


Crypteronia paniculata (Figs. 308, 31B-D), 
Dactylocladus stenostachys (Figs. 28A, C, E-G, 
29), and Axinandra zeylanica (Figs. 28B, D, 30C) 
were examined with SEM and TEM. Crypteronia 
sp. (Fig. 31A) was examined only with SEM and 
C. leptostachys (Fig. 30A) only with TEM. Cryp- 
teronia (Fig. 31A-D) pollen is dicolporate, syn- 
colpate, and bilaterally symmetrical. It is shaped 
like a football with the two endoapertures situ- 
ated at the opposite pointed ends. It is elliptic in 
polar view and in lateral view (away from the 
endoapertures, or facing the mesocolpium); and 
circular to square in lateral view facing the en- 
doaperture. The colpi have a smooth surface. 
They are united at both poles forming a circle 
around the grain. The endoapertures are lalon- 
gate, elliptic. The surface of the mesocolpia is 
rugulate. At the middle of each mesocolpium 
there is an equatorially elongated intercolpar 
concavity which has a verrucate-rugulate sur- 


| 
| 
| 


| 


910 ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL 7! | 


| 
Dactylocladus and Axinandra both have tri- ends which are sometimes united in tetracol- ? 


colporate (rarely tetracolporate in Dactylocla- porate grains. The obscure endoapertures ar | 
dus), heterocolpate, radially symmetrical, iso- slightly protruding and have extensions of the 
polar pollen (Fig. 28). Pollen is spheroidal in mesocolpia over them. The subsidiary colpi ar | 
lateral view and triangular-hexagonal in polar wide, with a granular surface, and irregular chan- 
view. In Axinandra, the surface of the mesocol- nels. At the poles the subsidiary colpi are united. | 
pia is psilate, with a few scattered punctae. The The exine of Crypteronia is thin (Fig. 30A, B) , 
colpi have acute ends, a smooth appearing sur- The narrow and more ог less uniform tectum 
face, and are narrower than those in Dactylocla- апа foot layer are separated by short, thick, and | 
dus. The obscure endoapertures are covered by simple (unbranched) columellae. The endexine 
exine extensions of the mesocolpia. The subsid- is thick below the colpi and intercolpar concav- | 
iary colpi are long and sometimes united at the ities but thin elsewhere. It is granular- 
poles. Often, they are wide, appearing like inter- near the endoapertures. In contrast, the exine dí 1 
colpar concavities. Their surface is punctate. The — Dactylocladus (Fig. 29А-С) is thick. It hasa thick 
margin of the mesocolpia around the subsidiary tectum and a broad foot layer which is often 
colpi is often more punctate than other areas of | dome-shaped (Fig. 298, mesocolpium to the lefi). 
the pollen grain. In Dactylocladus, the surfaceis A narrow columellae layer with thin, short col- 
psilate with some punctae and channels on the umellae separates the tectum and foot layer. In | 
mesocolpia around the subsidiary colpi. The col- some parts of the grain, the columellae layer fol 
pi are wide with a granular surface and obtuse lows a zig-zag pattern. The endexine is thick be , 
и 


— 


| 
FIGURE 24. Scanning electron micrographs of Penaeaceae pollen. A, B. Brachysiphon fucatus.—A. Later | 


2 јајопра 
view. The surface is rugulate while the subsidiary colpus has а verrucate-granular 5 ace. — B. Elliptic, ns of the | 
endoaperture as viewed from the inside of the pollen grain. The arrows show two lateral extension . are 
enc юра Polar view showing three colpi and three subsidiary colpi. Extensions of ee Res and two | 
evident over the endoapertures.—D. Brachysiphon rupestris. Lateral view with а colpus at the hamnus 
sidi : : d vede . E, F. Sonderot 


F. View of colpus. An ektexinous bar over the endoaperture gives the impression of two pores beris ЗА, | 
within each colpus. Ektexinous bars аге also common in some Melastomataceae pollen (see Figs- = 

C, D). The surface of th Ipia is psilate with few pits and channels while the colpus (and subsidiary 
of E) is granular. Scales equal 1 um. Я 


| 


ой ог: | 

FIGURE 26. Transmission electron micrographs of Penaeaceae pollen.— A. Penaea mucronata. undulating 
lpi 34 A nS í X n th 1.6 4 heidi 1 the right A very thin ров | 
electron translucent "line" separates the thick tectum from the thick foot layer. Near the ees is relative’? 
layers are thin and discontinuous; over the subsidiary colpus they are extremely thin. The ange ad 


thin in the middle of the mesocolpium and thick near the subsidiary colpus and endoaperture. с ctum is impe" 
it is also granular. B, C. Sonderothamnus petraeus.—B. ion of a mesocolpium ; uch thicker 
forate. An infratectal granular layer is partially obscured by osmium precipitate. The foot layer 15 a Tbe 

than the tectum. The endexine is thin and relatively uniform.—C. Section of a subsidiary the foot 
is thin with a wavy or lobed ou n. The infratectal layer is well developed Immediately below, ert 
layer (arrow) appears to be highly disrupted or ent re are no distinguishable columellae 

(en) is as thick or thicker than the ektexine. This section is reminiscent, in a sense, to sections of (on the 
(see Figs. 60-63).—D. Sonderothamnus speciosus. Section of a mesocolpium near a subsidiary colpus. ; 
right). Compare with B and С. The exine sections represented in Figure 26 should be compared with 


sections in Figure 14. Scales equal 1 um 


PATEL ET AL.—POLLEN CHARACTERS 


1984] 


PATEL ET AL.—POLLEN CHARACTERS 


913 


914 ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL 71 


low the colpi and subsidiary colpi and thin else- phology of Axinandra beccariana, Dactylocladus 
where. It is granular near the endoapertures. In stenostachys, Crypteronia paniculata, C. с 


ter 
the subsidiary colpi the tectum, foot layer, and mingii, C. griffithii, Rhynchocalyx lawsonioides | 


— 


columellae become very thin. In our TEM, we апа Alzatea verticillata. The latter two species - 
did not clearly recognize the small granules which аге treated now as separate monotypic families | 


Muller (1975) described as best developed on the — (i.e., RAynchocalyx in Rhynchocalycaceae, and 


lower tectum surface of Dactylocladus and weak- Alzatea in Alzateaceae). As discussed previously | 


ly developed on Crypteronia. (see Alzateaceae), three pollen types were rec- 
Axinandra (Fig. 30C) has a thin exine with a ognized in the Crypteroniaceae (Muller, 1975: 
narrow tectum and foot layer. The columellae 276) *. . . the tricolporate A/zatea-type, the het- 
are thick or thin and short. Occasionally, a zig-  erocolpate Dactylocladus-type (Dactylocladus, 
zag pattern of the columellae layer is seen. The Axinandra, and Rhynchocalyx) in which three 
endexine is thick below the colpi and subsidiary colporate apertures alternate with three 


~ 


рога се ШУ | 
colpi, thin elsewhere, and granular neartheendo- docolpi, and the bisyncolporate Crypteronia- 


apertures. In the subsidiary colpi tbe tectum Pine type." The less specified A/zatea-type was Те 
foot layer are narrow and garded as ancestral in the family. 
In a general sense, we are in complete agree 


Discussion 


Muller (1975) described with light and electron cud 
microscopy (SEM and TEM) the pollen mor- lastomataceae (see dicolpo | er ain оѓ Miconia 


o e. 
= 


FIGURE 27. Transmission electron micrographs of Penaeaceae pollen. —А. Glischrocolla formosa. Section 
two mesocolpia and an intercolpar concavity (center). The outer margin of tectum appears lobed due -i the 
punctae of the surface. A thin and uniform infratectal granular layer is p in Бу meso E 
intercolpar concavity. The foot layer i is dome-shaped in the mesocolpia. Its upper m and the 
In the intercolpar concavity, it is thin and highly disrupted. It is difficult to distinguish ош due 10 
irregular upper margin of the foot layer. The endexine is thick and uniform becoming be ed 


layer, or both. In the mesocolpium, however, distinct columellae and well-developed, dome-shaped e 
(not included here) are present. C, D. Saltera oe. —C. Section of an i concavity and k tectum 
mesocolpia.— D. Section of a | mesocolpium. Note ween the very gc rerus 
and foot layer. The colp i ses in thickness toward e ы E a iu 
ericoides. Section of a mesocolpi ium.—F. Penaea cneorum subsp. ruscifolia. Section of an € which 
Note that the very thick tectum and foot layer are нм by an undulating gap (columellae aye 
appears dark due to osmium precipitate. Scales equal 1 и 


FIGURE 28. Bhilai eser micrographs of Crypteroniaceae pollen. A, С, E-G. Расу locladus да ae 

chys.—A. (SPH 3975). Late iew with a subsidiary colpus at the center. The subsidiary со ipi по h ИП 1982. 

the poles. Compare also on; pla electron micrograph of Muller T + IV, figs. 1-3).— —C. (Chai, 
(732A). Polar view of a tetracolporate grain. —F. (SPH 3975). pee view d. 


rture is covered by colpus тсз visible 
ке were dues, ы noted in this collection. Rugulate surface of the subsidiary colpi of both grains 
les equa 


FiGure 29. a electron m с ћ А-С. р m ic i 
dos cA Cha OM i rograp 5 of а pope subsidia 
colpus. Note that кз а реа la ae ofthe 
B. (Chai 39708). Section sho 
the ri i 


ment with Muller (1975) that Axinandra and | 


——— 


| 


1984] 


PATEL ET AL.—POLLEN CHARACTERS 


1984] 


PATEL ET AL.—POLLEN CHARACTERS 


918 


ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 | 


| 


А verti | 
FIGURE 30. Transmission electron micrographs of Crypteroniaceae.—A. Crypteronia lean е је 


section of an entire grain Passing through two colpi (open arro whi ide are Miren 
i (soli .—B 


and | 
a panic tion o а пио 


—C. Axinandra zeylanica (GUT 4 н atilleke m Section of tw de indica 
. The right mes lpi 


ig-zag columellae layer. 


PATEL ET AL.—POLLEN CHARACTERS 


p auks 3I. 31. Scanni ing electron micrographs of pollen from e (A-D) and Melastomataceae (E, 
У; arged portio 


unding mesocolpia. The surface of the 


arrow). Thick arrow indicates an intercolpar 
ly.—E. Mer A ee orma i e i te.—F. Mouriri glazioviana. Lateral 


М, е the lit, — thick- margined endoaperture. The surface diste of fine, elongate, branched 
ales 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


1984] 


hondurensis, Fig. 35E), Combretaceae, Penae- 
aceae, Oliniaceae, and Lythraceae (Lythrum, 
Peplis, some species of Ammannia, Nesaea, and 
Rotala). Further, the Crypteronia-type pollen of 
Muller relates to Corynocarpaceae, Cunoni- 
aceae, E hi and Saxifi (Mull 


1975; see also Erdtman, 1971). In endomor- 
phology, Dactylocladus resembles Alzatea, 
Chrysobalanaceae (Patel et al., 1983a), and Cor- 
ynocarpaceae (Nowicke & Skvarla, 1983) in hav- 
ing the zig-zag columellae layer. 


MELASTOMATACEAE 


Pollen of Melastomataceae is tricolporate, ra- 
dially symmetrical, and isopolar. Grains are 
spheroidal to subprolate in lateral view with a 
circular, hexagonal, or triangular shape in the 
polar view. Monads are found in all taxa ex- 
amined with the exception of Tococa spadiciflora 
which has polyads (Fig. 35F, H), and Miconia 
melanotricha (Fig. 35A, B) which has tetrads (Pa- 
tel et al., unpubl. data). On the basis of exo- 


e оза (Fig. 33A, B), Dissochaeta celebica (Fig. 
re Osbeckia polycephala (Fig. 32B), Acan- 
Fi a sprucei (Fig. 33E), Memecylon normandii 
Mes 31E), Mouriri glazioviana (Fig. 31F), Vo- 
Pe monadelpha (Fig. 32E, F), Miconia hon- 
casia (ів. 35D), M. alypifolia (Fig. 36A), M. 
: га (Fig. 36D), Comolia stenodon (Fig. 36H), 

Tococa broadwayi (Fig. 36F). The surface 


PATEL ET AL.—POLLEN CHARACTERS 


921 


sculpture is variable. A more or less smooth sur- 
face with a few pits and punctae is present in 
Acanthella (Fig. 33E). In Dissotis (Fig. 33C, D) 
many channels, pits, and punctae are present on 
a smooth to rugulate surface. In Marumia (Fig. 
ЗЗА, B), Dissochaeta (Fig. 33F), and Memecylon 
the surface is coarsely rugulate-punctate. It is 
striate-rugulate in 7ristemma (Fig. 32D), Como- 
lia (Fig. 36H), and Osbeckia (Fig. 32B), with 
elongate, more or less parallel muri, which in the 
latter become shorter and separated at the poles 
where the surface then becomes verrucate-ru- 
gulate. In Trembleya (Fig. 32A) and Miconia aly- 
pifolia (Fig. 36A) it is striate. In the latter species, 
bundles of striae are separated by large channels 
at the poles (Fig. 36A-C). In Tibouchina (Fig. 
32C), it is smooth-punctate with a very faint 


32E, F) is composed of fine, elongate, branched, 
often overlapping muri that form a compact mesh 
with punctae. In Miconia hondurensis it is 
smooth-punctate (Fig. 35D, E). The surface of 
M. caesia (Fig. 36D) is distinctive in possessing 
a mesh of short, branched, cylindrical elements. 
In Tococa broadwayi (Fig. 36F), it is perforate. 
Colpi are long (some grains are syncolpate in 
Dissotis, Acanthella, and Dissochaeta), with acute 
ends, and a smooth surface except in Acanthella, 
Marumia, and Dissochaeta where the surface is 
granular. In Votomita, the colpus surface is cov- 
ered with bead-like elements. Endoapertures are 
lalongate (not clearly defined in Dissochaeta) and 
elliptic (circular to elliptic in Votomita). Exten- 
sions of the mesocolpia over the endoapertures 
are present (Figs. 32A, D, 33E, 36A). A hori- 
zontal bar is often persistent over the open en- 
doapertures (Figs. 32C, 33A, D). Subsidiary colpi 
are long except in Tococa broadwayi (Fig. 36F), 
narrow, and have either a smooth, scabrate, or 
granular surface (Fig. 33B). They are usually 


e exine 


Vip. 


л 

Mos. 3 2. Scanning elect micrographs of Melastomataceae pollen.— A. Trembleya  phlogiformis. Lateral 
owing extensions of the me ia the endoaperture (at ) and tı 

Surface is stria 


te.—B. Osbeckia polycephala. Lateral view. The exine surface is rugulate.—C. Tibouchina urvil- 


leana, Sublateral view with a subsidiary colpus at center. A horizontal ektexinous bar appears to divide the 


» Чай with bead.like units of the colpus. This surface is 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


JRE 33. Scanning ара micrographs of Melastomataceae pollen. A, B. Marumia nervos 
view ا‎ horizontal bar over endo d for 32C The exine — 
idi D. Diss 


w. T n 
А е 
nels and pits. Extensions of the mesocolpia over м Meer are promin 
Dissochaeta celebica. Lateral view. The sur rein is rugulate. Scales equal 1 


1984] 


shorter than the colpi but in Marumia and Dis- 
sochaeta they are as long as or longer than the 
colpi. Some grains of Miconia hondurensis (Fig. 
35E) are bilateral, dicolporate, syncolpate with 
two large intercolpar concavities. In addition to 
the usual tricolporate-isopolar pollen of M. aly- 
pifolia there are present: (1) grains with various 
arrangements of colpi and subsidiary colpi (Fig. 
36C), (2) heteropolar grains (Fig. 36C), and (3) 
grains with both subsidiary colpi and intercolpar 
concavities (occurring in pollen with more than 
three colpi, Fig. 36B). 

In the second group, “‘heterocolpate”’ with in- 
tercolpar concavities, there are present on the 
mesocolpia three intercolpar concavities — large, 
elliptic, thin-walled, depressed areas. The re- 
maining thick-walled portion of the mesocolpia 
forms a more or less narrow band around the 
intercolpar concavities. This type of pollen is 
illustrated by Adelobotrys tessmannii (Fig. 34A- 
C), Allomorphia caudata (Fig. 34D), Bredia hir- 
suta (Fig. 34F), Astronia cumingiana (Fig. 34E), 
Oxyspora paniculata (Fig. 34G, H), and Miconia 
melanotricha (Fig. 35A-C). The grains are sphe- 
roidal in lateral view and circular to triangular 
or hexagonal (Oxyspora) in polar view. Colpi are 
ong and narrow with acute ends and a more or 
less smooth surface. Extensions of the mesocol- 
pia are present over the lalongate, elliptic en- 
doapertures (Figs. 34D, E, 35A, B, D, not clearly 
ји in Allomorphia, not examined in As- 
гота). Adelobotrys differs from the other taxa 
2 Pris wide colpi that are united at the poles, 

nd by a granular-verrucate surface. The colpus 
E is raised over the endoaperture (Fig. 
di » arrow). This raised membrane is vertically 

€nted and does not seem to be analogous with 

ап operculum. 
“а surface ofthe meso- and apocolpia is vari- 
udi Psilate in Adelobotrys (Fig. 34A—C), sca- 
da Allomorphia (Fig. 34D, although not very 
H) с Striate-rugulate in Oxyspora (Fig. 34G, 
m rugulate-verrucate in Bredia (Fig. 34F), 
e "Punctate in Miconia (Fig. 35C), and 
e A many channels and pits (rugulate ?) 
tie di E (Fig. 34E). The intercolpar concav- 
ud piss In size and surface sculpture. In Bredia 
avidis | ота, the surface sculpture of the con- 
ds 15 similar to that of the rest of the grain 

Ept that it is finer. Adelobotrys and Allomor- 
Phia have а face while O h 
е IM irregularly shaped units on the sur- 
the eh, e intercolpar concavities. In Miconia 

ace 15 granular-verrucate. 


i 
i 


PATEL ET AL.—POLLEN CHARACTERS 


923 


Exine structure is similar in both pollen groups 
described above. In the meso- and apocolpia the 
foot layer is well developed and often dome- 
shaped (Figs. 37B, D, 38A, 39A). Here the end- 
exine is less developed and often very thin (Fig. 
38A, B). A “white line” between the foot layer 
and the endexine is often distinct (Figs. 37B, C, 
38A). The columellae are short, erect, and dis- 
tally branched. The tectum is thick, perforate, 
and has an undulating outer margin, although in 
Adelobotrys (Fig. 39A) perforations are rare and 
the outer margin of the tectum is smooth. Acan- 
thella (Fig. 38D) differs from the other taxa in 
having a very thick tectum (rarely perforate) and 
thick foot layer that are separated by columellae 
that appear granular and have lateral extensions. 

Toward the colpi and subsidiary colpi or the 
intercolpar concavities, the endexine becomes 
thicker whereas the ektexine layers taper. The 
foot layer is discontinuous and thinner at the 
margins of the mesocolpia: on the surface of the 
colpi, subsidiary colpi, and intercolpar concav- 
ities, it remains either as a very thin layer (Figs. 
38A, 39A, B, D) or is absent. The tectum is thin, 
the columellae are short and fine, or they are both 
absent. In the intercolpar concavities, the ver- 
rucae (or the irregular ele tsin Oxyspora) sh 
a thin, dome-shaped tectum below which one or 
more fine columellae are present (Fig. 39A, B, 
D). In Astronia the tectum is thin and columellae 
are irregular and short (Fig. 39C). 

In the region of the endoaperture, the endexine 
is thick and granular and often lamellate (e.g., 
Adelobotrys, Trembleya). The tectum is thinner 
and the columellae are shorter. The foot layer is 
tapered leaving the columellae and tectum di- 
rectly overlying the granular endexine (Figs. 38D, 
39A, C, D). Around the endoaperture in Astronia 
(Fig. 39C) the columellae and tectum are sepa- 
rated from the endexine. 

The third, tricolporate group, is represented 
by Tococa stephanotricha (Fig. 36E) and T. for- 
micaria (Fig. 36G), which have a rugulate surface 


is thicker, granular, and lamellate. The foot layer 
is also uniform in thickness. The columellae are 
short, erect or reclining, and rarely branched. 

e tectum is discontinuous with irregular dome- 
like units in section. 

A third species of Tococa, T. spadiciflora, could 
not be assigned to any of the three groups de- 
scribed above. It consists of polyads which are 


924 


composed of basic units of tetrahedral tetrads 
(Fig. 35F-I). Internal bridges on the proximal 
faces of individual pollen grains maintain tetrad 
unity while external bridges on the distal faces 
of the tetrads, frequently along the aperture mar- 
gins, maintain polyad unity (Fig. 356-1). Indi- 


a ——Q A wi ad 
with five or more colpi have also been noted. 
С: 1 : 1 +1 "n 4 vit ie +h 


surface. Some grains appear to have colpi of un- 
equal length. Endoapertures are lalongate and 
elliptic. The meso- and apocolpia surface is 
smooth-punctate. Subsidiary colpi are difficult to 
characterize and are either weakly developed or 
absent. In TEM (Fig. 40A), the endexine is more 
or less uniform in thickness except near the en- 
doapertures where it is thicker and granular. The 
foot layer is uniform in some areas but in others 
it is highly irregular and discontinuous with many 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor 71 


channels and gaps. Columellae are long, thick, 
and erect, and they split at their distal ends into 
fine, very short branches. The tectum is thick 
and uniform, with large perforations. The tectum 
as well as the columellae show fusion at the points 
of attachment between members of the polyads. 


Discussion 

As indicated earlier, Melastomataceae pollen 
has received little study above the light micro- 
scope level. Guers (1974) included scanning elec- 
tron micrographs of Dicellandra barteri, Calvo 
orientalis, and Osbeckia decandra. These wert 
part of a light microscope study of eight genera 
and 20 species from tropical Africa. Dicellandra 
and Calvoa compare favorably with our seco 
pollen group in possessing intercolpar concavi- 
ties; in contrast, O. decandra compares with our 
first pollen group. 


a | 


— 


FiGURE 34. арин ivi. micrographs of Tue unas pollen. A-C. паа та А. 
ercolpar 


Lateral view showing an cavity with a 


rrucate surface. The surrounding m 


and have a psilate surface. The colpi are united at the Minis (i.e., syncolpate). — —B. Lateral “a v а colpus. 


united colpi with à 


is 
granular еен The е sides of the pm gmin are due to the thin-walled inter аг concavis Ina 


intercolpar concavities is also rugulate but not as coarse as the rest of the grain.—F. Bredia hirsuta. Lateral view. 

The surface is rugulate. The intercolpar concavities are also rugulate pn eas a finer surface = a 
aniculata.—G. Lateral view. The surface is striate. The colpus is very w and long.— urface of | 
the intercolpar concavity and x У ы-ы area. Irregular, flattened ейн аге present on the 5 | 
the concavity. Scales equal 1 ш | 
„ha AA | 
E 35. Scanning electron pron of Melastomataceae pollen. A-C. Miconia melanotricha. z EI 
пон tetrad. Exine bridges connect tetrad m mbers.—B. Three grains of a tetrad. fourth | 
missing as indicated by broken brides (arrow). —C. The bridges are narrow and have a smooth at E 

surface of the mesocolpia is Pia asser that of the intercolpar concavities is -venia colpi- 

Miconia hondurensis.—D. Po ew of a tricolpo м 


—E. Astronia cumingiana 
rugulate. The od S is very narrow. Note the т mesocolpial extensions (see Fig, 


ith 
rate grain. Three subsidiary colpi alternate WI visible | 
E.  Sublateral view of a bini. dicolporate, eap grain with two intercolpar concavities. Here the 


1 й | 
indicates the position of an endoaperture. Е-Н. Tococa spadiciflora (Ascher 1976).—F. A polya + the centet | 
from а polyad showing bases of bos exine bridges on the m of a colpus. The colpus n < TWO 
(arrowhead) appears to be shorter than the one on the right, and also at a slight angle to the po ш 


FIGURE 36 
view. Note the striate-punctate surface near the e 


Polar view of a six-colporate кап with subsidiary ы un 
grains are rare. — C. Subpolar view s a heteropolar, conoidal (Muller, 1978b) en 
w.—E. Toco oca stephanotricha. Polar vi 


are united. — 


view 


. M. caesia . Polar v 


are nat 


ngated. In some оо syncolpate te grains, mall amo" _ 


ard the poles the surfa 
rrow) and intercolpar опата (arro 
The tw 


nar 
teral view 


ath 
ст 


Н.С Зевса idem Subpolar view. gea equal ] um 


taxa of the family. ns T. formicaria. La 


E шка | 
б 


Scanning лале micrographs of ененин cad pollen. A-C. Miconia alyp 
r. Tow. ce beco 


visible colpi "E 
roadway 
| 


u 
ра 
m 
= 
5 
« 
T 
Q 
= 
шщ 
4 
d 
© 
58 

| 
- 
< 
= 
m 
€ 
m 
~ 
< 
A 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


un 
| 
hd 
= 
5 
< 
T 
О 
Z 
W 
— 
ч 
О 
[7 

І 
= 
< 
= 
ш 
— 
ш 
zZ 


928 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


Је. жо 
FIGURE 37. Transmission electron micrographs of Melastomataceae pollen.—A. Тїї етта a d 


of a mesoco Ipium. —B. Trembleya phlogiformis. An obli 1 which 

que section of a mesocolpium : сала. А 
the collapsed grain. The columellae are numerous and markedly branched.—C. Tibouchina ‘cand ой 
portion of the mesocolpium near an endoaperture (not included here). The endexine is gran d 
E. Osbeckia polycephala.—D. Cross section of an entire grain. Because the section does not e Тк 


ог endoapertures, colpi and subsidiary colpi cannot be e —E. Mesocolpium near an € 
bai is deeply lobed due to striae. Scales equal 1 u 


1984] PATEL ET AL.—POLLEN CHARACTERS 929 


«pr» ear ~ 
TEL У 
А LA LH pet 


«v 


“о 38. Transmission electron micrographs of ронса роПеп. – А. Marumia nervosa. Section 

~ mesocolpia and a colpus or subsidiary colpus n them. The dome-shaped foot layer is similar to 

etaceae pollen (Fig. 20A, B, D, F).—B. eae y celebica Similar to Figure 37A.— C. Dissotis brazzae. 
igure Mesocolpi 


2 (У 
e 
B 
= 
= 


с 
оп 

= the thick foot layer is reduced while endexine increases in thickness and becomes granular. Note the 

‘ral similarity to the pollen of Oliniaceae (Fig. 14В-Е) and Penaeaceae (Fig. 26A, B, D). Scales equal 1 um. 


930 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


I Uu 


1984] 


Among the genera examined here, Mouriri, 
Votomita, and Memecylon have often been seg- 
regated with several other genera from Melas- 
tomataceae sensu stricto as Memecylaceae or 
subfamily Memecyloideae (e.g., Dahlgren & 
Thorne, 1984; Johnson & Briggs, 1984). All three 
of these genera belong to the heterocolpate group, 
but they are not delimited as a group in any way 
from the other heterocolpate genera of Melas- 
tomataceae, although Votomita is unusual in 
having four colpi and subsidiary colpi, and a 
bead-like colpus surface. Further studies on this 
group, including Lijndenia, Spathandra, War- 
necka, and more species of Memecylon, and par- 
ticularly Pternandra, are essential to a proper 
understanding of the relationships between Me- 
lastomataceae sensu stricto and Memecyloideae. 

Within the limited context of this study only 
those taxa in our first pollen type, that is, the 
heterocolpate type, show some similarities to 
other core families. At the SEM level some re- 
semblance is evident with Combretum (Fig. 15A, 
B), Bucida (Fig. 17A), Conocarpus (Fig. 17B), 
Pteleopsis (Fig. 17C), Terminalia (Fig. 17D), Ra- 
matuella (Fig. 17E), Guiera (Fig. 18E), Poivrea 
(Fig. 19C), and Lumnitzera (Fig. 19D) of Com- 
bretaceae; and Sonderothamnus (Fig. 25E) of 
Penaeaceae. Some of the bilateral, dicolporate, 
‘yncolpate grains in Miconia hondurensis (Patel 
et al., unpub. data) recall Crypteronia. At the 
TEM level the striking dome-shaped foot layer 
of the heterocolpate type (Figs. 37, 38, except 
Acanthella Fig. 38D) compares with that in 


e (Fig. 20). TEM of Acanthella (Fig. 


(Fig. ; 

. Saltera (Fig. 

and ( and Stylapterus (Fig. 27E) of Penaeaceae; 
Olinia (Fig. 14B-E) of Oliniaceae. 


um А 


PATEL ЕТ AL.—POLLEN CHARACTERS 


931 


TEM of the other two pollen types (Figs. 39, 
40) does not reveal any significant comparisons 
other than those already mentioned in the plate 
legends and pollen descriptions. Clearly, pollen 
in this family must be investigated in greater 
depth. 


MYRTACEAE (INCLUDING PSILOXYLACEAE 
AND HETEROPYXIDACEAE) 


In general, the pollen is tricolporate (triporate 
in Tristania nereifolia), radially symmetrical, and 
isopolar or heteropolar. In lateral view the pollen 
is oblate, elliptic with obtuse or truncate sides 
(Reitsma, 1970). In polar view it is triangular, 
goniotreme with straight or curved sides (convex 
or concave), and with acute or obtuse corners. 
Colpi vary in length, are either syncolpate or 
p у Ipat dg lly | smooth sur- 
face. Endoapertures are lalongate. Intercolpar 
concavities are present in some species. Hetero- 
polar grains are due either to the nature of the 
colpi (e.g., long on one pole and syncolpate on 
the other pole), or to the different shapes (con- 
cave, convex, straight) of the two polar faces. In 
Eugenia capuli, and in some grains of Luma 
chequen, Chamelaucium unciniatum, Temu di- 
varicatum, and Ugni molinae, one polar face is 
concave (or straight, in Chamaelaucium) and the 
other is convex. The pollen is free except in Myr- 
tus communis (Fig. 48D) and Psidium littorale 
(Fig. 46B), where tetrahedral tetrads are present 
along with the monads. 

Based on the nature of colpi, Pike (1956) rec- 
ognized three pollen types in the Myrtaceae from 
the southwest Pacific area: (1) longicolpate grains; 
(2) syn- or parasyncolpate grains, and (3) brevi- 
or brevissimicolpate grains. All three types are 
present in the taxa examined in this study. 


~ 


FIGURE 39, 


A. Sectio 


socolpia consist of a thick imperforate tectum, short columellae, 


mesocolpial extensions noted in scanning electron micrograph (see Fig. 34E). D, E. Oxyspora pani- 
| тезосојр OSS Section of approximately one-third of an entire grain including two colpi (on the sides), two 
la еме: and an intercolpar concavity.— E 
| ћршт. Scales equal | um. 


932 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


FIGURE 40. кеш electron micrographs of Melastomataceae pollen.— A. Tococa SP 
ofa sain Fusion of tecta of two adjacent members (arrowhea , C. Tococa stephanoiri e 
of an entire grain indue wo apertures. The tectum appears discontingóus s due to the v 
incu at a higher magnification. Note that foot layer and endexine are Mises 


adicifolia- Sed 


== 


PATEL ET AL.—POLLEN CHARACTERS 


. Subpolar view. Syncolpate colpi form 
Scattered some granular ektexinous elements. —D. Late dg new showing the outline of a lalongate, 
€ndoaperture and two i ntercolpar concavities.—E. Tristania nereifolia. Polar view. Note the smooth- 
pertures. Note close agreement with the scanning 
Tristania lactiflua. Lateral p and are pun 


PATEL ET AL.—POLLEN CHARACTERS 


„Коо URE 43. Scan nning electron micrographs of Myrtaceae pollen. A, C. Callistemon teretifolius.—A. Polar 
- Syncolpate grain. Intercolpar —Ó are distinct and have a coarse rugulate-verrucate surface. —С. 
un 


sent. The s 
5. Scales рн 1 u 


0 be 
element 


CD represents the cytoplasmic contents of the —— 2 apses к С-Е. samen ficifolia. — 
olar 


E Ma views of two grains from the same p: In С the grai pate, in D it is parasyncolpate. — 
la nified area near the equator (and endoaperture).—F. Pg uico pe Subpolar view. Sy ncolpate grain. 
*rcolpar concavities have a granular surface. Seve the surface is smooth. Scales equal | и 


936 


(1) Longicolpate type 


The colpi are long; ‘‘colporate grains are lon- 
gicolpate when the colpi are longer than the dis- 
tance between their apices and the poles” (Pike, 
1956: 51). Hypocalymna angustifolium (Fig. 44E, 
G), Myrceugenella apiculata (Fig. 47F), and Ugni 
molinae (Fig. 46D, E) belong to this type. In 
addition to the long colpi, pollen shape is also 
similar in Myrceugenella and Ugni: the trian- 
gular grains have convex sides and slightly pro- 
truding apertures in polar view and an elliptic 
shape with acute ends in lateral view. The surface 
in Myrceugenella is verrucate-granular with some 
larger verrucate elements at the poles (Fig. 47). 
Ugni shows a unique surface pattern with mul- 
tiangular units that have acute corners (Fig. 46E). 
These units are large and scattered at the poles 
but become smaller and more tightly packed to- 
ward the equator. The surface appears to be gran- 
ular around the endoapertures. In Hypocalymna, 
the grains are triangular with straight sides in 
polar view and elliptic with acute corners in lat- 
eral view. The surface has a pebbly appearance, 
with large units of different shapes, separated by 
deep, narrow spaces. This pattern becomes finer 
at the margins of the colpi and at the poles. The 
colpi in all three taxa are very narrow, with a 
smooth surface except in Myrceugenella which 
has a granular surface. 


(2) Syncolpate and parasyncolpate type 


In syncolpate grains, the colpi are either 
Straight, that is, meeting at the poles without 

coming wider, or curved where they are wider 
at the poles and form a triangular area. In para- 
syncolpate grains, the colpi bifurcate at the poles 
and their branches meet and outline a triangular 
apocolpium. Not all grains are strictly syncolpate 
or parasyncolpate; some are syncolpate on one 
pole and parasyncolpate on the other pole (i.e., 
syn/para), while others also combine with lon- 
gicolpate grains and result in long/syn and long/ 
para forms. These combinations were found in 
Myrtus communis, Psidium littorale, Eucalyptus 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


ficifolia (Fig. 42C, D), E. robusta, pu 
Eugena el- 


natalensis, Temu divaricatum, and 
liptifolia. The taxa included in the synodi dui 
parasyncolpate type are further grouped accord- 
ing to the presence or absence of intercolpar con- 
cavities. 

Pollen with intercolpar concavities. 
занин pollen examined | is oblate in geni 


4L 


ы апа elliptic] in shape. They : are ‘deh 
defined in Acmena smithii (Fig. 47B), Calliste- 
mon citrinus (Fig. 43B, D), C. teretifolius (Fig 
43A), Calothamnus validus (Fig. 43E), Eucalyp- 
tus ficifolia (Fig. 42C-E), E. robusta (Fig. 425) 
Heteropyxis natalensis (Fig. 42A, B), Melaleuca 
hypericifolia (Fig. 45A, B), М. rhaphiophylla (Fig 

45E), Tristania conferta (Fig. 41C, D), and Т. 


| (Fig. 41F). In Cleistocalyx operculata , 


ТА), Eugenia elliptifolia (Fig. 47D), Met- 
rina nervulosa (Fig. 41B), and M. poly- 
morpha (Fig. 41A) they xs not as и “де- 
pressed" as in the above mentioned taxa. In 
Acmena, Eucalyptus ficifolia, E. robusta, and 
Tristania lactiflua, the intercolpar concavities 

ave many punctae with fine, irregular channe 


|| 
[ 


Since the ` 


on a smooth surface while the sor; aras | 


of the mesocolpia are psilate. Sim ar surface 
sculpturing is present in Eugenia ER Б and 
Cleistocalyx. Melaleuca hypericifolia has a ver- 

rucate-granular surface in the intercolpar 007 
cavities and the surrounding areas are scabrate. 
In Callistemon teretifolius, C. citrinus, 
eropyxis, the surface of the ne is ad 
late, and it is are И in tercolpar 


43E) it is granular-verrucate in 
concavities and finely rugulate with fine c 2 
on the mesocolpia. In Metrosideros nervulosa 
M. polymorpha the intercolpar conca 
a е rugulate-verrucate surface. On ћете 
socolpia, it is finely rugulate in the former 
psilate in the latter (Fig. 41A, В). 

- FORM without intercolpar ¢ con 


мыз ЈА и 


ве Here, 


ийыш ae 


FIGURE 44. Scanning electron micrographs of Myrtaceae pollen.—A. Baeckea virgata. Su 


hier is psilate, P are short. —B. Н 
laustion microphyllum 


is pebbly, rugulate-verruc ate.—G. Pola 
F. Lateral view. The surface is smooth an 


omoranthus wilhelmii. some view showing a vas 


plateral view c Be 


d with pits. The colpus is short an 
Colpus is shorter than the lalongate, elliptic endoaperture below it 


. Scales anal 1 um. 


I 


cavities have ` 


view. Т | 
е surfa * | 


жа | 
| 


rA 
E 
a 
га 
< 
о 
У 
< 
ы 
Z 
< 
= 
О 
са 
[ 
е; 
О 
N 
Уз 
= 
ш 
је. 
m 
ш 
е 
A 
— 
< 
Z 
2, 
< 


ИУ 


) 


— TH ——" 


1984] 


grain. The surface in Myrtus communis (Fig. 48B— 
D), Psidium littorale (Fig. 46A-C), Eremaea 
pauciflora (Fig. 43F), Melaleuca preissiana (Fig. 
45D), and M. decussata (Fig. 45C) is similar: 
granular-verrucate-rugulate. There are fine, 
branched, irregular channels separating the sur- 
face elements. In M. communis (Fig. 48C), mi- 
nute lines and dots are seen on the surface ele- 
ments. 

The surface in Lurna chequen (Fig. 47E), Pi- 
lidiostigma glabrum (Fig. 46F), and Rhodamnia 
argentea (Fig. 48E) is verrucate-granular. In 
Luma, the colpi are curved and form a large thin- 
walled triangular area at the poles that has ir- 
regularly scattered verrucae and granules on it. 
In Pilidiostigma, at the yncolpate pole, scat- 
tered granules form a triangular apocolpium. The 
surface is smooth near the endoapertures in both 
of these taxa. In Rhodamnia, larger verrucate 
elements are present along the margins of the 
mesocolpia, even near the endoapertures. 

Austromyrtus bidwillii (Fig. 48F), Temu di- 


Present on the apocolpia. In Psiloxylon, the ru- 
gulate elements are larger on the equator. This 
genus has large apocolpia and differs from the 
rest of the parasyncolpate taxa in this respect. 
Eugenia capuli (Fig. 47C) has a slightly less coarse 
he te surface. In all the rugulate taxa, the sur- 
ace near the endoapertures is smooth. 

In TEM, the cross section of the Myrtus com- 
manis monad (Fig. 49C, D) shows that the end- 
e uniform except near the endoapertures 


m The thin foot layer has an irregular upper 
adl and is discontinuous. The short colu- 
ellae support а thick, infratectal granular layer. 


-S 


PATEL ET AL.—POLLEN CHARACTERS 


939 


The tectum is also thick, with an irregular upper 
margin, and shows many perforations. The sec- 
tion of the tetrad (Fig. 49A) indicates in places 
a discontinuous dome-shaped tectum with a 
granular layer below it. Figure 49B shows the 
fusion of tecta between two members of the tet- 
rad. 


(3) Brevicolpate and brevissimicolpate type 


In the brevicolpate grains the length of the 
colpi is equal to or less than the distance between 
their ends and the poles (Erdtman, 1971). In the 
brevissimicolpate grains, the colpus length is less 
than that of the underlying endoaperture (Erdt- 
man, 1971). Chamaelaucium uncinatum (Fig. 
44F, H) has brevissimicolpate grains. The sur- 
face is smooth with minute pits. The ends of the 
very short colpi are rounded. 


(4) Uncertain type 


Due to the lack of sufficient data the following 
taxa could not be assigned to any of the above 
pollen types. Baeckea virgata (Fig. 44A) and Os- 
bornia octodonta (Fig. 46G) appear to have 
curved syncolpi. However, they are often par- 
tially obscured or not well developed and then 
appear as short colpi which outline a faint tri- 
angular thin-walled area at the pole. Moreover, 
Baeckea appears to have intercolpar concavities. 
Homaranthus wilhelmii (Fig. 44B) and Thryp- 
tomene calycina (Fig. 44D) seem to be brevis- 
simicolpate. The surface is psilate in both taxa 
and Thryptomene shows a circular, thin-walled 
area at the pole. Balaustion microphyllum (Fig. 
44C) appears to be brevicolpate with a psilate 
surface and a circular, thin-walled area on the 
pole. Intercolpar concavities ma resent. 
Tristania nereifolia (Fig. 41E) differs from all the 
taxa of the family. The triangular pollen has 


— 


5 FIGURE 45, Scanning el 


crograph of Myrtaceae pollen. А, B. Melaleuca hypericifolia. — A. Sublateral 


Vi CETT] * -—- . А * 

*w. Distinct intercolpar concavities have a verrucate-granular surface. Elsewhere the surface is psilate. Colpi 

: pe (arcuate) and united at the pole.—B. View near the endoaperture.—C. Melaleuca сесим, Polar 
^ e fina 1 1 P3 + А + 44 e P" 22 s n 


contrast 


411101 111 


to | лла ти“ - “177 e r ۴ yd M m * б 
A the colpi are straight and united at the pole. Intercolpar concavities are absent.—D. Melaleuca КС. 


Polar view. 


Colpar (see A). Intercolpar concavities are absent. —E. М 
Concavities are not as distinct as іп M. Aypericifolia.—F. Psil 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


FIGURE 46. Scanning electron micro 
ofa m 


r view 
lucis чи Myrtaceae pollen. A-C. Psidium littorale.—A. ample) 101 
colpate and syncolpate grains are also present 1n 
etrahedra) tetrad (fourth grain is at E: back). — C. Surface — 
nular-verrucate-rugulate. D, E. Ugn iris . Late | 


· Colpi аге long. Note angular vader fe dedi nea 


the 
abrum. Polar view. The surface i 1S verrucate-rugulate. The arcuate colpi are бијен тел The apocol 


i 
) 


| 


——— 


1984] 


deeply concave sides. The surface is scabrate and 
the nature of the three apertures is difficult to 
interpret but the pollen appears to be triporate. 
Discussion 


Tea ће P е з Ре 


liography of myrtalean pal- 
ynology, Thanikaimoni (1984) lists only three 
references that allude to electron microscopy of 
Myrtaceae pollen, making it obvious that SEM- 
TEM investigations are greatly needed in the 
family, although, as discussed below, taxonomic 
investigations by Gadek and Martin (1981, 1982) 
are currently in progress. Since our intent in this 
study is the presentation of a broad overview of 
the Myrtales core families we shall not attempt 
à review of the extensive Myrtaceae pollen ref- 
erences, but shall only briefly mention a few of 
a recent/pertinent ones. The most com- 


4324 


| е g pe study was 
that of Pike (1956), which included 71 genera 
and 300 species from the southwestern Pacific 
area. Some of the conclusions reached from this 
Study were: 


(1) although the pollen in Myrtaceae is essen- 
ually uniform, in some taxa minor differ- 
епсеѕ make it possible to recognize particular 
genera or species; 
within the family (following Niedenzu’s clas- 
sification, 1893) “There appears to be no par- 
ticular feature that separates pollen of the 
Myrtoideae from that of the Leptos 
ideae, but pollen of the tribe Chamaelaucieae 
(placed by Niedenzu in the Leptospermo- 
Ideae) differs markedly from that of all other 
tribes in the family" (Pike, 1956: 46); 
within a tribe the taxa usually are similar, 
Myrtinae, Chamaelaucieae, but it 


— 
~ 
мї 


~ 
„ы 
мин 


Spermolepis, Leptospermum and Agonis, 
Baeckea and Balaustion, Wehlia and Pilean- 
thus. On the other hand, grains of widely 
Separated genera may show certain similar- 
ites, e.g., those of Regelia ciliata are difficult 
10 distinguish from those of some species of 
E ucalyptus, and those of Astartea and Agonis 
(4 mies similar" (Pike, 1956: 46); 
Brains of different species of the same genus 
are usually indistinguishable, e.g., Lepto- 
Suc ЕИН 


PATEL ET AL.—POLLEN CHARACTERS 


941 


spermum, or they may be similar in general 
features but show a comparatively large range 
in size, e.g., Eucalyptus. Rarely is it possible 
to make specific distinctions as in Regelia" 
(Pike, 1956: 47). 


McIntyre (1963) examined the pollen of 18 
New Zealand taxa and found that most genera 
could be recognized. Species within genera also 
could be recognized to some extent. As concerns 
fossil identification of Myrtaceae pollen, Mc- 
Intyre (1963: 104) stated: “There is little or no 
difference between the pollen grains of many gen- 
era of the Myrtaceae. Identification of living gen- 
era and species from fossil pollen, therefore, can 
only be reliable if there are no grains of similar 
type, from extinct genera and species, in the sam- 
ple under consideration .... When all factors 
are considered it is obvious that attempted iden- 
tifications of fossil Myrtaceae pollen on the basis 
of pollen characters of the indigenous species 
should be restricted to a period of time where it 
is reasonably certain that no other species or gen- 
era of the family were present... .” 

Most recently Gadek and Martin (1981) ex- 
amined the pollen of 28 species and seven genera 
of subtribe Metrosiderinae with light microscope 
and SEM. They found a greater range of pollen 
morphology within the family than was hereto- 
fore recognized and in some instances pollen 
could be identified to the generic and specific 
levels. With the SEM they were also able to cir- 
cumscribe three basic exine sculpture types: (1) 
Psilate to microscabrate, (2) microfossulate, and 
(3) microrugulate, rugulate. 

Lugardon and van Campo (1978) examined 
pollen of Tristania laurina and Myrtus com- 
munis with TEM and apparently encountered, 
at least with the latter, the same problem as we 
did, that is, a lack of staining contrast between 
the endexine and the foot layer. They described 
the thin, often discontinuous foot layer above a 
“white line" and a thick endexine below it as 
constituting the nexine. They further described 
an infractectal granular layer between the tectum 
and nexine but did not recognize columellae. In 
contrast, our section of M. communis (Fig. 49D) 
indicates very short columellae below the infra- 
tectal granular layer. This section also shows a 
distinct foot layer and endexine. The most de- 


~ 


10 be ed by scattered verrucate, granular elements. — С. Osbornia octodonta. Polar view. The surface appears 
ges Scabrate, colpi are short and at the pole form a weakly developed thin-walled triangular area. Scales equal 


942 


finitive TEM study is that of Gadek and Martin 
(1982: 75), in which pollen of Eucalyptus and 
Tristania were examined in great detail. Their 
general description for the pollen structure is as 
follows: “The species all show a typical angio- 
sperm exine differentiation consisting of two 
chemically different layers, an electron dense ekt- 
exine and a less dense endexine divided by a very 
thin electron-transparent lamella. They all differ, 
however, from the typical angiosperm architec- 
ture by the presence of a somewhat unstructured, 
nulate infratectal layer and the presence of a 
ш oe ib endexinous layer around the 
ores. Species differences relate to the granulate/ 
columellate organization of the infratectal layer; 
the extent or density of tectal perforations; and 
the КЕ and thickness ofa foot-layer around 
the 
Dekan (in Dahlgren & Thorne, 1984) re- 
gards both Heteropyxis and Psiloxylon as seg- 
regate monotypic families. Psiloxylon differs from 
other parasyncolpate taxa of Myrtaceae by hav- 
ing unusually large apocolpia and larger rugulate 
elements on the equator, but otherwise is similar 
to the rest of the family. Heteropyxis is not easily 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vo 71 


distinguished from other genera in the syncolpate 
and parasyncolpate group with intercolpar con- 
cavities. | 

In summary, Myrtaceae pollen as documented 
with SEM does not appear to have any close 
similarities to taxa from the other core families — 
of the Myrtales. Perhaps some superficial simi- 
larity exists with Onagraceae pollen but there iS 
no mistaking the two families. Erdtman (197!) 
suggests similarity to Lythraceae (perhaps through | 
Cuphea) but we have not been able to confirm 
it in this study. Furthermore, we do not have | 
sufficient data to compare Myrtaceae pollen with 
families outside of the Myrtales as suggested by | 
Erdtman (1971). It would be of interest to € — 
amine pollen of Cunoniaceae, Proteaceae, Lecy- 
thidaceae, and Sapindaceae in order to ch 
Erdtman's (1971) observations. Pollen of Lecy- 
thidaceae and Sapindaceae have been examined 
in SEM (Muller, 1972, 1973; Muller & Leen- 
houts, 1976; Mori et al., 1980) and are not sim- - 
ilar to Myrtaceae pollen. How in Sapin 
ceae there are several taxa tri ' 
parasyncolpate grains (Muller f pe 
1976). 


аи 


сапт; 1 


FIGURE 47. 


-— 


g electron micrographs of Myrtaceae pollen. —A. Cleistocalyx operculata. Subpolar ү = 


The psilat te surf: h t 


peli | 


В. Астепа doen Polar view. Surface i is psilate; punctae and channels are present in the intercolpar con surf 


(arro ow).—C. Eug 


is rugulate. Coli are united (i.e., syncolpate) but are obscured by 
the concave face usually has more distinct syncolpi.—D. Eugenia elliptifolia Sublateral view showing 


The psilate surface becomes coarser a 


—E. Luma 

nd has fine channels and puncta in the intercolpar concavities. pe of the 
chequen. Polar (upper) and “pie oe views. The surface is smooth to slightly coarse in the ed 
heidi he и! а а thin- | 


endoapertures. Toward middle p. 


area ч ise к that has pines and verrucae scattered over it. The colpi m ‘ews of Ш" 
eugenella apiculata. Lateral (left) йа subpolar (eight es equal 1 um. 


are syncolpate. — 


thin- 


thus 
ири oy полам и pollen. "The surface is granular-verrucate. Colpi are long. Scales 


jew of è 


Scanning electron micrographs of Myrtaceae pollen. —A. Temu divaricatum. Polar vi te. B-D. 


IGURE 48, 
parasyncolpate grain. Other colpi combinations were a 
Myrtus nad. A 


munis.—B. Polar view of a mo llc 


-granular. 
and at the pole. — Е. Austromyrtus bidwillii. Subpolar view. 


le. The surface is 
the same sample. ret cap о com 
sampl 


i are not united at this pole but diffe 


Large verrucate-rugul 


surface. 
w. Parasyncolpate ws rugulale 


The imei is formed by separate rugulate and verrucate elements. Scales equal i ve 


single e grain men through the three s iè 
ectal granular layer, pe: colume 

foot layer, and a well-developed endexine. The тате наан crograph of Lugardon mand уап 

(1978, Pl. 1, figs. 1—6) differs from C and D in that оса were not recognized. Scales eq 


punis. oe 
tectum (due 1 
е 


electron mi 


N 
24 
ш 
H 
5 
< 
T 
О 
РА 
u 
= 
= 
O 
T 
= 
< 
H 
E 
- 
m 
H 
< 
= 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


1984] 


PATEL ET AL.—POLLEN CHARACTERS 


E > 6 4 (а TO NP 
^ ~ P» е f uk ^ 


946 


The distinct SEM appearance of Myrtaceae 
pollen is countered by the TEM structure, which 
basically conforms with a typical post-and-beam 
organization of angiosperm pollen. The ‘granu- 
lar/alveolate’ endexine of Gadek and Martin 
(1982) does appear somewhat similar to Ona- 
graceae pollen but as further suggested by them 
it can also be found in other families, thus di- 
minishing the uniqueness of the character. Fur- 
thermore, the infratectal granular layer has been 
observed in a number of core families in this 
study 


ONAGRACEAE 


The scanning and transmission electron mi- 
crographs of Onagraceae pollen in Figures 50- 
63 and the data in Table 2 are intended as a 
general view of tl gy of the family 
(forthcoming studies with Nowicke & Praglowski 
will be more inclusive). Pollen characterized by 
a dominant central body (Praglowski et al., 1983) 
with markedly protruding apertures is typical of 
Fuchsia (Fig. SOA, B), Circaea (Fig. 50C, D), 
Clarkia (Fig. 52A, B, D), Gaura (Figs. 52H, 53 
A, B), Heterogaura (Fig. 54A, B), Calylophus (Fig. 
55А, B), Stenosiphon (Fig. 55E), and Oenothera 
(Fig. 56A, C). In comparison, the apertural pro- 
trusions are less pronounced in Xylonagra (Fig. 

E, F), Camissonia (Fig. 57), Ludwigia (Fig. 
58F, H), and Hauya (Fig. 50E), while in ач 
(Fig. 51A, B, D, G), Gayophytum (Fig. 53E, F), 
Gongylocarpus (Fig. 56D), Boisduvalia (Fig. 58A), 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


and Epilobium (Fig. 59A, В, E, J), the apertures 
are non-protruding. These latter genera, partic- 
ularly Lopezia (Fig. 51A, D), have a triangular 
outline in polar view. While most Onagraceae 
pollen is three-aperturate, that of Fuchsia (Fig. 
50A) is also characteristically two-aperturate in 
certain sections (Praglowski et al., 1983; No- 
wicke et al., 1984). Four-aperturate grains, as 
depicted for Lopezia (Fig. 51G) and Heterogaura 
(Fig. 54B), are less commonly represented, al- 
though occurring in many genera of the family. 
Most genera of Onagraceae shed their pollen 
exclusively as monads, but some also shed the 
pollen in tetrads or polyads. Pollen tetrads char- 
acterize Boisduvalia (Fig. 58A), most species of 
Epilobium (Fig. 59E, J), and some species of Ca- 
missonia (Fig. 57A, F-H) and Ludwigia (Fig. 584, 
F). In Epilobium brachycarpum (E. panicula- 
tum), most individuals shed their pollen as mo- 
nads (Fig. 59A, B), as do all species of sect. 
Chamaenerion (cf. Raven, 1976), while a few 
individuals are known to shed the pollen in tet- 
rads (Fig. 59E), as do all other species of Epi- 
lobium. Polyads are found only in some species 
and sections of Ludwigia (Praglowski etal., 1983), 
including L. longifolia (Fig. 58H) in this ed 
The internal bridges (Fig. 58G) connecting 
jacent tetrad members and the external bridges 
(Fig. 581) connecting adjacent tetrads appear 
identical to each is as well as to their respec 
tive exine surface volt 
All taxa except ME alpina subsp. imal s 
(Fig. 50D) are characterized by long ektexino 


FIGURE 50. Scanning apnd micrographs of Onagraceae pollen.— A. Fuchsia thymifolia subsp. 


— 


ћуте а 


Oblique lateral view with viscin threads associated with the proximal (top) pole. The arrow indicates 
area of threads showing a se seis) 
This two-aperturate condition is characteristic for the ir 
species of Fuchsia.—B. F. michoacanensis. Apertural p with crack extending from pore (at (al 
the central body. The arrow indicates endexine lamellae. T d-like to ei 
rugulate) elements. 7O Circaea cordata. Portion ofa pollen grain with apertural protrusion nanda l q. Lateral 
viscin thread. T ular and rod-like elements. — D. C. alpina subsp. — yx 
view showing = apertural protrusions. Note that the bo is essentially i: isopolar and in the absence termine 
threads (C. alpina is the only taxon in the On if not impossible, tO 387). Tw? 
the distal and proximal poles. E, F. "Two collections of Hauya elegans subsp. elegans. —E. (Mora QE hsia (A) 

pollen grains in proximal polar view showing masses of viscin threads. In contrast to the pollen of Fuchs? 
and Ci ircaea (D) the apertural protrusions are considerably less prominent.- —F. (Reno 9294). Two P nal 

p consists of several iden 
threads aligned in parallel fashion. Attachment with the globular elements of the uat e surface is partially 
in the thread group at the right. С. Н. elegans subsp. barcenae. зар of a fractured pollen grain e 
spongy ("paracrystalline") ektexine (ek) and solid, dense endexine (en). The short, irregular ex tente 
lower margin of the ektexine are columellae (see Fig. ки sa The slightly lamellate upper wee of D d 
suggests a foot layer but it has not been con transmission electron microgra of processint 
е (ѕее ty ел The separation of ektexine бош endexine is artificial, probably a e я 
5 equal 


protrusion is visible at the upper left. 


v 
га 
[s 
= 
E 
« 
X 
Q 
Z 
ш 
- 
- 
О 
1 
J 
< 
H 
55 
= 
5 
> 


TABLE 2. Summary of pollen characters in Onagraceae.* 


Columellae/ 
Apertural Tectum Endexine 
Pollen Type Protrusions Viscin Threads Surface Texture Columellae С «се Granularity 
M TIT Р Р NP BEB SM B Е IC IC G R-ERUG P F I A + TT T P NP МЕ 
Fuchsia + $ + (9 oT (9 + + 
Lopezia + т ay +t + + (+) 3 + 
сае + + + Ж р 

Сатіѕѕопіа + + + (+) t + + T 7 

Xylonagn + + * + (+) 12 + + 
Gongylocarpus + + + + + + SE + 
Gayophytum + + 4 т + + * E 
Hauya + + + + + + + 
Calylophus + + + + + + + + 
Gaura + + + + (+) + + + 
Heterogaura + + + + + + 
Clarkia + + + ко + + 

enothera т + + Qro + + + + 
Stenosiphon + + + + + + + + 
Ludwigia Ty T F t + + т + 
Boisduvalia + + + + + + + + + + + 
Epilobium + + + то + T ^4 EF + To X + 

а The data apply id the taxa listed in cate 2 Parentheses indicate that this observation was less common. Abbreviations for each category are: 
Pollen type: M (monad), T (tetrad), P (po 

Apertural Potro ions: P (prominent), m At: prominent), BCB (apertural protrusions blend into central body). 

Viscin threads: SM meet B (beaded), R (ropy), TC (tightly compound), IC (incised compound). 

Surface веза G (glob R-E (rod-like to pou ), RUG (rugulate), P (porous underlying sheet). 

e: P (prominent, | oe A (ab 
ин umellae and “sad approximately equal), C > T (columellae of greater thickness than tectum), C < T (tectum of greater 


thickness a а мч 
Endexine granularity: Р (prominent), NP (not prominent), NE (not evident in this study). 


8t6 


МУАЗУО 'IVOINV.LOS ІҸПОЅЅІИ JHL ЧО STVNNV 


IL 10A] 


PATEL ET AL.—POLLEN CHARACTERS 


Ficu URE 51. eae ы ezia) pollen. А—С. L. racemosa subsp. га 
Scanning electron micrographs of Onagr porn ( E —C. Surface detail showing tightly packed 
r more threads are often united at the exine surface. Rarely a beaded-granular surface 
cated ree the two ~“ unite. ‚ longifolia.—D. Polar surface containing numerous 
obably Ubisch bodies. These bodies seem to be most commonly associated 
бине Ла viscin threads аге absent when Ubisch bodies are present.—E. Enlargement 
h bodies and the exine is smooth rather than the more typically beaded 
emphasizing the dense paracrystalline prm (cf. Fig. 50G of 


isc 
4 

ам ance of Lopezia.—F. ono grain 

Уа).—С. 4-aperturate pollen grain. Unless indicated otherwise, the scales equal 1 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


B 


ни 000 


j 


| 


| 5 


1984] 


strands or viscin threads on the proximal polar 
face (Hauya, Fig. 50Е; Lopezia, Fig. 51A; Clark- 
ia, Fig. 52А, B, D; Саига, Fig. 53B; Gayophy- 
tum, Fig. 53E; Xylonagra, Fig. 54F; Stenosiphon, 
Fig. 55E; Gongylocarpus, Fig. 56D; Camissonia, 
Fig. 57C; Epilobium, Fig. 59B). In thin section 
it is clear that they are extensions of the exine 
surface (Fuchsia, Fig. 60A; Camissonia, Fig. 61A; 
Gaura, Fig. 62A; Clarkia, Fig. 62D; see also 
Skvarla et al., 1976) 

The threads have different surface patterns: 
smooth (Circaea, Fig. 50C; Clarkia, Fig. 52C, F; 
Gayophytum, Fig. 53H, I; Heterogaura, Fig. 54C; 
Boisduvalia, Fig. 58E; and Ludwigia, Fig. 58F, 
H, I); segmented (Hauya, Fig. 50F; Lopezia, Fig. 
1С; Gaura, Figs. 52E, С, 53C, Р; Gayophytum, 
Fig. 536; Calylophus, Fig. 55C; Oenothera, Fig. 
56B, E; and Camissonia, Fig. 57E); tightly com- 
pound-twisted (Stenosiphon, Fig. 55F; Boisdu- 
"alia, Fig. 58C; and Epilobium, Fig. 59F, H, 1); 
me incised-compound (Epilobium, Fig. 58B). As 


y (Skvarla 
et al., 1978), some patterns are difficult to cate- 
gorize and may represent intermediate or tran- 
sitional forms. For example, the obliquely in- 
clined segmented-beaded threads of Fuchsia (Fig. 
50А), Xylonagra (Fig. 54D), Gongylocarpus (Fig. 
360), and Camissonia (Fig. 57E) can also be 
considered as segmented-ropy. Sections through 
к. at (Figs. 60E, 61G, 62E, 63G) sup- 
the morphological patterns. Lopezia longi- 

p (Fig. 51D, E) commonly has prominent 
нео Particles on the polar face. These par- 
be may represent Ubisch bodies. They have 
s П observed most frequently on Lopezia pol- 
n, particularly in certain collections of L. lon- 
€ s hen they occur, viscin threads are usu- 


Pk: Must be stressed that we consider the viscin 
"a2 to be an integral part of the pollen grain 
; namely, the ektexine, and have document- 


PATEL ЕТ AL. —POLLEN CHARACTERS 


951 


al., 1984). The phrase “attachment point(s)” was 
used to indicate the specific area on the exine 
surface where the threads emerge. The area is a 
simple transition from ektexine surface elements 
to individually protruding threads or an enlarged 
region with several emerging threads. We now 
recognize that this phrase can be misleading and 
might be interpreted to mean that viscin threads 
are not an inherent part of the exine and instead 
are a later addition. Viscin threads form along 
with other exine units, as has been shown in 
developmental studies dating to the early twen- 
tieth century (Beer, 1905; Bowers, 1931). In or- 
der to avoid any existing or potential confusion, 
perhaps “attachment point(s)” should be re- 
placed by a more appropriate syntactic unit such 
as “emergence area," “extension area," etc. 

While viscin threads are evident in Onagraceae 
and some Ericaceae (Skvarla et al., 1978), equiv- 
alent structures have also been suggested in Le- 
guminosae (Cruden & Jensen, 1979; Graham et 
al., 1980). In certain species of Caesalpinia and 
Delonix, randomly located strands termed “‘ex- 
inial connections" link pollen grains, and al- 
though they are without free ends they are thought 
to be similar to viscin threads and to facilitate 
pollination (Cruden & Jensen, 1979). In pollen 
of Jacqueshuberia, the linkages are markedly 
longer and fewer. They are considered to be vis- 
cin threads and to indicate an adaptation to en- 
tomophily (Graham et al., 1980). Recent study 
(Patel et al., 1985) of Jacqueshuberia threads 
shows that the thread ends are attached to dif- 
ferent pollen grains, therefore indicating that they 
are long exinial connections rather than viscin 
hreads. 

Hesse has published a series of papers (sum- 
marized in Hesse, 1981) reviewing the well- 
known subject of pollen cement in Angiosperm 
families. He contrasts "pollenkitts" and "try- 
phine," the sticky, viscous, lipid-carotenoid ad- 
hesive substances that are synthesized in in the ta- 
petum (i.e., by plastids or ) 


+ 


M relationship clearly (Skvarla et al., 1975, 
1978; Praglowski et al., 1983; Nowicke et 
— и 

FIGURE 52. 
A Proximal ааа roel micrographs о 

15011 threads, 
Clements, B,D unguiculata.—B. Proximal polar 


a енед (top) pole (compare with C. alpina subsp. ма. Fig. 500). — 
иға lindheimeri. The viscin 1 threads are ri 
G 


9f exine sy 
beaded. Th ce and smooth viscin .—E. Ga 


Џеп. A, С. Clarkia speciosa subsp. speciosa. س‎ 
ooth 


y 
G mutabilis. _ 


yg wee" T 


CICE 


hart 


Dn beaded viscin threads. — Н. 
9f lamellar endexine within the protrusion. Unless sentir otherwise, the scales equal 1 um. 


ЈЕ 
i 7 
~ 
49 
ч | 
x ~ >. Ё. 
ъч : 
LS ie ` 
W 
———— 
—— 
у 
8 E 0 ographs of O 
О C аре а DIO O B 
aded ads and e : |; 
: à рто а! pola 
О О nezia aris " 


am 
^ 


э & 


E >. 1 У E ж у А, 
“м de E 
е бф ы. 
и 


~ 


ola 
роја 
аа 


PATEL ET AL.—POLLEN CHARACTERS 


10pm 


FIGURE 54, Scanning electron micrographs of к, dene. A-C. Heterogaura heterandra. — А. Dist 
Polar view... B. 4-a perturate pollen grain in proximal polar v w.—C. Smooth viscin threads with forked олн 
and a highly qo exine pr n pically semen rize би месне face. D-F. Xylonagra arborea subsp. 
vugginsii —D. Groups of twisted (segmented-ropy) viscin threads. — E. Distal polar face. —F. Proximal polar 
urface. Unless nosed gen the scales equal 1 um. 


‚о си 


— 


с пети: (Cresti et al., 1983). E, G, I. Gayophytum ramosissimum. —E. Proximal polar view.—G. A p 

ћ а branched viscin thread. In comparison. я with other areas of this thread which are ete (not rele 
ere), this area is segmente i y).—I. Three viscin threads (see E) extending from an exi ine surf 
ee 


э рост view 
oa ‘ous s short threads, ‘some appearing as ову твар off exine 
pos or striae (not illustrated e also have been noted along with normal threads. Unpublished 
Uni t that G. micranthum may also possess segmented- сива threads (as shown for G. ramosissimum). 
ess сама otherwise, the scale equals | um 


954 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


20 istal pola! 

FIGURE 55. Scanning electron аи of Onagraceae pollen. A-D. Calylophus toumeyi. ts А ж, 
view.— B. Lateral view.—C. A group of beaded viscin threads extends from a surface which cons? is d 

elongate elements.— D. Pore region showing internal construction of irregular sporopollenin a AE 


been peeled away leaving broken columellae on the endexine. Within the pore is lamell 
Stenosiphon linifolius.—E. Proximal polar view with three groups of viscin threads. —F. En rface. Unless 
showing smooth-twisted (tightly n) viscin threads on a globular to rod- like polar su 

indicated otherwise, the scales equal 1 


tt 
FIGURE 56. Scanning electron micrographs of Onagraceae. A, B. Oenothera brachycarpa. се ot up 9 


A gro 
similar Е Circaea alpina subsp. imaicola Fi 50D d Clarkia un iculata Fig 52D).—B. ments 
segmented-beaded viscin threads extends e Я а bum уан globu lar coe ы 
e 


E. O. texensis.—C. The pollen grain is collapsed as well as fractured. The uber protrusio 


PATEL ET AL.—POLLEN CHARACTERS 


mostly covered b 
Rand 


ans subsp. barcenae, Fig. 50G). Sev d viscin threads are on the surface of the 

. Gongylocarpus rubricaulis (Sharp 44846). Proximal polar view showing mass of viscin threads. 
other Onagraceae taxa, apertural protrusions are considerably less conspicuous. — F. G. fruticulosus 
. View of exine composed of short rod-like and globular elements of variable sizes. Unless indicated 
€ scales equal 1 um. 


Otherwise. th 


956 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


or as tapetal breakdown products (Dickinson, threads approach the ektexine when it is almost 
1973; Dickinson & Lewis, 1973), with viscin completely formed and fuse with the surface. He 
threads, which he considers to be non-sticky, non- further postulates that the viscin threads arose 
viscous, and att аз He regards as a chance mutation 

their d lar ma- Sculpturing of the exine surface is also variable 
trix of the anther асл аї the same time that throughout the family and is illustrated by glob- 
an ektexine is developing on matrix-encased mi- шаг elements (Hauya, Fig. 50F; Lopezia, Fig. 
crospores. Hesse (1981) shows transmission elec- 51С; Clarkia, Fig. 52F; Саига, Figs. 52E, 53C, 
tron micrographs in which he states that the Р; Heterogaura, Fig. 54C; Xylonagra, Fig. 54D; 


=} 


FIGURE 57. Scanning electron micrographs of Onagraceae о pollen. A, B, D, Е. С. arenaria.- 


A. Tetrad (unacetolyzed) which i is p artially disrupted at two apert s. The arrowhead designates the н 
containing the exine fragment (i.e., *spur" of Skvarla et al., 1975) 
y an arrow.—B. E ement of spur in A. The abundant ipn structures are the columellae which line M 


aperture protrusion. Also evident is a beaded viscin thread. — 
structure at the junction of the central body and apertural ecd. ion.—F. Acetolyzed tetrad. The arrow nicae 
a partial disruption in one aperture геріоп. C. C. tanacetifolia subsp. tanacetifolia. Monad pollen gr: 

merous viscin threads extend from different areas of ls колоч polar face. E, С. С. ew рм 
robusta. —Е. The viscin threads are primarily beaded-ro w are also лав (see Skvarla et al., 1978).— 
G. Intact tetrad (acetolyzed).—H. C. vele ie n pale oc Intact tetrad (unacetolyzed). Unless 
indicated otherwise, the scales equal 1 


FIGURE 5 hs of O —А. Вог lia stricta. View of tetrahedral 
nd ides all four | Mes members. ‚Н, С; ЕР у pan These three canines electron micrograph 
represent different collections and illustrate the diversity in viscin thread morphology which oc 2099 
іп some Onagraceae taxa. In В (Piper s.n.), the morphology is clearly incised-compound, іп С (Thompson 50%), 
t appears as tightly compound-twisted, and in E (Piper s.n.), | is smooth (see Skvarla et al., 1978 for d 

discuss In all three examples, the associated exine surface appears to be rugulate-perforate. D,G.L 
goiasensis. — D. The tetrad (fourth pollen member is not visible) is part of a polyad and is surrounded by ar 
of other tetrads. The bracketed area is enlarged below in G. Arrowheads indicate colpi.—G. Enlarge seg оя 
bracketed area in D showing internal bridges (arrows) between adjacent pollen grains of the te 


of the globular club-like structure associated with one of the bridges is unkn ut may be related or of a 
threads. The star represents union of adjacent pollen grain ape F. L. alternifolia "Three еш : 
iue ‚Пе large open arrows indicate prominent meridional Tidges characteristic of seve al Li ntrast 
and whic ith t ; 


joir W the 
to L. goiasensis (D) and L. "longfolia (H) the meridional ridges are best developed in L. alternifolia Mes L 


equatorial ridges are of equal prominence in all three species. The short, solid arrows 5 show 5 
longifolia. —H. Overall view of a polyad with basic tetrad composition. Arrow indicates an s Tends pi.—! 
connects adjacent үчин tetrad | pollen surfaces and main ntains polyad unity. Ато мин indicate «л 
External bridge (not from Н) scin threads. Une 
otherwise, the scales pie’ 1 um. 


FIGURE 59. Scanning electron micrographs of Onagraceae (Epilobium) ee A-D. E. bral “м 


In distal polar view the pollen outline is nearly circular. The surface is composed of numerous ran е oni 
short rod-like elements.—B. Viscin threads 5 (smooth and incised pain У see Skvarla | е al 197 hid 

from the center of the proximal polar indue o ye које 
Тће асе 5 тоге со the equator and consists of rod-like or rugulate Semen (ede 
Skvarla et al., 1978, Pl. 45). The тепе of the proximal polar асе is also composed of rod-like e rod-like of 
elements but they are not dense d.— ed view of exine surface showing that © channeled 


rugulate elements are underlain by a highly porous layer or sheet.—D. Fractured exine showing eh 
endexine сосе by a bracket) and а “columellae” layer composed of randomly arranged Lapse 
(arrows) w ich appear to be vertically oriented. The tectum is a continuous porous sheet (see О 


of tetrads.—E. А tetrad.—F. Smooth and incised compound viscin threads occur on a surface pue D).- 
50B.—G. View of fractured exine surface. The arrows indicate the (— ме as described above Vr att 


| 
| 


eh oe a 


H. E. glaberrimum. This vie of a viscin thread (tightly o origins | 


from an exine bridge connecting adjacent members of a tetrad.—I. Е. rigidum. Numerou A exine brio 


ig e morphology kvarla et al 
48).—J. урне ee as the viscin thread at the left margin (see see also de mec (arrows): 


nid designated otherwise, the : scales equal 1 um. 


эы Ra] 


PATEL ET AL.—POLLEN CHARACTERS 


PATEL ET AL.—POLLEN CHARACTERS 


60 I F 
9 ANNA 
SO 
THE M I Al 
I 
SSOURI BOTANI 
/ CAL G E [V 
ARD 
N 
OL. 71 


tion 4! 
to the 


has be 
en i 
clearl =. 
а ed). It i 
а tis ve 
es the Û an 
| а ilar t 
ча о the 
t oie d ve 
жазынан ule S бшедь 
nc elegans sub 
| not clearl р 
y distingui pe 
guished ause 
. b ня 


1984] 


and Camissonia, Fig. 57D); rod-like or elongate 
elements (Fuchsia, Fig. 50B; Boisduvalia, Fig. 
59C); rugulate or coarsely elongate elements 
(Fuchsia, Fig. 50B; Boisduvalia, Fig. 58B, C, E; 
Ludwigia, Fig. 58F, С, I; Epilobium, Fig. 59G); 
and combinations of globular and rod-like elon- 
gate elements (Circaea, Fig. 50C; Clarkia, Fig. 
52C; Gayophytum, Fig. 53H, I; Calylophus, Fig. 
55C; Stenosiphon, Fig. 55F; Oenothera, Fig. 568; 
Gongylocarpus, Fig. 56F; and Epilobium, Fig. 
591). As discussed for viscin threads, some of the 
patterns are difficult to precisely categorize and 
therefore are amenable to considerable subjec- 
tivity. For example, slightly enlarged globular 
elements could be interpreted as rod-like to elon- 
gate, and extension of the latter could be inter- 
preted as rugulate. Obviously, it is more impor- 
tant to be cognizant of these differences rather 
than being overly concerned with their exact cat- 
egorization. Similarly, there should be no conflict 
when other descriptive terms— granular for glob- 
ular and vermiculate for elongate and rugulate — 
are employed (Daghlian et al., 1984). Frequently, 
the surface elements are underlain by a highl 
perforate sheet or layer (Lopezia, Fig. 51C; Gaura 
lindheimeri, Fig. 52E; Oenothera, Fig. 56B; Bois- 

duvalia, Fig. 58B, C, E; Epilobium, Fig. 59C). 
Other surface features of significance are the 
long colpi and prominent ridges in Ludwigia (Fig. 
58D, F, H). The latter are of two types: meridi- 
onal ridges, which occur over the polar faces and 
extend to the “equator” in the area midway be- 
- th І 1 protrusi , and lateral ridges 
Which occur between the apertural protrusions 
and are joined with the meridional ridges (L. 
alternifolia, Fig. 58F). Of the two, the lateral ridges 
m to be the most consistent. In contrast, the 
meridional ridges are prominent in L. alterni- 
f olia (Fig, 58F) but poorly developed in L. goia- 
sensis (Fig. 58D) and L. longifolia (Fig. 58H). 
55А) Colpi also were noted in Calylophus (Fig. 
i, although of less prominence than in Lud- 
М нуд structure as observed in TEM as well as 
Р "-—. grains in SEM (Figs. 50G, 51F, 56E, 
2 is D, 59D, G) indicates that it is composed 
а network of spongy-paracrystalline ektexine 
чы: а dense, uniform endexine that frequently 
Fi veu gr anular, basal component (Ludwigia, 
él р Camissonia, Fig. 61А; Xylonagra, Fig. 
6 3D ongylocarpus, Fig. 61H; Epilobium, Fig. 
~ ) and less frequently an irregular upper sur- 
i iri 60B, D, F, 62D, 63E). The ektexine 
Out a foot layer and the columellae and 


са 


PATEL ЕТ AL.—POLLEN CHARACTERS 


961 


tectum units are not always clearly recognized. 
Several ektexine structural patterns are evident. 
In Hauya (Fig. 60C), Camissonia (Fig. 61A), Lo- 
pezia (Fig. 61B), Xylonagra (Fig. 61C), Calylo- 
phus (Fig. 61E), Gaura (Fig. 62A), Stenosiphon 
(Fig. 62F), and Epilobium cylindricum (Fig. 63F), 
columellae and tectum are evident. In Fuchsia 
(Fig. 60A), Ludwigia (Fig. 60B), Circaea (Fig. 
60D), Gayophytum (Fig. 61D), Heterogaura (Fig. 
62C), Clarkia (Fig. 62D), and Boisduvalia ma- 
rantha (Fig. 63A, B), columellae and tectum are 
absent and the ektexine is composed of the 
spongy-paracrystalline-beaded sporopollenin 
network. In fractured exines of E. brachycarpum 
(Fig. 59D, G), this network appears to consist of 
porous sheets. Clarkia (Fig. 62D) is further dis- 


endexine and their subsequent union in the aper- 
tural protrusions. In Gongylocarpus (Fig. 61H), 
Oenothera (Fig. 62E), Boisduvalia densiflora (Fig. 
63C), Epilobium hirsutum (Fig. 63E) and E. col- 
linum (Fig. 63G) extremely short columellae are 
present, although this is a highly subjective in- 
terpretation and it may be more accurate to re- 
gard this group as transitional. It is clear that 
Onagraceae pollen does not possess typical col- 
umellae, if indeed any columellae at all, and it 
might be more useful to consider the ektexine to 
be without them. This lack of columellae, cou- 
pled with the absence of a tectum and foot layer, 
leads to an interpretation of the Onagraceae ekt- 
exine as being without the tripartite units that 
characterize Angiosperm exines. 

Also subject to redefinition is the layer we re- 
gard as endexine. Whereas in previous studies 
we defined as endexine the dense, massive layer 
underlying the spongy-paracrystalline ektexine, 
we now might redefine it as the foot layer to the 
ektexine. Support for this interpretation can be 
found in the aperture protrusions, where the so- 
called endexine has the spongy-paracrystalline 
appearance of the ektexine (Figs. 60F, 61F, 628), 
and indeed is continuous with it (see also Skvarla 
et al., 1976; Nowicke et al., 1984). By this in- 
terpretation the narrow, granular layer that was 

ded as a basal endexine component is now 
the endexine. The endexine in Onagraceae pollen 
would be defined then as extremely narrow, spo- 
radic, and best developed in the apertures where 
co granul ident (Nowicke et 1984). 
We do not necessarily support this explanation, 
but discuss it as an illustration of the complexity 
and multiplicity of interpretations amenable for 


962 ANNALS OF THE MISSOURI BOTANICAL GARDEN [VoL 71 


It is apparent from observation of the exine chamber is remarkable in that lamellae line the 
sections in Figures 60—63 that there are differ- entire chamber. Grains fractured through the 
ences in the texture of ektexine sporopollenin apertural protrusions also clearly show these 
network. Fuchsia (Fig. 60A) has a coarse, irreg- endexine lamellae (Fuchsia, Fig. 50B; Gaura, Fig. 
ularly shaped network while Clarkia (Fig.62D) 52H; Calylophus, Fig. 55D). 
has a considerably finer network, and in Bois- Table 2 summarizes some of the pollen wall 
duvalia (Fig. 60A, B) the network appearstocon- characters of Onagraceae discussed above. 
sist of finely connected beads and porous sheets. 
This has yet to be critically analyzed. Perhaps 


this type of study, in conjunction with analysis эжинин 
of ektexine **porosity," would be of value in dis- Onagraceae pollen has been the object of stud- 
tinguishing the various taxa. ies using light (Mitroiu, 1961-1962; Ting, 1966; 


In the apertural protrusions, the apertural Brown, 1967) and electron microscopy (Skvarla 
chamber is usually overlain by spongy ektexine еї al., 1975, 1976, 1978). These studies have 
and underlain by thick layers of endexine la- shown that the pollen of the 17 genera and ap- 
mellae (Circaea, Fig. 60F; Calylophus, Fig. 61F). proximately 650 species possess the following 
The lamellae usually have fine channels and a distinctive features: viscin threads, a spongy- 

pongy-r similar to the  paracrystalline ektexine, apertural protrusions, 
ektexine. In Gaura (Fig. 62B), the apertural and a large central body; tetrads and/or polyads 


ENSE 


= 
FIGURE 61. Transmission electron micrographs of Onagraceae pollen.— A. Camissonia arenaria. View û | 
proximal face showing origin of viscin thread from the ektexine surface. Paracrystalline co umellae are broad 


and nearly as thick as the es paracrystalline t tectum. The lower ` margin of the endexine is compat ы | 
р 


an irregular granular sheet.—B olumellae are less 


than in C. arenaria.—C. X: yox arborea subsp. wigginsii. View at center of either the polar or lat e НИ | 


Pollen of this taxon is typically characterized by an irregular granular component at the lower pod 
endexine. —D. Суорун micranthum. View at center of distal polar face. Columellae are absent Section 
ektexine is in direct contact with the endexine. E, F. Calylophus berlandieri subsp. berian aa 
through center of either] lateral or polar face. Columellae development is somewhat intermediate d p з 
(В) апа Camissonia (А). Е. Section through aperture chamber. Note similarity to r: [^ 
dissimilarity to Gaura (Fig. 62B). G, H. ова rubricaulis (Davidse 9790).—G. Secti 


, 


viscin aci showing the segmented-ropy morphology.—H. Columellae are only slightly developed. San | 
ти! lu 


FIGURE 62. Transmission electron micrographs of Onagraceae pollen. A, B. Gaura coccinea. a 
proximal face. Note short columellae and viscin thread origin from the ektexine.— B. Section throu Hetero 
protrusion. Note close similarity to fractured apertural protrusion of Gaura mutabilis тч 61D) D Clarkia 

р ig. on 


Suggests a faint “outpocketing. ”—Е. Oenothera serene Se: at Sese face showing mark LF. St edly ш, 


— Section through center of either the polar or Зна face. Long, slender columellae are pro 


of a second pollen grain. The viec is composed of thin, beaded, porous piti we "Sky arla et 
Pl. 8D, Е, 9C, F).—B. Section through the center of a lateral face. Note the characteristically y highly € 


2E Section at jj geh 
£ h 2 Г. t 1 уз \£ 2: 41 Le : се с endexine 


upper ao if this irregular g 


beneath the area of viscin threads may ‘represent “outpocketing”’; е. it is not clear if 


actually a portion of the ektexine.—F. E. cylindricum. Section beneath aperture protrusion showing rr | 
јоп. — eee 
U 


otherwise, the es equal 1 ш 


minent. Scales | 


— A. Section 3! | 


pa ra | 


] 


ЕРЕ 


1984] 


PATEL ET AL.—POLLEN CHARACTERS 


964 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


PATEL ET AL.—POLLEN CHARACTERS 


965 


966 


in certain groups; and an exine surface composed 
of circular, globular, and elongate or rod-like ele- 
ments. Prior to this study our feeling was that 
Onagraceae pollen was unique in the angio- 
sperms, being easily recognizable and difficult to 
confuse with other groups. After this survey of 
Myrtales pollen our ideas have not changed: 
Onagraceae pollen morphology is distinctive in 
the order. In a remote sense—that is, by consid- 
can Lu age ae oe 


turing, and protruding apertures—the pollen of 
Ludwigia resembles Trapa (see discussion in 
Trapaceae), although there are no difficulties in 
recognizing these taxa. A distant similarity be- 
tween Myrtaceae and Onagraceae pollen exists, 

particularly in those grains having short colpi 
(compare Hauya, Fig. 50Е; Gongylocarpus, Fig. 
56D; and Boisduvalia, Fig. 58A; as well as Lo- 
pezia of Skvarla et al., 1976, with Myrtaceae 
SEM on Figs. 41—48). In addition, cross-sections 
of the subsidiary colpus of Sonderothamnus (Fig. 

26C, D) of Penaeaceae show a remarkable sim- 
ilarity to those of some taxa of Onagraceae hav- 
ing the spongy ektexine residing directly on the 
endexine. Lastly, although meridional ridges have 
been observed on Ludwigia pollen (L. alterni- 
folia, Fig. 58F), there is no confusing this genus 
with other taxa in the Myrtales also possessing 
meridional ridges. 


SUMMARY AND CONCLUSIONS 


Based on pollen morphology, the families that 
are considered to be the core members of the 
Myrtales (Dahlgren & Thorne, 1984) form a rel- 
atively cohesive group with the exceptions of 
Trapaceae, Myrtaceae, and Onagraceae. Each 
family is summarized below. 


1. Lythraceae. The taxa examined from this 
family show the greatest amount of variation in 
pollen morphology in the entire order, with di- 
versity evident at all levels: (1) shape (in lateral 
view: oblate-suboblate, spheroidal-subprolate, or 


~ 


or circular); (2) apertures (tricolpoidorate, tri- 
colporate, tricolporate-syncolpate, or porate); (3) 
subsidiary colpi (0, 3, or 6); (4) sculpture (striate, 
striate-spinulate, psilate, or verrucate e-rugulate); 
and (5) structure (normal ektexine-endexine lay- 
ers, highly reduced or complex columellae). Pu- 
nica granatum (subfam. Punicoideae) is similar 
to Lagerstroemia (Lythroideae) in the triangular 
shape (polar view) resulting from three meridio- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


nal ridges. Punica protopunica has faint subsid- 


iary colpi, meridional ridges and apertural fields, 
and thus resembles Crenea (Lythroideae). Son- 
neratia (subfam. Sonneratioideae) and Duaban- 
ga (subfam. Duabangoideae) are characterized 
by meridional ridges and apertural fields (true 
subsidiary colpi are absent). Sonneratia is sim- 
ilar to Lafoensia (Lythroideae), and Duabanga 
to Diplusodon (Lythroideae). 

2. Trapaceae. This family is unique in hav- 
ing colpi hidden within the protruding, swollen 
aperture domes of sharply triangular 
(in polar view) and in having three meridional 
ridges that are united at the poles. The ridges 
pass over the apertures and in this respect, a 
well as in structure, they differ from the meridio- 
nal ridges found elsewhere (e.g., in Lafoensia, 
Lagerstroemia, or Ludwigia). Trapa remotely re- 
sembles Ludwigia (Onagraceae) in having a gran- 
ular-beaded surface sculpture, an 
in general in exine structure (very thick endexine 
and indistinct foot layer and columellae), but 
overall Trapa is sharply distinct from Onagra- 
ceae and from other Myrtales. One sample of T. 


pollen grains | 


natans showed linked pollen grains indicating | 


possible polyads. 
3. Oliniaceae. 
show two unique features: asymmetrical colpi 


е . 
with unequal arms extending into bs oppo 


polar faces and 1 
ent on only one polar face. Olinia 
Penaeaceae in having a psilate 
and in exine structure (a very thick foot 
tectum, and a thin columellae-infrat 
ular layer). 
4. Combretaceae. The taxa examined have 
diverse morphology and five groups are 
nized: (1) heterocolpate, (2) heterocol ме 
distinct echinate surface sculpture, ( 
surface without subsidiary colpi, 
surface without subsidiary colpi, and 5 
late surface without subsidiary со1р1 a о! 
ће —— group indicates gene 
es to some deus Cryptero 

ie | и" 

5. ы Alzatea уе 
in pollen characteristics to Axin nandra and 
tylocladus (Crypteroniaceae) and R Y ary col 

ynchocalycaceae). Indistinct be 

ог intercolpar concavities appear tO 
In fine structure some resemblance is 
Chrysobalanaceae. 

n Rhynchocalycaceae. The pollen Ee] 
chocalyx lawsonioides is tricolporate an 


are ње 
pollen surface, 
layer and 

gran- 


are recog 
pate with û | 


| 
The five taxa examined all 


| 


D 


j 


„and | 
illata is simil | 
pynchot | 


shown ® 


| 


аы ар 


1984] 


colpate with three subsidiary colpi. In these and 
other characteristics the pollen of Rhynchocalyx 


(Melastomataceae) and Lumnitzera (Combre- 
ta 


ae). 

7. Penaeaceae. The taxa examined are het- 
erocolpate with tri- and tetracolporate pollen; 
Glischrocolla has 5-colporate pollen. E 
phic resemblances are with Melastomataceae 
(Tristemma, Dissotis), Combretaceae (Combre- 
tum, Quisqualis), and Crypteroniaceae (Dactylo- 
Ee us). Endomorphic resemblance is striking 

| Oliniaceae and Dactylocladus of Crypte- 
roniaceae. 

8. Crypteroniaceae. Dactylocladus and Axi- 
nandra are heterocolpate and can be favorably 
compared with some Lythraceae, Melastoma- 
taceae, Combretaceae, Penaeaceae, and perhaps 
in a general way with much of the Myrtales. 
Crypteronia differs from most Myrtales in having 
dicolporate pollen with two intercolpar concav- 
ities. 

9.  Melastomataceae. Pollen of the taxa can 
be divided into three basic types: (1) heterocol- 

ith subsidiary colpi alternating with colpi, 
(2) "heterocolpate" with intercolpar concavities 
alternating with colpi, and (3) tricolporate. The 
rst group resembles several of the heterocolpate 
Combretaceae. Also in this first group are several 
genera often segregated as Memecylaceae, but 
they are not delimited as a group within the het- 
*rocolpate Melastomataceae. Tococa ы 
њи: 4 occurs as polyads, the only member of th 
amily to the present time found to occur this 
way, and along with some Ludwigia of Onagra- 
ae (and perhaps Trapa natans as discussed 
above), the only taxa with polyads in the Myr- 
-- Similarly, Miconia melanotricha is the only 
м, in the family reported to have pollen in 


á ~ 5. Myrtaceae. An essentially consistent 

i Ology is found in all taxa examined. The 

vid MT triangular (in polar view) pollen is di- 
based i n part on previous reports, into 


micas Broups defined by colpus амир: (1) 


asd Parasyncolpate wit and without ee 

псауше5, and (3) brevi- or brevissimicolpate 
in 

о 


PATEL ЕТ AL.—POLLEN CHARACTERS 


967 


and Camissonia) and Miconia melanotricha of 
Melastomataceae. Psiloxylon has large apocolpia 
but overall is similar to most Myrtaceae pollen 
in group (2). Heteropyxis likewise is not distin- 
guished within the second group. Pollen of Myr- 
taceae is not clearly comparable with any other 
pollen in the Myrtales. 
11. Onagraceae. The pollen of the taxa ex- 
amined is variable within the family but, like 
Myrtaceae, is without any close similarity in the 
Myrtales. The distinctive characters are circular 
to triangular central body with markedly to 
slightly protruding apert ; globul anular), 
rod-like (elongate), or rugulate surface elements; 
tetrads and polyads in addition to monads; viscin 
threads, and thick endexine and essentially 
spongy-paracrystalline ektexine usually lacking 
columellae and always lacking a foot layer. 


LITERATURE CITED 


ARCHANGELSKY, D. R. 1971. Palynotaxonomy of the 
beet s.l. Pp. 104—234, in L. A. Kupri- 
anova & M. S. Jakovlev (editors), Pollen Mor- 
phology. Acad. Science USSR. Komarov Bot. Inst., 


Beer, R. 1905. On the development of the pollen 
grain and anther of тира magraceae. Beih. Bot. 
Centralbl. 19: 28 

BEUSEKOM-OSINGA, 2: C. F. vAN BEUSEKOM. 
n пуан а 


BOWERS, „С. G. 1931. The development of pollen and 
Bull. 


Torrey Bot. Club 57: 285-314. 

Brown, C. M 1967. Pollen morphology of the On- 
agraceae. Rev. Palaeobot. Palynol. 3: 163-180. 
CAMPO M. giu 1966. Pollen et phylogenie. Les 

breviaxes. Pollen & Spores 8: 57-73. 
Cos CAMPOS, D. 1964. Etude des grains de pollen des 
L cees du Perou. Drea peng 3 5. 
CRESTI, M. Е. CIAMPOLINI & R. N. КАРП. 1983. Ul- 
trastructure of S4S, genotype pollen Bp of Oe- 
nothera organensis. Acta Bot. Neerl. 32: 177-183. 
CRUDEN, R. W. &K. K.G. JENSEN. 1979. уйсш nn 


11 
UC 


J. Bot. 66: 875-879. 
DAGHLIAN, C. P., J. J. SKVARLA, D. T. POCKNALL & P. 
v 1984. Epilobium pollen from Oli- 
gocene sedimentation in New Zealand. New Zea- 
land J. Bot. 22: 285-294. 

DAHLGREN, R. 1967a. Studies on Penaeaceae. I. Sys 
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PRINCIPAL WORKS ON THE POLLEN 
MORPHOLOGY OF MYRTALES 


K. THANIKAIMONI! 


INTRODUCTION 


The following list covers 454 references to works based on replica, scanning, and transmission 
electron microscopic studies, and covers 320 genera and 23 families. These encompass not only the 
core families of the order Myrtales sensu Dahlgren and Thorne and others, but also those families 
now not included in the order but that have been «нане with it according to various one 
ordinal delimitations. This list has been drawn mainly from i 
of angiosperm palynological literature by G. Thanikaimoni | (1972, 1973, 1976, 1980), and supple- 


mented by more recent publications. 


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rique Noire, Sér. A, Sci. Nat t. 2 
1070. 
VAN DER HAMMEN, T i E 
logical systematic nomenclature. 


Bogota 4: 63-101. ' 

Уш. Ө: 1976. Pollens des "T 

tagnes du Sud de l'Inde. rps SIS i 

dichéry, Trav. Sect. Sci. ; 
VASUDEVAN МАЈЕ, R. а at 

of Rotala from Palghat, Kerala. 

bay Nat. Hist. Soc. 72: 56-60. i 
Ў . K. КАК. Зе of 
Fossil pollen comparable to po 


— 


— — 


анн — 


| 


1984] THANIKAIMONI— WORKS ON POLLEN MORPHOLOGY 985 


Barringtonia from the Laki sediments of 
Kutch. Pollen & Spores 10: 335-339. 
VENKATESWARLU, J. 1937. A contribu- 
tion to the embryology of Sonnerati- 
= Proc. Indian Acad. Sci. 5: 206- 

23. 


——. 1945. Embryological studies in 
the Thymelaeaceae. J. Indian Bot. Soc. 
24: 45-66. 

— —. 1947. Embryological studies in 
the Thymelaeaceae. J. Indian Bot. Soc. 
26: 13-39 

—. 19 . Embryological studies in 

Lecythidaceae—I. J. Indian Bot. Soc. 31: 

103-116. 

——— 1952. Contributions to the em- 
bryology of Combretaceae: I— Poivrea 
g РС. Phytomorphology 2: 231- 


—— & B. ACHUTHARAMAMURTHI. 
1955, Embryological studies in the Bo- 
тарпасеае. I. Coldenia procumbens Linn. 
J. Indian Bot. Soc. 34: 235-247. 

7 —- У. SESHAVATARAM. 1963. A 
У of the Pollen grains of Jussieua and 
р E remarks » the taxonom- 

ussieua suffruticosa Linn. 

Чаа Sci. 32: 443-445. 

Я U-MiTTRE & H. P. Gupta. 1964. 
udies of Indian pollen grains. III. Car- 

„к. Pollen & Spores 6: 99—111. 
€ в, J. W. & J.A. DOYLE, 1975. The 

IS of Angiosperm phylogeny: paly- 


nology. Ann. Missouri 
6 64-723. n. Missouri Bot. Gard. 62: 


Wana, Е. Н. 1960. Pollen Grains of 
China. [In Chinese.] 

WANG, J. L. 1962. General morphologi- 
cal study of the pollen grains of the Tai- 
wan species. Inform., Taiwan Forest. Res. 
Inst. 136 & 137: 1083-1096. 

WEE, У. C. & A. М. КАО. 1980. Anthesis 
and variation in floral structure of Par- 
kia javanica. Malayan Forester 48: 493- 
499. 


WHITMORE, T. C. 1974. Abdulmajidia, a 
new genus of Lecythidaceae from Ma- 
laysia. Kew Bull. 29: 207-211. 

WODEHOUSE, R. P. 1932. Tertiary pollen. 
I. Pollen of the living representatives of 
the Green River flora. Bull. Torrey Bot. 
Club 59: 313-340. 

———. 1935. Pollen Grains. Hafner 
Publishing Co., New York. [Reprinted 
in 1959. 

WRIGHT, J. O. 1978. A new species of 
Fuchsia L. Bot. J. Linn. Soc. 77: 113- 


115. 

YBERT, J. P. 1979. Atlas de pollens de 
Cote d'Ivoire. Initiat. Doc. Tech. OR- 
STOM 40: 1-40. 

ZAKLINSKAIA, E. D. 1953. Description des 
pollens et spores de certaines espéces de 
végétaux de la toundra polaire. Akad. 
Nauk, SSSR, Trudy Inst. Geol. Nauk 
142(Ser. Geol. 59): 3-59. [In Russian.] 

———. Morphology of pollen of 
some species of desert plants. Pustyni 
SSSR i ich Osvoenie, Nauk 2: 602-633. 
[In Russian.] 


Ы 


Studies in Fuchsia 


This special issue of the ANNALS OF THE MISSOURI BOTANICAL GARDEN (Vol. 
69, no. 1, 1982) is devoted to several papers on the systematics of the genus 
Fuchsia (Onagraceae). The large section Fuchsia, which contains such horticul- 
turally important species as Е. corymbiflora, F. triphylla, and F. fulgens, contains 
61 species, about 60% of the entire genus. Paul Berry’s monograph treats the 
section in detail: extensive descriptions of flowers, blooming periods, habitats, 
and distribution are given. These are supplemented with beautiful color plates of 
several species. In addition to traditional keys to all the species, principal mor- 
ological differences between similar species and hybrids are treated in table 
orm. 


CONTENTS 


The Systematics and Evolution of Fuchsia Sect. Fuchsia (On- 
agraceae) 
mE Hep. a 1 
Pollinator Maintenance vs. Fruit Production: Partitioned Re- 
productive Effort in Subdioecious Fuchsia lycioides. 
Peer A ADG A Php ама  —  . 199 
The Mexican and Central American Species of Fuchsia (On- 
agraceae) except for Sect. Encliandra. 
Dennis E. Breedlove, Paul E. Berry & Peter H. Raven 209 
Index 235 


ADM UE KU D желе ә Сө аө RUN UR UA И Ө ЕСЕГЕ ТЕ УОЙ ЕЕ MEN UR ЭЛЙ а аө ӨЙ e por 


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Contents continued from front cover 


Reproductive Anatomy and Morphology of Myrtales in Relation to System- 
atics Rudolf Schmid 
The ее and Relationships of А Ону. (Ећупсћосају- 
асеае) Hiroshi Tobe & Peter H. Rave 

The Н РА and Relationships of Wiha Ruiz & Pav. (Alzateaceae, 
Myrtales) Hiroshi Tobe & Peter H. Raven 
Flavonoids of Rhynchocalycaceae (Myrtales) John E. Averett & Shirley 
A GORIN c ЕР ee MM му 


Flavonoids of Alzateaceae (Myrtales) Shirley A. Graham & John E. Av- B 
erett 


Pollen Characters in Relation to the Delimitation of Myrtales Varsha d 


C. Patel, John J: Skvaria & Peter H. Raven. — e Qa 
Principal Works on the Pollen Morphology of Myrtales К. Thanikaimoni 


832 


836 


. 844 


853 


VOLUME 71 1984 


| 


i. Contents continued on back cover 


CONTENTS 


Lisianthius Pollen from the Eocene of Panama Alan Graham .. 
Steyermarkochloa unifolia, a New Genus from Venezuela and Colombia 
oo Arundinoideae: Steyermarkochloeae) Gerrit Davidse & R. 
li 


Occurrence of бышы in Iridaceae and Allied Families and Their Phy- 
Ee Significance Peter Goldblatt, James E. Henrich & Paula 
all 


A iw of Euphorbia (Euphorbiaceae) in Baja California Michael J. 
A Revision of Stenandrium (Acanthaceae) in Mexico and Adjacent Regions 
Thomas Е. Daniel 
A Bi ibliogr aphy of Numerical Phenetic Studies in Systematic Botany Ber- 
nard R. Baum, ders Duncan & Raymond B. Phillips —... 

Notes on Symphyt )in North America Т. W.J. · Gadella 

Two New Species of Pasiflora (Passifloraceae) from Panama, with Com- 

N ments on Their Natural History Sandra Knapp & James Mallet .... 
ew Species and Combinations in Apocynaceae from Peru and Adjacent 

N Amazonia Alwyn Н. Семіру еа 

ew Species of Galaxia (Iridaceae) and Notes on Distt and Evolution 
іп ће Genus Peter Goldblatt -1 


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ANNALS 


OF THE 


MISSOURI BOTANICAL GARDEN 


1984 


VOLUME 71 NUMBER 4 


LISIANTHIUS POLLEN FROM THE EOCENE OF PANAMA! 
ALAN GRAHAM? 


| 
АВЗТЕАСТ 


Fossil pollen similar to the extant p Lisianthius ч see has been recovered from the 
о to late Eocene Gatuncillo format e genus presently extends from Mexico, 
а iyi the Antilles and Central America, шы погї ae Colombia. The oldest fossil record for the 

m d is from the Paleocene (pollen) dne early Eocene (flowers) of the northern hemisphere. The 


„ ап 


U1dilUlllvlll 


bas for the family, migration of at lead one member as far south a: as central Panama by the end of 


with subsequent анод into northern South 
America, it has been suggested the family i is probably not a recent 


ocene 
relatively well е 
mea al. The 


of eker pollen in deposits as early as the Eocene in 


erica. Since the Gentianaceae is 


present- 


central Eni is peores with this suggestion. The genus has not previously been reported in 


the fossil record. 


unt the Eocene the present region of Cen- 
dd iw consisted of a series of volcanic 
уриб Ing southward from the North Атег- 
dn E inent (Dengo, 1973). Extensive vulca- 
чны RM in the Tertiary formations of 
ни the widespread occurrence of ag- 
а Ка 5 (angular volcanic ejecta), tuffs (water- 
80) cec ash), and basalts (Stewart et al., 
“oo activity resulting from the in- 
ini B^ east Pacific (Cocos), North Amer- 
1982. oe Caribbean plates (Coney, 
out Conny er, 1976) is equally evident through- 
"pm cn deposits in Central America. Along 
AE Qus zm Reach of the Panama Canal, 
аи „а 13 faults have been observed in a 
кита са. 3 km (Stewart, pers. comm.). In 
к M ben. left-handed fault motions total 
tn Isplacement in a distance of 4 km. This 
€ activity resulted in the uplift of the isth- 
lan region in latest Tertiary and Quaternary 


4 


nis earth s 
thn — were kindly provided by Dr. Joan Nowi 


1p Cooperati 
faex ion of Robert and Joanne opis and 


times (Marshall et al., 1976, 1981, 1982; Webb, 
1976). The biogeographic consequences of this 
event have been widely discussed (e.g., Gentry, 
1982; Graham, 1973; Raven & Axelrod, 1974; 
Woodring, 1966). 
und the periphery of these islands man- 
grove swamps developed and their remains con- 
tributed to the formation of bands of lignite con- 
taining fossil pollen of Rhizophora, Pelliceria, 
and other genera. One such deposit is the Eocene 
Gatuncillo formation of Panama. 

The Gatuncillo formation outcrops in south- 
central Panama east of the former Canal Zone. 
Near Alcalde Díaz, exposures consist of lignites 
interbedded between layers of claystone, silt- 
stone, and fine-grained sandstone. Samples were 
collected from a 30-foot roadcut section and pro- 
cessed for plant microfossils. The lignites con- 
tained a diverse and well-preserved assemblage 
of fossil pollen and р I g 


upported by NSF grants GB-5671, GB-1 1862, DEB-8007312, and DEB-8205926. SEM photo- 
cke (Smithsonian Institution). Field work was facilitated 


their assistance is via acknowledged 


of Biological Sciences, Kent State University, Kent, Ohio 44242. 


ANN. 
Missouri Bot. GARD. 71: 987-993. 1984. 


988 


of a vegetation that occupied the region ca. 40 
million years ago 

The collecting locality is reached by a gravel 
road off the Boyd-Roosevelt Highway. The gen- 
eral area is shown on the Alcalde Díaz (Penocito) 
quadrangle map (sheet 4243 11 NE) ofthe Army 
Map Service, and the specific collecting site at 
coordinates 100.8 x 660.8 on the recently com- 
piled “Geologic Map of the Panama Canal and 
Vicinity" (Stewart et al., 1980). 

The sediments near Alcalde Díaz represent a 
classic sequence of near-shore depositional en- 
vironments. At other sites in the region the sec- 
tion is capped by a marine limestone, and marine 
limestones surround the locality. Thus the Ga- 
tuncillo lignites were deposited along an ancient 
shoreline that can be traced on the geologic map 
as the contact between the Gatuncillo formation 
and strata mapped as pre-Tertiary (Stewart et al., 
1980). 

The age of the Gatuncillo is late Eocene, al- 
though lower in the section some middle(?) 
Eocene sediments may locally be included. The 
age assignment is based on larger foraminifera 
reported by Cole (1952) and is accepted on the 
most recent version of the geologic map of Pan- 
ama (Stewart et al., 1980). Almost all the species 
reported by Cole (1952) are upper Eocene fora- 
minifera, but two (of 21) were known elsewhere 
only from the middle Eocene. These are Yaberi- 
nella jamaicensis Vaughan from the middle 
Eocene of Jamaica, and Fabiania cubensis Cush- 
man & Bermúdez from Cuba and Florida. Con- 
sequently the age of the entire Gatuncillo se- 
quence is regarded as middle(?) to late Eocene. 


MATERIALS AND METHODS 


Lignite samples were macerated in a mortar 
and pestle then passed through НСІ, HF, HNO,, 
KOH, and acetolysis (one part concentrated 
H,SO, to nine parts acetic anhydride). The paly- 
nomorphs were mounted unstained in glycerine 
jelly and sealed with CoverBond. Light photo- 
micrographs were taken with a Wild microscope 
equipped with a Nikon 35 mm camera using 
Panatomic X film. SEM photomicrographs of 
extant pollen grains were prepared at the Smith- 
sonian Institution. Acetolyzed samples were 
sputter-coated with gold-palladium and photo- 
graphed with a Cambridge Stereoscan Mark IIA. 
The specimens are deposited in the 


| рајупојору 
collections at Kent State University. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


RESULTS 


The fossil pollen and spores presently identi- 
fied from the Eocene Gatuncillo formation of 
Panama include Selaginella, Ceratopteris, Pteris, 
Bromeliaceae, Palmae, cf. Campnosperma, Ilex, 
cf. Arrabidaea, cf. Protium, cf. Tetragastris, 
Combretum/Terminalia, Casearia, cf. Tontalea, 
Alfaroa/Engelhardtia, Crudia, Malpighiaceae, cf. 

icus, Eugenia/Myrcia, Coccoloba, Rhizophora, 
Faramea, Cardiospermum, Serjania, Paullinia, 
cf. Chrysophyllum, Pelliceria, and Mortonioden- 

ron. Also recovered were pollen grains de- 
scribed as follows (description of the microfossils 
is based on light microscopy at 400 x and 1,000х 
oil immersion magnifications): Pollen oblate to 
oblate-spheroidal, amb circular; tricolporate, 
colpi meridionally elongated, equatorially ar- 
ranged, equidistant, tapering to acute apex, mar- 
gin entire to slightly diffuse, faint margo formed 
by gradual diminution of reticulum near colpus 
margin, ca. 18 wm long (equator to apex), ех- 
tending within 6—7 шт of pole (polar index 0.2), 
pore circular, situated at midpoint of colpus, 
margin diffuse, 4—5 um diam.; reticulate, retic- 
ulum somewhat irregular, diameter of lumen са. 
2-3 um in equatorial mesocolpal region, dimin- 
ishing toward poles and margins of colpi, muri 
tall (ca. 2.5 um) in equatorial mesocolpal сна 
giving somewhat deep, boxwork effect to ret : 
ulum, muri surface psilate, margins entre; spor 
tectate-perforate, height of columellae 25 кет 
equatorial mesocolpal region, диирин is 
ward poles and margins of colpi; size 35-45 um. 

A second microfossil ine И 
scribed above was recovered an 
having a slightly finer and more regular pa 
lum. The microfossils have a low but pn 
frequency on the four slides counted, qup 
stitute ca. 0.596 of the total assemblage. aps 
scription is based primarily on five " (the 
served specimens from our Locality че 
Alcalde Diaz locality), sample 4 (near gë beled 
of the roadside section), slide 1 (slides га: pa 
Pan D, 4-1), although other specimens be a 
amined to establish size ranges 1n Lee 
features. Specimens with the coarser gx 
were more common than those with 
more regular reticulum (ca. 4: 1). 

The modern genus in our polle 
reference collection most similar to а cto) 
fossils is Lisianthius P. Browne poner 
The collection includes all New Wor! 
and most Old World genera of the Gen 


ffers only in 


= 


GRAHAM — LISIANTHIUS POLLEN 


| PIGURES 1-9. Fossil pollen of Lisianthius from the middle(?) to late Eocene Gatuncillo formation, Panama.— 
NC D 4-1, England Slide Finder coordinates X-23, 36 ит. — 2, 5. Pan D 4-1, ESF V-34,1, 45 um.— 3, 6. 
4-1, ESF Q-41,3, 41 um.— 7. Pan D 4-1, ESF Q-45, 45 um.—8, 9. Pan D 4-1, ESF O-39, 1-2, 38 um. 


ti collections for virtually all species 
sia anthius. The microfossils conform in all 
Morphological features to pollen of the 
~ genus, but differ slightly in shape. АП 
Microfossils were encountered in polar or 
"Polar view, reflecting their oblate to oblate- 


spheroidal shape. Most pollen grains of the mod- 
ern species orient in equatorial view reflecting a 
1 á E | 5-4 1.51. 1 * 1 z | 1 19 Also 


a 
pev р 


узы ае ан = z 
the margo formed by diminution of the reticu- 


lum g 


in the modern pollen. These are minor, quanti- 


990 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


ARN 
+ А 
е 

~ 
~. 
A 
С 
z 


FIGURES 10-16. Light photomicrographs of modern Lisianthius pollen. — 10-12. L. petes 
a, K; Morton & Alain 9000, Cuba, K).—13-16. L. nigrescens Cham. & 


preg: 1613, Cuba 
6477, Mexico, F; Ghiesbreght 702, Mexico, BM). 


tative differences, however, and given both the 
overall close morphological similarity, and the 
age of the fossils (upper Eocene), the specimens 
are considered within the range of variation of 
extant Lisianthius pollen (cf. Figs. 1-9 and 10— 
16). SEM photomicrographs of extant pollen 
(Figs. 17—22) proved useful in confirming details 
of morphology and relating these to interpreta- 
tion and identification of the microfossils. 


[VoL. 71 


A. Rich. 
(Breedlove 


lato) 
The modern pollen of Lisianthius (sensu 


has been studied by Nilsson (19708, 19708 4 
son in Elias & Robyns, 1975) an d Weaver ie 
Among the species with pollen similar 
microfossils are Lisianthius aurat 
capitatus Urban, L L. dominensis U : n 
dulosus A. Rich. (Figs. 10-12. 17, 13-16, 18, 
nigrescens Cham. & Schlect . (Figs. se : 
20, 22), and L. umbellatus Sw. The varia 


GRAHAM —LISIANTHIUS POLLEN 


21 22 


Ficures 17-22. ning electron photomicrographs of modern Lisianthius pollen.—17, 19, 21. L. glan- 


d [ Scan 
red ` Rich. (Morton & Alain 9000, Cuba, US).— 18, 20, 22. L. nigrescens Cham. & Schlect. (Weaver 2183, 
» US). 


992 


fineness of the reticulum noted for the fossils is 
matched among the pollen of modern species of 
Lisianthius. Pollen of L. nigrescens is similar to 
the more coarsely reticulate microfossils, and L. 
glandulosus represents the more finely reticulate 
t 


Both Nilsson (1970a, 1970b; Nilsson in Elias 
& Robyns, 1975) and Weaver (1972) agreed that 
Lisianthius pollen can be distinguished from oth- 
er genera of the Gentianaceae, and this finding 
is consistent with our survey of the family. For 
example, in the related segregate genus Macro- 
carpaea the grains are either in tetrads, or if in 
monads, they differ from Lisianthius by the pres- 
ence of conspicuous gemmae, or by a more open 
reticulum (viz., greater diameter of the lumen) 
and/or slightly coarser columellae. 


DISCUSSION 


Lisianthius is a New World genus of 27 species 
and two varieties of perennial herbs, shrubs, and 
small trees distributed from south-central Mex- 
ico, through the Antilles and Central America, 
into northwest Colombia (Weaver, 1972). The 
genus has been monographed by Weaver (1972), 
and treated floristically by Elias and Robyns 
(1975) for the Flora of Panama. Recently Sytsma 
et al. (1983) have studied the phylogenetics of 
the L. skinneri complex by endonuclease DNA 
mapping, morphology, flavonoids, and allo- 
zymes. The plants are entomophilous, but small 
percentages of pollen are quite likely to enter 
depositional basins. The conspicuous flowers are 
borne in clusters of about 15 to 30, and there 
may be between six and ten clusters per plant. 
At maturity the anthers extend beyond the co- 
rolla. Lisianthius seemannii (Griseb.) Perkins is 
especially floriferous with 100 or more flowers 
per plant, and L. skinneri (Hemsl.) O. Kuntze, 
the most common Central American species, also 
flowers profusely. Furthermore, several species 
of Lisianthius form thickets that locally domi- 
nate the habitat. As noted by Germeraad et al. 
(1968), outwashing is an important means of pol- 
len transport in tropical environments and ac- 
counts for the greater representation of pollen 

from entomophilous Species in tropical sedi- 
ments than in deposits from temperate regions. 

Lisianthius occurs from near sea level to about 
1,800 m and is found in a wide variety of hab- 
itats. For example, L. saponarioides Cham. & 
Schlect. grows from 600 to 1,200 m on rocky 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


limestone hillsides and in secondary scrub; L. 
meianthus Donn. Sm.—near sea level to 1,500 
m in pine forests, limestone thickets, and road- 
sides; L. oreopolus Robins.—100 to 1,800 m in 
dry to moist pine or mixed forests; L. pedun- 
cularis L. O. Williams—dense moist forests at 
1,000 m; L. jefensis Robyns & Elias—850 to 900 
m in cloud forests; and L. auratus Standley—sea 
level to 1,800 m in pine forests or savannahs. 
Thus the floral features of Lisianthius, its oc- 
currence in dense thickets, and its widespread 
distribution at moderately low elevations 
throughout Central America are consistent with 
the high-frequency, low-percentage recovery of 
microfossils from the Gatuncillo formation. 
The presence of Lisianthius pollen in the late 
Eocene Gatuncillo formation, and earlier records 
of the Gentianaceae in the Paleocene and lower 
Eocene of the northern hemisphere (Crepet & 
Daghlian, 1981), is consistent with a northern 
origin for the family, one member of which had 
reached the area of present-day central Panama 
by late Eocene times. Its occurrence there at least 
raises the possibility of an early introduction from 
North America into South America prior to the 
more extensive exchange at the end of the Ter- 
tiary. This possibility parallels the soe 
impression of Raven and Axelrod ure 
based on the affinities and biogeography ofm 4 
ern taxa: “Judging from their affinities, the и 
lowing taxa may also have gone from No 
America to South America. They 
resented there it seems probable that they za 
very recent arrivals: Boraginaceae, Clethracea®, 
Gentianaceae, Hydrophyllaceae, Logo. 
Buddleia, Onagraceae— Fuchsia, P 
Polemoniaceae, Scrophulariaceae, TheoP 
taceae, Viscaceae.” 


р 


formation of Panama; and the Gatun 
in Costa Rica (Graham, unpubl. : 
only the Culebra assemblage has ке 

апа Lisianthius pollen has not been ipe 
Fossil representatives of other Gentian: (198!) 
been discussed by Crepet and райе onl 
This is the first report of Lisianthius 10 

record. 


— anonut. " an 


ПЦ 


шине MIA 


1984) 


LITERATURE CITED 


Соте, W. S. 1952. Eocene and Oligocene larger fo- 
raminifera from the Panama Canal Zone and vi- 
cinity. Profess. Pap. U.S. Geol. Surv. 244: 1-41. 

Coney, P. J. 1982. Plate tectonic constraints on the 
En of Middle America and the Carib- 

n. Ann. Missouri Bot. Gard. 69: 432- 


СЕЕРЕТ, W. L. & C. P. DAGHLIAN. 1981. Lower Eocene 
and Paleocene Gentianaceae: floral and palyno- 
logical evidence. Science 214: 75—77. 

Denco,G. 1973. Estructura Geológica, Historia Tec- 
tónica y Morfológia de América Central, 2nd edi- 
^ ма Centro Regional de Ayuda Técnica, A.I.D., 


ELIAS, T. S. А Rosyns. 1975. 
10. Gentianaceae. Ann. Missouri Bot. Gard. 62: 

61-101. (Pollen description by S. Nilsson.) 
Gentry, A. H. 2. otropical floristic diversity: 
phytogeographical DM between Central 
South America, Pleistocene climatic fluctua- 
ions, oran чечан of the Andean orogeny? Апп. 

souri Bot. Gard. 69: 557—593. 

EL J. H., C. A. HOPPING & J. MULLER. 1968. 
Palynology of Tertiary sediments from tropical 

s. Rev. Palaeobot. Palynol. 6: 189-348. 
Didim, A. 1973. 
perate element in the Latin American biota. Pp. 
223-236 in A. Graham бараты aga 


Flora of Panama. 


" . 1981. Calibration of the beginning 
а age of mammals in Patagonia. Science 212 


: S. D. WEBB, J. J. SEPKOSKI, JR. & D. M. RAUP. 


GRAHAM — LISIANTHIUS POLLEN 


993 


1982. LV f z> | à 13 + + Amer. 
ican interchange. Science 215: 1351- 1357. 


RTIS & 


: TLER, R. E. DRAKE, G. M. Cu 
. M. TEDFoRD. 1976. Calibration of the great 
American interchange. Science 204: 272-279. 


Oa. Pollen morphological contribu- 
t. (Gen- 


NILSSON, S. 197 
tions to the taxonomy of Lisianthus L. s. la 
tianaceae). Svensk Bot. Tidskr. 64: 1—43 

. 1970b. Pollen morphological studies in the 
Gentianaceae. Acta Univ. Uppsala 165: 1-18. 

PLAFKER,G. 1976. Tectonic aspects of the Guatemala 
earthquake of 4 February 1976. Science 193: 1201- 


RAVEN, Р. H. & D. I. AxELRop. 1974. Angiosperm 


ama Canal and Vicinity, Republic of Panama. 
1:1000,000. Misc. Invest. Ser. U.S. Geol. Surv. 
Map I-1232. 

SYTSMA, К. J., B. SCHAAL & P. Н. RAVEN. 1983. Phy- 
logenetics of the Lisianthius skinneri (Gentiana- 
ceae) species complex in Central America. Amer. 
J. Bot. 70(5, part 2): 132. [Abstract.] 

WEAVER, R. E., JR. A revision of the neotrop- 
ical genus ' Lisianthus (Gentianaceae). J. Arnold 
Arbor. 53: 76-100, 234-311. 

Wess, S. D. 1976. Mammalian faunal dynamics of 
the great American interchange. Paleobiology 2: 


WOODRING, W. P. 1966. The Panama land et as 
a sea barrier. Trans. Amer. Philos. Soc. 110: 425- 


STEYERMARKOCHLOA UNIFOLIA, A NEW GENUS 
FROM VENEZUELA AND COLOMBIA (POACEAE: 
ARUNDINOIDEAE: STEYERMARKOCHLOEAE)! 


GERRIT DAVIDSE? AND В. P. ELLIS? 


ABSTRACT 
Steyermarkochloa unifolia Davidse & Ellis, gen. et sp. nov. and Steyermarkochloeae Davidse & 
рал ч, поу. аге сеет This species occurs in seasonally inundated white-sand soils in the 
Territorio Federal Amazonas, Venezuela, and Guainia, Colombia. It has dimorphic culm 
and s: Only a uds developed lé leaf i is produced per ve 


getative culm. The morphology of this leaf 
is unique in the Poaceae in its cylin , solid sheath wlan — pira and absence of a ligule. 
Plants are polygam -monoecious but most зато аге ual. АП spikelets are 3-flowered with 


stigmas are terminally exserted. Anatomical studies indicate that the plant is arundinoid the 
dermal characteristics except the absence of so „> in most diagnostic characteristics e 


in the blade. The blades, sheaths, and roots js ve an n extensive ees of lacunae, a feature typical 


aquatic plants. Although anatomical ан вагу роіп 


о ап arundinoid affinity, the тапу апот- 


ted position eben the subfamily that is best recognized 


at the tribal level. 


During his intensive studies of the savannas 
in the Territorio Federal de Amazonas, Vene- 
zuela, Otto Huber collected an unusual grass along 
the Río Temi in 1978 that could not be identified 
with any known Masses species. A thorough 
search int erbarium ofthe Dirección 
de Investigaciones Bd (VEN) led to the 
discovery of an earlier unidentified collection of 
the same species made by E. Foldats in 1960 
along the Río Atabapo, also in Amazonas. In 
1980, the remaining unstudied grass collections 
ofthe New York Botanical Garden's expeditions 
to the Guyana Highlands became available to 
Davidse. Discovered among these collections was 
a unicate specimen of this grass collected by B. 
Maguire, J. J. Wurdack, and G. S. Bunting near 
Cerro Yapacana, Amazonas, in 1953, which rep- 
resents the first collection of this species. 

At the invitation of Huber, Davidse had the 
opportunity in 1979 to join an expedition to 
west-central Amazonas in the Departamento of 
Atabapo where several new populations of this 
interesting grass were located. Subsequent stud- 


ical features, thorough anatomical studies gie 
required to clarify the systematic posue in 
relationships of this grass within the family. ~ 
studies were undertaken by Ellis and are repo 
here. 

Based on these studies, we conclude t ~ 
unusual grass represents а new monotypic већ 
and néw tribe of the Arundinoideae. ays 

The genus is named in honor of Dr. раде ЈА 
Steyermark, the most prolific botanical co 
of all time, discoverer of hun 
of plants and animals, author 
tanical publications, and a valu 
and field companion of ee 


hat this 


TAXONOMY 
ibus nov: 
Steyermarkochloeae Davidse & Ellis, e 
TYPE: Steyermarkochloa Davidse 
ramina perennia culmis et foliis dimoph 
folium evolutum singulare in quoque 


' Support for fieldwork was provided by NSF INT 76-14750 and CONICIT و‎ person Davi 


uber for providing him with 


ephen S. Tillett a н 


Otto H 
Julio Cerda Cordero also participated in the ад оне “er contributed mighty pa m success. W ble 10 us 
pecimen s avail 


to Dra. Zoraida gt de Febres (VEN) an 
and to Dr. John D 
by H. Botha and 5. Perold. 
? Missouri Botanical Garde 
3 Botanical Research Instit 


ANN. Missouni Bor. GARD. 71: 994-1012. 1984. 


en, P.O. Box 299, St. Louis, Missouri 63166. 
ute, Department of Agriculture, Private Bag X101, Pretoria, 


0001, South Afric 


1984] DAVIDSE & ELLIS—STEYERMARKOCHLOA 995 


getativo vagina cylindrica solida lamina com- 
planata ligula non evoluta. Inflorescentia spicata 
cylindrica; spiculae masculinae et/vel bisexuales 
infimae in infl ia, spiculae femi sum- 
mae. Spiculae solitariae, 3-florae, interdum uni- 
sexuales plerumque bisexuales, compressae dor- 
sales; disarticulatis sub elumis: el 2; flosculus 


summus rudimentalis; flosculus inferior spiculae 
femineae sterilis; palea flosculi feminei spongiosa 
curvata (5—)7-11-nervis lemmate longior; lodi- 
culae 0; stigmata 2, stylus 1; caryopsis fusiformis 
hilo lineari. 

Perennial grasses with dimorphic culms and 
leaves; developed leaf solitary on each vegetative 
culm, the sheath solid, cylindrical, the blade flat- 
tened, a ligule not differentiated. Inflorescence 
Spicate, cylindrical with male and/or bisexual 
spikelets lowermost and female spikelets upper- 
most. Spikelets solitary, 3-flowered, usually uni- 
Sexual, sometimes bisexual, dorsally com- 

; disarticulation below the glumes; glumes 
2; uppermost floret rudimentary; lower floret of 


rag spongy, curved, (5—)7-11-nerved, longer 
i the lemma; lodicules 0; stigmas 2, the style 
» Caryopsis fusiform, the hilum linear. 


Steyermarkochloa unifolia Davidse & Ellis, gen 
et sp. nov. TYPE: Venezuela. Amazonas: 
ento Casiquiare, sabana cerca de 
Yavita, a lo largo del Río Temi, lat. 3°0’, 
long. 67°25', са. 110 m, hasta 2 m de alto, 
formado densas colonias al borde del ma- 
em 25 Aug. 1978, O. Huber 2620 (ho- 
“beg MO; isotypes, US, VEN). Figures 


oe perenne caespitosum. Culmi non ra- 
~ E culmus vegetativus non elon- 
tn even, d iquot vaginas sine laminis et | foli- 

› т; culmus reproductivus elongatus 
б 3-8, Cavus, ferens vaginas sine laminis. 
aginae sine laminis Marginibus liberis; folium 


к }те\їрейїсеПайаз unisexuales vel bisexu- 
basin ас masculinae et bisexuales portatae 
aliter versus inflorescentia, spiculae femineae 
art р» versus. Spiculae infra glumas dis- 
tli; gl tes, 3-florae, flosculo supremo rudimen- 
Sumae 2, subequales, lemmatibus breviores; 
infer; ee rectae plerumque flosculis 
US Staminatis, paleis lemmatibus sub- 


equalibus staminibus 2 per flosculum; spiculae 
bisexuales rectae plerumque flosculo inferiore 
masculino et flosculo secundo bisexuali, paleis 
lemmatibus subequalibus; spiculae femineae 
curvatae flosculo inferior sterili palea plerumque 
absenti, flosculo secundo femineo palea (5—)7—11- 
nervi spongiosa lemmate longiore; lodiculae 
0; stigmata 2, stylus 1; caryopsis fusiformis; hi- 
lum lineare; embryo У;-рјо caryopside longior. 


Perennial, caespitose in dense clumps. Culms 
dimorphic; vegetative culms with the internodes 
not elongated, erect, the lower nodes bearing 
bladeless, st i ths much longer than 
the internodes, the sheaths progressively longer 
from the base upwards, the uppermost to 20 cm 
long, clasping the developed leaf, rounded on the 
back, glabrous adaxially, abaxially prominently 
tessellate-veined, densely beset with prickles 
along the veins towards the tip, the prickles often 
enlarged at the junction of the sheath and apicule, 
the margins free, overlapping, the midrib not 
well differentiated, slightly raised on the adaxial 


apiculum 
P 


0.5-11 mm long, 0.1—0.3 mm wide with tightly 
curved margins, the uppermost node bearing a 
single, developed leaf 80—300 cm long, the sheath 
cylindrical, 2–5.2 mm diam., glabrous, solid, in- 
ternally with conspicuous longitudinal lacunae 
regularly divided by cross-partitions, without a 
conspicuous midrib, ca. half-way splitting on one 
side into a narrow furrow, this opening into a 
flattened, glabrous blade, the blade 2.8-6.5 mm 
wide, differentiated into a narrow midrib, flanked 
on each side by a narrow line of bulliform cells 
and a thickened lamina, plano-convex in cross- 
section, the adaxial surface planar, the margins 
glabrous, the laminae abruptly narrowed and 
folded towards the tip, the distal 1-2 cm com- 
pletely fused to form a blunt, navicular tip, a 
ligule not differentiated in the region of blade 
expansion; reproductive culms 40—350 cm tall, 
3-13 mm diam., strictly erect, hollow, glabrous, 
often covered with a conspicuous, greyish waxy 
bloom, the basal internodes not elongated, the 
upper 3-8 internodes conspicuously elongated, 
all bearing bladeless sheaths similar to those of 
the vegetative culms, the sheaths clasping the 
culm with overlapping margins, the lower sheaths 
stramineous, the upper green, mostly 13-40 cm 
long, often with a waxy bloom, the uppermost 
shorter than the internodes. Inflorescences 7—49 
cm long, cylindrical, spicate, bearing densely ar- 
ranged, solitary, short-pedicellate spikelets in ir- 


996 


regular whorls, the spikelets irregularly spirally 
arranged toward the base of the inflorescence, 
male or bisexual in the lower part, female in the 
upper part; peduncle exserted at maturity, gla- 
brous; rachis ridged by the decurrent pedicels, 
densely covered by a waxy excrescence, the ped- 
icels 0.4-1 mm long in the middle of the inflo- 
rescence, 4—13 mm long at the base, 4-angled, 
covered with a waxy excrescence except at the 
glabrous tip, the abscission point shallowly dis- 
coid. Spikelets dorsally compressed to rounded, 
3-flowered, sometimes 2-flowered in male spike- 
lets towards the base of the inflorescence, the 
uppermost fi tal di 


у tary in all spike- 

lets and borne on a distinct rachilla segment; 
male spikelets with 2 functional male florets; bi- 
sexual spikelets usually with the lower floret male 
and the second floret bisexual; sometimes both 
lower florets bisexual; female spikelets with the 
lower floret sterile and the second floret female; 
glumes, lemmas and paleas scaberulous toward 
their tips with the tips dark brown and with single 
transverse veins between the nerves; glumes 2, 
equal or subequal, the lower glume 2.2—4.7 mm 
long, broadly lanceolate, 2-keeled, the keels sca- 
berulous in the upper half, flattened between the 
keels, hardened and thickened between and on 
the keels, especially at maturity, 3—7-nerved, only 
the keel nerves well developed, the midnerve 
often not evident or well developed, the margin 
herbaceous, sharply incurved, nearly clasping at 
the base, the tip obtuse or narrowly truncate, the 
upper glume 2.1-3.7 mm long, lanceolate, 
rounded on the back or sometimes slightly flat- 
tened, 3-6-nerved, the tip obtuse to erose-trun- 
cate; male and bisexual spikelets mostly 4.5—7.5 
mm long, straight, the lower lemma 4.3-7 mm 
long, broadly lanceolate, herbaceous, 3—7-nerved, 
€ nerves, except for the lateral pair, conspic- 
uous, the tip broadly acute, the palea subequal 
to the lemma, membranous, 2-keeled and usu- 


17 mm long, 
lemma 4.8- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


7 mm long, broadly lanceolate, herbaceous, 
5—9-nerved, the nerves conspicuous, the apex 
obtuse, the lower palea usually not developed, 
rarely present as a hyaline bract to 2 mm long, 
the second floret female, the lemma 6.1-9 mm 
long, broadly lanceolate, curved, (5-7-)9-11 
(-13)-nerved, the nerves conspicuous in the 
upper parts, the internerves sulcate, herbaceous 
along the margin, spongy-thickened in the mid- 
dle along the midnerve, membranous at the very 
base, obtuse to truncate at the tip, the palea 8.5- 
14 mm long, always longer than the lemma at 
maturity, convolute, conspicuously spongy-thick- 
ened at maturity except for the herbaceous tip 
and somewhat membranous base, (5-]7-ll- 
nerved, curved and slightly twisted, the apex 
forming a distinct orifice for stigma exsertion, 
truncate, the pistillate flower without lodicules 
and with 2 posterior staminodia, the ovary 
fusiform-cylindrical, the style 1, the stigmas 2, 
plumose, exserted terminally, the rudimentary 
upper floret 0.3-3 mm long, the rachilla 1.8-5 
mm long; caryopsis ca. 5 mm long and | mm 
wide, ca. fusiform but broadest below the mid- 
dle, the hilum linear, ca. 3.5 mm long, the em- 
bryo ca. one-fifth as long as the caryopsis. 


km S of San Fernando de Atabapo, E bank : 
Atabapo, 67°39’W, 3*50'N, 95 m, 29 Apr. gei 
vidse, Huber & Tillett 16850 (VEN); Depto. de la de- 
Santa Cruz, margen del Río Atabapo cerca Foldats 
sembocadura del Rio Atacavi, 10 Sept. өү: 
3848 (МО, VEN); Depto. Atabapo, lower + ој и 
Сапате, 67°23'W, 3°41’N, 95 m, 2 May 1 АН 
vidse, Huber & Tillett 17089 (MO, VEN); DeP Nov. 
Баро, Cerro Yapacana, savanna I, 125 m. с 
1953, Maguire, Wurdack & Bunting о 
to. priced sabanes al pié W del Cerro Yap ; 
Aug. 1983, Huber & Kral 7973 (MO, VEN); and 
Atabapo, between the W base of ФМ, IN, 120 
the headwaters of Caño Cotáa, 66°52'W, 196 (МЕМ, 


MG, MO, PRE, VEN, WIS); Depto. днн eM W, 


part o Caño Yagua at Cucurital de 
3°36'N, 120 m, 8 May 1979, Danid, Huber a 
17382 RI, COLD Саћо Pimichin, 67°42'0, 2554'N, 


quiare, orilla del alto e 
10 m, 1 Mar. 1980, Huber 4896 (MO, 


MORPHOLOGICAL DISCUSSION 


: along 
Steyermarkochloa grows in men 
the margins of large or small stream sand soils 


ally water-logged or inundated white- 


puse e а — 


= 


пп LL ”س‎ < 


1984] 


It is most commonly found as a component of 
savanna scrub or sabaneta (cf. Huber, 1982) or 
along the margins of white-sand savannas and 
morichales. Huber (pers. comm.) defines saba- 
neta as a “dense but low scrub formation with a 
rather dense herb layer and a more or less irreg- 
ular shrub or treelet formation, the trees with 
open, irregular crowns rarely exceeding 4-5 m 
in height and their crowns not forming a contin- 
uous canopy. Sabanetas are inundated during 
most of the rainy season, normally from May to 
November, the inundation generally reaching 30- 
cm.” Flowering plants (Davidse, Huber & Til- 
lett 17382) have been observed to grow in water 
to 1 m deep early in the rainy season, March 
1980 (Davidse, pers. observ.), and to 2 m deep 
ү the height of the rainy season in the same 
ocality, August 1983, (Huber, pers. comm.). In 
~ cases only the inflorescence was emergent. 
à vé na of lacunae in the roots and leaves is 
== š own feature of plants adapted to life in 
" quatic or semiaquatic habitats. 
Ps x у inhabited by Steyermarkochloa is part 
Ste azonas Savanna Refuge described by 
Yermark (1982) and is well known for its high 
mede) pum This high endemism, as 
и 2 teyermark, is probably due in large 


on ‘ ады | 

: E the nutritionally extremely poor, 
Cid sand soils with - i 

арып. low water-holding 


The basal internodes of both vegetative and 


ductive culms. 


were P зоа in the field, and, in all but one 
is ` solitary developed leaves. In the 
consistens on two leaves were observed. The 
Der g e duction of a single developed leaf 
epi thet); e culm (alluded to in the specific 
quite rare among grasses. Previously 

the ‘ examples of such a condition are in 
m com species Sucrea monophylla So- 
Puelia Dinca ое 1981а) апа 
(Clayton. 1967) na Pilger from Cameroon 
This К" 1 normally twisted in living plants. 
"и вео excellent field character to distinguish 
*rwise inconspicuous plants from the 


DAVIDSE & ELLIS— STE YERMARKOCHLOA 


997 


accompanying herbaceous species, dominated by 
Duckea, Monotrema, Lagenocarpus, Rhynchos- 
pora, and Scleria. 

The morphology of the fully developed leaf in 
Steyermarkochloa is unique in the Poaceae. The 
differentiation ofa sheath into a solid, cylindrical 
stem-like structure that does not clasp the culm 
has not been reported previously. Based on dis- 
section of plants in the field and on herbarium 
specimens, it appears that the terminal meristem 
becomes inactive and all further growth is chan- 
nelled into the production of the basally stem-like 
leaf borne at the uppermost node. The exact de- 
tails of the ontogeny and differentiation will be 
reported upon later, on the basis of anatomical 
studies of the apical region of vegetative culms. 

This highly specialized leaf sheath is analogous 
to a culm in its cylindrical shape, solid paren- 
chymatous interior (interrupted extensively, 
however, by lacunae), and the possession of two 
concentric rows of vascular bundles at different 
levels, as explained below. Functionally it means 
that the expanded blade is presented at a higher 
level and at a presumably more advantageous 
position for photosynthesis and light competi- 


tion. 
Cylindrical, solid blades in grasses are well 

known and, according to Bócher (1972), are 

probably primarily an adaptation to xeric habi- 


tats stud- 
ied are Miscanthidium teretifolium (Stapf) Stapf 
(Metcalfe, 1960) and Sporobolus rigens (Trin.) 
Desv. (Bócher, 1972). In such species the sheaths 
possess the normal, hollow cylindrical construc- 
tion typical of all grasses. In Steyermarkochloa, 
the sheath may be an unusual adaptation to the 
seasonally flooded habitats it favors. The elon- 
gated, stem-like sheath may be a means of allow- 


gan, th 

blade, to be fully functional at high water levels. 

The reduction of all other leaves to simple, 
essentially bladeless, clasping sheaths with over- 
lapping margins is unusual in aerial culms of 
nonbambusoid grasses. Similar sheaths, usually 
with rudimentary blades, are a characteristic fea- 
ture of woody bamboo culms (McClure, 1966). 
As in the bamboos, it seems likely that the pri- 
mary function of these sheaths is structural sup- 
port of young, tender, rapidly elongating culms. 
However, the fact that the upper sheaths retain 
their green color for a long period of time indi- 
cates that photosynthesis is also an important 
function. 

The apicula usually borne on the *'bladeless" 


998 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Vor. 71 


унд 


= = = 
SS —E a 


SS ~ 


۱ ss 
culm and 
FIGURE 1. е unifolia Davidse & Ellis.—A. Habit; plant with опе fertile 


of the fertile p | 
— culms each bearing one developed - Note the bladeless sheaths at the nodes view, х6 „сте 
and at the base of the emi кошо; x0.5.—B. Apiculum of a bladeless sheath, анил 
of a developed leaf. 

culm; 


x5. b= ш ot bladeless sheath; Ir = ligular regi | 
ss = solid, cj cylindrical А, 


ve = vegetative culm. [Based on Davidse 16848 CANB] | 


— 


МИРНИ 


ET cette 


| 


1984] DAVIDSE & ELLIS— STEYERMARKOCHLOA 999 


sheaths (Fig. 1B) are presumed to represent ves- 
tigial blades because of their position and differ- 
entiation from the sheath. They appear to be 
thickened extensions of the midrib of the sheath 
that are tightly incurved. Ligules are not distin- 
guishable at the junction of the apicula and 
sheaths. Ligules are also lacking in the developed 
leaves. Absence of ligules occurs sporadically 
throughout the family, and little taxonomic im- 
rtance can be ascribed to this character at the 
generic level or above. The prominent scabrosity 
on the inner surface of the leafless sheaths is 
unusual, It is due to large prickle hairs disposed 
In regular rows on the uppermost part of the 
sheath where it does not entirely encircle the culm 
and where it is somewhat looser. This scabrosity 
could be a deterrant to small insects, including 
UR damaging herbivores, that might uti- 
и: the space between the sheath and the culm. 
Ne пи (1966) noted that all bamboo sheaths 
vea lustrous inner surface in common. In most 
other grasses this also seems to be the normal 
condition. 
ы with some leaves reduced to 
Ra om without blades is a common fea- 
s r Izomatous grasses in all major taxo- 
meg groups. Typically they form a stiff, pun- 
Mis ie on the growing point of the rhizome, 
" 8 1t to pierce the soil. 
xd. моа resembles some genera and 
i bambusoid affinity in producing inflo- 
i a ае specialized, bladeless culms. This 
(мос е of | the genera Glaziophyton 
An на 7 Piresia, Diandrolyra, Mnio- 
ie <a manochloa, and certain species of 
( 8 ма риат Pariana, and Eremites 
idee. Soderstrom, 1980). In nonbambu- 
am ses this feature is found only in those 
"шш апа species known to produce sub- 
a" cleistogamous inflorescences, as in 
Chori; EM (Hitchcock & Chase, 1950), 
1974), cosi — Hitchc. (Anderson, 
(Chase 1929) patum amphicarpum Ekman 


> 


5 


Spi é : 
Mover are borne singly on simple, short ped- 
` though the appearance is spicate, the in- 
ее to E E raceme. The spikelet arrangement 
а i 
йш. indamentally spiral, but because of 
à near] iege: 
"чы whorled pattern is attained. 
Eee elets are typically 3-flowered but occa- 
: Staminate spikelets toward the base of the 
ce may be only 2-flowered, and sev- 
eral 
female spikelets with an extra empty lemma 


were observed in Davidse, Huber & Tillet 17089. 
The spikelets are largely unisexual with the fe- 
male spikelets borne above the male spikelets 
(Fig. 2A). In most of the observed inflorescences 
female spikelets predominate, typically consti- 
tuting 70% or more of the total. Certain speci- 
mens of Davidse 16848 are entirely female. How- 
ever, in most populations there is a great deal of 
variation in the proportion of male and female 
spikelets in an inflorescence, as shown by the fact 
that in another specimen of Davidse 16848, 70% 
of the spikelets in the inflorescence are male. 

though unisexual spikelets are by far the most 
common, certain plants bear spikelets with an- 
thoecia morphologically similar to those of male 
spikelets but containing bisexual flowers. In such 
plants the lowest spikelets in the inflorescence 
may be entirely male, followed by a few whorls 
of bisexual spikelets, and topped by numerous 
whorls of female spikelets. The bisexual spikelets 
may bear two bisexual flowers or only the second 
floret may be bisexual with the lower floret male. 
We do not know with certainty whether the gy- 
noecium of bisexual florets is really functional 
since no developed caryopses have been seen in 
such florets. The gynoecium seems to be of func- 
tional size, but the styles are usually completely 
separate to the top of the ovary (Fig. 3D), where- 
as they are united approximately one-half their 
length in female spikelets (Fig. 3C). This may be 
functionally related to the larger size of female 
florets (8.5—14 mm) compared to that of the bi- 
sexual florets (4.8-7 mm). Similar style-stigma 
dimorphism was reviewed by Connor (1979), who 
noted its occurrence in three genera (Cortaderia, 
Bouteloua, and Eriochrysis). 

The androecium is always present as a pos- 
terior pair of stamens, whether fully developed 
as in male (Fig. 3B) or bisexual spikelets (Fig. 
3D) or as staminodia as in female spikelets (Fig. 
3E). Staminodia ysp tin the second 
floret of female spikelets. In some female florets 
the staminodia are clearly differentiated into fil- 
aments and anthers, but they are never func- 
tional and do not exceed 0.3 mm in length. Rath- 
er unusual is that the two filaments in the male 
florets may be free (Fig. 3A) or fused nearly along 
their entire length (Fig. 3B) with the anthers al- 
ways free. Both conditions can be found in the 
same inflorescence, but fused filaments were not 
observed in bisexual florets. Fused filaments are 
quite rare in the family, being known only in the 
Bambusoideae, in which they may be partially 
fused, as in some species of Bambusa, or mon- 


о 


1000 


- 


—E. Lower glume of female spikelet, adaxial view; x6.5 


adelphous and completely fused into a tube, as 
in Schizostachyum, Oxytenanthera, and Gigan- 
tochloa (McClure, 1966), Froesiochloa, Strep- 
tochaeta, and Dendrocalamus (Soderstrom, 
1981b). 

As in many grasses with predominantly uni- 
sexual spikelets, there is a strong dimorphism 
between the male and female spikelets, although 
the glumes are identical in each kind of spikelet 
(Fig. 2). In Steyermarkochloa, the female spike- 
lets differ most significantly from the male spike- 
lets in that the former lack a flower and usually 
a palea in the lower floret, and the lemma and 
palea of the second floret are greatly enlarged, 
curved, more abundantly nerved, and spongy- 
thickened (Fig. 2C, D). Nervation of the lemmas 
and paleas, although somewhat variable, differs 
significantly in the different types of spikelets. In 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


dorsal view 


.—F. Male spikelet at early anthesis, e 36621 
with the lowest bract the back of the upper glume; x6.5. [A, B: based on Maguire, Wurdack & Bunting 
; C-F: based on Huber 2620 (holotype, MO).] 


male and bisexual spikelets, the lemmas of the 
male florets are predominantly 3-5-nerved. In 
female spikelets, the lower lemmas are 5-9- 
пегуе e second lemmas are predomi- 
nantly 9-11-nerved and only rarely 5-7- OF 
13-nerved. The differences are even more pro- 
nounced in the paleas which are almost always 
of the normal 2-keeled, 2-nerved type in male 
and bisexual florets, but convolute and (5-)7- 
11-nerved in female spikelets. 

Although we have made no direct observa- 
tions of this in the field, we believe that the spon- 
gy-thickened lemma and, especially, palea of the 
female spikelets are adaptations for dispersal 0 
the fruits by water. It is likely that the spongy 
tissue provides enough buoyancy to the — 
spikelet to enable it to float for some —€— oe 
Presume that fruit producti d dispersal wo 


we 


(Мог. 71 


reenact 


— 


| 
| 
| 
! 
| 
l 
| 
| 
| 
| 


1984] DAVIDSE & ELLIS 


1 1001 


Е 3. жык unifolia Davidse & Ellis. —A. Male floret just = anthesis with lemma and 
x13.— 


d; stamens two 


petas initis and sep: 


male ‘deans мене the lemma removed; stamens two with united ime х9, 5.—C. Gynoecium of 


Separa 


female s te at anthesis with a long united style; x6.5. —D. Young flower of a bisexual floret; stamens with 


LN 5 


arate Amen style short; x11.5. 


ulis take place during the latter part of the 

Fi season while the habitat is still flooded but 

Irect observations are lacking. 

: Unfortunately, only one mature caryopsis was 

Ound in all specimens presently available (Fig. 

k ). For this reason the im internal em- 

bi characteristics (Reeder, 195 7) could not be 
*rmined. In its overall shape, the caryopsis 


2 —E. Car 
*9. [A-D: based on Davidse 16848 (MO); E: “after Huber 2620 (holotype, МО).] 


, 


most closely resembles the type found in terete, 

1-flowered spikelets such as Aristida. The linear 
hilum is the normal type found in the Arundi- 
noideae, but the relatively small embryo is un- 
usual for that subfamily, although not unknown. 
Also unusual is that the embryo appears to oc- 
cupy the entire lower portion of the caryopsis 
rather than only the abaxial face, as is typical for 


1002 


of the adaxial and abaxial chlorenchyma groups 
x 250.— 8. Adaxial first order vascular 
interference contrast; x 400. la — lacuna; 


grasses. However, the demarcation of the em- 
bryo in the single caryopsis available to us is not 
sufficiently clear to establish the morphology un- 
ambiguously. It will need to be confirmed when 
better material becomes available. The combi- 
nation of a linear hilum and small embryo is 
most characteristic of the Pooideae and Bam- 
busoideae. 


LEAF ANATOMY 
LEAF IN TRANSVERSE SECTION 
Leaf blade (Figs. 4—8) 


S. ЖЕЕ | 41 Г. 1 


ing to 180° (Fig. 4); outline elliptical in infolded 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


separa 
bundle (1'vb) an 
; Im = leaf margin 


[Vor. 71 


$e 
8 


8: 
r1 


® 
Ce ~ 


t у lacunae; note the a epi 
d associated abaxial third order vascular bundles (3’vb); 


; Mv = midvein; p = prickle. [Based on Davidse 16848.] 


condition—each half of the lamina with a flat 
adaxial surface and a rounded, outwardly bowed 
abaxial surface (Fig. 5); when infolded, adaxial 
channel with very deep, vertical sides—the two 
halves of the lamina becoming closely juxta- 
posed. Twenty-one costal zones in section, but 
due to the arrangement of many lateral vascular 
bundles in two planes, the total number of vas- 
cular bundles in section is 39 (Fig. 5). Leaf blade 
narrow (2.8-6.5 mm) but thick (> 0.5 mm). Ribs 
and furrows: no adaxial or abaxial rib or furrow 
development except in association with the me- 
dian vascular bundle. Median vascular bundle: 
distinguishable by location only; structurally 
identical to the lateral first order vascular bun- 
dles; closely associated with two groups of bul- 


1984] 


liform cells. Vascular bundle arrangement: two 
distinct rows of vascular bundles positioned at 
different levels or planes in the lateral part of the 
leaf section; abaxial row composed of third order 
vascular bundles only but the adaxial row con- 
sists of alternating first order vascular bundles 
and third order vascular bundles (Fig. 5.). First 
order vascular bundles slightly more centrally 
located than third order vascular bundles which 
are more adaxially located (Figs. 6, 7); abaxial 
third order vascular bundles all equidistant from 
the epidermis; 11 first order vascular bundles in 
section; no second order vascular bundles. Vas- 
cular bundle structure: first order vascular bun- 
dies elliptical; metaxylem vessel de, some- 
what angular with slightly thickened walls (Fig. 
8); lysigenous cavity and protoxylem vessel pres- 
ent; phloem adjoins the inner bundle sheath; di- 
vided by intrusion of sclerotic fibers (Fig. 6). Third 
order vascular bundles irregular in shape but g 
erally vertically elongated; xylem and phloem 
distinguishable (Fig. 7). Vascular bundle sheaths: 
first and third order vascular bundles completely 
surrounded by an inner bundle sheath; com- 
posed of relatively large and rather thin-walled 
cells (Fig. 8). Outer bundle sheath parenchy- 
matous; cells with slightly thickened (Fig. 8) and 
lignified (Fig. 6) walls; chloroplasts entirely ab- 
sent (Fig. 7). Outer bundle sheath continuous but 
with well-developed adaxial and abaxial exten- 
sions consisting of parenchyma cells on either 
side of the sclerenchyma fibers (Figs. 6, 7); triseri- 
ate arrangement in the center of the blade (Fig. 
7); a vertical girder is formed by these extension 


running the full thickness of the leaf blade in 


of _ a e 
vascular bundles; cavities distinct without 
aerenchvm 4 11 141 ас T. 1 ZU A ES 


DAVIDSE & ELLIS— STEYERMARKOCHLOA 


1003 


cells are present at regular intervals along the 
length of each lacuna; 8—10 lacunae in each half 
of the leaf blade. Colorless cells: absent, except 
those forming t dle sheath extensions. Adaxial 
epidermal cells: bulliform cells absent except for 
a single, well-developed group on either side of 
the median vascular bundle (Fig. 5); restricted 


with slightly thickene 
tercostal prickles present (Fig. 7), barbs not well 
developed; no macrohairs or papillae visible. 
Abaxial epidermal cells: no bulliform cells de- 
veloped. Epidermal cells large, very regular in 
hape and size with noticeably thickened outer 
tangential walls (Fig. 8); no prickles, macrohairs 
or papillae. 
Leaf sheath (Figs. 9-12) 

Outline: terete, solid cylinder (Figs. 9, 11); 39 
vascular bundles in section with 21 vascular bun- 
dles associated with the continuous epidermis 
and the remaining 18 vascular bundles in two 
centrally situated rows (Figs. 9, 11); vasculature 
identical to the leaf blade except that no adaxial 
surface is developed. Ribs and furrows: not de- 
veloped. Median vascular bundle: a single first 
order vascular bundle equivalent to the median 
vascular bundle of the leaf blade distinguishable 
as is the region corresponding to the leaf margi 


argin 
(Figs. 9, 11). Vascular bundle arrangement and 
structure: the same as for the leaf blade. Vascular 
L 11 1. 1. е4 PS ^" x +1 LÀ 41 1 fblade 


except that the abaxial extensions are not in con- 
tact with the epidermis (Fig. 12); in the region 
ofthe ligule thi tact i de (Fig. 10); adaxial 
extensions of the central vascular bundles not in 
contact with an epidermis but with a system of 
additional lacunae in the center of the fused leaf 
sheath. Sclerenchyma: no strands or girders in 
the sheath proper (Figs. 11, 12) but there is a 
tendency for the development of a hypodermal 
sclerenchyma layer (Fig. 12). Closer to the ligule, 
however, there are girders developed (Fig. 10) 
that are similar to those of the leaf blade. No 
*adaxial" sclerenchyma developed. Mesophyll: 
chlorenchyma not radiately arranged; cells 
rounded and tightly packed (Fig. 12); confined 
to narrow, g y 

to the epidermis (Figs. 11, 12); not in direct con- 
tact with the outer bundle sheath cells; no chlor- 
enchyma associated with centrally located vas- 
cular bundles. In the vicinity of the ligule the 
continuous chlorenchyma ring becomes subdi- 


є. 


ачали 


1004 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


FIGURES 9-12. Anatomy of the leaf sheath of St 
section. 9, 10. Sections taken from 


I. L1 e & Fil 


tra ers 
the region of the ligule. ә. Сїгсшаг ише of the fused sheath; x 40.— "10. 


of the lacunae; x250. ve 12. Sections of the leaf sheath taken sabbia Dele the ligule and the base.— AL. 
bun 


си г outline; note absence of culm; х 40.— 


cantinianc 


12. . Detail of the lateral vascular 


dles ч the —— 
a; lm = 


band adjacent to the epidermis; х 250. la = la 


of sheath ‹ EDO to the margin in the leaf blade; mv = region of sheath equivalent to the E ено 


rege 
of leaf blade. [Based on Davidse 16848.] 


vided by sclerenchyma girders in contact with 
the epidermis (Fig. 10). Lacunae developed as in 
= leaf blade (Fig. 12) with an additional nine 

als being located in the central core of the 
pileo sheath (Figs. 9, 11). Colorless cells: 
absent. Adaxial epidermal cells: adaxial epider- 
mis not developed. Abaxial epidermal cells: no 
bulliform cells (Figs. 9, 11). Epidermal cells large, 
very regular in shape and size (Fig. 12); no mac- 
rohairs, prickles or papillae. 


LEAF EPIDERMAL STRUCTURE 


Abaxial epidermis of the leaf blade 
(Figs. 13, 14) 


Intercostal long cells: elongated cells with side 

s more or less parallel (not angled outwards); 
anticlinal walls heavily thickened and pitted (Fig. 
14); undulations irregular and slight; individual 
cell shape and size somewhat irregular but, 


nevertheless, constant throughout each and all 
intercostal zones (Figs. 13, 14); successive long 
cells never abut one another but are always sep- 
arated by stomata or short cells. Stomata: con- 
sistently low dome-shaped (Fig. 14); as many 
files of stomata as there are files of cells in each 
intercostal zone (Fig. 14). All intercostal long cells 
actually function as interstomatal long cells and 
either are in contact with stomata at both ends 
or sometimes only one end; usually only one 
interstomatal long cell between consecutive sto- 
mata іп a file (Fig. 14). Intercostal short cells: 
single or silico-suberose couples; cork cells 
rounded (Fig. 14); irregular occurrence through- 
out intercostal zones. Papillae: absent. Prickles: 
not observed. Microhairs: not seen. Macrohairs: 
absent. Silica bodies: costal bodies tall, saddle- 
shaped (Fig. 14); present throughout costal zones. 
Intercostal silica bodies irregularly rounded. 
Costal zones: composed of long cells longer than 


——s 


NM 3 


= ndi 
Lp EIL 
Sr ш ТУШЕ 
ERA at 


“= 


DAVIDSE & ELLIS— STEYERMARKOCHLOA 


о. 


1005 


|] ~“. LH Th 


Costal and intercosta 


1 zone dist 
tal sto 


hi & Ellis. 13, 14. Abaxial 
ribution and arrangement; x160.— 14. 
mata and short cells and the costal silica bodies; 


he costal and intercostal zones; note 
xial 


ime 


E ofthe intercostal zones but equally as wide; 

ín Separated by paired short cells; six files per 

- zone (Fig. 13); all files of similar compo- 
on, 


Adaxial epidermis of the leaf blade 
(Figs. 15, 16) 


оно! long cells: same as for the abaxial 
ace but tend to be slightly longer (Fig. 16). 


X е 
4 osta zones virtually absent due to the development of a hypodermal 
matal distribution and structure; pitted thickening of cell walls; x 400. [Based on Davidse 168 


band of chlorenchyma; x1 
48.] 


Stomata: regularly low dome-shaped (Fig. 16); 
arrangement as in the abaxial epidermis. Inter- 


prickles do occur (Fig. 15); small with the bases 
shorter than the stomata; barbs developed ba- 
sally from the apex to the base; barb longer than 
the base (Fig. 16) usually not staining well. Mi- 


1006 


crohairs: none visible. Macrohairs: absent. Silica 
bodies: tall, saddle-shaped as in the abaxial sur- 
face (Fig. 16). Costal zones: narrower than on the 
abaxial surface (Fig. 15), consisting of only four 
files of cells; costal cells somewhat shorter and 
more inflated than on the abaxial surface (Fig. 
16). 


Abaxial epidermis of the leaf sheath 
(Figs. 17, 18) 


Intercostal long cells: as for the leaf blade but 
pitting very evident (Fig. 18). Stomata: as in the 
leaf blade. Intercostal short cells: identical to those 
of the leaf blade but the intercostal zones much 
wider (Fig. 17). Papillae: absent. Prickles: very 
few asperites seen without development of barbs 
(Fig. 18). Microhairs: none seen. Macrohairs: ab- 
sent. Silica bodies: tall, saddle-shaped as in the 
leaf blade (Fig. 18). Costal zones: largely absent 
(Fig. 17) and only present in the region equiva- 
lent to the leaf margin in that part of the sheath 
closer to the ligule. 


Scanning electron microscopy of the leaf blade 
(Figs. 19-26) 


Leaf outline: narrow midrib region connecting 
the two symmetrical halves of the lamina (Figs. 
19, 20). Slight ribs and furrows noticeable; as- 
sociated with the lateral vascular bundles. Long 
cells: rectangular abaxial cells with uniform width 
(Fig. 21); not distinguishable on the adaxial sur- 
face (Fig. 22). Stomata: low dome-shaped sub- 
sidiary cells on both surfaces (Figs. 25, 26) with 
the adaxial subsidiary cells being slightly wider 
(Fig. 26); not sunken or associated with papillae. 
Papillae: absent although reduced, unbarbed 
prickles on the adaxial surface may be mistaken 
for papillae (Fig. 22). Microhairs: no microhairs 
observed on any part of the leaf blade segments 
examined. Prickles: very few barbed prickles (Fig. 
23) observed in the region of the midrib on the 
abaxial surface; adaxial prickles common (Fig. 
22) ends are conspicuously blunted and not 
barbed (Fig. 24). Macrohairs: absent (Figs. 19, 
20). Silica bodies: abaxial silica bodies only vis- 
ible (Fig. 21); tall, saddle-shaped; indented in the 
leaf surface. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


ANATOMICAL DISCUSSION 


Steyermarkochloa is unique among the grasses 
in possessing a fused, solid, terete leaf “sheath.” 
Morphologically the cylindrical "sheath" grad- 
ually grades into the dorsiventral blade without 
evidence of a ligule. An anatomical interpreta- 
tion of this transition from sheath to blade is 
given in schematic form in Figure 27. The ma- 
terial available for anatomical study did not in- 
clude blade segments taken close to the ligular 
region, and thus the exact manner of opening of 
the leaf blade could not be determined anatom- 
ically. 

It will be noted that, even in the basal portions 
of the leaf “sheath,” true radial symmetry does 
not exist and regions equivalent to the midrib 
and leaf blade margins can be distinguished by 
the configuration of the vascular bundles and 
lacunae. Near the ligular region this assymmetry 
is still evident and the vasculature pattern re- 
mains identical. Even in the leaf blade itself, one 
can observe homologous vascular bundles ar- 
ranged in basically the same pattern as in the 
sheath. It must be noted that the diameter of the 
“sheath” decreases towards the ligule, a process 
that continues along the length of the blade. For 
comparative purposes this fact has not been in- 
corporated in Figure 27 but should be borne in 
mind. 

A comparison of the basal and ligular portions 
of the sheath reveal that the continuous cloren- 
chyma cylinder present in the lower parts be- 
comes subdivided by the development of scle- 
renchyma girders linking all the outermost 
vascular bundles with the epidermis. This epi- 
dermis is undoubtedly homologous with the 
abaxial epidermis of the leaf blade proper. In the 
leaf blade itself the conti lerenchyma band 
located internally to the chlorenchyma becomes 
reduced and eventually is lost, resulting in the 
chlorenchyma, lacunae, sclerenchyma girder, and 
epidermal configuration so typical of the leaf 
blade. 

Although not anatomically studied in this 
study, an adaxial channel is rapidly established 
commencing in the region of the ligule in the 
area equivalent to the leaf blade margin. In order 


d i uasa 


-— 


DAVIDSE & ELLIS—STEYERMARKOCHLOA 


abaxial 


3587 ER C 
| TC X $5 
a 


7 


aa Y. 


iat 


=o 
~~ 


Truncated blunt prickle from the adaxial surface.—25, 26. Stomata from the abaxial and adaxial surfaces; 
600. [Based on Davidse 16848.] 


1008 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Vor. 71 


leaf sheath - base 
S Sclerenchyma 
chlorenchyma 


E-] lacunae 


| parenchyma 


for this to be effected an adaxial epidermis is laid 
down, chlorenchyma is developed in the paren- 
chyma ground tissue, and the most centrally lo- 
cated lacunae are lost. Once the hannel 
has reached its full depth then a pair of bulliform 
cell groups on either side of the median vascular 
bundle are developed and the anatomical struc- 
ture of the blade is complete. 

This unique leaf structure of Steyermarko- 
chloa deserves further intense investigation, and 
Pesca studies, ds particular, should be un- 
dertaken soon as living material becomes 
available. This leaf с: probably represents 
a highly advanced and derived condition. 


CONCLUSIONS 


Agrostologists have recently recognized that 
leaf blade anatomical characters can be satisfac- 
torily used as the principal means of defining the 
five subfamilies of the Poaceae (Renvoize, 1981). 
These five groups can be characterized according 
to the unique combination of anatomical fea- 
tures common to their constituent species, and 
the оно of subfamilies is now firmly 

based u differences in leaf blade anatomy 
(Clifford k Watson, 1977). The anatomical di- 
agnoses of these subfamilies (Renvoize, 1981) 
should, therefore, provide a sound basis for the 
classification of Steyermarkochloa into the cor- 
rect subfamily. With this objective in mind, the 
various combinations of leaf blade anatomical 
characters that are diagnostic of the various 
subfamilies will be discussed and compared with 
the anatomy of Steyermarkochloa already de- 
scribed. 


The presence or absence, and the shape of mi- 
crohairs are constant features and provide valu- 
able indications of subfamily relationships (Clif- 
ford & Watson, 1977). Microhairs are present in 
all subfamilies except the Pooideae, in which they 
have not been recorded. In this respect Steyer- 
markochloa resembles the Pooideae. However, 
a few exceptions are known. In Pseudopentam- 
eris of the Arundinoideae microhairs are absent. 
Cortaderia selloana is the only recorded species 


+ 
FIGURE 27. Diagrammatic representation of фе) ~ 

anatomy of St 

illustrating the distribution of comparable tissues in 

different parts of the leaf sheath and blade. К» 

side of diagram is equivalent to the median 

bundle of the leaf blade and the right-hand Му сог- 

responds to the leaf margin 


| 


1984] 


which may vary for the presence ог absence of 
microhairs (Metcalfe & Clifford, 1968) and, very 
often, microhairs may be lacking from the abax- 
" — ks ни leaf blade in species with 

ous leaves such as many Merxmuellera 
ат (Ellis, 19802. 1980b). 

o microhairs were observed on either the 
abaxial or the adaxial leaf epidermides or on the 
leaf sheath epidermis of Steyermarkochloa (Figs. 
13-18). This finding was corroborated by a scan- 
ning electron microscopy examination of both 
surfaces of the leaf blade (Figs. 19—26). This total 
absence of. microhairs on the leaf. blade is sig- 


the pooid grasses. yros arundinoid lai 15 
not ruled out completely, however, but bam- 
busoid, chloridoid, or panicoid connections are 
remote. 

The shape of the stomatal subsidiary cells of 
Steyermarkochloa is clearly dome-shaped (Figs. 
14, 16, 18, 25, 26)—a condition considered to 
be characteristic of arundinoid grasses and only 
sometimes present in bambusoid, chloridoid, and 
panicoid grasses (Renvoize, 1981). Dome-shaped 
subsidiary cells do not occur in the Pooideae, in 
which the subsidiary cells are parallel-sided. Sto- 
matal shape, in contrast with the absence of mi- 
crohairs, does not support pooid affinities for 
Steyermarkochloa. 

The long cell walls of Steyermarkochloa are 
neither straight (as in the pooid grasses) nor clear- 


resembles the condition in several o 
dinoid reed-grasses such as Arundo, pina 
and Gynerium (Gordon-Gray & Ward, 1971; 
Renvoize, 1981). An arundinoid relationship is 
again indicated. This similarity with the periph- 
eral, reed-like genera of the Arundinoideae ap- 
Pears to be significant and agrees with qs indi- 
cations of several other anatomical cri 

The silica bodies of RES Shick 
are tall, oblong or saddle-shaped, and often ad- 
jacent to crescent-shaped or oval cork cells, can 
also be accommodated in the arundinoid diag- 
nosis of Renvoize (1981). They definitely do not 
resemble the pooid, panicoid, or bambusoid 
types, and the saddle-shaped silica bodies of the 
Chloridoideae are меран equidimensional, 
Tather than elon 

The characters e the epidermis, therefore, in- 
dicate affinities of Steyermarkochloa with the 
Arundinoideae, but this conclusion must remain 


DAVIDSE & ELLIS— STEYERMARKOCHLOA 


1009 


somewhat tentative. The absence of microhairs 
makes a more definite decision impossible. A 
further search for microhairs on the sheaths of 
the fertile culms also proved negative. 

From the leaf blade anatomy, as seen in trans- 
verse section, it can be confidently inferred that 
Steyermarkochloa is definitely not bambusoid 
because the chlorenchyma is not comprised of 
arm cells, and fusoid cells are not present. Serial 
sections of the leaf blade clearly show that the 


(Figs. 6—8) arise from the breakdown of colorless 
cells and are, consequently, true lacunae and not 
fusoid cell cavities, because 


ent at intervals along the air canals. Stellate cells 
also occur in these cavities. Lacunae of this type 
are well known in the leaves of hygrophilous 
grasses. but appear to be of little inp او‎ in 


Thus 

iveria, of ti the Andropogoneae (Kammathy, а 
superficially resembles Steyermarkochloa іп the 
structure and distribution of the lacunae. In the 

oideae, lacunae have also been de- 
scribed in the midrib of the leaves of Gynerium 
sagittatum (Metcalfe, 1960; Conert, 1961) and 
the blade of Merxmuellera cincta (Ellis, 1982). 
Both these species are tall, reed-like grasses with 
M. cincta not conforming anatomically with the 
danthonoid grasses proper. In this respect Stey- 
ermarkochloa again resembles the arundinoid 
reed-grasses. 
The chlorenchyma cells of Steyermarkochloa 
do not have inward projecting invaginations of 
the cell walls (Fig. 8) and, consequently cannot 
be considered arm cells, which are diagnostic of 
bambusoid grasses. Instead, the chlorenchyma 
consists of cells that are smooth-walled, tightly 
packed, and isodiametric in shape and arranged 
in a nonradiate pattern (Figs. 7, 8). This non- 
radiate arrangement rules out the possibility of 
chloridoid or panicoid relationships (Ellis, 1977). 
Tightly packed, i cells 
are not typical of pooid grasses either. The me- 
sophyll cell shape and arrangement in Steyer- 
markochloa again resembles the condition in 
some arundinoid grasses such as Cortaderia sel- 
loana (Conert, 1961) and Merxmuellera cincta 
(Ellis, 1982). 

The bundle sheaths of Steyermarkochloa are 
double with the outer parenchymatous sheath 
devoid of chloroplasts. The absence of special- 

ized Kranz chloroplasts in either bundle sheath, 
duce with the nonradiate nature of the chlor- 


1010 


enchyma cells, most of which are not directly in 
contact with a bundle sheath cell, is enough to 
predict with confidence that Steyermarkochloa 
has the = зак ag А pbs pathway (Ellis, 1977). 
Once aga d out and 
метен) associations are most unlikely. All 
bambusoid and pooid grasses and most arun- 
dinoid grasses have the C, pathway (Renvoize, 
1981) 

Vascular bundles inserted at different levels in 
the leaf lamina, such as in Steyermarkochloa 
(Figs. 5—8), are very rare in the Poaceae and are 
only generally recorded from the midribs and 
keels of bambusoid grasses (Metcalfe, 1960). It 
is significant that in the bamboos and rices this 
complex system of vascular bundles is restricted 
to the keel and that the lateral vascular bundles 
are arranged in a single horizontal row. The only 
other grasses, in addition to Steyermarkochloa, 
in which the vascular bundles of the lamina have 
been reported to be in different planes in single 
sclerenchyma girders are Porteresia coarctata, a 
monotypic genus in the Oryzeae (Tateoka, 1965), 
Gynerium saggitatum of the Arundineae (Co- 
nert, 1961), and Merxmuellera cincta, an atyp- 
ical member of the Danthonieae (Ellis, 1982). 
Possible affinities between M. cincta and some 
of the arundinoid grasses have been discussed by 
Ellis (1982). Significantly, Gynerium, also an 
arundinoid reed-grass, and M. cincta share many 
characteristics with Steyermarkochloa. Apart 
y located vascular 
bundles in single sclerenchyma girders in the 


4h 
fr ош 


quently, anatomically strongly resembles Stey- 
ermarkochloa. 

The phylogenetic implications derived from 
leaf blade anatomy strongly corroborate those 
derived from features of the leaf epidermis. 
Arundinoid affinities are again suggested and an- 
atomical evidence suggests that Steyermarko- 
chloa is a peripheral genus of the Arundinoideae, 
and is best accommodated close to the reed- 
grasses such as Gynerium, Arundo, Phragmites, 
and TRysanolaena. All these genera are known 
to have som arundinoid anatomical 
characters, but Renvoize (198 1) did not consider 
these to be sufficient to justify the exclusion of 
these genera from the subfamily. This observa- 
tion further substantiates the placement of Stey- 
еттаткостоа in the Arundinoideae close to these 
other somewhat anomalous and peripheral gen- 
era 


- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


As noted earlier, we are in agreement with the 
practical approach to grass classification advo- 
cated by Renvoize (198 1), in — subfamilies 
are primarily based on a 
of the leaves, and tribes on gross morphological 
characteristics supplemented by information 
from cryptic characters. Having established with 
reasonable certainty on the basis of anatomical 
evidence that Steyermarkochloa is arundinoid, 
it now remains to establish its tribal affinity. For 
this purpose it is most useful to compare Stey- 
ermarkochloa with Renvoize's (1981) classifi- 
cation in which one large tribe, Arundineae, and 
seven small ones are recognized. 

In the Arundinoideae, Steyermarkochloa is 
unique in its combination of dimorphic culms, 
dimorphic leaves, solitary developed leaf with a 
cylindrical sheath lacking a ligule, polygamous 
breeding system, many-nerved, convolute palea, 
and 2-keeled glumes. On the basis of these im- 
portant differences, Steyermarkochloa clearly 
stands alone in the subfamily, and therefore trib- 
al status is warranted 

As noted earlier, Steyermarkochloa most 
closely resembles the Bambusoideae in having 
dimorphic culms and leaves, but the anatomy 
and morphology of the developed leaf defini- 
tively distinguish Steyermarkochloa from the 
bamboos. Developed bamboo leaves are usually 
flat, broad, lanceolate or linear-lanceolate, artic- 
ulate with the blade, petiolate, and ligulate. 

Grasses with a polygamous reproductive sys- 
tem are not known in the Arundinoideae and 
apparently not in the family. Connor (1979, 1981) 
in his extensive review of reproductive systems 
in the Poaceae did not list a single example. The 
predominance of unisexual flowers over bisexual 
flowers in Steyermarkochloa suggests that this 
represents a transitional stage in the evolution 
of unisexual from bisexual flowers. The breeding 
system in Steyermarkochloa is a good example 
of one of the intermediate steps in the model of 
the evolution of monoecism through a gyno- 
monoecious pathway that was proposed by 
Charlesworth and Charlesworth (1978) and dis- 
cussed by Connor (1981). It involves (1) a re- 
duction in male fertility i in | some bisexual Bowers 
to produce ), fol- 
lowed by (2) a reduction in 1 female fertility of the 
bisexual flowers to produce male flowers. In 
Steyermarkochloa step 1 of the model has been 
nearly completed. The lower florets of all female 
spikelets have completely lost all flowers, where- 
as the second floret has retained only female 


1984] 


flowers accompanied by staminodia. wei 
the model to its logical conclusion, the stam 
nodia would presumably be completely Bice 
nated in the ultimate step of this differentiation. 
Because the staminodia are always very sm 
and the female flowers occur only in morpho- 
logically differentiated female spikelets, we 
conclude that female unisexuality has been ge- 
netically firmly fixed in the genome of Steyer- 
markochloa. Step 2 of the model is apparently 
still in progress since all possibilities (2 bisexual 
flowers; 1 bisexual flower and 1 male flower; 2 
male flowers) are known. That this system seems 
to be moving in the direction of male unisexu- 
ality is indicated by the predominance of male 
flowers over bisexual flowers and by the inter- 
mediate condition of one male and one bisexual 
flower being more common than two bisexual 
flowers. 

Unisexuality is known in the Arundinoideae 
but is not very common. In the Arundineae, Gy- 
nerium and Lamprothyrsus are dioecious and 
Cortaderia is gynodioecious. A tendency toward 
floral simplification is also seen in Neyraudia and 
Phragmites, in which all florets are usually bi- 
sexual but the lowermost floret is sterile or 
sometimes male. In the Centosteceae, peta ie 
5 gynomonoecious whereas Zeugites and Cal- 
deronella are monoecious. Onis lai in itself 
has little utility as a tribal character because it 
has evolved repeatedly in unrelated groups of 
grasses (Connor, 1981). 

_Two-keeled glumes are unknown in the Arun- 
dinoideae but are common in many genera of 

dropogoneae and in Myriocladus of the Bam- 
busoideae. This similarity must have evolved 
independently because there is no other resem- 


bination of other characters ee: to inflores- 
cence and spikelet morphol although when 
considered individually hel characters are 

Own in other genera. Especially important in 
ы она аге rounded to somewhat dorsally 


DAVIDSE & ELLIS— STEYERMARKOCHLOA 


1011 


tendency for the palea to be rounded on the back 
and many-nerved, her than 2-keeled and 
2-nerved, when lodicules are lacking. Among 
elodiculate, nonbambusoid grasses, we are aware 

of only one species with a many-nerved palea, 
namely, Micraira sublifolia F. Muell., a moss- 
like grass from Queensland. In this species the 
palea is 5—7-nerved but remains 2-keeled. In the 
other seven described species of the genus, the 
paleas are 2-keeled and 2-nerved and also divid- 
ed to the base into two equal halves (Lazarides, 
1979). 

Among all other elodiculate, nonbambusoid 
grasses, the tendency is for the paleas to be of 
the normal 2-keeled, 2-nerved type (e.g., Munroa 
HEURE Phil 7. ing Shas pos rounded on the 

ack (e 4 atum L.), or com- 
pletely d (e.g., ат female plants of 


ough Steyermarkochloa anatomically re- 
Кге the reed-grasses Arundo, Gynerium, 
Phragmites, and Thysanolaena most closely, it 
is morphologically distinct in almost all char- 
acters of the leaves, inflorescence, spikelets, and 
flowers. This reinforces our decision to classify 
Steyermarkochloa in its own tribe. As is evident 
from the preceding discussion, many of the mor- 


Ene relationship with the Bambusoideae seems 
be definitively ruled out on the basis of ana- 
RS evidence. It seems likely, oda that 


possibly caryopsi 
of independent, parallel evolution, a process well 
established for other characters in the Poaceae. 
Furthermore, the highly specialized leaves and 

culms, spicate inflorescence, largely unisexual 
spikelets, lack of lodicules, and two stamens are 

the fam 

and it seems most likely | that Steyermarkochloa 


t below the 
бш, awnless lemmas, absence of lodicules, 


а 1 d tl lute, many- 
nerved palea of the female spikelet, which, to- 
већег with the second lemma, forms a tubular 
Structure, are correlated characters БЧ аге di- 
rectly related to terminal stigma exsertion. Mun- 
10 (1868) noted for the bamboos that there is a 


dibbidene. 
LITERATURE CITED 
ANDERSON, D. E 4. Taxonomy of the genus 
am Young Univ. Sci. 


y in Sporobolus rigens 
(Tr.) Desv. (Gramineae). Bot Not. 125: 344-360. 
CALDERÓN, C. E. & T. R. 1980. The 
genera of Bambu. soideae олсон) of the Ameri- 
can continent. Smithsonian Contr. Bot. 44: 1-27. 


1012 


CHARLESWORTH, B. & D. CHARLESWORTH. 1978. Pop- 
ulation genetics of partial male sterility and the 
evolution of monoecy and dioecy. Heredity 41: 
137-153. 

CHASE, A. 1929. The North American species of Pas- 

т. Со ntr. U.S. Natl. Herb. 28: i-viii, 1–310, 


Cuaron! W. D. 1967. Tabula 3642. Puelia coriaceae 

D. Clayton. Hooker’s Icon. РІ. gis 2): 1-5. 

Сток Н. Т, EL WATSON, 1977. entifying 

Grasses: Data, Methods and = Univ. 

на Press, St. 

Pan H.J. 1961. Die Systematiek pd Anatomie 

er Arundineae. J. Cramer, Weinhei 

s ead H.E. 1979. Breeding systems in i iic grasses: 
a survey. New Zealand J. Bot. 17: 547-574. 

1981. Evolution of reproductive systems in 

the Gramineae. Ann. Missouri Bot. Gard. 68: 48— 


ELLIS, R. P. 1977. Distribution of the Kranz syn- 


Panicoideae according to bundle sheath anatomy 
and cytology. Agroplantae 9: 73-110. 

Oa. Leaf anatomy of the South African 
Danthonieae (омса, П. Merxmuellera disti- 
cha. Bothalia 185-189. 

. 1980b. а anatomy of the South African 

Danthonieae (Poaceae). Ш. Merxmuellera stricta. 
Bothalia 13: 191-198. 

Leaf anatomy of dn South Меш 


——. 198 


Danthonieae (Р rxmuellera a 
dinaceae = M. cincta podani 14: 89 a 
N-G ; E A con- 


tribution id the knowledge of Phragmites in South 
rica, with parti (diee reference to Natal popu- 
lations. J. S. African Bot. 37: 1—30. 

Ниснсоск, А. 5. & A. ы 1950. Manual of the 
Grasses of the United States, 2nd edition. U.S. 
Government Printing Office, Washington, D.C. 

Huser, O. 1982. Significance of savanna vegetation 
in the Amazon Territory of Venezuela. Pp. 221 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


244 in G. T. Prance (editor), Biological Diversi- 
i a in the Tropics. Columbia Univ. Press, New 


ic 1969. Anatomy of Vetiveria zi- 
ADIRE MNA. Bull. Bot. Surv. India 10: 283- 
285. 


LAZARIDES, M. 1979. бесіда Е. Muell. (Poaceae, 
Micrairoideae). Brunoni —84. 

MCCLURE, Е. A. 1966. The M piis Harvard Univ. 
Press, Cambridge 

nera of bamboos native to the New‏ ا 
World (Gramineae: Bambusoideae). Smithsonian‏ 
Contr. Bot. 9: i-xi, 1-148.‏ 

МЕТСАТЖЕ, С. R. 1960. Anatomy of the Monocoty- 
ledons. I. Gramineae. Clarendon Press, Oxford. 

CLIFFORD. 1968. Microhairs on 
grasses. Kew Bull. 21: 490. 
Мане, W. 1868. A monograph of the papie- 
222 Tran: 


———— 


n. Soc. London 26: 1- 158, tab. 1—6. 
е. B R. 1957. The embryo in grass systematics. 
Amer. J. Bot. 44: 756—768. 
RENVOIZE, S. A. 1981. The лен Arundinoideae 
and its position in relatio: 


. Sucrea (Gramineae: Bam- 
ideae), anew sie from Brazil. Brittonia 33: 
198-210. 
. 198 1b. Some ilies trends in the Bam- 
busoideae (P n. Missouri Bot. Gard. 68: 
15-47. 


— ——— & С. E. CALDERÓN. 1974. Primitive forest 
grasses and evolution of the Bambusoideae. Bio- 
tropica 6: Hee З; 

STEYERMARK,J.A. 1982. Relationships of some Ven- 
ezuelan forest refuges with lowland tropical floras. 

82-220 in G. T. Prance (editor), Biological 
Diversification in the Tropics. Columbia Univ. 
Press, New York. 

TATEOKA, T. 1965. Porteresia, a new genus of Gra- 

mineae. Bull. Natl. Sci. Mus. 8: 405-406 


MEEN ee а ава 


OCCURRENCE OF CRYSTALS IN IRIDACEAE AND ALLIED 
FAMILIES AND THEIR PHYLOGENETIC SIGNIFICANCE! 


PETER GOLDBLATT,? JAMES E. HENRICH,? AND PAULA RUDALL* 


ABSTRACT 


1 4 1 los lat 


4*2 ће г 4 ДРА У + P Р | 


base d on previous reports of their — in several genera of both major subfamilies, and supple- 


mented here by further records in 75 o 


reported in ed 300 species of Iridaceae, e inch 


ca. 85 genera of the зге Styloids have now been 
32 


0 examined. These elongated crystals are lacking 


in a few scattered species but perhaps significantly from рана нај pies some closely allied genera. 


Fan, ilies and isolated genera possibly related to Iridacea 
loids are present in Gop Tecophilaeaceae and Campynemaceae 


including Geosiris and Isophysis, were also 


ariaceae have crystal sand. A few 
are absent in Geosiris. The difference 


in crystal types | taken together with some significant | differences in morphology suggest that кыр 


allied eith sugges 
at Campynemaceae may be better placed close to Melanthiaceae or Burmanniaceae. Jsophysis, "— 
thee stamens but a superior ovary, is мн best treated in its own ан of Iridaceae. Te- 


order i 1s supported. 


Data on the kinds of crystals of the calcium 
oxalate type (raphid 
occurring in plant tissues are widely scattered i in 
the literature and information concerning their 
distribution in the plant kingdom is not readily 
E i > Systema tty Although little i is pes 
about in plants, thei 
shape did location are often ve characters 
at different taxonomic levels (Franceschi & H 
ner, 1980). A brief mention by Metcalfe ( 1989 
that styloids (pseudoraphides) were particularly 
iar ce of Iridaceae seemed intriguing and 

rth further investigation to establish, as far as 
hti. reasonable, the frequency of styloids and 
Possibly other crystal types in the family. We 
have also surveyed the crystal characters in pu- 
tative relatives of — These include the 
monotypic Madagascan Geosiridaceae; Colchi- 
Caceae (Liliaceae: Colchicoideae): Uvulariace ceae 
(Liliace ceae-Uvulari asm 


sty loids, and 


api and Campynemanthe. The latter two 

Ta are variously assigned to Hypoxidaceae, 
debis ан (Dahlgren & Clifford, 1982), or to 
4 separate Campynemaceae (Dumortier, 1829: 


57-58; Dahlgren & Rasmussen, 1983) and have 
been suggested to be close to Iridaceae (Dahlgren 
& Rasmussen, 1983: 369-372). Uvulariaceae 
sensu Dahlgren & Rasmussen, postulated as an- 
cestral to Colchicaceae and to Iridaceae (Dahl- 


was proposed as close 
E by Hutchinson (1973), although there 
s little current support for his view. 


MATERIALS AND METHODS 


FAA-fixed living leaf samples were 
gathered аи at least one to а few species of 
many genera of Iridaceae from both subfamilies, 
ү pci including Sisyrinchioideae) and 
маздан mples were examined at Missouri 

наны Garden (МО) and Royal Botanic Саг- 
penes Kew (K). At MO samples were sometimes 
cleared in 5% NaOH for several hours or more 
until t ore often were 


cleared in household bleach. They were then 


Dahl 


mmentc 


' Supported by grants D" 78- 10655 and 81- 19292 from the Vue" лар расай Science Foundation. I 
for 


eat ating fo techn 


R.K 
for Suggestions including a p бен of Campynemaceae; and 3 бб grem for his independent examination 


0 the flowers of IsopAysis. 


ӨӨ 


. Krukoff Curator of African Botany, Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 


` Missouri Botanical Garden, Р.О. Box 299, St. Louis, Missouri 63166. 
Jodrell Laboratory, Royal Botanic аа Kew, Richmond, Surrey, Great Britain. 


ANN. MISSOURI Bor. GARD. 71: 1013-1020. 1984. 


1014 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


mounted immediately in glycerin or dehydrated 
through an alcohol series and permanently 
mounted in Canada balsam. At K samples were 
sectioned using a Reichert sliding microtome. 
Sections were stained in safranin and alcian blue, 
dehydrated through an alcohol series and mount- 
ed in Euparal. The samples were viewed between 
polarizing filters to detect the presence and type 
of crystals in the tissue. The sole species of 150- 
physis and Geosiris, one each of Campynema and 
Campynemanthe and several of Colchicaceae, 
Uvulariaceae, Liliaceae (sensu Dahlgren & Clif- 
ford, 1982) and Tecophilaeaceae (Table 1) were 
treated in the same way: at MO tor comparison: 
The genera an d Table 
1 together with the crystal types observed. 
Voucher or accession number information is 
available from the authors but is not reported 
here. 


OBSERVATIONS 


Slender styloids of the doe first described for 
Iridaceae in Iris, Crocus, Romulea, Witsenia, and 
Gladiolus by ition (1862s; 1863b, 1865) and 
later by Rothert and Zalenski (1899) (see Neto- 
litsky, 1929 for an early review) and in several 
other genera more recently (see below) were found 
in the leaves of uo | majority of species examined 
but notably not 
related genera. л styloids are typically long and 
slender, with pointed or forked ends (Figs. 1, 2, 
7) or occasionally square ends (Figs. 3, 4). They 
are strongly birefringent and vary considerably 
in size, the length being 100 to 200 (to 300) um 
or sometimes much longer. 

In a few species (Patersonia macrantha, P. se- 
ricea, P. umbrosa, Romulea atrandra) short, more 
or less isodiametric crystals, 16 to 25 um long, 
were observed (Fig. 8) of the type described by 
de Vos (1970) in Romulea and Rudall (1983) in 
Dietes. In transverse section styloid crystals ap- 
pear more or less square (Fig. 6) or rectangular 
(Fig. 5), occasionally with the longer walls con- 
vex. They occur both in the outer vascular bun- 
dle sheaths (Fig. 6) where they are difficult to 
detect in cleared leaves, and in scattered crystal 
idioblasts in the mesophyll (Fig. 5), usually in 
the outer chlorenchymatous layers if the leaves 
are very thick, observed also by de Vos (1970, 
1974). 

Crystal sand was noted in only two of several 
species of Sisyrinchium examined. This is the 
only record of crystal sand in Iridaceae. 


[VoL. 71 


TABLE 1. Species examined for crystals: st = sty- 


loids; cs = crystal sand; rb = raphides; Ca 


carb = cal- 


cium carbonate; x = no crystal inclusions seen. Brack- 
ets promi Pip type observed in some specimens, 


but n 


Campynemaceae 


Campynema linearis Labill. 


Campynemanthe viridiflora Baill. 
Liliaceae 
Calochortus tiburonense A. J. Hill 


Erythronium ae: Nutt. 
Lilium canadens 


Colchicaceae 


Ornithoglossum sp 


Baeometra inpr J e G. Lewis 


Gloriosa carsonii Bake 


Uvulariaceae 
Disporum hookeri (Torrey) Nicholson 


D. maculatum (Buckley) Britt. 
D. sessile Don 


Schelhammera pedunculata F. Muell. 


Streptopus amplexifolius DC. 
Tricyrtis affinis Makino 

T. latifolia Max. 

Uvularia sessilifolia L. 


Geosiridaceae 


Geosiris aphylla Baill. 


Tecophilaeaceae 


Cyanella lutea L. oe 
Walleria mackenzi 


yanastrum nar deg Oliver 
Iridaceae-Isophysidoideae 


Isophysis tasmanica (Hook.) 
T. Moore 


Iridaceae-Ixioideae 
Anapalina caffra (Ker ex Baker) 
G. Lewis 


Anomalesia cunonia (L.) N. E. Brown 


A. saccata (Klatt) Goldbl. 


Anomatheca fistulosa (E. Meyer 


A. verrucosa (Vogel) Goldbl. 
A. viridis (Aiton) Goldbl. 
Antholyza ringens L. 
Babiana erectifolia G. Lewis 
B. odorata L. Bolus 


B. virginea Goldbl. 
Chasma aed erigi gei (L.) 
N. E. B 


cs 
cs 
cs 


а 
b & cs 


Ame GG? Ga > S9 29» 


=> => 


=> 


=> => => => => 


1984] GOLDBLATT ET AL.—CRYSTALS IN IRIDACEAE 


TABLE 1. Continued. 


TABLE 1. Continued. 


1015 


C. bicolor (Gasp.) N. E. Brown 
C. floribunda (Salisb.) N. E. Brown 
Crocosmia aurea Planch. 


masonorum (L. Bolus) N. E. Brown 


С. pottsii (Baker) N. Е. Brown 


е 
С. carpetanus Boiss. & Кеш. 
. etruscus Parl 


C. flavus Weston 
C. hadriaticus Herbert 
C. heuffelianus Herbert 


alyi Vis. 
C. pulchellus Herbert 


C. veluchensis Herbert 

C. vernus Hill 

Dierama igneum Klatt 

D. pictum N. E. Brown 

D. pulcherrimum Baker 

D. tysonii N. E. Brown 

Freesia andersoniae L. Bolus 

F. Ка бока (Burm. f.) 
E. 


F. fergusoniae L. Bolus 
Geissorhiza aspera Goldbl. 


fs 
5 
Е 
5 

= 
— 
Q 
©. 
а. 
z 


G. longifolia (G. Lewis) Goldbl. 
Gladiolus carmineus С. Н. Wright 

G. dalenii van Geel 

G. debilis Ker 

б. punctulatus Schrank 

G. scullyi Baker 


Brie. Wenn: (Hook. f.) 


H. hilos ica Baker 
Н. falcata (L. f.) Ker 


Н. petitiana (А. Richard) Baker 
Н. radiata (Jacq.) Ker 


Ho the pue (L. Bolus) 
Н. muirii (L. Bolus) N. E. Brown 


Ixia macular 
l. orientalis L. Bolus 


Н. priori (N. E. Brown) N. E. Brown 
a L. 


Lapeirousia anceps (L. £) Ker 
bainesii Baker 


Melasphaerula ramosa (Burm. f.) 
N. E. Brown 
Micranthus plantagineus (Pers.) 


Ecklo 
Oenostachys dichroa те 
О. oe 
O. zambez о Goldbl. 
ie ин (Baker) 


L. Bolus 
Radinosiphon leptostachya 
N. E. Brown 


Romulea atrandra G. Lewi 

R. bulbocodium Sebast. & JR 

R. flava (Lam.) de Vos 

R. grandiscapa J. Gay ex Baker 
rde 


R. rosea (L.) Ecklon 

Savannosiphon euryphylla (Harms) 
Goldbl. & Marais 

Schizostylis coccinea Backh. & 


Harvey 
Sparaxis grandiflora d Ker 


Sy er 
атана lapeirousioides (Baker) 
G. Lewi 


Т. чы (L.) С. Lewis 
Tritonia crocata (L.) Ker 


T. flabellifolia (Delaroche) G. Lewis 


T. florentiae (Marl.) Goldbl. 
T. laxifolia (Klatt) Benth. ex Baker 
T. watermeyeri L. Bolus 
doen parviflora (Jacq.) 

edd de 


TUA ai (Roto ex Klatt) G. Lewis 


Wanna aletroides (Burm. f.) Ker 


W. stenosiphon 
Zygotritonia crocea Stapf 


Iridaceae-Iridoideae 
(incl. Sisyrinchioideae) 


Alophia di lii (Graham) 


R. Foster 
Anomalostylus grandis (Kranzl.) 
R. Foster 


1016 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


TABLE 1. Continued. 


TABLE 1. Continued. 


[VoL. 71 


Aristea alata Baker 

А. compressa Buchinger 
A. ensifolia 

A. lugens (L. f.) Hort. 


Bobartia nin (L. £) Ker 
B. gracilis B 
Calydorea campestris (Klatt) Baker 


C. xiphioides د‎ Espinosa 

Cardenanthus tunariensis R. Foster 

Cardiostigma longispatha (Herbert) 
Bake 


си» frigidum (Роерр.) 
Кауе 


Cipura fava Ravenna 

C. paludosa Aubl. 

Cypella hauthalii ае К. Foster 

C. herbertii (Lindl.) Her 

С. linearis (H.B.K.) inier 

Dietes bicolor (Steud.) Sweet ex 
Klatt 


D. flavida Oberm 

D. robinsoniana (F. Muell.) Klatt 
Diplarrhena moraea Labill. 
Eleutherine bulbosa (Miller) Urban 
Ennealophus euryandrus (Gris.) 


Ravenna 
E. foliosus (H.B.K.) Ravenna 
Fosteria guatemalensis (Standl.) 
Ra 


venna 

F. oaxacana Molseed 

Galaxia fugacissima (L. f.) Druce 
Gelasine azurea cod an il 
G. coerulea (Vell.) Ra 

Herbertia lahue (Molina) pomum. 
H. puchella Sweet Sweet 

Hesperoxiphion peruvianum Baker 
Homeria collina (Thunb.) Salisb. 


Larentia linearis (H.B.K.) Klatt 
Libertia caerulescens Kunth & 


Bouche 
L. chilensis (Mol.) Gunckel 
Poepp. 


M. neopavonia R. Foster 
M. spathulata n f.) xs 
M. tripetala (L. 
Nemastylis Ау Alesis Baker 
Neomarica caerulea (Ker) Sprague 
N. gracilis (Herbert) Sprague 
N. heloysa-mariae P. 
N. northiana (Schneev.) Sprague 
Nivenia corymbosa (Ker) Baker 
N. stokoei N. E. Brown 
Ona obscura (Cav.) Ravenna 
Orthrosanthus chimboracensis 

(H ) Baker 


nth. 
Patersonia fragilis (Labill.) Asch. & 
Graeb. 
P. glabrata R. Br. 
P. graminea Benth. 
P. juncea Lindl. 
P. longiscapa Sweet 
P. lowii Stapf 
P. macrantha орна 
Р. occidentalis К. В 
Р, -e 11 s. Gibbs 
P. pygmae dl. 
P. sericea » Br. 
P. umbrosa Endl. 
Phaiophleps biflora (Thunb.) 
R. Foster 
Pseudotrimezia barretoi R. Foster 
Sessilanthera citrina Cruden 
S. heliantha (Ravenna) Cruden 
Sisyrinchium acre Mann. 
S. alatum Hook. 
S. angustifolium Miller 
S. cuspidatum Poepp. 
S. chilense Hook. 


5. filifolium Gaudich 

S. grandiflorum Dougl. ex Lindl. 

S. idahoense Bicknell 

S. junceum E. М 

S. longipes (Bickn.) Kearney & 
Peebles 


S. macrocarpum Hier. 
S. micranthum Cav. 


preng. 
Solenomelus sisyrinchium (Gris.) 
Pax ex __Рах ex Diels 


: ar * D ERR “Oe Ge aR мы =“ RS и Saas 453 2 


1984] 
TABLE 1. Continued. 

S. pedunculatus (Gill.) Johnston st 
Sphenostigma mexicanum R. Foster st 
S. sellowianum (Klatt) Baker st 
Tapeinia pumila (Forst. f.) Baill. st 
Tigridia bicolor Molseed st 
T. dugesii S. Wats. st 
T. huajuapanensis Molseed ex Cruden st 
T. meleagris (Lindley) Nichols. st 
T. pavonia (L. f.) DC. st 
T. orthantha (Lemaire) Ravenna st 
T. seleriana (Loesener) Ravenna st 
Trimezia martii (Baker) R. Foster st 
T. martinicensis (Jacq.) Her st 
T. sincorana Ravenna st 
T. steyermarkii R. Foster st 
Witsenia maura Thunb. st 


The unusual Tasmanian relict Isophysis, often 
associated with Iridaceae because of its equitant 
leaves and three stamens, but a superior ovary, 
also has styloids, although not in all specimens 
examined. 

In contrast, Campynema and Campyne- 
manthe have typical raphides and no styloids. 
Members of Colchicaceae examined lack true 
raphides but have crystal sand. Crystal sand (de- 
scribed by Netolitsky, 1929) consists of small 
and scattered globose to ovoid birefringent gran- 
ules. Uvularia к 


g crystals. 
Two species of Disporum and one of Streptopus 
have both raphides and crystal sand, while a third 
Species of Disporum has crystal sand only. A 
Single species of Uvularia examined has a few 
scattered crystals that may be crystal sand and 
m Schelhammera we found no crystalline inclu- 
sions at all. The two species of Tricyrtis and the 
single species each of Erythronium and Lilium 
(both Liliaceae) studied here, have what appear 
to be large round crystals of calcium carbonate 
(the tissue bubbles in bleach and even more when 
dilute hydrochloric acid is added). No crystals 
were seen in Calochortus. 

3 Мо crystals of any kind were detected in Geo- 
siris but because this monotypic genus is a non- 
green leafless saprophyte the comparison of its 
leaf scales with the green fully developed leaves 
of other species may not be valid. 

Raphides were noted in Cyanellaand Walleria 
(Tecophilaeaceae) but no crystals of any sort were 

en in Cyanastrum, a genus often treated as а 

Separate family, Cyanastraceae. 


GOLDBLATT ET AL.—CRYSTALS IN IRIDACEAE 


1017 
DISCUSSION 


The occurrence of styloids already noted by 
Metcalfe (1961), Hegnauer (1963), Gibbs (1974), 
and others to be a peculiarity of Iridaceae, ap- 
pears to be a fundamental and nearly universal 
characteristic of the family on the basis of a sur- 
vey here of some 240 species in 75 genera. Our 
data supplements previous reports of styloids in 
the Ixioid genera Crocus, Romulea, and Gladi- 
olus (Gulliver, 1863a, 1863b; Rothert & Zalen- 
ski, 1899) and in Romulea, Syringodea, Homo- 
glossum, and Tritonia (de Vos, 1970, 1974, 1976, 
1982: 30). In Iridoideae, styloids have been de- 
scribed in a few genera including Iris, Witsenia, 
and Belamcanda (Gulliver, 1863a, 1863b; Roth- 
ert & Zalenski, 1899; Frey, 1929; Wu & Cutler, 
in press), Ferraria (de Vos, 1979), and Dietes 


tals in sectioned leaves). Chodat and Balicka- 
Iwanowska (1892) observed large styloids ar- 
ranged longitudinally and surrounding vascular 
bundles in the leaves of many genera of Irida- 
ceae. The absence of styloids in Sisyrinchium 
leaves was first noted by Gulliver (1865) in 5. 
anceps, S. striatum, and 5. bermudianum and 
later by Rothert and Zalenski (1899) in S. ber- 
mudianum, and confirmed in 20 out of 21 species 
in this study. The lack of styloids in Sisyrinchium 
and also the closely related genera Phaiophleps 
and Chamelum may well have some significance 
for the systematics of those genera, although sty- 
loids do occur in Libertia and Tapeinia, also 
close to this alliance. Rudall (in press) also found 
styloids completely lacking in rhizomes of Sisy- 
rinchium, whereas they are present in under- 
ground stems of most genera of Iridaceae. Apart 
from this, the occasional absence of styloids in 
a few scattered species appears to have no sys- 
tematic relevance. The size and shape of crystals 
in Iridaceae is also somewhat variable. The oc- 
currence of cuboidal crystals (Fig. 8) in a few 
A ылы: а 
crystal shape may depend to some extent on the 
shape of the crystal idioblast enclosing it (Fran- 
ceschi & Horner, 1980). However, Wu and Cu- 
tler (in press) have found that styloid shape and 
size in Iris may well be taxonomically useful at 
the species level. 

Styloids are relatively rare in the monocoty- 
ledons but are also characteristic of Agavaceae, 
Phormiaceae, and a few other families or sub- 


1018 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


FIGURES 1-8. Crystals in Iridaceae. x 2. Trimezia sincorana, E with а syi in LS leaf. (1. 


Polarized. 2. Bright field). x 700.—3, 4. Patersonia longiscapa, crystal with square ends in LS leaf. (3. m 
4. Bright field). x 700. —5. Gladiolus daleni, leaf TS. Crystals (arrowed) in scattered mesophyll cells. x 630.— 6. 
Crocus cancellatus, leaf TS. Crystals (arrowed) in vascular bundle sheath. x650.—7. Geissorhiza 


aspera, 
scanning electron micrograph. Crystals е mesophyll cells. х 500.—8. Patersonia umbrosa, leaf surface, 
showing cuboidal crystals (arrowed) immediately beneath epidermis, over veins. x 1,400. 


families of Asparagales (Dahlgren & Clifford, The discovery of raphides in Campynemaceae 
1982: 92). They have not, however, been re- appears to be the first report for the family and 
corded in any members of Liliales sensu stricto crystal sand appears not to have been recorded 
except Iridaceae. previously in Colchicaceae. Genera of Colchi- 


1984] 


caceae have long been known to lack raphides 
or styloids (Hegnauer, 1963; Gibbs, 1974). In 
Мр data КЕН кел аге contradic- 

ry, Hegnauer reporting raphides here but both 
pe (1974: 1915) na Эше» (1977) point out 
their absence, a condition we confirm. The few 
examples of the Uvulariaceae we examined in- 
dicate that the alliance as circumscribed to in- 
clude Tricyrtis, and the Disporum- Uvularia ий 


ofgenera, crystal types. er 
raphides and scattered crystel un occur rrr 
topus, Di. (Uvularia, 


Disporum) or no саип oxalate type crystals at 
all (Schelhammera, Tricyrtis) but possibly cal- 
cium carbonate in Tricyrtis. Gibbs (1974: 1915) 
has also reported raphides in Streptopus. The 
single мна Facit is Erythronium and Lilium 
(both d here, also have what ap- 
pear to be large round crystals of calcium car- 
bonate. 

The different crystal types found in Colchi- 
caceae, Uvulariaceae, and Campynemaceae con- 
tribute little to our understanding of their rela- 
tionships to Iridaceae but in our view, do 
constitute evidence for the continued separation 
of Campynema and Campynemanthe from Iri- 
daceae. In general raphides may be considered a 
primitive feature in flowering plant groups 
(Tomlinson, 1962). The presence of styloids or 
crystal sand is rare and presumably derived and 
the styloids of Iridaceae are consistent with the 
specialized position of Iridaceae in Liliales. 


also differ from Iridaceae in the basic leaf form, 
having bifacial rather than monofacial equitant 
eaves, and in having six stamens. Campyne- 
manthe also has a distinctive type of axile pla- 
centation in which the seeds remain attached to 
the vasculature of the central axis after dehis- 
cence or disintegration of the capsule. 

Isophysis shares with Iridaceae not only the 


Stamens, but also the distinctive styloids that 
appear fundamental in the family. It differs no- 
tably from Iridaceae only in | having a superior 
Ovary. Early f Isophysis 
are а the inner tepals (Bentham & Hook- 
ет, 1883) and hence пої comparable with Iri- 
daceae are incorrect. We have examined the lim- 
ited material available to us and confirm the 


GOLDBLATT ET AL.—CRYSTALS IN IRIDACEAE 


1019 


statement by Krause (1930: 260) that the sta- 
mens are opposite the outer tepals. It now seems 
desirable to include Jsophysis in Iridaceae on the 


s 
4 tact + +} > eae | р у 


whose affinities to the other subfamilies are dis- 


1. 
Similarities between Colchicaceae and Irida- 


restricted to the presence of a cormous rootstock 

in both families (Dahlgren & Rasmussen, 1983). 
However, we believe that it is very likely that a 
rhizome is the basic type of rootstock for Iri- 
daceae and that corms evolved at least twice in 
the family. In Ixioideae, the corm is basal rooting 
and has a stele, whereas in some specialized Iri- 


predominantly unspecialized characteristics, 
several of which are often treated as a separate 
subfamily Sisyrinchioideae. We are uncertain 
whether the corm is basic in а Colchicsceae, but 
ts stru rom that 
of the corm n types found in Iridaceae and, given 
our hypothesis that a rhizome is basic in Irida- 
ceae, the presence of corms in other families ap- 
pears irrelevant in questions of phylogenetic re- 
lationship. The absence of styloids and the 
presence of crystal sand in Colchicaceae seems 
to remove this family even further from a pos- 
sible close affinity with Iridaceae. Dahlgren's sug- 
gestion (pers. comm.) that Colchicaceae and Ir- 
idaceae may be independently derived from 
Uvulariaceae has merit although it is more dif- 
ficult to see similarities with Iridaceae than Col- 
chicaceae. In this connection it seems significant 
that Uvulariaceae is heterogeneous for crystals 
and provides a possible link between ancestors 
with the primitive condition of raphides alone 
and derived lines with specialized crystal types 
Although Tecophilaeaceae are not seriously 
considered to be allied to Iridaceae, and have 
been assigned to Asparagales by Dahlgren and 
Clifford (1982) rather than Liliales, the family 
was included in this study. The finding of typical 
raphides, very common in Asparagales, is con- 
sistent with their placement in this order on the 
basis of their phytomelan encrusted seeds and 
introrse anthers. The absence of any crystals in 
Cyanastrum, already recorded by Dahlgren and 


1020 


Clifford, in contrast to Cyanella and Walleria, 
lends some support to its treatment as a separate 
family, for example by Dahlgren and Clifford. 


LITERATURE CITED 


BENTHAM, G. & J. D. HOOKER. 1883. Genera Plan- 
each 3 (2). Reeve & Co., Lon 

Снор а. BALICKA- IWANOWSKA. 1892. La 
rate ep des Iridées, essai d’anatomie systématique. 

J. Bot. Меш 220-232, 253-267. 

ш до. R. & H. T ‚ CLIFFORD. 1982. The Mono- 
'otyledons: AC 
London. 


. RASMUSSEN. 1983. Monocotyledon evo- 
lution: characters and phylogenetic states. Evol. 
55-388. 


. 1970. Bydrae tot die morphologie en 
anatomie A Romulea II. Die blare. J. S. African 
Bot. 36: 27 
1974. я Suid-Afrikaanse genus Syringo- 
dea. J. S. African Bot. 40: 201-254. 
1976. Die Suid-Afrikaanse spesies van Ho- 
moglossum. 1 2 bs Afri rican Bot. 42: 301-359. 
——. 1977 


van die ossis en die systematiese posisie. 

Tydskr. Pp only esses -19. 

. 1979. The African genus Ferraria. 1. S. Af- 

rican Bot. is 295-375. 

1982. Die bou en ontwikkeling van die un- 
pee blaar van Tritonia en vewante genera. J. 

can Bot. 48: 23-37. 

Du B.-C. 1829. тю des Famille des 

PI 


- 1980. Calcium 
te crystals in plants. Bot. Rev. (Lancaster) 
46: 361–427. 

Frey, А. 1929, Calciumoxalat-Monohydrat und 
Trihydrat. Handb. Pflanzenanat. 3(1): 81—118. 
GIBBS, аа D. 1974. Chemotaxonomy of the соц 

ts. 1 & 3. McGill-Queens Univ. Press, Mon 


Женс 
GOLDBLATT, P. 1976. The genus Moraea in the winter 
ern Africa. Ann. Missouri 


—780. 
. Corm morphology in Hesperantha (Iri- 
e, 


onomy. Ann. Missouri Bot. Gard. 69: 370-378. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


GULLIVER, С. 1863a. On the ди» of British plants. 
Ann. Mag. Nat. Hist. 11: 13-1 

On raphides and “phaerapides of 

Phanerogamia; with a notice of the crystal prisms 

of Iridaceae. Ann. Mag. Nat. Hist. 12: 226-229. 
1865. Observations on raphides and other 

crystals in plants. Ann. Mag. Nat. Hist. 15: 38- 

40 


——. 1863b. 


HEGNAUER, R. 1963. тања move 
. Monocotyledonae. Birkhauser, 

HUTCHINSON, J: 1973. The Fa milies уе Flowering 
Plants. 3rd edition. Clarendon Press, Oxford. 
Krause, К. 1930. Liliaceae. In A. Engler & К. Prantl 

(editors), Nat. Pflanzenfam. 15a. Leipzig, Engel- 


МЕТСАІЕЕ, C. R. 1961. General introduction with 
special reference to recent work on monocotyle- 
y In Recen t Advances in Biology 1. Lectures 

ymposia, IX International Botanical Con- 
cdi мота 146-150. Univ. of Toronto Press, 


oronto. 
NETOLITSKY, F. 1929. Die Kalksalze als Zellinhalts- 
0-80. 


aene (Sparm.) Harv J. S. African Bot. 25: 357- 


Mr W. & W. ZALENSKI. 1899. Ueber eine be- 
sondere Kategorie von Krystallbehaltern. Bot. 
Centralbl. 80: 241—251. 

Еџрам, P. 1983. Leaf anatomy and relationships of 
Dietes (Iridaceae). Nordic J. Bot. 3: 471-478. 

п press. Taxonomic and е» =й 

plications of rhizome structure and secon 

thickening in Iridaceae. Bot. Gaz. но. 
ville 


STERLING, C. 1977. Comparative morphology of the 
lo the Liliaceae: Uvularieae. Bot. J. Linn 
45-354. 


Strip, A. К. 1974. A taxonomic revision of Bobartia 
L. (Iridaceae). Opera Bot. –45. 

TOMLINSON, Р. B. 1962. Phylogeny of Scitam 
morphological and anatomical D iion. 
ees 16: 192-213. 

Wu, Q.-G. & D. Е. CUTLER. In . Taxonomic 
evolutionary and ecological поена e of the leaf 
anatomy of rhizomatous Jris species. Bot. J. Linn. 


A REVIEW OF EUPHORBIA (EUPHORBIACEAE) 
IN BAJA CALIFORNIA! 


MICHAEL J. Hurr? 


ABSTRACT 


Study of the "Мета collections from Baja California reveals that there аге at least 13 species of 
. la, 


E uphorbia (exclud 


i Chamaesyce) there. Euphorbia chersonesa Huft, E 
scribed 


ro 
ecent “Flora of Baja California,” is reinstated. 


The taxonomy of subgenus Poinsettia i is updated, and a key to all Baja California species of Euphorbia 
ided. 


is provi 


In the recent “Flora of Baja California” (Wig- 
gins, 1980), seven species of Euphorbia are rec- 
ognized (excluding the 26 species of subg. Cha- 
maesyce Raf., which I recognize as the genus 
Chamaesyce S. F. Gray, and which will not be 
further considered here). These are distributed 


examination of the available herbarium material 
shows that there are actually 13 species of Eu- 
phorbia in Baja California. Of the six additions 
reported here, two are species of western Mexico 
reported from Baja California for the first time, 


one was cited from Baja California when it was 
published but was not included in the Flora, two 
are described as new, and one was previously 
recognized as a variety of E. heterophylla L., a 
species to which it has no close relationship, and 
is here described as a new species. In addition, 
the treatment of subg. Poinsettia is updated to 

e into account the work by Dressler (1961) 
that cleared up much previous confusion in that 


group. 
The following key will distinguish the species 
of Euphorbia now known from Baja California. 


1. Glands of the misa cup-like or bilabiate, usually 1 or 2 (3-5 in E. pumicicola) (subg. Poinsettia). 
abia 


2. Glands bil 


· Bracts над. red at base; gland usually 1 per cyathium; seeds cylindrical, arid tuberculate 


oo Murr. 


3. Bracts ке or white at base; glands 3—5 per cyathium; seeds ovoid, angular, de бесни o 
2. 


Е. pumicicola Huft 


2. Glands ith circular opening, usually 1 per — bracts green, pale, or purple-spotted at 


never red; seeds ovoid, angular, coarsely tu 


1. ба of the involucre fiat or shallowly concave, we 4 or 5. 
olete in Е. ERES stipules minute, glanduliform; 
a). 


3 Е пандан И L 


rae ecarunculate (except i in E. eriantha) (subg. Agalom 


5. Plan 


6. lavet and piu glabrous; herbage glandular-pubescent; leaves gp ae appendages 


green, unlobed, am 


ensis Brandegee 


may 
6. Involucres and На pubescent; herbage not glandular; leaves ци or opposite; ар- 
bsolete. 


pendages white or green, lobed, di 
7. А 


vided, or nearly о 
ppendages nearly obsolete; leaves alternate; seeds coarsely tuberculate 


E. chersonesa Huft 


е. Peel N 3 lobed or divided; leaves mostly opposite; seeds shallowly pitted or smoo 
and 4 ed. 


8. Plant delicate; appendages 3-lobed, green, spreading; seeds shallowly and poire 


sienne кан 


nculate; capsules broader than long, densely tomentose T 
6. 


the an 
Cars авн Huft 


I wish to thank the curators of the following herbaria for making their collections available for study: CAS, 


Ds, Fan MICH, MO, NY, SD, UC, US. I also 


Department, Field Museum of rages His 
issouri Botani 


ANN. MISSOURI Bor. GARD. 71: 1021-1027. 1984. 


thank Ke 
their critical comments on the man eei s The illustration was prepared by Elizabeth Liebman, Exhibition 


tory. 
Louis, Missouri 63166. Mailing address: 
of Natural НИ Roosevelt Road at Lake Shore Drive, Chicago, Illinois 60605. 


Barringer, Annetta Carter, and Michael Nee for 


tany Department, Field Museum 


1022 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


8. Plant robust; appendages 5-10-fid, white, arching over the glands; seeds smooth, 4-angled, 


carunculate; capsules longer than wide, densely white-tomentose all over 


7. E. eriantha Benth. 


5. Plants shrubs or leafless wax-coated perennials. 


9. Leaves scale-like or lacking; stems in dense clumps, erect, covered with a thick wax coat .. 
8. E 


. ceroderma 1. M. Johnst. 


o 


ir 


12. Petioles stouter, ca. 0.5- 
ery, pale yellowish green 


. Leaves fully formed; stems woody, highly-branched. 
10. Leaves verticillate; cyathia disposed in c 
10. Leaves alternate; cyathia occurring singly in axils of leaves. 
1 


cymes 9. E. xantii Engelm. ex Boiss. 


10. E. misera Benth. 


= 
4 
8 
— 
a 
2 
= 
= 
б 
~ 
с 
o 
m 
5 
A. 
о 
< 
D 
od 
Б 
с 
E 


nder, ca. 0.4 mm diam. or less, С or exceeding blade i 

length; leaf blade thin, н gree Па. 

1 пт dui: shorter ois blade? leaf blade thick, leath- 
11 


alifornica Benth. var. boo 


b, E. поље i var. hindsii (Benth.) Wigg. 


4. Glands exappendiculate; stipules lacking; seeds carunculate (subg. Esula). 
13. Plant annual; glands elliptic, lacking horns; capsules verrucose; seeds reticulate .________----- 


13. Plant perennial; glands with 2 short horns; capsules smooth; seeds pitted .. 


SUBGENUS POINSETTIA (GRAHAM) HOUSE 


1. Euphorbia aa Murr., Comm. Gót- 
ting. 7: 81. 


This species is here reported from Baja Cali- 
fornia for the first time. It is the common weedy 
poinsettia of the eastern and central United States 
with red-based bracts and is also common in 
Mexico and Central America. It is often confused 
with the widespread tropical weed, E. hetero- 
phylla, but the two species are quite distinct, as 
was first clearly pointed out by Dressler (1961). 


Specimens examined. MEXICO. BAJA CALIFORNIA 
SUR: Sierra Lázaro, 10 Oct. 1893, Brandegee s.n. 
(NY, UC); San Bernardo, 13 Oct. 1893, Brandegee s.n. 

С). 


2. Euphorbia pumicicola Huft, sp. nov. TYPE: 


. 2,000 

merly 175 (holotype, DS 293876, photo- 

graph at F— neg. no. 58289; isotype, CAS), 

distributed as E. heterophylla L. sensu la- 
tior. 

Herba annua, glabra. Folia e obovata, infra 
mediam leviter ER. supra Hier serrata; stipulae 
obsoletae. Inflorescentia termi у-н cymo- 

racteae similes foliis caulinis, prope basin inter- 

thia 2-: m alta, orificio 1.7- 


ina ovoidea-angulata, eca- 
tuberculis humilibus obtusis. 

Erect taprooted annual, 15-20 cm high, gla- 

brous, sparsely branched. Stem 1.8-2.5 mm diam. 

at base. Leaves opposite, 2—4 pairs, the upper 


. E. spathulata Lam. 
13. E. palmeri Engelm. 


ones crowded below the inflorescence, the lowest 
ones above the middle of the stem; petiole slen- 

er, 1–1.5 cm long; blade obovate, green, shal- 
lowly lobed below the middle, serrate above the 
middle, 2-3.5(-4) cm long, 1-1.6 cm wide; base 

uneate; apex obtuse to acute; stipules lacking. 
Inflorescence a compact terminal cyme; bracts 
similar to stem leaves but smaller, to 1.5 cm long, 
green, often white or pale toward base. Cyathia 
campanulate, green, 2-2.7 mm high, 1.7-1.8 mm 
diam. at orifice; lobes 5, 0.5-0.7 mm long, €x- 
ceeding the glands, laciniate, white toward apex; 
glands 3-5, 0.2-0. 3 mm high, ca. 0.5 mm wide, 
bilabiate, 1 flowers са. 
10; bracteoles lacking. Styles 3, ca. 1 mm long, 
undivided or very slightly bifid; gynophore 
exserted from the cyathium 1.5-3 mm, nutant. 
Сирай ovoid-deltoid to subglobose, 2.5-3.5 mm 

high, 3-4.5 mm diam., green; seeds truncate- 
ovoid, 2-2.3 mm long, 2-2.3 mm diam., angular, 
bluntly pointed at hilar end, covered with low 
blunt tubercles, ecarunculate, brown. 


Euphorbia pumicicola may be distinguished 
from the other annual species of subg. Poinsettia 
by the combination of a glabrous plant body, 
opposite leaves, 3-5 bilabiate glands per Cy- 
athium, and angular, bluntly tuberculate seeds. 
In its small stature and possession of more than 
one gland per cyathium it is reminiscent of E. 
inornata (Dressler) A. Radcliffe-Smith of Peru, 
but that species differs by it preading hab 
it, alternate phyllotaxy, nearly entire leaves, and 
more nearly smooth seeds 

Euphorbia pumicicola is known only from the 
type, which was collected on a plateau thickly 
strewn with lava rocks (whence the name). ^ 


1984] 


more extended description of the habitat with a 
list of associated species is given by Johnson 
(1958: 235-236). 


3. Euphorbia heterophylla L., Sp. Pl. 453. 1753. 


Although Wiggins (1980) recognized three va- 
rieties of E. hete rophylla, including the typical 


commonly recognized variety, based on a spec- 
imen of E. cyathophora with narrow leaves. Both 
E. heterophylla and E. cyathophora exhibit a wide 
range of leaf shapes, none of which have any 
geographical integrity or any correlation with 
other characters. It is worth pointing out that 
although the varietal name is often cited as E. 
heterophylla var. graminifolia (Michx.) Engelm. 
(e.g., in Fernald, 1950; Macbride, 1951; Radford 
et al., 1968; Standley & Steyermark, 1949; Wig- 
gins, 1980), presumably based upon E. grami- 
nifolia Michx. (which is typified by another nar- 
row-leaved specimen of E. cyathophora), 
Engelmann in fact named a new variety without 
reference to Michaux's name. 

The other heterotypic variety recognized by 
Wiggins is E. heterophylla var. eriocarpa Millsp. 
The type specimen of this name does not even 
belong to subg. Poinsettia, as was pointed out by 
Dressler (1961), but rather represents an other- 
wise уа. species of subg. Agaloma and 
is described below (E. chersonesa). 

Euphorbia не which is such an ар- 
gressive weed elsewhere in its range, does not 
seem to be very common in Baja California, and 
apparently occurs only in the southern quarter 
of the peninsula. 


Specimens examined. МЕ BAJA CALIFORNIA 
, 


region, Nov. 
party Si erra de ў Giganta, 
Ry er (NE of Misión San Javier), 

са. 25°52'N, 111°32% уу, са. 800—8 Sept. 1965, 
Carter 4967 (UC); Sierra de la Giganta, V mesa- 
like slope of Cerro Gabilán, ca. 25°50¥4'N, 111°24%'W, 
ca. 1,200 m, 4 Oct. 1965, Carter 5108 UG: mq de 
la Giganta, N slope above cliffs near summit, Cerro 
del Barreno, = s of Valle de los Pado (5 side of 
6*03'N, 111°35%, са. 1,260 m, 


~ Sept. 1967. С & Moran 5341 (UC); Sierra de 
ane у -facing slopes 5 of Portezuela 


Росно Е scondido), са. 25507, 111°23'%, са. 875- 
m, 5 Oct. 1970, Carter & Moran 5539 (UC); Mts. 


HUFT— EUPHORBIA 


1023 


W of Boca de la Sierra, near 23°23'N, ees W, 390 
ray 30 Sept. 1967, Howe s.n. (SD); San José del Cabo, 
1 Apr. 1930, Johansen 507 (DS); Borrego Ranch, 2 
Sept. 1930, Jones s.n. (DS); Primer Agua, near Loreto, 

19 Oct. 1930, Jones s.n. (UC). 


SUBGENUS AGALOMA (RAF.) HOUSE 


4. Euphorbia chersonesa Huft, sp. nov. TYPE: 
Mexico. Baja California Sur: ca. 1.5 mi. S 
of Mission Dolores landing, near 25?05'N, 
110°54'W, са. 275 ft., E-facing slope, rhyo- 
lite, 4 Dec. 1959, Wiggins, Carter & Ernst 
270 (holotype, UC 1303223, photograph at 
F—neg. no. 58288; isotypes, DS, US). Fig- 
ure 1: d-f. 

Euphorbia ا‎ var. eriocarpa Millsp., Proc. 
Calif. Acad. Sci., Ser. 2, 2: 230. 1889 non E. 
eriocarpa Bertol., 1839. TYPE: Mexico. Baja Cal- 
ifornia Sur: Comondú, 21 Mar. 1889, Brandegee 
26 (holotype, F), Brandegee s.n. (probable iso- 
type, UC). 


ba annua, erecta. Folia alternata vel opposita, 
inferiora saepe fugacia; petiolus gracilis; lamina ovata 
i parum lobata, pubescens 


glabrata, grosse 
glanduliformes. Cyathia dense puberula; glandulae 4, 


mi inutae, integrae vel crenatae; flores masculos 10-1 2 
bracteolae obsoletae; styli 3, profunde furcati, basi li- 
bri, vix divergentes. Capsula exserta, dense puberula; 

semina ovoidea-angulata, grosse tuberculata, ecarun- 


Erect taprooted annual, 2-6 dm high. Stem 
terete, glabrous, with scattered short hairs, or 
minutely puberulent near the nodes, faintly glau- 
cous, 1-4 mm diam. at base. Leaves alternate or 
opposite, often varying even on a single plant, 

often fugacious below the inflorescence; petioles 

, 5-40 mm long, puberulent to glabrate, 

shallow > canaliculate; blade ovate or elliptic, 
rarely with a few shallow lobes, 1—10 cm long, 
0.5–7.5 cm wide, 1.2—4.5 times as long as wide, 
thinly appressed-pubescent to glabrate above and 
below, the hairs to 0.5 mm long; base acute to 
broadly — apex T acute, or scarcely 
short-cuspidate rsely dentate to shal- 
lowly sitate or serrate, das subentire; stipules 
€ duliform, 0.2-0.4 mm long. Inflorescence a 

rminal cyme, the bracts similar to the stem 

ная Cyathia campanulate, 0.9-1.5 mm high, 
0.9-1.3 mm diam. at orifice, green, densely pu- 
berulent; lobes 5, deltate, ca. 0.5 mm long; glands 
4, stalked, reniform, green, somewhat creased 
longitudinally, ca. 0.5 mm long parallel to the 


1024 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Vor. 71 


ДРМ 


FIGURE |. a-c. Euphorbia lagunensis Huft.—a. Habit, Jones 27509. 
27509.—c. Seed, Brandegee 12. d-f. Euphorbia chersonesa Huft 
mature capsule, Wiggins et al. 270.—f. Seed, Wiggins et al. 270 


—b. Cyathium and mature capsule, Jones 
.—d. Habit, Moran 18927.—e. Cyathium and 


1984] 


rim of the cyathium, 0.1-0.2 mm wide; append- 
ages forming a minute rim around the gland, 
entire or crenate. Staminate flowers 10—15; brac- 
teoles obsolete. Styles 3, 0.6–0.9 mm long, free 
to the base, divided nearly their entire length, 
only slightly divergent; stigmas capitate; gyno- 
phore glabrous or sparsely pilose, exserted from 
the cyathium 1.5-3 mm, nutant. Capsule E. 
pressed-globose, strongly 3-lobed, 3-3.5 m 

igh, 4-6 mm diam., densely puberulent; seeds 
ovoid-angular, sg 2 mm long, 1.8-2. 

iameter, light gr o brown, coarsely tuber- 
culate, the ксн: eee ecarunculate. 


Thic di +; e а 4 1 


ber of subg. Poinsettia, much less i is it related to 
Е. heterophylla, as is clear from the flat or some- 
what creased, rather than bilabiate or cup-shaped, 
glands, and the presence of petaloid appendages. 
The presence of glanduliform stipules and mi- 
nute appendages dictates its placement in subg. 
Agaloma, where it would seem most at home in 
sect. Cyttarospermum Boiss., based on the an- 
nual habit, slender petioles, absence of bracteoles 
between the staminate flowers, and styles that 
are deeply bifid and free to the base. The sec- 
tional classification of subg. Agaloma, however, 
is in great need of revision (Johnston, 1974; Buck 
& Huft, 1977), so its placement hers must be 
provisional. Euphorbia 
to have any close relatives and can be easily dis- 
tinguished from other species of sect. Cyttaro- 
spermum by the densely puberulent cyathium 
and capsule, the nearly obsolete appendages of 
the cyathial glands, the short, erect styles, and 
the coarsely tuberculate seeds that are not pitted. 
Euphorbia chersonesa is apparently restricted 
to the southern quarter of the Baja California 
peninsula. Only two of the collections provide 
elevational data (275 m, 940 m), and little eco- 
logical data is available. Gentry 4096 was col- 
lected in “moist soil in shade of basaltic cliffs,” 
and the associates of Wiggins et al. 270 include 
Lysiloma candida, Ruellia, Colubrina glabra 
[= C. viridis), Aeschynomene, Olneya tesota, and 
ursera microphylla.’ 


be , UC; 2 other sheets of this number, col- 
: ed оп 13 Oct. 1890, ac heterophylla), Comondú, 
Gi 1938, H. S. Gentry 4096 (DS); Sierra de la 
Giganta, N ridge of Carr Mechudo, 24?48'N, 

0°43’W, ca. 940 m, 3 Nov. 1971, Moran 18927 (UC). 


HUFT— EUPHORBIA 


1025 


5. Euphorbia humayensis Brandegee, Zoe 5: 208. 
05. TvPE: Mexico. Sinaloa: Culiacán, 1 Oct. 

1904, Brandegee s.n. (lectotype, UC 110009, 
here designated, photographs at F— neg. no. 
58287 and MICH; isolectotype, F 196158). 


This species was not included in Wiggins 
(1980), even though one collection from the Cape 
region of Baja California was cited by Brandegee 
in the protologue, and two additional collections 
by Brandegee from Baja California are deposited 
in the herbarium of the University of — 
at Berkeley. Th from 
tropical deciduous forest and thorn к їп 
western Mexico, from Sinaloa south to Michoa- 
can. Curiously, this species has recently been col- 
lected in the savannas of Venezuela (Guarico, 10 

NWN of Altagracia de Orituco along high- 
way to Caucagua, 18 Nov. 1973, Davidse 4171, 
MO, distributed as Е. ocymoidea L. vel sp. aff.). 
This and E. chersonesa are the only represen- 
pees in Baja California of sect. Cyttarosper- 

a group of some 35—40 species that reaches 
а pene development in western Mexico. 


Ад Ном. тен examined. MEXICO. BAJA 
CALIFORN R: W side of Cape region, Nov. 1902, 
poscis s.n. п. (UC): “Todos a (Cape region), 4 
Oct. 1899, Brandegee s.n. (UC); Sierra de Laguna, 21 
Jan. e 10. (F, Uc), зена as Phyl- 
lanthus 


6. Euphorbia eriantha Benth., Bot. Voy. Sul- 
phur 51. 1844. 

Poinsettia eriantha (Benth.) Rose & Standley, Contr. 
U.S. Natl. Herb. 16: 13. 1912. 

The presence of five flat or convex cyathial 
glands, distinct petaloid appendages, and carun- 
culate seeds requires that this species be placed 
in subg. Agaloma, as pointed out by Dressler 
(1961), and not in subg. Poinsettia, where Wig- 
gins (1980) placed it. It belongs to sect. Zygo- 
phyllidium Boiss. where its closest relatives are 
E. lacera Boiss. of central Mexico and E. jalis- 
censis Robins. & Greenm. of western Mexico. 


T: ese Sn lagunensis Huft, sp. nov. TYPE: 

Mexico. Baja California Sur: The Laguna, 

км. 22 Sept. 1930, М. E. 

Jones 5 27300 (holotype, MO 1034346, pho- 

tograph at F—neg. no. 58290). Figure 1: 
a-c. 


Species haec ab E. os Engelm. glandulae cy- 
thii haud lobatis, appendicibus viridibus 2—4 lobatis, 
semine luteo-pustulato diffe 


1026 


Erect taprooted annual, 1.5-3.5 dm high. Stem 
glabrous or with a few hairs at the nodes, (0.8—)1— 
2 mm diam. at base; nodes 3—4 below the inflo- 
rescence; internodes (1.5—)2.5-5 cm long. Leaves 
opposite, the lower ones fugacious; petioles (2—) 
3-8 mm long, appressed-pubescent; blade lin- 
ear, 18—43 mm long, 1.8-5 mm wide, 7-12(-18) 
times as long as wide, sparsely to moderately 
appressed-pubescent above and below, the hairs 
to ino. E: mm long; base cuneate; pe obtuse; mar- 

nute, less than 


0. 1 mm long. Inflorescence a b insi cyme, the 
bracts similar to the stem leaves, the cyathia thus 
appearing solitary in the forks. qp campan- 
ulate, green, villous to pilose, 0.7-0.9 mm high, 
0.8–0.9 mm diam. below the glands, ur .5mm 
across the appendages; lobes 5, егоѕе, 0.3–0.4 
mm long, 0.4—0.5 mm wide; glands 4, green, re- 
niform, 0.6–0.8 mm long parallel to the rim of 
the cyathium, ca. 0.3 mm wide; appendages green, 
(2-)3-4-lobed (rarely merely crenate), exceeding 
the gland by 0.3-0.5 mm; gynophore glabrous, 
exserted from the cyathium 0.3-1 mm, erect or 
nutant. Staminate flowers ca. 15. Styles 3, ca. 
0.7 mm long, free to the base, nearly erect or 
only slightly divergent, divided nearly their en- 
tire length. Capsule subglobose, 1.7-2.2 mm high, 
2-2.2 mm diam., densely white-tomentose on 
the angles, otherwise glabrous; seeds ovoid-an- 
gular, 1.4-1.5 mm long, 0.8-0.9 mm diam., with 
2 transverse ridges, grayish to brown, covered 
with yellow pustules, ecarunculate. 


This species belongs to sect. Zygophyllidium, 
a group of ten species of the United States and 
Mexico that i is goccia by an annual habit, 
eds. Its closest 
relative i is E. apes Engelm. of extreme west- 
ern Texas, southern New Mexico, and south- 
eastern Arizona, but it differs from that species 
in its entire, rather than deeply bilobed, glands, 
appendages that are green and 2—4 lobate, rather 
than white and completely divided, and seeds 
that are yellow-pustulate, rather than bluntly and 
sparingly tuberculate. Most of the specimens of 
E. lagunensis were identified and distributed as 
E. bilobata and were found under that name in 
several herbaria. Hammerly 3874 is cited as E. 
cfr. bilobata in Johnson (1958), but the species 
is not included under any name in Wiggins (1980). 
Euphorbia lagunensis is apparently confined 
to high elevations of the Sierra de Laguna and 
Sierra de San Francisquito, where it occurs on 
rocky banks and in canyons, or in open grassy 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


meadows (cf. descriptions of collecting localities 
in Jones, 1935: 93—94, Goldman, 1951: 

and Johnson, 1958: 246-249, as well as a photo 
of the meadow at Sierra de Laguna in Johnson, 
1958: 235) 


Additional pesi Mr examined. MEXICO. BAJA 


MI AF R: Sierra de Laguna, 23 Jan. 1890, Bran- 
degee 12 (F, UO) Sierra de San Francisquito, 14 Oct. 


1890, Brandegee s.n. (F); Saucito, 14 Oct. 1893, Bran- 
degee s.n. (UC); El Taste, 14 Sept. 1893, Brandegee 
s.n. (US); El Taste, Nov. 1902, Brandegee s.n. (UC); 
Сиера devia-Pinus cembroides association, canyon 
of cabin, La Laguna, Sierra de Laguna, E of Todos 
Salis: 1,700 m , 24 Dec. 1947, Carter et al. 2309 (MO, 
cates to be distributed to K, MEXU, MICH, UC, 
Jorge to San Francisquito ‘and La Chu- 
parosa, E side of Sierra de la Victoria, “Rancho En- 
cenoso," headwaters of Arroyo de San Francisquito, 
23°29-31’N, 109°47-55'W, 12 Арг. 1955, Carter & 
Ferris 3343-A (DS); shady, ey bank above stream 
near the meadow on Sierra de la Laguna, ca. 5,000 ft., 
13 Oct. 1941, Hammerly 387A (CAS); Laguna Mts., 
2 Mar. 1928, Jones 24513 (NY). 


8. Euphorbia ceroderma I. M. Johnston, Proc. 
Calif. Acad. Sci., Ser. 4, 12: 1066. 1924. 
TYPE: Mexico. Sonore San Pedro Bay, 7 July 
1921, Johnston 4304 (holotype, CAS, pho- 
tograph at F— neg. no. 57898). 


This distinctive species is here reported from 
Baja California for the first time. It is known only 
from the collections in Baja California cited be- 

ow and from San Pedro and San Carlos Bays 
near Guaymas, Sonora, where, according to the 
protologue, it is abundant. 

Euphorbia ceroderma belongs to sect. Tricho- 
sterigma (Kl. & Gke.) Boiss., where its two clos- 
est relatives are E. antisyphilitica Zucc. of the 

hihuahuan Desert region and E. rossiana Pax 
of the Tehuacán Valley area of Puebla and Oa- 
xaca, Mexico. These three species are remarkable 
in their peculiar habit of forming dense clumps 
of erect, leafless, yellow-green stems. Euphorbia 
antisyphilitica has by far the greatest range of the 
three and is much more widely known, as it 15 à 
characteristic component of the Chihuahuan 
sert flora and is the source of a widely used 
wax (Hodge & Sineath, 1956). The three species 
may be separated by means of the following key. 


1. Cyathia 0.7-1 mm high; appendages e. en- 
tire; bracts 10-20 mm long, whip-li 
Е ` ceroderma 
1. Cyathia 2-3 mm high; appendages rounded or 
erose; bracts 1-2 mm long. 
2. Appendages entire, rounded; cyathia 1-3 


=> 


1984] 


per glomerule; bracts linear to linear-lan- 
ceolate, entire E EK O 
2. Appendages conspicuously uae or 
ularly dentate; cyathia m DUE. 
bracts broader, fimbriat E. rossiana 


In the protologue, Johnston distinguished E. 
ceroderma from E. antisyphilitica by the wax- 
coated stems and much smaller glabrous cyathia 
of the former, but of these characters, only the 
size of the cyathia holds up. All three species in 
this group have wax-coated stems, the heaviness 
of which apparently varies with the season, and 
the cyathia of E. ceroderma are not glabrous, but 
are puberulent, although not quite as densely so 
as in the other two species. 

Additional specimens examined. MEXICO. BAJA 
CALIFORNIA SU R: Sierra de la 

£0, ca. 12 km E of 
, 111?37'W, ca. 200 m 
1962, Carter 4452 (SD, UO); Sierra de la 
сала. Arroyo anto Domingo, ca. SW 
San Javier, ca. 25°41'N, 111°35’W, са. 200 m, 14 Oct. 
1964, Carter 4736 (MICH, MO, UC), 26 Oct. 1964, 
Carter 4872 (UC), 1 June 1965, Carter & Sharsmith 


4928 (MICH, UC); Sierra de la Giganta, Arroyo Santo 
Domingo, ca. 34 km SSW i 


k 
— 


uanico, near 26?16'N, 112°29’W, са. 80 m, 
Feb. 1973, Moran & Reveal 20100 (SD); nee 
Plain, 2 пи. S of Pozo Grande, near 25?43'N, 112°01'W, 
са. 10 m, Moran 21364 (SD). 


HUFT— EUPHORBIA 


1027 


LITERATURE CITED 
Buck, W. R. & M. J. Hurr. 1977. Two new species 
of Euphorbia пеи Agaloma from Mexico. J. 
Arnold Arbor. 43- 


DRESSLER, R. L. Te (1962). A synopsis of Poinsettia 
Аже KIA Ann. Missouri Bot. Gard. 48: 
341. 


PER. M. L. 1950. Gray’s Manual of Botany, 8th 
Van Nostran , New Yor! 
GOLDMAN, E. 1951. Bio logical investigations in 
] 


Mexico. Smithsonian Misc. Collect. 115: i-xiii, 1— 
476. 


НОРСЕ, W. Н. & H. Н. SINEATH. 1956. The Mexican 
candelilla plant and its wax. Econ. Bot. 10: 134— 
154. 

JOHNSON, B. H. 1958. Тће botany | of ! the Is 
i5 1941. Wasmann J. Biol. 16: 217-315. 

JOHNSTON, M. C. 1974. Euphorbia (subg. Agaloma) 
— new species from the Chihuahuan 


Dese : –375. 
JONES, n (i 1935. ard um of Mexican trip, 1930. 
. W. Bot. 18: 
ease! JT 1951 Did. In Flora of Peru. 
Field Mus. Nat. Hist., Bot. Ser. 13, part SA(1): 8– 
33 


RADFORD, A. E., H. E. AHLES & C. R. BEL 
anual 


phorbia. т Flora of Guatemala. Fieldiana, Bot. 
24(6): 90- 
WIGGINS, I. L. ios Flora of Baja California. Stan- 
ord Univ. Press, Stanford. 


A REVISION OF STENANDRIUM (ACANTHACEAE) 
IN MEXICO AND ADJACENT REGIONS! 


THOMAS Е. DANIEL? 


ABSTRACT 


WTS гс. x МТ. 


e southern United States, Mexico, 
One of 


and northern Central America (Guatemala, Belize, El Salvador, НЕ and Nicaragua). 
these T. Е. Daniel from Guerrero, omg tomi by its erect, caulescent habit 


se species, S. manchonense 
and large, whorled Eevee with. undulate to angular margins, is descri 
) T. F. Daniel апа S. ни ai T. F. Daniel, are made. 


as new to science, and two 


) 
Stenandrium is circumscribed i in relation to its closest iren Aphelandra : and Holographis. Each 
ofth Ti 


‘om its relatives 


for 8. manchonense, S. ая рен 5 jm 


Stenandrium Nees is a genus of perennial herbs 
and subshrubs found in tropical and subtropical 
regions of the New World, from the southern- 
most regions of the United States to central Ar- 
gentina and Chile. Over 50 species of Stenan- 
drium have been described, largely from Brazil, 
the West Indies, and Mexico. The genus has not 
been the subject of any detailed study since Nees's 
treatment in DeCandolle's “Prodromus” (1847). 
Recent regional accounts of Stenandrium in 
North and Central America have been provided 
by Wasshausen (1966) for Texas and Gibson 
(1974) for Guatemala. Standley did not include 
an account of the genus in his treatment of Acan- 
thaceae in “Trees and Shrubs of Mexico" (1926), 
sisi ашуы due to the inconspicuousness of its 
woody natur 

During ius study nine species were found to 
occur in Mexico. One of these is described as 
new to science and two new combinations in 
Stenandrium are made. Five of the species are 
endemic to Mexico. The range of S. barbatum 
extends into the western United States, and 5. 
pedunculatum and S. subcordatum have ranges 
extending into northern Central America. These 
regions are covered by this revision for the sake 
of completeness. Stenandrium dulce has a broad 

ic range, extending from the southern 
United States to Chile 

Vegetatively, plants of Stenandrium are often 
inconspicuous. Several of the species bear their 
leaves at or near ground level. Although these 


F 


plants are commonly referred to as acaulescent, 
they have an underground rhizome that bears a 
cluster of leaves at its apex. Stenandrium bar- 
batum i is somewhat intermediate between these 
spec ies and those th elongate, leafy 
stems. In this species the rhizomes frequently 
become aerial, although the leaves of the current 
season are typically clustered at their apices. In 
many individuals of S. barbatum, there is slight 
internodal elongation as well. Leaves of Stenan- 
drium are either opposite or whorled depending 
on the species. The blades are usually entirely 
green and membranous in texture. In S. nanum, 
however, they have a pale green or whitish col- 
oration along the major veins (also present 1n 
some individuals of S. subcordatum) and a co- 
riaceous texture. The inflorescence consists of a 
lax to dense, bracteate spike. The bracts are green 
and vary from small (ca. 2.5 mm long) and sub- 
ulate to large (ca. 21 mm long) and obovate. The 
flowers consist of a five-parted calyx and corolla, 
four short, monothecous stamens, an inconspic- 
uous staminode, and a bicarpellate gynoecium. 
The corolla is inconspicuously bilabiate and the 
limb usually appears somewhat actinomorphic, 
or at least the lobes are all similar in form. Only 
in S. subcordatum is the corolla distinctly zy- 
gomorphic with the lobes of the upper lip con- 
spicuously reduced in size relative to the lobes 
of the lower lip. The fruit is an ellipsoid capsule 
bearing four pubescent seeds. 
Lindau (1895) is ipt Stenandrium in his 


' For loans and various other courtesies provided, I am grateful to the curators of the following herbaria: A, 


ARIZ, ASU, C, CAS, DS, ENCB, F, GH, K, LL, MA, MEXU, MICH, M 
the manuscript and Mark Mohlenbrock for preparing 
е assistance of the following persons is also gratefully acknowledged: J. Henrickson, E. 


US. I thank Nancy Hensold for rea 
of S. manchonense. The 
Гоп, D. Wasshausen, and R. Worthington 


; RSA, TEX, UC, UNM, 
the illustration 


? Department of Botany and Microbiology, Arizona State University, Tempe, Arizona 85287. 


ANN. Missouri Bor. GARD. 71: 1028-1043. 1984. 


1984] 


subfamily Acanthoideae, tribe Aphelandreae, an 
assemblage of tropical American genera with a 
corolla imbricate in bud and with an upper lip, 
an androecium of four monothecous stamens, 
and tricolpate pollen. Bremekamp (1965) main- 
tained this status for Stenandrium in his sug- 
gested revision of infrafamilial classification in 
the Acanthaceae. He noted that members of this 
tribe are distinguishable by a distinctly bilabiate 
corolla. This is not the case in Stenandrium, 
however, which usually has a subactinomorphic 
corolla suggestive of Bremekamp's Stenandriop- 
sideae. Because infrafamilial classification in the 
Acanthaceae is unclear at the present time, no 
change in tribal status is suggested for Stenandri- 
um 


The closest I relatives of Stenan- 
drium that occurr in the region covered by this 
revision are Aphelandra (Mexico through South 
Айса) апа Н olographis (endemic to Mexico). 

sely 
related. In Mexico, where each genus нае been 
thoroughly studied, they can be distinguished by 
the following key: 


la. Corolla карает АН the lobes more or 
less 5 simi ilar in form (or the upper lip. consid- 


er yd in 5. subcordatum), the upper lip di- 
vided nearly to its bou into two prominent, 


obovate an 2.5 mm long; plants 
acaulescent (the bated clustered at or near 
ound) or caulescent; corolla pinkish or 
purplish (rarely white); anthers included 
corolla tube; stigma fi ~ Stenandrium 
lb. Corolla zygomorphic, the lobes dissimilar in 


зан corolla мит огапре, гед, pink. 
ish, ‚ purplish, ог white; anthers usually | par 


ri bilobed or funne lform 
2a. Corolla red or yellow, 30-70 mm long; 


en tin; 
or purple and дави toothed _--__ 
Aphelandra 
. Corolla yellow, pinkish, purplish, or 
white, 7-18 mm long; bracts inconspic- 
uous, 1-5(-11) mm n long, 0.5-2. ae mm 
wide, green, entir Holographis 


~ 
c 


It is evident from the above key that the dis- 
tinctions among these genera are subtle at best. 
Although I believe all three genera should be 
ee as such, mutually к сһагас- 
them. Th 
characte and trends separating phn me and 


о 


DANIEL— STENANDRIUM 


1029 

ТТАЈ L as E E арч il by Dan- 
iel (1 983). The distinctions between Stenan- 
drium and E are further discussed by 


Daniel dente Despite their close relationship, 
Stenandrium and ээрер are usually readily 
pitt he large, strongly zygomorphic 

corollas, usually E rted stamens, and con- 
spi icuous; often colored and/or toothed bracts of 


Using these generic distinctions, however, sev- 
1 „и fr eS | Aq ei. A ~ е * 


described in Aphelandra should be transferred 
to Stenandrium. 
Stenandrium in the West Indies and South 
America has not been thoroughly studied yet. 
ursory examination of the 15 or so species de- 
scribed from the West Indies reveals that none 


limited amount of material from South America 
in order to bener Oua species circum- 


this | region are also in need of further study. Be- 
cause species from South America are so poorly 
known and the relationships among them and to 
the Mexican species are still largely undeter- 
mined, I have used a conservative species con- 
cept in this revision. 


TAXONOMY 


Stenandrium Nees in Lindl., Introd. Nat. Syst. 
Bot., 2nd edition, 444. 1836, nom. cons. 
TYPE: Stenandrium mandioccanum Nees. 


Gerardia L. Sp. Pl. 610. 1753, pro parte. 


Acaulescent (arising from a woody rhizome or 
caudex) or caulescent perennial herbs or sub- 
shrubs to 5 dm tall. Leaves opposite or whorled 
(4 per node), sessile or petiolate. Inflorescence of 
axillary or terminal, elongate or head-like, usu- 
ally pedunculate spikes, the flowers sessile, sub- 
tended by 2 paired, isomorphic bractlets and a 
bract; bracts green, variable in shape, conspic- 
uously ciliate in several species; bractlets subu- 
late to linear to lanceolate. Calyx 5-lobed, the 
lobes divided nearly to the base, usually lance- 


er-central lobe outermost in bud, the tube cylin- 


Bu A 


1030 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


dric, apically ampliate into a short throat, the pollen prolate to spheroidal, tricolpate (in ours 
throat pubescent within, the limb bilabiate, as examined); style terminal, filiform, flared at 
5-parted, appearing subactinomorphic to bila- apex into an asymmetrically funnelform stigma. 
biate, the upper lip bilobed, the lower lip tri- Capsule ellipsoid, glabrous or pubescent. Seeds 
lobed, the lobes obovate, rounded to truncate at 4 (or fewer by abortion), laterally flattened, sub- 
apex; androecium of 4 stamens and a staminode, oval in outline, the surface variously pubescent, 
the stamens subdidynamous, included, the fila- the trichomes often with barbs, or branches. 

ments short (usually ca. 1 mm long), the anthers 
monothecous, pubescent, the staminode borne 
between the posterior pair of stamens, usually 
shorter than the filaments and lacking an anther; 


Distribution. Southern North America (from 
about Lat. 33°N southward), West Indies, Cen- 
tral America, and South America 


KEY TO THE SPECIES OF STENANDRIUM IN MEXICO AND ADJACENT REGIONS 


la. Plants caulescent (internodal elongation clearly evident, the leaves not clustered at or near the ground 
level). 


2a. Leaves whorled, 4 per n 
3a. Plants sprawling; leaves 6-14 mm long; peduncles 0.5-7 mm long; bracts 1-1. 2 mm wide; 
5.5-8.5 mm long, the lobes purplish near apex is. verticillatum 
3b. Plants erect; leaves 11-25 mm long; peduncles 20-110 mm long; bracts 1.5-2 mm сеа cal 
3.5-5.5 mm long, the lobes not purplish near apex 2. S. manchonense 
2b. rages opposit 
. Nodes callous leaves coriaceous, the upper surface glabrous, Agee green or whitish along major 
veins, the lower surface punctate-pitted; bractlets 0.7-1 mm wide . 3. S. nanum 
. Nodes not callous; leaves membranaceous, the upper => pubescent, concolorous, the 
lower surface not punctate-pitted; bractlets 0.3-0.7 mm wide. 
5а. Leaves congested, vertical or nearly so, oblanceolate to spatulate, 2~9 mm wide; capsule 
9-14 mm long; seeds 3-5.5 mm long, 2.5-4 mm wide; plants of the eas Desert 
. 8. barbatum 
. Leaves not congested, horizontal ог spreading, ovate to elliptic to obovate, ee mm 
wide; capsule 5.5-9(-13) mm long; seeds 1.5-3.5 mm long, 1-2.5 mm wide; plants 
occurring south of the Chihuahuan Desert. 
ба. Bracts lance-subulate to subulate, 1-1.5 mm wide; seeds covered with Dd nox 
like trichomes (rarely restricted to the margin) usually lacking branches o 


A 
= 


л 
= 


chameranthemoideu 
6b. Bracts obovate, 2.5-7(-12) mm wide; seeds covered with bristle-like ар bear: 
lateral barbs or branches _____ 6. S. pedunculatum 


in 
1b. ا‎ acaulescent (leaves clustered at or near the ground level). 
cts lance-subulate, 4.5-7 mm long, 0.5-1.5 mm wide; leaves truncate to cordate at not 
сеа шире SS EL К 7. 8. subcordatum 
7b. Bracts lanceolate to ovate to elliptic to obovate to strap-shaped, 6-21 mm long, 1.5-7. s mm wide, 
leaves rounded to acute to attenuate at base, usually decurrent on the petiole, or plants leafless at 


esis. 
8a. Leaf blades glabrous (although usually inconspicuously glandular along the basal portion of 
lower surface) or plants leafless at anthesis; bractlets linear to linear-lanceolate, tapering from 
ове e middle if at all; capsule entirely pubescent; plants of the northern Sierra Madre 
EES АЕ ИЕ 8. 5. pilosulum 
8b. cg ор 2m (rarely glabrous or only ciliate near base) at anthesis; bractlets subulate 
subulate, tapering from or r below the middle; capsule glabrous or pubescent only 
above the middle; plants occurring east and south of the northern Sierra Madre Occidental. 
9a. Internodes never elongated, plants strictly acaulescent, solitary; leaves spreading, ovate 
1 сје 


trichomes with flexuous or downward in 
ting 1 t 
9b و‎ to the Chihuahuan Decr pointing lateral barbs or branches m ©. S. dulce 
олана ЕЕ јего evident, pi plants commonly forming dense d 
y so, O 
E наук ceolate to spatulate (8-60 mm уй апа О а 


trichomes usually with conspicuously ге 
y recoiled la: lateral barbs or lg pants restricted 
tothe Chihuahuan Desert & . 5. barbatum 


DT o са verticillatum Brandegee, Zoe 5: 1 8°26/N, 97°2 4%, July 1905, E Purpus 
TYPE: Mexico. Puebla: El Riego, 1238 (holotype, UC!; isotypes, F!, GH!, МО), 


4 
ђ 
| 
] 


1984] DANIEL— STENANDRIUM 1031 


o8 08 юз кг 06 9 б м ~ ~. WV vM _ c 
o 
28 
26| S bi 
је : 
4 26 
24 v 
dud 
24 
3 H 
22 >}. 
7 ЈЕ Y 
St T 
20 | 
| 
| 
F 20 
• LJ | 
18 
18° 
Ty 
16° 
ry = t 
A S.chameranthemoideum , ‘a 
= О 
iz * S. manchonense 
| OL |р? 
© 5. nanum ~ 
IH- 

о 
| 8 S. pedunculatum = | lo 
| | 

ө в | 

8 . Subcordatum | o 
‚е E E SO | 8 

8 Е | a 

| S. verticillatum 

6 f 5 o 

108° т о о о o o o o o o o o о 6 

104 102 100 98 96 94 92 90 88 86 84 вг во 


ace 1. Distribution of Stenandrium chameranthemoideum, S. manchonense, S. nanum, S. peduncula- 
m, 5. subcordatum, and S. verticillatum. 


NY!, POM!, US!). Gerardia verticillata axes. Bracts lanceolate to lance-ovate, 4-7 mm 
(Brandegee) Blake, Contr. Gray Herb. 52: long, 1-1.5 mm wide, pubescent like leaves. 
101. 1917. Bractlets linear to lance-subulate, 2-5.5 mm long, 


0.5-0.8 mm wide, pubescent like leaves. Calyx 
5.5-8.5 mm long, the lobes 5-8 mm long, pur 
plish near apex, pubescent like leaves. Corolla 
rose-colored, 8-12 mm long, glabrous on outer 
surface, the tube 5—6 mm long, the upper lip 3- 
5 mm long with lobes 2.5-4 mm long, the lower 
lip 3-5.5 mm long with lobes 2.5-5 mm long. 
Stamens 1.5-2 mm long, the anthers 1.3-1.5 mm 
long. Capsules 7-8.5 mm long, sparsely pubes- 
cent to nearly glabrous; seeds 2.5-3 mm long, 2- 
2.5 mm wide, pubescent with bristle-like tri- 
chomes bearing lateral barbs or branches. 


; es caulescent herb to 10 cm tall from 
Woody base. Stems subquadrate to terete, evenl 
Pubescent it} + n * 7 ? A P 
i mm long. Leaves whorled, 4 per node, sub- 
ады: to short-petiolate, the petioles 0.5-5 mm 
E" the blades obovate to elliptic to suborbicu- 
la е, 6-14 mm long, 4-7.5 mm wide, 1.2-2 times 
Р nger than wide (the lowermost leaves often re- 
aii 1n size or scale-like), rounded to acute at 
"d; attenuate at base, the surfaces pubescent, 
А Ower more densely so, the margin ciliate. 

or 

ККЕ spikes to 1.5 cm long, the peduncles Distribution. Known only from the arid Te- 
5 et TEN long, the spike axes pubescent like the — huacán Valley (Fig. 1) of southern Mexico (Pueb- 
ems; flowers Opposite to subopposite along the 1а and Oaxaca) where it was collected at eleva- 


1032 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Мог 71 


FIGURE 2. Stenandrium тапсћопепзе. —а. Habit.—b. Lower nodes showing scale-like leaves.—c. Upper 
node with whorled leaves.—d. Leaves showing variation in form.—e. Leaf apex. —f. Floral bud.—g. Flower.— 
h. Flower (side view).—i. Developing (immature) capsule. 


| 
| 


1984] 


tions between 2,000 and 2,700 meters (May- 
July). 
Additional specimens examined. MEXICO. OAXACA: 
s Naranjas, vic. of San Luis Tultitlanapa, Puebla, 
C. Purpus 3083 (F, GH, MO, NY, UC, US). PUEBLA: 
Cerro de Castillo, C. Purpus 2512 (UC); Acatitlán, C. 
Purpus 3939 (UC). 


11 + 


This species is known from four 


VEIN LIVE 


of 
C. A. Purpus. It can be distinguished by its low, 


sprawling habit, short whorled leaves, and api- 
cally purplish calyx lobes. It is similar to S. man- 
chonense, with which it shares a caulescent habit 
and whorled leaves with a low length to widt 
ratio. 


2. Stenandrium manchonense T. F. Daniel, sp. 
: Mexico. Guerrero: Мапсћоп, 
18°07'N, 100*59"W, Distr. Mina, 10 J 
1937, G. Hinton et al. 10460 (holotype, US!; 
isotypes, DS!, ENCB!, F!, GH!, K!, LL!, 
MICH!, MO!, UC!). Figure 2. 

Herba caulescens usque ad 2.5 dm alta; caules pu- 
bescentes trichomatibus 0.2-1 mm longis; folia verti- 
cillata, nodo quatuor, laminae ovatae vel suborbicu- 


2 

N‏ دم 
Sg‏ 

8 

t 


an 
ceolatae, 2.5-4 mm longae, 1.5-2 mm latae; bracteolae 
lanceolatae vel lanci-subulatae, 2-3.5 mm longae; ca- 
lyx 3.5-5.5 mm longus; corolla 11-18 mm longa; cap- 
sula ignota. 

Caulescent herb to 2.5 dm high. Stems 
subquadrate, pubescent with flexuous-crinkled 
trichomes 0.2-1 mm long. Leaves whorled, 4 per 
node, the lowermost leaves scale-like, sessile, el- 
liptic to oblanceolate, 3-7 mm long, 2 mm wide, 
the upper leaves subsessile to short-petiolate, the 
petioles 0.5-3 mm long, the blades ovate to sub- 
orbiculate to obovate, 11-25 mm long, 4-20 mm 
Wide, 1-2.2 times longer than wide, cuneate to 
attenuate at base, rounded to acute at apex, the 
Margin ciliate, irregularly undulate, the undula- 
tions often somewhat angular, the surfaces pu- 


5 pubescent like the stems ог the rachis lacking 
ue: of the longer trichomes. Bracts ovate to 
anceolate, 2.5-4 mm long, 1.5-2 mm wide, the 
аһ axial surface sparsely pubescent, the margin 
ciliate, Bractlets lanceolate to lance-subulate, 2- 
iS mm long, 0.5-0.8 mm wide, ciliate. Calyx 
ы -5.5 mm long, the lobes 3—5 mm long, sparse- 
У pubescent to nearly glabrous on abaxial sur- 


DANIEL— STENANDRIUM 


1033 


face, the margins ciliate. Corolla color unknown, 
11-18 mm long, the tube 5—7 mm long, the upper 
lip 6-8 mm long, the lower lip 8-11 mm long, 
the lobes subequal (or the lobes of the upper lip 
slightly shorter), 6—9 mm long, glabrous on the 
abaxial surface. Stamens 1.5-2 mm long, the an- 
thers 1-1.2 mm long. Capsules not seen. 


Distribution. Known only from the type, 
which was collected in southwestern Mexico 
(Guerrero) in oak woods at an elevation above 
1,100 meters (June) (Fig. 1). 


This species is readily distinguished from all 


whorled leaves with an undulate to angular mar- 
gin. Its closest relative appears to be S. verticil- 
latum, the only other caulescent species with 
whorled leaves in Mexico. Stenandrium verticil- 
latum differs from S. manchonense by its scram- 
bling, bushy growth form, smaller leaves and 
bracts, and longer calyx with purplish lobes. In 
addition, the inflorescence of S. verticillatum 
consists ofa short (to 1.5 cm), few-flowered spike 
that is either sessile or borne on a peduncle 0.5— 
7 mm long. Іа 5. manchonense, the inflores- 
cences are longer (3.5-21 cm), many flowered, 
and borne on peduncles 2-11 cm long. 


p 


Stenandrium nanum (Standley) T. F. Daniel, 


comb. nov. P. 


CUILL 


dley, Publ. Field Columbian Mus., Bot. Ser. 
8: 46. 1930. TYPE: Mexico. Yucatán: Silám, 
s.d., G. Gaumer 1305 (holotype, F!). 


Caulescent perennial herb to 10 cm tall, from 
woody rhizome. Stems subquadrate, multi- 
striate, pubescent with straight trichomes 0.1- 
0.2 mm long, the nodes callous. Leaves opposite, 
petiolate, the petioles 3-6 mm long, pubescent 
like stem, the blades coriaceous, ovate to elliptic, 
16-48 mm long, 10-27 mm wide, 1.6-2 times 
longer than wide, acute, sometimes unequal at 
base, acute to rounded at apex, the upper surface 
glabrous, pale green or whitish along the major 
veins, the lower surface punctate-pitted, with 
some trichomes along the midvein, the margin 
revolute. Inflorescence of axillary or terminal, 
sessile (or borne on peduncles to 1 mm long) 
spikes to 6 cm long. Bracts lanceolate, 6-7 mm 
long, 1.5 mm wide, pubescent like stem. Bractlets 
lanceolate, 4–5.5 mm long, 0.7-1 mm wide. Ca- 
lyx 8-9 mm long, the lobes lance-subulate. Co- 
rolla 16-24 mm long, glabrous on outer surface, 


1034 


the tube 8—14 mm long, the lobes of the upper 
lip 5-6.5 mm long, the lobes of the lower lip 7— 
9 mm long. Stamens 2 mm long, the anthers 1.5 
mm long. Capsule 8-9 mm long, glabrous. Seeds 
not seen. 


Distribution. Known only from two collec- 
tions from the Yucatán Peninsula of Mexico (Fig. 
1) 


Additional specimen examined. MEXICO. YUCATAN: 
Progresso, s.d., Gaumer 2295 (F). 


Although Standley (1930) described this species 
in Pseuderanthemum and Leonard (1936) so 
maintained it, its proper position is in Stenandri- 
um. Neither Standley nor Leonard discussed the 
androecial arrangement or capsular form of this 
species. In Pseuderanthemum, the androecium 
consists of two bithecous stamens containing tri- 
colporate pollen and two staminodes and the 
capsule is stipitate. In Stenandrium, bow androe- 
cium consists of four with 
tricolpate (in ours as examined) pollen and the 
capsule lacks a stipe. Both specimens treated by 
Standley and Leonard have the diagnostic fea- 
tures of Stenandrium. 

Stenandrium nanum is readily distinguished 
by the callous nodes and coriaceous leaves with 
a pale green or whitish coloration along the veins 
on the adaxial surface, and punctate-pitted abax- 
ial surface. Its closest relative in Mexico appears 
to be S. chameranthemoideum. In addition to 
the above cited characters, it can be distinguished 
from 5. chameranthemoideum by its longer, lan- 
ceolate bractlets and longer corollas. The ranges 
of these two species are not known to overlap. 


4. Stenandrium barbatum Torr. & Gray, Pacific 
Rail. Rept. (Pope's Explor.) 2: 168. 1855. 
TYPE: United States. Texas: Pecos River, 
Mar. 1851, C. Wright 1453 (holotype, GH!; 
isotypes, GH!, K!, NY!). Gerardia barbata 
(Torr. & Gray) Blake, Contr. Gray Herb. 52: 
100. 1917. 


Dwarf acaulescent or subcaulescent perennial 
herb to 12 cm tall from a stout woody rhizome, 
often forming small, dense mats. Leaves verti- 
cally oriented, sessile or short-petiolate, the pet- 
ioles to 5(-25) mm long, the blades oblanceolate 
to spatulate, 8-60 mm long, 2-5(-9) mm wide, 
(34-11 times longer than wide, tapering-atten- 
uate at base, acute at apex, pubescent with a 
sparse to dense understory of erect or bent tri- 
chomes 0.1-0.2 mm long and an overstory 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


(sometimes restricted to the margin) of flexuous 
trichomes 1—4 mm long, the margin entire. In- 
florescence of leafy-bracteate, pedunculate spikes 
to 7 cm long, the peduncles to 35 mm long (not 
exceeding the leaves), pubescent with straight to 
retrorse trichomes 0.1–0.5 mm long and some- 
times with flexuous trichomes 1—2 mm long as 
well, the spike axis pubescent with straight tri- 
chomes 0.1–0.2 mm long (sometimes very 
sparsely so), the flowers opposite to subopposite 
along the spike. Bracts oblanceolate to obovate 
to elliptic, 7-21 mm long, 2—4 mm wide, pu- 
bescent like the e. Bractlets subulate, 1.5-6 
mm long, 0.30.6 wide, pubescent (some- 
times sparsely 50), "usually with a mixture of 


eglandular t I 
glands, the tricl ti tricted to the 
eor and жау consisting entirely of incon- 
spicu mm 


long, the lobes subequal, lance-subulate, pubes- 
cent like bractlets. Corolla pinkish purple with 
white streaks on the lower lip, 13-21 mm long, 
glabrous or sparsely pubescent on the outer sur- 
face, the tube 4—5 mm long, the upper lip 5.5-9 
mm long with lobes 4-8.5 mm long, the lower 
lip 6—11 mm long with lobes 6-9 mm long. Sta- 
mens 1.5-2 mm long, the anthers 1.5 mm long. 
Capsule 9-14 mm long, glabrous (rarely pubes- 
cent). Seeds 3-5.5 mm long, 2.5-4 mm wide, the 
testa densely pubescent with long, stiff, golden 
trichomes with usually conspicuously recoiled 
branches. 


Distribution. Chihuahuan Desert regions of 
southern New Mexico, western Texas, eastern 
Chihuahua, and western Coahuila (Fig. 3) on 
limestone slopes and in arroyo gravel in desert 
associations of Agave, Viguiera, Fouquieria, 


Larrea, Acacia, Dasylirion, Prosopis, and Yucca 


up to pinyon-juniper communities at elevations 
from 750 to 1,350 meters (Mar.—Oct.). 


Se аду n mid ae ca sired UNITED 
TES. NEW M , са. 2 ті. W of Ros- 

ii os ‘Smith 4374 (SRSO: Doña Ana Co., 
6 mi. W of aso, Hanson s.n. (TEX); Eddy Со» 
Carlsbad ks Nelson 11402 (DS, GH, POM, ae 


edu from , 


Culberson Co., Sie 
Correll & Rollins quies ее LL); ЕР 
Franklin Mountains W of El Paso, Warnock k 10328 


x". 


—— ee 


1984] 


DANIEL— STENANDRIUM 


| © S. barbatum 
B S. dulce 


4 S. pilosulum 


1035 


pe cmm 


FIGURE 3. Distribution of Stenandrium barbatum, S. dulce, and S. pilosulum. 


(LL), Ferris & Duncan 2402 (CAS, DS), Lundell & 
Lundell 16940 (LL), Barlow s.n. (UC), Correll & John- 
ston 21834 (LL, UC), Daniel 2713 (ASU, MICH, NY); 
Hudspeth Co., near summit of Hueco Mountains, 30 
P E of El Paso, Mc Vaugh 8147 (CAS, DS, K, POM, 
me UC); Jeff Davis Co., just W of Chispa summit, 

43'N, 104*47"W, Johnston et al. 10684 (LL); Pecos 
маа NE side of Sierra Madera, ca. 25 mi. 5 of Ft. 
gpa McVaugh 7914 (ASU, DS, TEX); Presidio 
б ys S of Shafter, Warnock 46642 (SRSC); Reeves 
: ^ mi. NW of Toyahvale, Rt. 290, Correll & Cor- 

ell 38527 (ENCB, TEX); Terrell Co., 9% mi. 

den, Cory 43864 (GH 

near Cd, j 


NY, PO > U " 
rickson & Lee 15821 (TEX). COAHUILA: just across riv- 
0 i Creek, Johnston et al. 
E 5J (LL); Sierra de las Cruces, vic. of Santa Elena 
Ines, Stewart 350 (GH, LL), 397 (LL). 


Stenandrium barbatum is one of the better 
known amd 11 PU . 4 p . а. а 


3 the United States and adjacent Mexico and 


woody rhizomes of S. barbatum are frequently 
aerial and often branch. The leaves and inflo- 


however, slight internodal elongation during the 
growing season commonly results in a short (to 
15 mm long) stem. Because of this unusual sit- 
uation and because of some intergradation be- 
tween the leaves and bracts, S. barbatum is listed 
in the key under both initial leads. 

The closest relatives of S. barbatum appear to 
be S. dulce and S. pilosulum. The close relation- 
ship between S. dulce and S. barbatum is illus- 
trated by a specimen from western Coahuila 
(Stewart 397, LL) which is treated as S. barba- 
tum because of its narrow, oblanceolate to spat- 
ulate leaves, long trich d glab ll 
lobes. However in several characters, including 
the lance-elliptic bract individuals, and 
often sparse pubescence, this collection is sugges- 
tive of S. dulce, which also occurs in western 
Coahuila. 

Stenandrium barbatum (Fig. 4) is readily dis- 
tinguishable from both S. dulce and S. pilosulum 
by its dense, mat-forming habit, nearly vertical, 
oblanceolate to spatulate leaves that are con- 


> 


1036 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


Ficure 4. Illustration of Stenandrium barbatum from John Pope's report to the War Department in 1855. 


spicuously pubescent with long (1-4 mm) stiff 
trichomes, leafy-bracteate spikes, and golden 
seminal trichomes that usually have recoiled lat- 
eral barbs or branches. 


5. Stenandrium chameranthemoideum Oerst., 
Vidensk. Meddel. Dansk Naturhist. Foren. 
Kjøbenhavn 1854: 139. 1854. type: Mexico. 
Veracruz: Colipa, Mar. 1841, F. Liebmann 


10750 (lectotype, C!, here designated; 150- 
lectotype, US!). Gerardia chameranthemo- 
idea (Oerst.) Blake, Contr. Gray Herb. 52: 
100. 1917. 


Caulescent perennial herb to 3 dm tall. Stems 
terete to subquadrate, pubescent with an under- 
story of straight to retrorse trichomes 0.05-0.1 
mm long and an overstory (sometimes sparse OF 
absent) of flexuous trichomes 0.5-1 mm long 07 


1984] 


evenly pubescent with straight to retrorse tri- 
chomes 0.1–0.6 mm long. Leaves opposite, pet- 
iolate, the petioles 3-40 mm long, the blades 
ovate to elliptic to obovate, 16—82 mm long, 10– 
mm wide, 1.1-2.6 times longer than wide, 
attenuate-decurrent at base, rounded to acute at 
apex, the surfaces pub t, ti parsely 
so, the margin entire to irregularly undulate to 
subcrenulate. Inflorescences of axillary or ter- 
minal spikes to 10 cm long, the spikes sessile or 
borne on peduncles 2-15 mm long, the peduncles 
and spike axes pubescent like the stem or nearly 
glabrous, the flowers subopposite to alternate 
along the spike axes. Bracts lance-subulate to 
subulate, 2.5-7 mm long, 1-1.5 mm wide, the 
abaxial surface pubescent, the margin ciliate (or 
bracts very sparsely pubescent with short tri- 
chomes). Bractlets lance-subulate, 2-4 mm long, 
0.5-0.7 mm wide, pubescent like bracts. Calyx 
4-9 mm long, the lobes subequal, lance-subulate, 
4-8.5 mm long, pubescent like bracts or nearly 
glabrous, the margin sometimes with inconspic- 
uous glands as well. Corolla pinkish or whitish, 
10-14 mm long, the tube 5-8 mm long, the upper 
lip 3.5-6 mm long with lobes 3.5-6 mm long, 
the lower lip 5-7 mm long with lobes 4.5-6.5 
mm long, the anterior lobe pubescent or glabrous 
on abaxial surface, the other lobes glabrous. Sta- 
mens 2-2.5 mm long, the anthers 1.5-1.8 mm 
long. Capsule 6-9(-13) mm long, glabrous. Seeds 
5-3.5 mm long, 1–2.5 mm wide, the testa cov- 
ered with papilla-like trichomes (restricted to the 
margin in some plants) mostly lacking barbs. 


Distribution. Eastern and southern Mexico 
(Veracruz and Chiapas) in canyons and on ridges 
at elevations from 250 to 1,000 meters (Sept.— 
Apr.) (Fig. 1) 


Additional specimens examined. MEXICO. CHIAPAS: 
13 к N of Berriozábal near Pozo Turipache and Finca 
El Sunim, Ар Breedlove 31226, 39893 (CAS). VERACRUZ: 


soquitla, Zacua 
US); Pachuquilla, Puente Nacional, Ventura А. 7364 
(ENCB, MICH). 


In the protologue of S. chameranthemoideum, 
Oersted (1854) cited two of Liebmann’s localities 
in Veracruz, “Ved Colipa og Hacienda de Sta. 
Barbara.” There are specimens on four sheets 
representing Liebmann’s collections of this 
Species at C. Three are from Colipa and bear the 
humber 70750. The other is from the Hacienda 
de Santa Barbara and is numbered 10749. The 


DANIEL— STENANDRIUM 


1037 


lectotype is here designated as и 10750 
i ets) 


suggest that there is considerable variation in 
pubescence of S. chameranthemoideum. Nevling 
& Gomez-Pompa 1026 contains three plants that 
differ markedly in pubescence of the stems, in- 
florescence axes, and bracts. 

The plants from Chiapas differ from those col- 
lected in Veracruz by their cauline pubescence 
(evenly pubescent with straight to retrorse tri- 
chomes 0.1–0.6 mm long), somewhat longer cap- 
sules (8—13 mm), and testa ornamentation (pa- 
pilla-like trichomes restricted to the margin). In 


The closest morphological relative of this 

spectes appears to be S. отет. Both species 

habit, , and nar- 

row bracts and bractlets. The distinctions be- 
tween them are discussed under S. nanum 


6. Stenandrium pedunculatum (Donn.-Smith) 
Leonard, J. Wash. Acad. Sci. 32: 187. 1942. 
Blechum pedunculatum Donn.-Smith, Bot. 
Gaz. се 49: 457. 1910. ТҮРЕ: 


Deam 6277 (holotype, US!; isotypes, СН!, 
MO!) 


X. + 1 + 


Erect огр ial herbs 
to 50 cm tall from a stout woody rootstock or 
rhizome. Stems pubescent with an understory of 
straight to retrorse trichomes, 0.2-0.5 mm long, 
and an overstory of flexuous trichomes, 0.5-1.5 
mm long. Leaves opposite, petiolate, the petioles 
to 20 mm long, the blades ovate-elliptic to ob- 
ovate, 12-90 mm long, 7-45 mm wide, 2-3.5 
times longer than wide, subtruncate to long-at- 
tenuate at base, rounded to subacute at apex, 
pubescent on both surfaces (often sparsely so), 
margin entire to crenulate, usually ciliate. Inflo- 
rescence an axillary or terminal, often somewhat 
head-like, pedunculate spike to 35 mm long, the 
peduncles (0.5—)1.5-5 ст long, the flowers op- 
posite or subopposite along the rachis. Bracts 
obovate, 5.5-14 mm long, 2.5-7(-12) mm wide, 
pubescent like leaves. Bractlets subulate, 1.5-5.5 
mm long, 0.3-0.7 mm wide, glabrous or sparsely 
pubescent. Calyx 3-6.5 mm long, the lobes lance- 
subulate, 2.5-5.5 mm long, glabrous to sparsely 
pubescent. Corolla pink to white, 10-19 mm long, 


1038 


the tube 5-7 mm long, the upper lip 4-8 mm 
long, the lower lip 5.5-11 mm long, the lobes 
subequal, 4-10 mm long or lobes of the lower 
lip to 1.3 times longer than those of the upper 
lip, the lower-central lobe pubescent on abaxial 
surface. Stamens 1.5 mm long, the anthers | mm 
long. Capsule 5.5-8 mm long, glabrous or sparse- 
ly pubescent above the middle. Seeds 2-3 mm 
long, 1.5-2.5 mm wide, pubescent with long, 
bristle-like trichomes with lateral barbs or 
branches. 


Distribution. Western and southern Mexico 
(Jalisco, Colima, Guerrero, and Chiapas) and 
northern Central America (Guatemala, Hondu- 
ras, and Nicaragua) in forests, especially along 
streams, and on grassy slopes at elevations from 
near sea level to 1,350 meters (May-Dec.) 
(Fig. 1). 


Representative specimens examined. MEXICO. 


, above Finca у 
along rd. from Acala to Pugiltik, Ton 2990 (F, LL, 
MICH, US); La Trinitaria, along rd. to Boqueron W 
of Hwy. 190 at point 18 km SW of La Trinitaria, Breed- 
love 42253 (MO). COLIMA: ca. 16 mi. of Santia- 
go, McVaugh 14972 (MICH), 15734 (MICH). 


ENANGO: Sierra de los Cuchumantes, between 
Ana Hista and Netón, Steyermark 51400 (Е). JUTIAPA: 
vic. of Jutiapa, Standley 75318 (Е). zAcAPA: Sierra de 
las Minas, near electric plant of Río Hondo, Standley 
74009 (F). HONDURAS. CHOLUTECA: mountains near El 
Banquito, Williams & Molina R. 10796 (F). EL PARAISO: 
i del Rio Lizapa, Llano de Lizapa, Molina R. 
3955 (F, MO). MORAZÁN: drainage of Río Yeguare near 
San Francisco, Molina R. 218 (F, GH), Williams 15911 
(DS, Е, GH, MO). NICARAGUA. ESTELÍ: de la: 
Animas, NE of Esteli, Standley 20325 (Е). 


This widely distributed species exhibits con- 
siderable variation in stem length, bract size, and 
pu nce. Plants of S. pedunculatum are dis- 
tinguishable from other Mexican species by their 
1 al 2, 24 : 1 pe 0 à. 1 


[^] 


and relatively short capsules. The specimens from 
Colima differ from some of the more southerly 
collections by their shorter (1-3 cm long) stems. 
In other characters, however, they are identical 
with the latter. 

Leonard (1942) noted the similarities between 
S. pedunculatum and S. mandioccanum Nees of 
southern South America, the distinguishing 
characters being the pubescent capsules and 
densely retrorse-pubescent stems of the latter 
species. Examination of several specimens of 5. 
mandioccanum from Brazil and Argentina re- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


veals that these characters will not distinguish 
the two species. Several specimens of S. pedun- 
culatum have pubescent capsules and the plants 
of S. mandioccanum that I examined all had 
strongly antrorse cauline trichomes. In fact, my 
cursory examination suggests that specimens re- 
ferred to S. pedunculatum and S. mandiocca- 
num may be part of the same species. Based on 
the few specimens of S. mandioccanum available 
to me, the distinctions in the following couplet 
serve to separate the taxa: 


a. Cauline trichomes uniform in length, antrorse; 
plants of southern South America 
BEEN UC eM ER E INE S. mandioccanum 

b. Cauline trichomes consisting of an understory 
of straight to retrorse trichomes and an over- 
story of longer, flexuous trichomes; plants of 
southern North America and northern Central 
"ENS S ooo on n . S. pedunculatum 


Perhaps these differences are more reflective of 
varieties of one species than separate species. 
Until 5. mandioccanum and its relatives in South 
America have been thoroughly studied, how- 
ever, it seems prudent to maintain these taxa at 
their present status and avoid possible future no- 
menclatural reductions. 


7. Stenandrium subcordatum Standley, J. Ar- 
nold Arbor. 11: 48. 1930. түре; Mexico. Yu- 
catán: Chichen Itzá, 3 June 1929, J. Be- 
quaert 20 (holotype, ан). 


Acaulescent perennial herb to 1 dm tall. Leaves 
petiolate, the petioles 10-57 mm long, pubescent 
with flexuous trichomes, the blades ovate to el- 
liptic, 19-56 mm long, 13-24 mm wide, 1.2-2.9 
times longer than wide, truncate to cordate (often 
asymmetric) at base, the blade not decurrent on 
the petiole, rounded to acute at apex, the surfaces 
pubescent, the upper surface sometimes раје 
green to whitish along the major veins, the mar- 
gin entire to irregularly undulate, ciliate. Inflo- 
rescence a pedunculate spike to 100 mm long, 
the peduncles (5—)20—65 mm long, pubescent with 
flexuous trichomes 0.2-1 mm long, the flowers 
alternate to subopposite along the rachis. Bracts 
lance-subulate, 4.5-7 mm long, 0.5-1.5 mm wide, 
pubescent on abaxial surface, the margin ciliate. 
Bractlets subulate, 2.5-4 mm long, 0.5-0.7 mm 
wide, pubescent like bracts. Calyx 4—6 mm long, 
the lobes subulate, 4-5.5 mm long, pubescent 
like bracts. Corolla pinkish purple, 14-17 mm 
long, the tube 8-9 mm long, the upper lip 3.5- 
5 mm long with lobes 3-4 mm long, the lower 
lip 5-8 mm long with lobes 5-7.5 mm long, the 


1984] 


lower-central lobe sparsely pubescent to nearly 


mm long, pubescent (trichomes sometimes very 
sparse). Seeds 1.5-2 mm long, 1–1.5 mm wide, 
covered with hair-like papillae. 


Distribution. Known only from the state of 
tan in Mexico and the department of Petén 
in Guatemala (Fig. 1) where the plants grow in 
clearings, dense forests, and along dry arroyos 
(Mar.-July) 

Additional specimens examined. MEXICO. YUCA 
Chichen Itzá, Valladolid rd., ipe & Lundell 751. 1 1 
(LL, MICH); Chichen Itzá, Steere 1451 (MICH); Ti- 
zimín, Swallen 2530 (MICH). GUATEMALA. PETÉN: 
Uaxactum, Bartlett 12283 (CAS, K, MICH, TEX). 


This rarely collected species is readily distin- 
guishable from other Mexican species of Stenan- 
drium by its leaf blades which are truncate to 
subcordate at the base and not decurrent along 
the petiole. Stenandrium subcordatum also has 


size of those of the lower lip. Unlike the corolla 
ш species of Holographis, however, the corolla 
of S. subcordatum has an upper lip divided near- 
ly to its base with obovate lobes. The affinities 
of S. subcordatum are with S. dulce from which 
it can be distinguished by the above mentioned 
characters as well as its shorter and narrower 
bracts and shorter capsules. 

Perhaps the closest morphological relative of 
this species is S. [yonii J. В. Johnston of Vene- 
Zuela. Both species have ovate to elliptic, basally 
truncate leaf blades sometimes with a whitish or 
pale green coloration along the major veins on 
the adaxial surface. Although S. /yonii was orig- 
inally described as acaulescent (Johnston, 1908), 
examination of the type reveals it to be subcau- 
lescent with slight са elongation. Other 
Specimens of S. /уо ined from Venezuela 
аге conspicuously Silent These species can 
be distinguished by the following couplet: 


а. Plants subcaulescent to caulescent; bracts (6-) 
7-10 mm long; bractlets 0.3-0.5 mm wide; со- 
rolla 8-13 mm long; capsule glabrous; plants 
of northern South America ______ S. бол 
Plants acaulescent; bracts 4.5-7 mm “long; 
bractlets 0.5-0.7 mm wide; corolla 14-17 mm 
long; capsule pubesce п ИЕ sparsely 
= plants of the Yasta Peninsula _____- 

SER S. subcordatum 


= 


DANIEL— STENANDRIUM 


1039 


8. Stenandrium pilosulum (Blake) T. F. Daniel, 
comb. nov. Gerardia pilosula Blake, Contr. 
Gray Herb. 52: 101 17. TYPE: Mexico. 
Chihuahua: vicinity of Madera, 27 May-3 
June 1908, E. Palmer 317 (holotype, GH!; 
isotype, US!). 


Acaulescent perennial herb to 7.5 cm tall from 
a woody rhizome, the rhizome bearing numerous 
fleshy roots along its length. Leaves (plants often 


oblanceolate to narrowly elliptic to dox (to 
ovate), 11-30 mm long, 3-7(-10 

4.7 times longer than wide, {нале to decur- 
rent at base, acute to rounded at apex, the margin 
entire, PR the surfaces glabrous i n 


dial 1 


elo 
the 8 portion) and punctate-pitted. bg 


0.05-0.2 mm long, the flowers opposite 
to subopposite along spike axis, sessile. Bracts 
ovate to narrowly elliptic to obovate, 6-11 mm 
long, 1.5-4.5 mm wide, pubescent like peduncles 
although the trichomes more numerous and the 
margin inconspicuously ciliate with trichomes 
0.05-0.3 mm long. Bractlets ud to linear-lan- 
ceolate, 6-10 mm long, 0.5-1 mm wide, pubes- 
cent like bracts. Calyx 7-14. mm long, the lobes 
linear-subulate to linear-lanceolate, subequal 

6.5-13.5 mm long, pubescent like bracts. Corolla 
purplish, 10-23 mm long, the tube 6-15 mm 
long, the upper lip 3-8 mm long, the lower lip 
4—8.5 mm long, the lobes subequal, 3-7.5 mm 
long, the lobes and tube glabrous or sparsely pu- 
bescent on the abaxial surface, the lower-central 
lobe often densely pubescent. Stamens 2.5-3 mm 
long, the anthers 1.5 mm long. Capsule 9-12 mm 
long, pubescent over the entire surface. Seeds 3- 
4 mm long, 3-3.5 mm wide, densely pubescent 
with long, bristle-like trichomes bearing lateral 
barbs or branches. 


Distribution. Sierra Madre Occidental of 
western Chihuahua and eastern Sonora (Fig. 3) 
on gravelly slopes in pine-oak associations at el- 
evations from 1,720 to 2,250 meters (Mar.-May) 


спою specimens examined. XICO. CHIHU 
of Guerrero, Correll & AUN 21612 
yu LL NY, US); 2 mi. E of Yepachi ic, ne 
75-3-58 (ARIZ). SONORA: ca. 5 mi. W of Yécora 
bell s.n. (ARIZ); 7 mi. NW of Yécora, Moran : al. 
E 965 (ENCB). 


1040 


This little known species was described by 
Blake (1917) as Gerardia reine based on a 
single collection from Chi ua. Recent col- 
lections have been either eee or mis- 
identified. Plants of S. pilosulum are readily rec- 
ognized by their diminutive stature and 
ascendant, glabrous (though inconspicuously 
glandular) leaves (which are often absent at an- 
thesis). Although its affinities to other species 
were not noted in the protologue, it is morpho- 
logically similar to S. dulce, from which it can 
be distinguished by the following couplet: 


a. Plants leafless at anthesis or leaves glabrous; 
kek not i need ciliate, the margin 
scent with trichomes 0.5-0.3 mm long; 
cien linear to Vb dS late, tapering to 
apex from above the middle if at all; capsule 
entirely pubescent; plants —€— to the 
northern Sierra Madre Occiden Sonora 
and Chihuahua де pilosulum 
Plants leafy at anthesis, leaves pubescent; bracts 
те ciliate, the trichomes (0.3—)0.5— 

m long; bractlets subulate to lance-subu- 
ae tapering to apex from at or below the 
middle; capsule glabrous or pubescent on up- 

per half; plants occurring east and south of 
Sonora and Chihuahua S. dulce 


9 


9. Stenandrium dulce (Cav.) Nees in DC., Prodr. 
11: 282. 1847. Ruellia dulcis Cav., Icon. Pl. 
6: 62, t. 585, f. 2. 1801. TYPE: Chile. Con- 
cepción: near Talcahuano, Née herbar. (not 
seen). Gerardia dulcis (Cav.) Blake, Contr. 
Gray Herb. 52: 101. 1917 


iiie اجا‎ Benth., Pl. Hartweg. 22. 1839. 
xico. Jalisco: Lagos, 1837, T. Hartweg 
182 eric K!; isotypes, 
vixi fasciculare 0 Wasshausen, Phyto- 
2: 427. 1965 


al 

Stenandrium dulce (Cav) N ees var. floridanum A. Gray, 
Amer. 2(1): 327. 1878. TYPE: United 
de dian River, 1894, E. Palmer 
350 у боа он) ете floridanum т (А. 
Gray USS. Ist edition. 1085. 

1903. Gerardia Poem (Cav. ) Blake var. floridana 
ray) Blake, € Gray Herb. 52: 101. 1917. 
Pre n, guatemalense Leonard, . Carnegie 
Inst. Wash. 461: 212. 1936. TYPE: Gua temala. 
ta Verapaz: Cubilguitz, 1892, H. von Turck- 

Ануй 3588 (holotype, US!; isotypes, GH!, K!). 
Stenandrium mexicanum Leonard, pon Bull. 1938: 
62. 1938. TYPE: Mexico. México: tepec, 
San Lucas, 7 July 1933, G. Hinton et al. 4292 
(holotype, K!; isotypes, ARIZ!, GH!, MO!, US!). 


Acaulescent perennial to 20 cm tall from stout 
rootstock or rhizome. Leaves (subsessile) peti- 
olate, the petioles 5-65 mm long, the blades ovate 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


to ovate-elliptic (to oblanceolate to strap-shaped), 
13-100 mm long, 4—44 mm wide, 1.5—5.5(-18) 
times longer than wide, rounded to acute to at- 
tenuate (to decurrent along petiole) at base, acute 
to rounded (rarely emarginate) at apex, the sur- 
faces pubescent (rarely glabrous), usually glan- 
dular-punctate, the margin entire, crenulate, or 
somewhat irregularly undulate, flat to slightly 
revolute, ciliate or eciliate. Inflorescence a sub- 
sessile or pedunculate, head-like or usually elon- 
gate spike to 85 mm long, the peduncles 5-200 
long, the peduncl d rachis pul t with 
trichomes 0.1-1.5 mm long or nearly glabrous, 
the flowers sessile, alternate or opposite along 
the rachis. Bracts lanceolate to elliptic (rarely ob- 
lanceolate, obovate, or strap-shaped), (6—)9-20 
mm long, 2—7.5 mm wide, usually conspicuously 
3-nerved, the outer surface densely pubescent or 
glabrous, the margin ciliate with trichomes 
(0.3—)0.5—2 mm long. Bractlets lance-subulate to 
subulate, 3-9 mm long, 0.3-1(-1.5) mm wide, 
ciliate or eciliate, sometimes inconspicuously 
ong the margin. Calyx 4—11 mm long, 
the lobes lance-subulate, 3.5-9 mm long, often 
ciliate at tips and usually inconspicuously glan- 
dular along the margin. Corolla pink to purple, 
marked with white within, (10—)16-20(-27) mm 
long, the tube (6—)9—16 mm long, the upper lip 
3-11 mm long with lobes 2.5-10 mm long, the 
lower lip 4-14 mm long with lobes 3.5-11 mm 
long, the lower-central lobe usually pubescent on 
abaxial surface, the other lobes mostly glabrous. 
Stamens 1.5-2.5 mm long, the anthers 1.2-1.5 
mm long. Capsule 6.5—12 mm long, glabrous or 
sparsely pubescent above the middle. Seeds 2.5- 
4 mm long, 2-3 mm wide, pubescent with long, 
appressed, bristle-like trichomes bearing flex- 
uose or downward-pointing lateral barbs or 
branches. 


Distribution. Southern United States (Flori- 
da and Texas), Mexico (Aguascalientes, Chihua- 
hua, Coahuila, Durango, Hidalgo, Jalisco, Méx- 
ico, Michoacán, Nayarit, Nuevo León, Oaxaca, 
Puebla, San Luis Potosí, Sinaloa, Tamaulipas, 
and Zacatecas), Guatemala, Colombia, Ecuador, 
Peru, Chile, Bolivia, and Argentina. Plants in 
Mexico and adjacent regions (Fig. 3) occur in 
arid associations (with Opuntia, Larrea, Con- 
dalia, Berberis, Flourensia, Yucca, and Parthe- 
nium), grasslands, deciduous thorn-forest, and 
pine-oak communities at elevations from 20 to 
2,700 meters. In Florida, the species occurs in 
seasonally wet pinelands (Feb.—Oct.). 


1984] DANIEL— STENANDRIUM 1041 


FIGURE 5. Illustration of Stenandrium dulce from A. J. Cavanilles’s “Icones et Descriptiones Plantarum,” 
Published in 1791. 


Representative specimens beri UNITED —Ó ston et al. 9003 (LL, MEXU). COAHUILA: Sierra del 
STATES. FLORIDA: Citrus Co., of Homosassa ^ Pino, Johnston & Muller 393 (GH, LL); vic. of Saltillo, 
Springs, Eyles & Eyles 8260 (GE piel Co. Fla. Palmer 529 (US), 578 (US). DURANGO: uan del 
46, Seminole Indian Reservation, Lakela 28987 Alamo, Robert 4024 (ENCB); ca. 12 mi. NW of Can- 

А); Dade Со. , Biscayne Вау, Curtiss 1945 (СН, К, айап along Rt. 39, Pinkava et al. 9373 (ASU). HI- 
US); Highlands Co. ‚ Rt. 18, 5 mi. W of Childs, Brass | DALGO: N of Jacala de Ledesma, Clark 701 1 (МО). 


Ў are ip US); Hillsborough со, Old Memorial JALISCO: n , Gto., 5 mi. SE ofjct. at Lagos 
of de no, McVaugh 17798 (MICH); near G 

Lala et al. 25084 (GH, RSA), Lokela 25243 e jara, Pringl MEXICO: Temascaltepec, 

o ., Vic. of Fort Meyers, Standley 71 (GH, U orrera, Hinton et al. 754 (ENCB, GH, K, LL, MO, 

unty undetermined, locali pecified, е NY, US), 8080 (К, LL, MICH, e US); Рећоп, Hin- 


N, 1889 (DS, US). Texas: Hidalgo C Co. Santa Ana ton et al. 6086 (F, GH, К, MO, NY, US). MICHOACÁN: 

atl. Wildlife Refuge, Fleetwood 7007 (TEX); Starr Тоша Santa Maria, vic. of Morelia, Arsène 2756 (US). 
Wet Hwy. 4, E of Fort Ri nggold, Runyon 3256 (TEX); T: 23 mi. NNW of Tepic along Hwy. 15, Marcks 
ebb Co., Rio Grande, Laredo, пита 1005 (ОН, 4 Marck 1182 (LL); between Acaponeta and Pedro 


Ба Willacy Co., ca. 4 mi. NNW о афа Sauz Рашо, Rose 3316 (US); 1-3 km W of El Venado along 
ch, Johnston 53266.6 (TEX). Ман ылайы Сю Јене Mita. Breedlove & Almeda 
km ientes, Reedowski 14020 45287 (CAS). NUEVO LEON: 1-2 mi. SW о £ Pablillo, 


ENCE, CHIHUAHUA: 14 mi. SE of Rancho La Gloria Correll & Johnston 19928 (LL, US). ОАХА i 
nrd. to Cerros Blancos, 27°15'40°N, 104°09’W, John- NW of La Ventosa along Trans-Isthmian Hwy, Ning 


1042 


(MICH). PUEBLA: vic. of San Luis Pe. or vn 
ar Oaxaca, Purpus 3340 (F, MO, UC). SAN L 
tis Bagre, Minas de San Rafael, Purpus 5229 (Р, 
МО, ОС, US). siNALOA: between Concepción and Ro- 


between Pefia Ne vada and Hermosa, Stanford et al. 
2522 (DS, US). ZACATECAS: 6.5 m: Tiburcio 
on rd. to Concepción del Oro, Johnston 26 1. 2 Se 


yarit or Sinaloa), Sessé et al. 2174 (MA). А 
PETEN: Chiche, Petén, Lundell 3707 (F, MICH). 


Stenandrium dulce (Fig. 5) is the most widely 
distributed species in the genus and the most 
morphologically variable. Plants from North and 
Central America show considerable variation in 
height, pubescence, leaf form, size of the corolla, 
bract shape, and density of flowers in the inflo- 
rescence. Several species have been described or 
proposed based on some of the diverse forms of 
S. dulce. Leonard (1936) described S. guate- 
malense and distinguished it from related Mex- 
ican species by its narrow, sharply acuminate, 
and pilose bracts. Later (Leonard, 1938), he de- 

scribed S. mexicanum and characterized it by 
broad leaf blades, obtuse or rounded bracts, and 
large purple flowers. He noted its close relation- 
ship to S. dulce from Chile. Gibson (1974) in- 
cluded S. guatemalense within S. dulce in her 
treatment of the Acanthaceae of Guatemala and 
S. mexicanum is here included in this common 
species. In 1932 Leonard labelled several dimin- 
utive, small-leaved specimens of S. dulce from 
north-central Mexico with a manuscript name at 
US. Several specimens from Michoacan and an 
unusual form from west-central Mexico were 
likewi iven manuscript names. Leonard ob- 
viously believed S. dulce to be a South American 
species and the various morphological entities 
from North and Central America to be worthy 
of specific status. Examination ofa large number 
of specimens from throughout America leads me 
to conclude that all of Leonard's entities are part 
of a single morphologically diverse species that 
lacks consistent gaps among the various forms. 
Species with large ranges and considerable mor- 
phological variability are well known in several 
other genera of American Acanthaceae (e. g., 
Aphelandra aurantiaca (Scheidweiler) Lindley, 
Carlowrightia arizonica A. Gray, Elytraria im- 
bricata (Vahl) Pers., Justica carthagenensis Jacq., 
Ruellia geminiflora H.B.K., and Tetramerium 
nervosum Nees). 

One of the entities “recognized” by Leonard 
is worthy of some discussion. Specimens from 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


southern Sinaloa and northern Nayarit (Breed- 
love & Almeda 45287; Marcks & Marcks 1182; 
Rose 1534, 3179, 3316; Sessé et al. 2174) are 
rather distinctive by their long, narrow (3-18 
times longer than wide), and strap-shaped or ob- 
lanceolate (rarely elliptic) leaves, long (100-200 

mm) peduncles, and glabrous corollas. In addi- 
tion, the bracts vary from emarginate to rounded 
to acute at the apex and the bractlets and calyces 
of these plants are frequently glabrous. In spec- 
imens of S. dulce from other regions the leaves 
are usually wide (1.5—3.5 times longer than wide) 
and ovate or ovate-elliptic; the peduncles are 
usually less than 100 mm long; the lower-central 
petal lobe is usually pubescent; the bracts are 
acute at the apex; and the bractlets and calyces 
are normally conspicuously pubescent. Further, 
most of the specimens from Sinaloa and Nayarit 
are from regions of deciduous thorn-forest 
(Breedlove & Almeda 45287 is from a savanna) 
whereas all other collections of S. dulce from 
west-central Mexico are from grassland com- 
munities at relatively high elevations. This as- 
semblage may eventually prove worthy of va- 
rietal or specific status — of ae minor mor- 
phological t land 
geographical distinctness. The general overlap of 
all of the characters mentioned above between 
these plants and more typical specimens of 5. 
dulce preclude formal taxonomic recognition of 

until the variation from through- 

out the range fof S. dulce has been considered. 
Indeed, some plants of S. dulce from Florida 
(e.g., Simpson s.n., 1889) closely и the 
specimens from Sinaloa and Nayari 

Asa Gray (1878) recognized S. (aed var. flori- 
danum on the basis of glabrous plants with only 
the upper bracts and bractlets lightly hirsute-cil- 
iate. Long (1970) noted the very similar appear- 
ance of S. dulce var. floridanum with S. dulce 
var. dulce and claimed the former differed by 
usually having the upper bracts and bractlets gla- 
brous or sparingly hirsute-ciliate rather than hir- 
sute. This distinction does not hold up when 
specimens from throughout the range of the 
species are examined. Long further noted the close 
relationship of this variety with S. mexicanum 
and the relationship between S. faciculare and 
S. dulce. Most of the variation encountered in 
S. dulce in the region covered by this revision 
can be seen among the diverse specimens from 
peninsular Florida. 

The various forms comprising S. dulce are held 
together by a suite of characters including the 


1984] 


acaulescent habit, usually conspicuously petio- 
late leaves lacking long (1—4 mm), white, shaggy 
trichomes, and lanceolate to elliptic (rarely ob- 


United States, north and west of the range of S. 
dulce. The ranges of these three species are not 
known to overlap. The distinctions among them 
are summarized in the key and are further dis- 
cussed elsewhere in the text. 


EXCLUDED TAXA 
Stenandrium pelorium Leonard, Wrightia 2: 83. 
1960. = Holographis ep ает ЋЕ 
Daniel, Madroño 31: 90. 


LITERATURE CITED 
BLAKE, S. Е. 1917. Descriptions of new жар 
phytes, ot from the collection of Prof. M. E 
Peck in British Honduras. Contr. Gray Herb. 52: 


59- T 
BREMEKAMP, C. E. B. 1965. Delimitation and sub- 
арто of the Acanthaceae. Bull. Bot. Surv. India 
7: 21- 


DANIEL, T F. 983. Systematics of qe 
(Acanthaceae) J. Arnold ano 64: 129-160. 
w and reconsi exican Acan- 


thaceae. Madrofio 31: 86-92. 


NOTE ADDED IN PROOF: 


DANIEL— STENANDRIUM 


1043 


GIBSON, D. N. 1974. Acanthaceae. Jn P. С. Standley 
et al., Flora of Guatemala. Fieldiana, Bot. 24(10): 
E 


Gray, A. 1878. Synoptical Flora of North America, 
Volume 2. Ivison and Co., New York. 

JOHNSTON, J. R. 1908. A collection of plants from 
з vicinity of La Guaira, Venezuela. Contr. 0.8. 

. Herb. 12: 105-111. 
Рт тен Е. С. 1936. The Acanthaceae of the Yu- 
eninsula. Publ. Carnegie Inst. Wash. 461: 
193-238. 

: "e Contributions to the flora of tropical 
Am XXXIV. Plantae Hintonianae: VI. Kew 
Bull. 19380): 59-73. 

————. 1942. New tropical American Acanthaceae. 
J. Wash. Acad. Sci.'32: 184—187. 


Linpau, С. 1895. Acanthaceae. Nat. Pflanzenfam. 
IV, 3b: i 4-35 
Томе, R. W. 1970. The genera of Acanthaceae in the 


ahi United States. J. Arnold Arbor. 51: 
257-309. 


NEES VON ESENBECK, С. С. 1847. Sap InA. 
. DeCandolle (editor), Prodr. 11: 4 

ОБЕЕ5ТЕР, А. S. 1854. Mexicos og Cent erikas 
canthaceer. Vidensk. ка ddel. Dansk "ава 

п. Кјађепћауп 6: 113-181. 

STANDLEY, Р. С. 1926. Trees and shrubs of Mexico 

ignoniaceae—Asteraceae). Contr. U.S. Natl. Herb. 
23: 13131 721. 

1930. Studies of American plants— HI. Publ. 
Columbian Mus., Bot. Ser. 8: 3—73. 
жыл D.C. 1966. Acanthaceae. In C. L. Lun- 
dell, Flora of Texas 1: 223-282. Texas Research 

Foundation, Renner, Texas. 


After this revision went to press, a chromosome 


count of л = 26 was obtained for 5. barbatum. Relationships among Sten- 
andrium, Holographis, and Aphelandra are discussed further by Daniel et 
al. (Syst. Bot. 9: 346-355. 1984) based on known chromosome counts of 


species in these genera. 


A BIBLIOGRAPHY OF NUMERICAL PHENETIC 
STUDIES IN SYSTEMATIC BOTANY 


BERNARD В. BAUM,! THOMAS DUNCAN,” AND RAYMOND B. PHILLIPS? 


INTRODUCTION 


The purpose of this paper is to supplement the bibliography in a review of numerical phenetics 
(Numerical phenetics: its uses in botanical systematics. 1981. T. Duncan & B. Baum, Annual Rev. 
Ecol. Syst. 12: 387—404). Due to space limitations, a listing of numerical phenetic applications in 
botany could not be included in that review. This compilation of applications in plant groups is 
provided below. Papers that deal with the development of methods with only incidental mention 
of plant groups have been excluded. These studies illustrating applications of numerical phenetics 
are listed according to the taxon covered by each author(s) (Table 1). Each study is listed using the 
lowest taxonomic rank to include all organisms examined. For studies involving two or more 
taxonomic groups of equal rank, the study is listed under each group mentioned. Genus is the lowest 
taxonomic rank used. We have included the references cited in Sneath and Sokal (1973) in order 
to provide a complete listing for botany arranged according to taxonomic group. Our literature 
search ends with 1982. The references included here complement the recent bibliography of cladistic 
studies of plant groups (A bibliography of botanical cladistics. I. 1981. V. Funk & W. H. Wagner, 
Jr. Brittonia 34: 118-124). These two bibliographies and the review cited above will serve as a basic 
guide to numerical taxonomic studies in botany. We would appreciate knowing of any additions, 


deletions, or other corrections to our list. 


TABLE 1. 


Numerical phenetic applications in bot- 


any arranged according to plant group studied. 


TABLE 1. 


Continued. 


Taxonomic Group 


Reference(s) 


Taxonomic Group 


Reference(s) 


Abelmoschus Chheda & Fatokun, 1982; Apocynum Balbach, 1965 
Singh et al., 1980 Aquilegia La Roche, 1980; Taylor & 
Abronia Pimentel, 1981 Campbell, 1969 
Acacia Farrell & Ashton, 1978 Arachis Brown et al., 1975; Stalker et 
Aegilops Kaltsikes & Dedio, 1970a, ., 1979 
1970b; Tsuji & Tsunewaki, Arceuthobium Hawksworth et al., 1968 
1976; Tsunewaki et al., Archochaetiaceae Gabany, 1979 
1976 Armoracia Rhodes et al., 1969 
Aesculus Wyatt & Lodwick, 1981 Arundinelleae (Po- ^ Clayton, 1970; Phipps, 1970, 
Allium Jacobsen, 1979, 1980 aceae) 1972a, 1972b, 1972c, 
Allium subg. Mo- Badr & Elkington, 1978 
ium ; ) Asclepias Gilmartin, 1980a 
Allium subg. Rhi- El-Gadi & Elkington, 1977 Asclepiadaceae Gilmartin, 1974, 1980b, 1981 
zirideum Atriplex Kowal & Kuzniewski, 1959 
Alloplectus Stearn, 1968, 1969 Athyrium Seong, 1972 
Нетпата Joly, 1969 уепа Baum, 1970, 1974, 1975, 
Andropogoneae Clayton, 1972a, 1972b 1977; Baum & Brach, 1975; 
оасеае) | Baum & Lefkovitch, 1972a, 
Anemia subg. Cop- Mickel, 1962 1972b, 1973 
tophyllum Baptisia Flake & Turner, 1968 
Anigozanthos Hopper, 1977, 1978 Basidiomycetes Kendrick & Weresub, 1966 
Antennaria Beals, 196 Beta sect. Vulgares Ford-Lloyd & Williams, 1975 
Anthyllis Gonnet, 1980 etula Baranov & Basargin, 1979 


' Biosystematic Research Institute, Research Branch, Agriculture 
: Department of Botany, University of California, Berkeley, 


Canada, Ottawa, Ontario, Canada K1A 0C6. 
California 94720. 


ent of Botany and Microbiology, University of Oklahoma, Norman, Oklahoma 73019. 


ANN. Missouri Bor. GARD. 71: 1044-1060. 1984. 


1984] 


TABLE 1. 


BAUM ET AL.—NUMERICAL PHENETIC STUDIES 


Continued. 


TABLE 1. 


1045 


Continued. 


Taxonomic Group 


Reference(s) 


Taxonomic Group 


Reference(s) 


Blue-green algae 
Blumea 


Boleum 
Brassica 


Brassiceae (Brassi- 
caceae 

Brassicinae (Brassi- 

Bromeliaceae 


Bulbostylis 
Bulnesia 


nabis 
Capsicum 
Carex 
Carya 
Cassia sect. Apou- 
couita 
Caucalideae (U m- 
belliferae) 


Chenopodium 
Chlorella 


гуѕо е 
Chrysothamnus 
Cicer 
Cirsium 
Citrus 
Clarkia 


Clethra 
Coelorhachis 


Whitton, 1969 
Dakshini & Prithipalsingh, 
977 


Gomez-Campo, 1981 
Cole & Phelps, 1979; Dass & 
m, 1967; Vaughan & 
Denford, 1968; Vaughan et 
al., 1970; Yamasishi & 


Takahata & Hinata, 1980 


Gilmartin, таа 1969, 
1974, 1 

Hall et al., AT 

Comas et al., 1979; Crisci et 
al., 197 

Cauwet-Marc et al., 1978 

Mooney & Emboden, 1968 

Rodman, 1980 

Bischler & Joly, 1970 


Kocková-Kratochvilová, 
1970; Shechter, 1973; 
Shechter et al., 1972 

Small et al., 1976 

Eshbaugh, 1970; Pickersgill et 


, 1979 
Krzakowa et al., 1978 
Stone et al., 1969 
rwin & Rogers, 1967 


McNeill et al., 1969 


Hassal, 1976 

Williams & Ford-Lloyd, 1974 

Crawford, 1974; Crawford & 
Julian, 1976; Crawford & 


olds & Crawford, 1980 
Cullimore, 1969 
McGuire, 1969 
Ducker et al., 1965 
Prance et al., 1969 
Van Valkenburg et al., 1977 
McArthur et 
Narayan & Maceóeld; 1976 
Davidson, 1963 
Barrett & Rhodes, 1976 
Bloom, 1976; Small et al., 

1 


Duncan, 1978 
Clayton, 1969 


0 
Conidiobolus 
Corr 
Pur, 
Cucumerinae (Cu- 
curbitaceae) 
Cucurbita 


Debaryomyces 
Dermatophytes 
Desmodium 
Dichanthelium 
igitari 
Dioscorea 


Ectocarpaceae 


Erechtites 


Ericales 
Eryngium 


Eucalyptus 


Flindersia 


Gleicheniaceae 
Glycine 


Wilken, 1978 


Stearn, 1968, 1969 
King, 1976a, 1976b 


їйїп, 197 
Bisby, 1970, 1973 
Dass et al., 1974 


Bemis et al., 1970; Rhodes et 
al., 8 


Petriella & Crisci, 1975 


Small, 1978b 
Kockova-Kratochvilova et al., 
197 


Komenda et al., 1973; Lan- 
dau et al., 1968; Shechter, 
1973 

Bhalla & Dakwale, 1977 

Allred & Gould, 1978 


Judd, 1979 

Watson et al., 1967 

Hideux et al., 1978; Van der 
Pluym & Hideux, 1977a, 
1977b 

Banks & Hillis, 1969; Hopper 
et al., 1978; Kirkpatrick, 
1974; Phillips & Reid, 
1980; Whiffin, 1981 


1961 
Bidault, 1968: Bidault & Hu- 
bac, 1967; Parreaux, 1972 
Hall et al., 1976 
Whiffin, 1982a, 1982b 
Jensen & Hancock, 1982 
Kendrick & Proctor, 1964 
itney et al., 1968 
Bisby & Nicholls, 1977 


Machol & Singer, 1977 


1978 
Broich & Palmer, 1980; Edye 
et al 


1046 


TABLE 1. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


Continued. 


TABLE 1. 


[VoL. 71 


Continued. 


Taxonomic Group 


Reference(s) 


Taxonomic Group 


Reference(s) 


Glycine subg. Gly- 
cine 


Gossypium 


Blepharodon 
Haptophyceae 
Helianthus 
Helminthosporium 


Hibiscus sect. Fur- 
caria 


Hordeum 


Humulus 
Hydrophyllum 
Hydropus 
Hyperthelia 


Hypoxylon 


Jansenella 
Juglans 
Juniperus 


Klebsielleae 
Kluyveromyces 
Labiatae 


о MM oo s 


Newell & Hymowitz, 1978 


Johnson & Thein, 1970 
Bjornstad & Friis, 1972 
Barabe et al., 1981 
Poncet, 1970 

Jackson & Crovello, 1971 
Ramon, 1968 


Van Valkenburg et al., 1977 
Schilling & Heiser, 1981 
Ibrahim & Threlfall, 1966 
Koek-Noorman, 1980 
Ernst, 1967 

Wilson, 1974 


Zandee & Glas, 1982 

Baum, 1980; Booth & Rich- 
ards, 1976; Kahler & Al- 
lard, 1981; Molina-Cano, 
1976; Molina-Cano & Ros- 
sello, 1978; Nevo et al., 
1979 

Small, 1978a, 1980 

Beckmann, 1979 

Kiefer, 1979; Machol & Sing- 

1977 


Clayton, 1975 

Whalley, 1976; Whalley & 
Greenhalgh, 1973a, 1973b, 
1975a, 1975b 


Adams & Turner, 1970; R. P. 


Adams, 1977; Flake et al., 
1969; Kelley & Adams, 
1978 


Barnett et al., 1975 


Kendrick а о 1964 
Curtis, 19 

Clifford E vibus 1980 
Ornduff & Crovello, 1968; 


Parker, 
Arroyo-Kalin, 1973 
Taylor, 1966 
Govoni, 1975 
Thomson, 1974 


Lotus Grant & Zandstra, 1968; Si- 
mon & Goodall, 1968 
Loudetia Lubke & Phipps, 1973 
Lupinus Riggins et al., 1977 
ychnis McNeill, 1978 
Lycoperdon Demoulin & Schumacker, 
197 
Lycopus Webber & Ball, 1980 
ygodium Duek et al., 1979 
Magnoliatae Young & Watson, 1970 
Magnoliophyta Dolph, 1976; Hill, 1980 
Mangifera Rhodes et al., 1970 
anihot Rogers & Fleming, 1973 
Meconella Ernst, 1967 
Medicago Classen et al., 1982; Simon & 
Goodall, 1968; Yamada & 
Suzuki, 1 
Melandrium McNeill, 1978 
Melastomaceae Gilmartin, 1981 
Melilotus ukowiecki et al., 1976 
Mentha Olsson, 1967 
Mentzelia Hill, 1977 
Menziesia Hickman & Johnson, 1969 
icraira Clifford, 1964 
Mimulus Wells, 1980 
Montieae (Portula- McNeill, 1974 
caceae 
Mosla Cheng, 1980 
Nanoplankton Van Valkenburg et al., 1977 
Nassauviinae Crisci, 1974 
(Compositae) 
Neottioideae (Or- Lavarack, 1976 
chidaceae) 
Nocardia Kurup & Schmitt, 1973 
Nodulisporium Van Valkenburg et al. 1977; 
Whalley & Greenhalgh, 
1975a 
Nymphaeaceae Bukowiecki et al., 1972, 1974 
Olea Loukas & Krimbas, 1983 
Oenothera Rostanski, 1968, 1969 
Oncidiinae (Orchi- ^ Wirth et al., 1966 
daceae) 
Ononis Ivimey-Cook, 1968, 1969 
Oplonia Stearn, 1971 
Orchidaceae Clifford & Lavarack, 1974 _ 
Oryza Janoria et al., 1976; Morishi- 
ma, 1969; Morishima & 
Oka, 1960; Ng et al., 1981; 
& Williams, 1978; 
Palanichamy & Siddiq, 
1977; Shahi et al., 1969 
Oryzopsis Kam & Maze, 1974 
xalis sect. Ionox- Denton & Del Moral, 1976 
alis 
Panicum Lloyd & Thompson, 1978; 
-o o ë Mosan 1970 .«— 


BAUM ET AL.—NUMERICAL PHENETIC STUDIES 


1047 


1984] 
TABLE 1. Continued. TABLE 1. Continued. 
Taxonomic Group Reference(s) Taxonomic Group m 
Parahebe Garnock-Jones & Langer, Relbunium Porto & Mariath, 5 
1980 Rhizopus Dabinett & E 1973 
Pennisetum sect. Brunken, 1979 Rhododendron ‚19 
Brevivalvula Rhynchosia Walraven, 1970 
Pennisetum Beillard et al., 1980 Rhytachne Clayton, 1969 
Petunia Natarella & Sink, 1974 Rosa Kuhns & Fretz, 1978 
Phaeophyta Russell & Fletcher, 1975 Rosa sect. Pimpi- Roberts, 1977 
Phaseolus M. W. Adams, 1977; Sagar et nellifoliae 
al., 1976; Sahai & Rana, i Gilmartin, 1981; Hogeweg & 
1977 Koek-Noorman, 1975 
Phlox Levin & Schaal, 1970; Levy & Sabatia Bell & Lester, 1978 
Levin, 1975 Saccharomyces Kocková-Kratochvilová et al., 
Phyllota Jancey, 1966 1969; Kocková-Kratochvi- 
Picea Birks & Peglar, 1980; Gor- lová, 1970 
don, 1976; La Roi & Dugle, Saccharum Gupta et al., 1978 
1968; Mitton & Andalora, Salix sect. Sitchen- СгоуеПо, 1968a, 1968b, 
1981; Taylor & Patterson, 1968c, 1968d, 1969 
= 980 Salvia El-Gazzar et al., 1968; John- 
Pichia Poncet, 1967a, 1967b son & Holm, 19 
+ Judd, 1982 Sarchina Hubac, 1967 
Prieta Young & Watson, 1969 Sarcostemma Johnson & Holm, 1968 
m E gl pe > Sarracenia Schnell & Krider, 1976 
таарав nes кк ifraga Jaworska & Nybom, 1967 
Black, 1963; Thielges, 1969 А А 
4 : Dedio et al., 1969a; Sencer & 
ету, Rahn, 197k: ай nm 
sis Sematophyllaceae Seki, 1968 
McNeill, 1982 А ew 
Platin Setaria Chikara & Gupta, 1980; Wil- 
Phe P 0 eie nd i liams & Schreiber, 1976 
Pl ape Та! annan Silene Aeschimann et al., 1981; 
eurothallidinae Pridgeon, 1982 i i 
: У McNeill, 1978; Prentice, 
(Orchidaceae) 1979 
Р ТРЕ “4° 
dis Williamson & Killick, 1978 Sinapis Vaughan & Denford, 1968 
оасеае Clayton & Cope, 1980; Clif- B &M 1976: Hei 
ford, 1965, 1969; Clifford & Solanum ОЕ МИНЬ PIG: Heuer, 
1, 1967; Clifford et 1972; Heiser et al., 1965; 
al. 1969; Hilu & Wright, ман DON 1972; 
1982 Raeuber et al., 1978; Schill- 
Polygonum McDonald. 1980 ing, 1981; Schilling & Heis- 
ss CLIONAIG, er, 1976; Soria & Heiser, 
ener: (Poaceae) MacFarlane & Watson, 1982 1961 
opulus Pallardy & Kozlowsky, 1979 
t - J 
E Gorske et al., 1979 ee An Whalen, 1979 
silanthele t 71 
eridop ey vH ud sect. Edmonds, 1978 
ola Haber. 1983 olanum 
коня : stt Solidago Melville & Morton, 1982 
Quercus Hicks & Burch, 1977; Jensen, | Sorghum Mendoza & Torregroza, 1978; 
1977a, 1977b; Jensen & De Wet & Huckabay, 1967; 
Eshbaugh, 1976a, 1976b; Gupta et al., 1978; Ivanyu- 
Knops & Jensen, 1980; Ols- пон & Malkina, 1978; 
son, 1975; Rushton, 1978, ang & ie 1966; 
ina Sheard. 1978 Spilanthes Jansen, s 
Ranunculus Duncan, 1980, 1981; Duncan Spiranthes Catling, 1981 
& Estabrook, 1976 Stellaria Whitehead & Sinha, 1967 
Raphanus Lewis-Jones et al., 1982 Stenotaphrum Busey et al., 1982 


1048 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Vor. 71 
TABLE 1. Continued. TABLE 1. Continued. 
Taxonomic Group Reference(s) Taxonomic Group Reference(s) 
Stipa Barkworth, 1978; Barkworth Umbelliferae Gilmartin, 1980b; Hideux et 
et al., 1979 al., 1978 
Stylidium Coates, 1981 Uredinales Shipton & Fleischmann, 1969 
Stylosanthes Burt et al., 1971; Mannetje, Vaccinium Smith, 1969; Van der Kloet, 
1969 1977b, 1978 
Suaeda Ungar & Boucaud, 1974 Vaccinium sect. Van der Kloet, 1977a 
Taphrina Snider & Kramer, 1974a, Cyanococcus 
1974b Vella Gomez-Campo, 1981 
Thelypodieae Hauser & Crovello, 1982 Verbena Barber, 1982 
(Brassicaceae) Verbenaceae El-Gazzar Watson, 1970; 
Thuidiaceae Gier, 1980 El-Gazzar, 1974 
Tiarella Taylor, 1971 Vernonia Dakshini P Dediani. 1976 
Tithonia La Duke, 1982 Verticillium Whitney et al., 1968 
Trifolium Mannetje, 1967; Parups et al., Vigna Sahai & Rana, 1977 
1966 Viola Gilmartin & Harvey, 1976 
Trigonella Simon & Goodall, 1968 Vitis Rogers & Rogers, 1978 
Tripsacum Stalker et al., 1977a, 1977b Yeasts Barnett et al., 1975; Jones, 
Triticale Dedio et al., 1969b; Kaltsikes, 1975 
1974 Zea Camussi, 1979; Camussi et 
Triticeae (Poaceae) Baum, 1977, 1978a, 1978b, al., 1980; Casas et al., 1968; 
1978c, 1982; Baum et al., Doebley & Iltis, 1980; Fuji- 
1980; Baum & Tulloch, no, 1980; Goodman, 1967, 
1982; Tulloch et al., 1980 1968; Goodman & Bird, 
Triticum Schulze-Motel, 1978; Syme & 1977; Jancey, 1975; Bird 
Thompson, 1981; Tsuji & & Goodman, 1977; Rhodes 
Tsunewaki, 1976; Tsune- & Carmer, 1966; Tarcicio 
waki et al., 1976; Wrigley et et al., 1978; Stalker et al., 
al., 1981, 1982 1977a, 1977b 
Tsuga Kessell, 1979 Zinnia subg. Katz & Torres, 1965 
Ulmus Jeffers & Richens, 1970; Mel- Diplothrix 
ville, 1978 


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| 


NOTES ОМ SYMPHYTUM (BORAGINACEAE) IN 
NORTH AMERICA 


T. W. J. GADELLA! 


ABSTRACT 


In this paper I present the results of a morphological comparison of the North American material 


of Symphytum with herbarium material of European hybrid populations for which cytolo 
are available. In addition to S. алелей зә, ү ж. and rarely S. as, 


48, 40) is pee 


Some species of the Old World genus Sym- 
phytum have escaped from cultivation (Ingram, 
1961) and become naturalized in various habi- 
tats in North America. They usually grow on 
(damp) roadsides, in waste wow. аи disturbed 
habitats, sometimes along ditches. Four species 
are dealt with in various floras: 


Symphytum asperum Lepech. (Jepson, 1925; 
Fernald, 1950; Abrams, 1951; Munz & Keck, 
1959; Hitchcock et al., 1959; Gleason, 1968; 
Rickett, 1966, 1971; Scoggan, 1979). 

S. uliginosum Kern. (Fernald, 1950). 

S. officinale L. (Fernald, 1950; Rydberg, 1954; 
Hitchcock et al., 1959; Steyermark, 1963; 
Rickett, 1966; Gleason: 1968; Scoggan, 1979). 

S. tuberosum L. (Fernald, 1950; Rickett, 1966; 
Gleason, 1968). 


Three species belong to subgenus Symphytum 
(= Ramosa Bucknall), one (S. tuberosum) to sub- 
genus Simplicia. The subgenus Symphytum is 
characterized by branched stems and fusiform 

ranched roots, subgenus Simplicia by simple 
Stems and creeping tuberous roots. The repre- 
sentative of subgenus Simplicia, S. tuberosum, 
is readily identifiable by those features and will 
Dot be treated further in this paper. Moreover, 
this species seems to be rather local in North 
America (Rickett, 1966; Fernald, 1950). The three 
other species hybridize and form hybrid swarms 
Consisting of Е, and backcross hybrids (Gadella, 
1972; Gadella & Kliphuis, 1973, 1978). Sym- 
Phytum officinale is cytologically heterogeneous: 
2n= 24, 2n = 40, 2n = 48—cytotypes occur in 
Various parts of Europe. Symphytum asperum 


а ЕНИ Ne 


gical data 
asperum, also ae m brid S. x 


o all taxa, S. tuberosum L., S. as, 


(2n = 32) does not hybridize with the diploid 
(2n = 24) form of S. officinale in Europe but pro- 
duces hybrids (and backcrosses) with the 2n = 
40 and 2n = 48 cytotypes of S. officinale. The 
primary hybrids, with 2n = 36, or 2n = 40, аге 
collectively known under the name S. x uplan- 
dicum Nyman. In Europe the parental species 
are largely allopatric with a very small zone of 
overlap in the northwest Caucasus (Kusnetsov, 
1910). In the zone of overlap, hybridization does 
not occur because S. officinale and S. asperum 
grow at different altitudes. Apparently the hy- 
brids arose outside the sasus (Tutin, 1956; 
Wade, 1958). In many parts of western, north- 
western, Or central Europe the hybrid swarms are 

Because 
of the widespread use of Symphytum officinale 
and its hybrids in “green drinks,”? and as a fod- 
der-plant (Farnsworth, 1979; Hills, 1976). Huiz- 
ing et al. (1982) focused their attention on the 
presence or absence of the hepatotoxic pyr- 
rolizidine alkaloids and ки their possible use as 
|| се 


lycopsamine, and Ета. ог their isomers 
were found in the S. officinale cytotypes, echim- 
idine and symphytine in S. asperum. The inter- 
specific hybrids contained all alkaloids men- 


© 


oned. 

ms nsultation of many North American floras 
clearly showed that the hybrid S. x uplandicum 
is not reported from North America. Some years 
ago I received 38 herbarium sheets of Symphy- 
tum on loan from the U.S. National segs 
(US) and 33 from Herbier Marie-Victorin 

tanical Institute of Montreal (MT). Кавана 
of these plants made clear that 5. х uplandicum 


"Department of Evolutionary Biology, State University of Utrecht, Padualaan 8, 3584 CH Utrecht, The 


Nether! lands. 


* Green parts of comfrey are blended with water and the filtrate is used as a “green drink.” 


ANN. Missourr Bor. GARD. 71: 1061-1067. 1984. 


1062 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Vot. 71 


was present in North America. For that reason 
I present in this paper the results of a morpho- 
logical comparison of the North American ma- 
terial with herbarium material of European hy- 
brid populations for which cytological and 
chemical data are available. 


MATERIALS AND METHODS 


Seventy-one herbarium sheets of North Amer- 
ican plants of Symphytum were compared with 
collections of European plants and hybrids. 


RESULTS 


Ofthe 71 North American specimens, 57 plants 
were originally identified as S. officinale, but only 
33 belong to that species. Although 45% of all 
plants (32 plants) belong to the interspecific 
hybrid S. x uplandicum, not a single plant of the 
herbarium collection from North America was 
referred to this taxon. Most plants that were re- 
ferred to S. asperum appeared to belong to S. x 
uplandicum (nine sheets), some to S. officinale 
(four sheets), and only two plants proved to be 

correctly id 


козше to S. officinale but appeared to belong 
to S. asperum. Symphytum peregrinum Ledeb. 
proved to be absent from North America—all 
sheets (three) under this name proved to belong 
to S. x uplandicum. At least two cytotypes of S. 
officinale occur in North America: 2n = 24 ог 
2n = 48 (these taxa are indistinguishable if the 
flower color of the latter is white; diploids are 
always white-flowered), and 2л = 40. Twenty- 
nine sheets studied proved to belong to S. offi- 
cinale (white-flowered plants: 2n = 24 or 2n = 
48; purple-flowered plants: 27 = 48). Plants with 
2n = 40 are usually purple-flowered and usually 
occur in very moist habitats. In the Netherlands 
the 27 — 40 cytotype is very common in the low 
lying peat lands of Noord Holland, Utrecht, and 
Friesland. Populations with 25 = 40 may have 
a much wider European distribution because 
some of the characters of this cytotype closely 
match those of plants from Hungary and south- 
ern Russia. These latter plants were referred to 
S. uliginosum Kern. by de Soo (1926) and to S. 
tanaicense Steven by Degen (1930). Symphytum 
tanaicense is the correct name. Four plants at US 
very closely match the 27 = 40 cytotype of 5. 
officinale in morphology. All other plants of S. 
officinale probably belong to the cytotype 2n = 
48 (or 2n — 24). In this paper the plants with 
2n = 40 are assigned to S. officinale and not to 


S. tanaicense because the European plants with 
the same morphological characters have to be 
studied more carefully both morphologically and 
experimentally before we can arrive at more def- 
inite conclusions on the taxonomic status of S. 
tanaicense. In the following survey the species 
and hybrids will be described in more detail and 
a key to all species and hybrids will be given. 


KEY TO THE NORTH AMERICAN SPECIES AND HYBRIDS 


la. Stems simple; roots tuberous, creeping ....... 
5,1 uberosum L 
1b. Stem branched; roots fusiform, branched ____ 2 
2a. Stem. not winged; 90-200 cm long; leaves 
usually 
on the stem not longer than 1 cm); corolla 
ne غ‎ anulate; connective not projecting be- 
ond the thecae; fruits brown and dull, are- 
Dite и ue 3 
. Stem winged, 30-120 cm long; leaves always 
decurrent, usually along the entire internode; 
coro urceolate, upper part of the corolla 
urved; connective projecting beyond the 
Poe fruits black and shining, not areolate- 
ate but smooth _____ — 4 
3a. Flowering stems very scabrid with curved 
subretrorse hairs, 90-200 cm long; calyx 
mm long, divided to % of its length; flower 
buds red, corolla sky blue, 9-14 mm long; 
corolla-scales lingulate, papillae of the mar- 
gin of the corolla scales long and narrow . 


2 


с 


3b. Em d g + 1 v: | Le lh iry 90-1 
cm long; calyx 5.5 mm long, divided to % of 
its length; flower buds purple or pink, corolla 
pink or blue-purple, 13-16 mm long; corolla 


argi 
4a. Stems hispid, 30-120 cm long, soft to the 


airs, or, if present, the hairs not de- 
ciduous or prickly; marginal setae of calyx in 
an irregular pattern; calyx without tubercu- 
lar-based scabrous hairs; corolla in үш" white 
or purple; corolla white or purple, red NK 
intermediate between red and purple) at 
шк 7 _ S. officinale L. (2n = ^ 48) 
4b. Stems scabrous, 30-70 cm long; stems with 
prickly tubercular-based stiff and scabrous 


with many scabrous tubercular-based (decid- 


ыа purple (rarely white), bud purple 
(rarely white) _______ S. officinale L. (2n = 40) 


tA 
D 
Б 
$ 
о 
3 
es 
о 
2,8 
У 
^ 
8 
3 
M 
53 
sÈ 
e 
F 
E 


the adaxial side of the leaves as in 4b; in- 
dument of the calyx as in 4b; scale apex nar- 


1984] 


rowly — өче ae in bud purple, blue 
purple when in flow 


oe E S. x uplandicum Nym. (2n = 36) 
i Indument of the stem a harsh to the touch; 


Cn 
= 


current to 1 
niens : many short appressed stiff setae, which 


as in 4a; scale apex broad rotundate: corolla 
pink in bud and pink or pinkish blue in flow- 
. X uplandicum Nym. (2n = 40) 


Symphytum officinale L. Sp. Pl. 136. 1753. TYPE: 
Herb. Linn. 185/1, photo. 


5. eile Schmidt, Fl. Boem. 3: 13. tab. 263. 


8. Ads Steven, ES Soc. Imp. Naturalistes Mos- 
cou 24: 577. 185 
S. uliginosum Kerner, j^ ase Bot. Z. 13: 227. 1863. 


Stem to 120 cm long, distinctly winged, hispid; 
the indument renders the stems soft to the touch; 
basal leaves lanceolate or ovate, to 60 cm long, 
acute at the apex, acuminate and attenuate at the 
base; lamina 10—40 cm long, 2-12 cm wide; pet- 
iole 2-20 cm long; middle and upper stem leaves 
ofthe same type, but much smaller; adaxial side 
of the leaves with many short and long hairs, 
Which are never scabrid; sometimes these hairs 
have a tubercular base that is not deciduous; 
abaxial side of the leaves with long appressed 
hairs along the veins and many shorter hairs be- 
tween the veins; the leaf base is decurrent from 
node to node; calyx to 8, mm long, arisen to ? 
ofits length, calyx lob 
acute, marginal stiff setae wiih M an irregular dis- 
tribution pattern; these marginal setae lack a tu- 
bercular base; corolla urceolate, 15—17 mm long, 
white or cream in diploids (2n = 24) and tetra- 
Ploids (27 = 48), purple or red (or various in- 
termediate colors between white and dark pur- 
ple) in the tetraploids; stamens to 7 mm long, 


nective projecting beyond the thecae; squamae 
of the corolla triangular-lanceolate, 7-7.5 mm 
long and 2 mm wide at the base; apex mucronate, 

Papillae obtuse, papillae more densely crowded 
at the tip of the scale margin; fruit black and 
shiny, 4—5 mm long, 2—2.5 mm wide; reproduc- 
tion: both Cytotypes are obligate allogamous, they 
are strictly self-incompatible. The production of 
fruits (nutlets) varies considerably among differ- 
“nt populations, Even plants with normal fertil- 
Ü have many flowers which produce only 3, 2, 

or even 0 viable nutlets. 


GADELLA — SYMPHYTUM 


1063 


The diploid cytotype was assigned to S. bohe- 
micum Schmidt by A. Murin and J. Majovsky 
(Acta Fac. Rerum Nat. Univ. Comenianae Bot. 
29: 1982) 

The exact status of S. bohemicum, S. tanai- 
cense and S. uliginosum appears to require fur- 
ther investigation. The West European cytotype 
2п = 40 of S. officinale L. (q.v.) and S. tanaicense 
Steven are supposed to be very closely related or 
identical. 


: Gran 

. 1950, Warren s.n. (MT). ONTARIO: 

Comté de Prescott, 18 July 1935, Rouleau 1132 bat 
Westport, 23 Sept. 1905, Godfrey s.n. (MT). QUEBEC: 
Abercorn, Co. de Brome, 23 yd 1935, nigh Victorin 


Specimens examined. CANADA. NOVA SCOTIA 
Kings Co., 9 Aug 


1900, Way s.n. (US). MASSACHUSETTS: ct 

ence unknown, 4 July 1906, Knowlton s.n. (US); exact 
prorsum unknown, 12 Aug. 18 

(US) 


m 
ymous 3429b (US); Plainfield, 29 May 1879, Т weedy 


s.n. US); exact provenience unkno 80, Hyams 
n EW JERSEY: Amsterdam C mandale, 
05, Fisher s.n. (US); Sussex Co., Stockholm, 18 
July 1894, Sickle s. NEW YO Hamburg, 


July 1918, Johnson 1 158 (US); Syracuse, s.d., Straub 
s.n. (US); Warsaw, 21 June 1925, Keeler s.n. (US). 
VERMONT: Peacham, 30 June 1889, Blanchard s.n. (US) 
Peacham, 7 July 1892, Bent n. (US). 
exact роты ence un 
WISCONSIN: Manitowa, 1 July 1936, Benke 5791 (US). 
WYOMING: Castile, 18 June 1916, Killip s. n. (US). 


Symphyíum officinale L. (27 = 40). 


Stem to 70 cm long, distinctly winged, prickly 
and asperous, harsh to the touch; decurrence of 
the stem usuall the 2n = 
24 and 2n = 48 cytotypes, at least in the upper 
leaves, but still distinctly present; shape of the 
leaf the same as in S. affici nale. Qn — 24, 48). 
Indument of the 1 fthe lamina 
very scabrous with many short tubercular based 
prickly setae that are deciduous; between the hairs 
curved or uncinate hairs with or 


divided to % of its length: calyx lobes triangular- 
lanceolate with an acute tip; stiff marginal setae 
in a very regular distribution pattern; some of 
the marginal and dorso-median hairs with a tu- 
bercular base; corolla eine 16-19 mm, usu- 
ally dark or light purple, 
stamens as in the 24/48 pec Rate of S. officinale, 
but stamens somewhat longer than squamae; pa- 


: 11 21.6 
ry occasionally уп, 


1064 


pillae of the corolla scales more densely crowded 
in the middle of the scale margin, otherwise the 
same as in S. officinale 2n = 24, 48; fruit as in 
the 2n = 24/48 cytotypes of S. officinale, repro- 
duction obligate allogamous, plants strictly self- 
incompatible. Even plants with normal fertility 
may have flowers that produce only 3, 2, 1, or 
even (and not occasionally) 0 viable nutlets. 


Specimens examined. U.S.A. NEW JERSEY: Com- 
munipaw Ferry, Hobokenville, 29 May 1880, Brown 
s.n. (US). NEw york: N of New York, 29 July 1929, 
Parker Phelps 704 (US); Hermon, 11 Aug. 1915, Par- 
ker Phelps 1716 (US). VIRGINIA: Roanche Girl Scout 
Camp, West Virginia, 10 Aug. 1946, Wood 6588 (US). 


Symphytum asperum Lepechin in Nova Acta 
Acad. Sci. Imp. Petrop. Hist. Acad. 14: 442. 
plate. 1850. TYPE: a specimen grown in the 
Botanical Garden of the Academy of Sci- 
ences in St. Petersburg (Leningrad). The seeds 
originated from the Caucasus (LE). 


S. orientale L., Sp. Pl. 136. 1753, pro parte excl. typ. 
5. asperrimum Donn ex Sims, in Bot. Мар. 24: 1. 929. 
1806 


S. echinatum Ledebour, Index Sem. Hort. Dorpat. 
Suppl. 5. 1811. 
S. patens Fries, Novit. Fl. Suec. Mant. 2: 13. 1839, pro 


5. majus Guldenst. ex Ledebour, Fl. Ross. 3: 115. 1847. 


Stem to 200 cm, never winged, very scabrid 
with aculeate curved subretrorse hairs; the hairs 
with a tubercular base; basal leaves ovate-ellip- 
tic, with an acuminate apex and a rounded cor- 
date base; lamina 15-19 cm long, 7-12 cm wide; 
petiole to 10 cm long; stem leaves gradually 
smaller, 10-20 cm long, 4-10 cm wide, ovate or 
elliptic, acuminate at the apex and cuneate at the 
base; leaves not decurrent; adaxial side of the 
leaf very scabrid with short more or less ap- 
pressed hairs with a small tubercular base and 
smaller shorter hairs without a tubercular base; 
abaxial side of the leaves with shorter uncinate 

irs and with setae on the veins; calyx to 3 mm 
long, divided to % of its length, calyx lobes linear 
oblong and obtuse in flower, becoming triangular 
in fruit; stiff marginal setae irregularly distrib- 
uted; setae with a small tubercular base; corolla 
campanulate, 9-14 mm long, red in bud, sky- 
blue in flower; stamens 4-5 mm long; corolla 
scales shorter than the stamens; anther longer 
than filament, connective not projecting beyond 
the thecae; squamae of the corolla lingulate, 6 
mm long, 1 mm wide, with a broad rotundate 
apex; marginal papillae fewer in number, longer 
and narrower than in all cytotypes of S. officinale; 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vou. 71 


papillae acute, regularly distributed along the 
margin; fruit brown and dull, urceolate-granu- 
late, 3-4 mm long and 3 mm wide at the base; 
reproduction strictly allogamous, plants self-in- 
compatible. The production ofripe nutlets varies 
considerably in different plants, even fertile plants 
may have many flowers which produce only 1, 
2 or 3 (and often O) nutlets which are able to 
germinate. 


Specimens examined. CANADA. QUEBEC: Cap Rouge, 
10 Aug. 1931, Michel 362 (MT). U.S.A. MASSA- 
CHUSETTs: Ashland, 6 July 1880, Morong 365 (US); 
Sherborn, 9 June 1918, Loomis 1853 (US). 


Symphytum x uplandicum Nyman, Syll. Fl. Eur. 
80. 1854—1855. TYPE: not seen. 


S. patens Fries, Novit. Fl. Suec. Mant. 2: 13. 1839, pro 


parte. 
S. orientale Fries non L., Novit. Fl. Suec. Mant. 3: 18. 
1842. 


S. x uplandicum Nyman (27 = 36). 


Stem to 130 cm long, not decurrent, rough to 
the touch, provided with scabrous hairs that are 
deciduous in older stems; scabrous hairs with a 
tubercular base; basal leaves elliptic-lanceolate 
with an acuminate apex and a rounded more ог 
less cordate base; lamina of basal leaves 15-30 
cm long and to 6 cm wide, petiole to 12 cm long; 
stem leaves smaller, often with winged petiole, 
the uppermost ones nearly sessile with a cuneate 
base; indument of the adaxial side of the leaves 
sometimes as in S. officinale (2n = 40), some- 
times as in S. x uplandicum (2n = 40), 9.У- 
abaxial side of the leaves with some tubercular 
based hairs along the veins and otherwise gla- 
brous; length of the calyx up to 5.5 mm, calyx 
divided to % of its length, triangular-lanceolate 
and obtuse at the apex; calyx lobes with stiff 
marginal setae with a regular distribution pat- 
tern; setae usually without a tubercular base; 00" 
rolla slightly campanulate 13-16 mm, purple 1" 
bud, blue-purple in flower; squamae of the co- 
rolla 7-7.5 mm long, 2 mm wide at the base. 
triangular-lanceolate, apex broad and rotundate: 
papillae acute and densely crowded at the middle 
of the scale margin; stamens 5-6 mm, shorter 
than the scales; anthers longer than the filaments 
connective not projecting beyond the thecae; fruit 
brown and dull, areolate-granulate, 3-4 mm long 
and to 3 mm wide at the base; reproduction 
strictly allogamous, plants self-incompatible. 
Most plants show a reduced fertility, but $01 
are as fertile as the parental species (q.v. 


1984] 
No m 
2 
22 
Ж 
2, 
2, 


22, 
2 
22, 
2 
22 
22 
22, 
22 
2 
2 
22 
22, 
22, 
22, 
22, 
2 
2, 


S. officinale 2 
2 


== 
== 
= 


(white) 
2n - 24 


= 


I 
MT 
= 
== 
== 
== 
== 
== 
== 


= 
== 
I 
== 
== 
== 
IT 
== 
= 
== 
= 
== 
== 
== 
I 
I 
== 
I 
== 
IL 
IL 
== 
== 
= 
I 
IL 
== 
== 
== 
== 
== 
== 
= 
== 
== 
== 
== 
== 
== 
I 
== 
I 
== 
I 
== 
Кус] 
MIT 
== 
— 


FIGURE 1. 
and calyx as well as the chromo 
S. x uplandicum hybrids are indicated. 


pecimens piis CANADA. BRITISH COLUMBIA: 
ада 3 Jun man 


Mauger 9 (MT). PRINCE EDWARD ISLAND: Springvale, 
hear Milton, з, е 1952, Erskine 1223 (МТ). г 
етіп St. d., Desmarais 647 (MT); Laprairi 
; Montreal Sher. 
TF 


У; п. (US). w. GTON: 
Used Islands, 25 Ae 1917. "Zeller & Zeller 1230 


S. x uplandicum Nyman (2n = 40). 


ficinale (2n = 40); leaf decurrence sometimes 
Present, but usually not longer than 1 cm along 
the in ternode; shape and size of leaves as in S. х 
uplandicum (2n = 36), q.v.; adaxial side of the 

ves with many apod setae, the majority 


GADELLA — SYMPHYTUM 


1065 


S.x uplandicum 


Crossing relationships in the Symphytum officinale/S. asperum complex. The shape of the — 
osome number of the three cytotypes of S. officinale, S. asperum, and the 


44 2.1 


of which h base; these setae 
are not deciduous; indumentum of the abaxial 
side of the leaf as in S. x uplandicum 2n = 36 
(q.v.); calyx to 4 mm long, divided to % of its 
length; Ede diis te qiiem and sub- 
-acute or acute; stiff m setae irregularly 
са. ie а. mm long, slightly 
campanulate, pink or pinkish blue in flower; 
squamae of the corolla with acute papillae, reg- 
ularly distributed along the scale margin; sta- 
mens as in S. x uplandicum 2n = 36 (q.v.); fruit 
as in S. x uplandicum 2n = 36 (q.v.); reproduc- 
tion strictly allogamous, plants self-incompati- 
ble; many plants show a reduced fertility and 
produce only a few nutlets; sometimes plants as 
fertile as the parental species (q.v.). 


Specimens examined. =: QUEBEC: Compte 
l'Assomption, 13 June 1936, 


532 (MT); Petit Saguenay, 30 June 19 
torin 9607 (US, MT); Pointe Preston, 21 July 1933 
Michel 2292 (MT); Montreal, Pointe-aux-Trembles, 


1066 


21 ар 1943, Marie Victorin & Rolland-Germain s.n. 
(MT, US). U.S.A. CONNECTICUT: Bridgepost, 3 Aug. 


1893, Eamesson s. n. (US). MICHIGAN: Emmet and Che- 


(US). 
high Co., 23 May 1964, Schaeffer 70187 (US). 


All North American plants of the genus Sym- 
phytum that I have seen can be identified with 
the aid of this key. The crossing relationships 
between S. officinale and 5. asperum are illus- 
trated in Figure 1. 


DISCUSSION 


Judging from this limited but probably rep- 
resentative sample of herbarium sheets, it ap- 
pears that S. officinale and the two S. x uplan- 
dicum hybrids are the most common taxa in 
North America. The two cytotypes of S. x 
uplandicum (2n = 36 and 2n = 40) are present 
in almost equal proportions. Symphytum aspe- 
rum seems to be much rarer in North America. 
Macbride (1916), who checked up the determi- 
nations of the genus Symphytum in the Gray 
Herbarium, cited 14 specimens from Canada and 
U.S.A. Two specimens came from Vermont, 
Townshend (collected by евр and from 

у Loomis), 
respectively. Both specimens were = by 
him to S. asperum Lepechin. I consulted two 
specimens, preserved in the herbaria of MT and 
US, from the same localities. The material col- 
lected in Vermont rit to S. x uplandicum 
(2n = 40), the material fr to S. 
asperum. This shows и со. of S. aspe- 
rum, and S. x uplandicum, even after a careful 
inspection, may occur. Symphytum peregrinum 
was not among the specimens I examined from 
North America. At least two cytotypes (25 = 48 
and probably 2n — 24; 2n — 40) of S. officinale 
are present. The 2n = 40 cytotype of S. officinale 
will not be assigned to S. tanaicense Steven in 
this pa because experimental studies that 
might €— definite conclusions i in this respect 


are lackin 


name for © uliginosum Kern., a name Бика 15 
used by Fernald (1950) in Gray’s “Manual of 
Botany.” The 2л = 40 cytotype does occur in 
North America, but further conclusions on the 
status of this taxon can only be reached after 
experimental studies and a careful comparison 
of all the relevant material. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


LITERATURE CITED 


ABRAMS, L. 1951. Illustrated Flora of the Pacific States. 
Stanford Univ. Press, Stanford. 

DEGEN, A. voN. 1930. Bemerkungen über einige or- 
ientalische Pflanzenarten LXXXIX. Über Sym- 
phytum uliginosum Kern. Magyar Bot. Lapok 29: 


FARNSWORTH, N. R. 1979. The present and future of 

cognosy. Newslett. Amer. Soc. Pharma- 
cogn. 16: 4-1 " 

FERNALD, M. L. 1950. Gray's €: of Botany. 

1972. са фанове and hybridiza- 

tion тиче in Wr genus Symphytum. Symp. Biol. 

Hung. 12: 199. 

& E. E 1973. Cytotaxonomic studies 

in the genus Symphytum V. Some notes on W. 

European plants with the ome number 

2n = 40. Bot. Jahrb. Syst. 93: 530- 

ае studies in 

the genus Symphytum VIII. Chromosome num- 

bers and САМ со of ten European species. 


Proc. Kon. pee Wetensch., Ser. C, Biol. 
Med. Sci. а pe 
GLEASON, Н. А. 1968. 24 New Britton and Brown 


Illustrated Flora of the Northeastern United States 
and Adjacent Canada, Volume 3. Hafner Publ. 


Со. York. 

Нии, Н, J. 1976. Comfrey: Present and Future. Fa- 
Faber, London. 

ыа C. L., A. CRoNQUIST, M. Ownsey & J. №. 
THOMPSON. 1959. Vascular Plants of the Pacific 
Northwest. IV. Univ. Washington Press, Seattle. 
HuiziNG, H. LW. J. GADELLA & E. Kur HUM. 1982. 
Ch th mphy- 
tum officinale polyploid complex and 5. S. asperum 
st 


Evol. 140: 279-292. 
INGRAM, J. 1961. Studies in the cultivated Boragi- 
naceae 5. Symphytum. Baileya 9: 92-99. 
Jepson, W. L. 1925. Manual of the Flowering Plants 
of California. Associated Students Store, Univ. of 
keley. 


ifornia, Berk 
Kusnetsov, N. 1910. Peters species of the genus 
acts (Tourn.) L. M cad. Imp. Sci. St.- 


urg, Ser. 8, Phys. е 25: 1-94. [In Rus- 


> 
MACBRIDE, F. F. 1916. The correct name of an in- 

troduced Symphytum. Rhodora 18: 23-25. 
Munz, P. А. & D. D. KECK. 1959. A California Flora. 

Univ. of California Press, Berkeley and Los An- 


les. 
Rickett, Н. W. 1966. Wild Flowers of the United 
reta Volume I. McGraw Hill Boo 


; n: Wild Flowers of the United States. The 
Northwestern States, Volume 2. McG Hill Book 


Co., New York. 
RYDBERG, P. A. 1954. Flora of the Rocky Mountains 
and Adjacent Plains. Hafner Publ. Co., New York. 
AN, H. T. T. 1979. The Flora of Canada IV. 
National etia of Natural Sciences, Publica- 
tions in Botany, 7. Ottawa, Canada. 


m" m 


1984] GADELLA — SYMPHYTUM 1067 


Soo, R. DE. 1926. Diagnoses plantarum novarum et Тотш,Т. Es 1956. Thegenus Symphytum in Britain. 


Repert Watsonia 3: 280—281. 
Spec. Nov d s Veg. 27: 316-322. WADE, А Е. 1958. The history of en d as- 
poem ТА 63. Flora of Missouri. Iowa perum Lepech. and S. x uplandicum Nym. 
State Univ. Press, Ames. Britain. Watsonia 4: 117-118. 


TWO NEW SPECIES OF PASSIFLORA (PASSIFLORACEAE) 
FROM PANAMA, WITH COMMENTS ON 
THEIR NATURAL HISTORY! 


SANDRA KNAPP? AND JAMES MALLET? 


ABSTRACT 


ee — улун and P. eueidipabulum are described from middle elevation wet habitats, 

umber of species of Passifloraceae in Panama to 34. Both these species are of uncertain 
affinities in he genus Passiflora. One of the species is a new host plant record for the heliconiine 
butterfly Eueides lineata, and is also found in the peculiar low cloud forest on the Osa Peninsula in 
Costa Rica. The occurrence of new 


sual species in middle elevation Atlantic slope forests and 
sed. 


and 
the urgency of collecting in these forests are briefly discus 


Passiflora macdougaliana S. Knapp & Mallet, sp. 
nov. TYPE: Panama. Colón: along the Río 
uanche about 1 km from the Portobelo 
Highway, 0—50 m, 9°30’N, 79°40’W, 11 Apr. 
1982, Knapp, Mallet & Huft 4587 (holo- 
type, MO; duplicates to be distributed). Fig- 
ures 1 and 3a 
Frutex scandens. Caulis teres glaucus. Stipulae line- 


ares falcatae caducae. Folia alterna ovata insuper nitida 
subter glauca, apicibus acutis retusis, basibus acutis. 


Flores ad nodos s a, bracteis triangularibus spad- 
iceis. Calycis tubus conicu anguste triangu- 
carnosa, apicibus s obtusis, aestivatione quin- 


о с 
cunciali, marginibus expositis glandu 
anguste triangularia alba, apicibus obtusis. Coronae 
filamenta 10-seriata alba, 8 extimis filamentosis cor- 
Tugatis, 2 intimis erectis rigidis brevibus. Operculum 
plicatum. Ovarium ellipticum glabrum nitide viride 
albo maculatum. 


Huge woody canopy liana, young stems round 
and glabrous; new growth erect and glaucous; 
stipules linear, 1.5-2 mm long, falcate, very early 
deciduous. Leaves coriaceous with petioles ca. 
25 mm long, biglandular just beyond the middle; 
the glands raised hemispheres ca. 2 mm wide; 
blades ovate, ca. 135 mm long, 80 mm wide, 
5-veined from the base; apex acute with a tiny 


' We thank Bob Dressler, Dave Roubik, and Во 


AT. 1 mom 


notch, base cuneate; upper leaf surface shining, 
lower surface glaucous with prominent green ve- 
nation, laminar nectaries absent. Flowers soli- 
tary at each node, erect, sweetly fragrant; pedicel 
ca. 45 mm long, joint ca. 25 mm from the base; 
tendrils present on new growth, but early decid- 
uous; floral bracts 3, scattered from the joint to 
10 mm below the joint, deltoid, ca. 1 mm long, 
1 mm wide at the base, pale brown; buds green, 
shining, coriaceous, aestivation quincuncial, with 
5 lenticular glands evenly spaced about the bud 
ca. 5 mm from top of the calyx tube; calyx tube 
ca. 13 mm wide, 5 mm deep; sepals thick and 
fleshy, ca. 30 mm long, 10-15 mm wide, паг- 
rowly triangular, apex obtuse, white adaxially, 
green and shining abaxially; with 5 raised circular 
glands 1 mm diam. on sepal margins outermost 
in bud, 5 mm from sepal base (2 sepals with 2 
glands, 1 with 1 gland, and 2 with no glands), 
petals ca. 35 mm long, 15 mm wide, narrowly 
triangular, apex obtuse, white; coronal rows 10, 
densely packed, grading into one another, all rows 
white fading to cream at base, the outer rows ! 
mm diam. at base tapering to crumpled zigzag 
tips; the outermost 5 coronal rows ca. 35 mm 
long, filamentous; the next 2 rows ca. 7 mm long 


b Schmalzel f d often 
for ту Gilbert r to collecting localities in times of vehicle trouble. ты We ebbe К онеши ео 


deed a first draft of this paper сЕ discussed passifloras. The personnel of the Servicio de dogm 
A. 


Bente Starcke King for the illustrations. 


oam freely in Corcovado National Park on the Osa Peninsula. RE.N 


allowed us qu same freedom to collect in Pan 


NSF grant DEB 79-22192 to W. G.D' Ar 


support 
2 


of the Missouri Botanical Garden and in Costa an Orga- 
„т and a Sigma Xi Grant-in-Aid for pdt The 


pical 
CHEM 42212-80 and NSF grant DEB 79.5601 m б eae гаса а тыф in Costa Rica by National Geographic 


Knapp was supported in Panama by 
Rica by 


L A. Arm Hortorium, Cornell Universit 
i y, Ithaca, New York 14 
? Department of Zoology, University of Texas, Austin, Texas 7871 2 


ANN. MISSOURI Bor. GARD. 71: 1068-1074. 1984. 


e 


5 


1984] 


FIGURE 1. 


followed by a filamentous row ca. 3 mm long; 
innermost 2 coronal rows 2 mm long, stiff and 
upright; operculum plicate, ca. 5 mm long, white, 
the upper surface incurved and covering the li- 
men; floral nectary arising just inside the base of 
the operculum, nectar secreting area а trough ca. 
4mm deep, 2 mm wide, lined with a yellow pad; 
limen red, arising from inner edge of the trough, 
1 mm high, covered by the tip of the operculum; 
androgynophore ca. 7 mm long from base to fil- 
ament origin, white, from above slightly asym- 


KNAPP & MALLET—PASSIFLORA 


Passiflora macdougaliana.—a. Habit.—b. 


1069 


New growth (from Knapp, Mallet & Huft 4587). 


metric; stamens 5, filaments ca. 7 mm long, green, 
anthers ca. 13 mm long, 6 mm wide, greenish 
yellow; style branches 3, ca. 15 mm long, 1 mm 
wide, white; stigmas discoid, revolute, ca. 7 mm 
wide, 5 mm long, creamy green; ovary ellipsoid, 
ca. 7 mm long, 6 mm diam., pale green with 
whitish specks, glabrous and shining. Fruit un- 
own. 


р 4]. 7 |] - 


; ee 
in mature forest. It appears to flower only when 


1070 


at the very tops of trees and therefore is very 
difficult to collect. This species is fairly common 
on Santa Rita Ridge, Colón province, judging 
from the number of individuals encountered as 
fallen leaves and flowers on the forest floor. 

This species has unclear affinities; it possesses 
a hodgepodge of characters of a number of Kil- 
lip’s (1938) subgenera. The glands on the sepals 
suggest P. variolata Poepp. & Endl. in subgenus 
Distephana and P. ernestii Harms in subgenus 
Adenosepala (subgenera sensu Killip, 1938). In 
having a single flower at each node and a many 
ranked corona, P. macdougaliana is similar to 

many species in subgenus Passiflora (incl. Gra- 

nadilla). The hemispherical petiolar glands sug- 
gest subgenus Astrophea or Passiflora. The pli- 
cate operculum is suggestive of subgenus 
Plectostemma or series Kermesinae of subgenus 
Passiflora. One peculiar group of Killip’s sub- 
genus Plectostemma, P. obovata Killip (section 
Mayapathanthus), is quite similar to P. mac- 
dougaliana in its leaf morphology, coriaceous 
buds, erect new growth, and scar-like petiolar 
glands, but differs in having the flowers paired 
at each node and in having fewer coronal rows. 

The species is named in honor of John 
MacDougal of Duke University, a student of 
Passiflora systematics, who has been most kind 
and patient with our many queries about Pas- 
siflora, and who has stimulated our interest in 
this fascinating genus. 


Additional specimens examined. |. PANAMA. COLÓN: 

ta Rita Prin 20 km from the Transisthmian High- 

way, 300—500 m, 9?25'N, 79°37'W, 22 May 1982, 

ub Be РАНЕ 5278 (MO, duplicates to be dis- 
tribute 


Passiflora eueidipabulum S. Knapp & Mallet, sp. 
nov. TYPE: Panama. Colón: Santa Rita Ridge 
Road 7 km from the Transisthmian High- 
way, 200 m, 9?22'N, 79*40"W, 21 May 1982, 
Knapp & Schmalzel 5256 (holotype, MO; 
duplicates to be distributed). Figures 2 and 
3b. 


suffrutescens. Caulis teres glaucus. Stipu- 

ae min лае е setaceae. Folia alterna peltata ovata subter 
glauca, apicibus acutis, basibus obtusis. Pedunculi ir- 
der di Г. 


tri seriata, ex- 
timis complanatis, intimis filiformibus inaequalibus. 
Operculum plicatum a rginem irregulariter fim- 
briatum. Ovarium ellipticum molliter oo 
Semina ferruginea, foveolata, 4-alata 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


Woody vine, about 2 cm thick at base, new 
growth recurved in a gentle acute angle, juvenile 
shoots softly pubescent with unicellular or uni- 
seriate distally glandular trichomes ca. 0.1 mm 
long; stems round, smooth and waxy; stipules 
minute, setaceous; ca. 1 mm long, 0.25 mm wide 
at base, yellowish green or glaucous white. Leaves 
peltate, petiole 45-80 mm long, petiolar glands 
4—6, in 2 or 3 subopposite pairs; blades ovate, 
100-180 mm long, 50-125 mm wide, petiole 
inserted 12-20 mm from basal margin on the 
midrib; base rounded, sometimes slightly cor- 
date, apex acute, apiculate; leaves prominently 
reticulate veined, glabrous above, papillose be- 
neath, long white papillose on the veins, with a 
few scattered unicellular or uniseriate distally 
glandular trichomes on leaves of juvenile shoots, 
laminar nectaries present at junctions of some 
veins below, 10—15. Flowers borne in pairs on 
the tendrils, 15—30 (or more) mm from the base; 
pedicels ca. 52 mm long, joint 42 mm from base; 
floral bracts 3, scattered above and below the 
joint; if above larger, lanceolate, to 15 mm long 
and 5 mm wide, apex blunt; buds soft white pu- 
berulent; еч sweetly fragrant; calyx tube са. 
15 mm , 2 mm deep, convex at point of 
pedicel ыйы sepals white with a green cen- 
tral stripe abaxially, ca. 25 mm long, 16 mm wide 
at base, broadly triangular, apex obtuse; petals 
white, very thin and delicate, ca. 25 mm long, 
15 mm wide at base, broadly triangular, apex 
obtuse; margins of petals undulate and nearly 
transparent; coronal rows 3, outer row ca. 15 mm 
long, linear and laterally compressed, basal 5 mm 
mottled olive green and maroon, terminal 10 
mm bright lemon yellow; second coronal row 4- 
5 mm long, grading into the third, mottled olive 
green and maroon, clavate, the clubs bristly; third 
(inner) coronal row 2—3 mm long, clavate, the 
clubs bristly, mottled olive green and maroon; 
operculum also mottled olive green and maroon, 
plicate, 5 mm long, round and covering the li- 
men, semi-circular in cross section; margin of 
operculum irregularly fimbriate and bristly, olive 
green; floral nectary ca. 2 mm wide, 1 mm deep: 
limen deep maroon, recurved, 2 mm long, 1 mm 
wide at base; androgynophore ca. 12 mm from 
base to point of filament origin, pale glaucous 
green; stamens 5, filaments ca. 8 mm long, green, 
anthers ca. 6 mm long, 2 mm wide, pale green. 
pollen bright yellow; style branches 3, puberu- 
lent, ca. 8 mm long, stigmas green, discoid and 
revolute; ovary ellipsoidal, 5 mm long, pale green 
with soft white pubescence. Fruit ovoid, ca. 70 


V 


— 


1984] KNAPP & MALLET— PASSIFLORA 1071 


FiGUnE 2, Passiflora eueidipabulum.—a. Нађи. —b. New growth (from Knapp & Schmalzel 5256). 


mm long, 50 mm wide, light yellow-green. Seeds — irregularly laciniate (fruit and seed description 
792). 


Tusty brown, narrowly elliptic lenticular, alate; from Antonio 1 
body of seed ca. 10 mm long, 3.5 mm wide, 
minutely pitted; wings 4, a pair on each of the Passiflora eueidipabulum is vegetatively very 
| long axes, ca. 5 mm long, each pair ca. 2 mm distinctive. The large peltate leaves, minute stip- 
“Part on narrow edge of seed, striate, margins ules, and tendril-bearing peduncles make this 


1072 


; ОА ШШ: (i SUSE 

Sa YS QS MO Су 
fr NAX A ZQAW) 2 (E WIR 
‹ LF YOR GIS Sts S CON [ (SESS W Р 
е ES SE eps SSK 


1 


"i (7 


= 


5 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


[0 mm 


—— EET E 
SS 


Dub 


> 
| ж 
7 EEE 
» نيج‎ m 
ор = м 
27 p: 3 
a " 
و‎ Ы у 
— E- 
Р T 
А, 
3 


b 


FIGURE 3.—a. Cross section of the flower of Passiflora macdougaliana (from Knapp, Mallet & Huft 4587). 
b. Cross section of the flower of Passiflora eueidipabulum (from Knapp & Schmalzel 5256). 


species immediately recognizable in the field. 
Only one other Panamanian Passiflora species, 
P. gracillima Killip (incorrectly equated with P. 
tryphostemmatoides Harms in Woodson & 
Schery, 1958), has flowers always borne on the 
tendrils. Passiflora eueidipabulum is easily dis- 
tinguished from P. gracillima by its much larger 
flowers, larger peltate leaves, plicate operculum, 
and prominent petiolar glands. Passiflora euei- 
dipabulum morphologically resembles P. dei- 
damioides a rare species from south- 
eastern Brazil. The two species both have plicate 
opercula and flowers borne on the tendrils, but 
their leaf morphologies are quite distinct (see 
Killip, 1938 for description). The relationships 
of P idipabul itin thes 


UIL. 


We therefore hesitate to assign this species tO 
one of Killip’s subgenera until character com- 
binations and relationships in the genus are саге- 
fully re-analyzed. 

Passiflora eueidipabulum is very closely relat- 
ed to another new species from lowland forest 
in Veracruz province, Mexico (to be described 
by L. E. Gilbert of the University of Texas, Aus- 
tin, in prep.). These two taxa are remarkably 
similar, but differ in certain key features. The 
leaves of the Mexican species are not peltate, and 
do not have the pronounced glaucous cast of 
those of P. eueidipabulum. The flower buds of 
the Mexican species are completely glabrous, 
while those of P. eueidipabulum are soft white 
puberulent. The flowers of P. eueidipabulum are 


| 


1984] 


shallower and more flattened in aspect, а feature 
not readily apparent on the herbarium sheet, but 
quite obvious in live specimens. The Mexican 
species has a peculiar juvenile morphology (Gil- 
bert, in prep.), which is lacking in P. eueidipa- 
bulum. The winged seeds are an unusual and 
distinctive feature of both species. 

assiflora eueidipabulum is the species pre- 
dicted by Mallet and Longino (1982) to occur in 
southern Central America. This prediction was 
made on the basis of the distribution of a but- 
terfly species, Eueides lineata Salvin & Godman, 
whose host plant was found to be the above men- 
tioned Mexican Passiflora (Mallet & Longino, 
1982). In lower Central America, E. lineata was 
present in three of the five areas where P. euei- 
dipabulum was seen: in the low cloud forest on 
the Osa Peninsula (Costa Rica), at Rio Blanco 
del Norte (Coclé, Panama), and on the slopes of 
the Santa Rita Ridge (Colón, Panama). On the 
Osa Peninsula we found eggs ofa Eueides species 
on the leaves, but were unable to rear these to 
adulthood. In Coclé province, all stages of E. 
lineata were found in abundance on the old and 
new growth of P. eueidipabulum. It is satisfying 
to report that the solution to a puzzle in butterfly 
biology has led to a botanical discovery. 

This elusive species is named in honor of the 
butterfly, Eueides lineata, which led us to the 
plant. The larvae of E. lineata feed on the leaves 
of P. eueidipabulum (eueides—after the butter- 
fly, meaning beautiful; and pabulum — fodder). 

Two ofthe following additional specimens are 
both sterile, but we are certain the ey represent 
individuals of P. eueidipabulum; the leaf mor- 
phology is unmistakable. We have also seen, but 
not collected, sterile individuals of this species 
in another locality in Panama and in one locality 
in Costa Rica. The species was discovered in the 
peculiar low cloud forest on the Osa Peninsula 
of Costa Rica (8°30’N, 83°27’ W) by Mr. J. Lon- 
gino in 1980. Passiflora eueidipabulum also oc- 
curs along the Rio Guanche (9°30’N, 79°40’W) 
in Colón province on the Atlantic coast of Pan- 
ama. We have seen this Passiflora only in de- 
graded forest and second growth. The large size 
Of the type specimen is perhaps indicative of its 
Canopy position in undisturbed forest. 


Additional specimens examined. PANAMA. COCLE: 
a above El Copé, 1,000 m, 8°40’N, 80°36’W, 13 
е bs Knapp & Ens 3440 eri: ae iu 


om Transis 


KNAPP & MALLET—PASSIFLORA 


1073 


eg 800-900 ft., 13 Sept. 1979, Antonio 1792 
(MO) (in fruit). 


Both of the new species described here owe 


niine butterflies (Gilbert, 1975; Benson 
1976). There are 34 described species of Passi- 
floraceae from Panama (Woodson & Schery, 
1958; Gentry, 1975), but we have found at least 
another eight species there. In some cases we 
have encountered only sterile plants, and in many 
cases the material may represent range exten- 
sions of South American species. Ecologists and 
zoologists working in the t d take spe- 
cial caution when identifying plants important 
to their work. Even in areas and countries well 
collected by general collectors (e.g., Panama), 
many species remain to be discovered. Those 
unfamiliar with plant ene анти may tend to 


bee 
pointed out by Gilbert (1982). Sterile material 


in MS онаш 
ly as useful as flowering material, and is usually 
identifiable by someone familiar with the group 
in the study area. Regional or complete keys to 
sterile material would be of great use to ecologists 
or others who use systematic botany as a tool. 
Both P. macdougaliana and P. eueidipabulum 
are found in very wet habitats and in low cloud 
forests, which generally occur on ridges below 
1,000 m that are often covered in clouds and 
mist. In both Central and South America Gentry 
(1976, 1978, 1982) has shown that the wetter the 
region, the richer it is in both plant species and 


in endemic and unusual species (Gentry, 1982). 
In Panama and Costa Rica wet forests are located 
all along the Atlantic slope, and in Costa Rica 
the isolated Pacific slope Osa Peninsula also re- 
ceives high rainfall. The mid elevation ridges of 
these areas usually do not have a pronounced 
dry season and are similar to low cloud forest 
areas such as Santa Rita Ridge and Cerro Jefe. 
The endemic flora (Lewis, 1971) of low cloud 
forest areas in Panama is probably not RRON 
ка any given summit or ridge, but is instead sca 

red throughout lower Central America in sim- 
"us habitats. Passiflora eueidipabulum and Pas- 
siflora macdougaliana are both found in one such 
*endemic" area, Santa Rita Ridge, but also occur 


1074 


on the lower Atlantic slopes of this ridge. The 
isolated mountain ridges of the central Osa Pen- 
insula merit distinction as a westward extension 
of ne low cloud forest habitat. This area has been 

poorly f Knapp and 
Mallet at CR and BH), but we suspect it will 
have floristic affinities with the Atlantic slope of 
Panama. The forest is physiognomically similar 
to that on the Santa Rita Ridge. That new and 
unusual species are being found in these mid 
elevation wet forests emphasizes the i importance 
of collecting in less accessible habitats. These 
interesting habitats should be visited repeatedly 
with an emphasis on the collection of unusual 
taxa, particularly seasonal bloomers and high 
canopy plants. Passiflora macdougaliana, for ex- 
ample, was found in an extremely popular col- 
lecting area in north central Panama. This mor re 
thorough collecting approach will undoubtedly 
result in range extensions of *endemic" taxa and 
additions to a rich and already relatively well 
known flora. 


LITERATURE CITED 


BENSON, W. W., K. S. BROWN, JR. & L. E. GILBERT. 
1976. C oevolution of plants and herbivores: pas- 
sion flower butterflies. Evolution 29: 659—680. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


GENTRY, A. Н. 1975. Additional Panamanian Pas- 
sifloraceae. Ann. Missouri Bot. Gard. 63: 341- 
345 


. 1976. Bignoniaceae of southern Central 
America: distribution and ecological specificity. 
Biotropica 8: 117-131. 

1978. Floristic knowledge and needs i Е Ра- 
cific Tropical America. Brittonia 30: 134-153. 

——. 1982. debates patterns as evidence 
for a Chocó refuge. Pp. 112-136 in G. T 
(editor), Biological Dau d. in the Tropics. 

olumbia Univ. Press, New York. 

GiLBERT, L. E. 1975. Ecological consequences of a 
coevolved mutualism between butterflies and 
plants. Pp. 210—240 in L. E. Gilbert & P. H. Raven 
er ad VM о of Animals and Plants. 

of Texa: , Aus 

982. увереним соме two free: species: 

ung. New York 


1938. The American species of Passi- 
floraceae. Publ. Field Mus. Nat. Hist., Bot. Ser. 
19: 3-613. 


Lewis, W. Н. 1971. High floristic endemism in low 
cloud forests of Panama. Био са 3: 76—80. 

MAE J. L. B. & J. T. Loncino. 1982. Hostplant 

ecords and descriptions ofj juvenile stages for two 

pecies of Eueides (Nymphalidae). J. Lep. 


1958. Passi- 
" Ann. Missouri 


.& R. W. 5СНЕКУ, Jn. 
floraceae. In *Flora of Panama 
Bot. Gard. 45: 1-25. 


и a a aaa a ae T 


NEW SPECIES AND COMBINATIONS IN APOCYNACEAE 
FROM PERU AND ADJACENT AMAZONIA! 


ALWYN Н. GENTRY? 


ABSTRACT 


Among recent peo from Peru and adjacent regions are the six new species 


described here. A n 
Mandevilla velutina. The e gen 


of Apocynaceae 


e ation is also Proposed for the widespread учет previously known as 


ru and the very unusual 


fruits of Allamanda ‘chimes described for the first time. 


Aspidosperma tambopatense A. Gentry, sp. nov. 
TYPE: Peru. Madre de Dios: Tambopata Re- 
serve, 26 km S of Puerto Maldonado on E 
side of Río Tambopata, 12?49'S, 69°17’W, 
280 m, subtropical moist forest life zone, 12 
Nov. 1979, G. Hartshorn 2421 (holotype, 
MO); isotypes, CR, F, USM) 


Arbor grandis. Lamina folii elliptica vel — ob- 
ovata, cuneata, obtusa, discoloria. Inflorescentia m 
tum m ramosa, ex Parte glabriuscula, pedicellis perder 
tibus, flo cutis, corolla 
tubulosa, sericea, ad tubi apicem савета 


Canopy tree to 30 m tall, producing white la- 
tex, the branchlets irregularly angled, more or 
less whitish lenticellate when young, glabrous or 

abrate. Leaves alternate, the blade elliptic to 
narrowly obovate, cuneate at base, obtuse to sub- 
acutish at apex, 5-16 cm long, 2-7 cm wide, 
chartaceous, glabrous or with a few scattered tri- 
Chomes near base of midvein, discolorous with 
the densely and minutely glandular-papillate un- 
ке strikingly paler; petiole slender, dark- 

ryi 


Spicuously and glabrescently о puberu- 
ous, н tric omes тоге соп centrated on the 
disti whitish, the 
five P lobes ovate, acute, 1-1.5 mm long; 
corolla tubular, densely whitish sericeous, slight- 
ly constricted at apex of tube, the round lobes 
Somewhat reflexed, 1 mm long, the tube 3-4 mm 
long, to 2 mm wide at broadest point; stamens 
inserted near middle of tube, the anther thecae 
slightly divergent, ca. 1 mm long, the connective 


Op RE 


acuminately extended; ; Ovary conical, | mm long 
an 


ridge, conspicuously whitish lenticellate. 
Distribution. Moist forests on relatively good 
soils along the base of the Andes, 280-400 m 
altitude. 
Additional collections examined, A on Manes DE 


r. 1980, 
ey EE 


DIOS: T 
P. Barbour 4985 (MO). SAN MARTIN: Mari 
Ramal de Aspuzana, Uchiza, 390-400 m, 16 July 1973, 
aig aed 6306 iin Mo, USM, to be d d). LORE- 

5 b uíz, R bank of Río Marañon op- 
koet age of Rio y Байар, 300-450 т, 2 Nov. 
1962, udo 2525 (MO). 


This species belongs to Woodson's (1951) se- 
ries Pyricolla on account of its small corolla with 
a constricted tube apex and ebracteate inflores- 
cence. It keys to A. parvifolium in Woodson's 
key because of its extremely short round corolla 
lobes less than one-quarter the tube length and 
the reddish inflorescence tomentum. Aspido- 
sperma parvifolium, presumably the closest rel- 
ative of A. tambopatense, is restricted to coastal 
Brazil (Bahia to Sao Paulo) and differs i in having 

тацпст bescent 
мей. a much denser and less iod in- 
florescence tomentum, and especially a reddish 
tomentellous corolla tube, the latter very differ- 
ent from the whitish sericeous corolla tube of A. 
tambopatense. Aspidosperma e is 
also very similar to A. vargasii, the only membe 
of series Pyricolla with which it is cidit and 
the Wurdack collection was identified as A. var- 


' Supported by NSF grant DEB-8006253 and AID grant DAN-5542-G-SS-1086-00. I thank Drs. A. Leeu- 


Wenberg, J. 


Zarucchi, and M. Fallen for providing information and/or reviewing various parts of this paper. 


? Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166. 


ANN. Missouri Bor. GARD. 71: 1075-1081. 1984. 


1076 


gasii by Woodson. It differs from A. vargasii in 
having a much more open inflorescence with a 
largely glabrescent tomentum (the inflorescence 
branches thus appearing blackish), mostly com- 
posed of reddish rather than grayish yellow tri- 
chomes. The calyces or A. тершен “ к 
atively Spar 

The leaves of A. vargasii are much more con: 
centrated near the branchlet tips than in A. tam- 
bopatense. The fruit described for A. tambopa- 
tense is a detached one picked up from the forest 
floor but comes from the type locality and is not 
referable to any other Peruvian Aspidosperma; 
this fruit is larger than that of A. vargasii (4—5 
cm by 2.5-3 cm) and has much thicker valves 
although its general form is similar. Apparently 
А. vargasii occurs in drier habitats than does A. 
tambopatense and in Peru appears to bloom pre- 
cociously whereas A. tambopatense blooms with 
the mature leaves. 

Aspidosperma provides an excellent example 
of the inadequacy of the coverage of Amazonian 
plants in the “Flora of Peru.” In Macbride’s 
(1959) “Flora of Peru" treatment, only three 
species of Aspidosperma were reported to occur 
in Peru, although several other species that might 
be expected were also noted in the Flora. Twelve 
additional species of Aspidosperma are now 
known from Peru, quintupling the number of 
species reported in the Flora. Besides 4. tam- 
bopatense, the additional Peruvian species are: 


A. australe Muell.-Arg. [Cajamarca, Mandan- 
guia (Woytkowski 6817 (МО)).] 

. capitatum L. Wms. [Huanuco, Rupa-Rupa 
(Gutierrez 95, fide Fieldiana, Bot. 31: 249. 
1967).] 


m. 


m. 


. cruentum Woods. [Loreto, Río Itaya (Revilla 
2367 (MO)); see Gentry, 1974, for correct 
use of this name.] 

. cylindrocarpon Muell.-Arg. [Huanuco, Pachi- 
tea, fide L. Williams, Fieldiana, Bot. 31: 18. 
1964; Junin, Río Colorado, 500-600 m 
(Gentry et al. 40109 (MO)).] 

. excelsum Benth. [San Martin, Tocache Nuevo 
(Schunke 10019 (MO)); Loreto, Mishana 
(Gentry & Aronson 25313 (MO), Gentry et 
al. 31693 (MO)).] 

A. macrocarpon Mart. [Loreto, Distrito Calleria, 
fide L. Williams, Fieldiana, Bot. 31: 18. 
1964; San Martin, Tocache Nuevo (Gentry 
et al. 25538 (MO); Schunke 8673 (MO)).] 

. marcgravianum Woods. [Huanuco, Codo de 
Pozuzo, 450 m (Foster 9274 (MO)); Madre 


~ 


m. 


~ 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


de Dios, 20 km W of Puerto Maldonado 
(Gentry et al. 19721 (MO)).] 

A. megaphyllum Woods. [Madre de Dios, Manu 
Park (Gentry et al. 26949 (MO)).] 

A. nitidum Benth. [Loreto, Mishana (Gentry et 
al. 25323, 25355, 25364, 36500 (all MO)), 
Laguna de Yarana, Río Nanay (Diaz et al. 
447 (MO), Río Tacsha Curaray (Croat 
20413 (MO)); a common species of season- 
ally inundated tahuampa forests, occasion- 
ally also on upland white sand, especially in 
poorly drained areas. Some of this material 
has been identified as A. marcgravianum but 
the Loreto collections have the leaf-op- 
posed, rather than terminal, inflorescences 
and larger less acuminate leaves of A. nitid- 
um and are clearly not conspecific with the 
specimens cited above as A. marcgravianum 
despite the very similar small verrucose 


fruits. 

A. schultesii Woods. [Loreto, Mishana (Gentry 
et al. 25312, 26169 (both MO)).] 

A. cf. verruculosum Muell.-Arg. [Loreto, Misha- 
na (Gentry et al. 25219, 25272, 26084 (all 
MO)); sympatric with and very close to A. 
schultesii but has red latex.] 

A. sp. nov. aff. pichonianum [Loreto, Mishana 
(Gentry et al. 31682, Gentry & Aronson 
25299 (both MO)). Although it is highly 
likely that this species is undescribed, it 
seems best to await the discovery of its flow- 
ers before describing it. The leaves are co- 
riaceous, and narrowly oblong with a round- 


ганыс base, and obscure sec- 
ondary veins. This species is vegetatively 
most similar to A. pichonianum of the 
Guayana Highlands, an unlikely identifica- 
tion on phytogeographic grounds. The fruit 
of the Peruvian plant is flattened and subor- 
bicular, ca. 10 cm by 8 cm, with a minutely 
roughened black-drying surface, very short 
stipe, and no raised midrib; the suborbicular 
seeds are ca. 8 cm diam. Another notewor- 
thy feature is the abundant red latex in the 
younger branches.] 

A. sp. [At least one additional species is repre- 
sented by a sterile transect voucher that 1 
have been unable to match in the herbar- 
ium.] 


Pacouria boliviensis (Mgf.) A. Chev., Rev. Int. 
Bot. Appl. 28: 455. 1948. Landolphia boli- 
viensis Mgf., Notizbl. Bot. Gart. Mus. Berlin 


| 


Па ес не а а а il rede с 


1984] 


9: 1041. 1926. TYPE: Bolivia. Steinbach 6537 
(not seen). 


The few American species generally attributed 


complicated by the fact that the oldest name for 
any member of the group, Pacouria Aublet, has 
been rejected against Landolphia. Pacouria gui- 
anensis, described from French Guiana (Aublet, 
1775), was not re-collected for well over a cen- 
tury, leading Bentham (1876) and others to sug- 
gest that Aublet’s plant might have been intro- 
duced from Africa. Monachino (1945) 
summarized the convoluted taxonomic history 
of the rarely-collected American members of this 
group, accepting three species, of which he had 
seen only four collections. 

At the time of Monachino’s summary, the Af- 
rican species of this alliance were usually retained 
in a rather heterogeneous sensu lato Landolphia. 
However, for better or for worse, taxonomic cus- 
tom has changed, and all African authors (e.g., 
“Flora of West Tropical Africa” and the various 
pun of plants or northwest Gabon) now 

accept , with di 
tinctive terminal inflorescences having curved 
lateral branches that apparently serve as “grap- 
pling hook" tendrils, as separate from Landol- 
phia, which has short contracted, mostly axillary 
inflorescences. The Am can species are closest 
to either Ancylobothrys podes 1945: 309) 
or Dictyophleba (because of the non-keeled an- 

ers and glabrous fruit, cf. Pichon, 1953: 39- 
40). While the American species are clearly not 
Very different from either ofthese African genera, 
Pichon (1953) elected to treat them as generically 
distinct under 
acouria 
Students of the Bu (Zarucchi, pers. comm 
Leeuwenberg, pers. comm.). мењана as Pi- 
chon ( 953) Шан remarked, American Ра- 
couria appears to be intermediate between the 
advanced African genera Dictyophleba, Vahade- 
nia, and Ancylobothrys and the — unspe- 

Cialized African genus Landolphia 

All of this becomes relevant to Peu because 
of the discovery of Pacouria boliviensis in Peru 
(Ancuash 339 (MO), Amazonas Dept., Quebrada 

uampi, determined as Landolphia boliviensis 
by Markgraf, Gentry 43294, 43408 (both MO), 
Madre de Dios, Cocha Cashu Biological Station, 
Manu National Park). 


Ф 


МАНИ 
1 


а derici 11 


Geissospermum, а small genus of three species 


GENTRY —АРОСУМАСЕАЕ 


1077 


plus the two additional ones described here, has 
not been reported previously from Peru. It differs 
fom Aspidosperma- in having пре rather 

n lacking slits 
in the corolla tube at the level of e anthers, and 
— in having a à non-compressed е 

or ovoid wingle ou 

rather мнн, seeds. The three “cei species 
are G. laeve (Vell.) Miers from coastal Brazil (G. 


lower Amazonian Brazil (mostly north of the Rio 
Amazonas except in the Xingu region). Accord- 
ing to Markgraf (1978), G. argenteum is a syn- 
onym of G. sericeum, but it is his own G. fuscum 
Mef. that is really conspecific with the type of С. 
sericeum (Sagot 966 (P)). Geissospermum seri- 
ceum Benth. & Hook. occurs from the Río Negro 
region of Venezuela and Brazil north to Surinam 
and east to Amapá. One of the new species de- 
scribed here occurs in southern Amazonian Bra- 
zil from the Tocantins and Tapajos to the Bo- 
livian border in Rondonia. The other is known 
only from an isolated patch of dry forest in Cen- 
tral Amazonian Peru. 


KEY TO THE SPECIES OF GEISSOSPERMUM 


1 Corolla t tube 9-10 mm long, the lobes 4-5 mm 


long and 3 cm 06 coastal 1 Brazil __ 
1. Corolla tube less than 6 
ess than 3 mm ie y; follicles obtuse to apic- 


and 3 cm wide; Amaz onia. 

2. Leaves possadi коренни below with sil- 
very or bro h trichomes, the tertiary 

venation hidden by the pubescence and 

Ama- 


zonia. 

Stem pu e brown, not appressed; 

leaf pubesce етина sericeous; со- 

rolla lobes 2-3 mm long ____ _ G. sericeum 
ubescen ssed 


2 


о 

Hin 
$76 

E 


lo ш G. argenteum 
2; е almost азу жаы кез below, the ter- 


ary 
по Am ог western Amazonia. 
4. Corolla tube 5—6 mm long, enlarged at 


sepa- 
. urceolatum 
Corolla tube Lo mm m long, uniformly 
tubular; inflorescence aay RNE 
calyx lobes fused at base, acute 
G. reticulatum 


^ 


1078 


Geissospermum reticulatum A. Gentry, sp. nov. 
TYPE: Peru. Huanuco: Pachitea, Carretera 
Miel de Abejas, | km arriba de Tournavista, 
Honoria, 300 m, Bosque Nacional de Iparia, 
bosque seco tropical, 29 Dec. 1966, J. 
Schunke 1446 (holotype, MO; isotype, P; 
other duplicates distributed by F as Aspi- 
dosperma aff. polyneuron). 


one клу Folia elliptica vel anguste ovata, cu- 
neata, 


centia lateralis, pedunculata, ramosa 
floribus оне calyce cupulato, 1.5 mm longo, acute 
5-lobato, puberulo, corolla tubulosa, dense sericea. 
Fructus immaturus ovoideus, dense velutinus. 


Tree 14 m tall, producing white latex; branch- 
lets more or less terete, appressed puberulous, 
elenticellate. Leaves alternate, elliptic to narrow- 
ly ovate, long acuminate, cuneate at base, 8-11 
cm long, 3-4.5 cm wide, chartaceous, minutely 
appustécd-puberdious on midvein above and be- 


and VCI whole 
surface below, the venation ойша promi- 
nulous above and below; petiole 4—7 mm long. 
Inflorescence mostly scattered along the branch- 
es, sometimes opposite the leaves, each inflores- 
cence with a well-developed peduncle, often ca. 
1 cm long with се ај main bifurcations, densely 
appressed-puberulous with tannish trichomes; the 
ultimate flower кодни subtended by са. 1 mm 
long appressed tannish-puberulous bracts. Flow- 
ers cream; the calyx cupular, ca. 1.5 mm long, 
the five acute lobes split У; to % of way to base, 
densely appressed tannish puberulous; corolla 
tubular, the round thick lobes reflexed at anthe- 
sis, са. 1 mm long, the tube 3—4 mm long, 1-1.5 
mm wide, densely tannish sericeous; stamens in- 
serted near top of tube, the parallel thecae com- 
pletely fused, ca. 0.6 mm long, the prolonged 
connective acute; ovary ovoid, puberulous, sul- 

cate. Very immature fruits (only 5 mm long) 
ovoid, densely tannish-velutinous. 


low 


Distribution. Known only from the strongly 
seasonal forest of the central Rio Ucayali drain- 
age south of Pucallpa. 


JU 7 


is most closely re- 
lated to G. argenteum, from which it is differ- 
entiated especially by lack of a conspicuously 
sericeous leaf undersurface and the intricately 
prominulous network formed by the leaf vena- 
tion. Although the type collection was identified 
as Aspidosperma aff. polyneuron, and G. reticu- 
latum is superficially somewhat similar to that 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


species and some other Aspidospermas, the 
prominulously intricately reticulate fine leaf ve- 
nation of G. reticulatum is quite unlike the leaf 
venation of any Aspidosperma species at MO. 


Geissospermum urceolatum A. Gentry, sp. nov. 
TYPE: Brazil. Pará: Belterra, 3 Nov. 1957, 
Black 47-1909 [holotype, MO; isotype, P, 
MG (not seen)]. 


Arbor lactifer. Folia elliptica vel ovata, acuminata, 
ad basim obtusa, plerumque glabrata. Inflorescentia 
lateralis, pauciflora, floribus viridibus, calycis lobis se- 
paratis, lanceolatis, corolla tubulo-urceolata, tubi apice 


cons 
lipsoideis ‘tomentosis compositus, seminibus compla- 
natis, exalatis 


Tree to 10 or more m tall, producing white 
latex, the branchlets subterete, distinctly longi- 
tudinally striate-ridged, pu s with short 
subappressed trichomes, elenticellate. Leaves al- 
ternate, the blade elliptic to ovate, acuminate to 
long acuminate, obtuse to broadly cuneate at base, 
4.5-12 cm long, 1.5-5 cm wide, chartaceous, 
mostly glabrescent, minutely appressed-puberu- 
lous only on midvein and very sparsely over low- 
er surface, the venation prominulous above and 
below; petiole 3-8 mm long. Inflorescence lat- 
eral, few-flowered, tannish puberulous with sub- 
appressed trichomes. Flowers greenish, the ca- 
lyx of 5 separate lobes, the lobes lanceolate, 
obtuse, ca. 1.5 mm long, appressed puberulous; 
corolla tubular-urceolate, the base distinctly 
swollen, the neck constricted, the tube 5-6 mm 
long, almost 2 mm wide at base, densely tannish 
puberulous, the trichomes over basal swelling 
not appressed, the lobes 1-1.5 mm long. Fruits 
of 2 ellipsoid follicles, rather densely but gla- 
brescently tannish tomentose, ca. 3 mm long, 
1.5-2 cm wide; seeds flattened, wingless, rather 
angular, 6—9 mm long, ca. 10 mm wide. 


Distribution. Amazonian Brazil south of the 


mazon 


Additional collections examined. aon PARA: 

reu Branco, Estrada de Ferro Tocantins, terra firme 
highland forest, 29 Sept. 1948, ed н 6 (MO). 
RONDONIA: Guajará-Mirim, campina, 17 Dec. 1949, 
N. Silva 338 (MO; two sheets, one with F ccaberebangod 
to “438” with pencil). 


This species resembles G. Јаеуе (G. vellosoi) of 
coastal Brazil in its relatively large flowers an 
few-flowered inflorescences but differs strongly 
from that species in its much smaller corolla lobes 
and urceolate corolla tube. Its leaves are similar 


1984] 


to those of G. reticulatum in lacking an obvious 
sericeous pubescence, but the corolla is larger 
and differently shaped, the inflorescences have 
fewer flowers, and the calyx is split to the base 
and has obtuse rather than acute lobes. 


Mandevilla arcuata A. Gentry, sp. nov. TYPE: 
Peru. Amazonas: Valle del Rio Santiago, 
77°40'W, 3°50’S, Quebrada 2-3 km atras de 
la comunidad de Caterpiza, 200 m, 29 Jan. 
1980, S. Tunqui 674 (holotype, MO; iso- 
type, USM). 

Herba glabra scandens. Folia anguste obovato-ellip- 
tica, acuminata, , margine ciliato excepto 
glabra. Inflorescentia racemosa, axillaris, fere glab 
floribus eburneis, calyce 2 mm longo, lobis subulato- 

ad 


positus, seminibus ad apicem plumosis 


Vine, stems terete, slender, glabrous or with a 
few scattered minute inconspicuous trichomes. 
Leaves opposite, narrowly obovate-elliptic, acu- 
minate, the base narrowly truncate, not at all 
cordate, 5-7 cm long, 1.5-2.5 cm wide, mem- 
branaceous, glabrous except the minutely sub- 
ciliate margin and a 


cence racemose, axillary, virtually glabrous, not 
at all 1-sided, the pedicels 7-8 mm long. Flow- 
ers cream, the calyx 2 mm long, 5-lobed, the 
subulate-acuminate lobes with a few short tri- 
chomes along margins; corolla narrowly tubular- 


tube ca. 1.5 cm long, less than 1 mm wide except 
toward base. Fruit apocarpous, the 2 follicles lin- 
Car, strongly constricted between seeds, glabrous, 
18-20 cm long, ca. 3 mm wide at thickest points; 
seed body narrow, conspicuously longitudinally 
grooved, 1 cm long, with a dense apical tuft of 
1.2-2 ст long brownish trichomes. 


Distribution. Known only from the Ecuador- 
еги border region of northeastern Amazonas 
Department. 


This species belongs in subgenus Exothoste- 
топ because of its strongly arcuate gibbous со- 
Tolla tube. It is most closely related to M. poly- 
атћа К. Schum. ex Woods. based on the unusual 
Corolla shape. Although the cream flower color 
Would key it out with M. polyantha, it does not 


GENTRY —APOCYNACEAE 


1079 


is A An 4 + 


lav used to distinguish 
M. polyantha in Woodson's (1933) key. Never- 
theless, a secund inflorescence, which in any event 
may be partially a pressing artifact, is not uni- 
versal in M. polyantha and that feature thus is 
not a major between M. 
arcuata and M. polyantha. One of the most ob- 
vious differences between these two species is 
that M. arcuata is essentially glabrous almost 
throughout—only a few minute and inconspic- 
uous trichomes are scattered over its stems, in- 


petioles, and inflorescence. Mandevilla arcuata 
has smaller leaves that taper to a narrow, abrupt- 
ly truncate base whereas the leaf of M. polyantha 
narrows to a distinctly cordate base. The flower 
of M. arcuata is apparently somewhat smaller 
than that of M. polyantha. Mandevilla polyantha 
is endemic to the lower Huallaga Valley around 
Yurimaguas but M. arcuata occurs further 
northwest in the Río Santiago Valley near the 
Ecuador border. 

Mandevilla is a large and taxonomically dif- 
ficult genus and it is with some hesitation that I 
propose a new species in it, even such a distinc- 
tive one. Thirty-five new species of Mandevilla 
have been published since Woodson’s mono- 
graph. I have seen no material of a number of 
these but have checked the descriptions of all 
species proposed from Central and western South 
America. None of these species is even remotely 
similar to M. arcuata or M. polyantha. 


Mandevilla pohliana (Stadelm.) A. Gentry, comb. 
nov. Echites pohliana Stadelm., Flora 24(1): 
Beibl. 73. 1841. TYPE: Brazil. Minas Geraes, 
Pohl s.n. (not seen). 

Гурани gentianoides Muell.-Arg. var. glabra Muell.- 

n Mart., Fl. Bras. 6(1): 124, n. 37, fig. 2. 
1860. “Mandevilla velutina (Mart. ‚ Var. 
glabra (Muell.-Arg.) W s. Ann. MO Bot. 
Gard. 20: 732. 1933. (9 adoni synonyms are 


474, Minas Geraes, Waddell s.n. (not seen 
Mandevilla pohliana (Stadelm.) A. Gentry var. 


velutina art. ex Stadelm.) A. Gentry, 
comb. nov. Echites velutina Mart. ex Sta- 


3. 1844. Dipladenia gentianoides 
Muell.-Arg. var. velutina (Mart. ex Sta- 


1080 


delm.) Muell.-Arg. in Mart., Fl. Bras. 6(1): 
124. 1860. Mandevilla velutina (Mart. ex 
Stadelm.) Woods. var. typica Woods., Ann. 
Missouri Bot. Gard. 20: 732. 1933. TYPE: 
Brazil. Sao Paulo, Martius 503 (not seen). 


The plant generally known as Mandevilla ve- 
lutina is one of the commonest and best known 
species of the genus, occurring through most of 

southeastern Brazil, Paraguay, and into Bolivia 
[Cardenas 5500 (MO) from between San Ignacio 
and San Miguel, Santa Cruz Department, is ap- 
parently a first report for Bolivia]. While not yet 
reported from Peru, this is the 08 of distri- 
ttern that might | f the plants 
that will be found in the botanically unexplored 
Pampas de Heath on the Bolivian : 

When Woodson (1933) proposed бе new com- 
bination for this species, he apparently failed to 
realize that the epithet “velutina” was already 
preoccupied in Mandevilla by M. velutina K. 
Schum. (in Engler & Prantl, Nat. Pflanzenfam. 
4(2): 171. 1895), a Costa Rican plant previously 
placed by Woodson in synonymy under Fernal- 
dia pandurata (DC.) Woods. Resurrection of the 
next available name for the plant usually known 
as M. velutina is unavoidable. This plant must 
thus be known as M. pohliana, based on Echites 
pohliana, published concurrently with E. velu- 
tina by Stadelmeyer. However, there are two dis- 
tinctive variants of this plant, a glabrous-leaved 

a pubescent-leaved form, the latter including 
the type of Echites velutina and designated M. 
velutina var. typica by Woodson. The type of 
Echites pohliana belongs to the glabrescent- 
leaved form, usually referred to as variety glabra, 
which thus becomes var. pohliana. Luckily an 
epithet older than Woodson’s "typica" is avail- 
able at varietal rank for the pubescent-leaved 
plant that Mueller-Argoviensis (1860) reduced 
to varietal status as Dipladenia gentianoides var. 
velutina long before Woodson Proposed his va- 
riety typica. Thus the pubescent taxon becomes 
M. pohliana var. velutina (Mart. ex Stadelm.) A. 
Gentry. 


Odontadenia macrostoma A. Gen ntry, sp. nov. 
ТҮРЕ: Peru. Amazonas: Valle del Rio San- 
Паро, 77°40’W, 3°50’S, Quebrada Caterpiza, 
2-3 km atras de la comunidad de Caterpiza, 
200 т, 14 Jan. 1980, 5. Tunqui 602 (ћо- 
lotype, MO; isotype, USM). 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


icis scandens. Folia elliptica, acuminata, basi ob- 
In аараан 


- 
=| 


а кы кана terminalis, floribunda, minut 
puberula, floribus luteis, calycis lobis ovatis, "obtusis, 
5-6 mm longis, puberulis, corolla late infundibulifor- 
mi-campanulata supra tubi partem basalem, dense 
PORUM antheris in tubi parte basali inclusis. Fructus 
ignot 

Liana; stems reddish brown, with conspicuous 
small raised blackish lenticels. Leaves opposite, 
elliptic, acuminate at apex, broadly cuneate to 
obtuse at base, very minutely and sparsely puber- 
ulous along main veins below and base of mid- 
vein above, otherwise glabrous, 9-12 cm long, 
3-4.5 cm wide, chartaceous; petiole 0.8-1 cm 
long; stipules not seen, early caducous, leaving 
an interpetiolar scar. Inflorescence corymbose- 
paniculate, terminal, many-flowered, the 
branches and pedicels minutely puberulous. 
Flowers with the calyx lobes ovate, obtuse, uni- 
formly 5-6 mm long, not at all or barely unequal, 
densely minutely puberulous outside, the squa- 
mellae thin and inconspicuous; corolla точ, 
broadly i b the 
narrow basal tube, the basal tube 1–1.5 ст long, 
2-3 mm across at basal bulge, 1-2 mm across 
above bulge, the upper tube (throat) ca. 2 cm 
long, 1.5-2 cm broad at mouth, minutely papil- 
lose-puberulous outside, especially conspicuous- 
ly so in bud, the anthers included in basal tu 
linear, 5 mm long, with acuminate connective 
and acuminate basal tails; ovary ovoid, densely 
minutely puberulous, 1.5 mm long, са. 1 mm 
wide, surrounded by the annularly accrescent 
nectaries. Fruit unknown. 


It is surprising that not a single new species of 
Odontadenia has been described since Wood- 
son’s (1935) monograph (although an apparently 
unpublished name suggested by Markgraf is rep- 
resented in the MO herbarium). Odontadenia 
macrostoma is closest to O. cognata (Stadelm.) 
Woods., a widespread and variable species, and 
keys out to that species both in the “Нога of 
Peru” and in Woodson’s (1935) monograph be- 
cause of its prominent lenticels, thyrsiform-sub- 
corymbose terminal inflorescence, infundibuli- 
form puberulous corolla, stamens inserted in basal 
part of the tube, acute-based leaves, and 5-6 mm 
long calyx lobes. However, I do not think that 
the broadly infundibuliform campanulate corol- 
la (1.5-2 cm broad at mouth) of O. macrostoma 
can possibly fit into the range of variation of O. 
cognata, the maximum orifice diameter of which 


eS ee ee о - 


ee 


1984] 


is | cm according to Woodson and in the material 
examined by me. The character of “corolla throat 
about 5.5 cm across” given in Macbride’s (195 
438) key is erroneous and presumably a typo- 
graphical error for 0.55 cm. The shape of the O. 
cognata corolla is also very different, with the 
upper part of the tube (throat) much more uni- 
formly tubular as well as narrower and broad- 
ening much more gradually from the narrow bas- 
al tube. In Peru O. cognata has red or red-orange, 
presumably hummingbird-pollinated flowers, 
whereas O. macrostoma has yellow flowers. Al- 
though flower color is too variable in this group 
to be very useful taxonomically — O. cognata has 
uniformly yellow flowers in Panama, coastal Co- 
lombia, and lower Amazonian Brazil —the dif- 
ference in flower color, shape, and size between 
O. macrostoma and O. cognata strongly suggest 
that differentiation of the two taxa involved an 
evolutionary shift between hummingbird and bee 
pollination in Peru. 


Allamanda weberbaueri Mgf., Notizbl. Bot. Gart. 
Berlin 9: 77. 1924 


The fruits ofthis species, endemic to the Balsas 
region of the Marafion Valley, have never been 
described. A recent collection (Dillon & Turner 
1710 (F, MO, USM)) is the first to include the 
distinctive fruits of this plant. Contrary to Mac- 

ride's suggestion that A. weberbaueri might be 
no more than a variant of widespread A. ca- 
thartica L., its fruits are so different from those 
of A. cathartica or any other species of Alla- 
manda as to suggest that generic separation might 
even be warranted. Allamanda weberbaueri has 


GENTRY —APOCYNACEAE 


1081 


brownish-winged seeds of A. weberbaueri, 4—5 
mm long and 4—6 mm wide, are generally similar 
to those of other species of Allamanda. The Pe- 
ruvian plant is | reported as being an erect shrub 
ortree to 5 m tall 

are scandent. The leaves of A. weberbaueri are 
sometimes whorled as in other species of A//a- 
manda but on some branches of the Dillon and 
Turner collection the leaf whorls are very irreg- 
ular or even lacking, the leaves becoming irreg- 
ularly apically clustered. The flowers of the new 
collection are much smaller than those ofthe two 
previous ones but of the same general form; their 
reported white corolla color is probably erro- 
neous (Dillon, pers. comm.). On balance, the evi- 
dence suggests that A. weberbaueri is best con- 
sidered a highly atypical species of A/lamanda. 


LITERATURE CITED 


AUBLET, F. 1775. Histoire des Plantes de la Guiane 

rancoise 1: 268-27 

BENTHAM, G. 1876. Apocynaceae. Ha Bentham & 

J. D. Hooker, Gen. Pl. 2(2): 6 

GENTRY, ЗА fee 1974. Notes on СЕ тапіап Аро 

n. Missouri Bot. Gard. 61: 891—900. 
упасеае. Jn Flora of Peru. 

3-455. 


ovedades de Apocynaceae. 
ta Bot. Venez. d 353-355. 
Morini. J. A. 45. A revision of Macoubea 
and the American species of Landolphia (Apo- 
cynaceae). Lloydia 8: 291—317 


MUELLER-ARGOVIENSIS, J. 1860. Apocynaceae. Inc. 
Martius, Fl. Bras. 6 1-196. 
ти М. 1953. on hie ea 


5 
m. Inst. og Afrique baji 45: 
S HUMANI, K. 1895. Apocynac T Ат сайы & 
К. Prantl, Nat. Pflanzenfam. 402): 1 
1933. Studies in the ae aceae 

. The American genera of Echitoideae. Ann. 
le Bot. Gard. 20: 605-790. 

1935. Studies in the Apocynaceae IV. The 
American genera of Echitoideae. Ann. Missouri 
Bot. Gard. 22: 153-306. 


hace R. E. 


1951. Studies in naceae VIII. An 
иин revision vida the genus caine gens Mart. 
с. Ann. Missouri Bot. Gard. 38: 119-204. 


NEW SPECIES OF GALAXIA (IRIDACEAE) AND NOTES ON 
CYTOLOGY AND EVOLUTION IN THE GENUS! 


PETER GOLDBLATT? 


ABSTRACT 


a kamiesmontana and G. parva are new species, both of subgenus Eurystigma. Galaxia’ 


Galaxi: 
но is restricted to the Kamiesberg 


overlying rock, while G. parva is known only from the Mierkraal flats near Bredasdorp in the 


omosome number is n = 9 in G. kamiesmontana and п = 6 in С. parva. Both numbers аге 
new for the subgenus, in which n = 8, 7, and 17 ата m recorded. The chromosome number in G. 


kamiesmontana us Eurystigma 


to the 


re specialized subgenus Galaxia in which x = 


links subgen 
9 is basic. Chromosome evolution in р reviewed i in the paper, is seen as having proceeded 
base = 9 by aneu ton=8,7 


uploid reducti 


and ultimately 6 by unequal translocation 


and centric loss. Galaxia kamiesmontana is ene a primitive relict species retaining the ancestral 
basic karyotype, while G. parva, an inbreeding, autogamous species with a highly derived karyotype 


is one of the most specialized. 


Galaxia is a small genus of Iridaceae subfamily 
Iridoideae restricted to the winter rainfall area 
of the southwestern coast and interior of south- 
ern Africa. All species of Galaxia are small corm 
bearing plants with a basal rosette of short bi- 
facial leaves and Crocus-like flowers with an un- 
derground ovary and a perianth tube that raises 
the flower well above the ground. The flowers 
are fugaceous, lasting for 3-6 hours, and this, 
together with their small size, makes the plants 
very inconspicuous. As a result, the genus is rel- 
atively poorly collected. In the recent revision of 
the genus (Goldblatt, 1979a) I recognized 12 
species in two subgenera. The two species de- 
scribed here were discovered subsequent to the 
publication of the 1979 revision, G. kamies- 
montana in 1980 and С. parva in 1981. Both are 
clearly very local endemics and in view of the 
high level of knowledge of the Cape Flora, it 
seems unlikely that they occur elsewhere. 


RELATIONSHIPS 


The two new species belong to subgenus Eu- 
rystigma, in which the stigma lobes are entire, 
the filaments typically united below and free for 
some distance above, and the flowers usually 
variously colored. In contrast, in the more spe- 
cialized subgenus Galaxia, the stigma lobes are 
irregularly fringed, the filaments typically entire- 
ly united and the flowers yellow or, rarely, yellow 


and white. Basic chromosome number for the 
genus is probably x = 9 (Goldblatt, 1979a, 
1979b), and x = 9 is the basic number for sub- 
genus Galaxia, in which only multiples of this 
base occur (Table 1). Until now numbers of x = 
8 and 7 only, had been recorded in subgenus 


Eruystigma (Table 1), although I postulated that 
f 


x = 9 probably occurred in the ancestral type 0 
this, the less specialized subgenus. Chromosome 
number has been determined for both new 
species, G. kamiesmontana having 2n = 18 and 
G. parva, 2n = 12. Both numbers are thus new 
for the subgenus and substantially expand the 
impression of Galaxia as a cytologically variable 
genus. My prediction that x = 9 was basic for 
subgenus Eurystigma seems to have been ful- 
filled with the discovery of this number in G. 
kamiesmontana. The karyotypes of the new 
species and the cytological evolution of the genus 
is dealt with in more detail below. 


CYTOLOGY 


Chromosome numbers were established for 
Galaxia kamiesmontana and G. parva using 4 
squash technique described previously (Gold- 
blatt, 1979b). In both species the type collections 
serve as the voucher specimens for the chro- 
mosome counts. 

The karyotype of Galaxia kamiesmontana, 
with 2n = 18, comprises five pairs of larger chro- 


= ! Supported by grants DEB 78- 10655 and DEB 8 1- 19292 from the United States National Science Foundation. 
nbosc 


Botanic Gardens, for their hospitality and help on field trips to South A 


staff of f the rien Herbarium, Kirstenbosch 


* B. A. Krukoff Curator of African Botany, Missouri Botanical Garden, TO: Box 299, St. Louis, Missouri 


63166. 


ANN. MISSOURI Bor. GARD. 71: 1082—1087. 1984. 


— 


TABLE 1. Chromosome numbers in Galaxia. 


The other counts were pre- 
viously reviewed by Goldblatt (1979b). 


Mean 
ngt. 
Haploid 
omo- 
Diploid some Set 
Species Number 
Subgenus Eurystigma 
G. rire Goldbl. 18 39.0 
G. citrina Lewi 16, 14, 34 39.3 
G. Кайн, си 16, 16 38.3 
G. versicolor que ex Klatt 16, 14 40.0 
G. variabilis Le 4 38.9 
G. parva Совы. 12% 42.0 
Subgenus Galaxia 
G. grandiflora Goldbl. 18 — 
G. ciliata Persoon 18 — 
G. luteo-alba Goldbl. 18,27 — 
G. ovata Thunb. 18,36,54* 40.9 
G. stagnalis Goldbl. 36 — 
G. fugacissima (L. f.) Druce 18, 36 — 
G. alata Goldbl 18, 27 — 
G. albiflora Lewis 18 — 
* Voucher Guasi 
G. kamiesm —Cape Province, Rooiberg, Ka- 


miesberg, “Goldblatt 5560 (MO). 


G. barnardii—Cape Province, Caledon, at the west- 
ев end of town, оона 6174 (МО). 
ратуа— Саре Province, Mierkraal flats, SSW of 


Bredasdorp, ( Goldblatt 61814 (МО). 
G. ova e, Mierkraal flats, SSW of 
Bedaio d PM 6928 (MO). 


mosomes, 4—6 um long, and four smaller pairs, 
Ca. 3 um long, all strongly acrocentric or nearly 
зар (Fig. 1B). This karyotype corresponds 
closely to that of G. fugacissima (Fig. 1A), a rep- 
resentative species of subgenus ппен with а 
Otype characteristic of that 
The karyotype of Galaxia parva, ни 2п = 
12, 18 structurally heterozygous. И comprises the 
following: a long pair of metacentrics, ca. 10 um 
long; a mismatched pair ca. 9 um long, one ac- 
госепігіс and one metacentric; another mis- 
matched pair 7-8 um long, also metacentric and 
acrocentric; a fourth pair of acrocentrics ca. 6.5 
ит long; an apparently mismatched fifth pair, 
Опе ca. 5.5 and the other ca. 4 um long; and a 
very small acrocentric pair ca. 3 ит long. This 
karyotype has been confirmed for the five indi- 
Viduals of the species so far examined. 


GOLDBLATT — GALAXIA 


1083 


„ÛÛ ÛJ Û ни 
„Û Û n unu 


cl U DO il (f i 

D | He wa 

nanan da 
A Mant == 


IGURE 1. Karyotypes of species of Galaxia. —A. 


).— 
DG. оа = а E Ait sa = 14).— 
Е. С. parva (2n = 12) (species В-Е all subgenus Eu- 
rystigma). 


Structural heterozygosity has also been re- 
corded in Iridaceae in three species of the allied 
southern African genus Homeria > 
1980), where it is associated with a my 


thus constituted complex heterozygotes. The 
possibility that such a situation prevails in G. 
parva, which is also autogamous, seems likely, 
but meiotic studies are very difficult to make in 
Galaxia and this remains to be established. 

In my review of cytology and karyotype change 
in Galaxia (Goldblatt, 1979b), I proposed the 
hypothesis that karyotypic evolution had pro- 
ceeded by decreasing aneuploidy from a basic 
and relatively symmetric acrocentric comple- 
ment with n = 9 to n= 8 and subsequently to 
n — 7. The reduction in chromosome number 
has been achieved by karyotypic reorganization 
with minimal юш of ee material (Ta- 

1), th 


ich 13 улу similar 


in all diploid species. This AG ae es is seen as 
having been achieved in two basic ways: either 
by unequal but symmetric translocation (Rob- 
ertsonian fusion); or by unequal asymmetric 


metacentric and a small centric fragment, while 
in the latter a long acrocentric and centric frag- 
ment result. 


1084 


Both processes appear to have taken place in 
the course of evolution of Galaxia subgenus Eu- 
rystigma. In G. citrina, with n = 8 (Fig. 1C), as 
well as in G. barnardii and the n = 8 PUE of G. 
versicolor, there is a large acrocentric in place of 

small acrocentrics in the basic Ga/axia 
karyotype (Fig. 1A). The formation of the karyo- 
type in the n = 7 form of С. versicolor (Fig. 1D) 
seems to have involved the fusion of two large 
acrocentrics to yield the very long metacentric 
pair in this karyotype. In G. variabilis, the same 
process may have taken place, but involving the 
fusion of two small acrocentrics to form the pair 
of long metacentrics found in this karyotype (Fig. 
1E). Further unequal reciprocal translocation 
must have occurred in the evolution of the un- 
usual karyotype of G. parva. It seems simplest 
to postulate that the species evolved from an 
ancestor with a karyotype like that found in the 
n=7 form of G. versicolor (if not from G. ver- 
sicolor itself), but not only has at least one un- 
equal reciprocal translocation event taken place 
in the reduction of base number from 7 = 7 to 
6, but a certain amount of structural rearrange- 
ment presumably occurred subsequently to re- 
sult in the heterozygous karyotype ofthis species. 


BIOLOGY AND REPRODUCTION 


The biology of both Ga/axia kamiesmontana 
and G. parva exhibits aspects that are unusual 
in the genus. Galaxia kamiesmontana is the ear- 
liest flowering species of Galaxia, blooming early 
in the winter, in May or June, typically three 
weeks after the first soaking winter rainfall. It 
grows in the rock shelf habitat characteristic for 
several other species of Galaxia. In these rocky 
sites, the thin covering of soil rapidly becomes 


y un 
mains available to the plants for several weeks 
even without further rain. Galaxia kamiesmon- 
tana completes its flowering by the end of June 
but ripening of the capsules is delayed until late 
spring or until the soil dries out. Then the stem 
elongates, pushing the cluster of leaves and ripe 
fruits well above the ground, before it breaks and 
the fruit cluster is dispersed by the wind. 
Galaxia parva is more typical of the genus in 
its flowering and fruiting cycle. It grows in the 
clay soil that is also favored by its allies, G. ver- 
sicolor and G. variabilis, and flowers in the early 
spring. The small, pale flowers open in the late 
morning and fade at about 3:30 р.м. The species 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


is self-compatible and, at least in the greenhouse, 
autogamous, and this breeding system is unique 
in its subgenus, but is curiously paralleled in sub- 
genus Galaxia by G. albiflora, a species also hav- 
ing very small, and white, short lasting flowers. 
Autogamy is known in at least two other species 
of subgenus Galaxia, G. stagnalis and the south- 
ern populations of G. fugacissima, where it seems 
to have evolved independently. 


SYSTEMATIC TREATMENT 


Galaxia kamiesmontana Goldbl. sp. nov. TYPE: 
South Africa. Cape: Kamiesberg, Namaqua- 
land, on Rooiberg, above 4,000 ft. in shal- 
low soil on rock shelves, Goldblatt 5560 (ho- 
lotype, MO; isotypes, К, NBG, PRE, $, 
WAG). Figure 2. 


Planta minuta, ad 2 cm alta, tunicis cormi pallido- 
brunneis, fibris reticulatis costis verticalibus, folia 2- 
5 falcatis, ad 3 cm longis 1 mm latis, floribus cam- 
panulatis pallido-purpureis, infra luteis, tubo perian- 
thii 5-10 mm longo, tepalis 10-12 mm longis ungui- 
culatis, unguibus ascendentibus, limbis I libus 
4—5 mm latis, filamentis connatis in columnam ca. 5 


lo 
ramis styli brevibus ad apices antherae extensis, mar- 
ginibus stigmatum integribus 


Plants tiny, to 2 cm high when in bloom. Corm 
ovoid, 3-5 mm diam., tunics light brown, fibers 
reticulate, with a few prominent vertical ribs. 
Leaves 2—5, falcate, lightly channelled or flat, to 
3 cm long and 1 mm wide, acute, with broad 
transparent sheathing bases below the ground, 
SUM engin. мет underground, reaching to 
10m Flow- 


ers Coca ie light purple with yellow nectar 
guides at the base of the limbs, claws yellow; 
perianth tube 5—10 mm long, cylindric; tepals 
10-12 mm long, distinctly unguiculate, claws as- 
cending, forming a narrow cup enclosing the fil- 
ament column, limbs extended horizontally, the 
outer to 5 mm wide, inner to 4 mm wide. Fila- 
ments ca. 5 mm long, united below in a cylin- 
drical column, free in the upper 0.5-1 mm and 
curving outwards, yellow; anthers just under 2 
mm long, diverging, yellow. Style diverging into 
three branches at mid anther level, stigmas with 
the lobes shorter than or barely overtopping the 
anthers, margins entire, minutely ciliate, incurv- 
ing opposite the anther, radial margins slightly 
raised. Capsules 6—7 mm long; seeds angular, less 
m diam. Chromosome number 2n = 
18 (Goldblatt 5560). 
Flowering time. 


~ 


Мау-Јипе. 


[ 
1 


1984] 


GOLDBLATT — GALAXIA 


FIGURE 2. Morphology of Galaxia kamiesmontana with the distribution of all species of subgenus Eurystig- 
ma: whole plant and single flower x 1; section of the flower and top view of the stigma lobes much enlarged. 


Distribution. Kamiesberg in central Nama- 
qualand, on the Rooiberg above 4,000 ft., in shal- 
low, seasonally waterlogged soil on rock shelves. 
Figure 2. 


Galaxia kamiesmontana is an unusual species, 
and quite distinct in subgenus Eurystigma not 
only in its small size but in the structure of its 
flowers. In the other species of Galaxia the flow- 
егѕ аге campanulate with flaccid, widely cup 
tepals, or in G. barnardii the flower is hypocra- 
teriform. In either case, there is little distinction 
between the limb and claw of the tepals. In G. 
kamiesmontana, however, the tepals are clearly 
clawed. The ascending claws form a narrow cup 
that encloses the filaments (Fig. 2), and the limbs 
are sharply flexed at right angles to the tube and 
extend horizontally. 

The rock shelf habitat of Galaxia kamies- 
montana is typical for the genus, several species 
of which are restricted to such situations. Galax- 
la kamiesmontana is the most northerly occur- 
nng species of subgenus Eurystigma, the other 
five species of which are found in the western 
Part of the Cape Flora Region between Bredas- 
dorp in the south and Nieuwoudtville in the north 
(Fig. 2). 


The karyotype, with a diploid number of 2n = 
18, is unique for subgenus Eurystigma, and as 
described in detail above, the other species of 
the alliance have numbers of 2n = 16, 14, and 


t 
specialized, seasonally moist habitat in the high 
mountains of semi-arid Namaqualand. 


Specimens examined. SOUTH AFRICA. CAPE: 30.18 
Kamiesberg) Rooiberg, E slopes near Welkom (AC), 
Goldblatt 5560 (К, MO, NBG, PRE, S, WAG), 57684 
(MO); Rooiberg, E slopes of ridge N of the main peak, 
Goldblatt & Snijman 5588 (MO, NBG, PRE, US). 


“~ 


Galaxia parva Goldbl. sp. nov. TYPE: South Af- 
rica. Cape: Mierkraal flats, SSW of Bredas- 
dorp, Goldblatt 6181A (holotype, MO; iso- 
types, K, NBG, PRE). Figure 3. 

Planta parva, 2-3 cm alta, tunicis cormi brunneis, 
fibris costis verticalibus, foliis plus minusve planis vel 
iculatis, prostratis acutis 15-35 mm longis ad 8 


t 
ongis, filamentis connatis in columnam ca. 
3 mm longam, supra liberis, antheris 1.5-2 mm longis, 


1086 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


FiGuRE 3. Morphology and distribution of Galaxia parva: whole plant x1; dissected flower parts much 
enlarged. 


ramis styli brevibus ad partem mediam antherae ex- 
tensis, marginibus stigmatum integribus. 


Plants solitary, small, 2-3 cm high. Corm tu- 
nics brown, with prominent woody vertical ribs. 
Leaves 3-4, bifacial, more or less flat or weakly 
channelled, the outer almost prostrate, acute and 
acuminate, undulate, 15-35 mm long, to 8 mm 
wide, margins hyaline, smooth. Stem under- 
ground, extending 2-4 cm above the ground in 
fruit. Flowers campanulate, white, with tur- 
quoise nectar guides and yellow in the center; 
perianth tube 7—10 mm long, cylindric; tepals 9— 
12 mm long, 5—6 mm at the widest point. Fila- 
ments 3—4 mm long, united in a cylindrical col- 
umn below, free in the upper 0.6-1.5 mm and 
diverging, yellow; anthers 1.5-2 mm long, yel- 
low. Style diverging near the base of the anthers, 
and reaching to about the middle of the anthers; 
stigma lobes with entire, minutely ciliate mar- 


^T Ar rm +. 


gins, 1 10005 
at the edges with the adjacent lobes, radial mar- 
gins slightly raised. Capsules not known. Chro- 
mosome number 2n = 12 (Goldblatt 61814). 
Flowering time. Late July to early Septem- 


r. 

Distribution. Known only from the flats at 
Mierkraal, SSW of Bredasdorp, on light clay in 
coastal renosterbos veld. Figure 3. 


Galaxia parva has the smallest flowers in sub- 
genus Eurystigma but it is in other respects а 
typical member of the alliance. The species seems 
most closely related to G. versicolor, the pink and 
purple flowers of which are similar in general 
shape and proportion, but G. parva differs sig- 
nificantly in having a short style so that the stig- 
ma lobes reach only to the middle part of the 
anthers. The pollen is thus in direct contact with 
the stigmas, and in fact G. parva is self-compat- 
ible, and at least under greenhouse conditions, 
autogamous. It is the only species in the subgenus 
that is not self-incompatible. The small white 
flower of this species is very similar to that of G. 
albiflora (subgenus Galaxia), which is also autog- 
amous and has the smallest flowers in its sub- 
genus. There seems no doubt that the two species 
are unrelated, and that the small white and yel- 
low flower evolved independently, together with 
autogamy, in each subgenus. 

Galaxia parva has the most easterly distribu- 
tion ofthe subgenus, occurring some 50 km from 
the nearest populations of G. barnardii, its clos- 
est neighbor in the alliance. It occurs south 0 
the east-west trending Bredasdorp Mts. which 
isolate it from suitable clay soils that are com- 
mon to the north and west of the range. It seems 
likely that G. parva evolved from G. versicolor 


—— ———"U————»emwere mn T 


ииет 


1984] 


or its immediate ancestors, on а esae 
isolated pocket of clay in an area of predom 

nantly sandy or limestone soils to which it is i 
suited. The evolution of the species has been 
accompanied by an aneuploid reduction in chro- 
mosome number. The base number for the sub- 


genus. The related G. versicolor has diploid num- 
bers of 2n = 16 and 14 (Goldblatt, 1979b). The 
karyotype, described in detail in the preceding 
pages, is structurally heterozygous (Fig. 3E) and 
because the species produces ample seed, its em- 


bryology will y prove to be ofunusual 
interest. 


GOLDBLATT — GALAXIA 


1087 


Specimens examined. SOUTH AFRICA. CAPE: 34.19 
(Caledon) flats at Mierkraal, SSW of Bredasdorp (DB), 
Goldblatt 61814 (К, MO, NBG, PRE). 


LITERATURE CITED 


GOLDBLATT, P. 1979a. Biology and systematics of 
e wm: (Iridaceae). J. S. African Bot. 45: 385- 


x 979b. Chromosome cytology and karyot 
change i in Galaxia (Iridaceae). Pl. Syst. Evol. 133: 
61-69. 


. 1980. Uneven diploid chromosome numbers 
and complex heterozygosity in Homeria (Irida- 
ceae). Syst. Bot. 5: 337-340. 


THE PHY TOGEOGRAPHIC SIGNIFICANCE OF SOME 
EXTINCT GONDWANA POLLEN TYPES FROM THE 
TERTIARY OF THE SOUTHWESTERN CAPE 
(SOUTH AFRICA)! 


J. A. COETZEE? AND J. MULLERT 


ABSTRACT 


Pollen assemblages of lower Miocene age from sediments in the southwestern Cape contain ancient 
Gondwana microfloras of considerable phytogeographic interest. The parent taxa, which are not 
represented in Africa today, in 
the Tertiary. This microfossil record supports the hypothesis that a commo 

an—Madagascar flora existed in the Gondwana fragments during the Cretaceous. The final 


related to the wide ranging effects of the glaciation of Antarctica. Sclerophyllous macchia has since 
become dominant and adapted to the present Mediterranean climate. 


The unique flora of the southwestern Cape is 
very well known for its species richness and high 
degree of endemism. This vegetation, which be- 
longs to the phytochorion Capensis (Taylor, 1978; 
Werger, 1978), occurs in the present summer- 
dry/winter-wet climate of the region. It does, 
however, extend eastward to the vicinity of Port 
Elizabeth, which receives precipitation all year. 
Rie ie outliers of this sclerophyllous vege- 

SO Occur at increasing altitudes to the 
north in the mountains of the Karoo and Na- 
maqualand and along the eastern mountain chain 
as far as Ethiopia (Axelrod & Raven, 1978; Tay- 
lor, 1978). With regard to its history and phy- 
togeography, the dominant sclerophyllous mac- 
chia (fynbos) of Capensis has been the focus of 
interest for a long time. Only in recent years have 
palynological investigations shown that this 
vegetation type, adapted to a Mediterranean cli- 
mate, is not as old as previously thought (Coet- 
zee, 1978, 1983). Pollen assemblages of Tertiary 
age from boreholes at Noordhoek on the Cape 
Peninsula and in the Saldanha region, both on 
the Atlantic margin, now indicate that entirely 
different vegetation and climates compared with 
the present had existed in the southwestern Cape. 

Some of the fossil pollen types belong to an- 
cient parent taxa that are extinct in Africa today 


(Coetzee, 1981; Coetzee & Praglowski, 1984). In 
this connection the pollen assemblages from 
Noordhoek on the Cape Peninsula are of partic- 
ular interest and will be mainly referred to in this 
discussion (Figs. 1—7). Further investigation of 
the pollen spectra has provided additional evi- 
dence of other extinct types and, because these 
records are of considerable phytogeographic in- 
terest, they will be discussed in relation to their 
past distribution and paleoecology. 

wo pollen assemblages have been distin- 
guished. The older assemblage contains seven 
extinct pollen types, some of which are signifi- 
cant for the explanation of present disjunct dis- 
tribution patterns of genera in the Southern 
Hemisphere. The younger assemblage does not 
contain these extinct microfossils but is charac- 
terized by the pollen of macchia (fynbos) vege- 
tation of a type dominant in the region today. 


LITHOLOGY AND AGE OF THE 
NOORDHOEK SEDIMENTS 


A pocket of sediments containing pollen-bear- 
ing peaty clay horizons occurs within 2 km of 
the present coastline in a fault-controlled valley 
flanked by mountains, between Noordhoek an 
Kommetjie (34°09'$ and 18?20'E) on the Саре 


' Special thanks are due to J. Praglowski from Stockholm for his assistance with pollen morphological as, 


Peter Raven, Misso 
California, for his useful commen 
winteraceous wood; an 

teraceae. Mn раа Survey of South A 


ssouri Botanical Garden, for his encouragement and guidance; D. I. 


Axelrod, University of 


ts; P. Baas, Rijksherbarium, Leiden, for evaluation of the description of fossil 
ijksherbarium, Leiden, for information on the ecol ogy О of recent 


stantial 


M Ioi making 


г иное. for 1 Environmental Sciences, University of the Orange Free State, Bloemfontein, South Africa. 


ANN. MISSOURI Bor. GARD. 71: 1088-1099. 1984. 


1984] COETZEE & MULLER—GONDWANA POLLEN TYPES 1089 


L 1 


FIGURES 1-7, с: tinct pollen bi ger —1. Microcachrys (Coniferae), Noordhoek 5836 no. 27, high focus. 2. 
Ascarinat one pe anthaceae). — а. (cf. A. rubricaulis-type), pinag k 5836 no. 25, holotype, optical sec- 
on.—2b. (cf. philipensis ypo) Noordh oek 5836 no. 36, holotype, Nomarski interference — lateral 
tee .—3. Си ien аайы, (Cupanieae, Sapindaceae), Fe a 51 7115 lega 7. Á oe 4).— E NOM 
aceaepollenites barungens 5 Harris, Qe rdhoek 5836 (co-ord. 16.2, 72.6), median focus nnulate pore 
5. Xylo oolaena-type вагона). Noordhoek Laps — 5а. no. 9, holotype, d at high focus level ped cee 
triangular island pis enclosed by 3 ridges 10, paratype, view of tetrad with common aperture 
arrow) between 2 grains. —6. евон e на. еҷ Nordik 5836, no. 8, tetrad at high focus showing 
pore (arrow), Nomarski interference contrast.—7. Casuarinaceae, Noordhoek 7241, SEM micrograph showing 
spinules on linear ridges. Scale bar = 25 s (nos. 1—6) and 10 um (no. 


1090 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


SOUTHERN 


m $ 


Cape Town 


Noordhoek 
520 


Cape 
Peninsulo 


FIGURE 8. Locality map. 


Peninsula (Fig. 8). These sediments, which lie 
below sea-level, have been subdivided into the 
following two Formations according to the sedi- 
mentological profile (Rogers, 1980): Bredasdorp 
Formation (Noordhoek member, —21 to 0 m) 
and Elandsfontyn Formation (—21 to —50 m). 
The Elandsfontyn Formation, characterized by 
coarse angular q sand, contains the bulk of 
the organic matter in the succession and shows 
no marine components. It is in this Formation 
that the older Tertiary pollen assemblage mainly 
occurs, while the younger assemblage falls main- 
ly within the Noordhoek member of the Bre- 
dasdorp Formation. Here at — 10 m rare sponge 
spicules are the only marine components. Fur- 
ther detailed parallel palynological and litho- 
logical investigations on these sediments are to 
be carried out in connection with paleoenviron- 
mental assessments. 

In the absence of present possibilities for firm 
age control the palynological assemblages of the 


[Vor. 71 


Elandsfontyn Formation at Noordhoek previ- 
ously had been assigned a relative Late Oligo- 
cene/Early Miocene age (Coetzee, 1978, 1983). 
This derivation had been made by comparison 
of the pollen types with apparently younger paly- 
nological assemblages in the Elandsfontyn For- 
mation belonging to sediments further north in 
the Saldanha region. Неге in Borehole 51 
(33°58.20’S and 18*6.97'E) this Formation fits as 
follows into the succession that contains the pa- 
leontologically dated Early Pliocene Varswater 
Formation (Coetzee & Rogers, 1982): 

Varswater Formation, Early Pliocene (ver- 
tebrate fauna) (Hendey, 1981а, 1981b). 

“Saldanha” Formation (gravel member), 
Late Miocene (Tankard, 1975; Hendey, 
1981a, 1981b) (now considered to be 
younger). 

Elandsfontyn Formation, Early to Middle 
Miocene (Coetzee, 1980) (now considered 
to be younger). 

Further palynological considerations by the 
present authors now confirm a Miocene age for 
the Noordhoek pollen assemblages and suggest 
an early rather than late Miocene age. Compar- 
ison is hardly possible with the well dated trop- 
ical Tertiary microfloral succession of Gabon 
(Salard-Cheboldaeff, 1979), Nigeria (Germeraad 
et al., 1968), and Senegal (Médus, 1975) because 
of the subtropical aspect of the Noordhoek mi- 
crofloras. Only a few fossil pollen types аге com- 
mon to all these regions. A more direct com- 
parison is, however, possible with the ecologically 
similar assemblages from the Ninetyeast Ridge 
and Australia. The time of the extinction of taxa 
obviously can not be used for age-comparisons. 
However, the first occurrence of widespread types 
is more significant and in this connection the 
pollen of Compositae is of paramount impor- 
tance. The earliest records of the Tubiflora type 
are from the Oligocene of North America, Eu- 
rope, and Ninetyeast Ridge, where they always 
occur in very low frequencies. They become more 
common worldwide in the Miocene (Muller, 
1981). The fairly regular but sparse occurrence 
of Compositae pollen grains ofthe Tubiflora type 
with very low diversity in the older assemblage 
of Noordhoek suggests a Lower Miocene age for 
these pollen-bearing horizons. Unfortunately 4 
section between the older and younger assem- 
blages contains no pollen and probably indicates 
a hiatus in deposition that is difficult to explain 
until the detailed correlation of the lithology and 
palynology has been completed. This may be 


1984] 


confirmed by the initial sharp increase and high 
diversity of Compositae in the younger assem- 
blage. Such high numbers of Compositae pollen 
are characteristic of Upper Miocene and Pliocene 
or even Quaternary sediments. 


GENERAL COMPOSITION AND FORMER 
DISTRIBUTION OF THE MICROFLORA 


THE OLDER ASSEMBLAGE 


Pollen of Родосаграсеае, Widdringtonia, 
Combretaceae (or Dissotis (Melastomataceae)), 
and Restionaceae are abundant at various pe- 
riods whereas mostly low numbers of Caloden- 
drum and Myrtaceae occur throughout the se- 
quence. Pollen of Compositae and Gramineae 
are also very sparsely represented. These Bes di 
КС. _- ra jag й 


fi t ini tofthe present 
теме» forest enclaves in the Cape Prov- 
ince extending from east of Knysna, the Knysna 
forests, and the relict forest patches in valleys or 

oofs” of the Capensis phytochorion (Axelrod 
& Raven, 1978; Taylor, 1978; White, 1978). In 
addition abundant pollen was recorded of Pal- 
mae that are extinct in these regions today. These 
pollen types are different from those of the pres- 
ent South African palms, the southernmost of 
which, viz. Phoenix occurs near Bathurst in the 
eastern Cape. These microfossils together with 
pollen types such as Croton, Cupanieae, and oth- 
ers indicate the presence of subtropical floral ele- 
ments. It is in this mixed type of vegetation that 
pollen of за following seven extinct taxa, already 
alluded to, has been recorded: Moca, 
e а Casuarinaceae , Ascarina-type, Sar 
colaenaceae, Cupan mons n and ом. 
aceaepollenites barungensis. Further discussions 
will center around these њи: 


THE YOUNGER ASSEMBLAGE 


The dominant microfossils in this assemblage 
belong to the Proteaceae, Ericaceae, Cliffortia, 
C podiacea i 


laeaceae and occasional Casua uarina/Myrica types. 
The contrast with the preceding assemblage is 
thus considerable. 


THE EXTINCT POLLEN TYPES (FIGS. 1—7) 


Microcachrys (Con iferae). The relatively rare 
but highly characteristic trisaccate Microcachrys 


COETZEE & MULLER—GONDWANA POLLEN TYPES 


1091 


pollen (Fig. 1) is often associated in its occur- 
rences with maxima of Casuarina pollen. At 
present the genus is restricted to Tasmania, where 
it occurs in the montane vegetation above 1,000 
m. Its past distribution was much more exten- 
sive, and it has been reported from the Jurassic 
and Cretaceous of India, the Lower Cretaceous 
of Madagascar, the Jurassic, Cretaceous and Ter- 
tiary of Australia, the Lower Cretaceous—Ter- 
tiary of New Zealand, the Lower Cretaceous of 
Argentina, the Tertiary of Kerguelen, and the 
Paleocene and Oligocene of Ninetyeast Ridge 
(Archangelsky & Gamerro, 1967; Couper, 1960; 
Herngreen et al., 1982; Kemp & Harris, 1977; 
Venkatachala et al., 1972). Scott (1976) reported 
this pollen from the Lower Cretaceous of the 
Algoa Basin on the southeastern coast of South 
Africa, and more recently McLachlan and Pie- 
terse (1978) recorded it from Lower and Uppe 
Cretaceous sediments of the DSDP Hess. site 
361, 180 miles southwest of Cape Town 

Winteraceae. Tetrads of this family are also 
highly characteristic of the older pollen assem- 
blage but occur scattered throughout the whole 
section. Two slightly different types appear to 
have been present. Comparison with the pollen 
morphological monograph ofthe family by Prag- 
lowski (1979) and a joint study with him of his 
reference material indicate that the larger type 
has most likely been derived from Drimys sec- 
tion Tasmannia. This plant group is at present 
confined to Malesia, Australia, and Tasmania, 
where it occurs in tropical forest, subtropical to 
temperate rain forest, and subalpine shrub vege- 
tation (Fig. 9). Its closest affinity lies with the 
pollen of Drimys piperita. The smaller type (Fig. 
6), however, closely resembles the pollen of Bub- 
bia isoneura, a New Caledonian species. The ge- 
nus Bubbia occurs at present from sea-level to 
montane habitats in New Caledonia, New 
Guinea, and the Moluccas but is found in Aus- 
tralia only in Queensland and thus appears less 
well adapted to colder climates (W. Vink, oral 
comm.). The oldest record of Winteraceae is from 
the Aptian/Albian of Israel (Walker et al., 1983) 
and it is of special interest that this is the only 
other extant angiosperm family besides the 
Chloranthaceae which, so far known, has a Low- 

er Cretaceous occurrence. 

It is of interest to note that the South African 
fossil pollen types appear to be more related to 
Old World representatives of the family than to 
the New World group of Drimys section Drimys. 
They also differ from Takhtajania perrieri (Bub- 


1092 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 


г“ ә 


С ES => x Ger OR 


~ r ~ 
-40 i) 
AA 
^ dd 
60 
Drimys, sect Drimys ----- Bubba еен Belliolum = Takhtajania 
Drimys,sect.Tasmannia —-—-— Pseudowintera © Exospermum +Zygogynum 


А Fossil occurrence 


Ficure 9. Distribution map of recent and fossil Winteraceae. 


bia perrieri}, the only representative of the family 
in Madagascar. 

Fossil pollen of Winteraceae has been de- 
scribed from the Maestrichtian of South Austra- 
lia and New Zealand as Gephyrapollenites by 
Stover and Partridge (1973), who recognized three 
species without indicating affinities with recent 

pollen types of the family. Martin (1978), how- 
ever, pointed out that its closest relationship is 
with Drimys section Tasmannia. Mildenhall and 
Crosbie (1979) considered Gephyrapollenites a 
junior sy ym of Pseudowinterapollis. They are 
of the opinion that this genus is similar to the 
recent endemic genus Pseudowintera of New 
Zealand. The specimens from South Africa do 
not fall within the circumspection of Pseudo- 
winterapollis as previously thought by Coetzee 
(1981). 

Casuarinaceae. The pollen type of this fam- 
ily (Fig. 7) is very common throughout the older 
assemblage and shows marked changes in abun- 
dance. The possibility that many of these forms 
could belong to this family has already been al- 
luded to (Coetzee, 1983) and it has now been 
proved beyond doubt at the SEM and TEM levels 
by Praglowski (Coetzee & Praglowski, 1984) that 
Casuarinaceae existed in South Africa in the Ter- 


tiary. The pollen can easily be confused at the 
light microscope level with that of Myrica, which 
also occurs in the assemblage (cf. also Muller, 
1981). 

Unfortunately it is not possible to differentiate 
between the pollen of the inland representatives 
of the family and that of the widespread Casuari- 
na equisetifolia, which is a pioneer of tropical 
sandy beaches. 

Casuarinaceae are adapted to a subtropical- 
tropical climate and are found today in a wide 
range of rainfall conditions. The main develop- 
ment of the family is undoubtedly centered in 
Australia with radiation into the Pacific and 
Southeast Asia, the range of C. equisetifolia being 
much wider. The probable native range of the 
family is indicated in Figure 10. 

Fossil pollen has been found in abundance in 
Tertiary sediments of New Zealand, Australia, 
the Ninetyeast Ridge, and Borneo, and recorded 
as Haloragacidites (= Triorites) harrisii or as Са- 
suarinidites cainozoicus. Macrofossils have been 
found in the Paleocene of Argentina, and the 
occurrences at Noordhoek fit in well with a for- 
merly much wider range of the family. 

Ascarina-type (Chloranthaceae). This pollen 
type (Fig. 2) is especially frequent in the lower 


f ~ 


— —————————————SÉPEÉETEÉERPERENI" 


OE aE EE TT TON RUN 


COETZEE & MULLER —GONDWANA POLLEN TYPES 


1093 


g 


f Ж 1) Why 
{7 e “1 MM 
^, Ф Mihi Tikes de. 


-% 2 mA B 


a 


UMMA Casuarinaceae A 


FIGURE 10. Distribution map of recent and fossil Casuarinaceae. 


part of the section, where it alternates with max- 
ima of Casuarina, Microcachrys, Podocarpus, 
Widdringtonia, Combretaceae/Melastomata- 
ceae, and Proteaceae pollen. More than one sub- 
type comparable to Ascarina rubricaulis (Fig. 2a), 
4. philippinensis (Fig. 2b), and Ascarinopsis 
coursii appears to be present. The last species, 
often included in Ascarina, is a rare endemic 
found in humid montane forests at an altitude 
of 1,700-1,800 m in the northeast of Madagas- 
car. The seven species of Ascarina occur in East 
Malesia and New Guinea in montane rain forest 
from 1,010—3,300 m and in the west Pacific in 
New Zealand also in a humid climate, but from 
sea-level to 1,500 m (Fig. 11) 

In this case also, the fossil occurrence of As- 
carina in the Miocene of South Africa fits in well 
With its formerly much more widespread range, 
Which in the Palaeogene covered Australia and 
the Ninetyeast Ridge (Fig. 11). In the Cretaceous 
this pollen type (as Clavatipollenites) was even 

in d in central 
South America, and Europe 
(Muller, 1981) while it has been reported for the 
wer Cretaceous by Scott (1976) from bore- 
holes along the southeastern African coast, and 
by McLachlan and Pieterse (1978) from the 
DSDP site 361, 180 miles A: id Cape Town in 
the Upper Cretaceous sedim 


Xyloolaena-type ући ти The very 


fossil occurrence 


characteristic pollen tetrads of this type (Fig. 5) 
are restricted to the genera Leptolaena, Rhodo- 
laena, Sarcolaena, and Xyloolaena of the family 
Sarcolaenaceae, which is endemic to Madagas- 
car. These tetrads occur scattered in the lower 
part of the older assemblage and appear to re- 
semble most closely the tetrads of Xyloolaena 
(Carlquist, 1964; Straka, 1964). 

small trees, rarely 
large trees, which occur mainly as rare elements 
in the humid forests of the eastern region of the 
island. Here they prefer the drier localities on 
sandy or rocky soil over a wide range of altitudes 
but are found also on coastal dunes (Sarcolaena) 
or, rarely, in the dry eastern region (Leptolaena 
arenaria) (Cavaco, 1952; Perrier de la Bathie, 
1920 


Cupaniopsis-type (Sapindaceae). This pollen 
type (Fig. 3), which is equivalent to the fossil 
genus Cupanieidites, is at present restricted to 
part of the tribe Cupanieae from America, Mad- 
agascar, and Australasia Mine it is conspicuously 
missing in genera Africa (Muller & 
Leenhouts, 1976; Muller, s 1981) The pollen oc- 

у in the -— 


mire in 
E" 


LI d Ба Tas 


of other pollen taxa. 

The fossil pollen genus Cupanieidites was 
abundant in the Upper Cretaceous both of cen- 
tral Africa, becoming extinct here in the early 


1094 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


^ bn 


2 aa 


scarinopsis 


A 


А Tertiary fossil occurrence 


GURE 11. 
fossil Ascarina-type pollen 


Tertiary (Muller & Leenhouts, 1976), and of 
South Africa from where it was reported from 
the Upper Cretaceous sediments from DSDP site 
361 (McLachlan & Pieterse, 1978). Cupa- 
nieidites has an Upper Cretaceous record in Bra- 
zil and the earliest record for Australia is from 
the Palaeocene (Muller, 1981). The genera of Cu- 
panieae with this pollen type occur at present in 
a wide range of humid tropical to subtropical 
environments (Fig. 12). 

Sparganiaceaepollenites barungenis Harris 
(Typhales) (Aglaoreidia qualumis Par- 
tridge). This pollen type (Fig. 4) probably has 
been derived from a taxon related to Typhaceae 
or Sparganiaceae but cannot be identified with a 
living species, although Martin (1973) suggested 
that the pollen of the living Sparganium anti- 
podum is rather similar. 

In the older assemblage it is common and fluc- 
tuates greatly in abundance as does the pollen of 
Restionaceae. Both pollen types probably are de- 
rived from marsh vegetation around fresh water 
inland lakes. 

The fossil pollen type was first described from 
the Eocene-Miocene of Australia and New Zea- 
land (Harris, 1972; Mildenhall & Crosbie, 1979). 
Sparganiaceaepollenites has also been recorded 
from the 


ne of Argentina (Archangelsky, 
1973). 


Distribution map of Ascarina and Ascarinopsis (Chloranthaceae) and Tertiary occurrences of 


DISCUSSION 


In general the Miocene pollen flora of the 
southwestern Cape, the composition of which 
has been broadly discussed by Coetzee (1978, 
1983), appears to represent lowland and mon- 
tane subtropical rain forest in which palms were 
prominent. This vegetation type does not occur 
in the area at present although the Knysna forest 
to the southeast possibly could be considered an 
impoverished remnant of it. This flora clearly 
antedates the development of a Mediterranean 
climate in the Cape region, possibly in the Plio- 
cene (Непдеу, 1981b) or Late Pleistocene (Ax- 
elrod & Raven, 1978), as discussed by Coetzee 
(1983). The humid forest in Madagascar that at 
present contains taxa similar to those of the Mio- 
cene rain forest of the Cape (Ascarinopsis, E 

eae VE XS 4 X зс also 


a modified descendant from this ancient vege- 
tation type, which was postulated by Axelrod and 
Raven (1978, Fig. 6) to have been present in the 
Late Miocene in both region 

It is obvious from the аа assemblages that 
links existed with the ancient floras of Gon- 
dwanaland (Raven & Axelrod, 1974). These flo- 
ras may have dispersed almost directly among 
the closely situated Gondwana fragments, pos- 
sibly from the mid-Cretaceous to the Palaeogene. 


1095 


1984] COETZEE & MULLER—GONDWANA POLLEN TYPES 
$ Cos 12 JoJo 
£ РА Ж o (2 A 
-70 У 2 PN Les ~ 


7, 


Wi 


WT д 
0; 


in] Ж 


hu 
u^ 
|- =- – – – - 


Ev] 


ee Å- -~ — ت‎ - 
.. 
.. 


% A Hui. RR 
Iron OER RELI 
Br Y 4 hy Mie 7 11 
@ | 
А 


+; 


My, 


i 

КЛ 1 

t 29 * 
+. , 
"эы жы тоу. 


Ln genera of Cupanieae with Cupaniopsis type 
A 


pollen (Sapindaceae) 


fossil occurrence of Cupaniopsis (Cupanieidites) type pollen 


FIGURE 12. Distribution map of genera of Cupanieae with Cupaniopsis-type pollen and fossil occurrences. 


In these latter periods the dispersal routes were 
either tropical or subtropical or more temperate 
wit Antarctica in both cases in the central po- 
sition (Raven & Axelrod, 1974). 

With regard to the common Africa-Madagas- 
car floral elements, recent geophysical evidence 
(Rabinowitz et al., 1983) indicates that the mo- 
uon of Madagascar relative to Africa was from 
the north and probably started in the mid-Ju- 
rassic (165 million years ago) or somewhat later 
depending on the postulated spreading rates. 
Separation from the continental margin of Kenya 
and Somalia must have been effective at least 
from the Cenomanian (95 million years ago) on- 
ward. This is confirmed by the presence, in the 
Albian of Madagascar, of a microflora indicative 
of the Gondwana province of Herngreen an 
Eülonova (1981; Herngreen et al., 1982), sug- 

ng soutl tact ther than east African 
| Ones at that time. Raven and Axelrod (1974) and 
. Axelrod and Raven (1978) visualized these con- 
| Tections, via the now largely submerged Mas- 
. Сагепе plateau, with India and Antarctica and 
. lasting till the late Cretaceous. This connection 
then could have provided a route for the Cre- 
| làceous dinosaurs as well as for the rich angio- 


sperm floras of Madagascar and the Seychelles. 

Microcachrys. This is undoubtedly the most 
prominent ancient Gondwana element with a 
probable continuous range in the Cape region 
from the Lower Cretaceous into the Miocene. 
The records of the former distribution of Micro- 
cachrys, as discussed earlier, are all from ancient 
fragments of Gondwanaland. This former range 
is in sharp contrast with the present day relict 
occurrence in Tasmania. The genus may have 
originated in the Jurassic or earlier and dispersed 
widely in the Jurassic-Lower Cretaceous, after 
which it became variably extinct. It is of special 
interest that Microcachrys survived much longer 
in South Africa than in India, which, during its 
northward drift, passed through totally different 
climatic zones. It is interesting that another Me- 
sozoic gymnosperm genus, Araucaria (Araucar- 
iacites), the pollen of which occurs concomi- 
tantly with Microcachrys in the Cretaceous of 
South Africa (McLachlan & Pieterse, 1978; Scott, 
1976), did not survive as long as Microcachrys 
in the Cape. 

Winteraceae. Like the other ancient angio- 
sperms represented in the Tertiary pollen assem- 
blages, this family forms a specific link with the 


1096 


austral floras, especially with the subtropical- 
temperate types. Of importance is the evidence 
in the Miocene of the Cape of representatives of 
the Australasian group of Winteraceae. That this 
family was formerly more widespread was al- 
ready suggested by the discovery of fossil wood 
in the Upper Cretaceous of North America (Page, 
1981). The nature of the wood has suggested a 
relationship with the Old World Winteraceae but 
the anatomical features are now thought to be 
correlated with climate rather than with taxon- 
omy (P. Baas, oral comm.). 

The primitive characters of the Winteraceae 
are well in accord with at least an early Creta- 
ceous origin as indicated by the presence of fossil 
pollen attributed to this family (Walker et al., 
1983) in Israel, which formed part of the ASA 
floral province at that time. According to Hern- 
green and Chlonova (1981) this province cov- 
ered the tropical-subtropical zone of a joint South 
American—African—Arabian continent including 
Israel, and overland dispersal in Gondwanaland 
was clearly possible in the early Cretaceous. The 
survival of the related genus Takhtajania in 
Madagascar indicates local evolution also from 
an ancient Gondwana matrix. To reach Mada- 
gascar the dispersal to this island must, according 
to Axelrod and Raven (1978), have occurred be- 
fore 80 million years ago. In view of its early 
separation from Africa, dispersal was probably 
from the south. Raven and Axelrod (1974: 616) 
inferred that the ancestors of the Winteraceae 
reached Australia in mid-Cretaceous time along 
a tropical or subtropical route. 

The present day American representatives of 
the Winteraceae grouped in Drimys section Dri- 
mys may be a later development from West 
Gondwana ancestors, separate from develop- 
ment in Austra 

The records i. Casuarina, Ascarina, and Cu- 
panieae, which will be discussed next, refer to 
elements that are less clearly restricted to tem- 
perate, subtropical, or montane tropical cli- 
mates. 

Casuarinaceae. This family is found in trop- 
ical lowland, montane, and subtropical climates. 
Fossil and present day distributions point to a 
wide range in the past covering the Pacific, 
Southeast Asia, Australia, Madagascar, and the 
southern parts of Africa and America (Fig. 10). 
Raven and Axelrod (1974: 616) suggested that 
the ancestors of Casuarinaceae may have reached 
Australia in mid-Cretaceous times by a subtrop- 
ical to tropical route from Africa. The oldest- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


known fossil pollen dates from the Palaeocene 
of New Zealand (Muller, 1981). Evidently the 
contraction of its range was related to the effects 
of cooling during the maximum glaciation of 
Antarctica in the Terminal Miocene. 

Ascarina-type. The relationship of Ascarina 
with the Lower Cretaceous Clavatipollenites 
group (cf. Muller, 1981), which may even have 
originated in Central Africa (Doyle et al., 1977), 
most likely refutes the postulation of Raven and 
Axelrod (1974) that this genus reached Mada- 
gascar from the east. Its abundant presence still 
in the Miocene of South Africa strongly suggests 
that a chloranthaceous matrix developed some- 
where on the African mainland and its descen- 
dants could easily have reached Madagascar while 
spreading out over Antarctica and other Gon- 
dwana fragments. The marked contraction of its 
range is probably connected with competition 
with younger angiosperm groups as well as with 
climatic change. Its survival in Madagascar (as 
Ascarinopsis) is evidently due to the isolation of 
this island and the continued equable climate at 
these latitudes. The climatic requirements may 
have been more subtropical to tropical-montane 
than was the case with Casuarina. 

Cupanieae. Cupanieae have also had a long 
history on the African continent as is shown by 
the abundance of Cupaniopsis-type pollen in the 
Upper Cretaceous of West Central Africa and 
the Miocene of South Africa. They presumably 
reached Madagascar in mid-Cretaceous time af- 
ter it separated from East Africa. 

The range contraction of those genera of Cu- 
panieae that were characterized by Cupaniopsis- 
type pollen was completed much earlier in trop- 
ical central Africa than in the subtropical south- 
егп region where some taxa still survived in the 
Miocene. The explanation for the extinction of 
part of the Cupanieae in Africa is at present ob- 
scure. In Madagascar the genera Molinaea and 
Tina of this group have survived until the pres- 
ent day and are widespread from sea-level up to 
more than 2,000 m. In Australasia and America 
the genera of this group are still widespread today 
and range from tropical to subtropical temperate 
climates (Fig. 12). 

Xyloolaena-type. For Sarcolaenaceae a sim- 
ilar development may be postulated, although a 
comparable fossil record is lacking. The occur- 
rence in South Africa of the highly developed 
Xyloolaena-type in the Miocene of the South- 
western Cape is the first fossil record ofthe family 
but certainly does not represent the oldest oc- 


1984] 


currence of the Sarcolaenaceae. It is not clear 
whether we are dealing here with an endemic 
African family that migrated to Madagascar and 
later become restricted to the island, as was in- 
ferred by Raven and Axelrod (1974). Its ecology, 
although slightly more specialized than that of 
Ascarina and Cupanieae, still fits into a humid 
subtropical to tropical-montane pattern. These 


parable and the contraction of their ranges may 

have been due to similar climatic causes. 
Sparganiaceaepollenites barungensis-pollen 

This is less indicative of former co 


mates. The occurrence of this Australian Tertiary 
pollen type indicates former connections of Af- 
rica with South America and Australia. It also 
fits into the general pattern of an austral Gon- 
dwana connection indicated by Microcachrys, 
Winteraceae, and Casuarina. Dispersal routes 
may have been via South America—Antarctica to 
Australia or via the islands of the Indian Ocean. 


persal capabilities for the parent plant or an ear- 
lier unrecognized occurrence of the ancestral 
complex. The fossil record of Typhales, however, 
goes back only to the Palaeocene (cf. Muller, 
1981). The extinction of the parent taxon of this 
pollen type at the end of the Tertiary in South 
Me Australia, and New Zealand is difficult 
0 expla 


CONCLUDING REMARKS 


The evidence discussed here not only throws 
light upon the relationship between Africa and 
Madagascar floras, but also on the contacts be- 
tween Madagascar and South America as dis- 
cussed by Raven and Axelrod (1974: 612). The 
data presented support the hypothesis that a 

Am tarctic-A 


Ceous, became fragmented due to plate move- 
ments and that taxa common to Madagascar and 
South America today had their origin in the West 
Gondwana-Antarctic section of Gondwanaland. 
The evidence does not support the postulation 
of long-distance dispersal of some of these an- 
cient taxa from Australia to Madagascar. 


COETZEE & MULLER—GONDWANA POLLEN TYPES 


1097 


Long distance dispersal around the Indian 
Ocean before the Pliocene desertification in the 
Middle East, however, may have been respon- 
sible for the distribution of such taxa as Adan- 
sonia, Hibbertia, and Nepenthes. 

The final problem on which the evidence dis- 
cussed has considerable bearing is that of the 
impoverishment of the African flora in the course 
of the Tertiary. This phenomenon has been dis- 
cussed by many authors, notably Moore (1973) 
for the palms and by Raven and Axelrod (1974). 
It would appear now that the hypothesis of local 
extinction, to explain the absence in Africa of 
many angiosperm taxa that are still present in 
South America, Madagascar, and SE Asia, finds 
support in the fossil record. A good example is 
the disappearance of the Nypa palm from trop- 
ical Africa at the end of the Eocene (Germeraad 
et al., 1968). For Cupanieae the disappearance 
from the microfossil record of the taxa charac- 
terized by the Cupaniopsis pollen type in the 
Palaeogene is documented by Jan du Chéne et 
al. (1978) and Salard-Cheboldaeff (1979). Their 
survival in South Africa well into the Miocene 
was presumably due to more stable and humid 
climatic conditions. Пена had become ех- 

inct over 1 uch earlier (Muller, 1981). 

It is thus evident he extinction may not have 
been a single event. It must have varied locally 
according to the severity of environmental 
changes associated with the maximum glaciation 
of Antarctica at the end of the Tertiary. Macchia 
must have spread during the Pliocene and Pleis- 
tocene when there were fluctuations of warm and 
cold water offshore (Axelrod & Raven, 1978; 
Tankard & Rogers, 1978). Some of these ele- 
ments were already present in the summer rain- 
fall climate of the Miocene and earlier and be- 

came adapted to summer droughts during periods 
of cold water. currents. Axe irod and even 1 2 

considered t 
which the hardiest macchia taxa have vost 
and profoundly speciated, to have originated in 
the Late Pleistocene. The older periods (not ear- 
lier than 5 million years ago) of this type of cli- 
mate were less intense (D. I. Axelrod, pers. 
comm.). On the basis of paleontological data, 
etii Hendey (1981b) postulated that the 
transition to the mediterranean type of climate 
could te occurred in the early Pliocene (5 mil- 
lion years ago). By that time the last relict oc- 
с tet htronical 


taxa discussed here could have disappeared from 
the southwestern Cape (Coetzee & Rogers, 1982). 


1098 


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AXELROD, D. I. & P. H. RAVEN. 1978. Late Creta- 
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23 1 25 
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IKE & M. 


Martin, H. А. 1973. The palynology of some Ter- 
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MILDENHALL, D. C. & Y. M. Crossi. 1979. Some 
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MOORE, H. E., JR. 1973. Palms in tropica forest eco- 
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& J. ROGERS. 1978. Late Cenozoic palaeoen- 
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MAIZE INTROGRESSION INTO TEOSINTE— 
A REAPPRAISAL’ 


JOHN F. DOEBLEY? 


ABSTRACT 


77 h neidered 


Maize (Zea mays L. subsp. mays) and its wild relativ: 
by many authors t to be undergoing substantial reciprocal introgression. While ‘there is evidence that 


has been largely circumstantial. A re-consideration of th id f gr te e 
proved it wanting. Red sheath color, large grain size, triangular fruitcase — and the presence of 


internal chromosome knobs, all characters attributed to maize introgression into teosinte, appear 


rather to reflect the adaptation of particular teosinte 


populations to the exigencies of specific ie ei 


Apparently, the taxa of teosinte have remained relatively free of Het inti maize contamination at 


from maize to teosinte, although possible, remains undocumented. 


Introgressive hybridization, or more simply, 
introgression, is the incorporation of genes from 
one population into another with a different 
adaptive norm rson & Hubricht, 1938). 
This process is of obvious importance to tax- 
onomists and evolutionists because, along with 
mutation, gene drift, and recombination, it is a 
potential source of evolutionary variation within 
and among species. Introgression is of particular 
interest to scientists studying cultigens апа their 

y lack 
barriers to hybridization and they often grow 
sympatrically. For these reasons, one would ex- 
pect introgression between crop species and their 
ancestors to occur with some frequency. 

The cultigen maize (Zea mays L. subsp. mays) 
and its wild relatives, the teosintes, have been 
considered model examples of reciprocal in- 
trogression (de Wet & Harlan, 1972; Heiser, 1973; 
Wilkes, 1977). The evidence for teosinte in- 

d ere farmers 
in Mexico encourage the hybridization of teo- 
sinte and maize in an effort to “improve” their 
maize strains, the resultant maize populations 
have many teosintoid characteristics (Wilkes, 
1970, 1977). The reverse introgression of maize 
germplasm into teosinte seems less likely to oc- 
cur because maize has many characteristics that 


lofteosinte in the wild. Low-level E 


prevent it and its hybrids with teosinte from sur- 
viving in nature. Nevertheless, the frequency of 
maize-teosinte hybrids in the wild in Mexico and 
Guatemala (1096 or more of the teosinte plants 
in a field may actually be hybrids), coupled with 
the fact that maize and teosinte show paralle 

variation over much of their range, has led some 
authors to conclude that many teosinte popula- 
tions have been substantially altered by maize 
introgression. In this paper, I will review and 
reinterpret the evidence for maize introgression 
into teosinte and articulate the viewpoint that 
the teosintes have not been substantially altered 
by maize introgression. 

A critical problem in the study of introgression 
is to distinguish natural evolutionary variation 
from that produced by introgressive hybridiza- 
tion (Anderson, 1953). This generally proves 4 
difficult task because within any taxon there ex- 
ists a certain amount of natural variation, some 
of which will inevitably be in the direction of 
other closely related taxa. For example, within 
many plant genera, one finds some natural vari- 
ability for seed and fruit size. This being the 
situation, claims that those populations with in- 
termediate-sized organs represent hybrids of the 
large and small organed forms should be viewed 
askance (cf. Weatherwax, 1918). Further, even if 


‘Tam arces to H. H. Iltis, R. R. Kowal, D. M. Waller, W. C. Galinat, and others for critically reading the 


research was supported primarily by gran 


ts to Н. Н. Iltis from Pioneer Hi-Bred International 


manuscript. 
of Johnston, Yon. and the National Science асн d (BM 57421861). Final preparation of the manuscript 


for publication was уо by NIH prei 
2 Herbari nt of Botany, Univers 


sconsin, Madiso 
Department of Biology, 7 Ton A&M Univer. College Station, Texas 7784 


ANN. Missouri Bor. GARD. 71: 1100-1113. 1984. 


со ме, СМ 11546. 


son, Wisconsin 53706. Present address: 
3. 


1984] 
aparticular t 1 trates int iacy for 
anumber of prema or genetic characters, 
thereby appearing t 


he introgression problem in Zea is particu- 
larly perplexing. Not only does cultivated maize 
commonly occur in the proximity of its wild rel- 
atives, but it has been observed to hybridize in 
the wild with all of them (Wilkes, 1967; Collins, 
192 1a; Iltis et al., 1979). In addition, there exists 

E variation in the shape an 
the teosintes, which easily lends 


introgression into teosinte seems difficult to re- 

pudiate. Yet, one may interpret the variation in 

teosinte as natural evolutionary variation, and, 

as will be shown below, such an interpretation 

coincides well with known ecological and evo- 

onary principle: 
In 


4 +1 


+ 


the reader have a basic knowledge of the taxo- 
nomic relationships in Zea. The и is divided 
into two sections. Section Luxuriantes contains 
three species: (1) Z. diploperennis fis Doebley 

uzman, a diploid perennial from Jalisco, 
Mexico; (2) Z. perennis (Hitchc.) Reeves & Man- 
gelsdorf, a tetraploid perennial from Jalisco, 
Mexico; and (3) 2. luxurians (Durieu & Asch- 
erson) Bird, an annual from southeastern Gua- 


ays, n 

mexicana (Schrader) Iltis, a large spikeleted an- 
nual fro m high elevation of central and northern 
Mexico, including races Chalco, Nobogame, and 


var. uete 
nangensis Iltis & Doebley, a genetically distinc 
orm of this subspecies from western Guatemala 
(Ilis & Doebley, 1980; Doebley & Iltis, 1980; 
Doebley, 1983). As this taxonomy suggests, the 
teosintes of section Luxuriantes are not partic- 
ularly closely related to the cultigen, whereas those 
of section Zea are so close as to be regarded as 
Conspecific. Finally, in this discussion, I will, at 


tribe Andropogoneae of the family Gramineae. 


DOEBLEY —MAIZE REAPPRAISAL 


1101 


HISTORICAL BACKGROUND 


ince the time when Ascherson, Beadle, Col- 
lins, Kempton, Longley, and others first began 
to document the extent of variability among teo- 
sinte EE енне have demonstrat- 
ed a bias in favo maize introgression to ex- 
plain this adipis Thus, Collins (1921a: 340, 
345), who noticed that both maize and teosinte 
of the Valley of Mexico have dark red, densely 
pilose sheaths, speculated that teosinte acquired 
these characters from maize via introgression. 
Part of Collins's reason for proposing this expla- 


dorf (1947: 165) and then Wilkes (1977) reiter- 
ated this idea. 
Collins also (1921a: 350) theorized that pe- 
rennial — inia teh on е hybridized 
e. However, 
he offered no evidence " support this idea other 
an his 


parallel variation wherever they co-occur. Col- 
lins apparently failed to recognize that such par- 
allel variation could easily result from either teo- 
sinte introgression into maize or simpl 
convergent evolution. A few years later, Collins 
(1925: 378, 1930: 201) modified his thesis some- 
what by suggesting that either Z. /uxurians (Flor- 
ida type) or Z. perennis might have hybridized 
with maize to produce the Mexican annual teo- 
sintes (Z. mays subsp. mexicana and subsp. par- 
viglumis). As nerd in support of this hy- 
pothesis, he reporte . forms resembling 
the Mexican type рл. nas з pibep. mexicana] 
always appear in hybrids between Florida teo- 
sinte [Zea luxurians] and maize" (Collins, 1925: 

78 


Kempton and Popenoe (1937: 216-217) dis- 
cussed “the assumption of other workers" that 
the triangular shape of the fruitcase of Mexican 
annual teosinte represents the by-product of 
maize introgression into Zea luxurians, which 
has trapezoidal fruitcases. However, Kempton 

and Popenoe questioned the validity of this hy- 
pothesis based on their observation that the tri- 
angular "fruited" Huehuetenango teosinte oc- 
curs in “almost pure stands,” and thus, is free of 
maize introgression. Ultimately, they decline to 
conclude, one way or the other, whether Mexican 
annual teosinte represents a good species or a 
hybrid of “pure teosinte” with maize (Kempton 
& Popenoe, 1937: 217). 

Longley (1937, 1941a) proposed that the in- 


1102 


ternal chromosome knobs (heterochromatic re- 
gions) of Mexican annual teosinte resulted from 
the contamination of “риге teosinte" (Zea lux- 
urians), which has many terminal knobs, with 
maize, which is characterized by many internal 
knobs. However, he declined to rule out the pos- 
sibility that the Mexican annual teosintes ac- 
quired their internal chromosome knobs via mu- 
tation, with 2. /uxurians being their more 
primitive ancestor. 

Mangelsdorf and Reeves (1938, 1939) went 
one step further than Collins, Kempton, and 
Longley and advanced their hypothesis that teo- 
sinte **. . . appears to be nothing more than Zea 
[the hypothetical wild maize] with a slight infec- 
tion of Tripsacum germplasm" (1939: 209). This 
idea actually originated with Edgar Anderson (cf. 
Mangelsdorf & Reeves, 1939: 212; Anderson, 
1969; Mangelsdorf, 1974: ix). Under the view- 
point of this hypothesis any variability in teo- 
sinte manifests nothing more than differences in 
the relative proportions of “wild maize" and 
Tripsacum germplasm (Mangelsdorf & Reeves, 
1939: 215). 

This view of variability in teosinte has influ- 
enced others as well. Thus, in his study of the 
genetic mechanisms controlling inheritance of 
inflorescence characters in maize-teosinte hy- 
brids, Rogers (1950), a student of Mangelsdorf, 
found evidence that, in his view, called the purity 
of the Mexican annual teosintes into question. 
He reported that hybrids with Nobogame (Zea 
mays subsp. mexicana) produced the most maize- 
like inflorescences and those with southern Gua- 
temalan teosinte (Zea luxurians) the least maize- 
like ones. go (Z. mays subsp. mexicana) 
and “northern” (western) Guatemalan (Z. mays 
var. huehuetenangensis) teosintes were inter- 
mediate in this regard. To Rogers, these results 
indicated that Nobogame teosinte is highly con- 
taminated with maize, the other Mexican teo- 
sintes are somewhat less so, and southern Gua- 
temalan teosinte is the least contaminated of all. 
He concluded that his evidence supports “7... 
the hypothesis that the m laize intes 
represent the original teosinte with a substitution 
of maize germplasm on various chromosomes” 
(Rogers, 1950: 555). 


Ммм» „уу. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


which are similar to those of the maize of this 
region (Wilkes, 1972: 1067-1077, 1977: 384- 
385). Wilkes (1967: 81), ostensibly disagreeing 
with Rogers (see above), found little evidence of 
maize introgression into teosinte in the Nobo- 
game area. Wilkes (1967: 72) considered the 
principal direction ofgene exchange in the Balsas 
river valley to be from teosinte to maize and not 
vice versa. Wilkes (1967: 82) reported hybrids 
to be rare in southeastern Guatemala, and thus, 
introgression unimportant. Wilkes (1967: 82) also 
concluded that teosinte in the Huehuetenango 
region of Guatemala was little introgressed by 
maize, though he found many hybrids of this 
teosinte and maize in the wild. Wilkes (1967: 
80-81) considered the teosinte of the Mexican 
Central Plateau to show signs of maize admixture 
in its pistillate spike, including paired spikelets 
and a nonbrittle rachis. In addition, he regarded 
the large grain size and triangular fruitcase of 
some Central Plateau populations and of Chalco 
teosinte as evidence of maize introgression 
(Wilkes, 1977: 278). More recently, Wilkes (1979) 
proposed that all the racial varieties of annual 
teosinte Ited from the hybridization of maize 
with Zea diploperennis, coming full circle back 
to Collins's (1921a) similar suggestion involving 
Zea perennis. 

Bird (1978: 362) also considered maize in- 
trogression to have played an important role in 
the morphology of extant teosinte populations. 
He regarded tall plants with large leaves, few 
tillers, a great number of and large fruitcases, and 
large caryopses as heavily introgressed by maize. 
Further, he hypothesized that Huehuetenango 
teosinte is a hybrid of maize and Zea luxurians. 

Many authors have reiterated these conten- 
tions concerning the introgression of maize 
germplasm into teosinte (Heiser, 1973; Galinat, 
1975; de Wet et al., 1978; de Wet & Harlan, 
1972). However, a few authors have adjured this 
line of reasoning, and taken either the viewpoint 
that teosinte is not significantly introgressed by 
maize or that the evidence for such introgression 
is wanting (Melhus et al., 1949; Kato, 1976; Iltis 
& Doebley, 1980). 

For many of the authors discussed above, кай 


of their models оп the origin of corn because ап 
understanding of teosinte is prerequisite to un- 
derstanding the evolution of maize. As stated by 
Collins (1921b: 505) *... the many resem- 

ces between maize and teosinte, together with 
the fact that the two forms interbreed with per- 


РИИ 


1984] 


fect freedom, make it certain that whatever the 
origin of maize it must be intimately associated 
with teosinte.” Thus, in the early part of this 
century, when very little was known of teosinte, 
hybridization and introgression theories seemed 
to solve the dilemma of teosinte being genetically 
the same species as maize but morphologically 
too dissimilar from maize to be its ancestor. 


RECONSIDERING VARIABILITY IN TEOSINTE 


Five trends in teosinte variation lend them- 
selves to easy interpretation as examples of maize 
introgression into teosinte. (1) Grain size. Be- 
cause some teosinte populations produce larger 
grains than others, various authors (Wilkes, 1977; 
Bird, 1978) have either hypothesized or stated 
quite unequivocally that the large-grained forms 
show the effects of introgression from the rela- 
tively giant-grained maize. (2) Fruitcase shape. 

е fruitcases of the teosintes vary from trape- 
zoidal through triangular but blunt on the axia 
side to triangular and pointed or “pinched” on 
the axial side. The pointed triangular forms, it 
has been argued, are the most introgressed and 
the trapezoidal the least (Kempton & Popenoe, 
1937; Mangelsdorf & Reeves, 1939; Reeves 
1953; Wilkes, 1977). (3) Sheath characters. Teo- 
sinte in the Valley of Mexico, like the native 
maize of this area, possesses densely pilose and 
dark red leaf sheaths. Teosinte is said to have 
Obtained these characters from maize through 
introgression (Collins, 1921a; Mangelsdorf, 1947; 
Wilkes, 1967, 1972, 1977). (4) Disease resis- 
tance. Teosinte from southeastern Guatemal 
expresses resistance to a common maize virus. 
According to one author it could have obtained 
this resistance from local races of maize, which 
me disease 
CU pelis. chromosome 


~ 


m 


temala possesses only termin 
knobs whereas the annuals of Mexico, as well as 
Cultivated maize, have many internal knobs. As 
discussed above, Longley (1937, 1941a, 1941b) 
pe ees ше Suggested that the Mexican an- 

alt their internal knobs from 


maize. 

Despite the facility with which these assertions 
Often have been made, there are other explana- 
tions that do not necessitate introgression. Phy- 
logeny and ecology of teosinte populations fur- 
nish the basis for a more parsimonious 
explanation for variability in teosinte than ad- 


DOEBLEY — MAIZE REAPPRAISAL 


1103 


mixture with maize. In the following discussion 
each of the aforementioned five trends is recon- 
sidered in the light of this viewpoint. 

_ Grain size. “Тһе seed is one of the least plas- 

с organs on a plant; plants respond to stress 
phenotypically by varying almost every other 
component of yield before seed size is affected" 
(Harper, 1977: 664). Seed size results from a 
delicate compromise between a great number of 
conflicting exigencies including available mois- 
ture, temperature, amount of competition, len 
of growing season, and many other factors (Har- 
per et al., 1970; Stebbins, 1972; Harper, 1977) 
Once a species has optimally adapted its grain 
or seed size to local environmental conditions, 
it will vary the numbers produced 100-fold be- 
fore varying size one-fold (Harper, 1977). Thus, 
one would expect natural selection against in- 
corporation of maize germplasm in teosinte 
plants, which would upset the fragile adaptive 
balance they have obtained in relation to grain 
size. This ecological principle impels us to con- 
clude that grain size is one of the least likely 
features of the teosinte plant to be altered by 
maize introgression. 

In addition to the above theoretical reason for 
expecting little alteration in grain size because of 
maize introgression, there exists some empirical 
evidence to support such a view. This evidence 
lies in the mean cupulate fruitcase weights (in- 
cluding caryopsis) for the different taxa of teo- 
sinte. Quite simply, if maize introgression ac- 
counts for the variability in grain weight (size), 
then one would predict those taxa geneticall 
closest to maize and crossing most frequently 
with it to have the largest fruitcases. The da 
however, fail to meet this expectation in ibn 
ways. de despite their greater genetic-evolu- 
tionary ce from maize, some species of 
ин the perennial teosintes, and Zea lux- 
urians, all produce much heavier fruitcases than 


more frequently with it (Table 1) (Wilkes, 1977; 
Iltis & Doebley, 1980). Second, Zea luxurians, 
long recognized as one of the least maize-like 
teosintes and crossing but rarely with maize in 
its native habitat, produces grains often heavier 
than those of the supposedly greatly contami- 
nated Chalco teosinte (Z. mays subsp. mexi- 
cana). 

If not maize introgression, what then explains 
the observed variability in the grain or fruitcase 
size among the teosintes? There are several fac- 


1104 ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


TABLE l. Average weight (mg) of teosinte cupulate fruitcases with caryopsis (N — number weighed). 


Species 
Population Collection Wt. N 
Tripsacum dactyloides, cult. 
Ft. Meade, Maryland 118 50 
Zea diploperennis 
Manantlan, Jalisco Iltis et al. 1375 75 100 
La Ventana, Jalisco Guzman 777 72 100 
Las Joyas, Jalisco Titis et al. 1250 68 100 
x 72 
Zea perennis 
Los Depositos, Jalisco Iltis et al. 1050 83 100 
Zea luxurians 
Honduras Galinat 76-2076-B 90 20 
Ipala, Chiquimula Iltis G-42 99 100 
Agua Blanca, Jutiapa Iltis G-38 86 100 
El Progreso, Jutiapa Iltis G- 5 84 100 
El Progreso, Jutiapa Iltis G-36 76 100 
t 4 87 
Zea mays subsp. mexicana 
Churintzio, Michoacan CIMMYT K69-3 62 100 
Quinceo, Mich Iltis & Cochrane 276 95 100 
Los Reyes, Mexico Iltis & Lasseigne 769 86 50 
+ 87 
Nobogame, Chihuahua Gentry 17973 58 30 
Nobogame, Chihuahua Wilkes (1967) 62 = 
Zea mays subsp. parviglumis 
Balsas drainge: 
Huetamo, Michoacan CIMMYT K67-15 50 50 
Valle de Bravo, Mexico CIMMYT K67-21 56 100 
Tzitzio, Michoacan Iltis & Cochrane 308 43 100 
Palo Blanco, Guerrero USDA 343237 31 100 
SW Jalisco: 
La Huertita Guzman s.n. 79 100 
El Palmar Puga 11065 73 100 
Guatemala: 
San Antonio Huista Iltis & Lind G-120 51 100 
х 
53 


tors that seem to influence seed size in plants. 
First, the amount of competition that a species 
normally encounters influences the size of seeds 
produced. Species whose seedlings face intense 
competition require larger seeds than those of 
open habitats (Harper et al., 1970; Abrahamson 
& Gadgil, 1973; Carlquist, 1974; Werner & Platt, 

1976). Plant habit also affects seed size, with 
perennials producing fewer and larger seeds than 
annuals (Salisbury, 1942; Hart, 1977; Primack, 

1979). This results partly from the general oc- 
currence of perennials in later seres (greater com- 


petition). Length of growing season influences 
seed size, with larger seeds being more easily 
formed in regions with long growing seasons 
(Baker, 1972). If other factors place a premium 
on small seed size in a region with a long growing 
season, then the plant will take advantage of the 
long growing season to produce a greater number 
of seeds rather than larger ones. Available mois- 
ture plays an important role in determining 
size, with small seeds common in wet areas and 
large seeds frequent in dry areas. Seedlings in 
Aennoht 


р жр » 
drier y encounter drought 


“a 


1984] 


CUITZIO 
1831 т 


MANUEL DOBLADO 


Ch кү £ MA 


DOEBLEY —MAIZE REAPPRAISAL 


1105 


CHAPINGO 
2250m 


TELOLOAPAN 


1 tati 


three diagrams represent 


х The и 
sites of Z Zea mays cata mexicana and the — three to of subsp. parviglumis. On the сони the 


a 


y temperatur 
exceeds is mm, шуй 15 К: at trun 
urve exceeds te rature curve, space 


). Where 
соса. Minn (1:10) and the portion above 100 mm is black. 


curves is filled by vertical lines (or black, if rainfall 


exceeds 100 mm) iE if kengi curve falls below temperature curve, that space is filled by small dots. At 


top left of ea 


stress during the early stages of growth (Baker, 


reduce the likelihood of severe drought stress 
during early life. Further, larger seeds may ger- 
minate deeper in the soil where the moisture 
supply is more reliable (Schimpf, 1977). 
idently. th logical d inati 


ad 


size is immensely complex. Nevertheless, it is 
clear that seed size is an important aspect of the 
adaptive strategies of plants. Further, with so 
many factors influencing seed size and number, 
and with these factors often in competition with 
Опе another, it would be unreasonable to expect 
easy explanations for all the known variability 

grain size among the ipe cen — upon 
examining the fruitcase (in g caryopsis) 
weights of these taxa AN = the correspon- 


ch diagram are name of station and altitude. These 
наст Weltatlas (Walter et al., 1967) using data from Garcia (1 (1974). 


agrams are patterned after those from the 


dence of this information to environmental pa- 


First, tl ial t latively few 
large fruitcases as predicted. Both perennial taxa 
Zea mays 


subsp. parviglumis, and ados as large as those 
of Z. mays subsp. mexicana. The large fruitcases 
of Zea luxurians could be explained by the rel- 
atively dry conditions under which this species 
grows with only 500-1,000 mm of rainfall an- 
nually, an environment similar in many ways to 
the Mexican Central Plateau. The difference be- 
tween the small *seeded" populations of the Bal- 
sas river drainage (Z. mays subsp. parviglumis) 
and the larger “seeded” ones of the Central Pla- 
teau and the Valley of Mexico (Z. mays subsp. 
mexicana) appears to be closely related to avail- 
able moisture. As shown by the climatic dia- 


1106 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


ES ? 
200 
| ^ 
Е mse 
о 
— O 
а. 
E 150 | 
È o 
125 | m1 
= 
ж | 
Е 
< 100 - e e 
| == 
2 e ө 
» eto 
* 
50 | 
» 
| | | | 
10 EE 26 25 


Mean Annual Temp. (°C) 


FIGURES 2-3. —2. А 


(Мог. 71 
0 
3 
O 
о 
Oo 
= $ 
e 
8 3 
Е $ 
9 О ж 
e 
E] 
& * 
1 | d ue] 


50 70 90 110 
Fruitcase Wt. (mg) 


graph of mean annual temperature (°C) versus mean annual precipitation (cm) for various 


teosinte populations: Zea perennis (hollow square), Zea luxurians (stars), Zea mays subsp. mexicana (solid 
circles), and subsp. parviglumis (hollow circles). Data for Mexico from Garcia (1974) and that for Guatemala 
Ро 1 иж : EC A چا‎ гаа А 1 аа 


from Urrutia (1964). — 3. Стар 


correlation between these two variables; large fruitcases in dry areas and small ones in wet areas. Symbols as 


grams (Fig. 1), the Balsas sites receive a much 
greater amount of rain during the growing season 
than the Central Plateau and Valley of Mexico 
sites. The difference between the climates in the 
regions of Zea mays subsp. mexicana and subsp. 
parviglumis is dramatically portrayed in Figure 
2, in which mean annual temperature is graphed 
against mean annual precipitation, while the re- 
lationship between fruitcase weight and precip- 
itation is graphically displayed in Figure 3. The 
Huehuetenango population of Z. mays subsp. 
parviglumis, which occurs in a very wet area with 
2,000–3,000 mm rainfall annually although with 
a longer growing season than Balsas teosinte, 
produces small fruitcases as well. Another point 


Бат tween 
the small and manv- 


be 
y-grained Z. mays subsp. раг- 
viglumis and the larger and fewer-grained Z. mays 
subsp. mexicana was noted by Wilkes (1967), 
namely that the grains of the later can success- 
fully germinate deep (6 in.) in the soil while the 
former must germinate near the surface. This 


coincides well with Schimpf's (1977) observation 
that species from dry habitats produce large seeds 
capable of successfully germinating deep in the 
soil where the moisture supply is more reliable. 
Finally, that Nobogame teosinte produces grains 
E а 


surprising but can be explained by the shortness 
of the growing season of this most northern of 
all teosintes, and by its adaptation to grow in 
thickets along streams (a locally and seasonally 
wet environment) (Wilkes, 1967, 1977). 

n summary, an examination of the evidence 
Suggests that for grain size and number the teo- 
sinte populations are highly variable, with each 
population adapted to the demands of its раг- 
ticular habitat and seasonal growth form. 

Fruitcase shape. The fruitcase in teosinte is 
composed of the female spikelet and its attached 
rachis segment. Its shape ranges from trapezoidal 
and Tripsacum-like through triangular though 
blunt on the axial side, and ultimately to trian- 
gular and sharply pointed, or “pinched,” on the 


1984] 


axial side. Many authors have considered that 
the sharply pointed forms display the effects of 
condensation produced via maize introgression 
Kempton & Popenoe, 1937; Reeves, 1953; 

Wilkes, 1977). According to this view, those teo- 
sinte populations with trapezoidal fruitcases are 
free of maize germplasm, whereas those with 
“pinched” triangular пае show a high de- 
gree of maize contamination. 

Using measurements p both male tassels 
and female spikes, the hypothesis that the tri- 
angularity of the teosinte cupulate fruitcase re- 
sults from condensation acquired via maize in- 
trogression can be tested. If genes for 
condensation obtained through maize introgres- 
sion account for the transformation of the trap- 
ezoidal fruitcases into triangular ones, then one 
would expect the procession from trapezoidal to 
triangular female rachis segments to be correlat- 
ed with a gradual shortening (condensation) of 
the internodes of the central spike and branches 
of the teosinte male tassel. This expectation 


( ; Montgomery, 

1906; Titis, 1911; Anderson, 1 1944). From Table 
‚ one can readily see that no such correlation 
К. Instead, those teosinte populations with 
trapezoidal fruitcases (sect. Luxuriantes) possess 
the shortest male internodes on both the central 
and lateral spikes, and those with triangular fruit- 
Cases (sect. Zea), the longest. Indeed, the trian- 
gular “fruited” teosintes do not have tassel in- 
ternodes pari in length between those of 
the trapezoidal types and maize, but rather they 
have the longest nae имей (i.e., the least 
condensed) in all of Zea. These facts cast doubt 


If maize introgression fails to хр {һе vari- 
ation in teosinte fruitcase shape, what then can 
explain the diversity of observed forms? The ап- 
Swer might be quite simply that the triangular 
Shape of the fruitcases of sect. Zea represents an 
evolutionary advancement over the more prim- 
itive trapezoidal shape found in sect. Luxu- 
riantes and the genus Tripsacum. The triangular 
shape might allow more efficient packing of the 
rachis segments in the individual spikes or easier 
dispersal. If triangularity allows more efficient 
packing, then one might expect the ratio of the 
weight of the cupulate fruitcase to that of the 
сагуорз15 to be lower for the triangular type. 


DOEBLEY — MAIZE REAPPRAISAL 


1107 


A comparison of internode sie (mm) 
for the male and female inflorescences of 


Male Internode Female 
iens Fruit- 
Central Lateral 
Species Spike Branch Length 
Sect. Luxuriantes 
Zea diploperennis 3.16 3.06 7:30 
Zea perennis 3.76 3.68 7.20 
Zea luxurians 4.39 4.48 8.33 
Sect. Zea 
Zea mays subsp. 
mexicana 5.13 5.65 6.92 
Zea mays subsp. 
parviglumis 5.54 5.96 6.05 


Measurements made on the fruitcases show this 
to be generally the case with a progression from 
large to small ratios from Tripsacum > Zea dip- 
pee > Z. perennis > Z. luxurians > Z. 
mays subsp. mexicana > Z. mays subsp. par- 
Mets (Table 3). However, there is consider- 
able overlap between Z. luxurians and Z. mays 
subspp. mexicana and parviglumis. 

In summary, the observations (1) that there is 
no clear-cut correlation between condensation in 
the male and female teosinte inflorescences to 
support the maize introgression hypothesis, and 
(2) that fruitcase shape may reflect different de- 
grees of divergence from the primitive trapezoi- 
dal Tripsacum-like condition to a more efficient 
triangular shape, undermine the interpretation 
that variation in fruitcase paes is evidence for 
maize introgression into teosin 


Sheath color and pilosity. = has 


ley of Mexico (Collins, 192 1a; Mangelsdorf, 1947; 
та 1967, 1972). Wilkes чен that 


er, 


asa а of inadvertent selection) that copy the 
coloration of the native maize of the region and 
thus are able to escape the eye and sickle of the 
campesinos weeding their corn fields. Wilkes 
(1972, 1977) like his - A Collins and 
Mangelsdorf, evoked maize introgression as the 
mechanism by which the шн of the Valley 
of Mexico acquired the genes for this 
tive” coloration, although i 
convergence " xe alternative hypothesis. Ini- 


tially have 


> 


1108 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


TABLE 3. Mean weight of the total fruitcase and caryopsis, and the ratio of these two values for some teosintes 


and Tripsacum (N = number weighed). 


Total 
Species Fruitcase Caryopsis 
Population Collection Wt. (mg) Wt. (mg) Ratio N 
Tripsacum dactyloides 
Ft. Meade, Maryland 122 35 3.69 10 
Zea diploperennis 
Las Joyas Iltis et al. 1250 75 25 2.98 10 
Manantlan Iltis et al. 1375 75 25 2.97 10 
+ 2.98 
Zea perennis 
Los Depositos Iltis et al. 550 106 36 2.92 10 
Zea luxurians 
Agua Blanca Iltis G-38 87 31 2.78 10 
Ipala Пиз G-42 125 38 3.05 12 
Progreso Iltis G-36 87 37 235 16 
Progreso Iltis G-5 90 37 2.40 12 
s 2.65 
Zea mays subsp. mexicana 
Quinceo Iltis & Cochrane 276 109 44 2.48 12 
Los Reyes Iltis & Lasseigne 769 85 36 2.36 10 
Amecameca Iltis & Cochrane 176 97 44 2.18 10 
Chalco Iltis & Cochrane 175 103 43 2.38 10 
Ф 2.35 
Zea mays subsp. parviglumis 
Tzitzio Пиз & Cochrane 308 45 23 2.04 10 
San Antonio Huista Iltis & Lind G-120 54 23 2.45 15 
La Huertita Guzman s.n., cult. 82 38 2.17 10 
С 2.22 


= S. шы pa БА 214. 1: 


р орр ction from teosinte 
into maize? Unfortunately, this possibility has 
received little consideration. 

In order to explore other potential explana- 
tions for tl f dark red pi sheaths 
in teosinte and maize from the Valley of Mexico, 
I will first review the functions these traits might 
fulfill in maize and teosinte. Red tissue color- 
ation results from the presence of anthocyanins, 
which fulfill many different functions for the 
species which produce them (McClure, 1975; 
Harborne, 1976). One particular function, cold 
resistance, has been attributed to anthocyanins 


pigmented than similar species at warmer lower 
elevations (Kerner, 1891; Bonnier, 1895; Clau- 


sen et al., 1940). Researchers have also noted 
that plants develop greater red coloration when 
artificially grown in cold environments. This is 
true for Hydrocharis (Overton, 1899), Impatiens 
(Alston, 1959), Pyrus (Creasy, 1968), Chrysan- 
themum (Rutland, 1968), and Euphorbia (Ma- 
rousky, 1968). M tly Ganders et al. (1979) 
noted that in populations of Collinsia, Mimulus, 
and Trifolium, phenotypes with dark red spotted 
leaves are more frequent in colder microhabitats. 
These latter authors hypothesized that the dark 
red pigmentation in the leaves of these species 
functions to absorb radiant energy, and thus, 
warm the plant. Galinat (1967) proposed this 
same hypothesis, viz. that red pigmentation acts 
to absorb radiant energy, thereby warming the 
plant, to explain the predominance of red plant 
color among high altitude varieties of maize in 
Latin America. Galinat noted the lack of exper- 
imental verification for this hypothesis. Since that 


1984] 


DOEBLEY — MAIZE REAPPRAISAL 


1109 


TABLE 4. Sheath pubescence* and color, altitude (т) and mean annual temperature (°С) for some teosinte 


populations. 
Species Sheath Sheath ean 
Population Collection Pubescence Color Annual Temp. Alt. 
Zea mays subsp. mexicana 
Valley of Mexico: 
Amecameca USDA 246 3 2 14.4 2,425 
Chalco Iltis & Fi on 401 3 2 15,9 2.250 
Los Reyes Iltis & Lasseigne 769 3 2 16.0 2,180 
Central Plateau 
Patambicho а. Prior 2 2 16.4 2.132 
шпсео Пиз & ad 276 2 2 17.6 1,940 
Churintzio CIMMYT K 69-3 1 15 Е 1,900 
Nobogame ex G. Beadle 1 1:5 — 1,850 
Degollado Puga 11066 1 1 — 1,625 
Zea mays subsp. parviglumis 
Balsas drainage: 
Valle de Bravo CIMMYT K 67-21 0 1 18.3 1,350 
Teloloapan CIMMYT W 71-3 0 1 21.9 1,610 
Palo Blanco USDA 343237 0 0 22.0 1,267 
Jalisco: 
Е! Palmar Puga 11065 0 0 — 980 
La Huertita Guzman s.n. 0 0 E 1,100 
Jirosto Iltis & Nee 1480 0 0 — 500 
Purificacion Iltis & Nee 1471 Е — 25.4 450 
Guatemala: 
San Antonio Huista Titis & Lind G-120 0 0 20.0 1,300 


bescent thro 


* 0 = essentially шы... 1 = hairy along upper sheath margins; 2 = pubescent throughout; 3 = densely ри- 
oughou 


^0 — green or slighty red; 1 = red; 2 = 


dark red. 
° This information from Garcia (1974) and Urrutia (1964). 


time, however, two studies have shown that va- 
rieties of maize with dark red sheaths stay warm- 
er than similar dilute red types (Greenblatt, 1968; 
Chong & Brawn, 1969). 

- Tanthocyanins do aid in warming t the teosinte 


E one would predict that those teosinte о 
ulations growing in the coldest environments 
would be the most heavily pigmented and those 
in the warmest areas the least pigmented. While 
looking for characters to distinguish various teo- 
Sinte populations, I took some notes on the de- 
&ree of coloration of the sheaths among 14 pop- 
ulations I had ine in Florida. Each lati 


Was grown in two different randomly assigned 
rows. Without knowing the origin of the plants 
in a row, I subjectively categorized the sheaths 
ОЁ the plants in it as either green or slightly red 
(0), red (1), or dark red (2) (see Table 4). A two- 
Sided Tau-test (a non-parametric test of associ- 


tion) sl ignificant lati f both mean 
annual (P « 0.02) and altitude (P < 
0.01) (which in Mexico is closely related to tem- 
perature) to sheath color (Table 4). This suggests 
that teosinte populations display varying degrees 
of red coloration not as the result of fortuitous 
hybridizations with maize or even as an attempt 
to mimic maize (though red coloration might 
rtainly function in that capacity and thus be 
hee. but rather tion to a local 
environmental condition — temperature 
The situation with sheath i is sim- 
ilar to that with anthocyanins. Again, naturalists 
and ecologists have often noted that dense pu- 
bescence functions to preserve the warmth with- 
in plants in cold environments (Daubenmire, 
1947: 186; Carlquist, 1974: 563-565). Dense pu- 
bescence increases the boundary layer surround- 
ing the organ it bedecks, thus causing tempera- 
ture fluctuations in the plant to lag behind those 


1110 


of the environment. In this way the plants may 
escape injury during short periods of extreme 
temperature (Daubenmire, 1947: 172). Various 
naturalists have commented on the correlation 
between the density of pubescence and temper- 
ature in Potentilla (Clausen et al., 1940: 141- 
142) and Senecio (Carlquist, 1974: 563-565). 
Returning to Table 4, it is clear that there exists 
in teosinte a correlation between temperature and 
density of pubescence, with the most hirsute pop- 
ulations found in the highest coldest habitats and 
the glabrous ones in the lower warmer sites. A 
two-sided Tau-test of association shows signifi- 
cant correlations of both mean annual temper- 
ature (P < 0.01) and altitude (P < 0.01) to the 
density of sheath pubescence. As with sheath col- 
oration these data suggest that pubescence in teo- 
sinte results not from haphazard hybridizations 
with maize, but from each individual population 
adapting to the exigencies of its particular hab- 


Although coloration and pubescence in teo- 
sinte have their adaptive functions, this does not 
preclude the possibility that teosinte obtained 
these characters from maize. However, teosinte 
is a natural wild plant that has undoubtedly per- 
sisted in the diverse climatic regions of Meso- 
America for tens-of-thousands of years. There 
can be little doubt that it achieved its present 
adaptation long before man and maize arrived 
on the scene. 

A final curious fact worthy of comment con- 
cerns the manner in which both maize and teo- 
sinte of the Valley of Mexico carefully restrict 
the intense expression of dark red pigmentation 
and dense pilosity to the leaf sheath, thus leaving 
the photosynthetic leaf blade essentially free of 

irs and red color. This, too, bespeaks the 
adaptive importance of the traits. The function 
of the leaf sheath is primarily protective rather 
than photosynthetic, its salient role being to shield 
the stem from both insects and desiccation. In 
this same manner, the red color and hairiness of 
the sheaths of certain teosintes might act to 
maintain the temperature of the stem ata slightly 
higher temperature than otherwise possible es- 
pecially late in the growing season when nights 
are cool. 


ments, (2) that maize and teosinte are C-4 plants, 
and thus, thermophiles, and (3) that there is a 
close correlation between both degree of red col- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


oration and pubescence on the one hand, and 
mean annual temperature on the other, it is high- 
ly unlikely that teosi juired tl haracte 

by sporadic hybridization with maize. Further, 
there is no better reason for presuming that dark 
red coloration and dense pubescence would have 
introgressed from maize to teosinte than there is 
for expecting the reverse introgression from teo- 
sinte to maize. In fact, given that teosinte is a 
highly successful wild species and that maize is 
not, the latter seems much more probable. 

Disease resistance. Brewbaker (1979) sug- 
gested that Zea luxurians obtained resistance to 
Maize Mosaic Virus and the rust, Puccinia sorghi, 
when genes for resistance to these diseases were 
transferred to it from local Caribbean maizes. 
However, introgression, if it occurred at all, 
probably moved in the opposite direction—from 
teosinte into maize. The reasons for this are quite 
simple. First, Zea luxurians is the most primi- 
tive annual species in Zea, and thus, closely re- 
lated to the perennials Z. perennis and Z. diplo- 
perennis (Doebley & IItis, 1980). These, and most 
perennials, of necessity, maintain high disease 
and insect resistance because their sedentary and 
long-lived life-style renders them easily locatable 
by pests, which they tend to accumulate (Nault 
& Delong, 1980; Nault et al., 1980). Annuals, 
however, which do not accumulate pests or dis- 
ease because of their annual habit, generally show 
less resistance to disease and predation (Feeny, 
1976). Thus, it appears likely that Zea luxurians, 
which мило hI +1 E : 1 рі 1 рі Пу 
cytologically, and genetically (cf. Doebley & Iltis, 
1980), retains, asa legacy of its phyletic affiliation 
with the primitive perennial taxa of Zea, a low 
susceptibility to disease. 

Chromosome knobs. Longley and others have 
argued that the internal chromosome knobs of 
the teosintes in Mexico came from maize, and 
that the original “pure teosinte" (Zea /uxurians) 
possessed only terminal knobs. On the surface 
of it, this suggestion seems fairly improbable, for 
if the Mexican teosintes are merely Zea luxuri- 
ans with a “slight infection” of maize germ- 
plasm, then one would expect them to have chro- 
mosome knob patterns more closely resembling 
the pattern of Zea luxurians than they do. Rath- 
er, the Mexican teosintes have knob patterns es- 
sentially identical to maize (i.e., they have many 
internal knobs). The similarity between the Mex- 
ican teosintes and maize would seem best ex- 
plained not by introgression, but by considering 
these teosintes as ancestral to maize (Kato, 1976). 


аи a i ~ се кали. 


1984] 


Other available evidence also lends little cre- 
dence to the thesis that knobs introgress from 
maize into teosinte. Kato and Galinat (1975), in 


clear-cut documentation for introgression in 
either direction. And, as Kato (1976) demon- 
strated, the annual teosintes of Mexico possess 
some knob positions that are found neither in 


Mexican annual teosintes. If these Mexican an- 
nuals, like other teosintes, are the products of 
gradual evolutionary development from a com- 

mon ancestor, M then the unique knob 
positions of thes tes, like their distinguish- 
ing нео! features, would have had suf- 
ficient time to arise in response to varying en- 
vironments (Kato, 1976) 


CONCLUSION 


Dat. E sire ee ЕТЕР MEE Вата 


аге numerous in the literature оп teosinte. As 


n have researchers 
displayed such a bias in favor of the introgression 
hypothesis? There is one primary reason. Au- 

ors who believed that maize evolved from an 
unknown wild maize sought an explanation for 
teosinte that could remove it as a possible ances- 
tor of maize. Thus, they interpreted the various 
forms of teosinte as nothing more than 7ripsa- 
cum or a primeval teosinte with varying degrees 
of maize germplasm. 

All things considered, there appears to be little 
or no clear-cut evidence to support the idea that 
the teosintes have been greatly altered by maize 
introgression. Whether one considers grain s 
fruitcase shape, sheath color and pilosity, dee 
тозоте knob positions, or disease resistance 
the patterns of variation among the populations 
of teosinte can best be explained on the basis of 
ecology and phylogeny. Seen from the viewpoint 

9f the ecologist and evolutionist, Zea is not a 
helter-skelter conglomeration of maize-Tripsa- 
cum or maize-Zea luxurians hybrids, but rather 
àn orderly product of allopatric variation among 
9cal populations that strikingly displays the ef- 


DOEBLEY —MAIZE REAPPRAISAL 


1111 


ум. of natural selection and geographic specia- 


nally, the goal here has not been to take the 
undoubtedly indefensible position that never in 


stantial evidence of such crossings can be found, 
and further, that such introgression holds little 
hope of permanently affecting characters essen- 
tial to the survival of the teosinte plant in the 


о 
populations а! as we perceive them пуча are in all 
m the con- 
dition in which they existed prior to mens domes- 
tication and dispersal of maize. 


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1112 


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DOEBLEY – MAIZE REAPPRAISAL 


11313 


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RECONSIDERATION OF OENOTHERA SUBG. 
GAUROPSIS (ONAGRACEAE)! 


WARREN L. WAGNER? 


ABSTRACT 


Oenothera havardii and O. dissecta, primarily of northern Mexico, and a third species, O. canescens, 


of the High Р 


lains of the U.S., previously were placed together in subg. Gauropsis by P. A. Munz. 


New data on morphology, cytology, and seed anatomy were gathered to evaluate the relationships of 


remaining two species are not closely related, but they do appear E 
other than either is to any other species. n this reason, they are here retained in 


Sect. Gauropsis is related to sect. Hartman 
иан апа О. Кип 
it a 


and to the remainder of the genus. Oenothera canescens is 


a, and es 
thiana. The е сама лаје of О. hava 
о represent a lineage that dive rged г relatively early in the evolution of the genus. It may 


s diploid, п = 


4; and O. havardii has both diploid and tetraploid populations. Mor- 
phological and anatomical data clearly demonstrate мәг Oenothera ha 


vardii is not closely allied wi 

О. havardii i is ‘al closely related to any other 
с section, sect. Paradoxus. The 

be more re closely related to each 

sect. Gauropsis. 

pecially to the white-flowered species, Oenothera 

rdii are obscure, at best, but 


have ocd a common ancestor with species of sects. Anogra, Gauropsis, Hartmannia, Kneiffia, 


Lavauxia, and Xylopleurum. 


Oenothera subg. Gauropsis has been studied 
relatively little. Only Munz (1932, 1965) has 
published taxonomic studies of these plants dur- 
ing the past 50 years. Munz included three species, 
Oenothera canescens, O. dissecta, and O. havar- 
dii, which had been placed in various segregate 
genera in the past: O. canescens in the monotypic 
genus Gaurella (Small, 1896); O. canescens and 
O. dissecta as members of the genus Megapter- 
ium (Britton, 1894; Small, 1896); and O. dissecta 
and O. havardii in the genus Hartmannia by 
Rose (1905). These species were apparently an 
enigma to Munz, one that was heightened be- 
cause his study was based on very few specimens, 
especially of O. havardii and O. dissecta. He 
grouped them together in subg. Gauropsis partly 


because they did not fit conveniently into any 
other of his subgenera. He stated that they shared 
several features such as bushy habit, ovoid cap- 
sules with angled or keeled valves, and seeds in 
several rows per locule. 

These three species do share a bushy to sprawl- 
ing habit, but it is difficult to ascertain whether 
this suggests a relationship between them or 
merely superficial similarity. Ovoid capsules not 
only occur in these species, but also in several 
other sections of the genus, some of which differ 
greatly in other respects. The disposition of the 
seeds in several irregular rows per locule occurs 
in О. canescens and О. dissecta, but not in О. 
havardii, which has seeds in one or two rows per 
locule. On the other hand, there are numerous 


' This work was supported by a = to Peter H. Raven from the U.S. National Science Foundation while I 


was at ies Missouri Botani 


d fo 


am grateful to Peter Raven ав many helpful discussions, assistance, 


Stubbe, Peter i Ching- 
| Sousa for 


NEB, NESH, NMC, NY, OKL, 


, NA, NCU, ND, NDA, NDG, KLA, 
OS, P, PENN, PH, POM, RM, RSA, SAT, SMU, SRSC, TAES, TEX, TTC, UC, UMO, UNM, US, UT, ОТС, 


VT, WIS, WS, 
2 


P. Bishop Museum, Department of Botany, P.O. Box 19000-A, Honolulu, Hawai’i 96817. 


ANN. MISSOURI Bor. GARD. 71: 1114—1127. 1984. 


WAGNER— OENOTHERA SUBG. GAUROPSIS 


1115 


1984] 


differences between these three species in char- 
acters such as flower color, habit, and capsule 
morphology, and there appear to be few if any 
characters that clearly link them. For these rea- 
sons, it is difficult to maintain subg. Gauropsis 


> | + ‘an Ф ~ Б4 


of Oenothera have been initiated, typically in- 
volving an investigation of crossing relation- 
ships, cytology, and examination of variation 
within and between populations in the field (Die- 
trich, 1977; Straley, 1977; Raven et al., 1979; 
Dietrich et al., 1985; Wagner, unpubl. data; Wag- 
ner et al., 1985). In 1978 I began study of the 
species Munz included in subg. Gauropsis at the 
Missouri Botanical Garden. The basic thrust of 
the study was to gain a better understanding of 
E relationships of these three ери species 
t e genus, 
and io provide an expanded UA treat- 
ment of them based on extensive field and her- 
barium study. Munz saw only limited herbarium 
material and apparently observed only Oeno- 
thera canescens in the field. This treatment is 
based on the study of over 500 pressed collec- 
tions, observations of populati feach speci 
throughout its range, and study of several cul- 
tivated strains of each species grown together. 
Evidence from a genus-wide study of the anat- 
omy and morphology of seeds (Tobe et al., un- 
publ. data; Wagner, unpubl. data) is also consid- 
ered here along with the other information. 

The information available was considered in 
the light of three alternative hypotheses: 1) all 
three species should be placed in monotypic sec- 
tions, 2) Oenothera canescens and O. dissecta 
Should be kept in sect. Gauropsis with O. ha- 
vardii removed to its own monotypic section, or 
3 one or more of these species should be placed 
With related species in sect. Hartmannia sensu 
lato. These possibilities were evaluated in rela- 
tion to the narrow sectional concepts of Lewis 
and Lewis (1955). 


CYTOLOGY 


Cytological observations to determine chro- 
mosome number, and in certain strains the 
meiotic configuration, were made on root-tips or 
buds from field collections or from greenhouse- 
grown progeny from field-collected pem Buds 
for meiotic chromosome studies were fixed and 
Stored in 1:3 acetic acid : absolute ethanol under 
refrigeration. Prior to staining in 196 acetocar- 


mine buds were hydrolyzed in a mixture of con- 
centrated HCl and 9596 ethanol for 20 minutes. 
Fresh root-tips were prepared for examination 

with a four hour treatment in 8-hydroxyquino- 
line and fixed for at least one hour in 1:3 acetic 
acid:absolute ethanol. The root-tips were then 
hydrolyzed for ca. six minutes in 10% НСІ and 
stained in 296 propionic-carmine. 

A total of 11 strains representing all thre 
species have been examined (Table 1), including 
ter Ra- 


nothera canescens examined was diploid, n = 7. 
In contrast, the majority of the counts made for 
O. dissecta and O. havardii were tetraploid. Oe- 
nothera dissecta, sampled throughout its range, 
appears to be entirely tetraploid, whereas О. ha- 
vardii, also sampled throughout its range, is tet- 
raploid in Arizona and Mexico, but diploid in 
western Texas. Quadrivalents occur frequently 
in meiosis in the tetraploids of both O. dissecta 
and O. havardii, indicating that the two diploid 
sets of chromosomes in each of these species 
would pair at meiotic metaphase I, and suggest- 
ing that they might literally be RESAD 

This fact, in conjunction with t urrence of 
diploid plants of O. havardii in Jonas suggests 
that polyploidy has occurred independently in 
both species. The addition of these two species 
brings the total number of polyploid or partly 
polyploid species in Oenothera to ten (ca. 896 of 
the genus), distributed in eight sections. Half of 
these, like O. ae include both diploid and 
tetraploid population 


GREENHOUSE STUDY 


The experimental study of Oenothera canes- 
cens, O. dissecta, and O. havardii at the Missouri 
Botanical Garden has been difficult. Most strains 
reproduced almost entirely vegetatively by ad- 
ventitious shoots from lateral roots, especially 
during stress periods, and all three species were 
particularly susceptible to fungus in the hot, hu- 
mid climate of St. Louis. Mare dein кйш апа 
О. canescens flowered sparsely w wn out- 
side, and O. dissecta produced Suv т?б flowers 


majority of the flowers produced in all three 
species were used to test for self-incompatibility 
by self-pollination. Plants grown from strain (a) 
of O. dissecta were self-compatible, as were those 


1116 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


TABLE l. Chromosome observations of plants in sects. Gauropsis and Paradoxus. All specimens deposited 
MO. 


at 
Source or Chromosome 
Species Locality Collection Investigator? Observations? 
sect. Paradoxus 
Oenothera havardii 
Mexico 
Chihuahua Wagner & Brown ү 2п = 28 
3922 
Durango Wagner & Brown У бе а“ 
3935 
U.S.A. 
Arizona 
Cochise Co. Wagner 3813 УУ 2n = 28 + 2-5 55 
exas 
Brewster Co. Powell 3901 У 2n = 14; 3 plants 
Presidio Co. Powell s.n. Ww 4 
in 1982 
Powell 2195 P. Raven 2n= 14 
W. Stubbe 2n= 14 
sect. Gauropsis 
Oenothera dissecta Mexico 
Jalisco McVaugh 16984 P. Raven Srv + 41 
Zacatecas Wagner & Solomon WwW 2п = 28 
4224 
Wagner & Solomon W 2n = 28 
4237 
Wagner & Solomon Ww 2n = 28; 2 plants 
4251 
Oenothera canescens U.S.A. 
Texas 
Lubbock Co. Raven 19293 P. Raven Su + O4 


* Literature source or investigator who made the determination; W — Warren L. Wagner. 
b 


O — ring at meiotic metaphase I or diakinesis; II — bivalent; IV — quadrivalent. 


of strains (a) and (b) of O. canescens; in contrast, 
plants of all four strains of O. havardii were self- 
incompatible. Attempts at interspecific hybrid- 
ization among the species listed in Table 2 uni- 
formly failed. 


MORPHOLOGY AND ANATOMY 


In this section the characters that are useful in 
delimiting Oenothera canescens, O. dissecta, and 
O. havardii and those that are critical in the eval- 
uation of relationships will be discussed. Careful 
comparison of a wide array of characters is es- 
sential in any attempt to evaluate the relation- 
ships of these isolated species to each other and 
to the rest of the genus. 

Habit. All three species begin growth as a 
rosette, as typical in Oenothera. The rosette leaves 
are normally quickly lost, but in O. canescens 


they are somewhat persistent. Plants of all three 
species form clumps of sprawling or decumbent 
stems. In O. havardii, and to some extent also 
in O. dissecta, the stems often twine among other 
grasses and herbs. Plants of O. canescens tend to 
form clumps up to 50 cm across from adventi- 
tious shoots from lateral roots. Both O. havardii 
and O. dissecta also have the ability to form 
adventitious shoots, but the above-ground leafy 
portion dies back during the dry season. When 
the rains return, numerous new shoots sprout 
from the roots. Consequently, they do not form 
clumps. In fact, this is the principal means of 
reproduction in these two species; both produce 
few capsules. 

Leaves. The three species have rather similar 
leaves (Figs. 1-7), ranging from lanceolate to lin- 
ear. In general, the rosette leaves in all three 
species (e.g., Fig. 7) are larger and have fewer 


1 c EM a m л”. жт. жи 


1984] 


and more shallow teeth than the cauline leaves. 


5, 6) has pinnately lobed to sinuate-dentate leaves 
1-5 cm long, whereas O. dissecta has mostly ir- 
regularly pinnatifid leaves with linear-oblong to 
linear lobes, the blades 2—8 cm long (Fig. 3) or 
the vite ones sometimes irregularly pinnately 
lobed (Fig. 4). Oenothera canescens (Figs. 1, 2) 
has тери to subentire or rarely ser- 
rate margins and blades mostly 0.6-1.5 cm long. 

Pubescence. These three species typically have 
only one hair type, rather than two or three as 
м common in many other species of Cain we 


Oenothera in Want et al. (1985). All ie 
species are predominantly strigillose, and the hairs 
are typically 0.1—0.3 mm long. In Oenothera dis- 
secta, the hairs are rarely to 0.4 mm, whereas in 
О. canescens they typically are 0.4-0.6 mm long, 
or rarely to mm. Oenothera dissecta also is 
occasionally өг н hirsute only on the mar- 
gins and veins of the leaves. The hairs of this 
pubescence type are mostly straight with slightly 
broadened bases and аге 0.6-1.5 mm long. Both 
the strigillose and hirsute types are similar in 
morphology and length to those same types in 
many other sections of the genus. 

Buds. The buds of all three species are erect. 
Oenothera havardii and O. canescens both lack 
free sepal tips, while in O. canescens they may 
occasionally be present and are 0.2-0.3 mm long. 
In contrast, O. uel has conspicuous free se- 
pal tips 1-6 mm 

The buds of all · three species split along one 
suture and are reflexed to one side as a u 
although those of O. canescens occasionally sali 
along two sutures and the sepals are reflexed in 
pairs. Similar patterns of anthesis are common 
ш several sections of the genus. The buds of О. 
havardii are unique in that they are often some- 

isted. 


= 


. Both Oenothera havardii and О. 
dissecta have one to occasionally several flowers 
Opening per day near sunset, the common flow- 
ering pattern for the genus, especially for the 
hawkmoth-pollinated species. Oenothera havar- 
dii is pollinated by Hyles lineata (Fabricius) ac- 
cording to Gregory (1963, 1964). СЕ pe 


iting flowers of this species in Zacatecas, Mexico 
(Wagner & Solomon 4217). 
In contrast to this widespread pattern, Oeno- 


WAGNER — OENOTHERA SUBG. GAUROPSIS 


1117 


TABLE 2. Voucher information for strains of Oe- 
‚1, = = 2 tal а. n | шт- 


E e 
11 а 11 } £ p 1 ж: 


іпр numbers, orai ытай oe herbarium vouchers. All 
Missouri 1 Gar 


den (MO), unless otherwise indica 


a) U.S.A., TX, Lubbock Co., 
Raven 19293 (seeds from 


O. canescens: 


Wagner 3691; CO-3. 


Mex., Durango, Breedlove 
44 134; M2088. 


a) Mex., Zacatecas, te чај & 


O. deserticola: 


О. dissecta: 


er & 
(o ina, 4224; ME x. 7A. 
c) Mex., Zacatecas, Wagner & 
sited os MEX-8. 
d) Mex., ge agi 
un 4251; MEX-9. 
a) Mex., Chihuahua, ере & 
Brown 3922; M 
b) Mex., Durango, eh & 


О. havardii: 


beara from Powell 
21 95; М1208. 

catecas, Wagner « 
ма 4226; MEX-7b. 


O. kunthiana: 


thorn 


typicall y has many fl open- 

ing per day at sunset. This specialization is per- 
haps related to a shift to pollination by noctuid 
moths (Raven, pers. comm.), which visit these 
flowers | greater abundance than hawkmoth 
pollinato 

Floral tube length is somewhat variable as is 
typical for many species of Oenothera. Those of 
O. havardii and O. dissecta fall into the typical 
range for species pollinated by short-tongued 
hawkmoths such as Hyles; those of O. havardii 
аге (3.7—)4.5—6(—6.5) cm long; whereas those of 
Е dissecta аге somewhat shorter, (2.6—)3.5—4.2 

m long. The floral tubes of O. canescens are 

denies ia (0.8—)1-1.5(-1.7) cm long, 

which presumably is related to visitation by the 
shorter-tongued noctuid moths. 

Each of the three species has petals of a dif- 
ferent color. мерне havardii has lemon = 
Ow petals, w chis the p 
for the genus. С contrast, О. dissecta has white 


1118 ANNALS OF THE MISSOURI BOTANICAL GARDEN [Vou. 71 


1 2 T3 0 
4 
3 
9 
wanes 
7 
6 
5 
10 
1 ст 
По о У 
FIGURES 1-13. Leaves, р‹ 1а1 d capsul f O , O. dissecta, and O. havardii. 1-7. Leaves 
1, 2, O. canescens, Sedgwick Co., Kansas, Stephens 55690 (KANU).—3, 4. O. dissecta, Mexico, Schumann 531 
(G 5-7. Two cauline leaves and one basal (7) of O. havardii, Chihuah xico, Wagner & Brown 3922 
(M 8 nescens, 5 Stephens 55690.—9. O. dissecta, Schumann 531.—10. O. havardii, Wag- 


nescens, Cheyenne Co., Colorado, Wagner 3691 (MO).— 12. 


L 
— San Luis Potosí, Mexico, Parry & Palmer 249 (BM).—13. O. havardii, Chihuahua, Mexico, Pringle 
146 (VT). 


petals, similar to those of the presumably related 
species, O. tetraptera and O. kunthiana (sect. 
Hartmannia). Apparently white petals have also 
evolved independently in the common ancestor 
of sect. Pachylophus (five species), in O. muelleri 


Munz and O. tubifera Sér. of an undescribed re- 
lated section, in both species of sect. Kleinia, and 
in O. centauriifolia Spach and O. acaulis Cav. 
of sect. Lavauxia. Oenothera canescens is unique 
in having petals that are pink or white and 


1984] 


WAGNER — OENOTHERA SUBG. GAUROPSIS 


1119 


streaked or flecked with red, a pattern possibly 
related to the shift in pollinators in this species. 


genus, (1.5—)2—4 cm long, whereas those of О. 
canescens are rather smaller, (0.8—)1—1.7 cm long. 
In contrast, the petals of 0. пахамі агр elliptic 


d only 


with events species of sect. Oenothera subsect, 


О. havardii are (1.8—)2.1—3(-3.2) cm long. 

The red anthers of Oenothera havardii are 
unique in the genus. It should be noted, however, 
that those of О. canescens often have a red lon- 
gitudinal stripe. With these exceptions, no other 
species of Oenothera is known to have any red 
in its anthers. 

Capsules in this group, as is typical 
for the genus, provide good diagnostic characters 
for identification and analysis of relationships. 
Within sections there is usually a degree of 
similarity in the capsule features among the 
species. However, the capsules of these three 
species differ in texture, shape, ornamentation of 
the margins of the valves, apex, and degree of 
dehiscence. 

Both Oenothera havardii and O. dissecta pro- 
duce relatively few capsules, and seem to repro- 
duce primarily by vegetative means. Although 
O. canescens also reproduces well vegetatively, 
it also produces large numbers of capsules. 

The capsule features of Oenothera canescens 
and O. havardii are clearly s 
in the genus. The CREE of d havardii а are 


ALL aU УУ woody i 


and ha . bx 


h valve. 
They are oblong-ovoid to ovoid, 8-13(-16) mm 
long, have short, blunt sterile beaks 2-3 mm long, 
and sharply angled valves. At maturity they are 
tardily dehiscent for about У the length of the 


that are also very hard at maturity, o 
9-12(-14) mm long, and abruptly constricted to 
а Conspicuous sterile beak mostly (2—)3— 
long. The margins of the valves ug narrow 
wings 0.8-1.5 mm wide running the entire length 
ofthe capsule. At maturity they are indehiscent, 
à feature that is unique in the genus and is most 
closely approached by O. havardii. 
In contrast, the capsules of Oenothera dissecta 
are hard and leathery rather than woody. They 


are ovoid to narrowly ovoid, (9—)13—20 mm long, 

d abruptly tricted to a sterile beak 2-6 mm 
long. The valves have a median ridge, although 
it is not as conspicuous as that in O. havardii, 
and the margins of the valves have triangular 
wings 2-2.5 mm wide that extend the length of 
the capsule. These capsule features of O. dissecta 
are rather similar to those of the capsules of O. 
tetraptera and O. kunthiana in sect. Hartman- 
nia. Oenothera dissecta further shares with the 
species of sects. Hartmannia and Kneiffia cap- 
sules that dehisce ca. Уз their length and have a 
sterile, basal portion that is pedicel-like. This 
stipe is 1-4 mm long in O. dissecta, whereas it 
is much longer in species of sects. Hartmannia 
and Kneiffia 

Seeds. Seed features have long been em- 
ployed as a principal consideration in the delim- 
itation of infrageneric groupings in Oenothera 
(Spach, 1835a, 1835b; Raimann, 1893; M 


tinguished his subgenera of Oenothera largely on 
seed and capsule сауне Therefore, it was pnt 
ical to examine in 

features of the seeds of Oenothera havardii, O. 
dissecta, and O. canescens in order to evaluate 
their proper placement and relationship to one 
another. Comparison of the gross features of the 
seeds of these species is summarized in Table 3. 
нше ES "Spo ee о 


of the three species based оп its seed characters. 
Both seed shape and the nonpersistence of the 
seeds on the placenta at maturity, however, are 
shared with O. canescens. In all other features 
the seeds of O. dissecta and O. canescens are 
essentially identical. Moreover, most of these 
characters are shared not only between these two 
species but also with the species of sects. Hart- 
mannia and Kneiffia. 
T 4 i features of the 
testa of these species based on a recent genus- 
wide study of the anatomical features of seeds 
(Tobe et al., unpubl. data). As with the external 
seed characters, the anatomical features of Oe- 
nothera havardii are clearly plein Like- 
wise, O. dissecta and O. canescens uall 
identical in their structure of the testa. They only 
differ in that the exotesta is much thicker in 
canescens. In fact, the exotestal cell thickness of 
O. canescens is the greatest in the genus. In sum- 
mary, comparison of the seed features of these 
species clearly demonstrates that Oenothera ha- 
vardii is different than the other two species and 


з алу т 


1120 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


TABLE 3. Comparison of seed features of О. havardii, О. dissecta, and О. canescens. 


Seeds O. havardii О. dissecta O. canescens 
# rows/locule 1-2 indefinite rows, reduced to 2-4 
one at maturity 

#/capsule 30-60 100-130? 50-100 

Shape asymmetrically cuneiform ovoid, obscurely angled asymmetrically cuneiform, 
to rhombic, angl angled 

Color yellowish green with pur- light brown light brown to brown, dark 
ple spots to purplish spot at distal end and 
brown micropyle 

Size (mm) 2-2.5(—3.3) by 1.2-1.5 1.5 by 0.6-0.8 1.2-1.5 by 0.4-0.5 

Surface distal wing, raised ridge, smooth and glossy, ob- smooth and glossy, ob- 


beaded 


Attachment to readily detaches 
placenta 


scurely reticulate 
persistent 


scurely reticulate 
readily detaches 


that O. dissecta and O. canescens share nearly 
all features, differing only modally in others. 


DISCUSSION 


The morphological and anatomical data gath- 
ered in this study clearly demonstrate that Oe- 
nothera havardii is not closely allied with either 
O. dissecta or O. canescens, and that it should 
not be included in the same section with them. 
In fact, it is not closely related to any other species 
in the genus, and therefore it is placed here in a 
new monotypic section, sect. Paradoxus, de- 
scribed below. Oenothera havardii possesses a 
number of unique derived characters including 
red anthers, twisted buds, and distinctively an- 
gled capsules, each valve with a prominent me- 
dian ridge. Closely related groups of species in 


Oenothera (i.e., species of a single section) gen- 
erally share similar capsule characters, and the 
fact that O. havardii has capsules unique for the 
genus argues for giving it sectional status. In fur- 
ther support of this, О. havardii possesses certain 
characters that in combination set it apart from 
other species of the genus, and especially from 
O. canescens and O. dissecta. These characters 
include the elliptic to oblanceolate yellow petals; 
seeds in 1—2 rows per locule; seed shape, size, 
and color; and mesotesta 2—5 cells thick, with 
sclerotic pitted walls and the seed surface with a 
beaded appearance. Retained primitive features 
of O. havardii include yellow petals; hawkmoth 
pollination; seeds that readily detach from the 
placenta; mesotesta 2—5 cell layers in thickness, 
the cells sclerotic and pitted; and capsules that 
dehisce ca. Уз their length. 


TABLE 4. Anatomical features of the testa of О. havardii, О. dissecta, and O. canescens. 


O. havardii 

Endotesta 

Thickness (um) 10.6-12.7 

Cell shape radially flattened 

Cell-wall inner w 

thickenings 

Mesotesta 

Thickness (cell-layers) 2-5 

Cell type sclerotic, pitted 
Exotesta 

Thickness (um) 67.6–99.3 

Cell shape radially elongated, 

papilla-like 


O. dissecta O. canescens 

5.3—6.3 .2—5. 
radially flattened radially flattened 
inner wall i 

0 
crushed crushed 
46.5-59.2 74—152 
radially elongated, radially elongated, 

pillar-like pillar-like 


1984] 


Certain characters that Oenothera havardii 
shares with other species of the genus appear to 
represent convergent evolution. The leaf size and 


two species, including the reduction of leaf size, 
could merely be the result of convergence related 
to their occurrence in xeric desert habitats. El- 
liptic to oblanceolate petals, another derived fea- 


pears very likely that this shape has evolved in- 
dependently in both groups, since they have little 
else in common. 

The seeds of Oenothera havardii are similar in 
a number of ways to those of species of sect. 
Lavauxia. The cuneiform seeds of O. havardii 
with a raised ridge, small distal wing, e and: beaded 


of sect. Lavauxia, e iam ithe North American 
members. Seed size is also similar. Moreover, 

th O. havardii and species of sect. Lavauxia 
share similar exotesta cell shape and have thick- 
enings only on the inner wall of the endotesta 
(Tobe et al., unpubl. data). This type of endo- 
testal cell-wall thickening, however, is found in 
a large number of species in the genus distributed 
in several sections. The unique similarities be- 
tween the seeds of O. havardii and those of sect. 
Lavauxia thus are restricted to their size and 
external morphology. Because of their exposure 
to the environment, external features of seeds 
are presumably much more subject to adaptive 
change than are the internal ones. Therefore, it 
is difficult to suggest any close relationship be- 
tween sect. Lavauxia and O. havardii since they 
differ in most respects except in the seed features 
listed above. On the other hand, the anatomical 


inner walls thickened, and greatly enlarged ex- 
Otestal cells, clearly ally it with that part of the 
8enus including sects. Anogra, Gauropsis, Hart- 
mannia, Kneiffia, Lavauxia, and Xylopleurum 
(Tobe et al., unpubl. data). 
The remaining two species, Oenothera canes- 
ны v» O. dissecta, are not particularly closely 
ate t y fet th the 
to each other denm уво 15 би апу other species. 
They are related to the same group of sections 


УЗАК 


WAGNER— OENOTHERA SUBG. GAUROPSIS 


1121 


AS do | 1 L rD L L "iil 1+1 L, +1 
©" 


аге more closely related to them than О. ha- 
vardii. Furthermore, they are most closely re- 
lated to sects. Hartmannia, Kneiffia, and Xylo- 
pleurum, based on a number of common 

capsules, seeds clus- 
tered in each locule, and similar seed size. Oe- 
nothera dissecta shares even more characters with 
these sections, including seeds persistent on the 


2 


acen nta, wings 
and a sterile, basal | part of the capsule only 1-4 
mm long, which is typically much longer in the 
other sections. Oenothera dissecta further shares 
white petals with О. tetraptera Cav. and O. ve 


50 
has suborbicular to elliptic, glabrous ds 
that are very similar to those of O. kunthiana 
and O. rosea L'Hér. ex Ait. of the same section. 
The full distribution of this cotyledon type, how- 
ever, is not presently known. These characters 
appear to be derived ones and suggest a shared 
common ancestor ар sects. Gauropsis, 
Hartmannia, Kneiffia, and Xylopleurum. Sect. 
Gauropsis probably is related most closely to O. 
tetraptera and O. kunthiana. This relationship 
has been suggested in dic past when Rose (1905) 
included O. dissecta in sect. Hartmannia. 
they are related to species ж sect. 

Hartmannia, Oenothera dissecta and O. c 

cens are clearly specialized and therefore саа 
be placed іп an adjacent section. То include them 
in sect. Hartmannia would make this section 
much more heterogeneous than it is at present 
and more so than many other sections of the 
genus. The principal unique derived features of 


testal cells. Vegetative reproduction by adven- 
titious shoots from lateral roots also distinguish- 
es these two species from sect. Hartmannia, 
although it is probably a retained primitive fea- 
ture. Both species are individually specialized in 
a number of ways that set them apart from other 
members of the genus, but especially from sect. 
Hartmannia. Oenothera dissecta appears to be 
entirely tetraploid and makes only fleeting ap- 


degree with O. havardii, but appears to have been 
independently derived in each. Related to this 
extensive vegetative growth is the very low seed 
production in Oenothera dissecta. nsec ca- 
nescens is even more 5 nut-like, in- 


1122 


dehiscent capsules are unique in the genus. It also 
has made a major shift in its breeding system to 
pollination by noctuid moths. Presumably relat- 
ed to this pollinator shift was the increase in the 
number of flowers, petal color change, and great 
reduction in floral tube length. In summary, O. 
dissecta and O. canescens do not fit well into any 
other section of the genus because they have cer- 
tain shared and unique specializations as well as 
similar retained primitive features. They are re- 
tained together here in sect. Gauropsis, which 
appears to be most closely allied to sect. Hart- 
mannia. This is most evident in the similarity 
of O. dissecta to O. tetraptera and O. kunthiana. 


SYSTEMATIC TREATMENT 


KEY TO THE SECTIONS OF GAUROPSIS 
AND PARADOXUS 


oe yellow, elliptic to th 
tirely red; ‘capsules t never winged, 
diem valve with a prominent median ridge; 
seed surface beaded, dull; караи 
. sect. Paradoxus 
. Petals pink, flecked with red, or completely 
white, obovate to broadly obovate or uid 
orbicular; anthers yellow or sometimes with 
a red stripe; capsules narrowly оа. the 
wings 1-2. 5mm wide, each valve with a low 


ara 


— 
. 


— 
- 


reticulate, appearing finely granul ular, 
glossy; Hk girme дА II. sect. Gauropsis 


I. Oenothera L. sect. Paradoxus W. L. Wagner, 
sect. nov. TYPE: O. havardii S. Wats. 
Oenothera subg. Gauropsis sensu Munz, Amer. J. Bot. 


66. 1932, pro parte. №. Amer. FI., Ser. 2, 5: 
93. 1965, pro parte. 


Herbae foliosae compactae ad decumbentes, pro- 
+: 1: т 1 A 414i A nk 


effusis, caulibus aliquando ad nodos radicantibus. 
saepe tortae, apicibus sepalorum cohaeren- 

tibus. Petala citrina, elliptica vel oblanceolata. An- 

therae rubrae. Capsula durissima, rear таоца н 

уша quoque crista mediana prominente. 

papillosa, i in loculo aque uni- vel biseriata, ee 

seminorum superpositi 


Leafy, compact to sprawling perennial herbs 
spreading by adventitious shoots from lateral 
roots, stems branched or simple, weakly erect 
becoming decumbent, often twining among 
vegetation, sometimes rooting at the nodes. 
Leaves y pinnately lobed to sinuate- 
toothed or dentate. Buds erect, the apex long- 
acuminate, often twisted, sepal tips coherent. 
Petals lemon yellow, fading orangish red, drying 
reddish purple, elliptic to oblanceolate. Sepals 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


splitting along one suture and reflexed as a unit 
to one side. Anthers red. Capsules few, very hard, 
8-15 mm long, 4-angled and with a prominent 
median ridge on each valve, tardily dehiscent for 
ca. У capsule length. Seeds in 1 row or 2 over- 
lapping rows in each locule, irregularly angled, 
the surface beaded. Self-incompatible, n = 7, 14. 


The sectional name, Paradoxus, refers to the 
obscure relationship of Oenothera havardii to the 
other species of the genus. 


1. Oenothera havardii S. Wats., Proc. Amer. 
Acad. Arts 20: 366. 1885. TvPE: Texas. Pres- 
idio Co.: Prairies near Marfa, 1,430 m, July 
1883, Havard 122 (lectotype, GH, photo 
MO; isolectotypes, CU, US; Munz, Amer. 
J. Bot. 19: 768. 1932). Hartmannia havardii 
(S. Wats.) Rose, Contr. U.S. Natl. Herb. 8: 
328. 1905 


Hartmannia palmeri сезе Contr. U.S. Natl. Herb. 8: 
329. 1905. TYPE: . Durango: near Santiago 
Papasquiaro [25*03N, 105°25'W, 1,900 m], Apr. 
and Aug. 1896, Palmer 45 (holotype, US-304795, 
photo MO; isotypes, GH, UC) 

Leafy, compact to sprawling perennial herbs, 
often producing adventitious shoots from 
spreading lateral roots, stems 5—25(—70) cm long, 
usually many-branched, sometimes simple, 
weakly erect becoming decumbent, often twining 
among vegetation, sometimes rooting at the 

nodes, canescent-strigillose, the hairs 0.1-0.3 mm 

long. Stem leaves lineuy-lnnecolate to linear, 1- 

5 cm long, 2-8 mm wide, pinnately-lobed to sin- 

uate-dentate, the lobes widely spaced, strigillose, 

sometimes more densely so along the margins, 
occasionally subglabrous; rosette leaves oblan- 
ceolate, few toothed, generally quickly decidu- 
ous, 2-5 cm long, 5-15 mm wide; petioles on 
both types 0—6 mm long. Buds erect, oblong, the 
apex long-acuminate, often twisted, sepal tips 
coherent. Flowers 1—few opening per day near 

sunset. Ovary canescent-strigillose, (7—)9—13 mm 

long, sessile. Floral tube (3.7—)4.5—6(-6.5) cm 

long, flaring to 3.6-4.1 mm at the mouth, densely 
strigillose, glabrous within. Sepals splitting along 
one suture and reflexed to one side as a unit at 

anthesis, (1.6—)1.8—2.6(—3) cm long, 1.5-2.3 mm 

wide, canescent-strigillose, the margins with a 
conspicuous reddish purple stripe. Petals lemon 
yellow, fading orangish red, drying reddish pur- 
ple, elliptic to occasionally oblanceolate, 
(1.8—)2.1-3(-3.2) cm long, (0.9—)1.2-1.5(-1.8) cm 
wide. Staminal filaments yellow, 15-18(-22) mm 


119°W 


о 50 100 200 зоо 400 


ж Oenothera canescens 
• Oenothera dissecta 


^ Oenothera havardii 


1984] WAGNER — OENOTHERA SUBG. GAUROPSIS 1123 
* 
* * 
* 
* 
ж ж 
* ~ 
$t 
33*N ~ 


FiGURE 14, Distributions of Oenothera canescens (stars), О. dissecta (dots), and О. havardii (open triangles). 


long. Anthers red, 6-13 mm long. Style (5.5-) 
= cm long; stigma lobes red, (2—)3.5— 
mm long, well elevated above the anthers at 


with a prominent broad median ridge, the mar- 
8ins of the valves sharply angled, tardily dehis- 


cent about У the capsule length. Seeds ca. 30- 
60 per capsule arranged in 1 or 2 partially over- 
lapping rows per locule, asymmetrically cunei- 
form to rhombic, often rather irregular (due to 
compression from packing arrangement), irreg- 
ularly angled, yellowish green with scattered pur- 
ple spots to sometimes purplish brown, 2-2.5 
(-3.3) mm long, 1.2-1.5 mm wide, sometimes 
with a small wing at the distal end or a raised 
ridge along one longitudinal margin, the surface 


1124 


minutely beaded. Self-incompatible. Gametic 
chromosome number, п = 7, 14. 


Distribution. Locally common in depres- 
sions, seasonally wet flats, stream banks or mar- 
gins of irrigated fields, sandy or clay soils, often 
growing among tufted grasses like Sporobolus 
wrightii Scribn., primarily in the Chihuahuan 
desert from Marfa (Presidio Co.) and Alpine 
(Brewster Co.), Texas, Cochise Co., Arizona, 
south to F. I. Madero, southeastern Durango, 
Mexico and Juan Aldana, Zacatecas, Mexico, 
1,300-2,000 m. Flowering from April to Octo- 
ber. Figure 14. 


Additional ec examined. МЕХ 
CHIHUAHUA: 5 mi. S of [Rancho feet Gallegos ai 
Hwy. 45, م‎ 15732 (DS); 10 mi. S of Monte- 
zuma on Hwy. 45, Dwyer 14157 (MO); 5 mi. E of 
Allende turnoff on Hwy. 159 from Parral to Camargo, 
Freytag & Baxter M64 (MO); 21.2 mi. SW of El Mor- 

, Lehto & Broome L22870 (ASU, МО); 5 of cd. 
Guerrero, са. 28°33'N, 107°30’W, McGill et al. 8363 
(ASU); Basuchil, 28°30'N, 107°24’W, Mexia 2544 (Е, 
GH, MICH, MO, NY, PH, POM, UC, US); vic. of 
Aldama, 28°30'N, 106°34’W, Palmer 252 (GH, NY, 
US); Valle del Rosario, 27?19'N, 106?18'W, Penning- 
ton 367 (TEX); Chihuahua, 28?38'N, 106*05' W, 1887, 
Pringle s.n. (MEXU); near Chihuahua, near 28?38'N, 
106°05'W, ‘Pringle 1146 (GH, VT); 15 km S of Esco- 
billas, near 28°49'N, 104°06’W, Stewart 2360 (СН); 5 

mi. E of cd. Jiménez, near 27°08’N, 104*54"W, Wagner 
& Brown 3922 (MO), White 2137 (MICH). DURANGO: 
on rd. to Juan Aldama, near 24?19'N, 103?21"W, Mol- 
denke 1591 (DS); Tepehuanes, 25°21'N, 105°44'W, 
Palmer 301 (F, GH, MO, NY, UC, 

uadalupe Victoria along Hwy. 
104°07'W, Wagner & Brown 3935 (МО); 1.7 mi. NE 
of F. I. Madero, 24?23'N, 104°19’W, Wagner & Sol- 
omon rs m parie (MO), vic. of cd. [Guadalupe] 
Victoria, 34—38 mi. NE of Durango, 24°27'N, 10407" W, 
Water & Wallis 13348 (ISC, OKL, RSA, SM 

: 0.5 mi. S of ieta, rd. to Franteras, ca 

3I*18'N, 109*34"W, White 3856 (MICH). deci 
STATES. ARIZONA: Cochise Co., along U.S. Hwy. 80 ca. 
3.5 mi. NE of Apache, 1962, e n. ), 
Wagner 3813 (МО); Elfrida, near Douglas, 1957, Jones 
s.n. (RSA). TEXAS: Brewster Co., Alpine, golf course, 
Sperry T1332 (TAES, US); Presidio Co., Marfa, 1936, 
Hinckley s.n. (SRSC), ae 657 (BH, F, GH, NY 
SMU), Hinckley 707 (ARIZ. 
(BH, CS, NY, RM, RSA, 
Hinckley 3477 (NY), Hinckley 350 
Orcutt s.n. (POM, US), am 14152 (SRSC); Pecos 
Co., near Leon Spring, near Fort Stockton, cde D nl 
s.n. (GH); without further кошу, Smith s. 


Oenothera ande: sometimes occurs in hab- 
itats similar ose of O. dissecta, and at the 
southern end үг, its range, northeast of F. I. Ma- 
dero, Durango, Mexico (Wagner & Solomon 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


4318), it grows together with it. They coexist here 
without any signs of hybridization. 


II. Oenothera L. sect. Gauropsis (Torrey & 
Frém.) W. L. Wagner, comb. & stat. nov. 
Oenothera L. sect. Euoenothera (Torrey & 
A. Gray) Torrey & Frém. subsect. Gauropsis 
Torrey & Frém. in Frém., Rep. Exped. Rocky 
Mts. 315. 1845. TYPE: O. canescens Torrey 
& Frém. Gauropsis (Torrey & Frém.) Cock- 
erell, Bot. Gaz. (Crawfordsville) 30: 351. 
1900, non Presl, Epimel. Bot. 219. 1851 
[1849] 

Gaurella Small, Bull. Torrey Bot. Club 23: 183. 1896. 
TYPE: G. guttulata (Geyer ex Hook.) Small, nom. 
illeg. = Oenothera canescens Torrey & Frém. 


Leafy, bushy to sprawling or compact peren- 
nial herbs, spreading by adventitious shoots from 
lateral roots, stems simple to branched, decum- 
bent to ascending. Leaves lanceolate to linear- 
lanceolate in outline, strigillose, rarely also 
sparsely hirsute, basal leaves often oblanceolate, 
petioles 0–1.5 cm long. Buds erect, with or with- 
out free sepal tips. Petals pink and streaked or 
flecked with red, to white, fading purple to pink, 
drying purple. Capsules ovoid, constricted to a 
sterile beak, the valves with narrow wings 1-2.5 
mm wide. Seeds in 2—4 irregular rows (or in О. 
dissecta 1 row at maturity by abortion), asym- 
metrically cuneiform to ovoid or oblanceoloid, 

angled, glossy, obscurely reticulate, appearing 
finely granular. Self-compatible. Gametic chro- 
mosome numbers, n = 7, 14. 


KEY TO THE SPECIES OF SECT. GAUROPSIS 


1. Petals white, fading pink, drying purple, 
(15-)20-40 mm long; ове 20-80 mm long, 
irregularly pinnatifid, the basal ones some- 
times merely dentate; capsules (9-)1 3-20 mm 
long, dehiscing ca. !^ the capsule > сар- 

sule wings 2-2.5 mm wide; Mexi 

lis TT 2. O. dissecta 

1". Petals pink flecked with red, fading and drying 
bright purple, (8-)10-17 mm long; leaves 
I eo mm long, sinuate-denticulate 

о subentire; capsules (7 —)9—12(—14) mm long, 
нч capsule wings 0.8-1. i mm wide; 
High Plains, U.S.A. . O. canescens 


2. Oenothera dissecta A. Gray ex S. Wats., Proc. 
Amer. Acad. Arts 17: 357. 1882. TYPE: Mex- 
ico. San Luis Potosí: sandy localities near 
San Luis Potosí [1,850 m], 1876, Schaffner 
168 (lectotype, GH, photo MO; isolecto- 
type, PH; Munz, Amer. J. Bot. 19: 767. 


| 
| 


1984] 


1932). Megapterium dissectum (A. Gray ex 
S. Wats.) Small, Bull. Torrey Bot. Club 23: 
184. 1896. Hartmannia dissecta (A. Gray 
ex S. Wats.) Rose, Contr. U.S. Natl. Herb. 
8: 328. 1905. 


Leafy, compact to sprawling perennial herbs, 
producing adventitious shoots from spreading 
lateral roots, stems simple to branched, 0.2-30 
(-80) cm long, weakly erect becoming decum- 
bent, older stems woody, strigillose, the hairs 
0.1-0.3(-0.4) mm long. Stem leaves lanceolate, 
2-8 cm long, 0.7-1.5 cm wide, irregularly pin- 
natifid, the lobes linear-oblong to linear, sparsely 
to densely strigillose, the hairs evenly distribut- 
ed, rarely more dense along veins and margins, 
sometimes also sparsely hirsute, these hairs 0.6— 
1,5 mm long and confined to veins and margins; 
rosette leaves oblanceolate, 2-6 mm long, 1-1.5 
cm wide, less divided than the stem leaves, den- 
tate, or pinnately lobed or with oblong lobes, 
usually deciduous before flowering; petioles on 
all leaves 0-1.5 cm long. Buds erect, oblong-lan- 
ceolate, with free sepal tips 1-6 mm long. Flow- 
ers one rarely more per stem opening per day 
near sunset. Ovary 1 1—16(—18) mm long, densely 
strigillose, sessile. Floral tube (2.6—)3.5-4.2 ст 
long, flaring to 3-6 mm at the mouth, densely 
strigillose, glabrous within. Sepals splitting along 
one suture and reflexed to one side as a unit at 
anthesis, 1.8-3.5 cm long, 2-3 mm wide, stri- 
gillose, the margins with a conspicuous purple 


8 

ovate to пере orbicular, (1.5—)2 
(1.4-)1.7-3.6 cm wide. Staminal filaments 10- 
17 mm long. бес ы yellow, (6–)8—11 mm long. 
Style (4.4-)4.7-7 cm long; stigma lobes (3-)5—6 
mm long, well elevated above the anthers at an- 
thesis. Capsules few, hard and leathery at ma- 
turity, ovoid to narrowly ovoid, (913-20 mm 
long, 3-5 mm diam. (excluding wings), the base 
cuneate, sometimes somewhat twisted, abruptly 
constricted to a sterile beak 2—6 mm long, with 
free tips ca. 0.5 mm long, the valves with a me- 
dian ridge, the margins of the valves with a wing 
2-2.5 mm wide extending the length of the cap- 
Sule, usually widest above the middle, tapering 
to a pedicel-like, sterile basal portion 1-4 mm 

long, dehiscing ca. % the capsule length. Seeds 


in mature capsules), narrowly ovoid, obscurely 
angled, light brown, ca. 1.5 mm long, ca. 0.6– 


WAGNER — OENOTHERA SUBG. GAUROPSIS 


1125 


0.8 mm wide, the surface glossy, obscurely re- 
ticulate, appearing finel nular, rather persis- 
tent on the placenta. Self-compatible, pe out- 
crossing. Mi 8. 


Distribution. Locally common in clay or 
sandy soils of arroyo banks or sometimes open 
flats, Acacia and Opuntia grasslands, Larrea 
scrub, in the Chihuahuan Desert from the vicin- 
ity of F. I. Madero, southeastern Durango to Za- 
catecas as far north as Concepción del Oro, 
southwest San Luis Potosí and vicinity of Ojue- 
los, northern Jalisco, 1,800-2,400 m. Flowering 
from May to September. Figure 14 


specimens examined. МЕХ 
DURANGO: vic. of ере ee ми T W, pulo 
er 966 (О d L 7 mi. of Fran I. Madero on Ln 
of Durango, ON. 10419" W, Wagne 
Solomon. 4318, pro parte 


r 


8, 

16984 (MEXU, RSA, US). SAN 
an Luis Potosí, 22°09’ N, 100*59"W, Barri s.n. 
(ON Pad eet 9(BH, ВМ, Е, Е, С, GH. MO, 
Н, US, УТ), есен. 6157 (ENCB), Schaffner 
52 ФМ .Ch МҮ. P US) 8 e Laguna А 
ee 22°17'N, 10052 W, пен 6325 (ЕМСВ, 
XU, RSA); 22 mi. МЕ о Luis Potosi, Straw 
1 pried 1430 cE MEXU, RSA); without further 
locality, 1891, Nirlen s.n. (P). ZACATECAS: 23 mi. S of 
Oro along Hwy. 54, pas a 6243 
Wagner & Brown 3980 (MO); 6 mi. WSW of 
; 0.9 mi. E of jct. Rt. 
tecas, Wagner & Solomon 4217 
MO); 7.4 m LE of Guadalupe on Rt. 45-49, Wagner 

& Solomon 4224 (MO); 7.5 mi. N of jct. Hwy. 45-4 
on Hwy. 45, Wagner & Solomon 4237 (MO); 8 mi. W 
of rd. to Sambrerete on Hwy. 45, Wagner & Solomon 
4251 (MO); without further locality, Schucé s.n. (RSA); 

aral, Schumann 531 (BM, Е, GH, US). 


3. Oenothera canescens Torrey & Frém 
Det Rep. Exped. Rocky Mts. 315. 1845. 
bably Colorado. Weld Co. or Wy- 
Ош. Morgan Co., along the South Platte 
River, “Upper waters of the Platte," 1-4 
July 1843, Fremont s.n. (holotype, NY, pho- 
to MO; isotype, GH). Locality and date re- 
constructed with aid of McKelvey (1955: 
845, 848). Megapterium canescens (Torrey 
& Frém.) Britton, Mem. Torrey Bot. Club 
5: 235. 1894. Gauropsis canescens (Torrey 
& Frém.) Cockerell, Bot. . (Crawfords- 
ville) 30: 351. 1900, nom. pa адра 
сапеѕсепѕ (Тоттеу & Егёт.) А. № 
Gaz. (Crawfordsville) 47: 437. 19 s ~ 
in Coult. & А. Nels., New Man. Bot. Cent. 
Rocky Mts. 341. 22 Dec. 1909. 


1126 


pulse мр раје де ара ex Hook., London J. Bot. 
222. 1847 ka or south- 


Wyoming county where 
collected), “Plains of the upper Platte т, June 
1843, Geyer 178 (holotype, K not seen; isotypes, 
BM, photo MO, С). Locality reconstructed with 
aid of McKelvey (1955: 777). Gaurella guttulata 


fordsville) 30: 351. 1900, nom. illeg. 


Low, bushy perennial herbs with a subterra- 
nean to superficial caudex, forming clumps 10– 
50 cm across by adventitious shoots from lateral 
roots, densely strigillose throughout, the hairs 
(0.1-)0.4—0.6(-0.8) mm long, the stems many- 
branched from the base, decumbent to ascend- 
ing, (10—)15—25(—38) cm long. Leaves canescent, 
lanceolate to linear, especially the smaller leaves, 
(3-)6-15(-25) mm long, (0.5—)1.5—4(—-6) mm 
wide, sinuate-denticulate to subentire, acute at 
the apex, cuneate at the base in the broader leaves, 
subsessile. Buds erect, lance-elliptic to lanceolate 
in outline, the apex long-acuminate, without free 
tips or rarely with free tips 0.2-0.3 mm long. 
Flowers many opening per day near sunset. Ovary 

escent, 5-10 mm long, sessile. Floral tube 
(8—)10—15(—17) mm long, flaring to ca. 2 mm at 
the mouth, glabrous within. Sepals splitting along 
one suture and reflexed to one side as a unit at 
anthesis, sometimes reflexed in pairs, (7—)8-12 
mm long, (1.3—)1.5-2.2 mm wide, canescent, the 
margins with a reddish purple stripe, sometimes 
flecked with reddish purple splotches especially 
toward the base. Petals pink, rarely white, 
streaked or flecked with red, fading bright purple, 
obovate, (6.8—)1—1.7 cm long, (0.5—)0.6-1(-1.2) 
cm wide. Staminal filaments pale yellow, 6—8 
mm long. Anthers yellow, often with a red lon- 
gitudinal stripe, 3-6 mm long. Style (16-22-27 
mm long; stigma lobes 1.5-3(-4) mm long, well 
elevated above the anthers at anthesis. Capsule 
ovoid, (7-)9-12(-14) mm long, 2-4 mm diam. 
(excluding wings), the base cuneate to truncate 
and slightly asymmetrical, abruptly constricted 
toa DM sterile beak (2—)3—4.5 mm long, 
ery hard at maturity, the margins of 
the valves Мч a narrow wing 0.8-1.5 mm wide, 


ule, asym- 
metrically cuneiform or oblanceoloid (probably 
resulting from compression from adjacent seeds 
during development), angled, light brown to 
brown with dark spots at the distal end and at 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


the micropyle, 1.2-1.5 mm long, 0.4-0.5 mm 
wide, the surface glossy, obscurely reticulate, ap- 
pearing finely granular. Self-compatible, but out- 
crossing. Gametic chromosome number, n = 7 


Distribution. Locally common in prairie 
depressions, playas, margins of ditches, and oth- 
er places with temporary water in the High Plains 
region from Goshen Co., Wyoming, southeast to 
Hayes Co., Nebraska, south through eastern Col- 
orado, the eastern tier of counties in New Mex- 
ico, western Kansas, and to Garza and Dawson 
Cos. in the Texas Panhandle; also disjunct pop- 
ulations from Stafford, Sedgwick, and Chautau- 
qua Cos., Kansas, (430–)750—1,700 m. Flower- 
ing from May to July, then sporadically through 
September. Figure 14. 


Representative specimens examined. UNITED 
. COLORA Kit Car- 


mi. SW of Limon, Ownbey 1303 
MO, MONT, NY, RM, UC, UTC, WS); Kiowa Co., 
0. 15 ті. W of Brandom, Stephens & Brooks 22705 
(DS, KANU); Kit Carson Co., Burlington, Lemaire 
195 0 (NEB); Logan Co., 0.5 mi. E of Fleming, Stephens 
5 А 


of J ulesburg, Stephens 55690 (KANU); W 
Co., 4 mi. N & 15 mi. E of Elba, ر‎ 56128 
(KANU, NY); Weld Co., 10 mi. SE of Grover, Dodds 
2125 (COLO, ЕМ). Kansas: Chautauqua Co., without 


further vg 1897, Hitchcock s.n. (KSC); Cheyenne 
Co, 1.5m of Whee ler, пене gigs (KANU); 
Clark Co., ri mi. W, 4 mi. N & 1 mi. E of Ashland, 


SW corner of Little Bean "Stephens 843 ^ (KANU); 
Ellis Co., without further locality, Smyth 2598 cud 
Finney Co., Buffalo Wallows, Hitchcock 162 (KS 
MO, NMC, NY, P, RM, US, X Gray 
NE of Montezuma, Stephens 
; Greely Co., Tri ге n yin (KSC, UC); 
Hamilton Co., Syra vag ads 143 (KSC, MO, 
US); Kearney Co., eae Lakin, 1928, Howe s.n. Ву 
Lane Co., 0.5 пи. У & 2.5 mi. S of Amy, Stephens 
55002 (KANU); Lincoln Co., without further locality, 
1902, Bergman s.n. (NDA); Meade Co., 5 mi. E of 
Meade, Horr 3375 (KANU); Norton Con without fur- 
ther locality, 1892, Smyth s.n. (KSC); Scott Co., Scott 
; Sedgwic 


, 1892, Carleton s.n. (ILL, KSC); . 
without further locality, 1931, Weber s.n. (KSC); Sher- 
man Co., Goodland, 1892, Smyth s.n. ( 

UMO); Stafford Co., without further locality, 1885, 
Kellerman s.n. (F, MICH, MIN, MO, NY, OS, UMO, 
US); Stevens Co., golf course at Hugoton, Shildneck 
C-4109 qus. Wichita Con 11. 5 mi. 5 of Leoti, Ste- 
46 (KANU). N 


rom ner Co., 20 mi. 
= ar Porter & he 875 1 (DS, GH, MIN, 
SC, RM, RSA, TEX, UC); Chase Co., near Lamar, 


Tolstead 411253 (ISC, MO, NEB); Cheyenne Co., 
Cheyenne, 1904, Fawcett s.n. (NEB); Deuel Co., 13 


1127 


1984] 


mi. E of Chappell, Stephens 45578 (KANU, o 
Hayes Co., 20 mi. W of s Center, Tolst 


BPE : 
Folsom, 1951, a s.n. (UNM). OKLAHOMA: Bea- 

Co., 12.5 ті. W of Forgan, Stratton 1338 (OKL 
OKLA); Texas pile Hitchland Playa near Hitchland, 
1949, Penfound s.n. (OKLA). Texas: Armstrong Co., 
8.75 mi. N of Paloduro, Cory 13464 (ARIZ, POM). 
Eco Do.. Ру mi. NW of Baileyboro, Rosson 844 (SAT, 
WTS); Briscoe Co., 1.2 mi. E of Silverton, White- 
E 9991 (SMU); Carson Co., 5 mi. N of Panhandle, 
Shinners 8109 (SMU); Castro Co. , lake S of Dimmitt, 
ork s oe we 425 (OKLA MU, T ochran 
E. i. S of Muleshoe, Muleshoe Wildlife Refuge, 
Бел 80202 (КА NU); Crosby Со., jct. of farm rds. 
40 & 651, 7 mi. S of SRM Map то s.n. 


ws o., on : Е 
of Lamesa, Lundell & Liga, 165 8972 ae ES Smith 
Co., 15 mi. reford, Waller 964 
(SMU, TIG Dickens Co., 2 mi. S ‘of M McAdoo, 1965, 
E n. (GH, KSC, OKLA, TTL DUE Floyd Co. 

1 mi. à Le South Plains, Spence 39 (DS); Garza Co., S 
11.1 air mi. NW of Po: st, — 679 (OKLA, SMU 
ampa, Stephens 76343 
(KANU, NCU); Hale Co., SW of Kress, 6.6 mi. S on 
Hwy. 87 & 4.1 mi. W, Whitehouse 9932 (MICH, NY, 
SMU, UC, US); Hall Co., 1 mi. W of Turkey, Stephens 

72179 чи ansford Co., just rest of Hitch- 


~ 


land, Oklahom Goodman 5288 (GH, „OKL, 
TEX); Hartley Co, 8 mi. E of На, Stephen 82120 
game 3932 

of абе Ste- 
- anti € ,:0:5 ae S of Am- 

herst, Stephens 75973 (KANU, “MASS, NCU); Lub- 
ME Co., 5 mi. N of Slaton, Rowell TE ИОН, OKL, 
KLA); hed mb Co., Booker on H Wale 


Ochiltree mi. 

rryton on U.S. Hwy. 83, Wallis 4751 [o 

KLA, S Nee eee W edge of Hub, Rowell 

8634 (G Gn OKLA, UC); Potter Co., Amarillo, Rev- 

erchon 3840 (CAS, AS са LL, MIN, 'MO, NY, POM, 

US); Randall O., ca. 1 mi. N of Canyon, d cem 
(ASU, BRY, MICH, NY, WTS); Sh herman Co. 

E, 12 mi. S & 4.5 mi. E of Stratford, Stephens 92387 


(KANU). WYOMING: Goshen Со., 5 of Springer Res- 
ervoir, Luce 94 (RM). 


LITERATURE CITED 
1894. Опаргасеае. In List of Pteri- 


tivation in northeastern "North America. Mem. 
Torrey Bot. a 5: 232-236. 

DIETRICH, w. 7 [1978]. The South Ameri 
pecies of PU sect. Oenothera Рини. 
Renneria; Onagraceae). Ann. Missouri Bot. Gard. 
64: 425-626. 


BRITTON, N. L. 


. RAVEN & W. L. WAGNER. 1985. Re- 
vision of Oenothera sect. Oenothera subsect. 
Emersonia (Onagraceae). Syst. Bot. 10: (in press). 
GREGORY, D. P. 1963. Hawkmoth pollination in the 
genus Oenothera. Aliso 5: 357-384. 
1964. Hawkmoth pollination in the genus 
Oenothera. Aliso 5: 
Lewis, H. C. & M. E. Lewis. 1955. The genus Clarkia. 
Univ. Calif. Publ. Bot. 20: 241-392. 
MCKELVEY, S. D. 19 Botanical Exploration of the 
Tr PON West, Head me ld Ar- 
Plain 


boretum, Jam 

Munz, P. vu 1932. Studies in Onagraceae УШ. Тһе 
subgenera 
Oenothera. The genus Gayophytum. Amer. Т Bot. 
19: 755-778. 

1965. Onagraceae. N. Amer. Е!., Ser. 2, 5: 


sect. uin thera (Onagraceae). Syst. Bot. 4: 242- 

252. 

Rose, С. М. 1905. Studies of Mexican and Central 
LAS plants. No. 4. Contr. U.S. Natl. Herb. 


–339. 
Swati ~ 1896. Oenothera and its segregates. Bull. 
y Bot. Club 23: 167-194. 
У 18352. Histoire Жерш des Végétaux. 
–416. 


——. 1835b . Nouv. 
Ann. Mus. 

STRALEY, G. B. 1977 [1978]. Systematic Y Оепо- 
thera sect. Ki issouri 
Bot. Gard. 64: 425-626. 

WAGNER, W. L., W. KLEIN. 1985. 


R. STOCKHOUSE & 
Systematics d evolution of the сарон caes- 
onogr. 5 


J 


Bot. Missouri Bot. Gard. 12. (in ови 


SYSTEMATICS OF OSMORHIZA RAF. (APIACEAE: APIOIDEAE)! 
PORTER P. Lowry II? AND ALMUT С. JONES? 


ABSTRACT 


The genus Osmorhiza comprises ten species and two subspecies of woodland umbellifers native to 
temperate Asia and the Americas. Quantitative evaluation of nine morphological characters supports 


along with an analytical key to the subgenera, sections, species, and subspecies. Phytogeographic data 
indicate that western North America is the center of distribution and diversity, and possibly the center 
of origin for Osmorhiza, although members of the genus are found in eastern North America as well 


America observed in the ranges of O. chilensis and O. depauperata (both sect. Nudae) are most likely 


the result of long-distance dispersal by migratory birds. By contrast, the disjunct populations of these 


example of the classical eastern North American-eastern Asian pattern of disjunction. Although these 


temi g Pleistocene. Ethnobotanical evidence 
indicates that at least five species of Osmorhiza were used for medicinal purposes by native Indian 
peoples of North America. The roots and greens of two species were also consumed as food by both 
North and South American Indians. 


TAXONOMIC HISTORY С É 
for epizoochory. Plants of Osmorhiza, common- 


Osmorhiza (Apiaceae: Apioideae) is a small ly known as Sweet Cicely, may be quite abundant 
genus of perennial woodland herbs with repre- in some areas, but they rarely form uninterrupted 
sentatives in temperate Asia and the Americas. stands, even under the most favorable of con- 
Members of the genus typically flower in the ditions. 
spring, setting fruit by mid-summer. These fruits Osmorhiza was first recognized as a distinct 
(schizocarps), which are armed with retrorse genus by Rafinesque in 1818, but it was not until 
bristles in all but one species, are well adapted the following year (Rafinesque, 18192) that this 


! This paper resulted from research done by the first author for an M.S. thesis at the University of Illinois. 
We are grateful to D. A. Young for advice and suggestions. Special thanks go to L. Constance for valuable 


provided the loan of specimens, photographs of types, and/or study facilities to examine collections in situ: 


> М NN, US, UWM, WIS, WTU, and Z. This work was supported in part 
by a Sigma Xi Grant-in-Aid of Research, an Illinois Academy of Sciences Research Grant, and the Robert 
они Grant from the University of Illinois for 1978. An extensive list of i imens 
а copy ot which is on permanent deposit in MO, is available from the first author on re uest = 

2 Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166, and sicot or Di Wash- 
ington University, St. Louis, Missouri 63130. ў У UAE оон. 

з Department of Plant Biology, University of Illinois, 505 South Goodwin, Urbana, Illinois 61801. 


ANN. Missouri Bot. GARD. 71: 1128-1171. 1984. 


1984] 


name was validly published. Prior to that, spec- 
imens of Osmorhiza had been referred to three 
other genera: Chaerophyllum L. (Thunberg, 1784; 
Persoon, 1805), Myrrhis Miller (Michaux, 1803; 
Sprengel, 1813), and Scandix L. (Muhlenberg, 
1813). During the next 80 years many new species 
were described in the genus. However, it was not 
until 1888, when Coulter and Rose published 
their “Revision of North American Umbellifer- 
ae,” that an attempt was made to clarify the tax- 
onomy of Osmorhiza. Twelve years later Coulter 
and Rose (19 
of the North American E of the genus, 
recognizing 12 taxa, including three new species. 
Mathias and Constance (1944), in their review 
of the Umbelliferae for the “North American 
Flora," listed eight species and two varieties of 
Osmorhiza. 

Osmorhiza was treated for the first time on a 
world-wide basis by Constance and Shan (1948), 
who recognized the conspecificity of the North 
and South American populations now included 
in O. chilensis and O. depauperata. These au- 
thors included all the Asian populations of the 
genus under O. aristata, and described one new 


matic techniques) were not used in their study; 
they based their conclusions entirely on the ex- 
amination and comparison of herbarium speci- 
mens. 


Work on the current study was begun in 1974, 
àt which time only two eastern North American 
species, O. claytonii and O. longistylis, were con- 
sidered. Later, the scope of our work was ex- 
panded to a systematic investigation of the entire 
genus. Toward this end several approaches һауе 
been used, including (1) quantitative evaluation 
ofnine morphological characters, (2) mapping of 
each species, (3) comparative examination of 
available type material, and (4) a broad survey 
of the literature on the genus. In addition, an 
analysis of electrophoretic banding patterns of 
Water soluble seed proteins for most Osmorhiza 
Species was conducted (Lowry & Young, 1979; 
Lowry, 1980). 

In addition to the nearly 400 collections of 
Osmorhiza on deposit in ILL, approximately 


Photographs of type specimens unavailable for 
loan were received from LE and SGO. Voucher 
SPecimens for the more than 200 collections made 
by the first author are deposited in ILL, along 
With photographs of all type material examined. 


LOWRY & JONES— OSMORHIZA 


1129 


The quantitative morphological data pre- 
sented here support a revised taxonomy for Os- 
morhiza in which ten species and one subspecies 
are recognized. Two well delimited subgenera are 
distinguished, one of which is further divided 
into three sections. These conclusions are further 
supported by seed protein data (Lowry & Young, 
1979; Lowry, 1980). Phytogeographic evidence 
indicates that "tem Pone Werin is the cen- 
ter y ibly the 
center of origin for ice although mem- 
bers of the genus have migrated to and survived 
in eastern North America as well as in Asia and 
in Central and South America. Nomenclatural 
problems within the genus are dealt with, and a 
brief discussion of the ethnobotany is given. 


NOMENCLATURE 


Generic names. Species of Osmorhiza were 
originally placed in three other genera: Chaero- 
phyllum L., Myrrhis Miller, and Scandix L. In 
1818 Rafinesque published three alternative ge- 
neric names for these taxa: Washingtonia, Os- 
morhiza, and Gonatherus. These were, however, 
invalidly published under Art. 34. (а) of the “In- 
ternational Code of Botanical Nomenclature” 
(Voss et al., 1983), because they were not ac- 
cepted by the author in the original publication. 
They may also be nomina nuda because they 
appear not to meet the requirements of Art. 41.2 
of the “Code” (cf. Lowry & Jones, 1978; Lowry, 
1985). In the same year Nuttall (1818) validly 
published the name Uraspermum for this taxon. 
Rafinesque (1819a), however, rejected Urasper- 
mum Nutt., considering it too similar to (i.e., an 
incorrectly spelled later homonym of) Urosper- 
mum Scopoli, a genus of Asteraceae, and vali- 
dated the name Osmorhiza with a reference to 
the description of Uraspermum Nutt. (Lowry & 
Jones, 1977, 1978). This interpretation has been 
followed by nearly all subsequent authors, al- 
though most have incorrectly considered Rafi- 
nesque (1819b) as the first place of valid publi- 
cation for the name Osmorhiza. Uraspermum 
Nutt., however, cannot be treated as a later hom- 
onym since it is not spelled exactly like Uro- 
spermum Scopoli (cf. Art. 64.1 of the “Code”). 
Strict prince or the rules of nomenclature 
would thus ap 
ee Nutt бог the taxa “currently rec- 
ognized in Osmorhiza. In order to avoid this 
clearly undesirable change and to maintain no- 


1130 


menclatural stability, a proposal has been made 
to conserve the generic name Osmorhiza against 
Uraspermum (Lowry, 1985). 

Subgeneric names. Two subgenera are rec- 
ognized within Osmorhiza, one with nine species, 
including the type for the genus (i.e., the type of 
O. claytonii), and one with a single species, O. 
occidentalis. When O. occidentalis was first de- 
scribed it was placed in a new, monotypic genus, 
Glycosma, by Nuttall (in Torrey & Gray, 1840), 
who provided both generic and specific descrip- 
tions. Drude (in Engler & Prantl, 1897), follow- 
ing Torrey (1859), judged this species to be an 
Osmorhiza, but placed it in a separate subgenus, 
citing Nuttall’s generic name G/ycosma as the 
basionym; the correct name for this subgenus is: 
Osmorhiza subg. Glycosma (Nutt.) Drude in Engl. 
& Prantl. 

Sectional names. Three sections are recog- 
nized within Osmorhiza subg. Osmorhiza (Low- 
ry & Jones, 1979b; Lowry, 1980). Constance and 

| for all three of these: 
т Aristatae, (2) Mexicanae, and (3) Nudae, al- 
ough not validly, because none of them was 
he cien by a Latin DRIED Or r diagnosis 
or a reference to a previously ely pub- 
lished Latin description or diagnosis of the same 
taxon (cf. Arts. 32.1 and 36.1 of the “Сойе”). 
Because the section Aristatae includes the type 
of the genus, its epithet is a synonym for Os- 
morhiza sect. Osmorhiza. Constance and Shan's 
sectional names Mexicanae and Nudae are val- 
idated herein. 

Specific epithets. Rafinesque (1830: 249) 
published three new species: Osmorhiza dulcis, 
O. vilosa [sic], and O. cordata. This publication 
reads as follows: “Osmorhiza dulcis, Raf. 1817 
(Myrrhis claytoni Mx?) Sweet Sisily [sic]. Root 
fusiform, with a sweet smell and taste, near an- 
iseed [sic], edible, carminative e, expectorant, de- 
mulcent, useful for coughs with Malva, for flat- 
ulent bowels with Heracleum, Eq. to Angelica. 
Children are fond of this root, may be poisoned 
by mistaking for it, two sp. of the same genus 
or Myrrhis Auct. called Poison or Bastard Sisily 
[sic], distinctive by the roots less aromatic, fo- 
liage the same, but in O. dulcis base of the folioles 
acute, in my O. vilosa [sic] or M. longistylis ob- 
tuse, in O. cordata Raf. cordate. These last pro- 
duce, when eaten, effects similar to those of the 
virulent Umbellate . ат = place- 
ment of th 5 has been based 
solely on this reference; 0. dulcis ue O. clay- 
tonii, and О. vilosa and О. cordata under О. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Уо1. 71 


longistylis. The type specimen of О. dulcis (PH!) 
is, however, clearly a plant of О. longistylis, not 
O. claytonii as suggested by Rafinesque; O. dulcis 
is therefore a synonym of O. longistylis. The cor- 
rect placement of the names O. vilosa and O. 
cordata may be inferred from Rafinesque’s ref- 
erence itself. Osmorhiza dulcis is said to have 
more aromatic roots than O. vilosa and O. cor- 
data; the roots of O. longistylis are more aro- 
matic than those of O. claytonii (Lowry & Jones, 
1979a). Since О. vilosa is a synonym for О. Іоп- 
gistylis, by inference O. vilosa and O. cordata 
belong in synonymy under O. claytonii. Rafi- 
nesque probably confused O. claytonii and O. 
longistylis when suggesting the synonymy for his 
new names. 

Rydberg (1894) validly published the combi- 
nation Osmorhiza aristata (Thunb.) Rydb. Меаг- 
ly all subsequent authors have incorrectly attrib- 
uted this combination to Makino and Yabe (in 
Makino, 1903), however; the only apparent ex- 
ceptions are Constance (1972), Lowry and Jones 
(1979a), and Lowry (1980). 

Accurate determination of the holotype of Os- 
morhiza mexicana Griseb. was possible only with 
the kind assistance of Professor Dr. G. Wagenitz 
(GOET). According to Wagenitz (pers. comm.), 
Grisebach usually marked voucher specimens he 
considered new by placing an “m” (for mihi), 
after the new name, while other vouchers were 
marked with “Gr.” Examination of the authentic 
material from the Grisebach Herbarium at 
shows that Schaffner 37 is marked “Osmorhiza 
mexicana m" in Grisebach's hand, while two 
other specimens (Mandon 594 and Lorentz & 
Hieronymus 668) are marked “Osmorhiza mex- 
icana Gr." Thus, the Schaffner collection has been 
annotated as the holotype, whereas the other 
specimens are paratypes: 

Lectotypes are d ted here for four specific 
epithets: O. brevistylis DC., O. depauperata Phi- 
lippi, O. laxa Royle, and bis renjifoana Phi- 
lippi. There are several syntypes for each of these 
names, and extensive search in the literature has 
not revealed previous lectotypification for any of 
them. 

The name Myrrhis longistylis Torrey (1824: 
310) was published with the following type in- 
formation: “In wet meadows near Albany, New 
York. Tracy. Near Geneva, N. Y. Paine. June. 
Near Hudson, N. Y. Alsop, & c.” These speci- 
mens would by syntypes, although none of them 

been located. An authentic collection by Paine 
marked “Myrrhis n. sp.” in Torrey’s hand (at 


1 
| 


1984] 


NY) is therefore designated as the neotype for 
Myrrhis longistylis Torrey. 


ETHNOBOTANY 


Species of Osmorhiza were used in a variety 
of ways by native peoples in many parts of North 
America, and by at least one tribe in South 
America. Available information indicates that 
O. brachypoda, O. chilensis, O. claytonii, O. lon- 
gistylis, and O. occidentalis were used for me- 
dicinal purposes, while O. chilensis and probably 
O. depauperata were also consumed as food. 
Many uses of Osmorhiza by Indians of North 
America were reviewed by French (1971) 

Perhaps the most widely used species was Os- 
morhiza chilensis. In their review of the ethno- 
botany of the Karok and other Indians of north- 
ern California, Schenck and Gifford (1952: 386— 
387) reported: “Тһе root of this plant is one of 
the most important medicines. It can be dried 
and kept in the house. The medicine requires a 
formula (charm) always, but it is used for almost 
everything. The house is smoked with it, if there 
has been illness in the house. The root is thrown 
on the fire at dances. If put under the pillow at 
night, it keeps sickness away. For headache, a 
little piece of the root is chewed. If a person is 
grieving over a lost relative, medicine is made 
from the root (with formula) and the mourner is 
bathed with the medicine. A piece of the root is 
carried as protection against the ‘devil.’ In the 
Spring the young tops are eaten as greens. It is 
Very good luck to find it growing in a place where 
It has never been seen before. Georgia Orcutt [a 
local Indian woman] says this is the only herb 
that is dried and kept on hand in the house. It 
Is good for ‘everything’.” Gunther (1945) re- 
Ported that the Swinomish Indians of north- 
Western Washington chewed the roots of Os- 
morhiza brevipes (— O. chilensis) as a powerful 
love charm. She also noted that the Lummi and 
Skagit tribes of the same area did not seem to 
use Osmorhiza. Schneider (1906) indicated that 
the seeds of “O. longistylis" (certainly O. chilen- 
sis) were used by California Indians (probably 
the Paiutes) for medicinal purposes, primarily as 


She stated that “they are known for their delicate 

avor and are especially ‘appetizing because of 
their aromatic character 

Other species of Osmorhiza were used by In- 


LOWRY & JONES—OSMORHIZA 


1131 


dians of western North America as ан гет- 

edies. The Paiutes prepared а decoction from the 
roots of O. brachypoda (Schneider, 1906), and 
several tribes from both Canada and the U.S. 
also used O. (Uphof, 
1968). 

Osmorhiza longistylis was used by many peo- 
ples of the midwestern U.S. According to Smith 
(1928: 249), the Meskwaki (i.e., Fox) Indians 
used this species for a variety of medicinal pur- 
poses: “It is chiefly used as an eye remedy. It is 
horse medicine, too, and the root is grated and 
mixed with salt for distemper. When hunting, 
they fed a pony with the root and he was thus 
enabled to catch the buffalo. Specimen 5/54 of 
the Dr. Jones collection is the leaves of Osmo- 
rhiza longistylis and the bark of Gleditsia tri- 
acanthos mixed to make a tea which is drunk to 
regain flesh and strength." Gilmore (1919: 107) 
wrote: “Тће Omaha and Ponca say that horses 
were so fond of the roots of Washingtonia |lon- 
gistylis] that if one whistled to them, while hold- 
ing out the bag of roots, the horses came trotting 
up to get a taste, and so could easily be caught. 
An Omaha said that the roots were pounded up 
to make poultices to apply to boils. A Winnebago 
medicine-man reported the same treatment for 
wounds. À Pawnee said that a decoction of the 
roots was taken for weakness and general debil- 


Smith (1932: 391) indicated that the Ojibwe 
(i.e., Ojibwa) Indians apparently did not distin- 
guish between Osmorhiza longistylis and the 
closely related О. claytonii. He stated: “А tea for 
making urition easier is prepared from the 
roots. The licorice flavor of the tea is said to be 
good for a sore throat." Osmorhiza claytonii was 
used by the Menomini Indians of northern Wis- 
consin to gain weight (Smith, 1923) 

Osmorhiza was also used by Indians in south- 
ern South America. According to Mrs. Natalie 
Goodall of Harberton, Argentina (in a letter to 
Mrs. Helen Sharsmith, dated May 12, 1965, a 
copy of which was obtained from Dr. Lincoln 
Constance), Osmorhiza “was one of the three 
plants eaten by the [Yahgan] Indians besides fun- 

eowwunim [a Yahgan name] was eaten 
taw Пиве, stems, and roots, ог the roots were 
baked in the fire . My mother-in-law says 
that she often saw the Indians eating it as a child. 
Now it is hard to say, as there are only about 
four Yahgans left, two of them work in Harber- 
ton, but have forgotten their language.” It is like- 
ly that the Yahgans did not distinguish between 


Osmorh. 

Haeret (55) a 

glabrata U2) 
exica 

ер. mexicana (3n H 
ssp. бие ah 

brachypoda (3 س‎ 

chilensis (90) —0—— 

серое (70) ong 

purpurea (55) Te 

longistylis (111) 

aristata (30) ——62-— 

claytonii ten س‎ 


L 1 1 1 BEA ый МИШЕ | 
О) See о 1s 0 124 30 35 
Style length (mm) 


smorhiza 
occidentalis (44) 


ешле 


brachypoda ‹ 


chilensis (86) 
depauperata (67) 
rpurea (4) 


Jongistyli$ (28) 
aristata (27) 
c/aytonii (27) 


| SESE QUAD! Ie РЕН 
(з) 80 100 120 140 160 180 200 220 240 
Fruit indi (mm) 


FIGURES 


characters in Osmorhiza spp.— 1. Style length (mm). — 2. Stylopodium height (mm). 
) 


4. Fruit appendage length (mm). 


Osmorhiza depauperata and O. chilensis, both 
of which grow throughout southern South Amer- 
ica, often together. If they did, however, Mrs. 
Goodall's comments probably apply to O. de- 
pauperata, a specimen of which ( Y. Mexia 7925), 
collected in Tierra del Fuego, Argentina, has 
written on its label ““Awanim (Yeagan)." 

The widespread use of these plants by native 
North and South Americans would suggest that 
other Indian groups, whose ethnobotany has not 
been studied, also used species of Osmorhiza. It 
is even possible that O. aristata was used by the 
people of Asia, although no record of this has 
been found 


MORPHOLOGY 


Nine morphological characters, selected for 
their potential diagnostic value, were evaluated 
for all 11 taxa of Osmorhiza. Representative 
specimens were selected for study from across 
the geographic range of each taxon. The quan- 
titative value for each character was obtained by 
taking the average of four measurements per 
specimen (occasionally two or three). Statistical 
significance of the data was determined using 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


Osmorh. 


аваа (55) eg 
glabrata 2 — gm 
mexicana . 

55р. Mexicana (3 — e 

ssp. bipatriata (10) i 
brachypoda (32) — و‎ 
chilensis (90) — — SC 
acid (70) — a 
purpure. 
fongistylis (29) — ——EÉBES—— 
aristata (30) E e 
c/aytonii (39) gg 


ps E Ман PASSARE REAR SONES GNN 
0) 0i. 02 бї ба On 06 Or Os 


Stylopodium height (mm) 


Osmorh 

ард А (47) سم‎ 
glabrata (e) 
mexicana 


= (30) 
chilensis (86) gg 
дердирегата (67) ——EÉEÓ————— 


purpurea (42) ——2-——— 


tongistylis (23) چچ‎ 
aristata (27) -ca 
claytonii (37) وچ‎ 
Dou ез ы c 
(%) о 20 60 80 100 120 


Fruit du length (mm) 


1-4. Mean, standard deviation, range of variation, and sample size of quantitative morphological 


—3. Fruit length (mm).— 


contingency table analysis solved by chi square. 

e tested the null hypothesis that departures 
from random expectation are attributable to 
chance alone (Woolf, 1968). Mean, standard de- 
viation, and range of variation of quantitative 
characters are presented in Figures 1-8. Sample 
izes are given in parentheses. Comparison of 
values from the ada eens disjunct areas of 
Osmorhiza chilensis, О. depauperata, and О. ar- 
istata is given in Tables 2—4, respectively. 

1. Style length. This is a diagnostic character 
for the members of Osmorhiza sect. Osmorhiza 
(O. longistylis, O. aristata, and O. claytonii) but 
is of little taxonomic value for the other species 
(Figs. 1, 9a—c). Statistical analysis of style length 
values for members of section Osmorhiza yield- 
ed a chi square significant far beyond the 0.0005 
probability level. The members of this section 
can readily be separated when this character is 
used in conjunction with geographic distribu- 
tion. Osmorhiza aristata, with intermediate style 
length values, occurs only in Asia, whereas О. 
longistylis and O. claytonii, both of which are 

ound in eastern North America, show no Over- 
lap in their ranges of values (Lowry, 1976; Lowry 
& Jones, 1979a; Ostertag & Jensen, 1980). Sev- 


| ——————————————ÁÉ—— 


1984] 


Osmorhiza 
occidentalis (36) EE a — — 
glabrata (11) — — gh... 
m jd cana 
ssp. Mexicana (30) —EEEEEEICLLILL— ——— — —— 


brachypoda (32) — ERES —— — — — — — 
chilensis (90) — — — —— 
depauperata (69) ES —— 

purpurea (54) 

longistylis (25) — — gea — — —— 

aristata (31) С) 

claytonii (35) 


Osmorhiz. 
юлат d (35) 


glabrata 8) 
mex. НЕКА 
55р. /nexici ) [TE 


brachypoda (31) ERUIT 

chilensis (89) 
depauperata (68) Ea ——————— 

purpurea (50) — — gg — ————— — 

longistylis (22) 

aristata (27) 
c/aytonii (35) 


و و ——M————————É——‏ 
120 100 80 60 40 20 )7( 


$ Ray length (mm), 1° umbel 


LOWRY & JONES—OSMORHIZA 


1133 


Osmorhiza 
occidentalis (44) 
mexicano. Ш) 
exicana 
vs mexicana (30) -2>— 
р. bipatriata (9) 
Pietas (32) 
chilensis (90) س‎ 
depauperata (70)  $— 
purpurea (54) H 
longistylis (25) n 
aristata (29) س‎ 
claytonii (35) > 
50 100 150 200 250 
Total o flowers per 1° umbel 


Osmorhiza 
occidentalis (55) 


g/abrata (10) 
mexicana Р = 
ssp. mexicana (3 

ssp. Sipatriata uo) gp 
brachypoda (32) a 
Chilensis (96) — gg 
— " — — — —— 
purpurea (5 — gm 


та (22) 


aristata (28) a ————— — —— 


ciay tonii n 


La gc‏ اا 
о 50 100 150 200- 250 300‏ 


€ Pedicel length (mm) 


FIGURES 5-8. Mean, standard tea т sni d of variation, and bese size of quantitative morphological 
tal 


characters in Osmorhiza spp.—5. To 
be 


. Hermaphrodite ray length бн 1° umbels (mm). 


eral authors have relied entirely on Pipe: length 
is from O. claytonii 
3) 


2. Stylopodium height. The high-conic sty- 
lopodia of Osmorhiza chilensis are distinctive, 
and separate it from the other members of the 
section Nudae, which pores low-conic to de- 
Pressed stylopodia (Figs. 2, 9i-k). Statistical 
analysis of this character for а members of О. 


p by its fairly high, conic stylopodia (Fig. 
3. Fruit length. This character is diagnostic 


for the taxa included in Osmorhiza sect. Nudae 
(Figs. 3, 9i-k). These species are, in fact, distin- 


yielded a highly significant chi square (P < 
0.0005) 


aphrodite flowers per 1 


mbel.— 6. Total staminate flowers per 
—8. Pedicel length of hermaphrodite flowers 


4. Fruit appendage length. The two subgen- 
era of Osmorhiza are separable on the basis of 
— or f absence of vias Rppeeiages on 

the base ps. All ten taxa comprising 

the peste subgenus have монан of varying 
lengths, while they are lacking entirely from the 
fruits of O. occidentalis (O. ti cst with 
a few rare exceptions (Figs. 4, 9). Within th 
typical subgenus, O. purpurea is аана from 
the other members of the section Nudae by hav- 
ing short appendages. Similarly, 0. mexicana 
subsp g 
other taxa in O. sect. Mexicana 

Constance and Shan (1948) ы out that 


note that O. chilensis and O. depauperata, both 
of which have wide disjunctions in their ranges, 
have conspicuously armed fruits. By contrast, O. 
occidentalis, which lacks both appendages and 
bristles, has a 

ed range in western North America. Similarly, 
O. mexicana subsp. bipatriata, with essentially 


1134 ANNALS OF THE MISSOURI BOTANICAL GARDEN (Мог. 71 
TABLE 1. Comparison of percentage of hermaphrodite flowers per 1° and 2° umbels in Osmorhiza species. 
1° Umbel 2° Umbel 
Total 6 Total à Total ¢ Total 8 Direction 
Fls./ Fis./ % à Fls./ Fls./ % $ of 
Umbel Umbel Fis. Umbel Umbel Fis. Change 
O. occidentalis 14.05 137.61 9.3 21.73 84.37 20.5 + 
O. aristata 19.32 22.24 46.5 11.84 19.24 38.1 — 
О. claytonii 13.94 8.20 63.0 10.68 10.32 50.9 ~ 
О. longistylis 18.80 4.92 79.3 15.52 36.39 29.9 = 
O. glabrata 20.73 32.50 39.9 11.60 21.40 35.2 = 
O. mexicana subsp. 
mexicana 13.35 11.47 54.1 12.08 14,46 45.5 » 
O. mexicana subsp. 
bipatriat 5.40 55.00 8.9 5.50 39.78 12.1 + 
О. brachypoda 19.38 11.97 61.8 13:72 11.44 54.5 m 
O. chilensis 16.49 5.10 76.4 11.39 7.84 59.2 = 
O. purpurea 14.96 6.46 69.8 9.75 4.71 67.0 m 
O. depauperata 13.20 3.04 81.3 9.98 2.67 79.0 = 


glabrous fruits and very short appendages, has а 
very narrow range in Texas and northern Mex- 
ico. 

5. Total hermaphrodite flowers per 1° um- 
bel. Species of Osmorhiza are andromonoe- 
cious, a feature common to many genera of Api- 
aceae; their inflorescences contain both 
hermaphrodite and functionally staminate flow- 
ers. The staminate flowers have well-developed 
stylopodia that secrete nectar, but lack styles and 
functional ovaries, and consequently do not de- 
velop fruit (Lowry & Jones, 1979a; Lowry, 1980; 
see also Већ, 1971). The total number of her- 


y um- 
bels i is quite uniform among Osmorhiza species 
(Fig. 5). Plants of each species produce similar 
numbers of fruits in their primary umbels (see 
below for the significance of this character). 

6. Total staminate flowers per 1° um- 
bel. This character is diagnostic in several ways. 
The two subgenera of Osmorhiza may be sepa- 
rated on the basis of this character; plants of O. 
occidentalis (O. subg. Glycosma) produce, on the 
average, more than twice as many staminate 
flowers per umbel as those of any taxon in Os- 
morhiza subg. Osmorhiza (Fig. 6). Furthermore, 
the members of O. sect. Osmorhiza are easily 
distinguishable from each other on the basis of 
this character. Values for the Asian O. aristata 
are intermediate between those for the North 
American О. claytonii and О. longistylis (Fig. 6). 
Statistical analysis of data for these three taxa 
yielded a very large chi square (P < 0. 0005). 

7. Percentage of hermaphrodite flowers per 1° 


and 2° umbels. The ratio of hermaphrodite to 
staminate flowers differs between the primary 
and secondary umbels in Osmorhiza species (Ta- 
ble 1). In members of the typical subgenus, the 
primary umbel has a higher percentage of her- 
maphrodite flowers than does the secondary um- 
bel. Therefore, the primary umbels of these plants 
contribute relatively more to the gene pool of the 
next generation through their ovules than do the 
secondary umbels. The only exception to this 
pattern in O. subg. Osmorhiza is O. mexicana 
subsp. bipatriata, for which there is a slight in- 
crease in the percentage of hermaphrodite flow- 
ers from primary to secondary umbel. This may 
be the result of the remarkably low number of 
hermaphrodite flowers in its primary umbels. 
This pattern of increasing **maleness" (or de- 
creasing *'femaleness") with successively later 
flowering umbels is correlated with protandry in 
the hermaphrodite flowers of many apiaceous 
taxa, including Ligusticum canadense (L.) Britt. 
and Daucus carota L. (Bell, 1971), and Osmo- 
rhiza longistylis (Torrey) DC. (Robertson, 1888), 
as well as the other species of Osmorhiza subg. 
Osmorhiza. 

By contrast, O. occidentalis (subg. Glycosma) 
shows a strong trend toward increasing “female- 
ness" from primary to later-flowering umbels 
(Table 1). In these populations, the percentage 
of hermaphrodite flowers is more than twice as 
high in th 1to the primary 
umbel. Schlessman (197 8, 1982) has shown that 
a similar increasing percentage of hermaphrodite 
flowers (expressed as a decreasing percentage of 


1984] 


LOWRY & JONES—OSMORHIZA 


1135 


LE 2. Morphological comparison of ig from the four major areas of distribution for Osmorhiza 


ae standard deviation, and sample 


Western Great Northeastern uthern 
North America Lakes Region North America outh America 
Character x succ $ Sd. ~ be s.d N x sd) М 

Style length (mm) 0.61 0.08 38 057 30.06 6 0.64 0.06 9 0.69 0.14 24 
Stylo dium ht. (mm) 0.42 0.09 38 0.38 0.04 6 0443 007 9 0:37: «008524 
Fruit length (mm) 16.66 271 36 1642 093 6. 1874 147 9 1497 172 22 
Fruit appendage 

length (mm) 5.45 IDN 30 5.02. 0:83 6 638 OI 9 492 EEE 
Тога! ¢ fis. per 

1° umbe 17.58 602 38 13.00 76.60 6: 1544 633 9 1650 70 24 
Total 8 85. per 

19 umbel 3.97 :433 38 4.00; £30.59 : 6 3.11 - 93,06. 9 937 5358.24 
$ ray length (mm) 

in l^ umbel 61.78 20.01 38 58.67 17.90 6: 79:78 2476 65.11 19:19 23 
$ pedicel length (mm) 9.65 3.26 38 11,39 03.39 67 7076 853 0 9:00:—3.81.:29 


staminate flowers) occurs in the protogynous 
species of tuberous lomatiums. Thus, although 
no observations have been made for O. occiden- 
talis, ci tantial evid ts that it 


~ 


be protogynous. T 

8. Hermaphrodite ray length in I° umbels. 
Two types of rays are typically produced in 
the umbels of Osmorhiza species, those whose 
umbellets contain both hermaphrodite and sta- 
minate flowers (hermaphrodite rays), and those 
with umbellets composed entirely of staminate 
flowers (staminate rays). Hermaphrodite rays are 
generally rather stiff when the fruits reach ma- 


ex pe 10 mm. Hermaphrodite ray length. is a 


useful 


istata from O. longistylis and O. “claytonii (Fig 
7). This character is also useful for separating O. 
brachypoda from the other members of O. sect. 
Mexicanae (Fig. 7). 
9. ecu length of hermaphrodite дау. 


ers, 
atin 
0. a from its North American ен 


10. Comparison of io populations of Os- 
Morhiza species. Comparison of values for 
Morphological chica from the four geo- 
graphically disjunct areas of О. chilensis (western 
North America, the Great Lakes region, north- 
astern North America, and southern South 
America) shows a remarkable similarity among 
the populations (Table 2). While a number of 


populations in the Great Lakes area, the north- 
east, and South America appear to have under- 
gone some divergence, there is no doubt as to 
their conspecificity with populations from west- 
em North America, where the species possibly 
originated. 

ie populations of O. depauperata from 
these same disjunct areas are morphologically 
very similar to one another (Table 3). While some 
divergence has occurred in South America, the 
specimens examined from this area are clearly 
within the range of variation found within the 
species in western North America. 

Constance and Shan (1948) recognized two va- 
rieties of Osmorhiza aristata, the variety laxa, 
from southwestern China and the Himalayan re- 
gion, and the typical variety from the Altai region 
and eastern Asia. These varieties were distin- 
guished on the basis of leaf characters; plants 
from Sachalin and Siberia show a maximum of 

eaf dissection, those from Japan are interme- 
diate, and those from the Himalayas have leaves 
that are much less divided. Although this vari- 
ation in leaf dissection is indeed recognizable, 
there is no apparent correlation with other mor- 
phological characters. Quantitative values for 


rn Asia 


and the Himalayan 1 region are quite similar, and 
do not support the recognition of infraspecific 
taxa within O. aristata (Table 4). 


PHYTOGEOGRAPHY 


Nearly 8,000 herbarium specimens were ex- 
amined to determine the limits of geographic 


[Уо1. 71 


1136 ANNALS OF THE MISSOURI BOTANICAL GARDEN 

TABLE 3. Morphological comparison of populations from the four major areas of distribution for Osmorhiza 
depauperata—mean, standard deviation, and sample size. 

Western Gre Northeastern Southern 
North America Lakes Scion North America South America 
Character x sd N x Nd. М x а № x SOs N 

Style length (mm) 0.46 0.07 33 0.46 0.10 7 0.46 0.09 7 0.55 0.08 9 
Stylopodium ht. (mm) 0:27 0.06 33 0.312008 7 027 006 7 039 006 9 
Fruit length (mm) ИШ UIN 3 Т1 083 7. 1479 086 7 1228 168 8 
Fruit appendage 

length (mm) 4.98 0.93 32 #25 1047 41 521 0567 400 076- 8 
Total ¢ fis. per 

1° umbel ОООО СЕ: 3 133 575 6 1386 24r 7 1222 346 9 
Total 8 fis. per 

1° um 3.09 13.30 33 0:05 123 6 257 T40 7 #22 $0 9 
$ ray length (mm) 

in 1° umbels Ке M WX 1007 6 5050 2019 7 55.33 1079 9 
$ pedicel length (mm) КИНЕ NM 3 6660. 236 Z 1674 432 7 1505 -2.72 10 


distribution for Osmorhiza species. Distribution 
was mapped for each taxon by placing dots on a 
base map; one dot (or occasionally two) for coun- 
ties in the U.S., and one dot per locality for other 
areas. A number of important collections re- 
ported by Hultén (1947), Constance and Shan 
(1948), Shishkin (1950), and Liu (1977) not 
available for study were mapped as circles. In 
general, the ranges obtained are in agreement 
with those given by other authors, notably Hul- 
tén (1947), Constance and Shan (1948), Con- 
stance (1963), Wood (1972), and Marquis and 
Voss (1981). 

OSMORHIZA SECT. OSMORHIZA. Two species, 
O. claytonii and O. longistylis, are widely dis- 
tributed in eastern North America and are sym- 
patric over much of their ranges (Lowry, 1976; 
Lowry & Jones, 1979a). Both occur on the Gaspé 
Peninsula, in Nova Scotia, and in southern Que- 
bec and Ontario, and reach their eastern limits 


south along the Atlantic Coast. In the south, O. 
claytonii ranges from the southern Appalachian 
Mountains of North Carolina and Tennessee to 
the Ozark Plateau, approximately along the 35th 
parallel. In the west, this species reaches its limits 
along a line close to the 100th meridian, with 
extensions into north-central Nebraska and 
southwestern Manitoba (Fig. 10). 

The range of O. longistylis extends farther to 
the south, reaching from the Piedmont Upland 
of central Georgia and South Carolina to Arkan- 
sas, eastern Oklahoma, and adjacent Texas. In 
the west, this species is found throughout the 
upper Great Plains, and has its limits along the 
base of the Rocky Mountains in Colorado, Wy- 
oming, Montana, and Alberta (Fig. 11). 

The third member of this section, O. aristata, 
occurs only in Asia, ranging from Sachalin and 
the lower Amur basin, through Japan, Korea, 
Taiwan, central and southern China, to the Hi- 


TABLE 4. Morphological comparison of populations of — aristata from eastern Asia and the Hi- 
malayan Region — mean, standard deviation, and sample s 


Eastern Asia Himalayan Region 

Character x s.d. N x s.d. N 
Style length (mm) 1.91 0.18 25 1.78 0.22 5 
Stylopodium height (mm) 0.52 0.07 25 0.51 0.09 5 
Fruit length (m 17.59 1.61 23 20.00 1.68 4 
Fruit appendage length (mm) 6.27 0.99 23 7.91 1.82 4 
Total 4 85. per 1° umbel 19.30 6.42 26 19.60 11.26 5 
Total ê 85. per 1° umbel 23.04 9.73 25 17.25 7.23 4 
$ ray length (mm) іп 1° umbels 71.09 14.17 23 80.29 26.18 4 
$ pedicel length (mm) 14.63 3.45 24 23.92 4.84 4 


LOWRY & JONES—OSMORHIZA 1137 


10mm 


of the ng % Osmorhiza species.—a. О. aristata.—b. О. claytonii.—c. О. longistylis. 
subsp. e . mexicana subsp. bipatriata. ок 


Fic Drawin 
X4 occidentalis —e. 70. glabrat 
brachypoda.—i. O. purpurea. e p chilensis. —k. О. depauperat 


ANNALS OF THE MISSOURI BOTANICAL GARDEN [Vor. 71 


1138 


FIGURE 10. Geographic distribution of Osmorhiza claytonii. 


Geographic distribution of Osmorhiza longistylis. 


FiGURE 11. 


1984] 


LOWRY & JONES— OSMORHIZA 


1139 


y adea Ж Rcx 


FIGURE 12. Geographic distribution of Osmorhiza aristata. 


malayas of Bhutan, Nepal, India, and Pakistan. 
Disjunct populations occur in the Altai region of 
central U.S.S.R. and have been reported by 
Shishkin (1950) from the Caucasus Mountains 
of southeastern U.S.S.R. (Fig. 12) 
species of Osmorhiza sect. Osmorhiza 
provide an excellent example of the well known 
fastern North American-eastern Asian pattern 
of disjunction, which is shared by many mem- 
bers of the temperate deciduous forests of the 
two regions (Hara, 1952, 1956, 1972; Li, 1952, 
1972; Constance, 1972; Wood, 1972; Ablaev et 
al., 1974). This pattern has long been recognized, 
e.g., by Linnaeus (1750; cf. Graham, 1966) and 
Thunberg (1784), but Asa Gray (1859) was the 
t botanist to examine it in detail. Gra 
cated that many — — — 
from eastern North and Japan appear 
to be conspecific, and ree ek ae out their 
| Conspicuous absence from western North Amer- 
- ica. To explain this phenomenon, he developed 
_ а hypothesis involving migration and exchange 
_ Of species between North America and Asia across 
. the Bering Strait, followed by their elimination 
| from western North America and northeastern 
_ Asia during the Pleistocene. 


Paleobotanical evidence confirms the wide- 
spread occurrence throughout much of North 
America and Eurasia of a number of genera, par- 


ticularly woody ones, now restricted to the east- 


matic conditions, especially th 
to dry summers, in relict habitats, particularly 
the mountains of southern Oregon and northern 
California. Wood (1972: 112) suggested that many 
plants occupying other regions of the Northern 
Hemisphere survived in a similar manner. He 
then stated: “Тһе largest, and ecologically most 
complex, of the relict areas are eastern Asia and 
eastern North America; those of western North 
America and EY asia Minor are —€— and 
m erly occurred in them have 
рањива ан " Wood река дни that e pattern 
of formerly widespread genera being restricted 
in distribution to eastern Asia and eastern North 
America by “orogenic movements, gradual cli- 
matic cooling, volcanism, and the Pleistocene 
glaciations seems to be well established." 

The three species of Osmorhiza sect. Osmo- 


cimilar. 


1140 


FiGURE 13. Geographic distribution of Osmorhiza 
purpurea. 


ity and have been regarded as conspecific by a 
number of authors (e.g., Gray, 1859; Clarke, 1879; 
Kuntze, 1891; Boivin, 1968). Constance and Shan 
(1948) suggested that this similarity may be 
ascribed to one of two factors: either there has 
been a relatively recent contact between the Asian 
and North American populations through Berin- 
gia, or these species have differentiated from a 
once widespread common ancestral population 
at a very slow rate. While Wood’s reasoning, as 
outlined above, tends to support the latter, Li 
(1972) took a different view, arguing that the 
observed morphological similarities between 
populations of eastern Asia and eastern North 
America may be the result of geographic and 
ecological similarities between these areas. He 
pointed out that the two areas lie at roughly the 
same latitude, are situated in the same relative 
position on their respective continents, are tem- 
pered by ocean currents from the south, and share 
features of their topography, soil, temperature 
ranges, precipitation distributions, ес. Li be- 
lieved that these g ities were 
probably tł It of parallel lution, and may 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


not always accurately reflect an underlying phy- 
logenetic relationshi 

If, however, one шон eastern Asia and east- 
ern North America as more or less stable, mesic 
refugia, it is possible that the species occupying 
these areas may have remained relatively un- 
changed both morphologically and genetically 
over long periods. Species of Osmorhiza appear 
to be stable taxa, with little or no indication of 
natural hybridization, and no “rapidly evolving” 
species. Rather than postulating the unlikely event 
of gene exchange in the recent past between the 
disjunct populations of this section, it seems more 
plausible to us to consider them parts of a rela- 
tively stable floristic assemblage that has per- 
sisted in eastern Asia and eastern North America 
over a rather long period. 

OSMORHIZA SECT. NUDAE. АП three species 
of this section occur in northwestern Nort 

merica, and two of them, O. chilensis and O. 
depauperata, have disjunct populations in the 
Great Lakes area, рвана North America, 
and southern South Am 

Osmorhiza purpurea чш a more restricted 
range, occurring more or less continuously along 
the Pacific Coast, from the redwood forests of 
northwestern California to Kodiak Island in 
southwestern Alaska. Inland, populations are 
found through the Cascade Mountains of Oregon 
and Washington eastward to the Rocky Moun- 
tains of Idaho, northwestern Montana, and ex- 
treme southwestern Alberta, and in much of 
иона иа Columbia (Fig. 13). 

occu lyin 

western North America, Кот! the Warner Moun- 
tains of northeastern California, through Oregon, 
Washington, and central British Columbia, to 
the northern “‘pan-handle”’ and the Kenai Pen- 
insula in Alaska. This species is much more com- 
monly represented in the Rocky Mountains, 
where it ranges from southern Arizona and New 
Mexico northward to British Columbia, Alberta, 
and the extreme southwestern part of the 
Mackenzie District. Disjunct populations of О. 
depauperata are recorded from the Black Hills 
of South Dakota and те Cypress Hills i in ccce 
andS 
found across the Prairie Provinces of Canada in 
central Alberta, eastern Saskatchewan, and in 
Riding Mountain National Park, Manitoba. In 
the Great Lakes region, populations occur along 
the northern shore of Lake Superior, on Manitou 
Island in Lake Michigan, near Lake Nipigon in 
Ontario, and on Charlton Island in the James 


OO ey ee 


~ 


У 
ПА д! AN, 


LOWRY & JONES—OSMORHIZA 


1141 


1000 km 


FiGURE 14. Geographic distribution of Osmorhiza depauperata. 


Bay Region (over 600 km to the northeast). In 
the east, O. depauperata ranges from Vermont 
and Lake Saint John in Québec, through the 
Gaspé Peninsula, Anticosti and Mingan Islands, 


Tierra del Fuego northward through the Andes 
of southern Argentina, reaching its northern lim- 
it at Termas de Chillán in Prov. Nuble, Chile 
(Fig. 14). 

Osmorhiza chilensis shows a similar overall 
pattern of distribution, and is sympatric with O. 
depauperata throughout much of its range, al- 
though it is much less common in the southern 
Rocky Mountains, particularly in Arizona an 
New Mexico. By contrast, populations of O. chi- 
lensis are common along the west coast, ranging 
from southern California, through Oregon and 
Washington, to Vancouver Island, the Queen 
Charlotte Islands, and southeastern Alaska. Oc- 
Currence of this species has also been reported 
from the coast of southwestern Alaska, with its 
Tange extending as far west as Unalaska Island 
in the Aleutian Chain (Hultén, 1947). With the 
exception of two populations in south-central Al- 


berta, O. chilensis appears to be absent from the 
Prairie Provinces of southern Canada. In the 
Great Lakes area, it is widely distributed along 
the western and southern shores of Lake Supe- 

rior, eastward to Lake Huron and the Georgian 
Bay; in eastern North America the range extends 
from northern New Hampshire and Maine, 

ы the Gaspé Peninsula, New Brunswick, 
and seio Scotia, to Newfoundland. South 
American populations occur from the Tierra del 
Fuego pecie the Andes and along the central 
Chilean coast northward to Prov. Aconcagua, 
Chile (Fig. 15) 

Two well known types of disjunction are ex- 
emplified by O. chilensis and O. depauperata; 
amphitropical disjunctions between North and 
South America, and disjunctions between west- 
ern and eastern North America. 

Similarities between the floras of temperate 
western North America and southern South 
America were recognized over 100 years ago by 
Gray and Hooker (1880). Since then, many bot- 
anists have dealt with this subject (e.g., Engler, 
1882; Reiche, 1907; DuRietz, 1940; Campbell, 
1944; Constance, 1963; Raven, 1963; and Moore, 
1972). Constance (1963) suggested that Osmo- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Уот. 71 


IN, 
Ve UN 


gh А) 


еа, 


FiGURE 15. Geographic distribution of Osmorhiza chilensis. 


rhiza chilensis and O. depauperata may have 
reached South America by a step-wise migration 
through the tropics along a route now marked 
by the members of the section Mexicanae. Raven 
listed about 130 species or species-pairs, includ- 
ing O. chilensis and O. depauperata, that exhibit 
patterns of disjunction between temperate North 
and South America. He also discussed the im- 
portant factors concerning this pattern, which he 
summarized as follows: “(1) North and South 
American populations are closely related; (2) the 
plants are almost without exception self-com- 
patible and often autogamous; (3) they constitute 
an unbalanced assemblage entirely unrepresen- 
tative of the floras of the two extratropical areas; 
(4) they grow almost exclusively in open com- 
munities, not in woodland or scrub associations; 
(5) there are no corresponding cases among ter- 
restrial vertebrates and very few among the in- 
— and (6) the floras e the two areas have 
iddle Cretaceous 

and are still very distinct at present.” Raven 
(1963: 166) concluded that the only reasonable 
explanation to account for these facts is that “at 
least the great majority of the plants reached their 
disjunct areas by long-distance dispersal rela- 


tively recently.” He noted further that, for tem- 
perate species, the Pliocene or Pleistocene were 
the most likely times for this kind of dispersal, 
and that the majority of species involved mi- 
grated from north to south. The distribution pat- 
terns of O. chilensis and O. depauperata fit very 
well into this overall syndrome. There is no doubt 
that the North and South American populations 
of each of these species are very closely related. 
Although a few South American populations of 
both taxa seem to have undergone some mor- 
phological divergence, the majority of them ap- 
pear to be virtually identical to their North 
American counterparts. Conversely, a number of 
morphological variants of both species that occur 
in North America seem to be absent from South 
America 

Obeervátions made as part of this study sug- 
gest that Osmorhiza species are facultatively au- 
togamous, a condition that would permit even a 
single propagule to establish a new population. 
Both O. chilensis and O. depauperata produce 
fruit armed with caudate appendages and nu- 
merous retrorse bristles, making them well 
adapted for epizoochory. Furthermore, the am- 
phitropical pattern of disjunction for these taxa 


1984] 


corresponds closely to the migration routes of a 
number of bird species (Raven, 1963). Altho 
many populations of both O. chilensis and O. 
depauperata occur in forest communities, these 
plants are also quite common in more open sit- 
uations, making them accessible to a variety of 
potential dispersers. When taken together, these 


the direction of migration has been from north 
to south 

The western North America-eastern North 
America pattern of disjunction observed in O. 
chilensis and O. depauperata is somewhat less 
striking (Figs. 14, 15). Nevertheless, this type of 
disjunction has received considerable attention 
since Fernald (1924, 1925, 1926, 1933, 1935) 
developed his “nunatak” hypothesis to explain 
it (see also Marquis & Voss, 1981). Fernald be- 
lieved that primarily arctic and western Cordil- 
leran taxa were able to survive in eastern North 
America during the Pleistocene in unglaciated 
areas (nunataks) located around Lake Superior, 


ed the failure of these гаме disj uncts to nis ORES 
their ranges following tl 
of their “antiquity,” stating that “at the close of 
the Pleistocene they were already too old and 
conservative to pioneer, although they were able 
to linger as localized relicts in their special un- 
disturbed crannies and pockets.” 

any of Fernald’s arguments have not with- 
stood the test of time. All of his nunataks were 
ш fact glaciated (Wood, 1972), and there is no 
ala бића the plants involved could not have 


tocene (Schofield, 1969, and references therein). 
Furthermore, the concept of senescence of species 
is no longer tenable (cf. Wood, 1972). 

An alternative explanation for this pattern of 
disjunction is given by Stebbins (1935), who ar- 
gued that each species involved migrated east- 
ward at the end of the Pleistocene along the front 
ofthe receding ice sheet, becoming progressively 
more rare to the east. However, this hypothesis 

oes not, by itself, explain the restriction of the 
majority of чире taxa to the Great Lakes area 
and the northea 

Schofield se 200) adopted a somewhat 


LOWRY & JONES—OSMORHIZA 


1143 


— version of Fernald's nunatak hypoth- 
es is, w (Tia ві 


ihe most 
Been explanation of their disjunctions is that 
th + + z + ^ 


widespread flora of the past, possibly of pre- 
Pleistocene arctic-alpine distribution in North 
America. The Pleistocene glaciations can be as- 
sumed to have eliminated the northcentral por- 
tion of the range, but since habitats were avail- 
able in northeastern and western North America 
the species survived, probably south of the gla- 
cial boundary, but possibly i in hunataks i or coast- 
al refuges, mo 
retreat of the ice sheet but being eliminated from 
their Pleistocene refugium by the encroaching 
vegetation and by a succession toward a more 
mesophytic temperate vegetation.” To this we 
would add the observation that these disjunct 
taxa are most likely restricted to their present 
localities by a variety of ecological factors: they 
tend to occur in areas where there is reduced 
competition from the dominant eastern boreal 
taxa (Rune, 1954), and where climatic condi- 
tions, particulariy snowfall and moisture avail- 
pena western North Am erica. 

Schofield’s hypothesis, as modified above, 
seems to be the most plausible to explain the 
western North American-eastern North Amer- 
ican pattern of disjunction observed in Osmo- 
rhiza chilensis and O. depauperata. Nowhere in 
the literature have we found any suggestion that 
long-distance dispersal may have played a role 
in producing this type of disjunction; at least in 
the case of Osmorhiza, this type of dispersal would 
seem unlikely because the distribution of these 
plants does not seem to be correlated with the 
migration routes of any birds. Movement over 
shorter distances, however (e.g., from the Rocky 
Mountains into Saskatchewan and Manitoba), 
may be the result of epizoochory following the 
Pleistocene glaciations. 

OSMORHIZA SECT. MEXICANAE. The repre- 

sentatives of this section form a “three-link c E 
extending from the southwestern p States 
to central Argentina and Chile. northern- 
most link is represented by ceres brachy- 
poda, which has a relatively restricted distribu- 
tion, ranging from the mountains of southwestern 
California northward through the Coast Range 
to Mount Diablo in Alameda County, and 
through the Sierra Nevada to Nevada and Sierra 
Counties, California. Disjunct populations occur 
in the Mazatzal Mountains of central Arizona 


VO сила p 


to those 


1144 


FiGURE 16. Geographic distribution of Osmorhiza 
brachypoda. 


(Fig. 16), although they have not been collected 
since 1 


Texas to northern Argentina. Osmorhiza mexi- 
cana subsp. bipatriata is known from only three 
localities: Madera del Carmen, Coahuila, 
rro Potosi, Nuevo León, Mexico, and Mou 
Livermore, Jeff Davis Co., Texas. It is very pos- 
sible, however, that this taxon also occurs on 
some of the other, as yet unexplored, mountains 
of вина and Nuevo León. Osmorhiza mex- 
icana subsp. mexicana reaches its northern limit 
in the Sierra Mohinora of Chihuahua and occurs 
together with subspecies bipatriata on Cerro Po- 
tosi. The typical subspecies ranges southward 
through the mountains of Mexico, Guatemala, 
and Costa Rica, into South America, where it 
occurs from the Рагато de Ruiz in Tolima, Со- 
lombia, through the Cordillera Oriental of south- 
ern Peru and adjacent Bolivia, and the moun- 
tains of northwestern Argentina, reaching its 
southern limit in the Sierra Grande of Cérdoba, 
Argentina (Fig. 17) 

Osmorhiza glabrata is restricted to the central 
Andes, ranging over a distance of less than 750 
km from Prov. Santiago, Chile, to southern Neu- 
quén, Argentina (Fig. 18) 

mbers of Osmorhiza sect. Mexicanae 
form a more or less continuous chain between 


discrete populations of the amphitropical taxa” 
in North and South America (Constance, 1963: 
113). As Constance pointed out, however, it is 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


` 
^ 
` 
~ 
Td 
п 
bod 
^ 
D, 
a 7 
` 
$ ^ 
Д 
e. 9 g 
, 2 
ГА 
"e 
ut 
a 
Ws Ба є 
~ 
° = 
o f К 
у 
0° ‹ 
x 
e X 
x S 
4 
4 
EN 
J 
= а ы, ы! en сч 
^ 
Nt hod ^ " 
wed TUN 
» 
P mor ms. Py 
^ 
r 
' 
4 
M 
E су сч 
1000 km 
# 
4 
"d 
(4 
i 
Џ 
/ 
z 
4 
P4 
[i 
ГА 
, 
24 
HE, 


FIGURE 17. пао надај distribution of фике 
техїсапа.— О. icana subsp. mexicana (9).—O 
mexicana subsp. qe (L1). 


difficult to imagine a polytopic origin of both O. 
chilensis and O. depauperata from an extant or 
extinct member of the section Mexicanae both 
to the north and south of the equator. 
Although one may be tempted to think of O. 
brachypoda and O. glabrata as northern and 
southern derivatives, respectively, of O. mexi- 
cana, there is no evidence to support this idea. 
A more plausible hypothesis is that all three 
species are derivatives of a once widespread 
common ancestral population whose distribu- 
tion spanned the tropics, much as O. mexicana 
does today. According to Constance (1963), the 


| 
| 
i 
| 


1984] 


Jg 
J 
>IM,09 


RRA- SYP 


RARER RAED 
500 km 


por 18. Geographic distribution of Osmorhiza 
&а 


mountains of Mexico and Central America were 
uplifted during the Pliocene or Pleistocene, oro- 
genic movements that would have provided a 
chain of mountain tops with temperate climatic 
Conditions suitable for the survival of such an- 
cestral plants 
SMORHIZA SUBG. GLYCOSMA. The sole 

member ds subgenus, О, occidentalis, is quite 
common 
Much of western United States and adjacent 
Canada. It is widely distributed in the Rocky 
Mountains, ranging from southern Utah and 
Southwestern Colorado northward to extreme 


Basin in Nevada, eastern Oregon, 
and southwestern Idaho, to the northern Sierra 
Nevada, and the Coast Ranges of northern Cal- 
ifornia and Oregon. This species also occurs in 


LOWRY & JONES—OSMORHIZA 


1145 


the Olympic and Cascade Mountains of Wash- 
Wash- 
daho, and in the Willamette Valley 
and бана! foothills of the Cascade Mountains 
in Oregon, but it has not been recorded in the 
central and eastern parts of the Cascades. 

No major disjunctions occur in the range of 
O. occidentalis, but this is not surprising when 
one considers how poorly adapted its fruits seem 
to be for к E the schizocarps 


rr о 


апа retrorse bristles (Fig. 9d). 

Constance and Shan (1948) erroneously in- 
cluded NM glabrata in their section “С/у- 
cosmae" (— в. Glycosma), leaving the group 
with a large ten American-South American 
disjunction that is жыны to explain. If the af- 
finities of O. glabrata are, however, recognized 
as lying with members of the section Mexicanae, 
the problem is eliminated. 

e phytogeographic oroe presented here 
indicates that Nort a is the center of 
diversity, distribution, and а also the сеп- 
ter of origin for the genus Osmorhiza. Although 
none oft (e.g., Myr- 
rhis, Chaerophyllum, Scandix) occurs in in the area 


aracters, is restricted to west- 
ern North America, and all three sections of the 


SYSTEMATIC TREATMENT 


Osmorhiza Raf., Amer. FASA Mag. & Crit. 
Rev. 4: 192. Jan. 1819, nom. cons. prop. 
yrrhis claytonii Mich aux [7 Os- 

Mts claytonii (Michaux) C. В. Clarke]. 


тим Raf., м —— Mag. & Crit. Rev. 
2: 176. 1818, nom. nud., non Washingtonia H. 
Wendland (1879): nom. cons. 

Osmorhiza Raf., eed Monthly Mag. & Crit. Rev. 2: 

6. 1818, nom 
Gonatherus Raf., Ami. Many Mag. & Crit. Rev. 2: 
‚ 1818, nud. 

Uraspermum. t бе: Amer. pl. 192. 1818, nom. 
reji 

ER Raf., J. Phys. Chim. Hist. Nat. Arts 89: 
157. 1819. nom. pit prop. (cf. Lowry, 1985). 

Spermatura Е. Reichb., Consp. Reg. Veg. 141. 1828. 

Glycosma Nutt. in n Torrey & A. Gray, Fl. N. Amer 
39. 1840. 


me Molina ex C. Gay, Fl. Chilena 143. 1874, pro 


Elieimataenia ر‎ Bull. Soc. Imp. Natu- 
tes Moscou 29: 164. 1916. 


1146 


Plants andromonoecious, slender to robust, 
perennial, herbaceous, aromatic, caulescent, 
дуња! variet toa basal оше ӨП iens stems erect 
to spre olitary to 
densely clustered, branching, fistulose, аи 
to glabrous. Roots fusiform, thick, fascicled, dif- 
fusely to extensively branched, surmounted by a 
branched se Leaves alternate, basal and 
cauline, membranaceous, bipinnate or 2—3-ter- 
nate; о. lanceolate to orbicular, serrate to 
pinnately divided, with mucronate ultimate seg- 
g the stem, with their 


д cili alahranc 
late to aviuus. 


man peti 


Umbels twice compound, umm to somewhat 
constricted; peduncles terminal and lateral, erect 
to ascending or spreading, usually exceeding 
the leaves; пбн v anting, or composed of 
1-several narrow, foliaceous, ciliate bracts; rays 
ascending to widely divaricate or reflexed, slen- 
der, unequal, the peripheral ones being longer; 
umbellets few to numerous, often of two kinds, 
those bearing hermaphrodite flowers or a mix- 
ture of hermaphrodite and staminate flowers (re- 
erred to as “hermaphrodite” umbellets), and 
those bearing only staminate flowers (referred to 
as "staminate" umbellets); involucel wanting, or 
of several linear to ovate, acuminate, ciliate, 

spreading to reflexed bractlets; pedicels ascend- 
ing to widely divaricate, those of the hermaph- 
rodite flowers longer than those of the staminate 
flowers. Hermaphrodite flowers in each umbellet 
borne peripherally to the staminate flowers (if 
any), sometimes slightly irregular; calyx wanting; 
corolla white, greenish white, or yellow, or tinged 
with green, pink, or purple, the petals spatulate 
to ovate, the apex with an inflexed appendage; 
anthers about 0.5 mm long, smaller in the sta- 
minate flowers, inflexed before anthesis, spread- 
ing as the flower opens; styles spreading to di- 
varicate, variable in length depending on the 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


species, but wanting in the staminate flowers; 
stylopodium conic to depressed, sometimes with 
a conspicuous disc, often nectariferous; carpo- 
phore 2-cleft from one-quarter to nearly one-half 
of its length. Fruit a schiz , deep brown to 
black at maturity, linear to обой. fusiform to 
clavate, beaked to obtuse at the apex, sometimes 
constricted just below the stylopodium, shallow- 
ly to deeply concave furrowed, slightly com- 
pressed laterally, the ribs filiform, equidistant, 
moderately to sparingly hispid with retrorse bris- 
tles, or glabrous, the base rounded or with two 
caudate appendages; oil tubes (vittae) obscure or 
wanting; seeds subterete or unequally pentagonal 
in cross section, the face shallowly concave or 
sulcate 


Osmorhiza is clearly distinct from the mono- 
typ uropean genus Myrrhis (apparently its 
closest relative) on the basis of the following 
characters: the leaves are 2—3-ternate or bipin- 
nate (they are 2-4 times pinnatisect in Myrrhis), 
the umbels are definite in number (numerous in 
Myrrhis), the rays are glabrous (densely EV 
cent in Myrrhis), and the fruit latively sm 
and lack winged ribs (fruit larger and а 
winged in Myrrhis). 

Drude (1897), in his classic treatment of the 
Umbelliferae, placed Osmorhiza in his subfam- 
ily Apioideae, tri candicineae, subtribe Scan- 
dicinae, along with the clearly related genera 
Chaerophyllum L., Myrrhis Miller, and Scandix 
L. A number of other genera, many of which are 
likely related to Osmorhiza, but some of which 
clearly are not, were also included in this sub- 
tribe. Bentham (1867) placed Osmorhiza in his 
series Heterosciadiae, tribe Ammineae, subtribe 
Scandicineae, along with the three genera men- 
tioned above, as well as some others. 


ANALYTICAL KEY 


la. Fruit glabrous, lacking caudate appendages; staminate umbellets 3-10 per umbel; staminate flowers 
(75-)90-225 per umbel; plants very robust; stems (1-)3-6(-8), densely clustered; leaves bipinnate 
(Osmo 


corolla yellow to greenish yellow 


die subg. Glycosma) 


One species 


morhiza occidentalis 


1b id with ret 
- 4 Suess мәр. 


in O. mexicana subsp. bipatriata), with данча 
bellets yates per umbel; : staminate flowers 0— 


ap 
0—90(-125) per umbel; plants slender to 


staminate um 
armsa stout; stems 1—3(-5), not densely clustered; leaves 2-3-ternate; corolla white, or tin 


le 


ged with 
(Osmorhiza subg. Osmorhiza) 


green, pi 
2a. Involucel conspicuous, composed of 1-6 spreading to reflexed, foliaceous bractlets. 
3a. Styles “cap a 1-3.6 mm long; stylopodium high-conic; involucre co 
( 


۰ ~)2-3(-5 


posed 
Osmorhiza sect. ыю) 


~ гое А речи hermaphrodite flowers (5-)9-30 mm long; rays 4.5-11 cm m long; fruit 


ear-clavate, obtuse or abruptly acute at the apex; plants restricted to 


x DU aristata 


1984] 


LOWRY & JONES—OSMORHIZA 


1147 


4b. pei of the hermaphrodite a: 4–10(-15) mm long; rays 1.5-8 cm ее fruit 


ong-fusiform, ried acute 
т Styles 1—1 


о attenuate at the apex; plants of North Ameri 
m long, flowers 4-7(-8) per umbellet; staminate lowers 237- 


smelling, = som 


о 


weakly 
5b. Styles : 2-3 6; mm 


ee flowers (7-)9-18 per umbellet; staminate Towers (23 


meti 
morhiza canton 
“wid -75 


(-86) per umbel; umbels dense and congested; roots with a strong, sweet, anise-like 
ell 


morhiza os 


sme 4. Os 
3b. Styles 0.5— к f mm ир stylopodium low-conic to somewhat cmo involucre 
d of 1–2(–3) reduced bracts morhiz 


or sometim 


ng, 
a sect. en E 
ong; 


com 
6a. Leaves "acm. lobed or pinnatifid; styles (incl. жоро). (0. 9.12 m m lon 
odium 0. 


stylop 
entina 


4—0.8 mm long; plants restricted to the central Andes of Chile ef. Ar- 


orhiza glabrata 


5. Osm 
6b. Leaves coarsely serrate to engins d lobed or divided at the base, never laciniate; 5 tyles 
mm азы stylopodium 0.2—0.5 mm long; plan tring in 


(incl. ee е 0. - 1.2 
North, Central, a 


Та. Pedicels of 2 hermaphrodite flowers 1–4.5 mm long, ascending; plants restricted 


uthern California and c 


ә 
с 


. Osm 
. Pedicels of the hermaphrodite lese 2-23. my 5 mm long, spreading ko 


Mun i лица 


ascending; plants occurring from southwestern Texas and northe ex n dieses d 


Osm ird TT 


pi 
да. Fruit (10–)11–20 mm long, n: to densely hispid ' иш retrorse bris 
0m 


) per bietet 


the appendages (1.5—)2-1 


plants rather widespread Ка northern Mexico southw. 
6a. Osm 


PH mexicana subsp. mexicana 


oo 
с 


. Fruit 9–11(–12) mm long, glabrous, or occasionally with a few bristles toward 
the base, the appendages lacking, or to 


.8 mm long; staminate ete diet a 


Mises, per isis plants restricted to three localities in southw 
sm 


adjacent 


rhiza mexicana subi. bara 
„ (Osmorhiz Nudae) 


2b. Involucel VE or very rarely canine of 1(-2) minute bractlets _ DONNA 
9a. ait linear-fusiform to linear-oblong, beaked at the apex; rays and pedicels е. 


scending 
10a, Stylopodium high-conic to somewhat gibbous, lacking a disc, (0.2-)0.3-0.6 mm Ped 
fruit ta 


the ais m: not constricted, 12-21(-25) "ar long, the 


smorhiza idi 


ed with a conspicuous disc, 0.1—0.4 mm n long; очи t con- 


stricted below the маркам: 8—15(—16) mm long, the appendages 1—5 m 


long ... 
. Osmorhiza purpurea 


9b. Fruit clavate, obtuse at the apex; rays and pedicels strongly divaricate to nearly 
10. 


air pr 


I. Osmorhiza Raf. subg. Glycosma (Nutt.) Drude. 
Glycosma Nutt. in Torrey & A. Gray, Fl. N. 
Amer. 1: 639. 1840. Mamie § [sect.] Gy- 
cosma (Nutt.) A. Gray, Proc. Amer. Acad. 
Arts 7: 346. 1868. diui subg. Gly- 
cosma (Nutt.) Drude in Engl. & Prantl, Nat. 
Pflanzenfam. 38; 153. 1897. панк 
Hn Glycosma (Nutt.) Coult. & Rose, Contr. 


nud. TvPE: Glycosma occidentalis Nutt. 
[= Osmorhiza occidentalis (Nutt.) Torrey]. 


Plants robust; stems densely clustered, (1-)3- 
6(-8), often glaucous. Root system deep, exten- 


ers than the secondary and later flowering um- 


bels; staminate umbellets 3-10 per umbel; sta- 
minate flowers (75—)90-225 per umbel; corolla 
yellow to greenish yellow. Fruit glabrous, with- 
out caudate appendages. 

When Osmorhiza occidentalis was first de- 
scribed, Nuttall (in Torrey & Gray, 1840) placed 
it in a new, monotypic genus G/ycosma. Plants 
belonging to this genus were distinguished from 
those of Osmorhiza by having unappendaged, 
glabrous fruit. Torrey (1859), Drude (1897), and 
Coulter and Rose (1900) united these genera, 
although in the latter two treatments G/ycosma 
was retained as a separate subgenus. 

Osmorhiza occidentalis is quite distinct from 
the other mem of the genus. However, the 
morphological differences between O. occiden- 
talis and the other species of Osmorhiza are much 
; с. hero these 


groups and related genera such as Myrrhis, 
Chaerophyllum, and Scandix. Furthermore, Os- 


1148 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


GURE 19. Geographic distribution of Osmorhiza 
occidentalis. 


morhiza, as treated here, is considered to rep- 
resent a distinct ПОЕНЕ group. For these 
reasons, G/ycos luded in Os- 
morhiza and placed in the monotypic subgenus 
Glycosma. 


1. Osmorhiza occidentalis (Nutt.) Torrey. С/у- 
cosma occidentalis Nutt. in Torrey & A. 
Gray, Fl. N. Amer. 1: 639. 1840. Osmorhiza 
pies (Nutt.) Torrey, Bot. Mex. bound. 
surv. 71. 1859. Myrrhis occidentalis (Nutt.) 
A. Gray, Proc. Amer. Acad. Arts 7: 346. 
1868. Washingtonia occidentalis (Nutt.) 
Coult. & Rose, Contr. U.S. Natl. Herb. 7: 
67. 1900. TYPE: U.S.A. Oregon: “Western 
side of the Blue Mountains,” Nuttall s.n. 
[lectotype, NY! (designated by Coulter & 
Rose, Contr. U.S. Natl. Herb. 7: 67. 1900); 
isolectotypes, BM!, GH!]. 

oe чеч A. Gray, Proc. Amer. Acad. Arts 7: 

868. Laramie bolanderi (A. Gray) A. Gray, 

r. Acad. Arts 8: 386. 1872. Osmorhiza 
аи var. bolanderi (A. Gray) Jepson, Ма- 

дгоћо 1: 120. 1922. type: U.S.A. California: 

Mendocino Co., Lambert’s Lake, Bolander 6525 

[lectotype, GH! (designated by Coulter & Rose, 

Contr. U.S. OL NYT. 7: 68. 1900); isolecto- 


types, K!, MO! 
Glycosma ambiguum A. Gray, Proc. Amer. Acad. Art: 
8: 386. 1872. vito ambigua (A. Gray) Coul м 


& Rose, Rev. №. Amer. Umbell. 119. 1888. = 
rhis ambigua (A. Gray) E. Greene, Fl. francisc 


[Vor. 71 


332. 1892. Washingtonia ambigua (A. Gray) 
. U.S. Natl. Herb. 7: 69. 
.S.A. Oregon: Marion Co., foot of 
scade Mts., Wolford’ s Orchard, Silver Creek, 
Hall 217 [lectotype, GH! (designated by Coulter 
& Rose, Contr. U.S. Natl. Herb. 7: 69. 1900); 
isolectotypes, F!, GOET!, K!, MO!, МҮ!]. 
Glycosma maxima ا‎ ded гов Club 40: 
67.1913. T U.S.A h: Juab t. Nebo, 
Rydberg & TU IR De e NY: isotype, 
RMY!). 


Plants robust, (3–)4–12 dm high; stems (1-)3- 
6(—8), erect or slightly ascending at the base, vil- 
lous to hirsute just below the nodes, villosulous 
to glabrous elsewhere, and often glaucous. Root 
system deep, extensively branched, the roots with 
a strong, heavy anise-like fragrance. Leaves bi- 
pinnate, oblong to ovate, (8—)10—22 cm long, hir- 
sutulous or more often glabrous; leaflets broadly 
md to Nous 2-10(-12) cm long, 1-4(-5) 
cm wide, , serrate and incised or lobed at 
the base; желде 5—25(—30) cm long. Umbels 
rather constricted; peduncles 2—4(—5), terminal 
and lateral, 6–18(–22) cm long; involucre want- 
ing, or occasionally composed of 1-2 minute, 
linear, foliaceous, ciliate, spreading bracts; rays 
spreading-ascending to nearly erect, (2.8-)3-8 
(-9.5) cm long; umbellets (3—)5-15 per umbel, 
(1-)3-10(-12) of them producing only staminate 
flowers; involucel wanting, or sometimes of 1 
(—2) minute, linear-lanceolate, acuminate, ciliate 
bractlets; pedicels (7—)9—22(—25) per hermaph- 
rodite umbellet, (6—8—16(-18) рег staminate 
umbellet, spreading to ascending, those of the 
hermaphrodite flowers (2-)2.5-7(-10) mm long, 
those of the staminate flowers 2—4.5(—6) mm long. 
Hermaphrodite flowers (1-)2-6 per umbellet, 
(1–)8–20(–45) per umbel, staminate flowers 
(6—8—-20(-22) per hermaphrodite umbellet, 
(73–)100–200(–225) per umbel; corolla yellow to 
greenish yellow, rather showy; styles plus stylo- 
podium (0.7-)0.9-1.4(-1.8) mm long, stylopo- 
dium (0.1-)0.3-0.6 mm long, low-conic, with a 
conspicuous disc; carpophore cleft about one- 
third of its length. Fruit linear-fusiform, slightly 
constricted below the apex, rather deeply con- 
cave furrowed, (12—)13—22 mm long, the ribs 
glabrous throughout, the caudate appendages 
lacking, or very rarely to 1.5 mm long. п = 11 
(Bell & Constance, 1957). Figures 9d and 19. 


Flowering period. May to early July. 
Habitat. Moist to rather dry forests, thickets, 
and open slopes. 


Common names. Bald cicely, Mountain 


3 
| 
l 
| 
| 
| 
j 


1984] 


sweet cicely, Sheep cicely, Sierra sweet cicely, 
Sweetanise, Sweetroot, Western sweet cicely, 
Western sweetroot. 


сена specimens. U.S.A. CALIFORNIA: Al- 
Lake, 2,440 m, Johnson 130 (CS, NY, 
UC); Humboldt Co., NW ppt. of poi Mr A. m, 


oc Co. 
S slope of Eagle Pea k, 2,440 m, SEC e E Kellogg 
5101 (UC); Mono Co., Sweetwater Canyon Creek, 
Sweetwater Mts., 2,440 m, Alexander & Kellogg 3924 
(JEPS, MO, UC); Nevada Co., S of Donner Pass, 2,600 
m, Heller 7183 (CAS, MICH, MO, NY, P, RM, UC); 
a Co., Lemmon 89 (MO, NY); Rose 34375 (K); 


— 


Siskiyou Co., Shackelford Creek, 1,220 m, Butler 1668 
f 


(CAS, MO, NMC, RM, UC); Tehama Co., 1 km 
Lassen Chalet, Lowry 849 (ILL, UC). COLORADO: Gar- 


| ngle Park, Klinger & 
Blumquist, 10 July 1959 (CS); Gunnison Co., R 
Baker 7 ШС); lata С ^ non Creek, 


W La Plata Mss. 3,050 m, Baker et al. 177 (MICH, 
O,NY,R M, UC): Larimer Co., Rabbit ПА Good- 
ding 1563 (MO, NY, RM, UC); Montezuma Co., 19 
km N of Mancos, Colyer 26 (CS); Pitkin се уана 
Lake, White River Natl. Fore eR 2 e m, КАМ, Nelso 
7720 (CS); Rio Blanco Co., 1 km SW of Wilson Creek 
Camp, 2,350 m, S. Tabar & 7. Die 368 (CS); Routt 
Co., Mts. S of Steamboat Springs, 2,595 m, Porter 5960 
(МО, NY, RM, SMU, TEX, UC). ipAHo: Bannock Со 
Mint Creek Canyon, 5 of Pocatello, Lingenfelter 685 
(NY, UC, WTU); Blaine Co., s der Creek Canyon, 
2,440 m, Thompson 14092 (С (CA S, MICH, MO, NY, 
UC, WTU); Bonneville Co., 17. 5 km SW of Victor, 
Lowry 1118 (ILL, UC); Cassia Co., Black Pine Mts., 
2,135 m, N. H. ; 


~ 


ick 8726 (МУ, UC, WTU); 
Lake, Centennial Mts., 2,665 m, Lowry 2609 (ILL, 
MONT, MONTU, UC); Lemhi Co., Quartzite Mt., 
Hitchcock 14218 (MO, NY, WTU); Owyhee Co., 3 km 
S of Silver City, Baker 8248 (NY, WTU); Teton yes 
Sof V tral Christ 5302 (NY); Twin Falls Co., 1.5 k 
S of Magic Mt. Ski Area, Holmgren & Holmgren 6013 
(00). ње ү Beaverhead Co., Red Rock Lakes, 
о 1325 (ILL, МО, UC); Cascade Co., Hawkins 

n. (MONT); Fergus Co., Half Moon ee Big Snowy 
Ms. Hitchcock 16083 (CAS, MO, MON 

C, WTU); Gallatin Co., хосаи Mts., oo & 
Bessey 4597 (K, MONT, RM, UC); Glacier Co., Mid- 
vale, Umbach 389 (CAS, MONT, WIS); Granite Cò., 


3 km W of Skalkaho Rd ES Hitchcock & Muh- 
lick 14479 , NY, UC, WTU); Mitte c Co., Mis- 
soula, Kirkwood 1228 (C (CAS, MO, MONT, UC); Park 


0., 3 km S of dessus Booth на (МОМТ); 
Silver Sow Co., Humbug Spires, Lowry 2886, 2913 
(ILL, MONT, MONTU, UC) NEVADA: Elko Co., Ruby 
Mts., Gentry & Davidse 1806 (ILL, NY, RM, TEX, 


be Mts., Tidestrom 10889 
(MO); Nye Co., N Kawich Range; 2 06 m, Beatley & 
E 11221 (CAS, NY, UC); Washoe Co., Hunter 
Creek, W of Reno, 1,830 m, Уб К MO, 
NY, RM, U UC); White Pine Co., Snake Range, Holm- 
gren & Reveal 1097 (NY, TEX, UC). OREGON: Baker 


LOWRY & JONES—OSMORHIZA 


1149 


Co., Powder River, Cusick 1819 (JEPS, P» Clack- 
amas Co., Goodding & Eran 27 June 1927 (OSC); 
Clatsop Co., Saddle Mt.. 715m, Cham reda ten (OSC, 

; Crook Co., 3 km у of Och hoco Summit, Krucke- 
berg 2153 (RM, UC, WTU); Deschutes Co., Ireland 
2663 RE Grant Co., 7 km S of Long Creek, Lowry 
1094 (ILL, MO, NY, , UC); Harney Co., Steens 
Mt., ps 894 (ILL, OSC, UC); Jackson v Green 
Springs Mt., Constance et al. 3629 (NY, SMU, UC); 
Klamath Co., 1.5 km N of Keno, Peck 2 (CAS, 


H, GOET, K, MO, NY); Tillamoo 
bers 4096 (OSC); ha Co., Gales Creek, near 
Forest Grove, Thompson CAS, MO, WTU); 
Wheeler Co., Wolf не "Сотим 7540 К К, NY, 
RM, UC, WTU). Hollow 
Canyon, 1,615 m, Ре 13739 (ЕМ, UC). Garfield 
Co., 16 km E of Cedar Breaks, 2,450 m, Graham 867 9 


cock 1399 (МО); Su 05 Bear River, 
Uintah Mts., Payson & Payson 4936 (CAS, MO, RM, 
UC); Co., Pro ,440 m E. Jones 5587 


ricane Ridge, Kuramoto, 18 July 1966 aper IN 
Co., Upper Cle Elum River, Kruckeberg 6 (CAS, 
NY, RM, UC, WTU); Okanogan Co. i hal Pass, 
1,525 m, Thompson 10881 (MO, NY, WTU); Spokane 
E Mt. Carleton, Kraeger 282 (NY, UC); Yakima Co., 
Mt. Aix, 1,830 m, Thompson iid (CAS, a? 
MO, NY, SMU, UC, G: Big Horn Co., 
Big Horn Mts., 2,835 m, СА. 1 790 (CS); ace 
Co., Lost Creek, k, Medicine Bow Mts., Porter 4076 (CAS, 
RM, SMU, TEX, UC); Sublette Co., Middle Piney 
Lake, 2,500 m, 6 5034 (CAS, МО, RM, SMU, 
ie Teton Co., 5 km W of Teton Pass, Lowry 1123 
ID UCI Uinta c Teton Mts., Nelson & Nelson 
uid (BM, ILL, K, MO 
CANADA. ALBERTA: Chief M 


pm 


nt'l. Hwy., Waterton 
(NY 


2102 оха, Mountain Hill, W of Pincher Creek, Moss 
56 (DAO); W of Beaver Mines, Moss 825 (DAO) 
ISH COLUMBIA: near int'l. boundary, between 
bia River and Kettle ust 1,220 m, Macoun 646 
(NY); near aid m, Macoun, 10 July ee 
(NY); Lightning Lake, cane Prov. Park, 1,220 пл, 
Beamish & a 60770 (DAO, Roh n 30, Flat- 
head Rd., Bell & Davidson 1 ig (DAO); 9 km SW of 
Rossland, Calder et al. 9460 (DAO); Mt. убаа SW of 
Penticton, Calder & Savile 11750 (DAO, UC); 1.5 km 
E of Phoenix, Calder & Savile 33076 (DAO); 21 km 
о, 900 m, McCabe 6572 (UC); 3 km N of 
Howell Creek Bridge We Flathead Rd., 1,525 m, Taylor 
& Ferguson 1018 (DAO, UC); 13 km N of Flathead 
Customs, Taylor & prie 2039 (DAO). 


II. Osmorhiza Raf. subg. Osmorhiza 


Osmorhiza grr Euosmorhiza Drude in Engl. & Prantl, 
Nat. Pflanzenfam. 3*: 153. 1897. nom. illeg. 


1150 
Scandix subg. Uraspermum (Nutt.) Koso-Polj., Bull. 
oc. Imp. Naturalistes Moscou 29: 143. 1916 

Plants slender to rather stout; stems not 
densely clustered, 1–3(–5), never glaucous. Root 
system shallow to deep, diffusely branched. 
Leaves 2-3-ternate; petiole bases moderately to 
densely ciliate. Primary umbel with more her- 
maphrodite and fewer staminate flowers than the 
secondary and later flowering umbels; staminate 
umbellets 0—4(—6) per umbel; staminate flowers 
0-90(-125) per umbel; corolla white, or var- 
iously tinged with green, pink, or purple. Fruit 
hispid with retrorse bristles, or occasionally gla- 
brous, with short to very long caudate append- 
ages (rarely lacking). 


IIa. Osmorhiza Raf. sect. Osmorhiza 


r § [sect.] енер (Raf.) Kuntze, Lex- 
n 582. 1904, pro 
с: 2. [sect.] = мй чири Koso-Polj., Bull. Soc. 
Imp. Naturalistes Moscou 29: ~ Papas pro parte. 
Osmorhiza sect. Aristatae Constance & Shan, Univ. 
Calif. Publ. Bot. 23: 112. 1948, | nom. nud. 


Involucre composed of (1—)2—3(—5) linear to 
pi ret reflexed bracts; involucel conspicu- 
s, composed of 3-6 reflexed bractlets. Styles 
including stylopodium) 1—3.6 mm long, stylo- 
m 0.4—0.8 mm long, high-conic, lacking a 

аа. 
There is no doubt that the three members of 
Osmorhiza sect. Osmorhiza (O. claytonii, O. ar- 
шо, oss EE longistylis) are e very closely day 


authors (e.g., Gray, 1859: Clarke, 1879; ae. 
1891; Boivin, 1968) have even treated them as 
conspecific. These taxa, however, appear to rep- 
resent distinct, natural populations. The Asian 
O. aristata is intermediate between the North 
American O. claytonii and O. longistylis for many 
characters but is clearly distinct for a number of 
others, including pedicel length and fruit shape. 
The North American representatives of this 
section are completely separable from each other 
by many characters, including style length, total 
number of flowers per , number of sta- 
minate flowers per umbellet, and pollen grain 
morphology (Lowry, 1976; Lowry & Jones, 
1979a). Every one of the more than 2,250 her- 
ium specimens examined was clearly refer- 
able to one or the other of the two species; not 
a single individual exhibiting an intermediate 

found. While 

pollen flow is likely in the numerous sympatric 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


populations, there is по indication of any natural 
hybridization or gene flow between O. claytonii 
and О. longistylis. | 


le 


ment of Osmorhiza тани ind: о. кобун: 
as distinct at the specific level (Lowry, 1976; 
Lowry & Jones, 1979a). The pollen grains of the 
two species have significantly different ratios of 
polar axis length to equatorial diameter (P/E ra- 
tio). Those of O. claytonii are generally prolate 
in shape, i.e., their P/E ratios are between 1.33 
and 2.00 (Erdtman, 1969; Kapp, 1969). By con- 
trast, the grains of О. /ongistylis are perprolate, 
with P/E ratios greater than 2.00 


2. Osmorhiza aristata (Thunb.) Rydb. Chaero- 
phyllum aristatum Thunb., Fl. Jap. 119. 
1784. Myrrhis aristata (Thunb.) Sprengel, 
Pl. Umbell. 29. 1813. Uraspermum arista- 
tum (Thunb.) Kuntze, Revis. gen. pl. 1: 270. 
1891, pro parte. Osmorhiza aristata (Thunb.) 
Rydb., Bot. surv. Nebr. 3: 37. 1894, pro 
parte (exclusive of North American popu- 
lations). Scandix aristata (Thunb.) Koso- 
Polj., Bull. Soc. Imp. Naturalistes Moscou 
29: 143. 1916. TYPE: Japan. Thunberg s.n. 
(holotype, UPS!). 


Osmorhiza laxa Royle, Ш. bot. Himal. 233, pl. 52, fig. 
1. 1839. Washingtonia ўр (Royle) Koso-Polj. 
. Asiat. Ross. 15: 52. 1920 


Polj. in Fedtschen 
pro syn. Osmorhiza aristata var. laxa (Royle) 
Constance & Shan, Univ. Calif. Publ. Bot. 23: 
130. 1948. TYPE: India. Punjab: “Simore [Sirmur] 
in the Himalayan Mountains," Royle s.n. [lecto- 
type (designated herein), КІ; isolectotype, K!]. 

О. 1 & Zucc., Abh. Math.-Phys. 
CI. Kónigl. Bayer. Akad. Wiss. IV. 2: 203. 1843. 
Based on Chaerophyllum aristatum Thunb. 

. Schmid 


29: 143. 1916. Washingtonia amurensis (Max- 
im.) Koso-Polj. in Fedtschenko, Fl. Asiat. Ross. 
15: 50. ie pro syn. ТҮРЕ: U.S.S.R ae vi. 
sk п the lower Amur River, near the vi- 
cinity of учи mouth of the Dondon, ‘at ае. іп 


of ses ILL!; plus two authentic specimens 
sotypes), K!, LE, photographs at ILL!J. 

оа: a clayton (Michaux) C. B. Clarke in Hook., 
1. India 2: 690. 1879, pro parte (exclusive 

of M. gei Michaux and M. longistylis Tor- 


Ойна aristata var. montana Makino, J. Jap. Bot. 
2: 7. 1918. Osmorhiza montana (Makino) E 
kino, J. Jap. Bot. 5: 28. 1928. Osmorhiza amuren 


1984] 


sis var. montana (Makino) Kitagawa, Rep. Inst. 
Sci. Res. Manchoukuo 2: 279. 1938. Type: Japan 
Honshu: Totigi, apex! очна, T. Makino 
ot been 
: . Ross. 15: 51. 1920. (No 
type material has been located.) 
Washingtonia o: subsp. occidentalis Koso-Polj. 
in Fedtschenko, Fl. Asiat. Ross. 15: 51. 1920. (No 
type material has been located.) 


Plants rather stout, 3-8(-10) dm high; stems 
-2(-3), erect to ascending, villous to glabrate. 
Root system rather deep, spreading, with an an- 
ise-like scent. Leaves 2-3-ternate, deltoid to 
broadly ovate, 7-20 cm long, hirsutulous (es- 
pecially along the veins) to glabrescent; leaflets 
oblong-oval to ovate-deltoid, (1.5—)2.5-9 cm 
long, 1–6 cm wide, obtuse to acuminate, coarsely 
serrate, incised, sparsely lobed to deeply pinnati- 
fid at the base; petioles 5-25 cm long. Umbels 
loose; peduncles 2-3(-4), terminal and lateral, 
(3.52)5-25 cm long; involucre composed of 1– 
3(-5) linear to lanceolate, foliaceous, ciliate, re- 
flexed bracts, or sometimes wanting, each (1—)2— 
10(-25) mm long, (0.3-)0.5—1.3(—4.5) mm wide; 
rays spreading to ascending, (3.5—)4.5-11 cm long; 
umbellets 3-6 per umbel; involucel of (3—)4—5 
linear to lanceolate, ac станы ciliate to hirsu- 
tulous € each (1-)2.5-10(-11) mm long, 
0.5-1.7 m wide, stro ee reflexed; pedicels 
(4-)5-15 per aa spreading, those of the 
hermaphrodite flowers (5-)9-30(-33) mm long, 
those of the staminate flowers 2.5-9(-10) mm 
long. Hermaphrodite flowers 2-6(-7) per um- 
bellet, (10-)15-30(-38) per umbel, staminate 
flowers (2—)3—7(—1 


—2.4) mm long, 
stylopodium (0.4—)0.45—0.7 mm long, high-con- 
ic, lacking a disc; carpophore cleft about to the 
middle. Fruit linear-clavate, obtuse or abruptly 
acute at the apex, concave furrowed, (13-)15- 
22(-23) mm long, the ribs sparingly to moder- 
ately hispid with retrorse bristles, especially to- 
ward the base, the caudate appendages (4.5—)5.5— 
11 mm long. n = 11 (Wanscher, 1932). Figures 
9a and 12. 


Flowering period. April to early June. 
Habitat. Moist woods, at lower and middle 
po 
mmon names. Shari (Nepalese), Hsiang 
Кёп Ts’ao Shu (Chinese), Miyama-yabu-ninzin, 
Nagajirami, Nagazirami, Onaga-yabu-ninzin, 
Yabu-ninjin, Yabu-ninzin (all Japanese). 


LOWRY & JONES—OSMORHIZA 


1151 


Representative ground CHINA. GUIZHOU: Ca- 

valerie & Fortunat 2961 (K, P, UC). HUBEI: Henry 5789 
(BM. K, P; S of W жару 2 10 
P) Paok'ang, Wilson 1 
huang-chen, Chiao & Cheo 3541 (NY). JIANGXI: 
295 (NY). JILIN: Manchuria, 
M.K. P. SICHUAN: Seaman 
Chu 3336, 3495 ade Tchen-keou-tin, 1,400 m, Far, 
72 (K, P, UC); Cheto Valley, Капе п пр (Tachienlu) 
Dist, 3, 100 т, Smith 10963 (BM); Kiala, Soulié 1 al 
(P); S of regi Wilson 1044, pars (K). XIZA 
Rongshar Valley, N of Mt. Everest, 2, E m, deem 
183 (K); Mind 97555 Без 


and Lilung, 29°04'N, 93°56’E, 3,100 m, Ludlow et al. 
4460 (BM); Peding, Tsangpo Valley, 29°30'N, 94°20’E, 
3,000 m, Ludlow et al. 4533 (BM); Pe, 29°31'N, 94°54’ E, 
4 iae d , Ludlow et al. 5320 (BM). YUNNAN: Ma-eul- 
an, 3, 000 m, Delavay 3902 (P); Yungning, Handel- 
jube 7049 (N —not seen; reported in Constance & 
ае теа N > M 2,600 m, Henry 10233 (K, 
F G: W of Tien-mu, Hu 1654 de 
PAN. HOKKAIDO: Hak i, Je 
Таке Albrecht ѕ.п. (К); Hakodate, Faurie 473 (Р); 
anai-tyo, Iwanai, сани. М: ue x Kamikawa-tyo, 
rite of Mt. Kuro-dake, Н 6628 (UC); Minami- 
huramo-tyo, Mt. Tom и. "Hiroe 6730 (UC); эрч 
betu-tyo, Monbetu, Faurie 709 (К, Р); гр dus 
bun Island, Hiroe 761 ; (UC); Risiri- -tyo, Mt. Ri 
Rishiri Island, Hiroe н 


r 


ken, Yokobori, Yushun, 23 July 1905 (NY); Aomori- 
ken, Moura, W coast of Natsudomari-hanto, Mimoro 
et al. 3551 m ре, Ikao, Lyle, May 1908 
(BM); Hukusima-ken, Asakawa, Mizushima, 27 Apr. 
1952 (UC); served foot of Mt. Tsukuba, Furuse, 
18 Apr. 1956 (UC); Iwate-ken, Nagamachi, lishiba, 16 


t. Kasuga, de 16236 (00); 
прага, Faurie 79 -hu, Mt. 
59 ee "ОС, W 15); Sai- 
ass, Kobayashi, 3 Aug. 1961 (UC); 
аз "foot of M LE Hiroe 68 (K, NY, UC, 
WIS); Sizuoka-ken, ascent way of Fujinomiya, Mt. Fuji, 
2,000 m, Hiroe 12683 (UC); Toivoo, Komae, Suzuki 
77007 (UC); Totigi-ken, Lake Kirikomi, Nikko City, 
Ono & Kobayashi, 4 Aug. 1963 (UC); Toyama-ken, 
atsuo village, 17 km SW of Toyama, Kirino 172 у; 
Yamagata-ken, Kabuto-iwa, я al. 708124 [sic] 
(BR, MO); T usan Shrine, base of 
of ено Charette 1680 


Niigata-ken, N 
cy ы 600 m, e 


1,200 m, Tokio 1009 
Mt. Ohtaki, 800 m, Hiroe 15500 (UC). 


KANGWON DO: Ullun un 
2290 (MICH); Mt. Odae, poem 8 (MIC H). 
KYONGGI Do: Kwangnung, Chung 2614, дё (MICH). 


1152 


BHUTAN. Chalimarphe Timpu, 2,290 m, Cooper 1405 
(BM); Drugge Dzong, 3,050 m, Ludlow et al. 16209 


(BM). 

NEPAL. PALPA: Lukarban Khola, W of Beni, 3,000 
m, Stainton et al. 451 (BM); Lete, S of Tukucha, Kali 
Gandahi Valley, 3,000—3,200 m, Stainton et al. 1034, 
5600 (BM) 

INDIA. HIMACHAL PRADESH: Raiengarb Mut, 2,135 m, 
Gamble 26799 (К); т, Maidan, Parbatti Мены 
3,050 m, Nath (NY); Kulu-Lahoul, гира ab, Dru 

ока. 23131, 23132 ae UC); Nagzuda, Simla 
Hills. 2,250 m, Hooker f. & Thomson, 9 June 1849 (K, 
P). JAMMU: Jangla, 2,750 m, Dudgeon & Kenoyer 386 
MO); Jammu, 2,000 m, Hooker f. & Thomson, 31 
ve 1868 (K). KASHMIR: Pahlgam, E рэн River, 43 
N of Anan nd [Islamabad], 2,290 m, Dickason 

с ау Pahlgam, 2,200 т, иа 9271 (NY). 
UTTAR PRADESH: are udhi, Byans, Kumaun, 2,600 
m, Duthie 5595 (BM, K); Bamon ја меки 2.135 m, 
Duthie, 15 May 1897 (P); Jaunsar Bahar, near Kinani 
Pani, 2,600 m, Gamble 1136 (K); Jaunsar, Сыгыр: 
Gamble 23589 (К); Kedar Kantah Mts., in iir 
0 (P); Kumaon, Lahai, 2,285 m, Strac і 
dn s.n. (BM, BR, K) Garhwal, Re mON 1254 


). 

PAKISTAN. KASHMIR: Kishenganga Valley, Rd. to 
Nanga Parbat via the Gangabal Lakes, Keran, 1,850 
m, Stewart 2 Ser 17 bee oos с): 

U.S.S.R tskoe Ozero Tulkuy, 
Koshurnikova on У Vishniona, er July 1927 (NY). 

ү: 1 mur River, at Dshare, 
Галан нуе; 18 Jul J 3N 1855. (К. LE). PRIMORSKIY KRAY: 
Kedrovaja Padj Reservation, SW of Vladivostok, Go- 
rovoy 8 (UC); S Ussuriysk, Pos’yet Dist., Saberkin 890 
(NY). SACHALIN: Sachalin Island, Schmidt 5.п. (К). 


Royle (1839) considered Himalyan popula- 
tions of Osmorhiza conspecific with short-styled 
populations in North America now treated as O. 
claytonii (Michaux) C. B. Clarke, and accepted 
the name О. brevistylis DC. for them. Similarly, 
several authors (e.g., Gray, 1859; Hayata, 1911, 
1912) incorrectly applied the name О. /ongistylis 
(Torrey) DC. to Asian populations of Osmor- 
hiza. 

Constance and Shan (1948) treated all the Asian 
representatives of Osmorhiza under O. aristata, 
although they distinguished two varieties on the 
basis of characters of the leaves. Quantitative 
evaluation of morphological characters, how- 
ever, does not support the recognition of infra- 
specific taxa within O. aristata (Table 4). 


3. Osmorhiza claytonii (Michaux) C. B. e 
Myrrhis claytonii Michaux, Fl. bor.-a 

1: 170. 1803. Chaerophyllum claytonii (Mi. 

chaux) Persoon, Syn. sp. pl. 1: 320. 1805. 

Osmorhiza claytonii (Michaux) C. B. Clarke 

in Hook., Fl. Brit. India 2: 690. 1879, sensu 

stricto (exclusive of M. longistylis Torrey 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


and O. /axa Royle). Washingtonia claytonii 
Semen Britt. in Britt. & Brown, Ill. fl. 2: 

18 Scandix claytonii (Michaux) 
Eg Bull. Soc. Imp. Naturalistes 
Moscou 29: 143. 1916. ТУРЕ: U.S.A. “Jn 
montibus Alleghanis," A. Michaux s.n. (ho- 
lotype, P!). 


Scandix dulcis Muhlenb., Cat. pl. 31. 1813. Myrrhis 
dulcis (Muhlenb.) D. Eaton, Man. bot. 326. 1818. 
Uraspermum dulce (Muhlenb.) Farwell, Amer. 
Midl. Naturalist i 273. 1925. Based on Myrrhis 
claytonii Mic 

Uraspermum ин Bigelow, Fl. boston. 112. 1824. 

.A. Massachusetts: ““Woods on the Con- 
cord turnpike, ” Bigelow s.n. (No type material has 


been 
сз: газа DC., Prodr. 4: 232. 1830. Myr- 
rhis brevistylis (ОС) Dietr., Syn. р, 2: 984. 1840. 
aristat brevistyle (DC ) 
Kuntze, Revis. gen. pl. 1: 270. нөт. Osmorhiza 
aristata var. brevistylis (DC.) Boivin, Phytologia 
17: 104. 1968. TYPE: U.S.A. New York: Range 
Pa. West Point, Torrey s.n., 1828 кемур О (des- 
gnated herein), G-DC!; eat ay (2), G-DCI]. 
simo iba villosa Raf., Med. fl. 2: 249. 1830 m **yi- 
losa"). (No type material has didi located.) 
Osmorhiza cordata Raf., Med. "a 2: 249. 1830. (No 
ype material has been located.) 
Uraspermum aristatum a m brevis Ма ] p 
integrifoliolum Kuntze, Re 
1891. (No type material has bien Bu 
Uraspermum dulce var. laevicaule Farwell, Amer. Midl. 
Naturalist " p Hs TYPE: U.S.A. Michigan: 
, O. A. Farwell 5267 [lec- 
totype, BLH! ашу by McVaugh et al., Bull. 
Cranbrook Inst. Sci. 34: 79. 1953); isolectotype, 
H 


fenhen 


GH]. 
Osmorhiza claytonii f. brevipilosa Salamun, nom. in- 
ra this name was provided with a Lat- 
т man and citati specimen, it 
was never effectively нА hed, having only been 
proposed in Salamun’s dissertation (1950: 82). 


Plants Eos stout, 4-8(-10) dm high; stems 
1-2(-3), erect to ascending, villous, villosulous, 
or sometimes essentially glabrous. Root system 
shallow, more or less horizontally spreading, the 
roots fibrous and limber, rank smelling, or some- 
times weakly anise-scented. Leaves 2—-3-ternate, 
more or less broadly ovate, 10—30 cm long, hir- 
sutulous; leaflets ovate to lanceolate, (3—)4—8 cm 
long, 1.5—3 cm wide, acute or acuminate, serrate- 
dentate, often parted or divided at the base; pet- 
ioles 5—15 cm long. Umbels loose; peduncles 2-3 
(-4), terminal and lateral, 3-10(-13) cm long; 
involucre wanting, or often composed of 1—2(-3) 
minute, linear-lanceolate, foliaceous, ciliate, re- 
flexed bracts; rays ascending, 2-8(-10) cm long; 
umbellets 3—5 per umbel; involucel of 3—5 linear- 
lanceolate, attenuate, ciliate bractlets, each 2—5 


1984] 


(-6) mm long, 0.4-1 mm wide, strongly reflexed; 

pedicels 4—7(-8) per umbellet, ascending, those 

of the hermaphrodite flowers (4—)6—12(—15) mm 
5 


5 
ga 
e 
= 
о 
uo 
[0] 
o 
| 
e 
a 
о 
ا‎ 
3 
B5 
~ 
oO 
zn 
о 
= 
[4 
| 
Ф 
~ 
> 
L 
دن‎ 
л 
| 
л 


ре 

(including stylopodium) 1—1.5(—1.7) mm long, 

stylopodium 0.5-0.75(—0.8) mm long, high-con- 

a E a conspicuous disc; pollen prolate in 
carpophore cleft about one-fourth of its 

ES Fruit oblong-fusiform, tapering to a short, 

attenuate beak at the apex, concave furrowed, 


cially toward the base, the caudate ас stn pa 
4.5-8.5 mm long. n= 11 (Bell & Constance, 
1957). Figures 9b and 10. 


Flowering period. April to early June. 
abitat. Dense to open deciduous forests, 
tending toward the more moist, lower areas. 
Common names. Clayton sweetroot, Hairy 
Sweet cicely, Sweet jarvil, Woolly sweet cicely. 


— specimens. U.S.A. ALABAMA: Mad- 
ville, Baker, 23 May 1897 (MO, NY). 


ison Co., Hunt 
AR ў VB cc о., Thomas 38940 (TENN) 
CONNECTICUT: Hartford Co., Southington, Bissell 83 


SE 
5. 
т 
a 
= 
Q 


· (NY). 

(GA). ILLINOIS: Bureau 80102 (ILLS); 
Champai о., Bro Woods, N of Urbana, 
Lowry 1206 ers Crawford Со., Evers 43236 (ILLS); 
Hancock Co., M. J. Warnock 215 (ILL); Lake Co., 

Waukegan, Umbach 5355 (UC); La wá Co., Starved 
Rock Ag OMIM et al. 27 (GH, NY, UC); 
Lee Co., Pew of Franklin Grove, G. N. Jones 
15839 (ILL, MO); Manns Co Spittler Woods, Mt. 
Zion, Lowry 545 (ILL, MO, UC) McLean Co., Funk's 

ove, S of Bloomington, Lowry 1140 (ILL); Piatt Co., 

Allerton Park, near Monticello, Lowry 211 (ILL, MO). 
INDIANA: Adam a: 3 km W of Geneva, Deam 50233 
(WIS); Fountain Co., Portland pens Lowry 1208 (ILL); 
Lake 2 ,6km N of Schneider, Salamun, 5 Aug. 1947 
(ILL, UC); Morgan Co., 4.5 km N of Martinsville, 
Heiser & Smith, 19 May 1950 (ILL, MO, 

Co., Turkey Run St. Park, Salamun, 6 Aug. 1 
MO). io WA: Os 

m 8. Aug 


& er Caves, Brown 40 осма Се А.Э 
om Boyd Со. line, Smith et al. 3 240 (F, 
n Co., Bere 4294 (MO). 


LOWRY & JONES— OSMORHIZA 


ки Cas Pike s Peak, Мог Shi- 
of 


1153 


1913 (WIS); Somerset Co., gt аа, Eaton, 30 June 
1903 (LL, NY). MARYLAND: All Co., Cumber- 
land, Shriver s.n. (NY); Howard Co., ооа City, Ar- 
séne, 26 July 1916 (MO). MASSACHUSETTS: Berkshire 
Co., Florida, Deerfield River, Fernald & Long 10088 
(GH); ал Co. dip cpi Матт, 6 June 1881 
м: Агепа „ Mud Lake, Sharp et al., 
20 сачы 1961 (МСН); шинди ig Big Limestone Mt., 
L’Anse, Fassett 21037 (WIS); Cheboygan Co., Monroe 
Lake, Ehlers 374 (GH, MO, US); Emmet Co., 3 km 
W of Mackinac City, McVaugh 9430 (MICH, мо 
сика Со., Gogebic одақ тари tt 19868 (Е, 
WIS), Ke eweenaw Co., Isle Royale, McFarlin dvd 
hool Со: of Gulliver, Sal- 
amun, 19 July 1946 (ILL, MO). DM Clearwater 
Co., Floating Bog Bay, Grant 2885 (MO, NY, UC); 
Co ok Co. Мик! Center, Rosendahl & Butters 4590 
uis Co., Duluth, Lakela 207 


(GH, NY); 
Wabasha Co., 10 = N of Reed’s Landing, M. J. War- 
nock 1463 (ILL). MISSOURI: Dallas Со., 8 km SW of 
Bennett Springs, Conrad 3496 arr Jackson Co., 
Kansas City, MacKenzie, 16 Баа С МО, 
Ш Creek, NE of Silex, Steyermark 25981 
(Р; NE of Saline, Palmer & 
ае 41324 (M yea Cherry Co., 
NE of Valentine, Churchill 4489 (MO, NY); C 
Co., 2 km SSE of Beemer, Churchill 5516 (NY); Hixon 
Со., Ропса, удица 4 ; Washington Co., 4 
km NW Calhoun, Churchill 5328 (MO). NEW 
HAMPSHIRE: Grafton Co., N Wo жк Fernald 386 
(BM, BR, CAS, DUKE, С, GH КА О, 
M , NY, PH, RM, SMU, TENN, ; UC 
US). NEW JERSEY: Bergen Co., W o eed i Wis Ison, 
19 July 1915 (NY); Middlesex n m арн 
СОЕТ). NEw YORK: Chautauqua Co., 
Lake Chautauqua, Churchill, 2 Aug: 1896 n oy sented 
Co., Big Hollow, Barnhart 2344 (NY); Herkimer Co., 
2.5 km SW of Dart Lake, Smith 2504 (WIS); Monroe 
Co., ven green EP 4164 (UC); Rensselaer о» 
wick, Hous вте (МО, o NORTH CA 
LINA: я Co. ue Ridge ы 
оп Hwy. 276, Lowry i 153 T и Со., 1 кт 
Lowry 1 152 (ILL, UG) 


w 


(M : rks Co 
Rhodora 74: 393. 1972); Richland Co., Leonard, Ste- 
vens 1343 (UC). OHIO: pide Co., Athens, Abbot 12 
eland, Greenman 710 (GH, 


H, MO). icu ren отри. о. 


E (PH, UC); Warren Co., Pohl 2461 
га adford 31734 (KANU). 
SOUTH DAKOTA: Broo gs Co., Warren's Woods, Wil- 
liams & Thordaer, 17 nah 1893 (MO); Roberts Co., 
e Stone Lake, Over vid- 
, Joelton, Svenson 93 (GA, GH); Grainger £o. 
SRUT 43562 (TENN); Greene Co., Paint Creek, 1 k 
N of French Broad River, Bufford. et al. 18119 (MO); 
Knox Co., Lane's Creek, Sharp & Herster 584 (NY). 


1154 


MONT: Bennington Co., Red Mt., Arlington, e 
mour 21637 (MO); Caledonia Co.; Pea cham , Blan 


of Plummer’s Island, Mathias 1394 (CAS, 
GH, MO. id RM, UC, US); Smythe Co., ger) 
Hill Gap, Walker Mt., Small, 13 June 1892 (F, G 
K, MO, P, UC). west viRGINIA: Cabell Co., па. 
Valley, Williams & Gilbert 445 (F, GH, MO, NY, 
SMU); Ohio Co., eeling, Mertz 1042 (F). Wis- 
CONSIN: Bayfield Co., Koch 6881 (KANU); Forest Co., 
He km SE of Crandon, Stearns, 23 June 1946 (NY); 
n Co., 7 km W of Monticello, Salamun, 10 July 
1947 ( (ILL, MO); Outagamie Со., Appleton, Chandler, 
18 May 1896 (UC); Trempeauleu Co., NW of Trem- 
peauleu, M. J. Warnock 1470 (ILL). 

CANADA. MANITOBA: 6.5 km N of Moon Lake, gd 
Mt. Nat'l. Park, Mosquin 6066 (DAO). NEW BRUNSWI 
Albert Co., Roberts 64-1655 (DAO); Charlotte бе, 
Grand M 
5 (DAO). МОУА 

1 Breton Co., George River, Bissell & Lin- 
der 22050 Ai: знай Co., Mabou, Robinson 229 
(NY); У a Co., Dingwall, Aspy Bay, Churchill, 7 
July 1909 ( (МО). ONTARIO: Algoma Dist., Jenkins 4909 


,M 1.5 km SW of Meadford, Soper 
& Shields 4603 (MO); Manitoulin Dist., Manitoulin 
Island, Salamu 


Thamesford, Soper & Shields 4506 (MO); Rainy River 
Dist., 8 km below 
, Cody & Calder 
540 (DAO, MO); Thunder Bay ag N bank of Pigeon 
River at Middle Falls, Garton 2062 (DAO , МО). PRINCE 


(а Richm 

Knowlton, 26 July 1923 (G (GH ^ 

Lac Tremblant, Churchill, 8 "ien 1922 (GH, MO). 
Osmorhiza claytonii is fairly uniform through- 

out its range. Although two varieties have been 


(Farwell, 1925; Salamun, 1950), examination of 
a large number of specimens shows that this 
character is highly variable in O. claytonii, and 
neither variety is upheld in this interpretation 
(Lowry, 1976; Lowry & Jones, 1979a). 


4. Osmorhiza (Torrey) DC. Myrrhis 
longistylis Torrey, Fl. U.S. 310. 1824. Os- 
morhiza longistylis (Torrey) DC., Prodr. 4: 
232. 1830. Uraspermum aristatum B [subsp.] 
longistyle (Torrey) Kuntze, Revis. gen. pl. 
1: 270. 1891, pro parte (with two varieties: 
laciniatum and subintegrifoliolum). Wash- 
ingtonia longistylis (Torrey) Britt. in Britt. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


& Brown, Ill. fl. 2: 530. 1897. Scandix lon- 
gistylis (Torrey) Koso-Polj., Bull. Soc. Imp. 
Naturalistes Moscou 29: 143. 1916. Os- 
morhiza aristata var. longistylis (Torrey) 
Boivin, Phytologia 17: 104. 1968. түре: “In 
wet meadows near Albany, N.Y. Tracy. Near 
Geneva, N.Y. Paine. June. Near Hudson, 
N.Y. Alsop & с." (None of these syntypes 
has been located; only an authentic speci- 
men collected by Paine was found, and is 
herein designated the neotype.) Canada. 
Québec: Montreal, Paine s.n. (neotype, NY!). 


Osmorhiza dulcis Raf., Med. fl. 2: 249. 1830. Myrrhis 
dulcis (Raf. Raf., Good book 53. 1840, pro syn., 
non Scandix dulcis Muhlenb. TYPE: U.S.A. “Mts 
Alleghy [sic],” Rafinesque s.n. [lectotype, PH! 
(designated by Lowry & Jones, Amer. Midl. Nat- 
uralist 101: 26. 1979); possible syntypes, G!, E 

rar dulce Fischer ex Steud., Nom PE 
33 41, non t Muhlenb. A E. 
materi al has been loca 

Osmorhiza clayton ta C. B. Clarke in Hook., 
Fl ndia 2: 690. 1879, pro parte (exclusive 

of M. с 7 pen Michaux and O. ade oyle). 

Osmorhiza aristata (Thunb.) Rydb., urv. Nebr. 

894, pro parte ае of Porth popu- 
lations). 

Osmorhiza longistylis var. villicaulis Fern., Rhodor 
10: 52. 1908. Washingtonia longistylis var. villi- 
caulis (Fern.) Coult. & Rose, Contr. U.S. Natl. 

erb. 12: 443. 1909. Uraspermum aristatum var. 
villicaulis (Fern.) Farwell, Pap. Mic Acad. 
Sci. 1: 96. 1931. TYPE: U.S.A. Penn 
caster Co., On t 

Heller, 21 June 1901 
(holotype, GH!; isotypes, F!, G!, US!). 

PUE cciam ! longistylis var. brachycom a S. F. Blake, 

ra 25: 110. 1923. Washingtonia es 
var. за левим (S. F. Blake) House, Bull. 
York State Mus. 254: 529. 1924. TY EA 
Maryland: Montgomery Co., slope in e vi- 
сву of Cabin John, x x Blake 6902 (holotype, 
US!; isotypes, GH!, T 

быны longistylis var. фан та Зајатип, m 

Midl. Naturalist 47: 253. 1952. түре: U.S.A. Sout 
ota: Lawrence Co., wooded 

Creek in Spearfish Canyon, approx. 

Bridal Veil Falls, 4. L. Thorne, 12 Aug. 1949 

(holotype, UWM!; isotype, WIS!). 


Plants rather stout, 6-10(-12) dm high; stems 
1–2(–3), erect, densely pilose to villous, or often 
glabrous. Root system rather deep, tending to- 
ward vertical orientation, the roots carnose 
(breaking with a snap), with a sweet, anise-like 
scent. Leaves 2—3-ternate, broadly ovate, 8-25 
cm long, sparsely hirsutulous (especially along 
leaflets ovate to oblong 
lanceolate, (334-10 cm long, 2-5 cm wide, acute, 
serrulate-dentate, often incised or parted at the 


the 


1984] 


base; petioles 5—16 cm long. Umbels loose; pe- 
duncles 2—4, terminal and lateral, 5-13 cm long; 
involucre composed of 1—3(—4) linear to lanceo- 
late, foliaceous, ciliate, reflexed bracts, each 5- 
10(-15) mm long, 1-1.5 mm wide; rays ascend- 
ing, 1.5—5(–7.5) cm long; umbellets 4–6(–8) per 
umbel, (0–)1–3 of them producing only stami- 
nate flowers; involucel of 4—6 linear-lanceolate 
to ovate, acuminate, ciliate bractlets, each 2.5— 
6(-7) mm long, 0.7-1.8 mm wide, often strongly 
reflexed; pedicels (7-)9-18 per hermaphrodite 
umbellet, 3—13 per staminate umbellet, ascend- 
ing, those of the hermaphrodite flowers 4–8(–9) 
mm long, those of the staminate flowers 3—6(—8) 
mm long. Hermaphrodite flowers (2—)3—5(—7) рег 
umbellet, (8—)15—30(—33) per umbel, staminate 
flowers (3—)4—10(—14) per d um- 
bellet, (23—)35—7 5(—86) per orolla white, 
showy; styles (including Орса) 2-3.6 mm 
long, stylopodium (0.4—)0.5—0.75(-0.8) mm long, 
high-conic, lacking a disc; pollen perprolate in 
shape; carpophore cleft about one-third of its 
length. Fruit oblong-fusiform, acute at the apex, 
concave furrowed, (10—)1 5—21(-22) mm long, the 
ribs sparsely to moderately hispid with retrorse 

ristles, especially toward the base, the caudate 
appendages 4-8 mm long. n — 11 (Wanscher, 
1932; Bell & Constance, 1957). Figures 9c and 
11. 


Flowering period. April to early June. 

Habitat. Dense to open deciduous forests, 
tending toward the somewhat drier, upland sites. 

Common na Aniseroot, Longstyle sweet- 
root, Smoother sweet cicely. 

Representative specimens. U.S.A. ALABAMA: Lauder- 
dale Co., Murchis publi k holes sa Co., War- 
rior River above Hurricane Creek, Harper 144 (F, GH, 


M). CONNECTICUT: Fairfield Co., dr = 
Green’s s Farm, Pollard 3 T pee Newcastle Co., 
Cuba, Commons, 25 June 1875 (MO). E OF 
COLUMBIA: Washington, Pennel 15005 (PH). GEORGIA: 
Burke Co., Shell Bluff, Pyro 


2627 (GH, MO); D е Co. „Ма perville, Umbach, 
8 June 1897 (МО); За ду Co., Evers 72569 ae 
Jo Daviess Co., Apple River Canyon State Park, С. М. 
e 15859 (ILL, MO); Macon Co., soupa Woods, 
t. UC); McLe 
Funk's Gro Bloom SUE Lowry 1141 
(ILL); Piatt Co., pedes. Park, near Monticello, Lowry 


LOWRY & JONES—OSMORHIZA 


1155 


540 (ILL). INDIANA: Blackford Co., Hartford, Deam 
1078 а Lawrence Со., Bedfo rd, Kriebel 1879 
DUKE, GH); Marion Co., отдана Friesner 
16672 (GH, MO, M MU). 10 A: Appanoose Co., 
, Shimek, 15 May 190 02 (WIS), ‘Decatur Co, Fitz- 
patrick & Fitzpatrick, E^ May 1897 (F, 
buque Co., NW of raria ek 3 July 1929 
C); Emmet Co., Ft. Defiance St. Park, Hayden 9426 
et Poweshiek D Grinnell, M. E. Jones 145 (CAS, 
RM, UC). KA KANSAS: Cow ана Winfield, 
pipes n. (MO); Crawford Co., Holland 381 (KANU); 
Douglas Co., N of Baldwin, Croat 116 (MO); Green- 
wood Co., Stephens 2 925 { 
5 


~ 


, UC); Greenup Со., Big реке 4.5 km Кот Boyd 
Co. line, wi et al. 3581 (GH, 

0.5 km N of Sand Ripple S eu (NY); 
Union Co., MC ios: pin 296 (GH, NY, 
SMU). MAINE: Aroostook Co., Ft. Fairfield, Fernald 
2020 (GH); Hancock Со., Vue ele Rand, 18 July 
e (UC); tup Co., Vassalboro, Mast ciens 
n. (GH). YLAND: Montgo mery Co., r Cabi 
pe Blake 6902 (GH, TEX, US). m Шаадат 
Berkshire Co., New Marlboro, Churchill, 13 June 1919 
(GH, MOJ; Essex Co., Manchester, Chamberlain s.n. 

olk Co., Waverley, Andrews, 16 July 1892 
(11). MICHIGAN: Emmet km 5 of G Hart, 
McVaugh 9282 (MICH, MO); Houghton Co., Calu- 


ertson 109 (M H). MINNESOTA: Chisag 
RM 


Cas ее Ма. Mon., Moore 23192 eene MIS- 
SISSIPP. о Co., Kral 8582 (LAF); 

Lott, 28 Am 0 ов Tate Co., ees 64276 
GA, Franklin Co., Arboret tum, Gray’s 
Summit, Shap 1 201 1 (МО); Сгип@ Со., 20 km W of 
Spickard, Steyermark 11 


я : y, Pool, 21 June 1912 (МО); 
Richardson Co., 1.5 km N of Barada, Reynolds rui 
(MO, UC); Sioux Co., Stephens 16324 ( 

— Cheshire Co., — пре gel 417 (ОВ). 
., Lebanon, Kennedy s . (GH). NEW JERSEY: 
ington або. Vincetown, Long 97 die (GH); eret 

ter Co., Fogg 8564 (PH). NEW Y laware 
Harpersfield, 7. opping 166 (ILL, US): Erie Co., а 
псе Со. o., Hermon, Phelps 


D 
8 July 1901 (NY, RM, US); Golden Valley Co., Ste- 


1156 


phens 49996 (KANU); Pembina Co., 3 km S of Wal- 
halla, Willenbring 687 (MO); Richland Co., Abercrom- 


со: Devil's Backbone, near Camden, Cobbe 104 (CAS, 
G, UC); Scioto Co., Camp Gordon, Friendship, De- 
maree 10647 (CAS, GH, MO, SMU, UC). OKLAHOMA: 
Canadian Co., Devil’s Canyon, Goodman 5060 (OKL, 
UC); се Со., Сатр Еғап, Е 


Н, РН); Іа Со 
Conestoga, near Binkley’s Bridge, Heller, 21. me 1901 
(F, G, GH, US); Le 


{ : er Co., Bozeman et al. 
8812 (AUA, CAS). souTH е Brookings Co., 

Brookings, Thornber, 4 July 1894 (ARIZ, MO, U UC): 
Harding Co., W Short Pines, Visher 459 (F); Lawrence 
Co., NW of Whitewood, D'Arcy 5761 (MO). TENNES- 
SEE: Cheatham Co., 2.5 km SE of Ashland City, Kral 
26796 (UC); Davidson € Nashville, Gattinger, 28 
Mar. 1886 (F, NY, US); Knox Co., Knoxville, Ruth 
442 (MO); Lauderdale Co., Sharp 12115 (TENN). 

arra 


Island, Mathias 1392 (CAS, GH, MO, NY, UC, “a 
и. 1 km W of Williamsburg, Grimes 3601 
(NY); S , Claremont Wharf, Fernald & Long 
8386 СНА dex NY,U US). west VIRGINIA: Berkeley Co., 
E of Martinsburg, A. G. Jones 4218 (ILL, MO); Mon- 
„ Mon River, Millspaugh 173 (NY); 
Pendleton Co., Snowy Mt., Rydbe erg 9122 (NY, PH). 
WISCONSIN: Brown Co., Green Bay, Schuette s.n. (F); 
Iowa Co., Blue Mounds, Clikenian et al., 5 June 1932 
(UC); Walwort h Co., Salam 


16 km W of Douglas, Porter 4511 (RM, WTU); Sher- 
idan Co., Tongue Creek, N of Big Horn Coal Mine, 
1,100 m, Brink 1366 (ILL, MO). 

ANADA. ALBERTA: Edmonton Dist, Moss 6363 
(DAO); Medicine Hat Des Macoun 858 (GH). MANI- 


TOBA: Po -la- ,4 km N of P ааа рү 
Prairie, Boivin & Bretung 65 01 (DAO); Winnipeg Dist., 
Winnipeg, Johns 44 (NY); Thalberg, К Krinda, 20 


June 1960 (NY); н. lic Macoun & Herriot 77116 

NEW BRU : Charlotte Co., St. Andrews, 
Malte 843/29 (GH US; Kent Co., Bass River, Fowler, 
5 July 1873 (GOET, W 
Co., -= G 


H, US); North- 

um C ., Presqu'ile Park, сўе & Shields 4644 

(МО); Rainy River Dist., Garton 8862 (DA 
i alls on 


, Res 
pedia, Collins & fertig 4. л. (6 


H); Gaspé 
„ Dansereau 180 (DAO); Missisquoi Co., 


Perron 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


66-210 (DAO); piney, Co., Charlebois 1401 (DAO); 
Temiscamingue Co., Gi rard, M.- Vict от 


: m 
Estevan, Boivin & Perron 11823 (DAO); Lake Centre 
Dist., Outlook, e mir & ех 8 PAO Moose Jaw 
Dist., Moose Jaw Cree acoun ; Qu'Appelle 
Dist., Qu'Appelle Ea near cian of Lake Katepwe, 
Boivin & Dore 7591 (DAO); Wood Mountain Dist., 
1.5 km S of Willowbunch, Boivin & Gillett 8838 (DAO); 
Cypress Hills, Breitung 4719 (DAO, MO). 


Clarke (1879) included all representatives of 
Osmorhiza sect. Osmorhiza, including О. lon- 
gistylis, under the name O. claytonii. Similarly, 
MacMillan (1892) included О. /ongistylis in his 
broad concept of Myrrhis aristata. 

Three varieties of Osmorhiza longistylis have 
been described on the basis of quantity of in- 
dument (Fernald, 1908; Blake, 1923; Salamun, 
1952). This character, however, was found to be 
highly variable, and thus none of these infraspe- 
cific taxa is upheld (Lowry, 1976; Lowry & Jones, 
1979a) 


IIb. Osmorhiza Raf. sect. Mexicanae Con- 
stance & Shan ex Lowry & Jones, sect. nov. 
TYPE: O. mexicana Griseb. 


~ 
~ 


1904, pro parte. 
eee 2. [sect.] Urascandix Koso-Polj., Bull. Soc. 

aturalistes Moscou 29: 143. 1916, pro parte. 
bh aes sect. Mexicanae Constance & Univ. 
if. Publ. Bot. 23: 112. 1948, nom. 


nvolucrum deficiens vel interdum ab 1-3 bracteis 


(R f.) Kuntze, Lexicon 582. 


–6 bracteolis patentibus vel reflexis consti- 
tutum. ve cum stylopodio 0.5-1.2 mm longi, sty- 
lopodium 0.2-0.8 mm longum, eave vel 
Sia saepe cum disco conspicu 


Involucre wanting, or ti composed of 
1-3 small, linear to lanceolate, spreading to re- 
flexed bracts; involucel generally conspicuous, 
composed of 1—6 spreading to reflexed bractlets. 
Styles plus stylopodium 0.5-1.2 mm long, sty- 
lopodium 0.2-0.8 mm long, low-conic to some- 
what depressed, often with a conspicuous disc. 


5. Osmorhiza glabrata Philippi. Linnaea 28: 653. 
1856. Uraspermum glabratum um 
Kuntze, Revis. gen. pl. 1: 270. 189 
Chile. Bío-Bío: Santa Barbara, C. isa 15 14 
(holotype, SGO; photograph of holotype, 
ILL!; 2 possible syntypes, P!). 


Myrrhis oe Philippi, Anales Univ. Chile 
125. 4. Elleimataenia renjifoana 0 


_ 1984] 
Koso-Polj., Bull. Soc. Imp. Naturalistes Moscou 


hill : 
[lectotype, SGO (no. AD region i icis. 
photographs oflectotype, ILL!, UC!; isolectotype, 
SGO (no. 041594); photograph of isolectotype, 
ILL!]. 


Plants rather stout, 1—5(—6) dm high; stems 1— 
2(-3), erect to ascending, villous to hirsutulous, 
or often glabrate. Root system rather deep. Leaves 
ternate-bipinnate, deltoid to broadly ovate, 5— 
10(-13) cm long, glabrous to hirsutulous along 
the veins and rachis; leaflets ovate, (0.6—)1—2.5 

5—1.3 cm wide, acute or acuminate, 

laciniately lobed to parted or pinnatifid, with lin- 
ear to SHOPS Ek TE ultimate divisions; peti- 
oles 4–12(–15) cm 


m long; involucre wanting; rays 
stiffly ascending, (1—)1.5—8(—9.5) cm long; um- 
bellets (2—)3—13 per umbel, 1–5(–6) of them pro- 
ducing only staminate flowers; involucel of (0—) 
1-2 minute, linear, acuminate, ciliate bractlets; 
pedicels (3—)4—10 per hermaphrodite umbellet, 

2-7(-9) per staminate umbellet, stiffly ascending 
to nearly erect, those of the hermaphrodite flow- 
ers (2—)2.5—7(—9) mm long, those of the stami- 
nate flowers (1.5—)2.3-5.5(—6.5) mm long. Her- 
maphrodite flowers (2-)3-5 per umbellet, (9—)15— 
30(-38) per umbel, staminate flowers (1-)2-7(- 
9) per КИШТЕ umbellet, (7—)15—60(—82) 
per umbel; corolla white, rather inconspicuous; 

m 


mm long, conic, often 
with a conspicuous disci eaters cleft about 
one-third ofits length. Fruit lin acute 
at the apex, concave A (13-)14-20(-25) 
mm long, the ribs glabrous to moderately hispid 
with retrorse bristles, especially toward the base, 

e caudate appendages (0.5—)1—6 mm long. Fig- 
ures 9e and 18 


Flowering period. November to January (with 
one collection flowering in Apri 
abitat. Seasonally moist Nothofagus for- 
ests to open, grassy slopes. 
ommon names. Glabrate sweet cicely, An- 
dean sweet cicely. 


а a specimens. ARGENTINA. NEUQUEN: 
р 


quén, 1,600 m, Boelcke et al. 10978 (UC); Cordillera 

del Viento, 2,000 m, Boelcke et al. 11634 (UC); Paso 

del Macho, 2,280 m, Boelcke et al. 13955 (UC). 
CHILE. Bio-Bio: Sierra Velluda, Poeppig 905 (BM, BR, 


LOWRY & JONES—OSMORHIZA 


1157 


P). COLCHAGUA: San Fernando, Termas Vegas del Fla- 
co, Montero O. 1214 dua apod de Colchagua, 
Pirian 159 (GH); Termas Vegas del Flaco, 2,500 m, 
rdg 6430 (UC). CURICÓ: hills NE of Los Baños, the 
Quebrada, 2, 500 m, Aravena 33301 (UC). MALLECO: 
, Constance & Sparre 3580 
(BM, F, K, MICH, MO, UC, US). NuBLE: Cordillera 


e Chillán, Germain s.n. , K); Termas de Chil- 
, Jaffuel 2035, 2837, dA tas (GH); Chillán, 
n 3469 (UC), s.n. (ph aphs in F, NY, 


fios de Chillán, Philippi & pacers s.n. (BM), Wer- 
dermann 1571 i 
quenes, 2,500 m, Biese 800 i 
н at 2964 (US); Valdes-Tal oo a ies 
m, Grandjot s.n. (MO, UC); valley of the 
near vios Baths of Colima, 2,500 m, ZA 9715 AN 
A: Laguna Maule, 2,400 m, Zöllner 5824 (ILL, 


Constance and Shan (1948: 120) included Os- 
morhiza glabrata in their section “Сіусозтае" 
[= subg. Glycosma], 
for its close similarity to O. occidentalis." How- 
ever, the evidence presented here indicates that 
the affinities of O. glabrata lie with O. mexicana 
and O. brachypoda rather than with O. occiden- 
talis. Constance and Shan’s misinterpretation of 
the relationships of O. glabrata most likely was 
due to the very limited amount of material avail- 
able to a they cite only nine collections of 
this speci 

In Gh discussion of Osmorhiza glabrata, 
Constance and Shan (1948: 120) stated, “Тһе 
single specimen kr caused the most trouble 
in our study was Pennell 12487, from Banos de 
Chillán, Chile. This plant has the ascending rays 
and long styles of O. glabrata, but combines these 
characteristics with appendaged, bristly fruit and 
subentire leaflets. We can only suggest that the 
plant in question may be the result of interbreed- 
ing between O. glabrata and either O. chilensis 
or О. obtusa [= О. depauperata], all three of which 
occur in this area." We have tried to locate this 
specimen, with no success. In any case, Pennell's 
collection is probably much less of an anomaly 
than Constance and Shan suggest; appendaged, 
bristly fruits are not at all uncommon in О. gla- 
brata. Furthermore, the occurrence of subentire 
leaflets in this specimen may represent an inter- 
mediate between O. glabrata and O. mexicana 
subsp. mexicana. The existence of such a spec- 
imen would not be surprising because the two 
taxa involved are closely related, and ses would 

nassum- 
ing intersectional hybridization Татара О. 
glabrata and either О. chilensis ог О. depaupe- 
rata 


1158 


Clos (1848) erroneously interpreted plants re- 
ferable to O. glabrata as being conspecific with 
the European species Myrrhis odorata (L.) Sco- 

oli. 


6. Osmorhiza mexicana Griseb., Abh. Kónigl. 
Ges. Wiss. Góttingen 24: 147. 1879. Wash- 
ingtonia mexicana (Griseb.) Rose, Contr. 
U.S. Natl. Herb. 8: 337. 1905. TvPE: Mexico. 
Schaffner 37 (holotype, GOET!; 2 isotypes, 
P!). [The holotype is marked in Grisebach's 
hand **Osmorhiza mexicana m(ihi)," his an- 
notation for the original material. Several 
paratypes in GOET are marked by Grise- 
bach “Osmorhiza mexicana Gr.," his an- 
notation for authentic material other than 
the holotype, according to G. Wagenitz, 
GOET ] 


Uraspermum aristatum В [subsp.] brevistyle var. laci- 
niatum Kuntze, Revis. gen. pl. 1: 270. 1891. (No 
type material has been located.) 

Plants slender to rather stout, stems 1—2, erect 
to ascending. Leaves 2-3-ternate, villous or pi- 
lose, especially on the veins below; leaflets ovate 
to ovate-oblong, acute to acuminate, coarsely 
serrate to divided at the base. Umbels loose to 
rather open; involucre wanting, or often com- 
posed of 1—2 linear, foliaceous, ciliate bracts; rays 
spreading-ascending; involucel of 1-4 linear, 
acuminate, ciliate bractlets. Styles (including sty- 
lopodium) 0.5-1 mm long, stylopodium low- 
conic to somewhat depressed, often with a disc; 
carpophore cleft about one-fourth of its length. 
Fruit variable in characters depending on the 
subspecies. 


At their morphological extremes, the two sub- 
species of Osmorhiza mexicana (subsp. mexi- 
cana and subsp. bipatriata, see below) are very 
distinct. A number of truly intermediate collec- 
tions, however, mark a transition between these 
taxa. For example, two specimens from Cerro 
Potosí, Nuevo León, Mexico (C. Н. Mueller 2231 
and R. A. Schneider 1108) have fruit with re- 
trorse bristles and short caudate appendages, but 
are in most other respects similar to specimens 
of the subspecies Pipatriata. Typical represen- 
tatives of both subspecies also occur on Cerro 
Potosi. Another collection, G. C. Rzedowski 
22915, from Hidalgo, exhibits a similar inter- 

: ы e Pa 


туа; ал+ e 


aracters. Also, a num- 
ber of collections from northern Mexico clearly 
referable to the subspecies mexicana have re- 
markably short fruit, indicating a certain simi- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


larity to the subspecies bipatriata. Furthermore, 
many individuals of otherwise typical O. mex- 
icana subsp. bipatriata observed on Cerro Potosi 
(Lowry & M. J. Warnock 3182, 3188) have fruit 
armed with a few bristles toward the base, while 
others have completely glabrous fruit. 

The strong similarity and intermediacy ob- 
served between the two subspecies of Osmorhiza 
mexicana has not gone unnoticed in the past. 
Constance and Shan (1948: 121) stated that O. 
mexicana subsp. bipatriata “was not included in 
the ‘North American Flora,’ because only the 
Mexican specimens had come to the attention of 
Mathias and Constance at the time that account 
was published (1944), and these had been re- 
garded as somewhat aberrant representatives of 
О. mexicana (subsp. mexicana).” 

Although Constance and Shan (1948) de- 
scribed the taxon Osmorhiza bipatriata as a dis- 
tinct species they, too, recognized its strong re- 
semblance to the plants of O. mexicana, citing 
two of the intermediates mentioned above 
(Mueller 2231 and Schneider 1108). 


6a. Osmorhiza mexicana Griseb. subsp. mexi- 
cana 

Plants slender to rather stout, 4—8(-10) dm 
high; stems hirsutulous throughout. Root system 
rather deep, the roots weakly to rather strongly 
anise-scented. Leaves 2—3-ternate, broadly ovate 
to deltoid, 5-12(-15) cm long, villous or pilose, 
especially below; leaflets ovate, (1.5—)2—4 cm long, 
1.5-2.5 cm wide, acute to acuminate, coarsely 
serrate to incised and pinnately lobed at the base; 
petioles 6-14 cm long. Umbels rather loose; pe- 
duncles 2—3(-4), terminal and lateral, 7-15 cm 
long; involucre wanting, or sometimes composed 
of 1-2 linear, foliaceous, ciliate bracts, each (2-) 
5-10 (-13) mm lon m wide; rays 
spreading-ascending, 2.2-10(-11) cm long; um- 
bellets 2-5(-7) рег umbel; involucel of (1-)2-4 
linear, acuminate, ciliate bractlets, each (1.5-)2.5- 
9.5 mm long, 0.3-1 mm wide, spreading to re- 
flexed; pedicels (2-)5-11 per umbellet, spread- 
ing-ascending, those of the hermaphrodite flow- 
ers (1-)2-8.5(-12) mm long, those of the 
staminate flowers 2-5(-6) mm long. Hermaph- 
rodite flowers (2—)3—6 per umbellet, (8-)12-32 
(-41) per umbel, staminate flowers (0—)2-7 per 
umbellet, (0—)5—25(—35) per umbel; corolla white 
or greenish white, somewhat showy; styles (in- 
cluding stylopodium) 0.6-1 mm long, stylopo- 
dium 0.2-0.5(—0.6) mm long, low-conic to some- 
what depressed, often with a conspicuous disc. 


1984] 


Fruit linear-oblong, tapering to a short beak at 
the apex, concave furrowed, (10-)1 1-20 mm long, 
the ribs moderately to densely hispid with re- 
trorse bristles, especially toward the base, the 
caudate M endages (1.5—)2—8.5(—10) mm long. 
п = 11 (Bell & Constance, Bac Constance et 
al., 1976). Figures 9f and 1 


Flowering period. Late May to July a AR 
July (Central America); November and Dece 
ber (South America). 

Habitat. Moist forests, at middle and higher 
elevations. 

ommon е Mexican sweet cicely, 

Mexican sweetroot, Cillandrillo (Mexican Indi- 
an; Oaxaca 


Representative Bare . ARGENTINA. см 
4, Comné , Jórgen- 


muchita, Sierra Arhala de Córdoba, Hieronymus, 3 
Dec. 1878 (UC); El Vallecito, Sierra Grande, 2,000 m, 
; La Cumbrecita, 1,500 
ta Barbara, Sier- 
29 С 


el Тисштап, Lorentz & Hierony- 
mus 863 peed ss near la Cienega, Lorentz & Hieron- 
ymus IM (GOET). 

VIA. COCHABAMBA: N of Yungas, 3,200 m, a 
tien 659 (GH, NY, US). LA PAz: Prov. Murillo, up: 
^ de Zongo, 3,500 m, Solomon 5228 (MO), Tate 

194 (NY); sami Sorata, 3,100 m, Mandon 594 (BM, 
G, GH, GO > > Р, m x 
OL чуна TOLIMA: Param 
mann 3074 (BM, K, rii Pd 3101 
Costa RICA. ALAJUEL 


Ruiz, 3,500 m, Leh- 
(NY, US). 


raza, 3,000 m, Tonduz 4273 (BR, 
; Saba eee rig of Volcán de Іга20, 2,900 m, 
E 44 (К). 200 (BR, CR, US). saN José: Cerro de 
las Vueltas, 2,800 m, Standley & Valerio 43592 (K, 
US), 43669 9 (US). 
EMALA. CHIMALTENANGO: Chichavac, 2,500 m, 
Skutch 499 (CAS, MICH); Volcán de Agua, 2,450 m, 
Johnston 809 (F). Micra near Hacienda de 
Ch tanes, 3,350 m, Nelson 


of Ostuncalco, Sierra 
om et al. 25467 (GH, NY, US). SACATEPEQUEZ: 
de Agua, above Santa Maria, Bell & Duke 16987 
(UO. SAN MARCOS: Sen Luis, 3.8 km W of Ixchiguan 
Оп road to e 3,450 m, "Beaman 3247 (GH, UC, 
US). soLoLA: Volcán Tolimán, side facing Volcan Atit- 
lán, 2,900 m, Steyermark 47581 
MEXICO. CHIAPAS: near San Cristobal, Nelson 3188 


LOWRY & JONES— OSMORHIZA 


1159 


(US). CHIHUAHUA: La Rocha, Sierra Mohinora, 2,300 
m, Correll & Gentry 23138 (GH, НӘ, Nelson 4864 
(GH, US); 16 km SW of Guadalupe alvo, Cerro 
Mohinora, Straw & Forman 2013 (О С). DISTRITO FE- 
DERAL: Miguel-Hidalgo Park, 3,200 m, Bell & Duke 
16778 (GH, K, MICH, MO, NY, j : о 
de los Leones, Kenoyer 562 (MICH), 9 July 1938 
ORO, MacDaniels 83 (F), Sharp & Gilly 22 (MICH); 
ontreras, Lyonnet 1623 (US); Sierra de Ajusco, 2,450 
m, Pringle 6615 (BM, BR, CAS, F, G, GH, GOET, K, 
uarto Dinamo, 3,100 
(G); Los Dinamos, 3,000 m 
rs Ventura A. 3492 (G). HIDALGO: 3.8 km SW of Ca- 
brera on Hwy. 105, d Lg m, Pe т. бетү 16813 
(MICH, TEX, UC); E ico Nat'l 16 km NE 
of E Z790, Weller 582 ск поља Monte, 
2,800 m, 64 (LL), Sharp 44593 (UC); 
Cerro de a Ventas re km N of Pachuca, 2,900 m, 
Rzedowski 26813 (CAS, MICH). JALisco: Nevado de 
ICH. UC), 12 


ma: 
tepec, 3, 200 т, ` Hinton 4899 (BM, K, US), arp 
5208 (MO, US); дуре ten Blanca, Temascaltepec, 
Hinton 2 al. 8324 (ARIZ, BM, G, GH, K, LL, MO, 
U 


m, Steingraeber & Steingraeber 150 
cM NUEVO ue Cerro El Infernillo, S of Gal- 


Warnock 3181а 
UM 2,000 m, и rp 45711 (NY, U 
beza de Vaca, trail to Cerro San Felipe, 2,750 

m, n. Bell & Duke 16884 (UC); Sierra San Felipe, 3, 
m, Pringle 5547 (F, US); jM de Oaxaca, 2,750 
; 21 km N of Ixtlán de Juárez, 
66 (UC). к. Orizaba, 3,000 m, 
Liebmann 12241 (Е, GH, US), Müller 1722 (ОН, NY), 
Rose & Hay 5726 (US), ops 12241 (UC); 3,650 
m, Seaton 195 dk GH, US); P кү, Rose & Нау 
6249 (US); Esperanza, Purpus 7456 (MO, NY, UC, 
US). SAN LUIS parum. Sierra de А ads Sierra Madre 
pipe oe 2,300 m, Palmer 127 (US), Pennell 17883 

Н, US). vERACRUZ: near El Puerto, 2,350 m, Sharp 
4680 pde NY). 
zco: Ollantiatambo, 3,000 m, Spin & Gil- 
eor 747 (US). Veronica, between Cuz 
pichu, 3,500 m, Rauh & Hirsch P1026 Ted uci 
Cachu-pampa ш Chile-chile, 2,500 т, Vargas 9697 
(GH, K, MO, UC), 3,000 m, Vargas 1352 (F) 


Weddell (1861) and Hemsley (1880) consid- 
ered Central and South American populations as 
Osmorhiza brevistylis DC. 


2 
=> 
E 


6b. Osmorhiza mexicana Griseb. subsp. bipatri- 
ata (Constance & Shan) Lowry & Jones, 
comb. et stat. nov. Osmorhiza mirigy 
Constance & Shan, Univ. Calif. Publ. Bot. 


1160 


23: 121. 1948. TYPE: U.S.A. Texas: Jeff Da- 
vis Co., in wet ground at spring, W branch 
Madera Canyon on slope of Mt. Livermore, 
Davis Mts., L. C. Hinckley, 26 July 1937 
(holotype, NY!; isotypes, or possibly para- 
types, because label data are not identical to 
those of the holotype, ARIZ!, GH!). 


Plants slender, 2-7 dm high; stems sparingly 
hirsutulous to glabrescent. Root system some- 
what shallow, with a weak anise-like scent. Leaves 
2-3-ternate, ovate to broadly ovate, 4-10(-14) 
cm long, villous or pilose, especially on the veins 
below; leaflets ovate to ovate-oblong, (0.7–)1.2— 
4 cm long, 0.5-3 cm wide, acute to acuminate, 
coarsely serrate-laciniate to lobed or divided at 
the base; petioles 4-10(-12) cm long. Umbels 
loose and rather open; peduncles 1—3, terminal 
and often lateral, 3-15(-18) cm long; involucre 
wanting, or often composed of 1(—2) linear, fo- 
liaceous, ciliate bracts, each 4-10 mm long, 0.5— 
0.8 mm wide; rays spreading-ascending, (1.4—) 
1.6-6.5 (-7.5) cm long; umbellets (2—)3-9 per 
umbel, (0—)1—4(—6) of them producing only sta- 
minate flowers; involucel of 1-4 linear, acumi- 
nate, ciliate bractlets, each (2–)3–4.5 mm long, 
0.3-1 mm wide, spreading; pedicels (3–)4–20 
(-22) per hermaphrodite umbellet, (3—)4—17 per 
staminate umbellet, spreading, those of the her- 
maphrodite flowers (3—)4—7.5(—8) mm long, those 
of the staminate flowers (1.5—)2—3.5(–4) mm long. 
Hermaphrodite flowers 1–3 per umbellet, (2-)5- 
10 per umbel, staminate flowers (4-)6-21 per 
hermaphrodite umbellet, (33-)40-70(-125) per 
umbel; corolla white, or sometimes tinged with 

urple, pink, or green, rather i inconspicuous; styles 
(including stylopodium) 0.5-0.75 mm long, sty- 
lopodium 0.25-0.3 mm long, low-conic, often 
with a conspicuous disc. Fruit linear-fusiform, 
tapering into a short beak at the apex, concave 
furrowed, 9-11(-12) mm long, the ribs glabrous, 
or with a few retrorse bristles at the base, the 
caudate appendages lacking, or sometimes to 1.8 
mm long. Figures 9g and 17. 


Flowering period. June and July. 

Habitat. Moist, generally потоња ravines and 
canyons, from 2,100 to over 2,75 

Common names. None. 


REPRESENTATIVE SPECIMENS. 
vis Co., Upper Made 
ermore, 2,300 m, Hinckley 408 (F, NY), 3589 (NY, 

C), B. H. Warnock & са 4147 (NY), В. Н. 
Warnock 7479 (SMU, ТЕХ). 

MEXICO. COAHUILA: NW of Campo Cinco, Madera 


U.S.A. TEXAS: Jeff Da- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


(Мог. 71 


del Carmen, 2,400 m, Lowry & M. J. Warnock 3130, 
3149 (ILL, MEXU, МО, NY, TEX, ЏО), Fryxell 2689 
(UC), 2703 (CAS); Upper Dos Canyon, Madera del 
Carmen, 2,450 m, Fryxell 2722 (МО, UC). NUEVO LEÓN: 
2.2 km below microwave tower, Cerro Potosi, 3,000 
m, Lowry & M. J. Warnock 3188 (ILL, MEXU, MO, 
NY, TEX, UC); microwave tower, Cerro Potosi, 3,200 
m, McGregor et al. 252 (UC), 339 (NY, SMU, UC); 
Cerro Potosi, Schneider 1043 (F) 


The following collections exhibit combina- 
tions of characters intermediate between О. 
mexicana subsp. mexicana and subsp. bipatria- 


MEXICO. HIDALGO: Penas Largas, near Tezoantla, 
2,750 т, Rzedowski 22915 (CAS, MICH, ORE, TEX). 
NUEVO LEON: Can below Las Canoas, Cerro Potosi, 
Mueller 2231 (GH); Hacienda La Jolla, 2,600 m, 
Schneider 1108 (F). 


7. Osmorhiza brachypoda Torrey in Durand, J. 
Acad. Nat. Sci. Philadelphia II, 3: 89..1855. 
Myrrhis brachypoda (Torrey) E. Greene, Fi. 
francisc. 332. 1892. Washingtonia r 
poda (Torrey) A. A. Heller, Cat. N. Amer. 
pl. 5. 1898. Scandix brachypoda Eo 
Koso-Polj., Bull. Soc. Imp. Naturalistes 
Moscou 29: 143. 1916. TYPE: U.S.A. Cali- 
fornia: Nevada Co., near the banks of Deer 
Creek, Nevada City, H. Pratten, July 1851. 
(This specimen has not been located.) 

м brachypoda var. fraterna Jepson, Fl. Calif. 
A 936. TYPE: прасе California: San Вег- 
т. Co., Arr о, San Gabriel Mts., 600 
m, Б, И. Реіғѕоп 45la y iei JEPS!). 


Plants rather stout, 3-8 dm high; stems 1-2 
(-3), erect, villous to hirsutulous. Root system 
rather deep, the roots weakly to moderately an- 
ise-scented. Leaves 2—3-ternate, ovate to deltoid, 
10-18(-20) cm long, hirsutulous, especially be- 
low and along the veins; leaflets ovate, 2-6(-8) 
cm long, 1-4 cm wide, acute or obtuse, coarsely 
serrate, incised and pinnately lobed at the base; 
petioles 5-18(-22) cm long. Umbels somewhat 
congested, peduncles 2—4, terminal and lateral, 
9-18 cm long; involucre wanting, or often com- 
posed of 1—3 small (or very rarely large and leaf- 
like), linear-lanceolate, foliaceous, ciliate bracts; 
rays spreading-ascending, (3.3—)3.8-12(-12.5) cm 
long; umbellets 2-5 per umbel; involucel of 2- 
6(—7) linear to lanceolate, acute, ciliate bractlets, 
each (1—)2—9.5(—15) mm long, (0.3-)0.5-1.3(-5) 
mm wide, spreading or reflexed; pedicels (2-)4- 
14(-16) per umbellet, ascending, those ofthe her- 
maphrodite flowers 1—4.5(—7.5) mm long, those 
of the staminate flowers (2—)2.8—6(—6.5) mm long. 


1984] 


Hermaphrodite flowers м? Peni per umbellet, 
(6-)10-35(-43) рег um minate flowers 
(0–)1–6(–8) per umbellet, rg per um- 
bel; corolla greenish white, somewhat inconspic- 
p styles (including stylopodium) (0.6—)0.7— 

1.2(-1.3) mm long, stylopodium 0.2–0.5(–0.6) 
mm АС low d 
with a conspicuous disc; carpophore cleft about 
one-third of its length. Fruit oblong-fusiform, ta- 
pering to a narrow beak at the apex, deeply con- 
cave furrowed, (12—)13—18(–20) mm long, the 
ribs densely hispid with retrorse bristles, espe- 
cially toward the base, the caudate appendages 
(0.5-)0.9-3.8(-4) mm long. n = 11 (Constance 
et al., 1976). Figures 9h and 16. 


, often 


Flowering period. March to early May. 
Habitat. Seasonally moist forests at lower to 
fairly high elevations in the mountains. 
mmon names. California cicely, Califor- 
nia sweet cicely, Orris root, Sweet cicely. 


Representative оно U.S.A. ARIZONA: Gila 
„ Collom , base M Peres Mts., 1,200 m, 


UC); Н n, Mazatzal 
Harrison et al. 7815, 7830 AR CALIFORNIA: Ama- 
9123 (CAS, 


34 , NY, ЕМ); 
n, N of Claremont, Lowry 1481, Hu: 
(ILL); Mire би: Arroyo Seco Camp, 29 km 

of Greenfield, Santa Lucia Mts., 760 m, анаа 
3311 (ARIZ, 


Ana Mts., 38 

RM): Riverside Co., Temescal, 

Hall - (UC); San Benito Co., Idria, Ferris 7028 (CAS, 
n Bernardino Co., near San Bernardino, 350 

m, Parish 4165 (BM, K, NY, UC); San — — 

Cuyamaca, Abrams 3838 (BM, CAS, G, K 

UC, Z); Santa Barbara Co., Santa eie mee 2 

(CAS, K K, MO, NY, WIS, Z); Santa Cla a Co. , Alum 


о mne с Неїс 
, Yosemite س‎ "a d on v — 4 
Babcock 3379 ARIZ, RM, 
Sulphur Mt. Spring, Sulphur Mts., e & ги 
Gregor 24 (CAS, G, NY, Z 


IIc. Osmorhiza Raf. sect. Nudae Constance & 
han ex Lowry & Jones, sect. nov. TYPE: 
chilensis Hook. & Arn 


Uraspermum § аша ш; (Raf.) Kuntze, Lexicon 582. 


190 
Scandix 2 зеље rascandix Koso-Polj., Bull. Soc. 
Imp. Naturalistes Moscou 29: 143. 1916, pro parte. 
Кома sect. Nudae niv. Calif. 


Bot. 23: 113. 1948, nom. 


=й deficiens vel гаго ab 1(—2) bracteis mi- 
nutis constitutum; involucellum deficiens vel raro ab 


LOWRY & JONES— OSMORHIZA 


1161 


1(-2) bracteolis minutis constitutum. Styli cum vut 
lopodio 0.2-1.1 mm longi, stylopodium 0.1-0.6 m 
longum, conicum vel leviter ta erra saepe cum 
disco conspicuo. 


Involucre wanting, or rarely composed of 1 d 
minute bracts; involucel wanting, or rarely com 
posed of 1(-2) minute bractlets. Styles including 


stylopodium) 0. 2-1. M mm long, нури 

0.6 mm long, ч 
with a conspicuous disc. 

8. Osmorhiza chilensis Hook. & Arn., Bot. 


Beechey Voy. 26. 1830. TYPE: Chile. Con- 
cepción: Concepción, Lay & Collie, 9—20 
Oct. 1825. (This specimen has not been lo- 
cated.) 


Osmorhiza berterii DC., Prodr. 4: 232. 1830. Myrrhis 

berterii (DC.) Dietr., Syn. pl. 2: 984. 1840. Ura- 

spermum berteroi [sic] (DC.) Kuntze, Revis. gen 
. 1: 270. 1891. ту ] 


G-DC!; isotypes, G!, GH LP 
kane chilensis pep ex Clos i in С. Gay, FI. chil. 
. 1848, pro 
Scandix clavata Banks RS Sol. ex Hook. f., Fl. antarct. 
8 


> 


бунга ‘nuda Torrey, "Pacific railroad ele 41: 93. 


1857. Uraspermum nudum (Torrey) Kuntze, Ке- 
vis. gen. pl. 1: 270. 1891. Myrrhis nuda (To orre ) 
A. Hell t. N. Amer. pl. Osmor- 


hiza divaricata var. nuda (Torrey) M. E. Jones, 
“о Univ., Biol. Ser. 15: 42. 1910. 
rrey) Koso-Polj, B Bull. Soc. Imp. 


Natural 

California: Napa Co., 

elow, 27 Apr. dee e 1854 [lectotype, NY! (des- 

ose, Contr. U.S. Natl. Herb. 
1. 


7: 66. 19 
Osmorhiza berterii var. y ior Philippi, Anales Univ. 
е 85: 726. 1894. TYPE: Chile. “In Andibus 
provinciae l d” Chihuim, О. Philippi, Jan. 1887 
(holotype, SGO; photograph of holotype, ILL!). 
Osmorhiza divaricata Nutt. ex Britt. in Britt. & Brown, 
HLA 2: 531. pro syn. на divar- 
icata (Nutt. ex Britt.) Britt. in Britt. & B 
Ш. fi. 22531. 1897. grae ge ee bse 
Й Im пи 
916. она ies var. di- 
varicata (Nutt. ex Britt. ) Jepson, Madroño 1: 119. 
1923. 1 tt. ex Britt.) 
Farwell, Amer. Midl. Naturalist 12: 70. 1930. TYPE: 
U.S.A. “Oregon woods," Nuttall s.n. [lectotype, 


die 


NY! (designated ” Coulter & Rose, Co ecd US 
Natl. Herb. 7: 00); plus ene entic spec- 
imens (likely syntypes): “Columbia plains,” Nut- 


tall s.n. (BM!); “Columbia se ” Nuttall s.n. 
(GH! 


Washingtonia brevipes Coult. & Rose, Contr. U.S. Natl 
6. 1900. Osmorhiza brevipes (Coult. & 
Rose) а Allg. Bot. 2. Syst. 12: 5. 1906. Os- 


1162 


morhiza nuda var. brevipes (Coult. & Rose) Jep- 
son, Мадгоћо 1: 119. 1923. Urasperum [sic] bre- 
vipes (Coult. & Rose) d idl. 
Naturalist 12: 70. 1930. түре: U.S.A. Са lifornia: 
Siskiyou Co., Mt. Shasta к vicinity, E. Palmer 
2481 (holotype, US». 

Wi Ryd m. New York Bot. 
Gard. 1: 289. 1900. sans ae урина (Rydb.) 
A. A. Heller, Mont. Coll. Agric. Sci. Stud., Bot. 
1: 93. 1905. ТУРЕ: U.S.A. Montana: Gallatin Co. 
Bridger Mts., 2,150 m, P. A. Rydberg & E. A. 
энне io [lectotype, NY! (designated by Con- 

& Shan, Univ. Calif. Publ. Bot. 23: 139. 
1948); isolectotypes, K!, MONT!, US!]. 

Uraspermum barbatum Farwell, Amer. Midl. Natu- 
ralist 12: 70. AP LUE TYPE: U.S.A. Michigan: Ke- 
weenaw Co., roc s, Copper Harbor, O. 4. 
iind 8490 е ВІН! (designated by 

Vaugh et al., Bull. рне ne Sci. 34: 79. 
1953) isolectotype, GH! (*isotype" fide Con- 
stance & Shan, Univ. Calif. РЧЫ. Вес 23: 139. 
1948), 


Plants slender to rather stout, 3—12(—15) dm 
high; stems 1—3(—4), erect, villous to hirsutulous, 
or sometimes essentially glabrous. Root system 
rather deep, well developed, the roots with a weak 
carrot- or anise-like scent. Leaves biternate, or- 
bicular to broadly ovate, 4–18(–23) cm long, ap- 
pressed-hispidulous to villosulous (especially 
along the veins), or sometimes nearly glabrous; 
leaflets ovate-lanceolate to nearly orbicular, 
(2—)3—8(—10) cm long, 1—5 cm wide, obtuse or 
acute, coarsely serrate to incised, parted or di- 

at the base; petioles 5—16 cm long. Umbels 
rather bom peduncles 2-4, terminal and lateral, 
5-25 cm long; involucre wanting, or rarely com- 
posed of 1(-2) minute (to very rarely large and 
с, e а foliaceous, ciliate, 
sprea cts; -ascending, (1 
xong d cm long; umbellets 3-8 per umbel; 
involucel wanting, or rarely of 1(—2) minute, lin- 
ear-lanceolate, foliaceous, ciliate bractlets; ped- 
icels (2-)3-9 per umbellet, spreading-ascending, 
those of the hermaphrodite flowers 4—20(-25) 
mm long, those of the staminate flowers (1—)2- 
7(-9) mm long. Hermaphrodite flowers (1—)2—6 
per umbellet, (5—)9—30(—39) per umbel, stami- 
nate flowers 0—4 per umbellet, 0—18(—25) per um- 
bel; corolla greenish white (rarely pink?), rather 
inconspicuous; styles (including stylopodium) 
0.4–1.1(–1.2) mm long, stylopodium (0.2-)0.3- 
0.6 mm long, high-conic to somewhat gibbous, 
lacking a disc; carpophore cleft about one-fourth 
of its length. Fruit linear-oblong, tapering to a 
slender beak at the apex, concave furrowed, (11-) 
12-21(-25) mm long, the ribs moderately to 
densely hispid with retrorse bristles, especially 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


toward the base, the caudate appendages (2-)2.5- 
8.5(-10) mm long. n= 11 (Bell & Constance, 
1957; Constance et al., 1976). Figures 9j and 15. 


Flowering period. April to early July (North 
America), November and December (South 
America). 

Habitat. Moist forested areas to somewhat 
drier, open, often disturbed areas. 

Common names. Common sweet cicely, 
Mountain sweet cicely, Mountain sweetroot, 
Spreading sweetroot, Sweet cicely, Sweetroot, 
Western sweet cicely, Western sweetroot, Wood 
cicely, Asta de Cabra. 


hg specimens. U.S.A. ALASKA: Hyder, 
McCabe 8426 (UC); Salmon nm T of Hyder, Ro- 
buck 1348 (RM); Deer Mt., E of Ketchikan, 
McCabe 8644 (UC); Sitka, id 966 (CAS); Todd, 
SE Chichagof Island, istis an 328 (DAO, photo- 
graph); Haines Hwy e 31, Walsh & Moore 6113 
(NY); Yakutat, Piper 4280, 4283 (UC); Shaw Island, 
N of Cape Douglas, Anderson 1382 (US); Unalas 

Island, Eyerdam 2256 (cited in Hultén, 1947). ARIZONA: 


Peebles et al. 4483 (US). CALIFORNIA: Butte Co., Jones- 
ville, 1,550 m, Copeland 391 (ARIZ, BM, BR, CAS, 
MO, NY, RM, UC, WIS); Fresno Co., Huntington 
Lake, 2,135 m, Grant 1 173 (ARIZ, JEPS); Humboldt 
Co., Lady Bird Johnson Grove, Redwood Nat'l. Park, 
Lowry 791, 795 (ILL); Lake Co., Summit Lake, near 
Mt. Sanhedrin, Heller 5879 (CAS, G, ILL, NY, RM, 
UC); Lassen Co., Diamond Mt., near Susanville, 2,000 
m, M. E. Jones, 28 June 1897 (BM, CAS, MO); Los 
Аан Co., Lily Spring, Mt. Hawkins, San Gabriel 
Mts., Thorne 41257 (RSA, UC); Mendocino Co., Noyo, 
Constance 2518 km CAS, NY, RM, UC); oc 
; 1,925 m, е 


UC); за 
1,400 m, Рон 4421 (BM, CAS, JEPS, K,M 
Santa Clara Co., W s Los Gatos, Heller 7430 (CAS. 
G, MO, NY, UC, WIS); Siskiyou Co., NE base of Mt. 
"ye паса 12467 iy G. ILL, MO, NY, UC, WIS); 
Petrified Forest, Heller 5737 (CAS, G. 
MO, NY, RM, UC); Tehama Co., 1 km S of Lassen 
Chalet, nt: 851 (ILL); Tuolumne Co., Sulliv. an Creek, 
of Twain Harte P.O., 1, e m, Alexander & 
уй 3673 (JEPS, NY, UO). co RADO: Archuleta 
Co., Piedra River, 11 km N of rece 2,250 m Н. 
D. Harrington 4108 (CS); Boulder Co., Boulder, 1, 650 
m, Hanson C2 arfield Co., 1.5 km 
N of { Douglas Pass 


| 
| 
| 
| 
| 


1984] 


W. R. Erickson & D. Bartman 688 (CS). IDAHO: Ban- 

nock Co., Mt. Putnam, Davis 4672 (NY); Benewah Co 

16 km S of St. Maries, Christ 10927 (NY, UC); Bonne- 

ville Co., 17.5 km SW of Victor, Lowry 1116 (ILL, 

arwater Co., E Fork Potlatch 
Є 


am 1608 (MO, UC, WTU); Lemhi Co., Jessie Creek, 
К; үз при и ens (CA s MO, NY, RM); 
, Mission Cree t. John et al. 6345 (NY, 

УТО); Nez Dane om cue River, ‘Helles & Heller 


uaretown, Fassett 3658 (WIS). MICHIGAN: Al- 
er Co., Miner’s Falls, near Munising, Fernald & Pease 
3450 (MICH , NY); Alpen na Co., Thunder Bay Island, 
Dodge, 23 June 1907 (MICH); Baraga Co., Big Lime- 
stone Mt. нөр, Fassett 21055 (WIS); Gogebic Co., 
17 Заре Ironwood, Voss 6238 (MICH); Kew- 
per Harbor, Fernald & Pease 3452 (K, 


0 
Lowry 2580 (ILL, MONT, UC); Carter Co., 1. 

of Alzada, Booth 2661 (MONT); Flathead Co., Colum- 
bia Falls, Williams, 22 June 1894 (MO, NY, RM); 
Glacier Co., Florence Falls, Glacier Маг 1. Park, 1,615 


0., Lamoille Canyon, Ruby Mts., 2,285 m, Holmgren 
1354 (UC); Washoe Co., Little Valley, 2,000 m, Baker 
1363 (G, NEW HAMPSHIRE: Coos 
Co., Carter Notch, Forbes s.n. ` (GH); Alpine Cascade, 
Gorham, didi 16432 (GH). NEW MEXICO: Taos Co., 

S of Talpa, Correll СЖ СРЕ 33135 (ТЕХ). 
ѕор Со., Іее ark, Lowry 
1310 (ILL, MO, OSC, UC); kis А Co. ., 16 km NW 
of Scapoose, Lowry 593 (ILL); Douglas Co., Iverson 
ipo Park, espe 1319 (ILL, MO, NY, OSC, UC); Grant 


06 (ILL, MO, OSC, UO); J Jefferson Co., Jack Creek, 
i km W of Camp Sherman, Lowry 747 (ILL, ке. 
Marion Co., Silver Creek, Hall 216 (СОЕТ, MO, 
Multnomah Co., Forest Park, Portland, Lowry 626 (ILL, 
MO, OSC, UC); Tillamook Co., Bay City, MT 162 
; Wallowa Co., 0.5 km S of Wallowa Lake, 1,340 
m, Consina & Jacobs 1304 (MO, UC); Wheeler Co., 
3 km NE of Ochoco — Lowry 1092 (ILL, OSC, 
UC). SOUTH DAKOTA: Lawrence Co., Deadwood, Carr 
HOMO, NY, АМ, WIS); Lead City, 1, 800m, р а 
н: Сасће gan Canyon, 1,550 m, 
E 3637 (RM, UO: Salt Ts Co., [2n Creek 
Canyon, M. E. Jones 1852 (BM, BR, G, NY, RM); 
Washington Co., 5 — Pine Malley dd 135m, Gould 
1846 (ARIZ, CAS, NY, UC). WASHINGTO lan Co., 
Stehekin, 400 m, Rose 48178 ӨМ UO: Columbia 
, Constance 


LOWRY & JONES—OSMORHIZA 


1163 


Jefferson Co., N Fork Quinalt River, Lowry 254a (ILL); 
King Co., Seattle, 1 е сте (CAS, МО, NY, 
WTU); Kittitas Co. of Teanaway Junction, 
Wenatchee Mts., Poma 17258 ( U); 
Klickitat Co., Bingen, Suksdorf 10037 (BM, CAS, ЊЕ 
К, МО, МУ, UC); San Juan Co., Friday Harbor, Zeller 
& Zeller 768 (CAS, K, MO, | i 
km E of Camas, Lowry 713 (ILL); Spokane Co., Clarks 
Spring, N of — — 44 (NY, UC , WTU); 
tcom Co., Fair ll., Belli wry 629 
(ILL, MO, NY E RH Bayfield Co., 4 km S 
of Little Sand Bay, Пиз & Kawano 20503 (BM, UC). 


Fremont Co., 
Lander, 2, 200 m, s 909 (NY, RM); Li 
Cottonwood Lake, of Afton, Porter 3776 (CAS, 
RM, TEX); bem a 5 hex W of Teton Pass, Lowry 
1120 (ILL, R ta Co., Teton Mts., Melos 
& Nelson 6473 о ILL, MO, NY, RM 
ADA. ALBERTA: Cameron Lake, Waterton Lakes 
Nat'l. Park, 1,660 m, paterson 16175 (DAO, UC); Chief 
Mt., bonis ai Lakes, 1, 
UO); Nordegg River, Brinkm man 
Fletcher 73 9 DAO): 13 km W of Pincher Creek, Moss 
6 (DAO). BRITISH COLUMBIA: 13 km N of Flathead 
Customs Sta., 1,370 m, Taylo rå Ferguson a pe 
5 km 


U bo ts. 
NY, RM); Glacier Nat'l. Park, Lowry 1012 (ILL, MO, 
NY, UC); 13 km W of Revelstoke, Lowry 1016 (ILL); 


Manning Pro Low 
Boston Bar, Т к > Staudt 4197 (DAO, UC); 11 km 
SE of Vedder’s Crossing, Lowry 1036 мет MO, NY, 
UC); 3 km S of Pemberton, Lowry 644 (ILL); NW tip 
Saturna ese Gulf Islands, чон & МасКау 28775 
(DAO); Cowitcham e, Vancouver Island, Rosen- 
dahl & Johnson 1857 (DAO). | jcluclét. Macoun 78607 
E of 150 Mile House, 1,000 m, Calder 
et al. "19030 AOL Bella Coola, McCabe 123, 1402 
George, E 4 


io 
E Tt 
26 at 1963 (DAO); Restigouche Co. 
Summit Depot, Cunningham, 21 July pe ср ит 
ps shane at N of Doctor Hill, Fernald & Long 
71 (K); Frenchman’s Cove, Bay of Islands, War 
ex QK). NOVA SCOTIA: 


nis ss Co., Brigend, Smith et al. 2589 (DAO, UC); 

s Co., Kentville, Prince & Atwo 011 ( 
MÀ ONTARIO: Algoma Dist., Garden River, Fassett 
o., Kincardine, Anderson & Fas- 


13282 (WIS); нес 
-— 21585 (UC, ; 

toulin Island, т 14833 (WIS); Thunder Вау 
Dist., "Talos Lake, Sibley Twp., Taylor et al. 1146 (UC). 
Chrétien, Cing-Mars et al. 


IEL, ,NY 
Е Scoggan 13595 (NY, О vi | 
viére-du-Loup, Churchill, 8 Aug. 1902 (SMU). sas- 


1164 


KATCHEWAN: Cypress Hills Park, Breitung 4720, 8102 
(DAO, UC). 

ARGENTINA. CHUBUT: Futaleufu, Lago Futalaufquen, 
lat 19823 (P, UC); Rio Futaleufu, Castellanos, 24 
Jan. 1945 (NY); Colonia de Octobre, Lahitte 52212 
UO) а. Lago Fontana, Moreno s.n ; Lan- 
guineo, Pa pa Chica, кон 2488 (ОС). MENDOZA: 
Tunuyan, Cerro de las Piedras, Ruiz Leal 3106 (BM, 
UC). NEUQUÉN: Aluminé, Lago Quillén, Valle et al. 
3074 (K); Huiliches, Lago Huechulafquen, Parque Nac. 
Lanín, Correa 5537 (UC); ud Verde, Parque Nac. 
Lanín m, Correa et al. 5774 (UC); Lacár, Hua 
Hum, "Cabrera 11229 (UC), ea 1754 (BR, MO, 

TEX), O Donell 2331 (NY); San Martin de los Andes, 
Hunziker 6910 (UC), Ruiz Leal & Roig 18128 (UC), 
Ruiz Leal 20265 e O’Donell 2399 (NY); Los La- 
el Huapi, DeBarba 1548 аяне 
duana 
Boelcke et al. 10826 (UC). RIO NEGRO: 
Baril е е Nac. Nahuel Huapi, Boelcke 5246, 
5659, 5842 (UC), Boelcke & Hunziker 3417 (UC), Ca- 
brera & Job 98 (NY), DeBarba 95 (NY, UC), 1127 (Р), 
Descole 25 (NY), Meyer 7456 (NY); Entre Llao- Llao 
y Bahia López, Meyer 8002 (NY). SANTA C go 
Argentino, Parque Nac. “Los Glaciares,” Correa et al. 
2998 (UC); Cerro Mayo, James 3002 (BM, UC); Lago 
Argentino, Ruiz Leal 26558 (UC); Lago Buenos Aires, 
Rio Jeinemeni, entre Lago Buenos Aires y Codo Rio 
ки, = m, von Platen & saves 150 vae VAS 

shuaia, Estan arberton, Con- 
Жане » 2 3860 (UC), си“ 4 (MICED, 549 
(MICH, NY), 3585 (UC); Lago Roca, Goodall 2439 
ep Estancia Fique, Ruiz Leal & Roig 15117 (UC). 
LE. ACONCAGUA: Los Ojos de Agua, Bridger 475 
(K); ааг ee тео, Johow, Nov. 1908 (ILL), Loos- 
er, 13 Oct. 1953 (UC), Moller, 8 Dec. 1951 (UC). 
ARAUCO: anime. Cerro Santa Elena, Ricardi 9248 
(UC). AYSEN: сое hes del Lago Seco, 750 
m, Schlegel 2321 (F); Pt , Río Pascue, 8 
m, Schwabe 45 (NY). seins UTÍN: Temuco, Elliot 276 (BM, 
NY); Temuco, Truf-Truf, cti O. 6371 (UC); Te- 
muco, Fundo Hui ilquilco, 2 km S of Quepe, Moore e 
Vilcan, 330 m, fis 334 (UC); P 
,250 m, Mahu 11425 йи: 
Victoria, 16 km from Termas de Tolhuaca on rd. t 
Curacautin, 950 m, Morrison & Wagenknecht 17486 
(С, UC); Volcan Llaima, 1,100 v Werdermann 
1246 (BM, CAS, F, G, K, MO, NY, UC, Z); Pass to 
Longuimay, 1,000 m, Zóllner 5617 с. CHILOE: An- 
cud, Chiloé Island, MacMillan & Erlanson 11 (MICH); 
Cucao — Chiloé Island, Philippi & Borchers, 2 
Feb. 1885 (BM ota, : ! (B Ti 
C oncepción, epus 289 (P), Holway 139 


LLANES: erto Natales, rd. to Punta 
Arenas, 30 m, Eyerdam et al. 24181 (K, MO, UCy; 
Sandy Point, Lechler 1186 (GOET); Estancia Vicufia, 


(UC). M undo Solan 

huelbuta, 1 200 т, Eyerdam Pree (F, UC); 1 km W 
of Agua Fria, W of Angol, Sierra Nahuelbuta, 650 m, 
Hutchison 293 (K, UC); Termas de Tolhuaca, 1,10 
m, Looser 2746 (UC), Solomon & Solomon 4479 (MO), 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


Zöllner 10201 (MO); Parque Nac. de Nahuelbuta, Мали 
5767, 8272, 8417, 8733, 8734, 8735, 11451 (ILL), 
Pincheira 7881, 8218 (ILL). NuBLE: Termas (Baños) 
de Chillán, 1,750 m, Moore 414 (UC), Philippi & 
Borchers s.n. (BM). O’ HIGGINS: La Leona, Rancaque, 
Bertero 446 (P), i cgi 446 (P); Agua de la Vida, 
Borchers s.n 05, Cauquenes, Philippi, Sept 
1896 (BM); “upper 108: iy ore iver Cachapoal, Zóllner 
ei (ILL). OSORNO: Termas de Puyehue, ra Sparre 
2128 (K). SANTIAGO: Manzano, Looser, 11 Nov. 1928 
pring Foy de Macul, 1,100 m, Pisano V. & Bar- 
C); Los Valdes, near Río Maipo, 2,500 
m, mein ad oo 9 (ILL). VALDIVIA: Valdivia, Bridges 
768 (K), DeCandolle m. 418 (P), Gay 124 (P), Hoh- 
enacher 481 (K), Hollermayer 334 эе Cabo Blanco, 
Rio Cruce — s.n. (UC); La Unión Reserva 
Forestal "ven acura, Mahu 11424 (ILL). VALPARAÍSO: 
Valparaíso, Bertero 74 (F, NY, UC—all photos ex B), 
Cuming 335 (K); Limache ика iu), Garaventa Н. 
2270 (UC), Bertero, Oct. 1828 (BM), Bertero 1163 (С, 
Р), Steudel 1163 (Py; Laguna Verde, Garaventa Н. 2378 
(UC); Granizo, Сајбп Grande, foot of Cerro Campana, 
near Olmue, 15 km E of Limache, Meyer 9704 (MO, 
UO), Zóllner, Nov. 1977 (ILL); 8 km from La Dormida 
on trail to Las Vizcachas, 1,100 m, Morrison 16832 
(G, K, MO, UC); Quilpué, Zóllner 8353 (MO). 


Constance and Shan (1948) were the first to 
recognize the conspecificity of North and South 
American populations of Osmorhiza chilensis. 
Previous to that, the North American material 
had been referred to a variety of names, including 
Osmorhiza brevipes, O. divaricata, O. interme- 
dia, O. nuda, and Uraspermum barbatum, while 
South American specimens were identified as 
either O. berterii or O. chilensis. However, the 
similarity of plants from the two areas was men- 
tioned by Coulter and Rose (1895) and Reiche 
(1902) 


It has been established that the names Os- 
morhiza chilensis and O. berterii were both pub- 
lished in 1830 (Constance & Shan, 1948; cf. also 
Jackson, 1893; Rickett, 1945). While the month 
of publication for O. berterii most likely is Sep- 
tember, that for O. chilensis is not known. How- 
ever, Hooker and Arnott (1833), J. D. Hooker 
(1846), and Gray (1854) accepted the name O. 
chilensis, placing O. berterii in synonymy under 
it, and it was on this basis that Constance and 
Shan (1948) adopted the former name. We have 
uncovered no additional evidence that would re- 
quire a different interpretation. | 

Bongard (1833) included Alaskan populations 
of Osmorhiza chilensis in O. brevistylis DC. Sim- 
ilarly, W. J. Hooker (1840) used an expanded 
concept of O. brevistylis to include populations 
from western North America now included in 
O. chilensis. 


I 


1984] 


9. Osmorhiza purpurea (Coult. & Rose) Suksd., 
Allg. Bot. Z. Syst. 12: 5. 1906. Washingtonia 
purpurea Coult. & Rose, Contr. U.S. Natl 
Herb. 7: 67. 1900. Osmorhiza chilensis var. 
purpurea (Coult. & Rose) Boivin, Natural- 
iste Canad. 93: 644. 1966. TYPE: U.S.A. 
Alaska: Sitka, F. V. Coville & T. H. Kear- 
ney, Jr., 14-17 June 1889 (holotype, US!). 


Washingtonia leibergii Coult. & Rose, Contr. U.S. Natl. 
j 1900. Osmorhiza d yes & 
ge Blankinship, Mont. Coll. Agric. 
1: 93. 1905. rvPE: U.S.A. а м 
lan a (formerly Okanogan) Co., Sandy slopes of Na- 


1,370- 
2. Pa m, J. H. Sandberg & J. B. Leiberg 666 
[holotype, US!; isotypes, BM!, BR!, CAS!, MO!, 
NY!, ORE!, P!, UC! (or possibly paratypes, as 
label data are not identical to those of the holo- 
type)] 


Plants slender, 2-6(-8) dm high; stems 1-2 
(-3), erect to ascending, sparingly hirsutulous to 
glabrescent. Root system relatively deep, well 
developed, the roots with a weak carrot- or anise- 
like scent. Leaves (1—)2—3-ternate, orbicular to 
deltoid or broadly ovate, 3-10(-12) cm long, 
sparingly hirsutulous along the veins and mar- 
gins, to glabrous; leaflets lanceolate to ovate, 1.5- 
6(-8) cm long, 0.5-4 cm wide, acute or acumi- 
nate, coarsely serrate to incised, lobed or deeply 
divided at the base; petioles 5-10(-12) cm long. 
Umbels rather loose; peduncles 2—3(—4), termi- 
nal and lateral, 3-9(-11) cm long; involucre 

anting, or very rarely consisting of 1 minute, 
linear-lanceolate, foliaceous, ciliate, spreading 
bract; rays spreading-ascending, (2.7-)3-9.5(-11) 
cm long; umbellets (2-)3-7 per umbel, some- 
times 1-2 of them producing only staminate 
flowers; involucel wanting; pedicels (2-)3- 
hermaphrodite umbellet, 3—5 per staminate um- 
bellet (when present), spreading-ascending, those 
of the hermaphrodite flowers (8-)9—25(-33) mm 
long, those of the staminate flowers 2—5(—6) mm 
ong. Hermaphrodite flowers (1-)2-6 per um- 
bellet, (6—)10—22(-29) per umbel, staminate 
flowers 0-5 per hermaphrodite Irwin 0-18 
(-24) per umbel; corolla purplish 


у 


4 тт Лонд strongly ge- 


about one-fourth of its length. Fruit linear-fusi- 
form, with an apical beak that is strongly con- 


LOWRY & JONES—OSMORHIZA 


1165 


stricted below the stylopodium, concave fur- 
rowed, (7-)8-15(-16) mm long, the ribs glabrous 
above and slightly to moderately hispid with re- 
trorse bristles below, the caudate appendages 1– 
5(-6) mm long. 2n = 22 (Taylor & Mulligan, 
1968). Figures 9i and 13 


Flowering period. Late April to July. 
Habitat. Moist coniferous forests in areas 
with tA la regular precipitation. 
оттоп names. Purplish sweet cicely, Pur- 
ple sweet gent Purple sweetroot. 


Representative specimens. U.S.A. А er Mt., 
Revillagigedo Island, McCabe 3644. СЕ Loring 
Chamberlain po (US); У es Bay, Gorman 23 (K, NY); 


Texas Creek Summit, NW of Hyder, McCabe 8934 
Ше, Misty Fjords Nat’l. Mon., Vorobik 413 (ORE); 


У, 
SMU); Sitka, Jepson 489 (ЈЕР); Young Вау, Admi- 
ralty Island, Robuck 1311 (RM); Douglas Island, 8 of 


Juneau, Trelease 4527 (US); Juneau, Anderson 6322 
AO, RM, TEX t. Harris, St. Eli ts., Cowles 
1402 (ILL, MO); Thum Bay, land, Prince 


мо) Mt. Marathon 

NY, UC); Stetson Creek aar. r 
6479 (DAO, УТО); Three Saints Bay, Kodiak Island, 
Eyerdam 386 (K). ңе EA Del Norte Co., Wilson 
Creek, between Requa and Crescent City, Abrams & 
Bacigalupi 8323 (CAS, RM); Redwood Nat’l. Park, 
Lowry 785a (1 


(BM O, NY); Shoshone Co., Sohons Pass, 1,650 
m, тебет 1 427 (CAS, К, NY, ЕМ, UC). MONTANA: 
Glacier Co., Midvale, Umbach 249 (MONT, RM, WIS); 
Park Co., 10 km W of Four Mile Ranger Sta., Boulder 
River Canyon, Hitchcock 16381 (CAS, МҮ, UC, WT 

mas Со., 5 slope of Mt. H 


dm et al. 5341 (MO, UC, WTU); Sno- 
rry Creek Trail, 1,000 m, Thompson 
€ WTU). 


Lake, Waterton Lakes 


BRITISH COLUMBIA: 16 km N o 
Ferguson 2714 (DAO); S Fork Kas 
kanee Glacier, McCabe 4779 (UC); Glacier Магі. Park, 
Haber & Shchpanek 1492A (CAS, NY); a 
Valley, Selkirk Mts., Brown 273 (MO, NY); Quin 


1166 


Lake, Ashnola Range, Calder et al. 19635 (DAO, NY, 
UC); Manning Prov. Park, Lowry 1026 (ILL, UC); 
Copper Canyon, 800 m, Schmidt 51-53 (DAO); Lake 
nie, Marble Mts., 1,500 m, Thompson & 
(WTU); Moat Lake, Forbidden Pla- 
teau, Vancouver Island, Calder & pages 32303 
E of Bakerville, 
; Mt. Fougner, Bella Coola, Calder 
et al. en 7 (DAO); Safety Cove, Calvert Island, 
McCabe 4189 (UC); Swanson Bay, Graham Reach, 
McCabe 3458 (UC); 5 km WNW of Tyee, E of Prince 
Rupert, Calder et al. 15038 (DAO); Bigsby Inlet, Mo- 
-— Island, Calder et al. 34908 (DAO); trail to Mer- 
cer Lake from Empire Anchorage, Graham Island, 
Calder & Savile 21 494 (DAO, UC); Stewart, Whited 
1226 (MO). 


Osmorhiza purpurea is clearly a distinct species, 
although it is often confused with the closely re- 
lated O. chilensis. Osmorhiza purpurea is the only 
taxon in the section Nudae that does not exhibit 
disjunctions to the Great Lakes region, north- 
eastern North America, and southern South 
America. Constance and Shan (1948) noted that 
the fruits of this species seem equally well adapt- 
ed for long-distance dispersal as those of O. chi- 
lensis and O. depauperata. Osmorhiza purpurea, 
however, has a very restricted habitat preference, 
occurring only in areas with substantial, regular 
precipitation, often at higher elevations or along 
the Pacific Coast, in sharp contrast with its more 
widespread relatives. 

Coulter and Rose (1900) published two names 
for plants now included in O. purpurea: Wash- 
ingtonia leibergi and W. purpurea. When these 
taxa were combined by Mathias and Constance 
(1944), they adopted the name Osmorhiza pur- 
purea, and accordingly, under Art. 57 of the 

"Code" (Voss et al, 1983), this choice of 
epithet must be Ык а. 


10. Osmorhiza depauperata Philippi, doer 
Univ. Chile 85: 726. 1894. TYPE: Chile. М 
ble: Valle de las Nieblas, near Termas J 
Chillán, F. Philippi 2030 [lectotype (desig- 
nated herein), SGO (no. 041589); photo- 
graph of lectotype, ILL!; isolectotype, SGO 
(no. 053461); photograph of isolectotype, 
ILL!]. 


Washingtonia pare Coult. & Rose, Contr. U.S. Natl. 
: . 1900. nnd obtusa (Coult. & 
Rose) rem. Rhodora 4: 154. 1902. Type: U.S.A. 
о. аади (1.е., Ishawooa) 
KJ. ON. Rose 476 (holotype, US). 
== obtusa var. cupressi-montanum Boivin 
Canad. Field-Naturalist 65: 20. 1951. eto in 
chilensis var. cupressimontana (Boivin) Boivin, 
Naturaliste Canad. 93: 644. 1966. TYPE: Canada. 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


Saskatchewan: Cypress Hills Park, aspen woods, 
A. J. Breitung 4742 (holotype, DAO!). 


Plants slender, 1.5—6.5(-8) dm high, stems 1- 
3(-5), erect to spreading-ascending or decum- 
bent, sparsely to rather densely hirsutulous, or 
sometimes glabrescent. Root system rather deep, 
well developed, the roots with a weak carrot- or 
anise-like scent. Leaves 2—3-ternate, orbicular to 
broadly ovate, 4—10(—12) cm long, sparingly his- 
pidulous to glabrous; leaflets broadly lanceolate 
to ovate, 1.5—5(-6) cm long, 1—3 cm wide, obtuse 
or acute, coarsely serrate to incised, parted, or 
divided at the base; petioles 3—20(—23) cm long. 
Umbels open, peduncles 1-3, terminal and often 
lateral, 5—15 cm long; involucre wanting, or rare- 
ly consisting of 1 minute (to very rarely large and 
leaf-like), linear-lanceolate, foliaceous, ciliate, 
spreading bract; rays widely spreading to nearly 
reflexed, (2.5—)3—9(—10) ст long; umbellets 2-6 
per umbel; involucel wanting, or rarely of 1-2 
small, linear-lanceolate, foliaceous, ciliate bract- 
lets, each 0.3-2.5 mm long, 0.2-0.4 mm wide; 
pedicels (2—)3—7 per umbellet, widely divaricate, 
those of the hermaphrodite flowers (4—)8—12(-32) 
mm long, those of the staminate flowers 2-12 
(-13) mm long. Hermaphrodite flowers 2—6 per 
umbellet, (3—)7-20(-25) per umbel, staminate 
flowers 0—2(—3) рег umbellet, 0—10(—15) per um- 
bel; corolla greenish white, rather inconspicuous; 
styles (including stylopodium) 0.3–0.6(-0.7) mm 
long, stylopodium (0.1—)0.2—0.4(—0.5) mm long, 
low-conic to depressed, with or without a disc; 
carpophore cleft about one-third of its length. 
Fruit clavate, obtuse at the apex, concave fur- 
rowed, (9—)10-18(-19) mm long, the ribs mod- 
erately to densely hispid with retrorse bristles, 
especially toward the base, the caudate append- 
ages (2.5—)3—8.5(-9) mm long. n= 11 (Bell & 
Constance, 1960; Constance et al., 1976); 2n = 
22 (Crawford & Hartman, 1972). Figures 9k and 
14 


Flowering period. April to early July (North 
America) November and December (South 
Americ 

Habitat Moist to fairly dry forests, wood- 
lands, and open slopes. 

Common names. Blunt-fruit sweet cicely, 
Blunt-fruit sweetroot, Blunt-fruited sweet cicely, 
Bluntseed sweetroot, Snub cicely, Sweet cicely. 


маке е 

о Anderson 35 (K); Pt tavus, 
GI acier Bay, Coville & Kearney 429 (US); Lu Piper 
4288 (US); Kenai Lake, Calder 5688 (DAO); Cooper 


Representative specimens. p v 


NR e и 


1984] 


Landing, W of Kenai Lake, Anderson 6882 (RM); 12 
km E of mouth of Moore River, Kenai Peninsula, Lutz 


MO ua 
Mts., Ferris 9950 (MICH, TEX, , UC); Coconino 5 Cab 
MacDougal 397 
(ARIZ, G. NEF 0 , UC); Pima Co., Santa Catalina 
odman & Hitchcock 1253 (MO, NY, RM). 


, G. N. Jones 


Delta Co., Cedaredge, 2,150 m, Baker (K, RM, 
UC); El Paso Co., Jack Brook, 2,600 m, Clements & 
Clements 236 (NY, RM); Garfield Co., So f Rifle, Os- 


terhout 2151 (NY, RM, WIS); Gunnison Co., Elko 
Park, N of Gothic, Mathias 3264 (UC); La Plata Co., 


Plata, Baker et al. 849 (BM, K, MICH, MO, 
RM); Mineral Co., near Pagosa Peak, 2,750 m, Porter 
3932 (CAS, RM, UC, WTU); r 


4 Up 
. 188 (BM, 
RM); Rio Blanco Co., Black 
Sulphur Creek, үз: 5 km SW of confluence with Swize r 
№. В. Erickson 594 (CS); Summit Co., 
S). 


Holmgren & Murttala 5415 , UC); Bonneville Co., 
18 km SW of Victor, Lowry 1114 (ILL); Cassia Co., 
Pole Canyon, SE of Burley, 2,000 m, Holmgren & Jen- 
sen 3499 (NY, WTU); Clark Co., Centennial Mts., 2,350 
m, Lowry 2485 (ILL, MONT, UC); Custer ce Challis 
Creek, 1 ee m, Macbride & Payson 3332 (CAS, K, 
MO, NY, RM, UC); Fremont Co., Henry’s Lake, 1,800 
m n, Payson @ Payson 1946 (CAS, MO, NY, RM). MICH- 

Keweenaw Co., Isle Royale, McFarlin 2049 
(MICH, MONT); Leelanau Co., E end of Manitou Is- 
land, Richards 3123 (MICH). MINNESOTA: Cook Co., 
Mountain Lake, Butters et al. 3 . MONTANA: 


WTU); Gallatin Co., Mystic 
Lake, Blankinship 220 (BM, MO, MONTU); Silver 


; Elko 
moille ont 2,450 m, eb & McKnight 168 (NY); 
White Pine Co., Snake Creek, Snake Каме 2, eds m, 
Holmgren & Revea 1 1627 . NEW M 
Co., Hillsboro Peak, Black Range, 3, 050 п m, - Metcalfe 
1206 (М (MO, NY); Lincoln Co., 11 km W of Ruidoso, 


: , Santa Fe Canyon, E 
my Fe, Heller & pes 3822 (BM, CAS, K, MO, 
REGON es Co., Paulina Creek, 

: бот, Leiberg 353 Ec UO); Jackson Co., Wim- 
t, Hammond 157a (CS); Klamath Co., Crater Lake 
Natl Park, 1, y Heller 13469 (CAS, ILL, WTU). 
SOUTH DAKOTA: Lawrence кас . S of Deadwood, 
ET 5707 (M O, NY). UTAH: Duchesne Co., 6 km 
on Lake, 2,350 m, Harris & Larsen 7612 


LOWRY & JONES— OSMORHIZA 


1167 


(MO, RM); Garfield Co., Henry Mts., 2,400 m, 
McVaugh 14681 (CAS, MICH, NY, SMU, TEX); 


1 
(ARIZ, CAS, ILL, NY, TEX, UC, WIS, WTU); 
Juan Co., Abajo Mts., Goodman & Hitchcock 1437 


Со., Wenatchie region, ми 794 (NY, UC. King 
Co., Seattle, Talcott, 15 E 1891 (MICH); Okanogan 
ers Cre h St. John et al. ~ 186 (МО, 
А НЕ Alban Laramie 
Range, 2; 500 т, Hartman 3122 (RM); Big Horn Co; 
42 km W of Burgess rested be; Horn Mts., Lowry 
1423 (ILL); жес p СО: reek Campground, 
Medicine Bow Mts., Lowry nee (ILL, MO, NY, RM, 
UCE Subletis Се. Middle Piney Lake, 2,600 m, € 
& Meyer 2402 (M MO, NY, UC); Teton Co., 5 кт W 
bec Pass, Lowry 1119 (ILL, MO, NY, JU 
ADA. ALBERTA: Hide Hills, 1,450 m, Boivin 
= Gilt 8929 (DAO); Chi ; 
ark, 1,45 по 15881 


Pase dt hi Bannan 5470 cime SMU): Elbow 
River Valley, —€— Moodie 1056 (NY, U 

below Canmore, 1 m, Ewan 18685 тев ы г 
land Park, E of Ft. tacet Turner 4498 (DAO); 
Battle La 


UC); Geraldine Lakes per, Lowry 961 (ILL, 

UC); near Atauwan ein Slave Lake Dist., Brinkman 

4335 (NY); SW of Spirit River, Moss 8415 (DAO); 

Saddle Hills, N of Sexsmith, Moss 9948 (WIS); 

bley, Wallace for Jenkins 734 (DAO). 
f Waterton Lakes, 1,550 


Lowry 1005 (ILL, MO, RM 

land, 600 m, и 466 (NY, RM); 

Botanie Valley, 1,200 m, Beamish et $e 8204 (DAO); 
hree Mile, on Lac ache-Williams Lake Rd., 

Calder et al. 18970 uw 24 km SW of vae Kleene, 


МЕСТО km W of Puntataenkut Lake, 
of Quesnel, 1,150 A ‚ Calder et al. 18212 (DAO): 
hene. KlnskusLa kes, I лс 5); се George, 


600 m, Florian 94 (DAO), T km W of Burns Lake, 
Calder et al. 12780 (DAO); 5 km S of Ft. McLeod, 
Calder et al. 12445 (DAO, UC); ts River, 67 km W 

on Creek, Taylor 


reek Village, 1,050 m, Calder et al. 
1 13702 (DAO): = km S of Takla Landing, SS 7916 
ў 40 km NW of Takla Lake, abe 
7998 vens геты Lake, SSW of Ft. Nelson, 1 400 m, 
Calder & Kukkonen 27162 (DAO, UC); Laird Hot- 
springs, 500 m, Calder & Gillett 25575 (CAS, DAO, 
UC); mile 578, Alaska Hwy., alder & Gillette 
25655 (DAO). MANITOBA: Mont Dauphin, Norgate, 


1168 


Boivin et al. 10682 (DAO); 13 km W of Norgate, Rid- 
ing Mt. Nat ^ Ó 
try 


NORTHWEST TERRITORIES: Charlton (€ James Bay, 
Porsild 4506 (ОАО — photo ex CAN); M 
Cody & Spicer 11787 (NY, SMU, UC). NEW B 
brum waska Co., Claire, Eaton M-89 (LL) NEw- 
OUNDLAND: Dildo, Notre Dame Bay, Fernald & Wie- 
uns 5952 (К, NY); Benoit's Cove, Humber Arm, Bay 
of Islands, Fernald & Wiegand 3767 (BM); French- 
man’s Cove, Bay of Islands, Waghorne 15 (MO); Port 
au Port, MacKenzie, 30 July 1921 (NY, UC); Nameless 
Cove-Mistaken Cove, Straights of Belle Isle, Wiegand 
et al. 28767 (GH, US); Forteau, Labrador, Waghorne, 


= 


Algoma Dist., Marie-Victorin & Rolland-Germain 
27340 (CAS); Thunder Bay Dist., Mortimer Island, 
Slate Islands, Hosie et al. 2187 (UC); зла анар: Вау, 


Lake Nipigon, Garton 7248 (ЮАО). ОЏЕВЕС: Gaspé 
Co., Grand River, Fernald s.n. (MICH. | ; La 
Jean—Ouest Co., Chambord, Roberval, Leduc L-69- 


25 June ee се Riviére-du-Loup Со., 
Rivi p, Cayouette & Cing-Mars, 19 June 
aa Pen аар Со., Кіуіёге du Renard, An- 
ticosti Island, Marie- Victorin & Rolland-Germain 
27139 (MO, WIS); Niapisca, Mingan Islands, Hamel 
& Genereux 3140 (DAO). SASKATCHEWAN: Maple Creek 
Dist., Cypress Hills, Hudson 1838 (DAO); Melfort Dist., 

McKague, Breitung, 30 Jan. 1935 (DAO); Qu’Appelle 
Dist., Cherry Lake, SE of Indian Head, Jones & Led- 
ingham 742 (DAO): Wallwort, Breitung 651 (DAO, 


9 


m 


ARGENTIN UT: Rio Senguerr, Lago La Plata, 
Krapovickas ‘4241 ( 1 (ОС). NEUQUEN: Los Lagos, Fortin 
hacab 


stance 3845 (G, K, UC); Correntoso, Lago Nahuel Hu- 
api, Edwards s.n. (BM). Río NEGRO: Bariloche, Parque 
Nac. Nahuel Huapi, Boelcke 5405, 5436 (UC); Estacis 
Lago Roca, 350 m, James 411 ü 


Cristina, 850 m, Vervoorst 4387 (MO). TIERRA DEL 


FUEGO: Ushuaia, Lago Fagnano, Boelcke et al. 15236 
(UC), Moore 2845 (K); berton, Constance et al. 
3861 (UC), Goodall 164, 1025 (UC); Bahía Aguirre, 


tados, Goodall 1579 (UC), Moore 2079 (K); Estancia 
Viamonte, Goodall 2823 


6 bis (Z), Monte 
Olivia, Hunziker 8206 (UC); Estancia la Esperanza 
210 m, Mexia 7925 (BM, G, K, MO, NY, UC), Moore 

5 ); Sierra Alvaer, Е of Paso Garibaldi, Moore 
1818 (K). 

CHILE. a Rosvig, 200 m, Donat 346 (BM, 
CAS, К, NY); y Pt., Cunningham s.n 
DeCandolle m. eres (P) Buncombe Bay, Commerson 
s.n. (P); Punta Arenas, 20 m, Ey seen et al. 24105 
(G; K, UC) "Stafford 26 (NY), sigs 61, is (P), 
McLean D.A.14 (BM), Hatcher s ; Estancia 
Maria Cristina, 80 km NE o Рини. Arenas, Goodall 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Уо1. 71 


4018 (UC); Puerto Williams, Navarino Island, Godley 
884 (K, UC); Pecket Harbor, Hombron s.n. (P); Orange 
Harbor, Hyades 472 (P), U.S. S Pac. Expl. Exped. (P), 
Port Famine, Le Guillou s.n. (P), Marivault s.n. (P); 
Estancia Cameron, NW shore Lago Blanco, Moore 2145 
(К, UC); Estancia Уісића, 200 m, Moore 2177 (UC); 
Port Galant, ааш s.n. (Р). NUBLE: Termas de Chil- 
prs Jaffuel 3765 (GH, cited in Constance & Shan, 

48). VALDIVIA: Valdivia, Lechler 225 (СОЕТ); Phi- 
loots n. (G). 


Osmorhiza depauperata was described by Phi- 
lippi (1894) from material collected in South 
America. At the time Constance and Shan (1948) 
prepared their treatment of Osmorhiza, they were 
uncertain as to the identity of this name, and 
tentatively placed it in synonymy under О. chi- 
lensis. Instead, they accepted the name Osmor- 
hiza obtusa for the taxon with clavate fruit and 
divaricate rays and pedicels. In 1954, Constance 
visited the Museo Nacional de Historia Natural 
in Santiago, Chile, where he examined the type 
material of Osmorhiza depauperata (Constance, 
pers. comm.). Three years later, this name was 
first used for North American plants by Mathias 
and Constance (1957: 11), with the following 
footnote: “Examination of Philippi's type at San- 
tiago, Chile, has verified the necessity of substi- 
tuting this name [O. depauperata] for the here- 
tofore accepted O. obtusa (c. & R.) Fernald. 3 
Although Philippi’s typ 
for loan, we were able to obtain photographs of 
the two specimens through the courtesy of Dra. 
Менса Mufioz S., Curator of Botany at 500. 
While examination of these photographs does 
not, by itself, reveal with certainty the identity 
of Philippi’s specimens, information contained 
in Constance а notes on them indicates that pe 
name О 
to the taxon earlier referred to as O. obtusa. 


LITERATURE CITED 
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& L. CONSTANCE. 1957. Chromosome num- 

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— & 


Chro 
Um belliferae. III. Amer . J. Bot. 53: 
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| Leip 
ERDTMAN, G. 


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A GUIDE TO COLLECTING PASSIONFLOWERS! 


P. M. JORGENSEN, J. E. LAWESSON, AND L. B. HOLM-NIELSEN? 


ABSTRACT 


Collections of passionflowers are often inadequate for taxonomic studies because и Е 
description of their complicated flower structures, і.е., corona, operculum, nectar ring, and lim 
These structures are highly important to the taxonomy of Passiflora. Instructions are Oc aye on 
how to make good, properly labelled collections of passionflowers. 


Passifloraceae comprises four genera and about 
400 species in the New World, most of which 
occur in South America. The four genera are: 
Passiflora (including Tetrastylis) with 390 species, 
Dilkea with five species, Mitostemma with three 
species, and Ancistrothyrsus with one or two 
species. 


FLORAL MORPHOLOGY 


Different terms have been used to describe the 
floral parts of Passifloraceae. The terminology of 
H. Harms (1893) and E. P. Killip (1938) is used. 
Variation in these characters is shown in Fig- 
ure 1. 

Corona. The corona usually consists of nu- 
merous elongate extensions. They are often dif- 
ferently colored than the sepals and petals and 
arranged 1 in one 19 ten filament series Or rows. 
Whether tł liguliform, 
or spathulate; straight or falcate; terete or angled 
is important in distinguishing the species. 

Operculum. The operculum is normally a 
membranous structure below the corona, which 
rarely has filiformous extensions. It represents a 
“closed door” to non-pollinating visitors. It is 
most important as a distinguishing character at 
the subgeneric and specific level. Whether it is 
curved, straight, recurved, or plicate should be 
noted when collecting because such details are 
difficult to see in dried specimens. The nature of 
the operculum margins (entire, bs lobu- 
late, or filiform) should also be noted. 

Nectar ring. The nectar ring is a low narrow 
ring below the operculum, at the bottom of the 
tube. Its presence or absence (it is often absent) 


should be noted and, when present, its shape and 


The limen may be similar to the nec- 
tar ring, or it may be a cup-shaped membrane 
more or less closely surrounding the base of the 
gynophore. Because the limen is not present in 
all species, its presence or absence should always 
be noted when collecting, as well as the nature 
of its margin (serrulate, lobulate, entire, dentic- 
ulate). 


How TO COLLECT 


Information that should be gathered when col- 
lecting is listed in Table 1. Passifloras are her- 
baceous and woody vines, or sometimes scan- 
dent shrubs or treelets. Treelets and lianas show 
much variation in leaf size, the lower leaves often 
being several times larger than leaves of flow- 
ering and terminal branches. It is therefore im- 
portant to collect both types of leaves. 

Passifloras should always be examined care- 
fully when collected. Do not wait a few hours 
because the flower will often collapse. Because 
of the importance of the inner floral characters, 
notes on these will help in identification. Large 
and long-tubed flowers (e.g., subg. Granadilla and 
Tacsonia) should be opened, or partly cut lon- 
gitudinally, before pressing, so the internal struc- 
tures are clearly visible. Small flowers (e.g., subg. 
Plectostemma) can be pressed without this sec- 
tioning, but should be pressed with the flowers 
open. 

Whenever possible, flowering material should 
also be preserved in FAA, together with pieces 
of stem, leaves, etc. Large fruits should be cut 


" We are indebted to Mrs. Kirsten Tind who made the drawings and Dr. Robert В. Haynes for reading the 


manuscri 


3 Botanical Institute, University of Aarhus, 68 Nordlandsvej, DK-8240, Risskov, Denmark. 


ANN. MISSOURI Bor. GARD. 71: 1172-1174. 1984. 


1984] JORGENSEN ET AL.—COLLECTING PASSIONFLOWERS 1173 


stigma 


anther androgynoph. 


corona 


17 m 
У operculum pedicel 


T—calyx tube 
—androgynophore 


and rogynophore 
operculum 


| 


Ман 
nectar 


bract 


pedicel 


B C 


FIGURE 1. Variation in Passiflora. — A. subg. — T" capsularis L.—B. subg. Granadillas- 
trum. Р.) manicata (Juss.) Pers.—C. subg. Tacsonia. Р. mixt 


1174 


TABLE 1. 


Checklist for notes of passifloras. 


Faua y rae 


SD Ou 


8 


— 


terete, spiny, branching pattern 


eral data. (Fi 


Gen g. 2) 
. Collector and dcn num 


mber. 
Locality: province, closest village/city, latitude, 


longitude. 


Habitat: vegetation, substrate. 
Elevation in meters. 


Common name E" use. 

Specimen data 6:2) 

Habit: herb, ne tree, liana; and height in me- 
ters. 


iamatar 


mooth. striate , winged, 


racts: present, absent, united/free, color. 
аи aristilation, color outside and inside. 


rm, spathu- 


um: present/absent, plicate/nonplicate, 
curved rved, horizontal. Margin of opercu- 
lum (entire, menus. serrulate, filiform). 

Nectar ring: present/absent. 

Limen: present/absent, margin (entire, crenulate, 


denticulate). 
0. Andr 


ogynophore: color of stamens, anthers, ovary, 
styles, stigma. 
Fruits: mature size, shape, color, seed color. 
Special data. 


. Transplant: seeds, cuttings 


gs. 
Preservation in FAA: stems, leaves, flowers, or 
fruits. 


. Photographs: flowers, fruits, etc., picture number. 
4. ed. 


Pollinators observ 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


into halves or smaller slices, and some seeds dried 
separately. 

Color photographs of the flower are valuable 
tools in the description ofthe flower and its colors. 


LIVING MATERIAL 


The easiest way of transferring passifloras into 
cultivation is by seeds, although these are some- 
times difficult to germinate. Seeds from mature 
fruits are removed from the pulp and dried. Cut- 
tings of Passiflora are very easy to grow if planted 
within a few days of collection. 


LITERATURE CITED 


Harms, H. 1893. Passifloraceae in H. G. A. Engler, 
Nat. Pflanzenfam. 3(6a): 67-92. 

KirLiP, E. 1938. Passifloraceae. Publ. Field Mus. Nat. 
Hist., Bot. Ser. 19: 1-613 


FLORA OF ECUADOR 
Collected by L. Holm-Nielsen & R. Andrade. 


No. 18545 

Passiflora manicata (Juss.) Pers. 
Prov. COTOPAXI: 
Ro 
Alt. 1250 m. (79°05’W 1909'5) 7. July 1979. 


ad Angamarca-El Corazon just below Pinllopata. Remnants of montane forest. 


Passifloraceae 


Liana 3 m, weakly branching. Bracts united, pale green. Sepals aristilate, bright red 
outside and inside, base white. Petals same colour as sepals, veins white. Filaments 
purple, apex white, 5 rows, no. 3 at base membraneous, upper part split. Operculum 
nonplicate, recurved, margin minutely denticulate, white. Nectar ring absent. Limen 
membraneous, erect, margin lobulate 
Photo, FAA, Transplant. 


Botanical Institute, University of Aarhus, Denmark (AAU). Project di 


FIGURE 2. Voucher label for a Passiflora collection. 


і 
| 
| 
q 
1 
d 
: 


а каса 


TEMERE 


iS i а ава NEN ISIN ITINERE Tn 


ur new species of Rubiaceae are descri 
(Hillia ара. One variety is described from 
Th 


Miescuri Botanic У шс 


al 
Investigations, Nationa itute, Herbari 


Since 1977 the Missouri Botanical Garden, re- 
cipient of a grant from the National Science 
Foundation of the United States, and the Her- 
bario Nacional of Venezuela, recipient of a sim- 
ilar gran 


joint botanical explorations into various por- 
tions of Venezuela to make inventories of the 
flora i in those areas previously unexplored, M 


to the construction of dams, drainage projects, 
or agricultural and lumbering activities. 

These explorations have resulted in a large 
number of additions to the known flora of Ven- 
ezuela, as Wd as a considerable assemblage of 
undescribed ta 

In the Бе paper а few taxa of undescribed 
Rubiaceae are presented. 


Guettarda leiantha Steyerm., sp. nov. TYPE: Ven- 
ezuela. Amazonas: along road between Paso 
El Diablo and Сапо de Culebra, 25—30 km 
SE of Puerto Ayacucho, 100 m, 12 May 1980, 
Steyermark, Davidse & Guanchez 122318 
(holotype, VEN; isotype, MO) 

Arbor 5- -metralis, Panis glabris; foliis ans get pe- 
tiolis 1-2 cm longis modice cris s; laminis 
elliptico-ovatis а. ед acuminatis besi haaat 12- 17cm 
longis, 5.5-7.5 cm latis, subtus p r axillas barbel- 
pus е alque nervos breviter crispato-villosulos glabris, 


pilosula 

ter glabris, nervis lateralibus utroque latere ca. 7 
Es adscendentibus ante marginem 3-4 mm an- 
astomosantibus; inflorescentia semel dichotoma, quo- 
que ramulo inflorescentiae 8—15-flora semel vel non 
Eu dichotoma; pedunculo tenui 4 cm | longo, 0. ~ 


E calyce hypant thioque l. 5 mm longis s, hypan- 
thio 1 mm longo, 0.8 mm lato glabro, lobis calycis 


w taxa have erii from a joint project of роне 
National Science F Foundation co to cal 
1 Рагк d o Nacional of Caracas, fhe eto by CONICIT (Con- 
sejo Nacional de Investigaciones Cientificas y Tecnológicas). 


NEW RUBIACEAE FROM VENEZUELA 
JULIAN A. STEYERMARK! 
ABSTRACT 


d from Venezuela: three from Territorio Federal Ama- 
zonas (Guettarda leiantha, Psychotria m Psychotria «чн 
Es Yara 


ii), and one from Estado Zulia 
tado uy (Psychotria а var. villipila). 
in Venezuela under a grant to the 
e Division of Biologi 


paullo inaequalibus suborbiculari-ovatis obtusis 0.3— 
0.4 mm longis, 0.3-0. 4 mm latis 5 sparsim ciliolatis; 
10mm longa, tubo 
8 mm longo, 1 mm lato extus glabro intus basi annulo 
tructo inde 5 mm pea Gig слон 
£i. 


latis, uno vel duobus lobis parce crenulatis i intos ma mar- 


iil 
$ 11 


eh glabro. | 


Tree 5 m tall, үи glabrous. Leaves pet- 
iolate, petioles 1-2 cm long, moderately crisp- 
pilose; leaf-blades elliptic-ovate, acuminate at 
apex, б at base, 12-17 cm long, 5.5-7.5 cm 
wide, ли to moderately appressed-pilosu- 
lous above on midnerve, elsewhere glabrous, leaf 
axils beneath slightly barbellate, shortly crisp- 
villosulous on main and secondary nerves, gla- 
brous on surface, lateral nerves ca. 7 each side, 
slender. Inflorescence with 2 primary axes either 
not forked or once-forked, each fork bearing 8— 
15 flowers; peduncle slender, 4—5 cm long, 0.5 
mm thick, moderately minutely crisp-pilosu- 
ou calyx and hypanthium 
|, 5: mm long, hypanthium 1 mm long, 0.8 mm 
wide; calyx lobes slightly unequal, suborbicular- 
ovate, obtuse mm by 0.3-0.4 mm, 
sparsely citiolate; corolla slenderly hypocrateri- 
orm, 10 mm long, the tube 8 mm long, 1 mm 
broad, glabrous without, sparsely pilose in the 
basal m within with a dense pilose ring at 
the very base, lobes oval-oblong, rounded at apex, 
1.5 mm by 1.5 mm, glabrous without, papillate 
within on margins, 1 or 2 of the lobes incon- 
spicuously crenulate; anthers linear, included, 2.7 
mm long, inserted in the uppermost % of tube; 
filaments 0.5 mm long; style filiform, 9 mm long, 
glabrous; fruit not seen. 


— 


د 
Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166.‏ ' 


ANN. MISSOURI BOT. GARD. 71: 1175-1179. 1984. 


1176 


This taxon is allied to G. acreana Krause and 
G. ulei Krause, from which it may be distin- 
guished by the completely glabrous exterior of 
the corolla, glabrous hypanthium, inflorescence 
with only two slender primary axes either once 
or not at all forked, and glabrous lower surface 
of the leaf blade. 


Hillia zuliaensis Steyerm., sp. nov. TYPE: Ven- 
ezuela. Zulia: Mara, vicinity of Río Guasare, 
between Rancho 505 and Cerro Yolanda, 
10°53-56'N, 72?26-28'W, 200-270 m, 29 
May 1980, Steyermark, Davidse & Stoddart 
122876 (holotype, VEN; isotype, MO). 
PARATYPE: Venezuela. Zulia: Cerro Los 
Manantiales, forested Окем slopes and 
ridges, E of Rio Guasare, W of Hacienda 
Los Manantiales on property of lee 
Morales, 12 km W of Corpozulia Cam 
mento oa 11°1'N, 72?20'30"W, 600 
m, 3 June 1980, Steyermark, Davidse & 

Stoddart аи (МО, УЕМ). 


Planta epiphytica lignosa отпіпо glabra; stipulis 
caducis late obovatis. acutis striatis 15 mm longis, 


ante marginem 1-3 mm ап 


Glabrous duin Stipules caducous, apical, 
broadly obovate, acute, 15 mm by 7 mm, striate. 
Leaves shortly petiolate, petioles 1-5 mm long; 
leaf blades coriaceous, broadly ovate to oblong- 
ovate, abruptly acute at apex, rounded to broadly 
obtuse at base, 9-12 cm long, 5-7 cm wide, pin- 
nately nerved with 7-8 prominulous, ascending 
nerves on each side, anastomosing 1-3 mm from 
margin, tertiary venation loosely reticulate as seen 


equally split into 6 lanceolate or triangular-lan- 
ceolate, acute lobes 3-15 mm long, 3-8 mm wide; 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


squamellae numerous within at base of tube, 
dentiform, 0. 5 mm long. Corolla al 
m iong, 
the tube 12 mm long, 9.5 mm wide at жың 

mm wide below; lobes 5, ligulate-rounded and 
cucullate at apex, 9 mm long, 4 mm wide; sta- 
mens 5, included, attached halfway up tube; 
anthers 10 mm long; filaments 2 mm long; style 
21 mm long, glabrous; ovary subcylindric, nar- 
rowly obconic, 10-12 mm long, 5 mm wide at 
apex, glabrous. 


The рех species differs from H. costanensis 
Steyerm., the group 
with spathiform calyx, in having a shorter ови 
tube with longer calyx lobes. 


Psychotria aubletiana Steyerm. var. villipila 
Steyerm., var. nov. TYPE: Venezuela. Ya- 
racuy: Sierra de Aroa, 15-20 km NW of 
Cocorote on road to Aroa, from 1 km SE of 
Los Cruceros to El Refugio, ca. 11 km W of 
San Felipe, 10°24’N, 68°51'W, 1,200-1,600 
m, 5 Apr. 1980, Liesner & Gonzalez 10107 
(holotype, VEN; isotype, MO). PARATYPE: 
ips: Yaracuy: Sierra de Aroa, Cerro 
Negro, primary forest 8 km SW of San Fe- 
lipe, ner 69?01"W, 1,200-1,800 m, 1- 
2 Apr. 1980, Liesner & Gonzalez 9939 (MO, 
VEN). 

Suffrutex 1-1.5-metralis, ramulis superne villosis pilis 
laxis munitis; stipulis i in vaginis extus tomentosis con- 
ра is, 

2.5-3.5 mm longis glabris ornatis; foliorum laminis 
costa media subtus laxe pilosa pilis laxe adscendenti- 
bus; кеги axillaribus terminalibusque; inflo- 
rescen week involucralibus dimidio parte infer- 
iore гаан: pilis patentibus 1-1.5 mm longis 
praeditis. 


Suffruticose, 1-1.5 m tall, stems shortly ap- 
pressed between nodes, hirtellous to villosulous 
below the inflorescences, stipules, and petiolar 
attachment, villous apically and on uppermost 
nodes. Stipular sheath 0.5-1 mm long, tomen- 
tose without, the teeth lanceolate, acute to acu- 
minate, 2.5-3.5 mm long, 0.5-1 mm wide, gla- 
brous. Leaves petiolate, petiole 3-10 mm long, 
densely hirtellous-pilosulous with loosely as- 
cending hairs; leaf-blades lance-elliptic or ellip- 
tic-lanceolate, acuminate at apex, acute at base, 
4.5-8.5 cm long, 1–2.7 cm wide, glabrous above, 
midrib below lub pilose with ascending hairs, 
glabrous elsewhere; lateral nerves 8—9 each side, 
with finer intermediate nerves. Heads terminal 
and axillary, subhemispheric, 8-10 mm high, 13- 


тами. 


1984] 


15 mm wide; involucre hirtellous-villous at base 
and in lower half with spreading hairs 1-1.5 mm 
long; floral bracts cucullate, pilosulous near apex 
and upper half, elsewhere glabrous; corolla tube 
and lobes glabrous. 


This variety differs from P. aubletiana Stey- 
erm. var. aubletiana in the lanceolate, acute to 
acuminate stipular teeth, the loose pubescence 
of the upper portion of the stems, exterior por- 
tion of the involucre, similarly loose pubescence 
of the lower midrib, in the terminal as well 
as axillary Вогез вон From Р. aubletiana var. 
producta Steyerm. it differs in the shorter stipular 
teeth and villous pubescence of the lower midrib, 
while from var. andina Steyerm. f. pubescens 
Steyerm. it is differentiated by the acute to acu- 
minate stipular teeth and villous spreading pu- 
bescence. Because of the terminal as well as ax- 
illary inflorescences, future collections may well 
indicate specific status for this taxon. 


Psychotria davidsae Steyerm., 
Venezuela. Amazonas: Atures, vi 


2 


sp. ПОУ. TYPE: 
rain- 


forest along Rio Cataniapo, on N side of 


river at dam site, 48 km SE of Puerto Ayacu- 
cho, 5?35'N, 67°15’W, 200-300 m, 10 May 
1980, Steyermark, Davidse & Guanchez 
122197 (holotype, VEN; isotype, MO). 
PARATYPES: Venezuela. А. 


al este de Puerto Ayacucho hacia Gavilan, 
5*35'N, 67°22'W, 120 m, 11 June 1977, 
Steyermark, Berry, Huber & Redmond 
113893 (VEN). Bolivar: Sierra Pakaraima, 
frontera no. 10, 4?7'N, 65°43’W, 1,200 m, 
2 May 1973, Steyermark, Gil, Quintero & 
F. José García 107206 (VEN). 


Suffrutex 0.5- ees ramulis debis modice 
Vel dense puberulis pilis brunneis bre s munitis; 
stipulis in vaginam 1. 5 mm longam, 3 mm pem mo- 
dice puberulam connatis, utroque latere in dentes duos 
lanceolatos acuminatos 2-2.5 mm longos, 0.5-0.7 m 
latos desinentibus; foliis | oppositis petiolatis, petiolis 


lamin late ovatis vel  elliptico-o ovatis. vel oblongo-ti- 
6)cm 
26) ст 
ay 4-7, 5(—13) cm latis, supra praeter costam me- 
diam puberulam glabris, subtus sparsim vel modice 
Subadpresso- puberulis, c osta media nervii 


s laterali 

p паду pilis patentibus vel crispatis 

Instructis, marginibus ciliatis; nerviis lateralibus ut- 
entibus in margi 


bus umbellatim ramosis 2— 
(pedunculo amewa 2. is cm lata pedun- 
culata, peduncullo 5-25 mm longo, 1.5 mm diam. dense 


STEYERMARK —NEW RUBIACEAE 


1177 


tomentoso pilis patentibus 0.2-0.4 mm longis munito; 
inflorescentiae axibus 4—5 patentibus 7-12 mm longis 


tremitatibus us axi um disposi tis, floribus i in quoque 


5 
vel lato obtusis 4—5 mm x m carinatis extus 


capitulo ae apice rotundata ‹ carinata 10 mm x 4 
mm utrinque modice puberula; calyce h 
1.8- 2 mm m longo, hypanthio subgloboso hirsutulo pilis 


lanceo 


latis ius 1-1. 3 mm longis, 0. 7-1 тт latis extus ad 


apicem s, marginibus valde ciliatis intus gla- 
bris, basi sinu jute lobos 1-glanduliferis; corolla bre- 
viter in ibuliformi 6-6. 5m m longa extus puberula, 

tubo 3–3.5 mm longo basi 1.5-2 m das Del io 3 


mm lato, lobis 5-6 EE apice tg 
vato attenuato 3 mm x * 1- 1. 5 mm intus s glabris, orificio 
intus dense villoso; antheris 5—6 linearibus 2mm longis 
vix exsertis medio tubi ipea, forem longistylorum 
stylis 6.5-7 mm longis; disco e 


Subligneous plant 0.5 m tall, the young stems 
moderately to densely, short а cogi one 


ascending hairs, the sheath e than кей. 
1.5m 


broadly ovate or elliptic-ovate, acute at apex, 
cuneately acute at base, 6–15(–26) cm long, 4- 
7.5(-13) cm wide, glabrous above except the 
midrib puberulent, midrib and lateral nerves be- 
low moderately puberulous with spreading or 


pressed hairs, margins ciliolate; lateral nerves 6– 
10 each side, arcuately ascending, ending at mar- 
gins. Inflorescence terminal, pedunculate, in- 
cluding peduncle 2-3 cm long, 2.5—5 cm wide, 
the main or lower axes umbellately branched; 
peduncle 5-25 mm long, 1.5 mm thick, densely 
tomentose with spreading hairs 0.2-0.4 mm long, 
axes of inflorescence 4—5, spreading, 7-12 cm 
long, densely brown-tomentose; flowers subcap- 
itate at the ends of each axis, in groups mainly 
of 3 heads with 10-13 flowers in each group; 
heads subtended by 4-7 lingulate to subspathu- 
late, rounded to broadly obtuse, cucullate bracts 
4-5 m rinate, mod- 


hirsutulous with spreading brown hairs, 0.5-1 
m high; calyx lobes 5, ovate-lanceolate, acute, 


1178 


1-1.5 mm long, 0.75-1 mm wide, hirsutulous 
apically without, glabrous within, strongly cil- 
iate, with 1 or sometimes 2 elliptical squamellae 
in the sinus between each calyx lobe within; disk 
exserted, about У; length of calyx lobes. Corolla 
white-creamy, short infundibuliform, 6-6.5 mm 
long, puberulous-pilosulous without, tube 3-3.5 
mm long, 1.5-2 mm wide at base, 3 mm wide 
at orifice, densely villous within at orifice, base 
of lobes and upper part of tube; lobes 5—6, lan- 
ceolate, cucullate-incurved and attenuate at apex, 
3 mm long, 1-1.5 mm wide, glabrous within; 
stamens 5—6, anthers linear, 2 mm long, barely 
exserted, inserted У up tube; filaments 0.5 mm 
long; style exserted in long-styled flowers, 6.5-7 
mm long. 


This species is closely related to P. brazoi Stey- 
erm., of northernmost Brazil (Serra da Neblina) 
and southeastern Colombia. From that taxon, P. 
davidsae differs in the following being more 

ensely pubescent: stipules, peduncles, axes of 
the inflorescence, calyx, and hypanthium, and 
lower surface of the leaf blades; the petioles are 
shorter, the calyx lobes more densely ciliolate; 
the corolla more densely pubescent in the upper 
half ofthe interior and orifice. It affords me great 
pleasure to dedicate this species to Dr. Gerrit 
Davidse, Coordinator for the Missouri Botanical 
Garden ofthe joint exploration project with Ven- 
ezuela. 


Psychotria plowmanii Steyerm., sp. nov. TYPE: 
Venezuela. Amazonas: Atures, virgin rain- 
forest along Río Cataniapo, 44-45 km SE 
of Puerto Ayacucho, 3 ownst 
dam site, 5?35'N, 67°15'W, 200-300 m, 9 
May 1980, Steyermark, Davidse & Guan- 
chez 122132 (holotype, VEN; isotype, MO). 

PARATYPES: Venezuela. Amazonas: Atures, 
bosque alto denso, a aproximadamente 2 
E. за suroeste del сазепо San Pedro de Са- 

, al suroeste de Puerto Ayacucho, 
PIN 671 1’W, 90-110 m, 1980, Guan- 
chez 140 (VEN); hillside "ape immediately 
behind “El Tobogán de la selva" camping 
area, 35 km S of Puerto rdiet 85 m, 
21 Feb. 1979, Plowman 7715 (F) 


Frutex 1.5-2-metralis; foliis Misi uem petiolatis, pe- 
tiolis 6-9 mm longis glabris; stip -4 
mm longam, 3-6 mm latam extu к чын connatis, 
тро late deltoideis obtusis dense albo-ciliatis 1.5 

m longis, vetustioribus apice truncatis; laminis char- 
em ceis oblanceolatis vel elliptico-oblanceolatis apice 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[Vor. 71 


acutis vel acuminatis basi cuneatim acutis vel acu- 
minatis 13-20 cm x 4-9 cm utrinque glabris, nervis 
lateralibus utroque latere 9-13 divaricate adscenden- 
tibus ante marginem 2-4 mm anastomasantibus ut- 
rinque elevatis, venulis t 

tus manifeste а inflorescentia terminali 1.5-3.5 
cm longa, 2-4 c ta pedunculata, pedunculo 2.5-4.5 
mm wea ] mm veh uides sparsimque papillato- 
puberulo; inflorescentiae axibus quinque vel sex 6-11 
mm longis, infimis patentibus vel reflexis longioribus 
quam Superioribus multifloris; floribus quu ag- 


subaxibus е i е 0. ds 5 mm 
longis ciliolatis calyce hypanthioque 1.2 mm longo, 
cune anthio breviter иш Lon 0.9 mm longo dimidia 

e inferiore minute puberulenti, calycis tubo lo- 
t 0.3 mm longis, lobis quinque leviter ына 
subobtusis minute papillato-ciliolatis, tubo sparsim 
cremosa infundi- 


tubo intus dimidia parte superiore den 

lobis имне lanceolatis obtusis apice cucullato-in- 

flexis 1 mm .9 mm; antheris oblongis 0.9 mm 

коњ pistillo 3mm longo, stylo dimidio parte supe- 
ore sparsim papillato-puberulo. 


Shrub 1.5-2 m tall. Stipular sheath 2-4 mm 
long, 3—6 mm wide, glabrous without, truncate 
or nearly so at the summit of older sheaths, up- 
permost sheath densely white-ciliate on border, 
uppermost stipule broadly deltoid, obtuse, 1.5 
mm high. Leaves petiolate, petiole 6—9 mm long, 
glabrous; leaf blades oblanceolate to elliptic-ob- 
lanceolate, acute to acuminate at apex, cuneately 
acute to acuminate at base, domatia absent in 
leaf axils beneath, 13—20 cm by 4—9 cm, glabrous; 
lateral nerves 9—13 each side, elevated both sides, 
divaricately ascending, anastomosing 2-4 mm 
from margin, tertiary venation coarsely reticu- 
late, conspicuous and elevated below, impressed 

ve and less conspicuous. Inflorescence ter- 
minal, about as broad as long, 1.5-3.5 cm long, 

cm wide, many-flowered toward the apices 
of the lateral axes, with 5—6 axes, the lowest pair 
spreading to reflexed and longer than the upper 
ones, 9-11 mm long, papillate-puberulent; pe- 
duncle 2.5-4.5 mm long, 1 mm thick, slender, 
minutely and sparsely papillate-puberulent; 
flowers sessile; bracts subtending axes of inflo- 
rescence suborbicular-ovate, subacute, 0.8-1.5 
mm long, ciliate. Calyx and hypanthium 1.2 mm 
long, hypanthium short-cylindric, 0.9 mm long, 

.5 mm wide, sparsely minutely puberulent in 
lower half: calyx tube and lobes 0.3 mm long, ! 
mm wide, sparsely papillate-puberulent on calyx 
tube to glabrate; calyx lobes 5, shallowly deltoid, 
subobtuse, minutely papillate-ciliolate, 0.3 mm 
high, 0.4 mm wide; corolla creamy, infundibu- 
liform, 3 mm long, basally narrowed to 0.7 mm 


| 


1984] 


wide, expanded at the limb to 1 mm long and 

3 mm wide at summit, glabrous without; co- 
rolla tube densely pubescent within midway at 
base of stamens; corolla lobes 5, lanceolate, ob- 
tuse at the cucullate inflexed apex, 1 mm long, 
0.7-0.9 mm wide. Stamens 5, anthers oblong, 
attached 1 mm above base of corolla tube; style 
0.6 mm long, rounded at apex, sparsely papillate- 
puberulent in upper half. 


STEYERMARK—NEW RUBIACEAE 


1179 


This taxon differs from P. ventuariana Standl. 
& Steyerm. in the puberulent hypanthium and 
shorter inflorescence nearly as broad as long with 
йе axes. ‚ From P. coussareoides ины. it ту 


1L 


the short кл 
er, differently shaped inflorescence with fewer 
es 


NOTES ON NEOTROPICAL LAURACEAE 
HENK VAN DER WERFF! 


ABSTRACT 


The following notes are based on a study of herbarium specimens of neotropical Lauraceae and are 
the first results of a long-term project on the American representatives of that family. Unless otherwise 
stated, all specimens studied are deposited in the herbarium of the Missouri Botanical Garden (MO). 
were softened by boiling for about half an hour. Softening with detergent 
ually about two hours) and this method was ү ев Lauraceous 
flowers are trimerous and ка of two (usually equal) whorls of three tepals and four whorls of three 


stamens, which are numbered from outside to inside with 


Roman numerals; the anthers of whorl IV, 


the innermost ones, are reduced to staminodia or lacking. 


Aiouea lundelliana Allen, J. Arnold Arbor. 26: 
419. 1945. TvPE: Panama. Chiriqui, White 
225 (holotype, МО!). 


Allen (19 OA 5) cited n H 11 PS. (th 


type) and two fruiting collections i in her descrip- 
tion. Kostermans annotated the type in 1959 as 
Aiouea costaricensis (Mez) Kostermans, a species 
restricted to Costa Rica and Panama. However, 
Renner (1982) excluded the species from Aiouea 
and referred it to Ocotea. In Ocotea it would key 
to O. tonduzii Standley, known from Costa Rica 
and Panama; indeed, Allen (1945) mentioned in 
the discussion of O. tonduzii that fruiting ma- 
terial is often confused with that of Aiouea (which 
she called Aniba by mistake) and that differences 
are very hard to formulate. Aiouea lundelliana 
and A. costaricensis are said to differ in leaf char- 
acters: leaves to 16(—18) cm long and 7.5 cm wide 
with apex obtusely and shortly acuminate and 

ghtly prominent beneath in A. /un- 
delliana and leaves to 12(-13) cm long and 6 cm 
wide with obtuse or rounded apex (very occa- 
sionally shortly acuminate) and reticulation very 
prominent beneath in A. costaricensis. These dif- 
ferences are weak and it is likely that only one 
species of Aiouea occurs in Costa Rica and Pan- 
ama 


Renner (1982) transferred A. lundelliana to 
Ocotea because the type specimen has anthers 
with four cells, while Aiouea has 2-celled anthers. 
The difference in number of anther cells is the 
only good character separating Ocotea from 
Aiouea; other characters mentioned in literature 
either do not apply to the Central American 
Aiouea species (Aiouea is said to have conspic- 
uous staminodia; in Ocotea staminodia are in 
conspicuous or lacking, but Renner (1982) do- 


scribes A. costaricensis as having minute 
staminodia, 0.5 mm long, or without stamino- 
dia) ог are not sufüicient for the separation of 

d with 


БУУН анчы 


a a thickened Margin in оце in ‘Ocotea leaves 
dry variously and thickened margin is not a rule). 
The different generic identifications by Allen and 
Kostermans on one hand and Renner on the oth- 
er stimulated me to check the number of anther 
cells in several flowers of the same specimen in 
order to verify if that number is constant. As 
controls, I also checked several flowers from col- 
lections identified as Aiouea costaricensis and 
Ocotea tonduzii. These species were chosen be- 
cause of their great resemblance to A. /undel- 
liana. 


Aiouea costaricensis 

Hartshorn 1121. Nine flowers checked. An- 
thers I, II and III all had 2 cells. 

Utley 3040. Five flowers checked; all anthers 
had 2 cells. 


Ocotea tonduzii 

Poveda 429, 1091 and Stevens 14131. Of each 
collection ten flowers checked. All anthers (I, П, 
and III) had 4 cells. 


Aiouea lundelliana 

White 225. Eight flowers checked. Anthers I 
and II were usually 2-celled, but sometimes only 
1 cell was developed. Anthers III were 4-celled 
in two flowers, 2-celled in one flower, and some- 
times rudimentary (no cells visible). 

Mori & Kallunki 5680. Six flowers checked. 
One flower had anthers I and II 4-celled and III 
rudimentary; three flowers had I and II 2-celled, 
III not sufficiently developed for counting, and 


' Missouri Botanical Garden. P.O. Box 299, St. Louis, Missouri 63166. 


ANN. Missouri Bor. GARD. 71: 1180—1183. 1984. 


uem да. а. m um 


= = 


1984] 


one flower was entirely 2-celled with open anther 
cells (were closed in other flowers). 

Lao 333. Two flowers checked. Some anthers 
were 2-celled, some 4-celled. On the 4-celled an- 
thers the upper two cells were usually much 
smaller than the lower two. 


To exclude the possibility that Aiouea lundel- 
liana is represented by pistillate specimens of a 
dioecious Ocotea species with poorly developed 
anthers, I checked seven flowers of an obvious 
dioecious Ocotea species (Ocotea cernua (Nees) 
Mez, represented by Brigada Doranthes 3015, 
Mexico). This species is not similar to the other 
three species. In all seven flowers, anthers I and 
II were 4-celled; in three flowers, anthers III were 


Aiouea lundelliana cannot be regarded as a pis- 
tillate specimen of a dioecious Ocotea species. 

The number of anther cells is one of the im- 
portant characters in the generic classification of 
_ Lauraceae. It has always been assumed that this 
_ number is constant and I have not found any 
references to examples of flowers with varyin 


ri 
- having anthers I and II 2-celled iud anthers Ш 
_ 4-celled, but these numbers are constant: I and 
II are always 2-celled and III always 4-celled. 
-. Similar conditions are also reported for Phoebe 
| and Persea species). The ‘variation in number of 
1 ther cells in Aiouea strong 
- Contrast to ite constancy of the number of anther 
- Cells in the Aiouea and Ocotea species and sug- 


area, 
3 iqui province, Panama; the collections were 

made in 1938, 1971, and 1975. The Mori and 
Kallunki collection has young fruits, so it is likely 
that the population on Cerro Punta ios pert 

Although Meis hybrids in ceae 
have been reported (Kubitzki, ^s а 
knowledge, пої 


ization and this hybridization makes the need 
for a reassessment of the genera even more ur- 
gent. 


| Nectandra kunthiana (Nees) Kosterm., Meded. 
Bot. Mus. Herb. Rijks Univ. Utrecht 25: 19. 


WERFF—LAUREACEAE 


1181 


1936. Acrodiclidium kunthianum Nees, Syst. 

Laur. 269. 1836. түре: French Guyana, Po- 

iteau s.n. (P, n.v.). Ocotea kunthiana (Nees) 

Mez, Jahrb. Kónigl. Bot. Gart. Berlin 5: 291. 
1889. 


Ocotea cooperi Allen, J. Arnold Arbor. 26: 335. 1945. 

2 DES ma. Bocas del Toro, Cooper & Slater 

96 (holotype, F; пене 
E meyeriana Lasse 

184. 1948. TvPE: neni a 


n, 
Bot. Gard. 10(5): 121. 1963. TYPE: Venezuela. 
Amazonas, Maguire, Cowan & Wirdack 29830 
(holotype, NY, n.v.). 
Nectandra kunthiana, a wide-ranging species, 
is characterized by 


young twigs, inflorescence, and flowers. It does 
not fit very well in any of the neotropical lau- 
raceous genera. It differs from typical Nectandra 

n being dioecious and from Ocotea in the po- 
po of the anther cells (not in two superpose 
rows, but more or less in an arc). Its generic 
Hirn can be determined only after the neo- 

opical lauraceous genera are much better de- 
in Differences cited by Allen (1965) between 
Nectandra kunthiana and N. meyeriana (leaves 
more consistently oblong, sharply reticulate 
throughout, with presumably a narrow, slightly 
acute cusp) are insufficient to separate these two 
species. A character given by Allen (1963) for 
Pleurothyrium cowanianum, leaf margins with 
dense pubescence, applies only to young leaves 

occurs also on Peruvian and Ecuadorian ma- 
terial; older leaves, found on fruiting material, 
are much less pubescent. 

Because Ocotea cooperi, Nectandra meyer- 
iana, and Pleurothyrium cowanianum cannot 
separated from Nectandra kunthiana, they are 
here placed in synonymy under the latter species. 

Nectandra kunthiana is now known from the 
Guyanas, Venezuela, Peru, Ecuador, Colombia, 
Panama, and Costa Rica, and I expect it occurs 
in Brazil as well. 


N tini is Mez, Mitt. Bot. Vereins 
Kreis Freiburg 47, 48: 421. 1888. ТҮРЕ: 
Trinidad, Sieber 99 (lectotype, G, n.v.; iso- 
lectotype, MO) 


— — MÀ — Técn. Minist. Agric. 


. 1942. TYPE: Ven Miranda, Pit- 
ле 570 (holotype, VEN!). “For additional syn- 
, see Howard, 1981. 


1182 


Nectandra martinicensis is an inconspicuous, 

widespread species that has been described three 
times from Central America (Bernardi, 1967). 
Characteristic for this species is the én bihition 
of membranaceous leaves, densely gland-dotted 
above, and the whitish pubescence on inflores- 
cence and buds. Pittier 8270 is in no way differ- 
ent from N. martinicensis and therefore N. glan- 
difolia is reduced to synonymy under that species. 
The known distribution of N. martinicensis is 
Mexico, Belize, El Salvador, Nicaragua, 
Rica, Panama, Colombia, Ecuador (fide Bernar- 
di, 1967), Venezuela (coastal mountains from 
Zulia to Miranda), Trinidad, Tobago, and Mont- 
serrat. 


Ocotea calophylla Mez, Jahrb. Kónigl. Bot. Gart. 
Berlin 5: 298. 1889. Pleurothyrium а 
num Meissner іп DC., Prodr. 15(1): 170. 
1864. ТУРЕ: Colombia. Near Antiquia, Jer- 
vise s.n. (К, n.v.). 


мее" acera Standley & L. O. Williams, Ceiba 1: 
1951. ТУРЕ: Costa Rica. Cordillera de Ta- 
ак 2,800 т, Leon 2166 (isotype, МО!). 


Ocotea calophylla Mez is one of the very few 
species of Ocotea restricted to high montane for- 
ests of the Venezuelan and Colombian Andes, 
usually above 2,500 m. Diagnostic characters are, 
in addition to its habitat, the sessile leaves with 
dense, ferruginous pubescence on the lower sur- 
face, the recurved base of the €— ‚апа he two 
vernation lines on the leaves. Whe y and 
Williams published Ocotea аде. they с com- 
pared it only with other Central American species, 
from which they considered it distinct because 
of its dense and persistent pubescence. Because 
Ocotea fulvescens agrees in all characters with 
Ocotea calophylla, it is here placed in synonymy 
under the latter species. 


Phoebe cinnamomifolia (Kunth) Nees, Linnaea 
21: 488. 1848. Persea cinnamomifolia 
Kunth, Nov. Gen. 2: 160. 1815. TYPE: Co- 
lombia, Humboldt & Bonpland s.n. (P, n.v.). 


e queso Meissner in DC., Prodr. 15(1): 31. 
. SYNTYPES: Mexico. Near Jalapa, Galeotti 

306 (BR, n.v. X Mirader, Linden 20 (BR, n.v.). 
Phoebe filamentosa Allen, Mem. New York Bot. Gard. 
15: 69. 1966. түре: Venezuela. Merida: along Río 
ems Steyermark 56740 (holotype, F!; isotype, 
О!). 


Phoebe cinnamomifolia is а wide-ranging, 
rather variable species, characterized by its al- 


ANNALS OF THE MISSOURI BOTANICAL GARDEN 


[VoL. 71 


most glabrous, tripliveined leaves, lower leaf sur- 
faces pale green due to the densely papillose epi- 
dermis, and the erect axillary or terminal 
inflorescences. Size of the leaves and pubescence 
of the flowers vary; plants from higher elevation 
tend to have smaller, more coriaceous leaves and 
pubescent inflorescences and flowers, whereas 
material from wet lowland forest (Barro Colo- 
rado, Panama; Rio Оша, Venezuela) has larger 
leaves and glabrous inflorescences and flowers. 
Phoebe johnstonii Allen, known only from Pan- 
ama, was separated by Allen from P. mexicana 
because of its shorter inflorescences (to 15 cm 
long in Р. mexicana, usually less than 12 cm in 
P. johnstonii), flowers not white-pubescent, and 
thinner and narrower leaves. It is doubtful 
whether it can be maintained as distinct from P. 
cinnamomifolia 

Phoebe rune miblia occurs throughout 
Central America, where it has been named P. 
mexicana, and in Venezuela, Colombia, and Peru. 


Phoebe triplinervis (Ruíz Lopez & Pavon) Mez, 
Jahrb. Kónigl. Bot. Gart. Berlin 5: 211. 1889. 
Laurus triplinervis Ruíz Lopez & Pavon, Fl. 
Peruv. 4: 30, t. 363. 1957. TYPE: Peru. Cu- 
chero, Ruíz Lopez, & Pavon s.n. 

Phoebe ее С. Smith, Bull. Torrey Bot. Club 

38: 103. 1931. TYPE: Peru. Junin, Killip & Smith 
22410 (holotype, NY!; isotype, F!). 

Macbride (1938) separated P. pichisensis from 
P. triplinervis by the leaf venation: pinnate in P. 
pichisensis, and tripliveined in P. triplinervis. 
However, venation on the type material of P. 
pichisensis does not differ from the venation of 
isotypes of P. triplinervis (MO!, F!). Since there 
are not other differences, P. pichisensis is reduced 
to synonymy under P. triplinervis. Phoebe par- 
aguayensis Hassler (isotype Hassler 11305, F!) 
is very similar to P. triplinervis and may Very 
well prove to be conspecific with it once more 
material is available. 


LITERATURE CITED 

ALLEN, СА. 1945. Studies іп Lauraceae, VI. Prelim- 

Central American 
species. um Arnold Arbor. 26: osi 34. 

. 1963. Lauraceae. In B. M . J. Wur- 

dack & collaborators, Botany of the жеде vnd 

land, V. Mem. New York Bot. Gard. 10(5) 

123. 


————, 1965. Lauraceae. In B. Maguire, J. J. Wur- 
dack & collaborators, Botany of the Guyana high- 


1984] WERFF—LAUREACEAE 1183 


land, VI. Mem. New York Bot. Gard. 12(3): 102- Lauraceae of the Lesser Antilles. J. Arnold Arbor. 
5-61 


; 62: 4 : 
_ BERNARDI, L. 1967; De nr spatio et ob for- Kusitzki, К. 1982. Aniba. Fl. Sere 26 рам 
у man—nonnularum specierum Nectandrae. Can- — МАСВЕШЕ, J. Е. 19 uracea 

dollea 22: 69-84. Field Mus. Маі. Hist., Bot. Ser. nor CORN 
_ Howarb, R. A. 1981. Nomenclatural notes on the RENNER, $. 1982. Aiouea. Fl. Neotrop. 31: 85-116. 


NOTES 


ALECTRA ASPERA (CHAM. & SCHLECHT.) 
L. O. WILLIAMS 


While writing the account of the genus Alectra 
Thunberg for the forthcoming Flora Mesoam- 
ericana, covering the area from Chiapas to Pan- 
ama (Gentry, 1981), we encountered a problem 
concerning the correct name for the Central 
American species 

Pedicularis melampyroides L. C. Rich. (1792) 
is the first published name for the species. The 
species was transferred into the genus Alectra by 
Kuntze (1891). Melchior (1941), in his revision 
of the genus Alectra, accepted А. melampyroides 
(L. C. Rich.) O. Kuntze as the valid name. How- 
ever, this is a later homonym of Alectra melam- 
pyroides Benth. (1846), which is a synonym of 
Alectra sessiliflora (Vahl) O. Kuntze (1891). The 
name A. melampyroides (L. C. Rich.) O. Kuntze 
is therefore illegitimate and cannot be used. Ben- 
tham (1846) used the name Alectra brasiliensis 
for the Central American species. 

Another name, Scrophularia fluminensis, was 
published for the species by Vellozo (1831) in 
“Florae Fluminensis.” Carauta (1973) stated that 
the effective date of publication of “Florae Flu- 
minensis” was 1829 for the text volume, not 
1825 as indicated on the title page. The “Florae 
Fluminensis Icones" vol. 6, containing the illus- 
tration of S. fluminensis Vellozo, was not pub- 
lished until 1831, although the title page is dated 
1827. Stearn (1971) transferred the species into 
Alectra with the combination A. fluminensis 
(Vellozo) Stearn. 

further name, Glossostylis aspera Cham. & 
Schlecht. (1828), was published for the same 
species and transferred to the genus Alectra by 
Williams (1972). 

The title page of Vellozo's “Florae Fluminen- 
sis" would indicate that Scrophularia fluminen- 
sis was the earliest valid specific epithet. How- 
ever delay in distribution of this work means that 
the earliest epithet is from Glossostylis aspera 


ANN. Missouri Bor. GARD. 71: 1184. 1984. 


and the correct name for the species 15 Alectra 
aspera (Cham. & Schlecht.) L. O. Williams. The 
synonyms of this taxon are listed below. 


-Alectra aspera (Cham. & Schlecht.) L. O. Wil- 


liams, Fieldiana, Bot. 34: 118. 1972. Glos- 
sostylis aspera Cham. & Schlecht., Linnaea 
3: 23. 1828. TYPE: Brazil. Provincia Rio Ja- 
neiro in fossis prope St. Annam, xii, Beyrich 
s.n. (HAL?, not seen). 


Alectra brasiliensis Benth. in DC., Prodr. 10: 339. 1846. 
Melasma brasiliense m) erani & Hassler, 
Bull. Herb. Boissier 4: 291. 

Alectra p (Velloz d. "s Arnold Arbor. 
52: 635. 1971. агага аи Vellozo, 
Florae Fluminensis 263. 

Alectra ма Lao B С. Hor x O. Kuntze, Revis. 
Gen. : 458. 1891, non ie 1846. Pedicu- 
laris ауда І. С. Rich., Actes Soc. Hist. 

s ОТН 1792. sehn melampy- 

i i en. 


Porto Rico & Virgin Islands 6(2): 188. 1925. 


We would like to thank Dr. C. E. Jarvis for 
comments on the manuscript. 


LITERATURE CITED 


CARAUTA, J. P. P. 1973. The text of Vellozo's Florae 
Fluminensis and its effective date of publication. 
Taxon 22: 84. 

GENTRY, A. (editor). 1981. 
Taxon 30: 709—713. 
MELCHIOR, H. 1941. Die Gattung Alectra Thunb. No- 

tizbl. Bot. Gart. Mus. Berlin-Dahlem 15: 423-447. 

VELLOZO, F. J. M. DA C. 1831. Florae Bp 
Icones 6: Tab. 87. Senefelder, Parisii 

WILLIAMS, L. О. 1972. Tropical пен plants, 
ХП. Fieldiana, Bot. 34: 101-132. 


— Rachel Hampshire and David Sutton, British 
Museum (Natural History), Cromwell Road, 
London SW7 5BD, United Kingdom. 


Flora Neotropica News. 


س ازا —— 


CIRCAEA ALPINA L. (ONAGRACEAE) IN THAILAND 


Craib (1931) included Circaea alpina L. in his 
“Florae Siamensis Enumeratio” on the basis of 
a collection made by Kerr at Doi Chiengdao. 
Fifty years later Shimizu et al. (1981), without 
citing specimens or references, included C. a 


China," and described and illustrated (p. 983, 
fig. 107: 17-22) C. mollis Sieb. & Zucc., the only 
species known at the time from the region he was 
treating. 

In my monograph of Circaea (Boufford, 1982) 


specimens of the Kerr collection cited by Craib. 
These specimens are Circaea alpina L. subsp. 
imaicola (Asch. & Mag.) Kitamura; they appar- 
ently remain as the only collection of the genus 
made to date in Thailand. Label data of the Kerr 
specimens are: Thailand, Doi Chiengdao, ca. 
2,100 m, on mossy rocks, A. F. G. Kerr 6607 
(ABD, K). 

Circaea alpina subsp. imaicola has been col- 
lected in similar situations in north and west 
тп Vietnam 


i 
latitude is somewhat south of the main range of 


distribution, it is not as far south as the popu- 
lations in southern India at about 10°N latitude 


` ANN. Missouni Вот. GARD. 71: 1185. 1984. 


where the subspecies is found at about the same 
elevation. Another species, C. mollis Sieb. & 
Zucc. has been collected in northern 


occurs at lower elevations and generally at lower 
oe than C. alpina subsp. imaicola. It is also 
o be expected i in Thailand, and both taxa should 


1 
Ue sought WiC VOL HM 


I would like to thank P. S. Ashton, H. Koyama, 
P. H. Raven, T. Shimizu, and T. Smitinand for 
their help int Circaea 
from Thailand, and the director of ABD and K 
for their loan of sepcime 


LITERATURE CITED 


Bourronp, D. E. 1982. The systematics and evolu- 
tion of Circaea و‎ e). Ann. Missouri Bot. 
Gard. 69: 804— 

CRAIB, W. С. psi "Сава Fl. Siam. 1: 734. 

GAGNEPAIN, F. 192 otheracées. In M. Н. Le- 
comte, Fl. UE es 981—993. 

T. SANTISUK 


E . 1981. Con 
of Southeast Asia VI. Taxonomy 
raphy of some Temperate Species in Thailand (2). 
Acta Phytotax. Geobot. 32: 37—46 


— David E. Boufford, The Arnold Arboretum of 
Harvard University, 22 Divinity Avenue, Cam- 
bridge, Massachusetts 02138. 


A NEW SPECIES OF GUATTERIA (ANNONACEAE) 
FROM PANAMA 


Guatteria jefensis Barringer (Annonaceae) a 
new species from Cerro Jefe, Panama is distin- 
guished from G. inuncta Fries by its smaller, 
thicker leaves, larger petals, umbonate anthers, 
and fruits with short thick stipes. It seems to be 
most closely related to species in section Tylodis- 

cus R. E. Fries. 

The genus Guatteria Ruiz & Pavon consists of 
about 250 species of neotropical trees and shrubs. 
Species are found from southern Mexico and the 
West Indies to Bolivia and southern Brazil, with 
the greatest density of species in the Amazon 
basin. The genus is distinguished from other An- 
nonaceae by its axillary flowers with ebracteate 
pedicels, imbricate petals, anthers with thick, 
flattened apices, and carpels with solitary basal 
ovules. 

The genus was revised by R. E. Fries (1939), 
who recognized 212 species. Fries continued to 
describe new species and by the time he wrote 
the treatment for the Flora of Panama (Fries, 
1962) he recognized nine Panamanian species, 
only five of which had been included in the re- 
vision. After Fries's death, little work was done 
on the family until Paul Maas and his group at 
Utrecht began their studies. The difficulty in in- 
terpreting Fries's concepts has been a major cause 
for the decreased interest in the family. Whereas 
many of Fries's taxa are good, his keys and di- 
agnostic characters are difficult to work with and 
are sometimes inaccurate. This has caused a 
buildup of undetermined material in herbaria. 
The species described here has been in herbaria 
for over a decade, but has been unrecognized 
until now. 


Guatteria jefensis Barringer, sp. nov. түре: Рап- 
ama. Panama: Cerro Jefe, near radio tower 
in Clusia forest, 3,000 ft., 3 Mar. 1979, B. 
Hammel 6302 (holotype, MO!). 


Guatteria inuncta R. E. Fries affinis sed foliis mi- 
noribus, coriaceis, ad basim rotundatis, petalis ma- 
jioribus, antheris umbonatis, monocarpis et stipitibus 
majioribus. 

Shrub or small tree, 3—4 m tall; young branches 
sericeous with adpressed yellow-red hairs, gla- 
brescent. Leaves alternate, often distichous; pet- 
iole 3-5 mm long thick, black, caniculate above, 
sericeous when young; lamina ovate, 7-12 cm 


long, 3-5 cm wide, coriaceous, stiff, often slightly 
conduplicate, the base rounded, the apex acute 
to acuminate, venation pinnate, 10—13 second- 
ary veins per side, secondaries not forming a 
canspicpous, arching submarginal vein, the ter- 


above, sericeous on veins below. Flowers 1—2 per 
axil on leafless portions of branches or in the 
axils of older leaves; pedicels 15—18 mm long, 
articulate 3-5 mm above the base, sericeous, 
thickened above; sepals 3, rounded-triangulate, 
densely yellow sericeous outside, often slightly 
sericeous within, the apex obtuse; petals broadly 
obovate to ovate, 10-15 mm long, 9-15 mm 
wide, the apex sometimes serrate on older petals, 
the outer three densely yellow sericeous below 
and less so above on outer surface, the inner 
surface with very fine brownish pubescence, the 
inner three slightly yellow sericeous on outside, 
with fine brown pubescence near apex on inner 
surface and dark brown and glabrous at base 
within; stamens many, 1.5-2 mm long, the apex 
expanded and flattened, slightly umbonate, the 
disk plane to slightly convex, pilose between the 
stamens and the carpels, the hairs concealed by 
the dense packing of the stamens and styles; car- 
pels many, 2—2.5.mm long, slightly sunken at the 
center of the disk, the ovule solitary, basal, erect. 
Monocarps ovoid, obtuse, 10-12 mm long, green 
turning purple, borne in dense clusters, the stipes 
thick, 8-12 mm long, г 


Additional specimens examined. PANAMA. Cerro 
Jefe, 11 Apr. 1977, = 11376 (MO); 21.7 km from 
Panamerican Highway, 22 June edi Folsom 3852 
(MO, 2); cloud forest, 850-900 m, 1.5 km WNW of 
weather station, 11 Apr. 1977, MM a d D'Arcy 
2510 (MO); thick forest near top of Cerro, 13 Sept. 
1970, Foster & Kennedy 1897 (MO); summit and along 
road on E slope, low cloud forest, 5 Apr. 1982, Knapp 
& Huft 4580 (MO); cloud forest dominated by Clusia 
spp. and Colpothri и 
along on ridge running om 
m, 11 May 1975, Mori & Виа 6078 (MO); 5 June 
1975, Mori & Kallunki 6501 (MO); 800 m, 10 EY 
1976, Sullivan 230 (MO); cloud forest, 850-900 m 
km of wi station, 7 Oct. 1980, Syts о. 

1476 мо top of Cerro, 3,140 ft., 7 Apr. 1966, Tyson 
3593 


Guatteria jefensis is recognized by its shrubby 
habit, small, coriaceous leaves, large flowers on 
older portions of the branches, umbonate ап- 


ANN. Missouri! Bor. GARD. 71: 1186-1187. 1984. 


Мао а а а р с 


1984] 


thers, and ovoid fruits with short, thick stipes. 
Also, the leaves are often slightly conduplicate 
and appear folded on herbarium sheets. It is most 
easily confused with G. inuncta R. E. Fries, the 
only other shrubby species of Guatteria in Pan- 
ama. Guatteria inuncta has larger leaves with 
cuneate bases, smaller flowers, anthers with flat 
apices, and fruits on long stipes 

It is often difficult to judge when the flowers 
have matured. Petals of most Guatteria species 
are never tightly closed in bud. Even when the 
flowers are quite young, the anthers and stigmas 
are easily seen. As the flowers mature, the petals 
enlarge and spread until, at anthesis, the anthers 
are fully exposed. Flower color changes during 
the development, gradually turning from green, 
to yellow and sometimes to a brownish yellow. 

According to Fries’s (1939) classification, G. 
Jefensis should be placed in section 7 ylodiscus 

. E. Fries along with G. dolichopoda J. D. Smith. 
Guatteria jefensis has the umbonate anthers and 


NOTES 


1187 


the dark, glabrous patches at the base of the pet- 
alst 


borne on slender stipes as found in all species of 
that section. 


Ith Loa ТА وء‎ с 11 m 


the Mesoamerican material of E. and 
William Burger for his help and his critical read- 
ing of the manuscript. This research was sup- 
ported by NSF grant DEB-8103184 to William 
Burger 


LITERATURE CITED 


T R. E. 1939. Revision die Arten einiger zm 
onaceen Gattungen. V. M Ruiz & Pav 
rore Hort. Berg. 12(3): 2 
oo T س‎ n & Schery 
Flora a. n. Missouri Bot Gard. 49: 
PR d 2. 184-188.) 


— Kerry Barringer, Department of Botany, Field 
Museum, Chicago, Illinois 60602-2496. 


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Contents continued from front cover 


The Phytog Signifi of Some Extinct Gondwana Pollen Types 
from the Tertiary of the Sive Cape (South Africa) J. A. 
Coetzee & J. Muller 

Maize Introgression into Teosinte— A Reappraisal John Е. Doebley ...... 

Reconsideration of Oenothera Subg. Gauropsis (Onagraceae) Warren L. 
Wagner 

Systematics of Osmorhiza Raf. (Apiaceae: Apioideae) Porter P. Lowry II 
& Almut G. Jones 

A Guide to Collecting Passionflowers P. M. Jorgensen, J. E. Lawesson 
& L. B. Holm-Nielsen 

New Rubiaceae from Venezuela Julian A. Steyermark 

Notes on Neotropical Lauraceae Henk van der Werff 

NOTES 

Alectra aspera (Cham. & Schlecht.) L. O. Williams Rachel Hampshire & 
David Sutton 

Circaea alpina L. (Onagraceae) in Thailand David E. Boufford u... 

A New Species of Guatteria (Annonaceae) from Panama Kerry Barringer