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Full text of "Malacologia"

HARVARD UNIVERSITY 




LIBRARY 

OF THE 

DEPARTMENT OF MOLLUSKS 

IN THE 

Museum of Comparative Zoology 
Gift of: 



VOL.40, NO. 1-2 1998 



MALACOLOGIA 



International Journal of Malacology 
Revista Internacional de Malacologia 
Journal International de Malacologie 
Международный Журнал Малакологии 
Internationale Malakologische Zeitschrift 



Publication dates 

Vol.30, No. 1-2 1 Aug. 1989 

Vol.31. No. 1 29 Dec. 1989 

Vol. 31. No. 2 28 May 1990 

Vol.32. No. 1 30 Nov. 1990 

Vol. 32. No. 2 7 Jun. 1991 

Vol.33, No. 1-2 6 Sep. 1991 

Vol.34. No. 1-2 9 Sep. 1992 

Vol. 35, No, 1 14 Jul. 1993 

Vol.35. No. 2 2 Dec. 1993 

Vol. 36, No. 1-2 8 Jan. 1995 

Vol.37, No. 1 13 Nov. 1995 

Vol. 37. No. 2 8 Mar. 1996 

Vol. 38. No. 1-2 17 Dec. 1996 

Vol. 39, No. 1-2 13 May 1998 



VOL. 40, NO. 1-2 MALACOLOGIA 1998 

CONTENTS 

J.A.ALLEN 

The Deep-Water Species of Dacrydium ToreW, 1859 (Dacrydiinae: Mytilidae: 
Bivalvia), of the Atlantic 1 

RÜDIGER BIELER, ALEXANDER D. BALL, & PAULA M. MIKKELSEN 

Marine Valvatoidea - Comments on Anatomy and Systematics with Descrip- 
tions of a New Species from Florida (Heterobranchia: Cornirostridae) .... 305 

GEORGE M. DAVIS, THOMAS WILKE, CHRISTINA SPOLSKY, CHI-PING QIU, 

DONG-CHUAN QIU, MING-YI XIA, Yl ZHANG, & GARY ROSENBERG 

Cytochrome Oxidase l-Based Phylogenetic Relationships Among the Po- 
matiopsidae, Hydrobiidae, Rissoidae and Truncatellidae (Gastropoda: Cae- 
nogastropoda: Rissoacea) 251 

A. J. DE WINTER & E. GITTENBERGER 

The Land Snail Fauna of a Square Kilometer Patch of Rainforest in South- 
western Cameroon: High Species Richness, Low Abundance and Seasonal 
Fluctuations 231 

RICHARD G. GUSTAFSON, RUTH D. TURNER, RICHARD A. LUTZ, & 

ROBERTC. VRIJENHOEK 

A New Genus and Five New Species of Mussels (Bivalvia, Mytilidae) from 
Deep-Sea Sulfide/Hydrocarbon Seeps in the Gulf of Mexico 63 

MARY ELLEN HARTE 

Is Cyclininae a Monophyletic Subfamily of Veneridae (Bivalvia)? 297 

WALTER R. HOEH, MICHAEL B. BLACK, R. GUSTAFSON, ARTHUR E. BOGAN, 

RICHARD A. LUTZ, & ROBERTC. VRIJENHOEK 

Testing Altenative Hypotheses of Neotrigonia (Bivalvia: Trigonioida) 
Phylogenetic Relationships Using Cytochrome С Oxidase Subunit I DNA 
Sequences 267 

RACHEL E. MERKT & AARON M. ELLISON 

Geographic and Hapitat-Specific Morphological Variation of Littoraria (Lit- 
torinopsis) angulifera (Lamarck, 1 822) 279 

JAY A. SCHNEIDER 

Phylogeny of Stem-Group Eucardiids (Bivalvia: Cardiidae) and the Signifi- 
cance of the Transitional Fossil Perucardia 37 

JAY A. SCHNEIDER 

Phylogeny of the Cardiidae (Bivalvia): Phylogenetic Relationships and Mor- 
phological Evolution within the Subfamilies Clinocardiinae, Lymnocardiinae, 
Fraginae and Tridacninae 321 

MARÍA VILLARROEL & JOSÉ STUARDO 

Protobranchia (Mollusca: Bivalvia) Chilenos Recientes Y Algunos Fósiles . . 113 



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Address: Malacologia 

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AWARDS FOR STUDY AT 
The Academy of Natural Sciences of Pfiiladelphiia 

The Academy of Natural Sciences of Philadelphia, through its Jessup and 
McHenry funds, makes available each year a limited number of awards to support 
students pursuing natural history studies at the Academy. These awards are primar- 
ily intended to assist predoctoral and immediate postdoctoral students. Awards usu- 
ally include a stipend to help defray living expenses, and support for travel to and 
from the Academy. Application deadlines are 1 March and 1 October each year. 
Further information may be obtained by writing to: Chairman, Jessup-f\/lcHenry 
Award Committee, Academy of Natural Sciences of Philadelphia, 1900 Benjamin 
Franklin Parkway, Philadelphia, Pennsylvania 19103-1195, U.S.A. 



VOL 40, NO. 1-2 1998 



MALACOLOGIA 



International Journal of Malacology 
Revista Internacional de Malacologia 
Journal International de Malacologie 
Международный Журнал Малакологии 
Internationale Malakologische Zeitschrift 



MALACOLOGIA 

EDITOR-IN-CHIEF: 
GEORGE M. DAVIS 

Editorial and Subscription Offices: 

Department of Malacology 

The Academy of Natural Sciences of Philadelphia 

1900 Benjamin Franklin Parkway 

Philadelphia, Pennsylvania 19103-1195, U.S.A. 



EUGENE COAN 

California Academy of Sciences 

San Francisco, CA 



Co-Editors: 



Assistant Managing Editor: 

CARYL HESTERMAN 

Associate Editor: 

JOHN B. BURCH 

University of Michigan 

Ann Arbor 



CAROL JONES 
Denver, CO 



MALACOLOGIA is published by the INSTITUTE OF MALACOLOGY, the Sponsor Members of 
which (also serving as editors) are: 



RÜDIGER BIELER 

President 

Field Museum, Chicago 

JOHN BURCH 

MELBOURNE R. CARRIKER 
University of Delaware, Lewes 

GEORGE M. DAVIS 
Secretary and Treasurer 

CAROLE S. HICKMAN 

President Elect 

University of California, Berkeley 



ERIC HOCHBERG 

Santa Barbara Museum of Natural History 

California 

ALAN KOHN 

University of Washington, Seattle 

JAMES NYBAKKEN 

Vice President 

Moss Landing Marine Laboratory, California 

CLYDE F E. ROPER 

Smithsonian Institution, Washington, D.C. 

SHI-KUEI WU 

University of Colorado Museum, Boulder 



Participating Members 



EDMUND GITTENBERGER 

Secretary, UNITAS MALACOLOGICA 

Rijksmuseum van Natuurlijke 

Historie 

Leiden, Netherlands 



JACKIE L. VAN GOETHEM 
Treasurer, UNITAS MALACOLOGICA 
Koninklijk Belgisch Instituut 
voor Natuurwetenschappen 
Brüssel, Belgium 



Emeritus Members 



J. FRANCIS ALLEN, Emérita 
Environmental Protection Agency 
Washington, D.C. 

KENNETH J. BOSS 

Museum of Comparative Zoology 

Cambridge, Massachusetts 



ROBERT ROBERTSON 

The Academy of Natural Sciences 

Philadelphia, Pennsylvania 

W. D. RUSSELL-HUNTER 
Easton, Maryland 



Copyright © 1998 by the Institute of Malacology 
ISSN: 0076-2997 



1998 
EDITORIAL BOARD 



J.A.ALLEN 

Marine Biological Station 

Millport, United Kingdom 

E. E. BINDER 

Museum d'Histoire Naturelle 

Geneve, Switzerland 

A.J.CAIN 

University of Liverpool 
United Kingdom 

P. CALOW 

University of Sheffield 
United Kingdom 

J. G. CARTER 

University of North Carolina 

Chapel Hill. U.S.A. 

R. COWIE 
Bishop Museum 
Honolulu, HI.. U.S.A. 

A. H.CLARKE, Jr. 
Portland. Texas, U.S.A. 

B. С CLARKE 
University of Nottingham 
United Kingdom 

R. DILLON 

College of Charleston 

SC. U.S.A. 

C.J. DUNCAN 
University of Liverpool 
United Kingdom 

D.J. EERNISSE 
California State University 
Fullerton, U.S.A. 

E. GITTENBERGER 
Rijksmuseum van Natuurlijke Historie 
Leiden, Netherlands 

F. GIUSTI 

Universita di Siena. Italy 

A. N. GOLIKOV 
Zoological Institute 
St. Petersburg, Russia 



S.J.GOULD 
Harvard University 
Cambridge, Mass.. U.S.A. 

A. V. GROSSU 
Universitatea Виси rest i 
Romania 

T. HABE 

Tokai University 

Shimizu, Japan 

R. HANLON 

Mahne Biological Laboratory 

Woods Hole, Mass., U.S.A. 

J. A. HENDRICKSON, Jr. 
Academy of Natural Sciences 
Philadelphia, PA, U.S.A. 

D. M. HILLIS 
University of Texas 
Austin, U.S.A. 

K. E. HOAGLAND 

Association of Systematics Collections 
Washington, DC, U.S.A. 

B. HUBENDICK 

Naturhistoriska Museet 
Göteborg. Sweden 

S. HUNT 
Lancashire 
United Kingdom 

R.JANSSEN 

Forschungsinstitut Senckenberg. 
Frankfurt am Main, Germany 

R. N. KILBURN 
Natal Museum 
Pietermahtzburg. South Africa 

M.A. KLAPPENBACH 

Museo Nacional de Histoha Natural 

Montevideo. Uruguay 

J. KNUDSEN 

Zoologisk Institut Museum 

Kobenhavn. Denmark 

A. LUCAS 

Faculte des Sciences 

Brest, France 



с. MEIER-BROOK 

Tropenmedizinisches Institut 
Tubingen, Germany 

H. К. MIENIS 

Hebrew University of Jerusalem 

Israel 

J. E. MORTON 
The University 
Auckland. New Zealand 

J. J. MURRAY. Jr. 
University of Virginia 
Charlottesville. U.S.A. 

R. NATARAJAN 
Marine Biological Station 
Porto Novo, India 



S. G. SEGERSTRALE 

Institute of Mahne Research 
Helsinki. Finland 

A. STAÑCZYKOWSKA 
Siedlce. Poland 

F. STARMÜHLNER 

Zoologisches Institut der Universität 

Wien. Austha 

Y. I. STAROBOGATOV 
Zoological Institute 
St. Petersburg, Russia 

W. STREIFF 
Universite de Caen 
France 



DIARMAIDOFOIGHIL 
University of Michigan 
Ann Arbor, U.S.A. 



J. STUARDO 
Universidad de Chile 
Valparaiso 



J. 0KLAND 
University of Oslo 
Norway 

T. OKUTANI 
University of Fisheries 
Tokyo, Japan 

W. L. PARAENSE 

Instituto Oswalde Cruz, Rio de Janeiro 

Brazil 

J. J. PARODIZ 
Carnegie Museum 
Pittsburgh, U.S.A. 

J. P. POINTIER 

Ecole Pratique des Hautes Etudes 

Perpignan Cedex. France 

W. F. PONDER 
Australian Museum 
Sydney 

Ol Z. Y 

Academia Sínica 

Qingdao, People 's Republic of China 

D. G. reíd 

The Natural History Museum 

London, United Kingdom 



S. TILLIER 

Museum National d'Histoire Naturelle 

París. France 

R. D.TURNER 
Harvard University 
Cambridge. Mass., U.S.A. 

J.A.M. VAN DEN BIGGELAAR 
University of Utrecht 
The Netheríands 

N. H. VERDONK 
Rijksuniversiteit 
Utrecht, Netherlands 

ANDERS WAREN 

Swedish Museum of Natural History 

Stockholm, Sweden 

В. R. WILSON 

Dept. Conservation and Land Management 

Kallaroo. Western Australia 

H. ZEISSLER 
Leipzig. Germany 

A. ZILCH 

Forschungsinstitut Senckenberg 

Frankfurt am Main. Germany 



N. W. RUNHAM 

University College of North Wales 

Bangor, United Kingdom 



MALACOLOGIA, 1998, 40(1-2): 1-36 

THE DEEP-WATER SPECIES OF DACRYDIUM TORELL, 1859 
(DACRYDIINAE: MYTILIDAE: BIVALVIA), OF THE ATLANTIC 

J.A.Allen 
University Marine Biological Station, Millport. Isle of Cumbrae, Scotland, KA28 OEG^ 

ABSTRACT 

Species of the genus Dacrydium ate ubiquitous, mostly at bathyal and abyssal depths within 
the world's oceans. Here, 11 species are described from the Atlantic at depths greater than 
500 m, and of these six are described for the first time. In addition, a bibliography of the world's 
species described to date is appended. The Dacrydiinae are neotenous mytilids, many being as- 
sociated with sponges to which they are byssaliy attached. Multiple fine byssal threads are pro- 
duced, which may form a nest. The shells are small, rarely more than 4 mm total length, fragile, 
and transluscent, white or pale cream in colour. Ornamentation, when present, consists of fine 
concentric striae, sometimes with very fine radial lines and occasionally a scattering of tiny shell 
granules. The hinge is narrow, with fine, multiple, nepioconch teeth retained throughout life. The 
ligament is small, internal, and amphidetic. Ventral to the posterior hinge plate is a shell buttress 
parallel to the dorsal shell margin, which probably provides necessary strength to an extremely 
fragile shell at times subject to adduction. The viscera occupy the dorsal-most third of the man- 
tle cavity, the organs within being arranged parallel to the dorsal shell margin. Sexes are sepa- 
rate. The palps and gills are reduced in size. The outer demibranch, if present, develops late in 
life at the time the gonads are begining to mature. At most, it occupies a third of the gill axis and 
acts as a repository for sperm or eggs when they are first released. At the same time, the fused 
inner folds of the posterior mantle edge, ventral to the point of the attachment of the gill axis, en- 
large and form an aperture that is probably related to the release of sperm or eggs, or spat in the 
case of those species that brood. 

Key words: Dacrydium. Mytilidae, Bivalvia, deep-sea, Atlantic. 



INTRODUCTION 

Of the mytilids present in the deep sea 
(>500 m), the vast majority belong to the 
genus Dacrydium Torell, 1859. The first 
species to be described was Dacrydium vit- 
reum (Möller, 1842) from off West Greenland 
and which is now known to occur in relatively 
shallow water at shelf and upper slope depths 
in northern seas (Appendix 2). Although a 
shallow-water species, D. hyalinum, was de- 
scribed by Monterosato (1870, 1875, 1878) 
from the Recent of Sicily and another, D. oc- 
cidentale, by Smith (1885) from the Carib- 
bean, and six varieties of D. vitreumwere rec- 
ognized by Locard (1898), until 1959 all 
records from the North Atlantic were referred 
to D. vitreum. Then, Ockelmann (1959), rec- 
ognizing differences in shell shape and shell 
characters in specimens from northern seas, 
tentatively identified three species that he re- 
ferred to as species a, b, and с one of which 
(b) he was later to describe as D. viviparum 



(Ockelmann, 1983). In the years between 
Ockelmann's two papers, others also recog- 
nized that species other than D. vitreum oc- 
curred in the North Atlantic (Soot-Ryen, 1966; 
Allen, 1979). One of these, D. ockelmanni. 
was described by Mattson & Waren (1977). 

Elsewhere, species of Dacrydium had been 
described from Australasian waters (Medley, 
1904, 1906), from the Southern Ocean (Pel- 
seneer, 1903: Theile, 1912), and the Pacific 
(Dall, 1916). 

With the upsurge of deep-sea exploration in 
the last 25 years, a number of new species 
have been described from the world oceans 
(Okutani, 1975; Bernard, 1978; Knudsen, 
1970; Routiers, 1989; Okutani & Izumidate, 
1992; Hayami & Kase, 1993; Salas & Gofas, 
1 997), bringing the total, prior to this paper, to 
28 known species in the world oceans. This 
total includes five species that have not yet 
been given specific names and may yet prove 
to be synonymous with other species. A list of 
all the above species and a bibliography to 



^Address for correspondence. Also: Woods Hole Océanographie Institution, Massachusetts, 02543, USA. 

1 



ALLEN 



them is given in Appendix 2. Unknown until 
shortly before publication, Salas & Gofas 
(1997) and the present author had been work- 
ing simultaneously on Atlantic species of the 
genus. This paper takes account of their work. 
Apart from D. ockelmanni (Mattson & 
Waren, 1977), D. angulare and, to a lesser 
degree D. viviparum (Ockelmann, 1983), and 
a note on their nephridia by Odhner (1912), 
the species of Dacrydium are known from 
their shell features alone. Here are added de- 
tails of their internal morphology. 



MATERIAL AND METHODS 

The species described here were present in 
the deep-sea samples taken by the research 
vessels of the Natural Environment Research 
Council, U.K.; of the Woods Hole Océan- 
ographie Institution, U.S.A.; and of the Centre 
National pour l'Exploration des Oceans, 
France. These ships and the names of the 
various expeditions are included in the list of 
material in Appendix 1 . For the most part, the 
specimens were collected with a Sanders 
epibenthic sledge (ES) or some variant of it 
(Oban - OS; Wormley - WS), and a few were 
collected by other means, namely. Anchor 
Dredges (AD, DP), Beam Trawls (CR CLG), 
Agassiz Trawl (CV), Reineck Box Corer (KR), 
large Boillet Trawls (GBO, GBS), small Boillet 
Trawl (PBS). 

The samples were elutriated on board, 
using sieves (mesh 0.42 mm USA and UK; 
0.25 mm and 0.50 mm France), fixed in 4% or 
1 0% formal saline and then after 24 h, washed 
and transferred to 70% or 95% ethanol. In- 
ternal morphology was studied using whole 
mounts stained lightly in Ehrlich's haema- 
toxylin and sections cut at 10 \.im and stained 
with Meyer's haemotoxylin and eosin and with 
Azan. 



DESCRIPTIONS 

Family Mytilidae Rafinesque, 1815 
Subfamily Dacrydiinae Ockelmann, 1983 

Adult shell eqivalve, markedly inequilateral, 
small, rarely more than 4 mm total length, ho- 
mologous to nepioconch of other mytilids; 
sculpture of fine concentric lines, marked in 
some species; fine radial lines present in 
some species; colour white or, occasionally, 
cream, frequently hyaline; umbo far anterior 
and somewhat dorsal to anterior limit of shell; 



highest part of shell varying in position from 
anterior to posterior to the mid-vertical axis; 
hinge may have derivatives of provincular 
teeth adjacent to primary ligament, a dorsal 
series of fine, transverse nepioconch teeth 
persist, the posterior series usually much 
more numerous than anterior; "subligamental 
ridge" (Ockelmann, 1983), or dorsal buttress 
shelf, ventral to and more or less parallel to 
posterior hinge plate; antero-ventral ridge, in- 





Abbreviations Used in Figures 


AA 


anterior adductor 


AF 


axial muscle fibres 


AL 


ascending lamella 


AN 


anus 


AP 


anterior (upper) palp 


AR 


anterior pedal retractor 


ВС 


basiphyliic gland cells 


BG 


byssal groove 


CG 


cerebral ganglion 


DD 


digestive duct 


DG 


digestive diverticula 


DL 


descending lamella 


EC 


eosinophyllic gland cells 


FM 


posterior fused inner mantle fold 


FT 


foot 


HG 


hindgut 


GA 


gill axis 


GF 


gill filament 


GS 


gastric shield 


GV 


ventral margin of inner demibranch 


HB 


hinge buttress 


ID 


inner demibranch 


Li 


ligament 


LP 


lip 


MI 


mantle isthmus 


MT 


mouth 


OD 


outer demibranch 


OB 


oesophagus 


CR 


rudiment of outer demibranch 


OV 


ovary 


PA 


posterior adductor muscle 


PG 


pedal ganglion 


PM 


longitudinal palliai muscle 


PP 


posterior (lower) palp 


PR 


posterior pedal retractor muscle 


RA 


reproductive aperture 


SB 


suprabranchial cavity 


SP 


sperm 


ST 


stomach 


TE 


testis 


UC 


umbonal cavity 


VE 


ventricle 


VG 


visceral ganglion 



SPECIES OF DACRYDIUM 



ternal to anterior hinge plate, variously devel- 
oped; primary ligament small, internal and 
amphidetic; if present, secondary ligament 
very small, slender, opisthodetic. Viscera oc- 
cupying dorsal third of shell space, digestive 
glands and gonads elongate, following line of 
dorsal margin; mantle margins simple, un- 
fused, except where gill axis attaches to man- 
tle margin; adductor muscles sometimes 
subequal in size, but usually heteromyarian, 
with the posterior muscle the larger; labial 
palps minute, few, if any, palp hdges; inner 
demibranch of gill extending length of mantle 
cavity, but with relatively few filibranch fila- 
ments; when present, outer demibranch de- 
veloping late in life as a small posterior trian- 
gular flap; foot relatively small, with functional 
byssus, producing many fine threads. 

Genus Dacrydium ToreW, 1859 
Type species by monotypy, Modiola? vitrea 
Moller, 1842;92. 

Description as for subfamily. Occurs from 
shelf to abyssal depths, most species being 
found from mid-slope to lower slope depths. 

The genus Quendreda was proposed by 
Iredale (1936:271) but without diagnosis. He 



Abbreviations of Museums 



AHF 


Allan Hancock Foundation (see 




LACMNH) 


AMS 


Australian Museum, Sydney 


BMNH 


Natural History Museum, London 


IRSNB 


Institut Royal des Sciences 




Naturelles, Belgique 


LACMNH 


Los Angeles County Museum of 




Natural History 


^У1NHNP 


Muséum National d'Histoire 




Naturelle, Paris 


NMNZ 


National Museum of New Zealand 


NSMT 


National Science Museum, Tokyo 


SBMNH 


Santa Barbara Museum of Natural 




History 


SMNH 


Naturhistoriska Riksmuseet, 




Stockholm 


TRFRL 


Tokai Regional Fisheries Research 




Laboratory 


UMUT 


University Museum, University of 




Tokyo 


USNM 


United States National Museum 


ZMHU 


Zoologisches Museum Humbolt- 




Universitat, Berlin 


ZMUB 


Zoological Museum, University of 




Bergen 


ZMUC 


Zoological Museum, University of 




Copenhagen 



designated D. fabale Hedley, 1904, as the 
type species, remarking that it "differs in 
shape, form and sculpture from the Spitz- 
bergen shell, the type of Torell's genus." 
There is debate as to whether this distinction 
is justified (Soot-Ryen, 1955; Bernard, 1978; 
Ockelmann, 1983). 

Dacrydium sandersi, new species 

Figs. 1-3 

Type Locality: Atlantis II, Sta. 66, North 

Amenca Basin, 38°46.7'N 70°08.8'W, 

2802 m. 
Type Material: Holotype, BMNH 1996136; 

paratypes, BMNH 1996137. 
Material: North America Basin: Atlantis II, 
sta. 62, 69 spec; sta. 64, 175 spec; sta. 66, 
12 spec; sta. 72, 132 spec; sta. 118, 5 spec; 




FIG. 1 . Dacrydium sandersi. Lateral views from the 
left side of two specimens from Atlantis II sta. 72. 
North America Basin, 2864 m. Scale = 1 mm. 




FIG. 2. Dacrydium sandersi. Lateral internal view of 
right valve from Biogas III sta. DS41 , Bay of Biscay 
3548 m. Scale = 1 mm. 



ALLEN 




[ \ 

FIG 3 Dacrydium sandersi. Semidiagrammatic view of the internal morphology of a specimen from the left 
side from Atlantis II sta. 72, North America Basin. 2864 m. Scale = 0.5 mm. Refer to Materials & Methods for 
list of abbreviations. 



Sta. 119, 32 spec; Chain, sta. 76, 133 spec. 
Brazil Basin: Atlantis II, sta. 1 55, 90 spec: sta. 
156, 396 spec: sta. 167. 39 spec: sta. 169, 
1 7 spec. West European Basin: Biogas II, sta. 
DS31. 10 spec; Biogas III, sta. DS41. 61 
spec: Biogas IV. sta. DS58, 6 spec; sta. 
DS59. 2 spec; Biogas VI, sta. 74, 17 spec: 
sta. CV38, 7 spec. Azores Mid Atlantic 
Ridge: Biacores, sta. 126, 19 spec. 

Distribution: Occurs nnost commonly at 
lower slope depths (2500-3000 m), although 
the overall range is much wider (587-3783 
m). It occurs across the Atlantic predomi- 
nantly at boreal latitudes in the North America 
and West European basins, although in the 
West Atlantic it has been taken from the 
northern part of the Brazil Basin. 

Shell Description (Figs. 1, 2). Shell small 
(<4 mm), fragile, modioliform, greatest shell 
height postehor to mid-vertical axis, relatively 
wide, transluscent white, occasional growth 
lines and faint concentric striations, otherwise 
smooth; umbones large, distant from antero- 
ventral limit of shell margin; ventral margin 
convex in small specimens, with slight sinu- 
osity anteriorly in larger specimens; posterior 



margin broadly curved; dorsal margin very 
slightly concave, slightly angled where poste- 
rior limit of hinge meets margin; anterior mar- 
gin relatively long and straight, except close to 
umbo where it curves inwards; hinge plate in- 
terrupted by ligament pit; antehor hinge plate 
moderately elongate, with 13-15 nepioconch 
teeth; posterior hinge plate approximately the 
same length as anterior but broader, with 
10-12 nepioconch teeth; narrow buttress 
shelf extending from anterior limit of posterior 
hinge plate along the dorsal margin to the 
highest point of the shell; a narrower buttress 
shelf extending from posterior limit of the an- 
terior hinge plate along the antehor margin to 
a point where the margin starts to curve to the 
ventral margin; ligament small, internal, am- 
phidetic, separating anterior and postehor 
hinge plates. Prodissoconch length: 123 цт. 
Internal Morphology (Fig. 3). The mantle 
margin has outer, middle sensory and inner 
muscular folds. Posteriorly, there is fusion of 
the latter to form an extensive exhalent aper- 
ture. The area of fusion is relatively broad and 
is much more prominant in large than small 
specimens. The gill axes attach to the dorsal 



SPECIES OF DACRYDIUM 



edge of the fused tissue. In large specimens, 
thie area of fusion might be mistaken for an in- 
turned and contracted inhalent siphon (Fig. 
3), but in the present specimens neither whole 
mounts nor sections reveal a clear lumen 
from the exterior to the mantle cavity, although 
sections show that there is an inner cavity. It 
will be seen that in fully mature specimens of 
other species a lumen does connect the man- 
tle cavity to the exterior, and it would appear 
that the aperture when formed is used for the 
discharge of eggs and sperm. Neither Matt- 
son & Waren (1977) nor Ockelmann (1983) 
mention this, despite its presence in the 
species that they describe. 

The adductor muscles are small and equal 
in size. The gills consist of only the inner 
demibranchs. No rudiment of an outer demi- 
branch is present, even in specimens with 
maturing ova. The inner demibranchs com- 
prise of a relatively broad descending lamella 
and an ascending lamella about half the 
length of the descending. The filaments are 
typically filibranch without interlamellar and in- 
terfilamentar junctions. The main axes are at- 
tached dorsally to the body wall and to the 
mantle posterior to the foot. 

The palps are very small, slight enlarge- 
ments to the lateral limits of the lips. The 
mouth opens to an oesophagus that has a 
lumen with six longitudinal grooves. The 
course of the oesophagus is straight, opening 
to the anterior part of the stomach. The latter 
is also elongate and tubular, lying along the 
antero-postehor axis. There is an extensive 
gastric shield that extends over much of the 
dorsal and left lateral walls of the stomach. 
The ciliation on the remaining wall appears to 
be relatively simple; however, there is a major 
typhlosole that extends the length of the com- 
bined style sac and mid gut. The hind gut 
turns immediately dorsal to the style sac, first 
taking an anterior course as far as the mid 
point of the stomach, and then turns sharply 
on itself and continues directly and mid-dor- 
sally over the posterior adductor muscle to the 
anus. There is a very short digestive duct 
opening from what appears to be a simple 
caecum on the left side of the stomach. The 
duct connects with a digestive diverticulum 
that forms a longidinal tube on the left ventral 
side of the viscera. There is also a second 
duct opening anteriorly on the right side of the 
stomach. This branches, one branch connect- 
ing with a longitudinal diverticulum on the right 
side that parallels the one on the left, the other 
branch connecting with a smaller diverticulum 



ventral to the stomach. The right and left di- 
verticula are finger-like and extend one each 
side of the oesophagus and terminate a short 
distance anterior to the mouth. 

Dorsal to the paired diverticula are a pair of 
tubular gonads dorso-lateral to the digestive 
system. Sexes are separate; 30-35 ova (68 
|im diameter) were present in a specimen 
2 mm in length. 

The kidneys are a pair of simple sacs pos- 
terior to the posterior adductor. The nervous 
system is of the typical bivalve design; how- 
ever, all the ganglia are small in size. 

Diagnosis: D. sandersi is characterized by 
the greatest shell height being posterior to the 
mid-vertical axis, the posterior hinge being 
short and of similar length to the anterior, the 
umbo being relatively distant from the antero- 
ventral point of the shell, and the adductor 
muscles being small and dimyarian. 

Other species of similar shell shape are D. 
rostriferum. D. occidentale and Dacrydium sp. 
of Poitiers (1989), but these differ from the 
present species in that the posterior hinge is 
significantly longer than the anterior. The posi- 
tion of the umbo in D. occidentale and Da- 
crydium sp. is much closer to the antero-ven- 
tral limit of the shell (see Poitiers, 1989: fig. 3) 

Dacrydium vit re и m (Mo Her, 1842) 
Figs. 4-7 
Type Locality: West Greenland. 
Type Material; originally ZMUC; appears to be 

lost (Waren, 1991). 
Original description: Moller, 1842; 92 (for 

other references, see Appendix 2). 
Cited specimen (figured in text): BMNH 

1996144 
Material: North America Basin: Atlantis, sta. 
D, 3 spec: Chain, sta. 88, 34 spec; sta. 105, 
43 spec; Knorr, sta. 346, 3 spec. 

Also, specimens from off East Greenland 
identified and donated by Kurt Ockelmann to 
Howard Sanders of the Woods Hole Océano- 
graphie Institution, have been examined. 

Distribution: In the past, D. vitrea m has been 
recorded widely from the North Atlantic south 
to the Azores and Florida (Ockelmann, 1959; 
Abbott, 1 974), but it is now clear that southern 
specimens have been misidentified. It is a 
cold-water, panarctic species (Ockelmann, 
1959; Mattson & Waren, 1977; Waren, 1991) 
and possibly circumglobal (Bernard, 1983; 
Salas & Gofas, 1997). Although the present 
specimens come from the shelf edge off Cape 
Cod at a boreal latitude, these relate to the 
southward extension of the Labrador Current, 



ALLEN 




FIG. 4. Dacrydium vitreum. Three views of a shell from Knorr sta. 346, North America Basin. 475 m. (a) lat- 
eral from left side; (b) dorsal; (c) anterior. Scale = 1 mm. 





FIG. 5. Dacrydium vitreum. Lateral internal view of 
right valve from Atlantis 227 sta. D, 466-508 m. 
Scale = 1 mm. 



FIG. 6. Dacrydium vitreum. Lateral internal view of 
right valve of a specimen from off East Greenland 
(Ockelmann, 1953: 175). Scale = 1 mm. 



SPECIES OF DACRYDIUM 

HGPG VE 



VG 




FIG. 7. Dacrydium vitreum. Semidiagrammatic view of the internal morphology of a specimen from the left 
side from Chain 58 sta. 105, North Amehca Basin, 530 m. Scale = 1 mm. Refer to Matehals & Methods for 
list of abbreviations and Fig. 3 for identification of other parts. 



other species of Arctic bivalves are found at 
the same stations (Allen et al., 1995). Depth 
range: 5-698 m, deeper records down to 2258 
m need to be confirmed (Ockelmann, 1959). 

Shell Description (Figs. 4-6). Sars (1878) 
gave good descriptions and figures of the shell 
(Mattson & Waren, 1 977), and since then other 
good figures and photographs have been pro- 
vided by Ockelmann (1959, 1983), Mattson & 
Waren (1977), Waren (1991), and Salas & 
Gofas (1 997). For completeness and for com- 
parative purposes, shells from the North 
America Basin and from East Greenland are 
figured and described and, for the first time, 
the internal anatomy is described. 

Shell small (<6 mm total length), semi-trans- 
parent or opaque, white, periostracum cream 
in larger specimens, semi-ovate, equivalve; 
shell relatively high, maximum height mea- 
surement immediately posterior to mid-vertical 
axis; umbo prominant, dorsal, slightly poste- 
rior to the anterior limit of the shell; ventral 
margin a shallow convex curve; posterior mar- 
gin smoothly rounded; postero-dorsal margin 
broadly convex; antero-dorsal margin a shal- 



low convex curve indented at juxtaposition of 
umbo and internal ligament; postehor hinge 
plate elongate, occupying 1/3 postehor dorsal 
margin, present specimens with 55-65 nepio- 
conch teeth (number increasing with size); 
posterior hinge plate strengthened by broad 
buttress shelf thickened along ventral edge 
("subligamental hdge" of Ockelmann, 1983); 
shelf extending just posterior to summit of dor- 
sal shell margin, thereafter merging with palliai 
line of shell; anterior hinge plate short, with 5-8 
nepioconch teeth; antero-ventral corner of 
shell somewhat thickened where antehor ad- 
ductor muscle inserts; insertion of postehor 
adductor close to postero-dorsal palliai line 
posterior to buttress shelf; ligament internal, 
amphidetic, with very short fine external ex- 
tensions not usually visible unless shell is dis- 
solved. Prodissoconch length; 120-136 |im 
(Ockelmann, 1983; Salas & Gofas, 1997). 

Internal Morphology (Fig. 7). The morphol- 
ogy is similar to that described for D. sandersi. 
The mantle margins are relatively unmodified, 
with three simple folds that are unfused, ex- 
cept postehorly where the gill axes meet the 



8 



ALLEN 



margin and where the inner muscular folds 
are fused and thicl<ened over a short dis- 
tance. No papillae are present on the middle 
sensory lobe, and there is no extension of 
sensory and inner folds to form siphons. Very 
fine scattered radial palliai muscle fibres are 
present as a band internal to the inner mus- 
cular fold. The adductor muscles are relatively 
well developed, the anterior being of a similar 
size to the posterior, except that it is crescent- 
shaped in cross section as opposed to oval. 
The gill axes are attached latero-ventrally to 
the body and to the mantle posterior to the 
body. The inner demibranch, with approxi- 
mately 25 filaments in a specimen 3 mm total 
length, is well developed, with the descending 
and ascending lamellae of similar size. The 
outer demibranch is restricted to a small, pos- 
terior, triangular structure close to where the 
axis meets the mantle margin, and it has up to 
nine short filaments. The anterior filament of 
the inner demibranch is situated somewhat 
distant from the minute palps, there being a 
long distal oral groove between gill and 
mouth. 

The viscera are confined to a narrow band 
in the dorsal third of the shell cavity. This re- 
striction is reminiscent of the condition in the 
deep-sea limopsids, in which the viscera oc- 
cupy less than a third of the available mantle 
space (Oliver & Allen, 1980). Thus, in D. vit- 
reum. the oesophagus, stomach, style sac 
and intestine are arranged in a longitudinal 
fashion within the body. The oesophagus is 
relatively elongate, joining the stomach anteri- 
orly, the midgut is combined with the style sac; 
the hind gut is first reflected anteriorly, along 
the dorsal 2/3rds of the length of the stomach, 
and then posteriorly, passing through the heart 
and dorsal to the posterior adductor, to the 
anus. The major portion of the digestive diver- 
ticula comprise a pair of parallel tubules, one 
each side of the stomach and oesophagus. In 
addition, there are a few short tubules ventral 
to the stomach. The gonads are paired elon- 
gate tubes lying dorsal to the oesophagus and 
stomach. The sexes are separate. The kidney 
lies ventral to the hindgut, anterior to the pos- 
tehor adductor. The foot joins the viscera pos- 
terior to the style sac. In preserved specimens, 
it is small and cylindrical enclosed by the gill 
lamellae. There is a functional byssus gland at 
the postero-ventral limit of the foot, and clearly 
in life the latter must be capable of consider- 
able extension. Two paired posterior pedal re- 
tractor muscles insert immediately anterior to 
the posterior adductor, and a pair of fine ante- 



rior pedal retractors attach to the shell imme- 
diately dorsal to the umbones. 

Dacrydium ockelmanni 

Mattson & Waren, 1977 

Figs. 8-15 

Type Locality: Korsfjorden, W. Norway, 

60^08. 58'N 05°00.67'W, 260-290 m. 
Type Material: Holotype ZMUB 58 633; 

paratypes ZMUB 58 634. 
Ohginal Description: Mattsen & Waren, 1977: 

2, figs. 4-6, 10-13 (for other references, 

see Appendix 2). 
Cited Specimens: BMNH 1996138 and 

1996139. 
Material: North America Basin: Atlantis II, 
sta. 73, 90 spec; sta. 115, 50 spec; sta. 119, 
24spec.;sta. 128, 37 spec; Chain, sta. 87, 16 
spec; sta. 103, 1 spec; sta. 210, 77 spec. 
Brazil Basin: Atlantis II, sta. 142, 89 spec; sta. 
144, 2 spec; sta. 147, 9 spec. Argentine 
Basin: Atlantis II. sta. 239, 9 spec; sta. 240, 2 
spec; sta. 245, 21 spec. West European 
Basin: Sarsia, sta. S33/2, 1 spec; sta. S44, 
1 9 spec; sta. S50, 52 spec: sta. S66; 1 spec; 
Discovery, sta. 7601 , 1 spec; Challenger, sta. 
E80-73, 24 spec; Biogas I, sta. DS11, 1 
spec; Polygas, sta. DS15, 9 spec; sta. DS17, 
2 spec; DS18, 5 spec; sta. DS25, 1 spec; 
sta. DS31, 4 spec; Biogas II, sta. DS32, 3 
spec; Biogas III, sta. DS36, 1 spec; sta. 
DS37, 3 spec; sta. DS38, 1 spec; sta. DS50, 
7 spec; Thalassa, sta. Z397, 5 spec; sta. 
Z400, 13 spec; sta. Z413, 2 spec; sta. Z417, 
4 spec; sta. Z427, 1 spec; sta. Z447, 1 spec; 
Biogas IV, sta. DS52, 13 spec; sta. DS61, 4 
spec; sta CP01, 2 spec; sta. DS62, 8 spec; 
sta. DS63, 6 spec; sta. DS64, 14 spec; 
Biogas VI, sta. CP08, 3 spec; sta. CP09, 7 
spec; sta. DS71, 3 spec; sta. DS86, 36 
spec; sta. CP23, 1 spec; sta. DS87, 30 
spec; Incal, sta. DS01, 12 spec; sta. CP01, 
41 spec; sta. DS02, 31 spec; sta. CP08, 1 
spec; Chain, sta. 313, 7 spec; sta. 318, 1 
spec; sta. 321, 24 spec. Canary Basin: 
Discovery, sta. 6701, 13 spec; sta. 6704, 5 
spec. Azores Mid Atlantic Ridge: Biacores, 
sta. 105, 2 spec; sta. 120, 1 spec. 

Distribution: Ockelmann (1958), Mattson & 
Waren (1977) and Waren (1991) reported D. 
ockelmanni as occurring WSW and SE of 
Iceland, SW of the Faroes, NW of Ireland and 
probably Bay of Biscay. The species is con- 
firmed as common in the Bay of Biscay and, 
further, as being present throughout most of 
the Atlantic with the possible exception of the 
Angola and Cape basins. It is also reported as 



SPECIES OF DACRYDIUM 




FIG. 8. Dacrydium ockelmanni. Lateral views of six 
shells from the left side to show variation in shell 
outline with increasing size. Specimens taken from 
Atlantis II sta. 73, North America Basin, 1330-1470 
m. Scale = 0.5 mm. 





FIG. 10. Dacrydium ockelmanni. Detail of the hinge 
of a right valve from Atlantis I! sta. 240, Argentine 
Basin, 2195-2323 m. Scale = 0.5 mm. 




FIG. 9. Dacrydium ockelmanni. Dorsal view of shell 
from Atlantis II sta. 73, North America Basin, 
1330-1470 m. Scale = 0.5 mm. 



FIG. 11. Dacrydium ockelmanni. Lateral internal 
views of five right valves to show variation in form, 
(a) Discovery sta. 6704, Canary Basin, 2129 m; (b) 
Sarsia sta. S44, Bay of Biscay, 1739 m; (c) Atlantis 
II sta. 142, Brazil Basin, 1624-1796 m: (d) Atlantis 
II sta. 239, Argentine Basin, 1661-1669 m; (e) 
Atlantis lista. 73, North Amenca Basin, 1330-1470 
m. Scale = 1 mm. 



10 



ALLEN 





FIG. 12. Dacrydium ockelmanni. Semidiagram- 
matic view of the internal morphology of a male 
specimen from Atlantis II sta. 73, North America 
Basin, 1330-1470 m. Scale = 1 mm. See Fig. 3 for 
identification of the parts. 




FIG. 13. Dacrydium ockelmanni. Semidiagram- 
matic view of the internal morphology of a female 
specimen from Atlantis II sta. 73, North Amehca 
Basin, 1330-1470 m. Scale = 1 mm. See Fig. 3 for 
identification of the parts. 



a Pleistocene fossil from the Mediterranean 
(Salas & Gofas, 1 997). It occurs at lower shelf 
to lower slope depths with an extreme range 
of 1 00-31 00 m, but most of the above records 
are from mid to lower slope depths (1000- 
2500 m). 

Shell Description (Figs. 8-11). The shell is 
described and figured by Mattson & Waren 
(1977), Waren (1991), and Salas & Gofas 
(1 997). Here further detail is added. 

Shell small (<6.0 mm), semi-transparent, 
white or tinged with yellow/green, semi-ovate, 
greatest height coincident with mid-vertical 
axis or, in largest specimens, posterior to it: 
umbo moderate in size; ventral shell margin 
slightly concave in smallest specimens, as 
length increases ventral margin first becomes 



FIG. 14. Dacrydium ockelmanni. Semidiagram- 
matic view of the internal morphology of an imma- 
ture specimen from Atlantis II sta. 142, Brazil Basin, 
1624-1796 m. Scale = 0.5 mm. See Fig. 3 for the 
identification of the parts. 




FIG. 15. Dacrydium ockelmanni. Transverse verti- 
cal 10 цт sections through a specimen from 
Atlantis II sta. 73, North America Basin, 1330-1470 
m. (a) through region of mouth; (b) through oe- 
sophagus; (c) through stomach and gastric shield. 
Scale = 0.5 mm. Refer to Materials & Methods for 
list of abbreviations. 



SPECIES OF DACRYDIUM 



11 



straight and then slightly convex; posterior and 
dorsal margins forming smooth, broad, con- 
vex curve; antero-dorsal margin dorsal to 
umbo almost straight, ventral to umbo slightly 
sinuate, then straight for short distance before 
curving sharply to meet ventral margin; poste- 
rior hinge plate occupying <1/4 dorsal shell 
margin, with 33-38 nepioconch teeth in pres- 
ent specimens (larger numbers are present in 
larger specimens, e.g. Salas & Gofas, 1997: 
fig. 8), supported by relatively wide buttress 
shelf that extends beyond hinge for a similar 
distance but short of the highest point of the 
shell; in intact specimens, ventral edge of but- 
tress usually visible through shell; posterior 
limit of hinge plate frequently marked by slight 
angulation of shell margin; anterior hinge plate 
short with 5-7 nepioconch teeth, very small 
provincular tooth at proximal limit of anterior 
hinge plate; antero-ventral part of shell slightly 
thickened, with inner ventral ridge originating 
at anterior limit of anterior hinge plate; liga- 
ment internal, amphidetic, seated in pit be- 
tween hinge plates. Prodissoconch length: 
1 41 -1 50 um (Ockelmann, 1 983). 

Dacrydium ос/<е/тапл/ (height/length 0.72- 
0.77) differs from D. vltreum (height/length 
0.63-0.71 ) in being slightly more elongate and 
less high, with the ventral margin concave in 
larger specimens. The posterior hinge plate is 
shorter in D. ockelmanni with fewer nepio- 
conch teeth, and the buttress shelf is some- 
what less wide. The antero-dorsal margin is 
straighter and the umbo smaller and less dis- 
tant from the antero-ventral limit of shell. 

Ockelmann (1 959) reported on a number of 
possible species, including one later de- 
scribed as D. ockelmanni, within a relatively 
small area of the North Atlantic off Iceland. The 
species described here, including D. ockel- 
manni, have fairly wide distributions. Because 
it is known that shell shape and internal mor- 
phology changes with increasing size, internal 
shell characters from specimens from different 
basins have been figured (Fig. 11), as well as 
differences in shell outline with increasing size 
from a large sample (Fig. 8). This confirms the 
variation, with that seen in a single sample 
being as great as the interbasinal differences. 
The variation is not consistant enough to war- 
rent naming subspecies or varieties. 

Internal Morphology (Figs. 12-1 5). Although 
their figures are diagrammatic, the morphol- 
ogy of D. ockelmanni is well described by 
Mattson & Waren (1977). Immature and ma- 
ture whole mounts are illustrated here, and 
additional information given. Thus, the anterior 



adductor muscle is more round in cross-sec- 
tion and smaller than the posterior adductor. 
The gill filaments on the inner demibranch are 
more widely spaced compared with those of 
the outer demibranch, and specimens 1 .6 mm 
in length have only a rudiment of the outer 
demibranch (Fig. 14). Ventral to the attach- 
ment of the gill axis with the mantle margin, the 
inner muscular mantle fold is fused and thick- 
ened over some distance and extended in- 
wards to form an internal "collar." This struc- 
ture is much more developed in larger 
specimens, particularly so in specimens that 
have mature gonads. The posterior pedal re- 
tractor muscles are not particularly well devel- 
oped. The presence of a longitudinal palliai 
muscle is confirmed, and is perhaps better de- 
veloped than the diagrammatic drawing of 
Mattson & Waren (1 977) might indicate. Sexes 
are separate, and large female specimens 
from Station 73 were mature, with approxi- 
mately 400 eggs (75 цт diameter) in speci- 
mens >4 mm total length (Figs. 13, 14). 

Dacrydium abyssorum, new species 

Figs. 16-19 

Type Locality: Knorr 25, Station 287, Guyana 

Basin, 13"16.0'N 54^'52.2'W 13°15.8'N 

54 '53.1 'W, 4980-4934 m . 
Type Material: Holotype BMNH 1996140; 

paratype BMNH 1996141. 
Material: Newfoundland Basin: Chain, sta. 
331 , 2 spec; North America Basin: Atlantis II, 
sta. 70, 3 spec; sta. 93, 1 spec; Chain, sta. 
80, 1 spec; sta. 83, 2 spec; sta. 84, 5 spec; 
sta. 84, 8 spec. Guyana Basin: Knorr, sta. 287, 
27 spec; sta. 288, 14 spec; sta. 306, 2 spec; 
Vema, sta. CP02, 2 spec; sta. DS05, 2 spec. 
West European Basin: Biacores, sta. 245, 
11 spec; Polygas, sta. DS20, 89 spec; 
sta. DS21, 26 spec; sta. CV13, 17 spec; sta. 
DS22, 59 spec; sta. DS23, 21 spec; sta. 
DS26, 9 spec; Biogas II, sta. DS30, 12 spec; 
Biogas III, sta. DS42, 1 spec; sta. DS44, 4 
spec; sta. DS45, 8 spec; sta. DS46, 3 spec; 
sta. DS48, 2 spec; Biogas IV, sta. 54, 4 spec; 
sta. DS55, 264 spec; sta. KR31 , 1 spec; sta. 
DS56, 15 spec; sta. KR35, 2 spec; Biogas V, 
sta. DS67, 23 spec; sta. DS68, 10 spec; sta. 
DS69, 4 spec; sta. CP07, 1 spec; Biogas VI, 
sta. DS75, 1 spec; sta. DS76, 579 spec; sta. 
CP13, 32 spec; sta. CP14, 53 spec; sta. 
KR60, 5 spec; sta. KR64, 2 spec; sta. DS77. 
148 spec; sta. DS78, 21 spec; sta. CP16, 13 
spec; sta. DS79, 9spec.;sta. CP17, 17 spec; 
sta. CP18, 1 spec; sta. DS80, 2 spec; sta. 
DS81 , 1 spec; sta. CP21 , 2 spec; sta. DS87, 



12 



ALLEN 





FIG. 16. Dacrydium abyssorum. Lateral views of 
three shells from the right side, (a & c) Chain 50 
sta. 85, North America Basin, 3834 m; (b) Knorr sta. 
287, Guyana Basin, 4980-4934 m. Scale = 0.5 mm. 



FIG. 18. Dacrydium abyssorum. Semidiagrammatic 
view from the left side of the internal morphology of 
a mature female from Knorr sta. 287, Guyana 
Basin, 4980-4934 m. Scale = 0.5 mm. See Fig. 3 
for the identification of the parts. 




FIG. 17. Dacrydium abyssorum. Lateral internal 
view of right valve of a specimen from Knorr sta. 
288, Guyana Basin, 441 7-4429 m, and the detail of 
the hinge of two right valves from Chain 50 sta. 85, 
North America Basin, 3834 m. Scale = 0.5 mm. 



13 spec; Incal, sta. CP10, 6 spec; sta. DS11, 
5 spec; sta. CPU, 30 spec; sta. WS02, 
64 spec; sta. OS03, 19 spec; sta. OS05, 26 
spec; sta. KR14, 3 spec; sta. WS07, 388 
spec; sta. DS14, 73 spec; sta. DS15, 
42 spec; sta. DS16, 123 spec; sta. WS08, 



274 spec; sta. OS06, 63 spec; sta. OS07, 
515 spec; sta. WS09, 111 spec; sta. WS10, 
280 spec; sta. OS08, 145 spec. Sierra Leone 
Basin:AtlantisN,sta. 148, 1 spec; sta. 149, 13 
spec. Cape Basin: Walvis, sta. DS02, 2 spec; 
sta. KG14, 1 spec; sta. DS05, 39 spec; sta. 
DS06, 43 spec; sta. DS07, 2 spec. 

Distribution: Dacrydium abyssorum is wide- 
spread at abyssal depths throughout the 
Atlantic. It occurs at depths from 1913-5280 
m, but predominantly at depths >4000 m. 

Shell Description (Figs. 1 6, 1 7). Shell small, 
modioliform, fragile, transluscent, white, 
greatest height posterior to mid-vertical trans- 
verse axis; umbo relatively large, distant from 
the antero-ventral limit of shell; antero-ventral 
margin broadly rounded; ventral margin sinu- 
ous; posterior margin a smooth, broad curve; 
postero-dorsal margin a smooth convex 
curve; antero-dorsal margin much less con- 
vex, angulate at posterior limit of hinge plate; 
antero-dorsal margin almost straight; antehor 
margin dipping slightly where umbo meets 
margin; anterior and posterior hinge plates 
continuous, although edentulous section 
below umbo narrow; anterior hinge-plate 
short, but relatively broad, with 5-9 nepio- 
conch teeth; posterior hinge-plate elongate, 
broadening distally, with approximately 42 ne- 
pioconch teeth in specimen 4.5 mm total 
length; buttress shelf broad, except ventral to 
the anterior half of the posterior hinge plate, 
where it narrows, usually making a sinuous 
curve with the broader posterior part; internal 
ridge from anterior limit of hinge plate curving 
postero-ventrally, forming margin of antero- 



SPECIES OF DACRYDIUM 



13 




FIG. 19. Dacryc//um abyssorum. Transverse vertical 
10 цт sections through a mature male specimen 
from Knorr sta. 287, Guyana Basin, 4980-4934 m, 
(a) through the mouth; (b) through the stomach. 
Scale = 0.5 mm. Refer to Materials & Methods for 
list of abbreviations. 



ventral triangular area to which antehor ad- 
ductor muscle attaches; ligament small, inter- 
nal, amphidetic. Prodissoconch length: 191- 
204 цт. 

Internal Morphology (Figs. 18, 19). The in- 
ternal morphology is similar to that of D. 
sandersi. The adductor muscles are small, 
the anterior slightly larger in size. The gill is 
without an outer demibranch, and the inner 
demibranch comprises both ascending and 
descending lamellae. There are relatively few 
filaments, 17 and 27 in the demibranchs of 
specimens 1.8 mm and 3.0 mm total length, 
respectively. There are no interfilamentar con- 
nectives and no interlamellar connectives. 
The posterior mantle margin is thickened at 
the point where the gill axes attach to it and 



also ventral and dorsal to the point of attach- 
ment. Fusion of the inner mantle folds occurs 
at the point where the gill axes meet the man- 
tle margin and ventral to this. In mature spec- 
imens, through this is a channel from mantle 
cavity to the exterior, homologous to an in- 
halent aperture, which is probably used for 
the passage of sexual products. Inhalent repi- 
ratory and feeding currents pass through the 
extensive pedal gape. Internally, the margin of 
this reproductive aperture is characteristically 
curved, forming a funnel. Anteriorly, the lips 
and mouth also form a wide buccal funnel; 
this is directed postero-ventrally and so 
placed to receive material traveling the length 
of the gill margin. The palps are reduced to 
slight thickenings at the extremities of the lips, 
and it would appear that little or no sorting of 
incoming material can occur. The oesopha- 
gus is wide and the stomach relatively volu- 
minous. The digestive diverticula are more 
branched than in D. sandersi. but similar in 
their distribution. The pedal musculature is 
relatively stout compared with that of D. 
sandersi. Mature specimens were present in 
the samples, 10 and 24 large eggs (115 |im 
max. dimension) were present in specimens 
1 .8 mm and 3.0 mm total length, respectively. 
Diagnosis: Dacrydium abyssorum is a 
species in which the maximum shell height is 
posterior to the vertical mid-line and thus is 
similar to D. sandersi. It differs from the latter 
in the more pronounced angulation of the 
shell margin opposite the postehor limit of the 
hinge, the more sinusoidally curved ventral 
margin of the shell, and in the difference in 
length of the hinge plates and the numbers of 
nepioconch teeth. 

Dacrydium waren/ Salas & Gofas, 1997 

Figs. 20-25 

Type Locality: Off northwestern Morocco, 

35' ЗГМ 07°42'W, 1510 m. 
Type Material: Holotype and paratypes 

MNHNP;paratypesSMNH. 
Description: Salas & Gofas 1997: 271, figs. 
94-96, 97-99 (for other references, see 
Appendix 2). Cited specimen: BMNH 
1996146. 
Material: North America Basin: Atlantis II, 
sta. 73, 2 spec; sta. 118, 1 spec. West 
European Basin: Sarsia, sta. S61, 1 spec; 
sta. S63, 4 spec; Thalassa, sta. Z400, 1 
spec; sta. 435, 2 spec; Biogas IV, sta. DS51 , 
1 spec. Canary Basin: Discovery, sta. 6696, 1 
spec 
Disthbution: This species occurs at mid- 



14 



ALLEN 




FIG. 20. Dacrydium viviparum. Lateral view from 
the left side of the shell of the paratype BMNH 
1983035. Scale = 1 mm. 




FIG. 21. Dacrydium wareni. Lateral view from the 
left side of two shells from (a) Sarsia sta. S63, Bay 
of Biscay, 1336 m and (b) from Atlantis II sta. 73, 
North America Basin, 1330-1470 m. Scale = 1.0 
mm. 



slope depths in the temperate North Atlantic 
and western Mediterranean (depth range: 
952-2340 m). Maximum length of present 
specimens, 4.4 mm. 

Shell Description (Figs. 20-23). Salas & 
Gofas (1997) give a description D. wareni, 
which is extended here. The present speci- 
mens were recognized as belonging to a new 
species before the description by the latter 
authors was published. The present speci- 
mens correspond in every respect with their 
excellent description. Salas & Gofas (1997) 
do not describe the internal morphology. 

Shell small, transluscent white, semi-ovate. 




FIG. 22. Dacrydium wareni. Lateral internal views of 
right valves from (a) Sarsia sta. S63, Bay of Biscay, 
1336 m; (b) Thalassa sta. Z400, West European 
Basin, 1175 m and (c) Atlantis II sta. 118, North 
America Basin, 1135-1153 m. Scale = 1 mm. 




FIG. 23. Dacrydium. Comparative detail of the 
hinges of four left valves, (a) Dacrydium viviparum. 
Paratype, BMNH 1983035, Ingolf sta. 78, Reyk- 
janes Ridge, 1505 m; (b) Dacrydium wareni. Tha- 
lassa sta. Z400, West European Basin, 1175 m, (c) 
Sarsia sta. S63, Bay of Biscay, 1336 m and (d) 
Atlantis II sta. 1 1 8, North America Basin, 1 1 35-1 1 53 
m. Scale = 0.5 mm. 



greatest height dimension usually anterior to 
mid vertical axis, but may be coincident or 
slightly posterior to axis in larger specimens; 
umbo small, distant from the antero-ventral 
limit of shell; maybe one or two faint radial 
lines from umbo to mid-dorsal and postero- 
dorsal margin respectively, faint incremental 
lines present; anterior shell margin ventral to 
umbo a shallow, convex curve dorsal to umbo 
almost straight, steeply inclined, meeting 
broadly convex dorsal margin in slight break 



SPECIES OF DACRYDIUM 



15 




FIG. 24. Dacrydium wareni. Semidiagrammatic 
view from the left side of tine internal morphology of 
a male specimen from Atlantis II sta. 73, North 
America Basin, 1 330-1 470 m. Scale = 0.5 mm. See 
Fig. 3 for the identification of parts. 




FIG. 25. Dacrydium wareni. Detail of (a) the distri- 
bution of gland cells at junction of the filaments of 
the inner demibranch with the gill axis; (b) ventral 
margin of two filaments of the outer demibranch 
and (c) of the inner demibranch. Scale = 50 цт. 
Refer to Materials & Methods for list of abbrevia- 
tions. 



opposite dorsal limit of hinge plate; dorsal and 
posterior margins forming a smooth curve; 
ventral margin almost straight or very slightly 
concave; hinge with short anterior plate with 
up to 8 teeth; posterior plate in tv/o parts, that 



close to umbo is of similar length to anterior 
plate and with up to 8 teeth, narrow, edentu- 
lous posterior to this section, followed by elon- 
gate section with 16-34 nepioconch teeth 
(dependent on specimen size) similar to the 
posterior hinge plates of other species; rela- 
tively broad buttress extending from umbo to 
a point opposite highest point of shell; small 
ridge extending for short distance ventral to 
anterior hinge plate; internal ligament am- 
phidetic, ventral to umbo; secondary external 
ligament, opisthodetic, slender, consisting of 
fused periostracum. Prodlssoconch length: 
121-130 |.im. 

Internal Morphology (Figs. 24, 25). The in- 
ternal morphology is similar to that of D. ock- 
elmanni. The adductor muscles are relatively 
small and similar in size. The anterior muscle 
is crescent-shaped in cross section, and the 
posterior adductor is oval. The gills have an 
inner demibranch comprising of descending 
and ascending lamellae and a short posterior 
outer demibranch comprising of a descending 
lamella. The size of the latter varies according 
to the length of the animal. In a specimen 2.4 
mm total length, there are 16 closely arrayed 
filaments forming the outer demibranch. In the 
same specimen, there are 25 filaments in the 
inner demibranch, but these are much more 
widely separated than those of the outer 
demibranch. The latter occupies less than a 
fifth of the total gill area. The reflected as- 
cending filament of the inner demibranch is 
approximately half the length of the descend- 
ing. As in other species, at the tips of the fila- 
ments of the outer demibranch and at the 
point of reflection (ventral edge) of the inner 
demibranch, there are a pair of horn-like 
processes oriented along the horizontal axis 
and which bridge the interfilamentar gap. In 
addition, dorsally the gills are well supplied 
with gland cells (Fig. 25). These comprise 
8-1 small eosinophilic cells on the outer pos- 
terior face of the filament close to where it 
joins the axis, and numerous large squamous 
basiphyllic cells lining the arch of axial tissue 
joining the filaments ventral to the axial mus- 
cle. The mouth is a particularly broad, shallow 
cone without palps on the lower lip and tiny 
palp rudiments on the upper lips, with traces 
of two or possibly three ridges. The viscera 
are similar to those of the previous species. 

No mature specimens or specimens brood- 
ing eggs were present in the available sam- 
ples. 

Not mentioned by Salas & Gofas (1997) is 
the similarity in shell and hinge form to D. vi- 



16 



ALLEN 




FIG. 26. Dacrydium angulare. Lateral view of a shell from the right side, an internal view of a left valve and 
detail of the hinge of a right valve Uom Atlantis II sta. 202, Angola Basin, 1427-1643 m. Scale = 0.5 mm. 



viparum (Ockelmann, 1983) (Figs. 20-23). 
This might be within the range of variation to 
be expected within a species of Dacrydium, 
but, because of the great difference in size of 
the prodissoconch of specimens of D. vivipa- 
rum described by Ockelmann (1983) (252- 
292 цт) and the lack of evidence of viviparity 
in the present specimens, the case for syn- 
onymy is doubtful. The Ockelmann material 
was taken from latitude 60'N-64N', in com- 
parison with 32'N-48°N for the present spec- 
imens, and it seems unlikely that there could 
be so much variation in egg size and devel- 
opment between northern and southern pop- 
ulations. Nevertheless, the prodissoconch 
length of D. и/алел/ reported by Sales & Gofas 
(1997) is larger (approx. 170 цт) than that of 
the present specimens. This is the only differ- 
ence in our respective descriptions. 

Dacrydium angulare Ockelmann, 1 983 

Figs. 26-28 

Type Locality: Vema Sta. 54, Cape Basin, 

34°35'S 17°31'E, 1849 m. 
Type Material: Holotype and paratypes 

ZMUC: paratypes USNM 822398. 
Original Description: Ockelmann 1983: 114, 

figs. 46-48, 51 (for other references, see 

Appendix 2). 
Cited specimen: BMNH 1996147. 




FIG. 27. Dacrydium angulare. Lateral view of shell 
from the right side and detail of the hinge of a left 
valve from J. Charcot Walda sta. DS13, Angola 
Basin. 3985 m. Scale a = 1 mm: scale b = 0.5 mm. 



Material: Angola Basin: Walda, sta. DS13, 
1 spec: Atlantis II, sta. 202, 7 spec. 

Distribution: This species occurs at lower 
slope to abyssal depths in the Cape Verde, 
Angola and Cape basins. Depth range 
1427-3985 m. 

Shell Description (Figs. 26, 27). Shell small 
(<4.0 mm), fragile, semi-transluscent, moder- 
ately elongate, greatest height coinciding with 



SPECIES OF DACRYDIUM 



17 




FIG. 28. Dacrydium angulare. Semidiagrammatic views from the left side of the internal morphology of a ma- 
ture male and an immature specimen from J. Charcot Walda sta. DS13, Angola Basin. Scale = 1 mm. Refer 
to Materials & Methods for list of abbreviations and to Fig. 3 for identification of other parts. 



the mid-vertical axis, extremely fine close 
concentric sculpture with faint growth lines; 
umbo moderately small, some distance from 
the antero-ventral limit of shell; ventral margin 
slightly sinuous in large specimens, otherwise 
broadly convex, joining posterior margin in 
smooth, deep curve; dorsal margin broadly 
convex, somewhat angulate at limit of poste- 
rior hinge plate; antero-dorsal margin slightly 
convex, high-angled in relation to ventral mar- 
gin; anterior margin indented ventral to umbo 
particularly in large specimens, then slightly 
convex dorsal to antero-ventral margin; ante- 
rior hinge plate, narrow, short, with 3-7 indis- 
tinct nepioconch teeth, narrow edentulous 
subumbonal section joining relatively short 
posterior hinge plate, 20-28 nepiconch teeth; 
posterior buttress relatively broad, extending 
beyond dorsal limit of hinge plate to a point 
approximately twice the length of the posterior 
hinge plate; antero-ventral ridge short, ex- 
tending to posterior limit of anterior adductor 
scar, less sharply deliniated than posterior 
buttress; ligament small, internal, amphidetic. 
Prodissoconch length; 159-165 цт (Ockel- 
mann, 1983), 165-170 цт (Salas & Gofas, 
1997), present specimens 170 цт. 
The present specimens differ slightly from 



the excellent description given by Ockelmann 
(1983). The sinuous ventral shell margin of 
larger specimens is somewhat more pro- 
nounced than those described by Ockelmann 
(1983), but similar to those of Salas & Gofas 
(1997). The present specimens also have a 
more marked indentation ventral to the umbo 
and have a less extended antehor hinge plate 
with fewer teeth (see Ockelmann 1983; fig. 
47). Such slight variation can be expected in 
specimens of differing size and from different 
basins. 

Internal Morphology (Fig. 28). The internal 
morphology was described in detail by 
Ockelmann (1983), but, except for the oral 
field, not figured. Minor additions are given 
here. The adductor muscles are moderate 
and equal in size. Both inner and outer demi- 
branchs are present in the largest specimens, 
and the filaments are relatively short. The first 
rudiments of the outer demibranch appear in 
specimens of approximately 2.0 mm length. 
The palps, although minute, are larger than 
other species examined. Ockelmann (1983) 
notes that "posterior fusion of the inner man- 
tle folds large and muscular" and that "gills at- 
tach slightly below its upper border." He then 
further notes that the "inner mantle lobes sur- 



11 



ALLEN 



rounding the inhalent and pedal opening" are 
well developed. He clearly believes that the 
pedal and and inhalent openings are com- 
bined, although he has noted the thickened 
muscular development ventral to the gill at- 
tachment. It has been possible, in the present 
samples, to demonstrate that the posterior 
inner mantle fold enlarges as the outer demi- 
branch develops and the gonads mature. One 
mature male was found with sperm packed in 
the space enclosed by the outer demibranch 
(Fig. 28), and this specimen showed the 
greatest development of the posterior inner 
mantle fold and a channel to the exterior. 
Dacrydium hedleyi, new species 
Figs. 29-31 
Type Locality: Knorr Cruise 25 sta. 287, 
13°16.0'N 54°52.2'W-13°16.8'N 54" 
53. rW, 4980-4934 m. 
Type Material: Holotype BMNH 1996143. 

Material: Guyana Basin: Knorr, sta. 287, 2 
spec; sta. 288, 9 spec; sta. 291, 23 spec; 
Biovema, sta. DS11, 2 spec. 

Distribution: This species appears to be re- 
stricted to abyssal depths in the Guyana 
Basin. Depth range: 3859-5867 m. 

Shell description (Figs. 29, 30). Shell small, 
fragile, modioloid, transluscent when fresh, 
turning opaque white on death or preserva- 
tion, growth lines faint, without other orna- 
mentation, greatest height anterior to mid-ver- 
tical axis; umbo relatively large, distant from 
the antero-ventral shell margin; ventral mar- 
gin concave in smallest specimens, with slight 
antero-ventral sinuosity in larger specimens, 
joining posterior and postero-dorsal margins 
in a broad curve; postero-dorsal margin 
slightly angulate at posterior limit of hinge 
plate; anterior margin almost straight, angled 
to meet ventral margin in acute curve; antero- 
ventral margin less acute in larger specimens; 
hinge plates extremely narrow, barely wider 
than shell thickness; both anterior and poste- 
rior plates with 10-15 extremely fine nepio- 
conch teeth; posterior and anterior buttresses 
faint, barely extending beyond the limits of the 
hinge plate; ligament small, internal, am- 
phidetic, more or less globular, supported by 
two very small nymphs ventral to umbo. 
Prodissoconch length: 167 ¡am. 

Internal Morphology (Fig. 31). The internal 
morphology differs little from any of the de- 
scribed species above. The adductor muscles 
are relatively small. The posterior inner man- 
tle folds are fused in the manner described 
above. The gills comprise the descending 
lamella of the inner demibranchs. These com- 




FIG. 29. Dacrydium hedleyi. Lateral views of three 
shells from left side from Knorr sta. 291, Guyana 
Basin, 3859-3868 m to show changes in shell out- 
line with increasing size. Scale = 0.5 mm. 

prise 12-13 widely spaced gill filaments, the 
distal half of which are typically angled anteri- 
orly. No outer demibranchs were developed in 
any of the specimens in the collection. 

It is likely that the specimens are all juve- 
niles. No maturing sperm or ova were seen. 

The species is named after Dr. Charles 
Hedley who described Australiasian species 
of Dacrydium. 

Diagnosis: This species is characterized by 
the slender hinge plates and that the greatest 
height measurement is anterior to the mid ver- 
tical shell axis. In shape, D. bed/ey/ resembles 
that of D. nipponicum (Okutani, 1 975), but the 
ventral margin is less concave. The latter 
species also has stouter hinge plates and 
shell buttresses, and the adductor scars are 
much larger. 

Dacrydium albidum Pelseneer, 1 903 

Figs. 32-34 

Type Locality: S. Y. Bélgica, Sta. 1046, 

71"18'S88°02'W, 400 m. 
Type Material: IRSNB. 
Cited Specimen: BMNH 1996145. 

Matenal: Weddell Sea: IWSOE, sta. 001, 
12 spec; sta. 002, 3 spec; sta. 004, 1 spec; 
sta. 005, 1 spec; sta. 007, 3 spec; sta. 008, 
2 spec; sta. 010, 2 spec. 

Distribution:Circum-Antarctic, occurring at 
outer shelf to mid-slope depths in the Ross, 
Davis and Weddall seas and off the South 
Shetland Islands (depth range: 122-1437 m). 

Shell Description (Figs. 32, 33). The origi- 
nal description (Pelseneer 1903), although 
short, is accurate. The description was later 
extended by Nicol (1966). 



SPECIES OF DACRYDIUM 
HB 



19 




I 1 

FIG. 30. Dacrydium hedleyi. Internal view of a left valve and internal view of an intact hinge and ligarnent of 
specimens from Knorr sta. 291 , Guyana Basin, 3859-3868 m. Scale = 0.5 mm. Refer to Materials & Methods 
for list of abbreviations. 




FIG. 31. Dacrydium hedleyi. Semidiagrammatic 
view of the internal morphology as seen through the 
transparent shell of a specimen from Knorr sta. 291 , 
Guyana Basin, 3859-3868 m. Scale = 0.5 mm. See 
Fig. 3 for identification of parts. 




FIG. 32. Dacrydium albidum. Lateral views of three 
shells from the International Weddell Sea Océano- 
graphie Expedition sta. 002, 412 m, to show differ- 
ences in outline with increasing growth. Scale = 
0.5 mm. 



Shell small (<5 mm), fragile, greatest height 
varies from slightly anterior to mid-vertical 
axis to slightly posterior, opaque white or hya- 
line, with faint growth lines, periostracum very 
pale brown: umbo moderately large, relatively 
distant from antero-ventral limit of shell; ven- 
tral margin almost straight, in large specimens 



sometimes very slightly sinuous; posterior 
margin broadly rounded, joining postero-dor- 
sal margin in a smooth curve; anterior margin 
ventral to umbo relatively elongate, convex, 
slightly incurved at umbo; antero-ventral mar- 
gin smoothly rounded; anterior hinge plate 
short, slightly expanded internally, with 7-8 



20 



ALLEN 




^/\ 



FIG. 33. Dacrydium albidum. Detail of hinge of right 
valve of a specimen from the International Weddell 
Sea Océanographie Expedition sta. 001, 728 m. 
Scale = 0.5 mm. 




FIG. 34. Dacrydium albidum. Semidiagrammatic 
view from the left side of the internal morphology of 
a specimen from the International Weddell Sea 
Océanographie Expedition sta. 004, 793 m. Scale = 
0.5 mm. See Fig. 3 for identification of the parts. 



nepioconch teeth; short edentulous section 
dorsal to ligament connecting with long poste- 
rior plate, terminating just short of the highest 
point of shell, with 50-55 nepioconch teeth; 
broad posterior buttress extending from liga- 
ment and slightly angled to hinge plate, termi- 
nating opposite highest point of shell; short, 
curved antero-ventral buttress terminating 
dorsal to anterior adductor muscle; ligament 
internal, ventral to umbo, amphidetic, elon- 
gate-oval. Prodissoconch length: 213 |.im. 

Nicol (1966) orientated the shell such that 
his dorsal margin equates with the anterior 
margin as described here and by others. He 
also overlooked the anterior nepioconch 
teeth. 

Internal Morphology (Fig. 34). The internal 
morphology differs little from those described 
above. The adductor muscles are larger than 



in most other species. In addition, the outer 
palps, although still much reduced, are larger 
than in other species and have two well-de- 
fined ridges. The gills comprise of the inner 
demibranch, with descending and ascending 
lamellae and a rudiment of outer demibranch 
with a few unreflected filaments at the poste- 
rior end of the gill axis. In a specimen of 2.5 
mm total length, the outer demibranch com- 
phses two very short unreflected filaments. 

Dell (1 990) figure a specimen from the R. V. 
Eltanin collections from the Ross Sea which, 
although identical in other respects, has the 
highest point of the shell slightly postehor to 
the mid-vertical axis, and he refered to shell 
variation, though without definition, when he 
stated that "valves varying to such a degree" 
that he, like Nicol (1966), could not separate 
D. albidum from D. modioliforme Theile 
(1912). Poitiers (1989) also remarked on the 
confusion and refers to a bathyal complex of 
forms involving D. albidum and D. modio- 
liforme. 

The original deschption of D. modioliforme 
(Theile, 1912) does differ little from the de- 
scription of D. albidum. and the type speci- 
men came from a depth (385 m) within the 
range of the latter species. Specimens identi- 
fied as D. modioliforme from abyssal depths 
(e.g., Theile & Jaeckel, 1 931 ) do differ from D. 
albidum (Knudsen, 1970) (see below). 

Dacrydium knudseni, new species 
Figs. 35-37 
Type Locality; International Weddell Sea 
Océanographie Expedition sta. 023, 
72''47.6'S 30-^29. 7'W, 3697 m. 
Type Material: Holotype BMNH 1996142. 

MatehaLWeddell Sea: IWSOE, sta. 022, 3 
spec; sta. 023, 6 spec; sta. 027, 10 spec 

Distribution: This species is disthbuted at 
abyssal depths in the Weddell Sea. Depth 
range: 3111-4636 m. 

Shell Description (Figs. 35, 36). Shell small, 
fragile, relatively short, maximum height more 
or less coincident with mid-vertical axis, 
opaque white, with fine concentric growth 
lines; umbo moderately large, distant from an- 
tero-ventral limit of shell; ventral margin a 
shallow convex curve in small specimens, 
straight and sometimes faintly concave in 
larger specimens; postero-ventral and poste- 
rior margins forming a smooth, broad curve; 
postero-dorsal margin slightly flattened in 
most specimens; anterior margin slightly in- 
dented ventral to umbo, forming a relatively 
long convex curve, making a characteristic 



SPECIES OF DACRYDIUM 



21 




FIG. 35. Dacrydium knudseni. Lateral views of 
three shells from the International Weddell Sea 
Océanographie Expedition sta. (a) 022, 3111 m; (b 
& c) 023, 3697 m, to show variation in outline. Scale 
= 1 mm. 




FIG. 36. Dacrydium knudseni. Lateral view of a 
shell from the left side and detail of the hinge of a 
right valve. Specimens taken by the International 
Weddell Sea Océanographie Expedition sta. 023, 
3697 m. Scale = 0.5 mm. 

acutely rounded antero-ventral shell margin; 
anterior and posterior hinge plates narrow, 
each with 15-17 nepioconch teeth, moder- 
ately long, narrow edentulous section ventral 
to umbo joining the toothed parts; posterior 
hinge plate short; posterior buttress moder- 
ately narrow, extending from anterior limit of 
posterior hinge plate to a short distance pos- 
terior to the postehor plate buttress, continu- 
ing ventral to umbo and accommodating the 
resilifer; ligament ventral to umbo, am- 
phidetic, oval. Prodissoconch length; 195 |.im. 
Internal morphology (Fig. 37). The internal 
morphology is similar to that of D. albidum. 
Differences include smaller adductor mus- 
cles, gills that comprise only the descending 




FIG. 37. Dacrydium knudseni. Semidiagrammatic 
view of the internal morphology of a specimen from 
the International Weddell Sea Océanographie 
Expedition sta. 027, 4575 m. Scale = 0.5 mm. See 
Fig. 3 for the identification of parts. 



lamellae of the inner demibranchs and no 
outer demibranchs. The dorsal lip is charac- 
teristically elongate and with a minute palp 
rudiment. 

Dacrydium knudseni is named after Dr. 
Jörgen Knudsen, distinguished deep-sea 
malacologist who first recognized that there 
was a clear difference between the deep- 
water Antarctic specimen collected by the R. 
V. Valdivia and the more shallow water 
species D. albidum. 

Diagnosis; Dacrydium knudseni is charac- 
terized by an acutely angled antero-ventral 
shell margin and approximately equal num- 
bers of nepioconch teeth on the anterior and 
posterior hinge plates. It most closely resem- 
bles D. panamensis Knudsen, 1970, the latter 
differing in having a more foreshortened an- 
tero-ventral shell margin, a shorter anterior 
hinge plate with fewer teeth, a shorter eden- 
tulous section, and a more extensive inner 
buttress. 

Dacrydium s p. a 
Figs. 38, 39 
Specimen; MNHNP 

Material; Cape Basin; Walvis, sta. DS05, 2 
spec. 

Distribution; These are juveniles of an 
abyssal species that has only been recorded 
from one locality at abyssal depth (4560 m) 
immediately south of the south west extremity 
of the Walvis Ridge. 

Shell Descnption (Figs. 38, 39). Shell tiny, 



22 



ALLEN 




FIG. 38. Dacrydium sp. a. Lateral views of two 
shells from the left side from J. Charcot Walvis 
Expedition sta. DS05, Cape Basin, 4560 m. Scale = 
0.5 mm. 




FIG. 39. Dacrydium sp. a. Internal view of a right 
valve from J. Charcot Walvis Expedition sta. DS05, 
Cape Basin, 4560 m. Scale = 0.5 mm. 



broadly ovate, semitranslucent, with a few 
faint growth lines; greatest shell height very 
slightly anterior to the mid-vertical axis, only 
slightly longer than high; umbo moderately 
large, prominent, distant from the antero-ven- 
tral margin; ventral margin almost straight, at 
most slightly convex; posterior and dorsal 
margins broadly rounded; anterior margin in 
hinge region almost straight, antero-ventrally 



meeting ventral margin in a broad curve; hinge 
plates short, narrow; posterior plate with 12- 
14 nepioconch teeth; anterior plate with 2-4 
teeth; plates reinforced by narrow buttresses 
that parallel the shell margin rather than devi- 
ating from it; ligament internal, amphidetic, 
rounded. Prodissoconch length 185 цт. 

Internal Morphology. The internal morphol- 
ogy, as seen through the transparent shell, 
appears to be similar to that of D. hedleyi. The 
adductor muscles are moderately large, and 
only the inner demibranch is present. The foot 
is particularly slender and secretes a byssus 
composed of many extremely fine strands. 

Although the shell shape with its great 
height is so distinctive, because only two tiny, 
fragile, juvenile specimens (1 mm and 1 .5 mm 
total length) were taken, it was decided not to 
name a new species at this stage. 

Dacrydium sp. b 
Fig. 40 
Specimen; BMNH 1996148. 

Material; Brazil Basin: Atlantis II, sta. 167, 
20 spec. 

Distribution; This species was taken at one 
mid-slope station in the Brazil Basin, 943- 
1007 m. 

Shell Description (Fig. 40). Shell, tiny, ex- 
tremely fragile, broadly ovate, with very fine, 
close, concentric lines, opaque white, great- 
est height coincident with or slightly anterior to 
mid-vertical axis; umbo relatively large, dis- 
tant from antero-ventral shell margin; ventral 
shell margin straight or slightly convex; poste- 
rior margin broad, rounded, joining dorsal 
margin in a smooth curve; antero-dorsal mar- 
gin angulate at limit of posterior hinge plate; 
anterior margin straight, almost vertical to 
rounded antero-ventral margin; ventral mar- 
gin varies from slightly convex in smallest 
specimens, through straight, to slightly con- 
cave in largest specimens; hinge plates rela- 
tively short, narrow; posterior plate with 1 5-1 6 
nepioconch teeth; anterior plate slightly 
shorter with 9-10 teeth; posterior shell but- 
tress, narrow, not extending far beyond limit of 
hinge faint anterior buttress extending short 
distance towards anterior adductor; ligament 
internal, amphidetic, relatively large, globular. 
Prodissoconch length; 122-129 цт. 

Internal Morphology (Fig. 40). The internal 
morphology is similar to that of the preceeding 
species. The adductor muscles are small and 
round, the anterior somewhat smaller than the 
posterior. Mantle fusion is similar to that in 
other species but little thickened, suggesting 



SPECIES OF DACRYDIUM 



23 




AP FT 



FIG. 40. Dacrydium sp. b. Lateral view of (a) shell from the right side; (b) outline of shell from left side; (c) in- 
ternal view of right valve; (d) detail of hinge of left valve; (e) semidiagrammatic view of the internal morphol- 
ogy as seen through a transparent shell from the left side. Specimens from Atlantis II sta. 1 67, Brazil Basin, 
943-1 007 m. Scale = 1 mm a, b, с and e; = 0.5 mm d. Refer to Materials & Methods for list of abbreviations. 



that these are juvenile specimens. There is no 
outer demibranch, and the inner demibranchs 
consists of 1 0-1 2 unreflected descending fila- 
ments in a specimen of 1.7 mm total length. 
Unlike other species, in which the foot ex- 
tends anteriorly within the canopy of the gill fil- 
aments, here the foot is recurved so that the 
tip is facing posteriorly, but this is is likely to be 
an artifact of preservation. The palps are 
small, distal enlargements of the lips, the 
upper of which are extended. The course of 
the gut is similar to that of other species, but 
the digestive diverticula comprise of a pair of 
sacs lateral to the stomach. In this, they re- 
semble the post-larval gut of other bivalves. 

The internal features all suggest that these 
specimens are the juveniles of a larger 
species rather than neotenous adults of a 
miniature species. In addition, the shell shape 



is reminiscent of the nepioconch stage in 
mytilid development. It is for these reasons, 
and the fact that the shells of all but two or 
three of the specimens have disintegrated, 
that this species is not named, even though it 
has characters unlike those any other de- 
scribed species. 



DISCUSSION 

The species of the genus Dacrydium are 
present throughout the world's oceans and, 
for the most part, in deep waters (>500 m). 
They are anchored by a fine tuft of byssus 
threads and may form nesting congregations 
incorporating fine sediment, without the shell 
fragments and sediment particles that form 
the nests of Lima iiians, as described by 



24 



ALLEN 



Gilmour (1967). In many cases, there ¡s clear 
evidence in the form of attached tissue and 
spicules that they are associated with 
sponges. It is not known whether this is a uni- 
versal association. Other mytilids are known 
to occur with sponges, tunicates and, even, 
skulls of whales, although not necessarily all 
the species of a genus are associated with a 
particular phylum. 

All species are small (<6 mm and the ma- 
jority approximately 3 mm) and fragile, with 
unpigmented shells that are either translus- 
cent or opaque and with little or no ornamen- 
tation. Some species may have faint radial 
and/or concentric lines. The species can be 
distinguished by the shell outline and hinge 
morphology. This includes the position of the 
greatest height of the shell in relation to the 
mid-vertical axis of the shell, the extent of 
the anterior and posterior hinge plates, the 
number of nepioconch teeth on the hinge 
plates, and the degree of development of a 
shell buttress associated with the hinge plate. 
Ockelmann (1983) points out that the dacry- 
dines have shells that are homologous to the 
nepioconch stage of other mytilids, some- 
times with provincular teeth present, and al- 
ways with a series of antehor and posterior 
teeth homologous with nepioconch teeth. 

There is a degree of variation in the shape 
of the shell outline and hinge features in all 
species, and this has been noted by other au- 
thors (e.g., Nicol, 1966; Poitiers, 1989). This 
involves variation irrespective and respective 
of size. The curvature of the ventral margin 
changes with growth, becoming straighter or 
more concave or more sinuous. In addition, 
the position of maximum shell height tends to 
shift posteriorly with growth. 

The internal morphology displays a number 
of features characteristic of the genus. While 
the adductor muscles vary in size and, as in 
the case of other mytilids, the anterior may be 
smaller than the posterior, the latter is always 
relatively well-developed. The posterior ad- 
ductor muscle is not excessively enlarged. 
There must be a balance between the size 
and strength of the muscle and the strength of 
such a thin, fragile, shell. It is clear that the 
buttresses play a part in the balance of ad- 
ductor forces and shell strength. The mantle 
margins are specialized in only one respect, 
namely the development of an aperture coin- 
cident with gonad maturity. It is homologous 
with the inhalent aperture of other lamelli- 
branchs. It would appear that it develops as a 
channel for the release of sexual products 



and is probably not concerned with the in- 
halent flow, which is through the extensive 
pedal gape. The "inhalent" aperture is formed 
from the inner mantle folds, which are devel- 
oped inwards. There no development of ten- 
tacles or papillae from the middle sensory 
mantle fold, and the structure has never been 
seen extended beyond the shell margins. It is 
more developed in the larger specimens of 
each species and only in specimens with ma- 
turing gonads has a lumen to the exterior 
been clearly identified. Prior to discharge, the 
eggs and sperm appear to be shed into the 
space enclosed by the outer demibranchs of 
species that develop them. Like the aperture, 
the full development of the outer demibranchs 
coincides with maturity. 

The gills are unusual. In the juveniles, and 
in some species the mature adult, only the 
inner demibranchs are present. Species in 
which the outer demibranchs are absent in 
the adult are among those that occur at 
abyssal depths. The inner demibranchs con- 
sist of a relatively few widely spaced filaments 
(approx. 1 0-20). There are no interlamellar or 
interfilamentar connectives. Although the gill 
filaments in a few of the smallest specimens 
hang vertically within the mantle cavity, in 
most others the filaments are characteristi- 
cally bent in an anterior direction at a point 
half way along their length. The outer demi- 
branchs develop from gill rudiments at the 
posterior limit of the axes. The outer demi- 
branchs at maximum extend anteriorly to 
about a third of the axial length. Their fila- 
ments are more closely set together and are 
not bent forward. It is hypothesized that the 
aperture and, when present, the outer demi- 
branch combine to form a reproductive mech- 
anism that canalizes the movement of eggs 
and sperm to ensure successful fertilization 
and the release of eggs or larvae. Sexes are 
separate. Although Ockelmann (1983) and 
Salas & Gofas (1997) showed that in D. vivi- 
parum, D. hyalinum and D. balgimi the eggs 
are incubated in the suprabranchial chamber, 
none of the species described here had em- 
bryos developing within the mantle cavity. 
Egg and prodissoconch size varies consider- 
ably among species, but it appears in general 
that those of abyssal and high latitude species 
are significantly larger than those of bathyal or 
shelf species in lower latitudes. 

Other features characteristic of the genus 
include the dorsal position of the viscera. The 
oesophagus, stomach and combined style 
sac, and midgut are elongate and lie parallel 



SPECIES OF DACRYDIUM 



25 



to the antero-posterior axis close to the shell 
buttress. Similarly, the foot is elongate and 
tubular and in the contracted state also lies 
parallel with this axis within the space en- 
closed by the inner demibranchs. The shell 
buttress provides the attachment surface for 
the pedal retractors. 

Another unusual feature involves the palps 
and lips. The palps are extremely small, with 
no more than the rudiments of two small 
ridges being present. However, the upper lips 
tend to be elongate and attached vertically to 
the mantle such that they form a collecting 
area immediately ventral to the mouth, at the 
point where food particles from the filaments 
accumulate. The ventral margin of the fila- 
ments of the inner demibranch, which is con- 
strued as the main food collector, are laterally 
extended so that the lateral cilia interlock with 
those of the adjacent filaments. It is likely that 
there is little sorting of food particles on gills 
and palps. 

The combination of these features gives a 
unique functional design, which fully supports 
Ockelmann (1983) in his decision to erect a 
new subfamily. Ockelmann (1 983) argues that 
the dacrydines are probably derived from the 
crenellines rather than the modiolines as sug- 
gested by Soot-Ryen (1969), and the present 
study supports this view. 

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Revised ms. accepted 4 December 1997 



APPENDIX 1. 
Stations from which material was collected 



Cruise Station Depth (m) Latitude Longitude 

NEWFOUNDLAND BASIN 



Date 



Gear 



Chain 106 


331 


4793 


41°13.0'N 


41°36.7'W 


29.8.72 


ES 






NORTH AMERICA BASIN 






Atlantis 277 


D 


466-508 


39°54.5'N 


70^35.0'W 


23.5.62 


AD 


Atlantis II 12 


62 


2496 


39°26.0'N 


70°33.0'W 


21.8.64 


ES 




64 


2886 


38°46.0'N 


70°06.0'W 


21.8.64 


ES 




66 


2802 


38°46.7'N 


70^08.8'W 


21.8.64 


ES 




70 


4680 


36°23.0'N 


67'58.0'W 


23.8.64 


ES 




72 


2864 


38°16.0'N 


71°14.0'W 


24.8.64 


ES 




73 


1330-1470 


39°46.5'N 


70°43.3'W 


25.8.64 


ES 


Atlantis II 17 


93 


4926-5007 


34°39.0'N 


66°26.0'W 


14.12.65 


ES 


Chain 50 


76 


2862 


39°38.3'N 


67 = 57.8'W 


29.6.65 


ES 




80 


4970 


34°49.8'N 


66"34.0'W 


2.7.65 


ES 




83 


5000 


34°46.5'N 


66'30.0'W 


3.7.65 


ES 




84 


4749 


36°24.4'N 


67'56.0'W 


4.7.65 


ES 




85 


3834 


37°59.2'N 


69'26.2'W 


5.7.65 


ES 


Chain 50 


87 


110 


39°48.7'N 


70°40.8'W 


6.7.65 


ES 




88 


478 


39°54.1'N 


70°37.0'W 


6.7.65 


ES 


Chain 58 


103 


2022 


39°43.6'N 


70°37.4'W 


4.5.66 


ES 




105 


530 


39°56.6'N 


71 03.6'W 


5.5.66 


ES 


Atlantis II 24 


115 


2030-2050 


39°39.2'N 


70'24.5'W 


18.8.66 


ES 




118 


1135-1153 


32°19.4'N 


64°34.9'W 


18.8.66 


ES 




119 


2095-2223 


34°15.8'N 
32°16.1'N 


64°31 .6'W- 
64^32.6'W 


19.8.66 


ES 


Atlantis II 30 


128 


1254 


39"46.5'N 


7045.2'W 


16.12.66 


ES 


Chain 88 


210 


2024-2064 


39°43.0'N 
39°43.2'N 


7046.0'W- 
70 49.5'W 


22.2.69 


ES 


Knorr35 


346 


475 


39^^54.1 'N 
GUYANA BASIN 


70°10.7'W 


3.12.73 


ES 


Knorr 25 


287 


4980-4934 


13 16.0'N 
13'16.8'N 


54 52.2'W- 
54^53.1 'W 


24.2.72 


ES 




288 


4417-4429 


ir02.2'N 
11°03.8'N 


55"05.5'W- 
55"04.8'W 


25.2.72 


ES 




291 


3859-3868 


10"06.6'N 


55 1 5.4'W 


26.2.72 


ES 




306 


3392-5073 


09°31.1'N 


56 24.4'W 


2.3.72 


ES 


J. Charcot 


CP02 


5073 


10°59.0'N 


45"15.0'W 


14.11.77 


CP 


Biovema 


DS05 


5100 


10'46.0'N 


4240.3'W 


18.11.77 


ES 


(Vema) 


DS11 


5867 


11 '37.5'N 
11"37.6'N 


32'53.8'W- 
32°52.8'W 


26.11.77 


ES 



SPECIES OF DACRYDIUM 



29 









BRAZIL BASIN 








Atlantis 1131 


142 


1624-1796 


10'30.0'N 


17°51.5'W 


5.2.67 


ES 




144 


2051-2357 


10^36.0'N 


17°49.0'W 


6.2.67 


ES 




147 


2934 


10°38.0'N 


17°52.0'W 


6.2.67 


ES 




155 


3730-3783 


00°03.0'S 


27°48.0'W 


13.2.67 


ES 




156 


3459 


00°46.0'S 


29°28.0'W 


14.2.67 


ES 




167 


943-1007 


07°58.0'S 


34=17.0'W 


20.2.67 


ES 




169 


587 


08°38.0'S 
ARGENTINE BASIN 


34 23.0'W 


21.2.67 


ES 


Atlantis II 60 


239 


1661-1669 


36°49.0'S 


53°15.4'W 


11.3.71 


ES 




240 


2195-2323 


36°53.4'S 


53^10.2'W 


12.3.71 


ES 




245 


2707 


36°55,7'S 


53''01.4'W 


14.3.71 


ES 






WEST EUROPEAN BASIN 






Sarsia 


S33/2 


1537-183 


43=41.0'N 


03°36.0'W 


13.7.67 


ES 




S44 


1739 


43°40.8'N 


03'35.2'W 


16.7.67 


ES 




S50 


1102 


43°46.7'N 


03°38.0'W 


18.7.67 


ES 




S61 


952 


46°20.5'N 


04=36.0'W 


24.7.67 


ES 




S63 


1336 


46°17.5'N 


04'45.2'W 


24.7.67 


ES 




S66 


1472 


40°16.3'N 


04°44,0'W 


25.7.67 


ES 


Discovery 


7601 


3100 


43^51. 8'N 


03''43.4'W 


4.9.76 


AD 


Challenger E 


80-73 


900-2300 


'Off Rockair 


-.-.73 


ES 


Chain 106 


313 


1491-1500 


51"32.2'N 


12°35.9'W 


17.8.72 


ES 




318 


2560 


50"27.3'N 


13°20.9'W 


19.8.72 


ES 




321 


2868-2890 


50=12.3'N 


13='35.8'W 


20.8.72 


ES 


J. Charcot 














Biacores 


245 


4270 


40'57.0'N 


22='16.0'W 


14.11.71 


CLG 


La Perle 














Biogas 1 


DSU 


2205 


47°35.5'N 


08^^33.7'W 


8.8.72 


ES 


J. Charcot 


DSI 5 


2246 


47°35.2'N 


08''40.1'W 


21.10.72 


ES 


Polygas 


DSI 7 


2103 


47'='32.0'N 


08 45.5'W 


22.10.72 


ES 




DS18 


2138 


47°32.2'N 


08"'N.9'W 


22.10.72 


ES 




DS20 


4226 


47°33.0'N 


09°36.7'W 


24.10.72 


ES 




DS21 


4190 


47^31. 5'N 


09=40. 7' W 


24.10.72 


ES 




CV13 


4252 


47°31.8'N 


09°34.2'W 


25.10.72 


CV 




DS22 


4144 


47°34.1'N 


09=38.4'W 


25.10.72 


ES 




DS23 


4734 


46°32.8'N 


10°21.0'W 


26.10.72 


ES 




DS25 


2096 


44"08.2'N 


04°1 5.7'W 


1.11.72 


ES 




DS26 


2076 


44'=08.2'N 


04'=1 5.0'W 


1.11.72 


ES 




DS31 


2813 


47°32.5'N 


09°04.2'W 


19.4.73 


ES 


Biogas II 


DS32 


2138 


47°32.2'N 


08°05.3'W 


19.4.73 


ES 


Biogas III 


DS36 


2147 


47°32.7'N 


08=36.5'W 


24.8.73 


ES 




DS37 


2110 


47"31.8'N 


08"34.6'W 


25.8.73 


ES 




DS38 


2138 


47°32.5'N 


08°35.8'W 


25.8.73 


ES 




DS41 


3548 


47°28.3'N 


09^07.2'W 


26.8.73 


ES 




DS42 


4104 


47°32/N4 


09=35.6'W 


27.8.73 


ES 




DS44 


3992 


47°33.2'N 


0942.0'W 


27.8.73 


ES 




DS45 


4260 


47°33.9'N 


09°38.4'W 


27.8.73 


ES 




DS46 


4521 


46°28.6'N 


10'23.0'W 


29.8.74 


ES 




DS48 


4203 


44°29.0'N 


04''54.0'W 


31.8.73 


ES 




DS50 


2124 


44°08.9'N 


04^15.9'W 


1.9.73 


ES 


J. Charcot 


DS51 


2430 


44'=11.3'N 


04"15.4'W 


18.2.74 


ES 


Biogas IV 


DS52 


2006 


44°06.3'N 


04-22.4'W 


18.2.74 


ES 




DS54 


4659 


46^'31.3'N 


10"29.2'W 


21.2.74 


ES 




DS55 


4125 


47'34.9'N 


09=40.9'W 


22.2.74 


ES 




KR31 


4097 


47°37.0'N 


09'=41 /W6 


22.2.74 


ES 




DS56 


4050 


47^^32.7'N 


09°28.2'W 


23.2.74 


ES 




DS58 


2775 


47^34. 1'N 


09"08.2'W 


23.2.74 


ES 




DS59 


2790 


47°31.7'N 


09°06.2'W 


24.2.74 


ES 




DS61 


2250 


47°34.7'N 


08°38.8'W 


25.2.74 


ES 




CP01 


2245 


47°34.6'N 


08°38.8'W 


25.2.74 


ES 




DS62 


2175 


47°32.8'N 


08°40.0'W 


26.2.74 


ES 




DS63 


2126 


47°32.8'N 


08'35.0'W 


26.2.74 


ES 



30 






ALLEN 










DS64 


2156 


47°29.2'N 


08^30.7'W 


26.2.74 


ES 


Biogas V 


CP07 


2170 


'№09.8'N 


044 6.4'W 


21.6.74 


ES 




DS67 


4150 


47°31.0'N 


09=35.0'W 


17.6.74 


ES 




DS68 


4550 


46°26.7'N 


10^23.9'W 


19.6.74 


ES 




DS69 


4510 


'№21.9'N 


04^52.4'W 


20.6.74 


ES 


Biogas VI 


CP08 


2177 


'№33.2'N 


08'38.5'W 


20.10.74 


CP 




CP09 


2171 


47°33.0'N 


08"N.1'W 


20.10.74 


CP 




DS71 


2194 


47°34.3'N 


08 33.8'W 


20.10.74 


ES 




DS75 


3250 


47°28.1'N 


09 07.8'W 


22.10.74 


ES 




DS76 


4228 


47°34.8'N 


09^33.3'W 


23.10.74 


ES 




CP13 


4134 


47°34.4'N 


09'38.0'W 


23.10.74 


CP 




CP14 


4237 


47°32.0'N 


09=35.9'W 


23.10.74 


CP 




KR60 


4220 


47°32.3'N 


09 37.2'W 


24.10.74 


KR 




KR64 


4700 


46^30.8'N 


10=20.8'W 


24.10.74 


KR 




DS74 


2777 


47°33.0'N 


09 07.8'W 


21.10.74 


ES 




DS77 


4240 


47°31.8'N 


09' 34.6'W 


24.10.74 


ES 




DS78 


4706 


46°31.2'N 


10'23.8'W 


25.10.74 


ES 




CP16 


4825 


46°27.6'N 


10^26.8'W 


25.10.74 


CP 




DS79 


4715 


46°30.4'N 


10'27.1'W 


26.10.74 


ES 




CP17 


4706 


46°30.8'N 


10'19.5'W 


26.10.74 


CP 




CP18 


4721 


46°30.0'N 


10'26.0'W 


26.10.74 


CP 




DS80 


4720 


46°29.5'N 


10 29.5'W 


27.10.74 


ES 




DS81 


4715 


46°28.3'N 


10 24.6'W 


27.10.74 


ES 




CP21 


4453 


44°21 .2'N 


04-49. 3'W 


30.10.74 


CP 




DS86 


1950 


44^04. 8'N 


04 18.7'W 


31.10.74 


ES 




CP23 


1980 


44'04.6'N 


04 21.4'W 


31.10.74 


CP 




DS87 


1913 


44°05.2'N 


04°19.4'W 


1.11.74 


ES 




CV38 


2690 


47°30.9'N 


08''59.5'W 


24.2.74 


CV 


Thalassa 


Z397 


511 


47^^33.8'N 


07'12.'W6 


22.10.73 


GBO 




Z400 


1175 


47°33.4'N 


07 18.1' W 


22.10.73 


GBS 




Z413 


805 


48°03.1'N 


08'29.4'W 


24.10.73 


PBS 




Z417 


865 


48°12.0'N 


09'09.5'W 


24.10.73 


PBS 




Z427 


330 


48"27.0'N 


09 48.4'W 


25.10.73 


PBS 




Z435 


1050 


48°39.7'N 


09'53.2'W 


26.10.73 


PBS 




Z447 


1430-1530 


48°47.3'N 
48°47.4'N 


11 12.0'W- 
11 14.3'W 


27.10.73 


CP 


Incal 


DS01 


2091 


57°59.7'N 


10 39.8'W 


15.7.76 


ES 




CP01 


2041 


57 57.7'N 


10 55.0'W 


16.7.76 


CP 




DS02 


2081 


57°58.8'N 


10 48.5'W 


16.7.76 


ES 




CP08 


2644 


50°14.7'N 


13'13.5'W 


27.7.76 


CP 




CP10 


4823 


48°25.5'N 


15'10.7'W 


31.7.76 


CP 




DSU 


4823 


48°18.6'N 


15'12.0'W 


1.8.76 


ES 




CP11 


4823 


48°20.4'N 


15 14.6'W 


1.8.76 


CP 




WS02 


4829 


48°19.2'N 


15'23.3'W 


1.8.76 


WS 




OS03 


4829 


48"19.2'N 


15'15.9'W 


2.8.76 


OS 




OS05 


4296 


47 31.3'N 


09 34.6'W 


7.8.76 


OS 




KR14 


4299 


47°29.8'N 


09 37.4'W 


7.8.76 


KR 




WS07 


4281 


47"30.6'N 


09' 37.1 'W 


7.8.76 


WS 




DS14 


4254 


47'32.6'N 


09 35.7'W 


7.8.76 


ES 




DS15 


4211 


47 33.4'N 


09' 39.1 'W 


8.8.76 


ES 




DS16 


4268 


47°29.8'N 


09'^36.2 'W 


9.8.76 


ES 




WS08 


4287 


47''30.5'N 


09 33.7'W 


9.8.76 


WS 




OS06 


4316 


46"27.3'N 


09 36.2'W 


9.8.76 


OS 




OS07 


4249 


47°31 .8'N 


09 34.3'W 


10.8.76 


OS 




WS09 


4277 


47°28.8'N 


39°34.0'W 


10.8.76 


WS 




WS10 


4354 


47''27.3'N 


09 39.9'W 


11.8.76 


WS 




OS08 


4327 


47°29.8'N 
CANARY BASIN 


09 39.2'W 


11.8.76 


OS 


Discovery 


6696 


1564 


27°57.0'N 


13 ^36.2'W 


15.3.68 


ES 




6701 


1934 


27°45.2'N 


14'^13.0'W 


16.3.68 


ES 




6704 


2129 


2744.9'N 


14°25.0'W 


17.3.68 


ES 



SPECIES OF DACRYDIUM 
AZORES MID-ATLANTIC RIDGE 



31 



J. Charcot 














Bioacores 


105 


1675 


39°35.0' N 


ЗГ23.0'\Л/ 


20.10.71 


DP 




120 


2100 


39°03.5'N 


32°43.5'W 


22.10.71 


ES 




126 


3360 


39°19.5'N 
SIERRA LEONE BASIN 


33°47.0'W 


23.10.71 


ES 


Atlantis II 


148 


3828 


10'37.0'N 


18 = 14.0'W 


7.2.67 


ES 




149 


3861 


10°30.0'N 
ANGOLA BASIN 


18=18.0'W 


7.2.67 


ES 


J. Charcot 














Walda 


DS13 


3985 


14^21.5'S 


09°46.2'E 


?8.71 


ES 


Atlantis 1142 


202 


1427-1643 
1643 


08°56.0'S 
08'M6.0'S 

CAPE BASIN 


12°15.0'E- 
12 47.0'E 


23.5.68 


ES 


J. Charcot 


DS02 


5280 


33°54.7'S 


05°08.3'E 


26.12.78 


ES 


Walvis 


KG14 


4610 


33°20.9'S 


02=38.0'E 


29.12.78 


KG 




DS05 


4560 


33°20.5'S 


02^'34.9'E 


30.12.78 


ES 




DS06 


4585 


33°24.5'S 


02'32.9'E 


31.12.78 


ES 




DS07 


5100 


26°59.7'S 
WEDDELLSEA 


01 ^07.1 'E 


3.1.79 


ES 


IWSOE 


001 


728 


74'^07.0'S 


39 38.0'W 


6.2.68 


ES 




002 


412 


75°31.5'S 


30 = 08,0'W 


25.2.69 


AD 




004 


793 


77°05.5'S 


35=04.0'W 


26.2.69 


AD 




005 


1079 


77°19.8'S 


36^41.3'W 


27.2.69 


AD 




007 


512 


77=16.0'S 


42'38.0'W 


1.3.69 


AD 




008 


585 


77"36.2'S 


40"30.0'W 


2.3.69 


AD 




010 


659 


77°50.0'S 


42'05.2'W 


4.3.69 


AD 




022 


3111 


73°28.4'S 


30''26.9'W 


13.3.69 


ES 




023 


3697 


72°47.6'S 


30^29. 7'W 


14.3.69 


AD 




027 


4575 


64''46.2'S 


41=30.1'W 


19.3.69 


ES 



APPENDIX 2. DESCRIBED SPECIES OF 
THE GENUS DACRYDIUM 

?Dacrydium sp. Pelseneer, 1911. Probably a 
juvenile Amygdalum (Mattson & Waren, 
1977;Ockelmann, 1983). 

Dacrydium sp. Salas, 1996 
Location of specimens: MNHNP 
Dacrydium sp. Salas, 1996: 53, figs, 97-99. 
Distribution: Western Mediterranean, 
890-2035 m. 

Dacrydium sp. a Ockelmann, 1959 
Location of specimen: ZMUC. 
Dacrydium sp. a Ockelmann, 1959: 50, 195. 
Dacydium sp. a Okutani, 1968: 15. 
Distribution: Restricted to "depths of 
Norwegian Sea." 

Dacrydium sp. с Ockelmann, 1959 
Location of specimen: ZMUC. 
Dacrydium sp. с Ockelmann, 1959: 50, 195. 
Dacrydium sp. с Okutani, 1968: 15. 
Distribution: North Atlantic, WSW and SE 



Iceland, SW Faroes and W. Norway. 
Depth range: "intermediate depths." 

Dacrydium sp. Routiers, 1989 

Location of specimen: MNHNP. 

Dacrydium sp. Routiers, 1989: 214, 215, fig. 

3d. 
Distribution: Benthedi Sta. 87, SE Glorieuse 

Is. ir44'S 47"35'E. Depth range: 3716 

m. 

Dacrydium albidum Pelseneer, 1 903 

Type locality: Southern Ocean, 7ri8'S 

88"02'W, 200 fm. 
Type specimen: IRSNB. 
Dacrydium albidum Pelseneer, 1903: 26, pi. 

VIII, fig. 100. 
Dacrydium albidum. Hedley, 1906: 72. 
Dacrydium albidum, Thiele, 1912: 21, pi. 17, 

figs. 10, 10a. 
?Dacrydium albidum. Theile, 1912: 226, pi. 

17, figs. 9, 9a. 
Dacrydium albidum. Lamy, 1937: 70. 
Dacrydium albidum, Soot-Ryen, 1951 : 20. 



32 



ALLEN 



Dacrydium albidum, Powell, 1958: 175. 
Dacrydium albidum, Powell, 1960: 174. 
?Dacrydium albidum, Clarke, 1961 : 378. 
Dacrydium albidum. Nicol, 1966: 25, pl. 3, 

figs. 2, 8. 
Dacrydium albidum. Okutani, 1968: 15, flg. 

ig- 

Dacrydium albidum. Egorova, 1982: 64, figs. 

271,272. 
Dacrydium albidum. Bernard, 1983: 19. 
Dacrydium modlollf arme. Bernard, 1983: 19. 
Dacrydium albidum. Ockelmann, 1983: 112, 

118. 
Dacrydium albidum. Poutiers, 1989: 214, 215, 

fig. 3i. 
Dacrydium albidum. Muhlenhardt-Siegal, 

1989: 161, pl. 2, flg. 20. 
?Dacrydlum albidum. Dell, 1990: 33, figs. 

55-57. 
?Dacrydlum modlollforme. Dell, 1990: 34. 
Distribution: Southern Ocean, Davis and 

Ross seas, South Shetland Isles. Depth 

range: 122-1473 m (possibly to 4758 

m-ee Dell (1990) and D. knudseni 

above). 

Dacrydium angulare Ockelmann, 1983 
Type locality: Cape Basin, Vema Sta. 54, 

34"35'S 17 = 31'E, 1849 m. 
Type specimen: Holotype ZMUC; paratypes 

ZMUC, USNM 822398. 
?Dacrydium albidum. Clarke, 1961 : 378. 
Dacrydium angulare Ockelmann, 1983: 114, 

figs. 46-48, 51. 
Dacrydium angulare. Poutiers, 1989: 214, 

215, fig. 3j. 
Dacrydium angulare. Salas &: Gofas, 1997: 

266, figs. 15-19. 
Distribution: South Atlantic. Depth range: 

1849 m. 

Dacrydium balglml Sa\as & Gofas, 1997 
Type locality: Off northwestern Morocco, 

35°12'N07 53' W, 2035 m. 
Type specimen: Holotype and paratypes 

MNHNP. 
Dacrydium balglml Sa\as & Gofas, 1997: 275, 

figs. 52-57. 
Distribution: North Canary Basin. Depth 

range: 2035 m. 

Dacrydium dauvlnl Sa\as & Gofas, 1997 
Type locality: Atlantis Bank, 34 05.1 'N 

30-13.6'W, 260 m. 
Type specimen: Holotype and paratypes 

MNHNP; paratypes SMNH. 
Dacrydium dauvlnl Sa\as & Gofas, 1997: 273, 

figs. 44-48. 



Distribution: Atlantis Bank, Canaries Basin. 
Depth range: 280-330 m. 

Dacrydium flllferum Salas & Gofas, 1 997 
Type locality: Atlantis Bank, 34'04.8'N 

30"14.9W, 330 m. 
Type specimen: Holotype and paratypes 

MNHNP. 
Dacrydium flllferum Salas & Gofas, 1997: 

275, figs. 49-51. 
Distribution: Atlantis Bank, Canaries Basin. 

Depth range: 330-340 m. 

Dacrydium elegantulum elegantulum Soot- 
Ryen, 1955 

Type locality: Bahía de Gardner, Islas 
Galapagos, Sta. BS 453, 35 fms. 

Type specimen: Holotype AHF. 

Dacrydium (Quendreda) elegantulum Soot- 
Ryen, 1955:87, pl. 8, fig. 41. 

Dacrydium elegantulum. Bernard, 1978: 62. 

Dacrydium (Quendreda) elegantulum. 
Bernard, 1983: 19. 

Dacrydium elegantulum Ockelmann, 1983: 
112, 113. 

Distribution Bahía de Gardner, Islas Galap- 
agos: Baja California: off Redondo 
Beach, California. Depth range: 45-64 m. 

Dacrydium elegantulum hendersoni Salas & 

Gofas, 1997 
Type locality: Florida, off Sand Key, 100 fm. 
Type specimen: Holotype and paratypes. 

USNM 459094; paratypes USNM 

459098. 
Dacrydium elegantulum hendersoni Salas & 

Gofas, 1997:278, figs. 61-65. 
Distribution: off Sand Key, Florida. Depth 

range: 155-200 m. 

Dacrydium fabale Hedley, 1 904 

Type locality: 16 m. E of Wollongong, New 

South Wales, 100 fm. Type specimen: 

Holotype AMS. 
Dacrydium fabale Hedley, 1904: 199, pl. X, 

fig. 39. 
Quendreda fabale. Iredale, 1936: 271. 
Dacrydium fabale. Lamy, 1937: 70. 
Dacrydium (Quendreda) fabale. Soot-Ryen, 

1955:87, pl. 8, fig. 41. 
Dacrydium fabale, Ockelmann, 1983: 112, 

113. 
Distribution: off New South Wales. Depth 

range: 182 m. 

Dacrydium glorlosense Poutiers, 1989 
Type locality: Benthidi Sta. 87, 11° 44'S 

47'35'E, 3716 m. 
Type specimen: Holotype MNHNP. 



SPECIES OF DACRYDIUM 



33 



Dacrydium gloriosense Routiers, 1989: 210, 

212, 215, figs. 2a-c, 3g. 
Distribution: SE of thie Glorieuse Isles. Depth 

range: 3700-3718 m. 

Dacrydium hyalinum (Monterosato, 1875) 

Type locality: Off Palermo, Sicily. 

Type specimen: Lectotype USNM 199198, 

paralectotypes from the same lot USNM. 
Dacrydium sp. Monterosato, 1870: 43-46. 
Dacrydium hyalinum Hidalgo, 1870: 128, 

nomen nudum. 
Mytilus vitreus. Jeffreys, 1870: 68. 
Dacrydium vitreum, Monterosato, 1872: 18. 
Mytiius (Dacrydium) liyalinus Monterosato, 

1875: 10. 
Dacrydium hyalinum, Monterosato, 1878: 

66. 
Dacrydium vitreum. Jeffreys, 1883: 394. 
Dacrydium hyalinum. Clessin, 1889: 156. 
Dacrydium hyalinum. Locard, 1891 : 342. 
Dacrydium hyalinum, Locard, 1896: 205. 
Dacrydium vitreum y эх. hy aliña, Lamy, 1937: 

68. 
?Dacrydium sp. Soot-Ryen, 1966: 8. See 

Okutani (1968: fig. If) and Mattson & 

Waren (1977). 
Dacrydium hyalinum, Okutani, 1968: 15. 
Dacrydium hyalinum. Mattson & Waren, 

1977: p. 1,figs. 3, 9. 
Dacrydium hyalinum, Ockelmann, 1983: 112, 

113, 120. 
Dacrydium hyalinum, Nordsieck, 1989: 30. 
Dacrydium hyalinum. Salas, 1996: 53, figs. 

91-93. 
Dacrydium hyalinum. Salas & Gofas, 1997: 

266. figs. 20-24. 
Distribution: Off Palermo and possibly lusi- 

tanean (35 34'N 07"35'W. See Soot- 
Ryen (1966) and Mattson & Waren 

(1977). Depth range: 76-1615 m. 

?Dacrydium méridionale Smith, 1885. Prob- 
ably a phylobryid. See Bernard (1897), 
Melville & Standen (1907), Lamy (1937), 
Powell (1960), Okutani (1968), and 
Poutiers (1989). 

Dacrydium minimum Okutani & Izumidate, 

1992 
Type locality: Yamatotai Bank, Sea of Japan, 

39'45.77'N 135'00.00'E, 1200 m. 
Type specimen: Holotype NSMT Mo-69662; 

paratype NSTM Mo-69663. 
Dacrydium minimum Okutani & Izumidate, 

1992: 149, figs 1-3. 
Distribution: Sea of Japan. Depth range: 

394-1200 m. 



?Dacrydium modioliformeJheWe, 1912 
Type locality: Gauss Station, Davis Sea, 

400 m. 
Type specimen: ?ZMHU 
Dacrydium modioliforme Theile, 1912: 226- 

227, fig. 10, 10a. But see Nicol (1966), 

Knudsen (1970), Poutiers (1989), and 

Dell (1990). Probably synonymous with 

D. albidum See also D. knudseni. 
?Dacrydium modioliforme, Thiele & Jaeckel, 

1931: 170. 
Dacrydium modioliforme, Lamy, 1937: 70. 
Dacrydium modioliforme, Soot-Ryen, 1951: 

20. 
Dacrydium modioliforme, Powell, 1960: 

174. 
Dacrydium modioliforme, Nicol, 1966: 26. 
Dacrydium modioliforme, Okutani, 1968: 15. 
Dacrydium modioliforme, Knudsen, 1970: 92, 

178. 
Dacrydium modioliforme, Bernard, 1978: 63. 
Dacrydium modioliforme, Poitiers, 1989: 214. 
?Dacrydium modioliforme, Dell, 1990: 34. 
Distribution: Southern Ocean. Depth range: 

400-74758 m. 

Dacrydium nipponicum Okutani, 1975 

Type locality: Soyo-Maru Sta. B2 (11-XII- 

1967) 34'22.2'N 139'41.9'E. 1080-1205 

m. 
Type specimen: Holotype and paratypes 

TRFRL. 
Dacrydium pacificum {non Dali 1916), 

Okutani, 1968: 14, fig. la. 
Dacrydium nipponicum Okutani, 1 975: 68, fig. 

1,pl. Ill, fig. 2. 
Dacrydium nipponicum, Bernard, 1978: 62. 
Dacrydium nipponicum, Ockelmann, 1983: 

112. 
Dacrydium nipponicum, Poutiers, 1989: 214, 

215, fig. 3k. 
Dacrydium nipponicum. Hayami & Kase, 

1993:47. 
Dacrydium nipponicum, Salas & Gofas, 1997: 

263. 
Distribution: Off Miyake Isle, Sea of Japan. 

Depth range: 1000-1250 m. 

Dacrydium occidentale Smith, 1885 

Type locality: Challenger Sta. 24, off Culebra 
Isle, 18 38.5'N 65' 05.5'W, 390 fm. 

Type specimen: Syntype, BMNH: type mater- 
ial completely destroyed by Bynes' dis- 
ease; no other material exists. 

Dacrydium occidentale Smith, 1885: 282, pi. 
XVII, fig. 1, la. 

Dacrydium occidentale, Lamy, 1937: 69. 



34 



ALLEN 



Dacrydium occidentale, Okutani, 1968: 15 fig. 

1b. 
Dacrydium occidentale. Nordsieck, 1969: 30, 

pl. IV, figs. 20. 12. 
Dacrydium occidentale, Bernard, 1978: 63. 
Dacrydium occidentale, Ockelmann, 1983: 

112. 
Dacrydium occidentale, Routiers, 1989: 214, 

215, fig. Зе. 
Dacrydium occidentale. Kayami & Käse, 

1993:47. 
?Dacrydium occidentale. Salas & Gofas, 

1997:270, figs. 33-35. 
Distribution: West Indies. Depth range: 702 m. 

Dacrydium ockelmanni Mattson & Waren, 

1977 
Type locality: W. Nonway, Korsfjorden, 

60°08.35'N 05"00.40'E, 260-290 m. 
Type material: Holotype ZMUB 58633, 

paratypes 58634. Other paratypes 

MNHNand USNM. 
?Dacrydium SÇ). Lande, 1975: 10, 12. 
Dacrydium ockelmanni Mattson & Waren, 

1977:2, figs. 4-6, 10-13. 
Dacrydium ockelmanni. Ockelmann, 1983: 

112, 113, 116. 
Dacrydium ockelmanni. Hoisaeter, 1986: 115. 
Dacrydium ockelmanni. Smith & Heppell, 

1991:60. 
Dacrydium ockelmanni, Waren, 1991: 114, 

115, fig. 40A-C. 
Dacrydium ockelmanni. Salas & Gofas, 1997: 

264, figs. 7-14. 
Distribution: Bay of Biscay, NW of Ireland, 

WSW and SB of Iceland, SW of Faroes, 

off W Norway. Depth range: 145-600 m. 

Dacrydium pacificum Dal I, 1916 

Type locality: Albatross Sta. 3604, 54''54'N 

168^^59'W, 1401 fm. 
Type material: Syntypes USNM 214092, 

SBMNH 34061, paratypes ZMUC. 
Dacrydium pacificum Dall, 1 91 6: 405. 
Dacrydium pacificum, Dall, 1921 : 22. 
Dacrydium pacificum. Oldroyd, 1924: 72. 
Dacrydium pacificum. Lamy, 1937: 69. 
Dacrydium pacificum. Clarke, 1962: 58. 
Dacrydium pacificum. Boss et al., 1968, p. 

335. 
Dacrydium pacificum, Knudsen, 1970: 89, fig. 

52C-E. 
Dacrydium pacificum. La Rocque, 1973: 38. 
Dacrydium pacificum, Abbott, 1974: 437. 
Dacrydium pacificum. Okutani, 1975: 69. 
Dacrydium pacificum. Bernard, 1978: 62. 
Dacrydium pacificum. Bernard, 1983: 19. 
Dacrydium pacificum. Ockelmann, 1983: 112. 



Dacrydium pacificum, Routiers, 1989: 212, 

215, fig. 3b. 
Dacrydium pacificum, Scott et al., 1990: 11 . 
Distribution NE Pacific and SE Bering Sea. 

Depth range: 2562 m. 

Dacrydium panamensis Knudsen, 1970 
Type locality: Galathea Sta. 726, 05°49'N 

78 52'W, 3270-3670 m. 
Type specimen: Holotype ZMUC. 
Dacrydium sp. Wolff, 1961 : 150, fig. 19. 
Dacrydium sp. Okutani, 1968: 15, fig. le. 
Dacrydium panamensis Knudsen, 1970: 91, 

figs. 53, 54. 
Dacrydium panamensis, Abbott, 1974: 437. 
Dacrydium panamensis, Bernard, 1978: 62, 

63. 
Dacrydium panamensis, Bernard, 1983: 19. 
Dacrydium panamensis, Ockelmann, 1983: 

112. 
Dacrydium panamensis. Routiers, 1989: 212, 

215, fig. 3h. 
Dacrydium panamensis, Dell, 1990: 34. 
Distribution: East Pacific, Gulf of Panama. 

Depth range: 3270-3670 m. 

Dacrydium pelseneeri Hedley, 1 906 

Type locality: 'continental shelf, New Zea- 
land. Type specimen: ?NMNZ. 

Dacrydium pelseneeri V\eô\ey, 1906: 72, pl. II, 
fig. 8. 

Dacrydium pelseneeri. Lamy, 1937: 70. 

Dacrydium pelseneeri. Soot-Ryen, 1955: 87. 

Dacrydium pelseneeri. Ockelmann, 1983: 
112. 

Distribution: Depth range, shelf depths. 

Dacrydium radians Suter, 1908. Gatliff & Gab- 
riell (1 91 6) and Lamy (1 937-71 ), indicate 
probably a senior synonym of Modiolaria 
rhyllensis Gatliff & Gabriell, 1912. 

Dacrydium rostriferum Bernard, 1978 

Type locality: West of Cape Flattery, 
48 26.6'N 126 54.5'W, 2532 m. 

Type specimen: Holotype LACMNH 1880, 
Paratypes USNM 771804, NSMT 
.55441, California Academy of Sciences 
59409, Oregon State University Bio- 
logical Institution 01501. 

Dacrydium (Dacrydium) rostriferum Bernard, 
1978:62, figs. 1, 12. 

Dacrydium rostriferum, Bernard, 1983: 19. 

Dacrydium rostriferum, Ockelmann, 1983: 
112. 

Dacrydium rostriferum. Routiers, 1989: 214, 
215, fig. 3f. 

Dacrydium rostriferum, Hayami & Kase, 1 993: 
47. 



SPECIES OF DACRYDIUM 



35 



Distribution: Off the coast of Wasfiington, 
USA, between 44°38'N 125°35'W and 
48°22'N 126°54'W. Deptli range: 2530- 
2865 m. 

Dacrydium speculum Routiers, 1989 

Type locality: off SW Sri Lanka, Safari II Sta. 2 

SIRAN 19, SW of Sri Lanka, 05°37'N 

78°24'E, 3660 m. 
Type specimen: Holotype MNHNR. 
Dacrydium speculum Routiers, 1989: 210, 

212, 214, 215, figs, la-c, 3a. 
1 Dacrydium cf. speculum Salas & Gofas, 

1997:277, figs. 58-60. 
Distribution SW of Sri Lanka; ?Cape Verde 

Basin (Salas & Gofas, 1997). Depth 

range: 3660 m, (4580 m if present in 

Cape Verde Basin). 

Dacrydium vitreum (Moller, 1842) 

Type locality: Sukkertoppen, West Greenland, 

73 m. 
Type specimen: originally ZMUC, probably 

lost (Waren, 1991). 
Modiola? vitrea Holböll MS, in Moller, 1842: 

92 
Dacrydium vitreum, Torell, 1859: 138, pi. i, fig. 

2a, b. 
? Dacrydium vitreum. Hidalgo, 1870: 128. 
Modiolaria (Dacrydium) vitrea, Mörch, in 

Jones, 1875: 133 
Dacrydium vitreum. Jeffreys, 1876: 429. 
Dacrydium vitreum. Friele, 1878: 222. 
Dacrydium vitreum. Sars. 1878 (in part): 28, 

pi. 3, fig. 2a, b. 
Dacrydium vitreum, Jeffreys, 1879: 569. 
Dacrydium vitreum. Verrill, 1882: 579, pi. 44, 

fig. 8. 
Dacrydium vitreum. Verrill, 1884: 281. 
7 Dacrydium vitreum. Smith, 1885: 282. 
? Dacrydium vitreum, Dautzenberg, 1889: 77. 
Dacrydium vitreum. Clessin, 1889: 155, pi. 6, 

figs. 16, 17. 
Dacrydium vitreum. Dall, 1889: 38. 
Dacrydium vitreum, Rosselt, 1895 (in part): 

66. 
Dacrydium vitreum. Locard, 1896: 205. 
Dacrydium vitreum. Dautzenberg, 1897: 199. 
? Dacrydium vitreum. Bernard, 1898: 71. 
Dacrydium vitreum, Locard, 1898: 364. 
Dacrydium vitreum. Rosselt & Jensen (in 

part), 1898:21. 
Dacrydium vitreum. Locard, 1899: 170. 
Dacrydium vitreum, Friele & Grieg, 1901 : 24. 
Dacrydium vitreum, Whiteaves, 1901 : 121 . 
Dacrydium vitreum, Jensen, 1905: 325. 
IDacrydium vitreum, Dautzenberg & Fisher, 

1912:373. 



Dacrydium vitreum, Jensen (in part), 1912: 

54. 
Dacrydium vitreum, Johnson, 1915: 34. 
Dacrydium vitreum, Odhner, 1915: 82. 
Dacrydium vitreum. Grieg, 1916: 8. 
IDacrydium vitreum, Dautzenberg, 1927: 

275. 
Dacrydium vitreum, Thorson, 1934: 6. 
Dacrydium vitreum, Johnson, 1934: 28. 
Dacrydium vitreum, Theile, 1935: 798. 
Dacrydium vitreum, Lamy, 1937: 66. 
Dacrydium vitreum. La Rocque, 1953: 38. 
Dacrydium vitreum, Ockelmann, 1959: 48, pi. 

1,fig. 19. 
Dacrydium vitreum, Scarlato, 1960: 61, pi. 1, 

fig. 3. 
Dacrydium vitreum, Soot-Ryen, 1966: 8. 
Dacrydium vitreum, Okutani, 1968: 14, 15, fig. 

Id. 
Dacrydium vitreum, Knudsen, 1970: 90, 92, 

fig. 52A, B. 
Dacrydium vitreum, Abbott, 1974: 436, fig. 

5102. 
Dacrydium vitreum, Mattson & Waren, 1977: 

1-3, figs. 1,2,7. 
Dacrydium vitreum, Bernard, 1978: 62. 
Dacrydium vitreum, Scarlato, 1981: 242, fig. 

141. 
Dacrydium vitreum, Bernard, 1983: 19. 
Dacrydium vitreum, Ockelmann, 1983: 112, 

113, 115, fig. 49. 
Dacrydium vitreum, Hoisaeter, 1986: 115. 
Dacrydium vitreum, Nordsieck, 1989: 29, pi. 

IV, fig. 20.10. 
Dacrydium vitreum. Routiers, 1989: 212, 215, 

fig. 3c. 
Dacrydium vitreum. Smith & Heppell, 1991: 

60. 
Dacrydium vitreum, Waren, 1991: 114, 115, 

fig. 40D-R 
Mytilus vitrea (= Dacrydium vitreum), Schlotte 

& Waren, 1992: 14. 
Dacrydium vitreum. Salas & Gofas, 1997: 

263, figs. 2-6. 
Distribution: W and E Greenland, Baffinland, 

off Nova Scotia, N and E of Iceland, Jan 

Mayen, Spitsbergen, W. Norway south to 

Lofoten Isles, Barents, White and Kara 

Seas, Bering Sea, North of Gulf of 

Alaska, Kamchatka, Sea of Okhotsk. 

Depth range: 5-2258 m, but most fre- 
quently found 5-200 m. 

Dacrydium viviparum Ockelmann, 1983 
Type locality: Ingolf Stas 78, 80, 90, 64°45'N 

29 06'W south to 60°37'N 27 52'W, 

1070-1505 m . 



36 



ALLEN 



Type specimen: Holotype MZUC, paratypes 

BMNH 198335, USNM 822399. 
?Dacrydium vitreum var. elongata Locard, 

1898:364. 
Dacrydium vitreum, Jensen, 1912 (in part): 

56-65. 
Dacrydium sp. b Ockelmann, 1959: 50. 
Dacrydium sp. b Okutani, 1968: 15. 
Dacrydium wV /рашт Ockelmann, 1983: 118, 

120, figs. 52-54, 56, 57. 
Dacrydium viviparum, Waren, 1991 : 115. 
Dacrydium viviparum, Hayami & Kase, 1993: 

48. 
IDacrydium cf. fiyalinum. Salas & Gofas, 

1997:269, figs. 27-32. 
Dacrydium viviparum. Salas & Gofas, 1997: 

269. 
Distribution: West European, Canary and 

North America Basins and possibly 

the Mediterranean. Depth range: 952- 

2430 m. 

Dacrydium wareni Salas & Gofas 1 997 
Type locality: Off northwestern Morocco, 
35°31'N07°42'W, 1510m. 



Type specimen: Holotype MNHMP; paratypes 

SMNH. 
Dacrydium ci. hyalinum, Salas 1996: 53, figs. 

94-96. 
Dacrydium ivaren/ Salas & Gofas 1997: 271, 

figs. 36-43. 
Distribution: Mediterranean off Morocco, Gulf 

of Sirte (JAA pers. obs.); off northwestern 

Spain, West European and Canary Basin. 

Depth range: 395-2018 m. 

Dacrydium zebra Hayami & Kase, 1993 
Type locality: "Devil's Palace," Shimoji Islet, 

Miyako Islands, 24°49.6'N 125°08.2E, 

25 m. 
Type specimen: Holotype UMUT, RM1 9432a; 

paratypes UMUT RM1 9432-41 . 
Dacrydium sp. Kase & Hayami, 1992: 448. 
Dacridium sp. Hayami & Kase, 1993a: 3, 

fig. 7. 
Dacrydium Zebra Hayami & Kase, 1 993b: 46, 

figs. 148-158. 
Distribution: Submarine caves. Sea of Japan. 

Depth range: 12-40 m. 



MALACOLOGIA, 1998, 40(1-2): 37-62 

PHYLOGENY OF STEM-GROUP EUCARDIIDS (BIVALVIA: CARDIIDAE) AND THE 
SIGNIFICANCE OF THE TRANSITIONAL FOSSIL PERUCARDIA. 

JAVA. SCHNEIDER 
Museum of Zoology. University of Michigan, Ann Arbor, Michigan 48109-1079, U.S.A.^ 

ABSTRACT 

Acladistic analysis of stem-group eucardiids produces a phylogenetic hypothesis in which the 
subfamily Profraginae (Aptian [late Early Cretaceous] - Maastrichtian [latest Cretaceous]) is the 
sister taxon to Perucardia (Maastrichtian) + Cenozoic eucardiids. Character analysis of the ra- 
dial ribs and external ornamentation of cardiids indicates that the morphology of the ribs and or- 
nament on Cenozoic eucardiids is the result of fusion of two adjacent ribs. Furthermore, the ra- 
dial ribs and ornament on Perucardia is a mosaic of Cretaceous profragine and Cenozoic 
eucardiid ribbing and ornament. Perucardia may be considered a "transitional fossil," because it 
is morphologically and stratigraphically (Maastrichtian) "intermediate" between profragines and 
Cenozoic eucardiids. 

Key words: cardiids, phylogenetics, paleontology, evolution, homology, Perucardia, Pro- 
fraginae, Profragum. 



INTRODUCTION 

In a preliminary phylogenetic analysis of the 
Late Triassic to Recent bivalve family Cardi- 
idae (Schneider, 1992), it was found that the 
subfamilies Cardiinae, Clinocardiinae, Lym- 
nocardiinae, Fraginae and Tridacninae 
formed a monophyletic group, informally 
dubbed the "eucardiids" (Schneider, 1995). 
Nemocardium + Laevicardiinae formed the 
sister taxon to eucardiids (Schneider, 1992). 
In a detailed analysis of basal cardiids (Tu- 
longocardiinae, Protocardiinae, Lahilliinae, 
Pleuriocardiinae and Laevicardiinae [which 
therein included Nemocardium]; Schneider, 
1995), it was found that the Pleuriocardiinae 
and eucardiids are sister taxa, and together 
are in turn the sister taxon to Laevicardiinae. 
As part of an ongoing study of the evolution- 
ary history of the bivalve family Cardiidae, the 
aim of the present study is to gain an under- 
standing of the morphological evolution of the 
stem-group eucardiids. (Smith, 1994: 94-95, 
provides a lucid discussion of the concepts of 
stem-group and crown-group). For this goal to 
be realized, a robust phylogenetic hypothesis 
for these cardiids must be proposed. 

MATERIALSAND METHODS 

To gain an understanding of the phyloge- 
netic relationships, homologies and morpho- 



logical evolution of stem-group eucardiids, a 
cladistic analysis of 20 taxa with 16 charac- 
ters comprising 52 character states (Table 1) 
was performed using PAUP 3.1.1 (Swofford, 
1993) on a Macintosh Quadra 650 computer. 
The heuristic branch-swapping routine with 
random addition and tree-bisection-reconnec- 
tion options was used. The accelerated trans- 
formation option (ACCTRAN) was used, and 
steps were not added to taxa with polymor- 
phisms (Schneider [1995] discusses these 
options). One character, shell shape (charac- 
ter 2) is ordered on the basis of ontogeny. All 
other characters are unordered. There is no 
ordering of characters based on stratigraphie 
occurrence or morphoclines. Unless other- 
wise indicated (Appendix 1, material exam- 
ined), all coding of characters came from ex- 
amination of specimens. Missing data are 
coded by a question mark ("?"). The results 
are presented in Figures 1 and 2. 

The following abbreviations are used for 
repositories: AMNH, American Museum of 
Natural History; ANSP, Academy of Natural 
Sciences of Philadelphia; DSIRGS, New Zea- 
land Department of Scientific and Industrial 
Research, Geology and Geophysics; GSI, 
Geological Survey of India; IRSNB, Institut 
Royal des Sciences Naturelles de Belgique; 
MACS-RI, Maharashtra Association for the 
Cultivation of Science Research Institute; 
MNHN, Muséum National d'Histoire Naturelle; 



Present address: Department of Geology and Geophysics, 1215 W. Dayton St., University of Wisconsin, r\/ladison, Wis- 
consin 53706, U.S.A. 

37 



38 



SCHNEIDER 



TABLE 1. Data matrix for Cretaceous to Eocene 
cladistic analysis. Missing data indicated by "?". "X" 
indicates taxon polymorphic for states and 1 . 



Pleuhocardia 


XF00000001300110 


Granocardium 


0A00101110101200 


Criocardium 


0B00101110101200 


Ethmocardium 


OAOOIOIOOOIOOOOO 


Profragum 


OGOOOOIOOOIOOOOO 


Indocardium 


0B00100200100020 


Austrocardium 


0D00000200000220 


Perucardia 


7C01102300100100 


Hedecardium 


0K11100001400100 


Agnocardia 


0D11010101400100 


Orthocardium 


0D11110101400100 


Loxocardium 


0E11000001400130 


Schedocardia 


ILlllOOlOllOOlOO 


Sawkinsia 


1?01100101?0??00 


Plagiocardium 


1H11000001100040 


Papillicardium 


1111000001000040 


Parvicardium 


1111000001000040 


Goniocardium 


1J11000001210050 


Avicularium 


1J11000000217051 


Byssocardium 


1J1100000021?0?1 



Key to Abbreviations 



ac 


anterior cardinal 


a! 


anterior length 


als 


anterior lateral socket 


bg 


byssal gape 


cl 


crossed-lamellae 


CS 


cross-sthae 


dh 


dorsal height 


fp 


fibrous prisms 


h 


height 


i 


interspace 


is 


intercalary spine 


isp 


irregular simple prisms 


1 


length 


ml 


midline (line connecting midpoints of 




anterior and posterior adductor muscles) 


pc 


posterior cardinal tooth 


pes 


posterior cardinal socket 


phi 


post-hinge length 


Pl 


posterior length 


pis 


posterior lateral socket 


pit 


posterior lateral tooth 


prt 


primary radial threads 


ps 


primary spine 


r 


rib 


s 


spine 


sc 


scute 


srt 


secondary radial threads 


ss 


secondary spine 


u 


umbo 


vm 


ventral margin 




NHM, The Natural History Museum London; 
NMB, Naturhistorisches Museum in Basel; 
PRI, Paleontological Research Institution; 
PUDG, Purdue University Department of 



Pleuriocardia 
Granocardium 
Criocardium 
Ethmocardium 
Profragum 
Indocardium 
Austrocardium 
Perucardia 
Hedecardium 
Agnocardia 
Orthocardium 
Loxocardium 
Schedocardia 
Sawkinsia 
Plagiocardium 
Papillicardium 
Parvicardium 
Goniocardium 
Avicularium 
1^"^ Byssocardium 

FIG. 1. One of six most parsimonious trees. Syna- 
pomorphies for each node are given in Table 2. 

Geology; UNC, University of North Carolina- 
Chapel Hill, Department of Geology; USNM, 
United States National Museum; UWIGM, 
University of the West Indies Geological 
Museum; YPMIP, Yale Peabody Museum, 
Invertebrate Paleontology Collection. 

(1 ) Selection oflngroup taxa: AW genera and 
subgenera of eucardiids that have any mem- 
bers that are known to have lived at anytime 
from the beginning of the Cretaceous to the 
end of the Eocene are represented in the 
analysis (Appendix 2). If the type species of 
the genus or subgenus occurs during the Cre- 
taceous to Eocene interval, then the type spe- 
cies is used to represent the taxon in the 
cladistic analysis {Criocardium is the one ex- 
ception). The method of representation of 
other cardiid (sub) genera is given in Appen- 
dix 2. 

(2) Selection ofoutgroup: Schneider (1995) 
found that the subfamily Pleuriocardiinae is 
the sister-group to eucardiids. The Pleurio- 
cardiinae is therefore used as the outgroup in 
the present analysis, represented by Pleuho- 
cardia eufaulense (Conrad, 1860). 

Description of Characters and 
Character States. 

1. Posterior margin (Schneider, 1995: fig. 
5): (0) digitate, (1) crenulate. 

2. Shell shape (Fig. 3-5). Cardiids, like 



CARDIID PHYLOGENY: EUCARDIIDS AND PERUCARDIA 



39 




Pleuriocardia 

Granocardium 

Criocardium 

Ethmocardium 

Profragum 

Indocardium 

Austrocardium 

Perucardia 

Hedecardium 

Agnocardia 

Orthocardium 

Loxocardium 

Schedocardia 

Sawkinsia 

Plagiocardium 

Papillicardium 

Parvicardium 

Goniocardium 

Avicularium 

Bvssocardium 





Pleuriocardia 

Granocardium 

Criocardium 

Ethmocardium 

Profragum 

Indocardium 

Austrocardium 

Perucardia 

Hedecardium 

Agnocardia 

Orthocardium 

Loxocardium 

Schedocardia 

Sawkinsia 

Plagiocardium 

Papillicardium 

Parvicardium 

Goniocardium 

Avicularium 

Bvssocardium 




Pleuriocardia 

Granocardium 

Criocardium 

Ethmocardium 

Profragum 

Indocardium 

Austrocardium 

Perucardia 

Hedecardium 

Agnocardia 

Orthocardium 

Loxocardium 

Schedocardia 

Sawkinsia 

Plagiocardium 

Papillicardium 

Parvicardium 

Goniocardium 

Avicularium 

Bvssocardium 



Pleuriocardia 

Granocardium 

Criocardium 

Ethmocardium 

Profragum 

Indocardium 

Austrocardium 

Perucardia 

Hedecardium 

Agnocardia 

Orthocardium 

Loxocardium 

Schedocardia 

Sawkinsia 

Plagiocardium 

Papillicardium 

Parvicardium 

Goniocardium 

Avicularium 

Bvssocardium 




Pleuriocardia 

Granocardium 

Criocardium 

Ethmocardium 

Profragum 

Indocardium 

Austrocardium 

Perucardia 

Hedecardium 

Agnocardia 

Orthocardium 

Loxocardium 

Schedocardia 

Sawkinsia 

Plagiocardium 

Papillicardium 

Parvicardium 

Goniocardium 

Avicularium 

Bvssocardium 



FIG. 2. Remaining five most parsimonious trees. 



40 



SCHNEIDER 



most bivalves, change the shape of their shell 
during ontogeny (Schneider, 1995). The 
structure of a mollusc shell is completely de- 
termined by the temporal process of its devel- 
opment (Wagner, 1994), and therefore the 
molluscan shell can be seen as a record of its 
own growth (Jones, 1983). The ontogenetic 
history of the shell shape of a single specimen 
can usually be traced by examining the 
growth lines. I have found that virtually all 
cardiids pass through at least two discernible 
"states" of shell shape during ontogeny, and 
that the sequence of these shape changes is 
orderly, predictable, and consistent (Table 2). 
Because of accretionary growth of bivalve 
shells, the shape of the shell at time 1 de- 
pends upon the shape of the shell at time 0. 
This is a causal sequence and can be order 
under Alberch's (1985) criterion (Schneider, 
1998). 

Various methods have been proposed to 
deschbe the ontogeny of bivalve shell shape 
(Raup, 1966; Lovtrup & Lovtrup, 1988; 
Checa, 1991; Johnston et al., 1991; Ackerly 
1992a, b). However, a rigorous method of 
converting morphometric information on bi- 
valve ontogeny into cladistic character states 
has yet to be invented. In fact, Bookstein 
(1994) adamantly argues that any attempt to 
link morphometries and systematics would be 
"futile"; that "morphometries cannot supply 
homologous shape characters" (p. 198); that 
biometrics and cladistics are logically, alge- 
braically, and geometrically incompatible; 
and, finally, that "the languages of homology 
and of morphometries are mutually incompre- 
hensible" (p. 224). 

However, shell shape is obviously a herita- 
ble attribute of bivalves, and to exclude shell 
shape in any cladistic analysis of bivalves 
would be at best using an incomplete data 
set in an attempt to propose a phylogen- 
etic hypothesis and at worst a nihilistic exer- 
cise in purposeful ignorance. Therefore, as in 
Schneider (1995), shell shape is considered a 
character, the states of which can be deter- 
mined by using a key. This key is meant to be 
used on adult shells that have attained their 
terminal shape state. However, shell shape 
character states are not solely defined by the 
adult shell shape, but by the ontogenetic path- 
way taken to that terminal (i.e., adult) shell 
shape (Jones, 1983; Wagner, 1994; Mabee & 
Humphhes, 1993). For this reason, Profra- 
gum's (Fig. 3B) terminal shell shape (trigonal) 
is not considered a homologue to other trigo- 
nal terminal shell shapes, for the latter group 



TABLE 2. Shell shape character states detected 
during ontogeny of species considered in the pre- 
sent analysis. Shell shapes are listed in their order 
of ontogenetic appearance. All character analyses 
conducted with specimens in hand, except for 
Granocardium (Granocardium) carolinum and 
Parvicardium (Parvicardium) triangulatum, for 
which illustrations were examined. No shell shape 
character states recognized in any other cardiids 
were detected in Sawkinsia matleyi: therefore this 
species is not listed. 

Pleuriocardia eufaulense: ovate, oblique-ovate 
Granocardium (Granocardium) carolinum: 

quadrate 
Granocardium (Granocardium) kuemmeli: 

quadrate, ovate 
Granocardium (Etiimocardium) whitei: quadrate 
Profragum praecurrens: quadrate, ovate, 

pseudotrigonal 
Indocardium blanfordi: quadrate, ovate 
Austrocardium acuticostatum: circular-ovate, circu- 
lar 
Perucardia brueggeni: ovate, circular-ovate 
Loxocardium obliquum: circular, loxoform 
Hedecardium waitakiense: circular, hedeform 
Agnocardia dissidepictum: circular-ovate, circular 
Orthocardium porulosum: circular-ovate, circular 
Sctiedocardia tiatciietigbeense: circular, schedi- 

form 
Plagiocardium granulosum: circular, oval 
Parvicardium (Papillicardium) ettieridgei: oval, trig- 
onal 
Parvicardium (Parvicardium) triangulatum: oval, 

trigonal 
Goniocardium ractiitis: oval, trigonal, triangular 
Avicularium aviculare: oval, trigonal, triangular 
Byssocardium emarginatum: oval, trigonal, trian- 
gular 



arrive at this shell shape via a different onto- 
genetic pathway. A detailed analysis of the on- 
togeny of Profragum will be published else- 
where, 

Sawkinsia (Fig. 4E), with its double keel 
and concave ventral margin, has a unique 
shell shape in the Cardiidae. I have been un- 
able to discern any of the other cardiid shell 
shape states during its ontogeny. Therefore, 
Sawkinsia's shell shape character cannot fit 
into the character state tree, and is coded as 
missing (?) for this character. 

There are numerous terms that exist to de- 
scribe bivalve shell shape. Many of these shell 
shapes have been figured and given verbal 
definitions by Cox (1969). However, there has 
been no attempt to define bivalve shell shape 
in an objective quantitative or semi-quanti- 
tative manner. Therefore, as in Schneider 



CARDIID PHYLOGENY: EUCARDIIDS AND PERUCARDIA 



41 




FIG. 3. Shell shapes. All figures display external views of right valves. A, Pleuriocardia eufaulense (ANSP 
36491; scale bar = 10 mm); oblique/ovate. B, Profragum praecurrens (GSI 1061 [plaster cast of cotype], 
scale bar = 10mm); pseudotrigonal. C, Plagiocardium granulosum (ANSP 6268; scale bar = 5 mm); oval. D, 
Loxocardium obliquum (FMNH RE 3642; scale bar = 5 mm); loxoform. E, Avicularium aviculare (ANSP 6279; 
scale bar = 5 mm); triangular. F, Hedecardium waitakiense (DSIRGS 10837; scale bar = 10 mm); hedeform. 




FIG 4 Shell shapes. A, external view of right valve of Granocardium kuemmeli (AMNH 45042; scale bar - 10 
mm)- quadrate В external view of left valve of Perucardia brueggeni (PRI 4827 [holotype]; scale in mm indi- 
cated in figure)- circular-ovate. C, external view of left valve of Schedocardia hatchetigbeense (USNM 645087 
[syntype]- scale bar = 10 mm); schediform. D, external view of left valve of Orthocardium porulosum (ANSP 
6266; scale bar = 10 mm); circular. E, external view of left valve of Sawklnsia matleyi (NMB G 14096; scale 
bar = 20 mm). F, external view of right valve of Austrocardium acuticostatum (PUDG 1 62; scale bar = 1 mm); 
circular. 



CARDIID PHYLOGENY: EUCARDIIDS AND PERUCARDIA 



43 




FIG. 5. Determination of shell shape. Goniocardium 
rachitis (ANSP 12429), length (L) = 31 mm. In this 
example, G. rachitis has a carina and PL > (0.6) / 
L, so it has a triangular shell shape. Z' is a line par- 
allel to Z which begins at the posteriormost point 
along line L and ends at line W. Post-hinge length 
(PHL) is the distance from the postehormost point 
of the posterior lateral tooth (pit) to Z'. 



(1 995), shell shape is determined using a shell 
shape character key (Fig. 5). Length (L) is de- 
fined as a line parallel to the line connecting 
the midpoint of the adductor muscles (the mid- 
line, ML) which starts at the antehormost point 
of the shell margin (AL). Height (H) is defined 
as the line perpendicular to L which results in 
the greatest value of dorsal height (DH). Lines 
W and X are the two furthest possible lines 
(dorsal and ventral) parallel to L which contact 
the shell. Apparent height (AH) is the distance 
between W and X. On most shells, AH = H. 
Lines Y and Z are the two furthest possible 
lines (anterior and posterior) parallel to H 
which contact the shell. Apparent length (ApL) 
is the distance between lines Y and Z. In many 
shells, the greatest values of both ApL and L 
will occur along the same line, in which case 
ApL = L. Anterior length (AL) is that portion of 
line L which is anterior of line H; posterior 
length (PL) is that portion of line L which is pos- 
terior of line H; AL -(- PL = L. In this paper, 
"quadrate" = "quadrate-short" of Schneider 
(1995). Also, "quadrate-long" of Schneider 
(1995) is subdivided into "schediform" and 
"loxoform", based on "post-hinge length" 
(PHL), which the length of the shell posterior of 
the posterior lateral teeth of the hinge. 



SHELL SHAPE CHARACTER KEY 

1 . Cahna present 9 

Carina absent 2 

2. Posterior length < anterior 

length oblique-ovate 

Posterior length > anterior length .... 3 

3. H/L > 1 .2 ovate 

1 .1 < H/L < 1 .2 circular-ovate 

H/L < 1.1 4 

4. Apparent height > true height oval 

Apparent height = true height 5 

5. H/L > 1.0 6 

H/L < 1.0 7 

6. ApL > L quadrate 

(= quadrate-short of Schneider, 1995) 

ApL = L circular 

7. ApL>L 8 

(= quadrate-long of Schneider, 1995) 
ApL = L hedeform 

8. PHL < (0.2) X L schediform 

PHL > (0.2) X L loxoform 

9. PL > (0.6) X L triangular 

PL<(0.6)xL 10 

10. Juveniles/early growth 

stages oval trigonal 

Juveniles/early growth stages ovate pseu- 
dothgonal States: (A) quadrate, (B) ovate, (C) 
circular-ovate, (D) circular, (E) loxoform, (F) 
oblique-ovate, (G) pseudothgonal, (H) oval, 
(I) trigonal, (J) triangular, (K) hedeform, (L) 
schediform. 

Character state tree: 

A— B— C— D— E 



-H— I— J 



G 



рК 



3. Underside of anterior and posterior ribs 
(Fig. 6): (0) solid, (1) grooved. 

4. Underside of central ribs (Fig. 6): (0) 
solid, (1) grooved. 

5. Primary radial threads (prt: Fig. 6): (0) ab- 
sent, (1) present. These are raised threads 
that run from the umbo to the ventral margin, 
either along rib tops or in rib interspaces, con- 
necting rows of primary (large) spines. 

6. Rib shape (Fig. 7B): (0) flat/convex, (1) 
concave. 

7. Secondary spines (ss; Fig. 6): (0) absent, 
(1) present over entire shell, (2) present only 
on anterior and posterior slopes of shell. 
(Keen [1980: 13, fig. 6] provides a diagram- 
matic representation of anterior, central and 



44 



SCHNEIDER 



Granocardium 

U (Aptian - Maastrichtian) 





cross section 



В 



г I 



srt A 



Schedocardia 

(Danian - Upper Eocene) 





cross section 



D 



FIG. 6. Schematic diagrams of ribbing and ornamentation, illustrating how the Granocardium-type morphol- 
ogy can give rise to the Cenozoic eucardiid-type morphology by fusion of adjacent ribs. A, B, Granocardium: 
C, D, Cenozoic eucardiids, represented by Schedocardia. External views of shell margins on left, corre- 
sponding cross-sectional views on right. 



posterior slopes.) These are small spines 
which are found in rib interspaces. 

8. Secondary radial threads (srt; Fig. 6): (0) 
absent, (1) present over entire shell, (2) pres- 
ent on posterior slope only, (3) present on 



anterior and posterior slopes. These are 
raised threads which run from the umbo to the 
ventral margin, always in rib interspaces, 
often connecting rows of small (secondary) 
spines. 



CARDIID PHYLOGENY: EUCARDIIDS AND PERUCARDIA 



45 




1л A 




FIG. 7. A, schematic diagram of the ventral margin 
of a shell of a hypothetical eucardiid. Primary 
spines are on top of ribs. Cross-striae are in inter- 
spaces. B, Cross-section of a eucardiid with "con- 
cave" ribs. The ribs are wide and the rib tops are 
low, only slightly higher than the interspaces. Com- 
pare with Fig. 6D. 



9. Intercalary ribs (Fig. 6): (0) absent, (1) 
present. These are radial ribs that occur be- 
tween two rows of secondary spines. 

10. Cross-striae (cs) are concentric raised 
threads in rib interspaces (Fig. 7A): (0) cross- 
striae absent, (1) cross-striae present. 

11. Primary spines. 

(0) Absent (Fig. 4F). 

(1) Simple. External morphology: circular to 
subcircular knobs (Figs. 4A, 8). Micro- 
structure: crossed-lamellar structure at 
base grading upward to fibrous prismatic 
structure with crossed lamellar structure 
distally; microstructurally continuous with 
shell (Fig. 9). 

(2) Scutes (sc): External morphology: curved 
plates, width several times greater than 
height (Fig. 10). 

Microstructure: predominantly branching 
crossed lamellar structure at base, with 
local inclined complex crossed lamellar to 
fibrous prismatic structure distally (to- 
wards tip of scute): microstructurally con- 
tinuous with shell (Schneider, 1998: fig. 
17). 

(3) Non-imbricated concave-down triangles. 
External morphology: see Schneider 
(1995: fig. 8C, D, F, G). Microstructure: un- 
known (Schneider, 1995: 334). 

(4) Complex. External morphology: knobs or 
imbricated concave-down triangles (Fig. 
IIA). Microstructure: predominantly fi- 
brous prisms, microstructurally separated 
from shell by basal layer of irregular sim- 
ple prisms (ISP) (Fig. IIB, С). 

(5) Composite (Schneider, 1998): External 
morphology: small circular knobs. Micro- 




FIG. 8. External ornamentation of right valve of Pro- 
fragum praecurrens (GSI 1061). A, ventral margin. 
Scale bar = 5 mm. B, central slope. Scale bar = 1 .88 
mm. Note presence of secondary spines (example 
indicated by arrow) and absence of cross-striae. 



structure: outer portion of spine like state 
1), inner portion of formed entirely of fi- 
brous prisms, microstructurally separate 
from rest of shell, but basal irregular sim- 
ple prismatic layer lacking (Schneider, 
1998: fig. 21). 
(6) Fibrous prisms: External morphology: 
subcircular, wider than high (Schneider, 
1998: figs. 19, 20). 

Microstructure: spine entirely of fibrous 
prisms which are microstructurally sepa- 
rate from shell, no basal layer of irregular 
simple prisms (Schneider, 1998: fig. 18). 

Because all body fossils of all species of 
Sawkinsia are recrystallized, the microstruc- 
ture of the spines is unknown. Therefore, 
Sawkinsia is coded missing (?) for character 
11. 

12. Adductor muscle scar shape and loca- 
tion (Fig. 12): (0) anterior and posterior ad- 



46 



SCHNEIDER 




FIG. 9. Radial sections through shells of pro- 
fragines. A, section through a portion of the middle 
of a rib of a Profragum praecurrens (UNC 15564, 
right valve). Ventral margin is at left, the direction of 
the umbo would be to the right. Note microstructural 
continuity of ornament with underlying shell. Scale 
bar = 1 mm. B, section through a portion of the mid- 
dle of a rib of a Granocardium kuemmeli (AMNH 
45043, right valve), displaying microstructural rela- 
tionships of primary spine to underlying shell. Di- 
rection of the ventral margin would be to the left, di- 
rection of the umbo would be to the right. Scale bar 
= 1 mm. 



FIG. 10. Byssal gapes and scutes. A, Posterior of 
right valve of Goniocardium rachitis (ANSP 12429; 
scale bar = 5 mm.). Byssal gape absent. B, poste- 
rior of right valve of Aviculahum aviculare (ANSP 
6279; scale bar = 5 mm.). Byssal gape present. C, 
posterior of left valve of Byssocardium emargina- 
tum (IRSNB I.G. 10591 ; scale bar = 5 mm.). Byssal 
gape present. 



RESULTS 



ductor muscle scars equal in size, equally dis- 
tant from shell margin, (1) posterior adductor 
muscle scar larger and located further from 
shell margin. 
See Figures 1 3- 1 6 for characters 13-15. 

13. Left anterior lateral socket (als): (0) ab- 
sent/weak, (1) moderate. 

14. Left posterior lateral socket (pis): (0) ab- 
sent/weak, (1) moderate, (2) large. 

15. Right anterior cardinal (ac) shape. 
States to 5. (In Schneider 1995, figs. 17B 
and 17C were erroneously reversed, fig. 17B 
is Pleuriocardia eufaulense; fig 17C is Gra- 
nocardium kuemmeli.) 

16. Byssal gape (bg; Fig. 10): (0) absent, 
(1) present. 



PAUP 3.1.1 found 6 most parsimonious 
trees with a length of 54 steps (Figs. 1,2). The 
consistency index (CI) = 0.741 and the reten- 
tion index (Rl) = 0.851. Synapomorphies for 
the internal nodes for one of the six trees are 
indicated in Table 3. 

The subfamily Profraginae, members of 
which are known only from the Cretaceous 
(Table 4), is the sister taxon to Perucardia + 
Cenozoic eucardiids. Profraginae is united by 
the presence of secondary spines (7:1) and 
an absent or weak left posterior lateral socket 
(15:0). 

Granocardium and Criocardlum are sister 
taxa and differ only in shell shape (character 
2). For this and other reasons it is recom- 
mended that Criocardlum be considered a 




FIG. 1 1 . Ornamentation of Agnocardia dissidepictum (ANSP 1 1 035). A, external view of posterior of left valve. 
Note rows of imbricated concave-down triangular spines (s). Scale bar = 10 mm. B, radial section through a 
portion of a rib and spine, scale bar = 0.1 mm. Direction of umbo to the right; direction of ventral margin to 
the left. C, close-up of ISP layer between fibrous prismatic (FP) spine and crossed lamellae (CL) CL of un- 
derlying shell, scale bar = 0.01 mm. 



48 



SCHNEIDER 



anterior 
adductor 



anterior 
adductor 




FIG. 12. Camera lucida drawings of interior of right valves. Scale bars equal 10 mm. A, Gonlocardium rachi- 
tis (ANSP 12429); B, Avicularium aviculare (ANSP 6279); C, Byssocardium emarginatum (IRSNB I.G. 
10591). 



subjective junior synonym of Granocardium 
(Appendix 3 for a discussion of the Grano- 
cardium/Chocardium taxonomic problem). 

The two characters that unite Perucardia 
with Cenozoic eucardiids are shell shape (2:2) 
and the presence of central ribs with grooved 
undersides (4:1). Cenozoic eucardiids (united 
at node 8) share shell shape (2:3), presence of 
cross-striae (10:1), and anterior and posterior 
ribs that have grooved undersides (3:1). 
Loxocardium, Orthocardium, Agnocardia, and 
Hedecardium (the Orthocardium -дюир) are 



united by the possession of ornament with a 
basal ISP layer (11:4) and Orthocardium and 
Agnocardia are united by concave ribs (6:1) 
and presence of striations across the entire 
shell (8:1). The Orthocardium-group is the sis- 
ter taxon to other Cenozoic eucardiids, which 
are united (node 11) by a crenulate posterior 
margin (1:1). 

Plagiocardium and Parvicardium were con- 
sidered to be members of the Fraginae by 
Kafanov & Popov (1977) and Schneider 
(1992). In the present study, Plagiocardium is 




FIG. 13. Stereo electron micrographs of cardinal area of right hinges. A, Pleuriocardia eufaulense (ANSP 
36491; scale bar = 2 mm.). Same as Fig. 17B (NOT 17C) in Schneider (1995). Antenor cardinal shape 1. B, 
Loxocardium obliquum (FMNH PE 3642; scale bar = 2 mm.), anterior cardinal shape 3. C, Plagiocardium 
granulosum (ANSP 6268; scale bar = 2 mm.), antenor cardinal shape 4. 



SCHNEIDER 





FIG. 14. Hinges. A, В. Stereo photographs of hinge of Granocardium kuemmelli. A, right valve (AMNH 
45046); B, left valve (AMNH 45048); als moderate, pis large. Scale bars = 10 mm. C, left hinge of Schedo- 
cardia hatchetigbeense (USNM 645087 [syntype]; scale bar = 10 mm); als weak, pis moderate. 



found to be the basal member of a clade con- 
sisting of Papillicardium, Parvicardium, and 
the three tridacnines {Goniocardium, Avicu- 
larium and Byssocardium). This clade is united 
by shell shape (2:H), loss of rib thread (5:0), 
primary spine structure (11:2), an absent or 
weak left posterior lateral socket (14:0) and 
shape of right anterior cardinal (15:4). 



Papillicardium has usually been considered 
a subgenus of Parvicardium (Keen, 1969, 
1980; Voskuil & Onverwagt, 1989) or a close 
relative thereof (Kafanov & Popov, 1977). 
These two taxa are sister taxa in three of the 
six most parsimonious trees; in the other 
three trees they form a trichotomy with the tri- 
dacnines. 



CARDIID PHYLOGENY: EUCARDIIDS AND PERUCARDIA 



51 




FIG. 15. Hinge stereo photographs and electron micrographs. A, right valve of Granocardium kuemmeli 
(AMNH 45046, scale bar = 2 mm.). Same as Fig. 17C (NOT 17B) in Schneider (1995), anterior cardinal 
shape 0. B, right valve of Austrocardium acuticostatum (PUDG 162, scale bar = 12 mm.), anterior cardinal 
shape 2. 



DISCUSSION 

From their appearance in the Norian (Late 
Triassic) through the Neocomian (Early 
Cretaceous), cardiids either have simple, un- 
ornamented ribs or have lost the ribs entirely 
(Schneider, 1995; figs. 7, 11). In the Early 
Cretaceous, cardiids with spines upon their 
ribs appear in the fossil record. Nemocardlum 
has round spines atop its posterior radial ribs 
(Schneider, 1995: figs. 8A, 9C, D). On the 
profragine Granocardium (Figs. 4A, 6A, B), 



there is a row of large spines with a rib on ei- 
ther side of the large spine. These rows of 
large spines are followed by one to three rows 
(variable not only within a species, but within 
an individual [Stephenson, 1941, 1955; Scott, 
1978; personal obs.]) of small spines, which 
are also between ribs. The two size classes of 
spines are herein termed primary (for the 
larger spines) and secondary (for the smaller 
spines). The space between ribs is called the 
interspace. Running down the middle of the 
rows of both the primary and secondary spines 



52 



SCHNEIDER 




FIG. 16. Hinge stereo photographs of Goniocardium rachitis (ANSP 12429). A, right valve, scale bar = 4 mm. 
Anterior cardinal shape 5. B, left valve, scale bar = 2 mm; als absent, pis weak. 



are fine raised threads, herein called radial 
threads. The ribs are narrow and solid under- 
neath; this is also the condition found in all 
Protocardiinae, Laevicardiinae, and the out- 
group taxon Pleurlocardia. On Granocardium, 
interspaces bearing rows of primary spines 
are raised slightly higher than the interspaces 
bearing rows of secondary spines. At the ven- 
tral margin, ribs extend further than the inter- 
spaces. The rows of secondary spines are not 
manifested by marginal serrations at the com- 
misure. 
When the character states of the primary 



and secondary spines, their respective 
threads, ribs, and interspaces are analyzed 
throughout the Cardiidae, it becomes appar- 
ent that in the evolution of Cenozoic eucardi- 
ids, two adjacent radial ribs have fused into a 
single radial rib. On Cenozoic cardiids (Fig. 
6C, D), the primary spines and their radial 
threads are not between ribs, but on top of 
them. The ribs are wide and flat-topped. The 
primary spines and radial threads are on top 
of wide ribs that are grooved underneath. On 
some forms, there are threads, not associated 
with any spines, in the interspaces. Appar- 



CARDIID PHYLOGENY: EUCARDIIDS AND PERUCARDÍA 



53 



TABLE 3. Synapotnorphies for interior nodes. 
Nodes numbered as in Figure 1. 



Node 

1 

2 

3 

4 

5 

6 

7 

8 

9 

10 
11 
12 
13 
14 
15 
16 
17 



Synapomorpinies (character:state) 

2:B, 5:1, 10:0, 11:1, 15:0 

14:0 

7:1 

2:A 

8:1,9:1, 13:1, 14:2 

8:2, 15:2 

2:C, 4:1 

2:D, 3:1, 10:1 

11:4 

6:1,8:1 

1:1 

2:L, 8:1 

2:H,5:0, 11:2, 14:0, 15:4 

2:1 

11:5 

2:J, 12:1, 15:5 

10:0, 16:1 



TABLE 4. Stratigraphie ranges of cardiid genera 
and subgenera represented in the present analysis. 
Except where noted, stratigraphie ranges from J. J. 
Sepkoski Jr.'s unpublished compendium of marine 
invertebrate stratigraphie ranges. Abbreviations of 
stratigraphie units from Harland et al. (1990). 



Paleuriocardia 
Granocardium 

( Granocardium) 
G. {Ethmocardium) 
Profragum 

Indocardium 

Austrocardium 

Perucardia 
Hedecardium 

(Hedecardium) 
Agnocardia 
Orthocardium 
Loxocardium 
Sawkinsia 
Schedocardia 
Plagiocardium 
Papillicardium 
Parvicardium 
Goniocardium 

Avicularium 
Byssocardium 



Alb- 
Alb- 



laa 
laa 



Cmp-Maa 

Alb-Maa (Badve, 1977; 

Schneider, unpubl.) 
Alb-Cmp (Chiplonkar & 
Badve, 1976) 
Cmp-Maa (Schneider, 

unpubl.) 
Maa 
Brt-Aqt (Schneider, 

unpubl.) 
Ypr-Zan 
Tha-Ypr 
Dan-Mio 

Brt-Prb (Jung, 1976) 
Dan-Prb (Keen, 1980) 
Dan-Mio 
Eoc-Hol 
Eoc-Hol 
Lut-Rup (Schneider, 

1998) 
M. Eoc.-Rup. 
M. Eoc.-L. Mio. 



ently, the radial threads on the ribtops on 
Cenozoic cardiids are homologous to the 
primary radial threads of Granocardium, 
whereas the radial threads in the interspaces 
on Cenozoic cardiids are homologous to sec- 



ondary radial threads of Granocardium. At the 
ventral margin, the rib sides extend further 
than both the rib tops and the interspaces. 

If the rib pattern of the Cretaceous Grano- 
cardium is compared with those of Cenozoic 
eucardiids, it appears that the interspace 
bearing the primary spine on Granocardium — 
and this interspace is raised relative to other 
interspaces — is homologous to the rib top 
of Cenozoic eucardiids. On Cretaceous cardi- 
ids, the ribs are narrow and solid underneath, 
whereas on Cenozoic eucardiids, the ribs 
are wide and grooved underneath. Appar- 
ently, the individual ribs on Granocardium 
are homologous to the sides of the ribs on 
Cenozoic eucardiids. Some Cenozoic eu- 
cardiids even have a furrow running down the 
tops of the ribs, or have concave ribs. This 




FIG. 17. Details of ribbing and ornamentation mor- 
phology of Perucardia brueggeni (PR! 4827 [co- 
type]). Scales indicated in mm in figures. A, anterior 
slope of left valve. B, posterior slope of left valve. 
On anterior and postenor slopes, rows of large 
spines are separated by one or two rows of small 
spines similar to the ornamentation pattern of the 
Cretaceous profragine Granocardium (Fig. 6A, B). 



54 



SCHNEIDER 



.У 



): 



ш 




FIG. 18. Perucardia brueggeni, detail of ribbing and 
ornamentation morphology on ventral margin of 
central slope of right valve (PRI 4829 [paratype]; 
scale bar = 5 mm. Spines occur on top of wide ribs 
that are grooved underneath, as on Cenozoic eu- 
cardiids (Fig. 6C, D). 



furrow is apparently homologous to the rib 
interspace, with the sides of the ribs being 
homologous to single ribs in Cretaceous 
cardiids. 

Perucardia is intermediate in morphology 
between Cretaceous eucardiids and Ceno- 
zoic eucardiids. Perucardia is known from a 
few specimens from Maastrichtian sediments 
of Peru, Colombia, and Venezuela (Olsson, 
1944). The ribs on the central slope of Peru- 
cardia (Fig. 18) are as in Cenozoic eucardiids, 
with spines on top of wide ribs, whereas the 
anterior and posterior slopes (Fig. 17) are as 
in Cretaceous eucardiids, with rows of sec- 
ondary spines between rows of primary 
spines. These primary spines on the anterior 
and posterior slopes may be described as 
being on top of adjacent ribs with a very nar- 
row interspace in between them; the two ribs 
have nearly "fused" into a single rib. 

Perucardia is both morphologically and 
stratigraphically intermediate between Creta- 
ceous and Cenozoic eucardiids (Fig. 19). 
Cladistically, rib fusion is manifested by the 
presence of ribs on the central slope that are 
grooved underneath (4:1), the character that 
unites Perucardia with Cenozoic cardiids. Pe- 
rucardia shares the primitive state of anterior 
and posterior ribs that are solid underneath 
(3:0) with Cretaceous cardiids. One of the 
characters that unites Cenozoic cardiids is 
anterior and posterior ribs that are grooved 
underneath (3:1). This means that there were 



at least two episodes of rib fusion in the eu- 
cardiid lineage (Fig. 17 arrows). First, adja- 
cent radial ribs on the central slope fused {Pe- 
rucardia: arrow A). Subsequently, adjacent 
ribs on the distal slopes fused (Cenozoic eu- 
cardiids; arrow B). The lineage of cardiids with 
fusion of only the central ribs became extinct 
in the Maastrichtian with the demise of Peru- 
cardia, whilst the lineage that further under- 
went fusion of the more distal sets of ribs 
diversified (Fig. 19). A seemingly more com- 
plicated scenario would be that Perucardia 
represents one lineage that underwent rib fu- 
sion along on the distal slopes; whilst the 
Cenozoic eucardiids are a separate lineage 
that underwent rib fusion across the entire 
shell. In any event, the above statement that 
there were at least two episodes of rib fusion 
within the eucardiid lineage is accurate. 

Gabb (1869), who erected Granocardium, 
and Weiler (1907), are the only workers I 
know of who have previously recognized the 
similarity of the rows of primary spines in the 
interspaces of a species of Granocardium to 
the rib tops of most Cenozoic cardiids. Gabb 
described Granocardium as having two series 
of radial ribs, with the "larger" ribs bearing 
spines. However, Gabb did not recognize the 
homology between the sides of the "larger" 
ribs and a single "smaller" rib. Neither did 
Gabb perceive that the tops of the "larger" ribs 
were homologous to interspaces (Appendix 
3). In describing Granocardium l<uemmeli 
(Weiler, 1907) (the representative of Criocar- 
dium in the present analysis), Weiler (pp. 
586-7) writes, 

Each third interspace is occupied by a row of strong 
and thick spines . . . their bases occupying the en- 
tire width of the furrow, in which case the two 
bounding costae with the row of spines rising from 
the intervening furrow, appear to form altogether, 
one broad rib supporting a row of strong spines . . . 
In some specimens the bases of the larger spines 
or nodes are confluent and appear to fill the inter- 
space occupied by them, so that the two bounding 
costae with the row of spines together seem to con- 
stitute a single broad rib crowned with a rib of strong 
nodes . . . 

Weiler (p. 587) then goes on to write, 

. . . the surface of the shell is apparently marked 
by radiating rows of tubercles which apparently do 
not rise from interspaces between costae, but di- 
rectly from the surface. 

Weiler recognized that at on least one 
species of Cretaceous cardiid, the ribbing pat- 



CARDIID PHYLOGENY: EUCARDIIDS AND PERUCARDIA 

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55 






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FIG. 19. Phylogenetic relationships of basal eucardiids plotted against geologic time. Time scale and abbre- 
viations from Harland et al. (1990), 



tern approached that of most Cenozoic cardi- 
ids. However, with Perucardia yet to be col- 
lected, Weiler couid not go further in recog- 
nizing the implications of G. kuemmelis 
morphology for determining homologies and 
reconstructing phylogenetic history of the 
Cardiidae. 

Cardiid diversity and evolution during the 
Cretaceous to Eocene interval has been been 
misinterpreted not only by failing to recognize 
proper rib and ornamentation homologies, but 
by erroneously assigning numerous species 
of Cretaceous cardiids to genera otherwise 
known only from the Oligocène to Recent (Ap- 
pendix 2). These generic assignments were 
based on superficial resemblances, usually 
shell shape. This situation is not dissimilar to 
that of flowering plants (angiosperms). For 
decades Cretaceous angiosperms were as- 
signed to extant genera and families primarily 
on the basis of leaf outline, without taking into 



consideration any other characters, such as 
internal venation of the leaves (Doyle & 
Hickey, 1976; Hickey & Doyle, 1977). There- 
fore, the evolutionary history of flowering 
plants was erroneously interpreted as rapid 
diversification in the Cretaceous with little ex- 
tinction and diversification since then (Doyle, 
1978). 

Cardiid evolution has likewise been misun- 
derstood, although not to the degree as in an- 
giosperms. Keen (1 969, 1 980) and Kafanov & 
Popov (1977) rejected all records of pre- 
Oligocene species of Cardium s.S., Bucar- 
dium, Acanthocardia {Acanthocardia), and 
Fragum. However, Keen (1969, 1980) consid- 
ered (1) Perucardia to be a subgenus of 
Vepricardium, and (2) the Late Cretaceous 
pleuriocardiine Incacardiumto be a subgenus 
of Acanthocardia, thus giving Vepricardium 
and Acanttiocardia stratigraphie ranges of 
Late Cretaceous to Recent. Keen (1969, 



56 



SCHNEIDER 



1 980) also considered all Cretaceous eucardi- 
ids, as well as the Norian (Late Thassic) anom- 
alodesmatan Septocardia (Schneider, 1995: 
322) as members of the subfamily Cardiinae. 

The case of Profragum deserves special at- 
tention. Stoliczka (1871) erected the species 
Fragum praecurrens for some fossils from the 
Cretaceous of India. Badve (1977) erected the 
subfamily Profraginae and the genus Pro- 
fragum for this one species. On the basis of its 
adult shell shape, strong carina, and alleged 
cross-striae, Badve thought that Profraginae 
was closely related to Fraginae. Badve dis- 
cusses and figures strong cross-striae on the 
interspaces of the type specimen of Fragum 
praecurrens. Cross-striae are present in most 
fragines (Keen, 1951, 1969, 1980). However, 
examination of the type specimen of Fragum 
praecurrens shows that the sculpture on the 
interspaces is not cross-striae but secondary 
spines, as in the Cretaceous Granocardium 
(Figs. 4A, 9). The only Cretaceous cardiids 
that have cross-striae are the pleuriocardiines 
(Schneider, 1995); cross-striae are absent on 
the Cretaceous taxa Granocardium, Indo- 
cardium, and Austrocardlum. Furthermore, 
Profragum's ornamental microstructure is the 
same as that of Granocardium (Fig. 9) and not 
at all like that of Fragum (Schneider, 1 998: fig. 
18). Freneix (1956, 1957; Dartevelle & Fre- 
neix, 1957) assigned several other Creta- 
ceous cardiids to Fragum (Table 5). Although 
microstructural work has yet to be done on 
these species, their hinge and ornamentation 
characters are clearly those of Profragum, and 
not Fragum. 

Diversity of eucardiid subgenera using the 
taxonomy advocated in Table 4 is plotted in 
Figure 20. 

CONCLUSIONS 

A phylogenetic analysis of stem-group eu- 
cardiid bivalves produces a phylogenetic hy- 
pothesis that the Cretaceous subfamily Pro- 
fraginae is the sister taxon to Perucardia + 
Cenozoic eucardiids. The Maastrichtian (lat- 
est Cretaceous) Perucardia displays a mosaic 
of profragine primitive characters and Ceno- 
zoic eucardiid derived characters. 

The subfamily Cardiinae is a paraphyletic 
grade, not a monophyletic group. Cretaceous 
taxa belong to the Profraginae, which became 
extinct at the end of the Cretaceous. The Or- 
thocardium-group is the sister taxon to the re- 
maining eucardiids in the analysis, with Sche- 



TABLE 5. Species of Cretaceous cardiids referred 
to Fragum by Freneix. These species are herein 
considered members of the genus Profragum, 
except for Cardium pulchrum, which is considered a 
species of Granocardium. Unless otherwise indi- 
cated, assignments by Freneix were made in 
Dartevelle & Freneix (1957). 



Cardium amotapense Olsson, 1934 




Cardium cerevicianum Pasic, 1951 




Cardium perobliquum Koenen, 


(Freneix, 


1897 


1957) 


Fragum praecurrens Stoliczka, 




1871 




Cardium pulciirum Bruggen. 1910 




Cardium subperobliquum 


(Freneix, 


Riedel, 1932 


1956, 1957) 




FIG. 20. Eucardiid diversity from the Lower Cre- 
taceous Aptian stage through the Eocene. 

docardia + Sawkinsia the sister group to {{Pla- 
giocardlum (Fraginae -t- Tridacninae)). 

The origin of Cenozoic eucardiids is marked 
by the evolutionary innovation of fusion of ad- 
jacent radial radial ribs into a single rib. The 
ribs on Cretaceous cardiids are homologous 
to the sides of ribs on Cenozoic eucardiids, 
and the interspaces of Cretaceous eucardiids 
are homologous to Cenozoic eucardiid rib 
tops. The Maastrichtian taxon Perucardia Is 
morphologically and stratigraphically interme- 
diate between Cretaceous eucardiids on one 
hand, and Cenozoic eucardiids on the other. 
There were at least two episodes of hb fusion 
in the eucardiid lineage. 

ACKNOWLEDGEMENTS 

I would like to thank the following people and 
institutions for permission to examine and bor- 



CARDIID PHYLOGENY: EUCARDIIDS AND PERUCARDIA 



57 



row specimens from their collections: G. 
Rosenberg, E. Benamy (ANSP); T. R. Waller, 
W. Blow, F. Collier, J. Thompson (USNM); N. 
Morris, R. Cleevely (NHM); W. D. Alimón, R 
Hoover (PRI); Y. Gayrard, S. Freneix (MNHM); 
G. Buckley, S. Lidgard (FMNH); P Jung, R. 
Panchaud (NMB); A. Beu, I. W. Keyes 
(DSIRGS); K. R. Chowdhury (GSI); R. M. 
Badve (MACS-RI); A. Dhondt (IRSNB); W. J. 
Zinsmeister (PUDG). Financial support for this 
project came from the Jessup Fund of the 
Academy of Natural Sciences of Philadelphia, 
Western Society of Malacologists, Santa 
Barbara Shell Club, National Capital Shell 
Club, Lerner-Gray Foundation of the American 
Museum of Natural History, Sigma Xi, 
Conchologists of America, The Paleontol- 
ogical Society, the Hinds Fund of the Uni- 
versity of Chicago, and the Gurley Fund of the 
University of Chicago. During my graduate 
study at the University of Chicago I was sup- 
ported by a grant from the National Science 
Foundation (EAR-90-05744) to D. Jablonski. 
D. Jablonski, R. Bieler, M. LaBarbera, J. J. 
Sepkoski, Jr., P. Sereno, J. B. С Jackson, T 
R. Waller and G. Paulay reviewed the manu- 
script, and P. W. Wagner III, D. Miller, K. Roy, 
and D. Fischer offered advice and criticism. 



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Cretaceous) fossils from Crowley's Ridge, south- 
eastern Missouri. Geological Survey Profes- 
sional Paper 274-E: 97-139. 

STEWART, R. В., 1930, Gabb's California 
Cretaceous and Tertiary type lamellibranchs. 
Academy of Natural Sciences of Philadelphia 
Special Publication. 3: 314 pp. 

STOLICZKA, F, 1871, Cretaceous fauna of south- 
ern India, Volume III, The Pelecypoda, with a re- 
view of all known genera of this class, fossil and 
Recent. Paleontología Indica, series 6, 3: 537 pp. 

SWOFFORD, D. L., 1993, PAUP: Phylogenetic 
analysis using parsimony, version З.1.1., D. L. 
Swofford, Smithsonian Institution. 

VIDAL, J., 1997, Large Trachycardiinae from the 
Indo-West Pacific: the group of Vasticardium ór- 
bita (Broderip & Sowerby, 1833) (Mollusca, 
Cardiidae). Molluscan Research. 18: 11-32. 

VOKES, H. E., 1984, Notes on the genus Agnocar- 
dia (Mollusca: Cardiidae) with the description of a 
new species from the Pliocene of Florida. Tulane 
Studies in Geology and Paleontology. 1 8: 37-45. 

VOKES, H. E., 1989, Neogene paleontology in the 
northern Dominican Republic, 9, The family 
Cardiidae (Mollusca: Bivalvia). Bulletins of Amer- 
ican Paleontology. 97: 95-181. 

VOSKUIL, R. R A. & W. R H. ONVERWAGT, 1989, 
Inventarisation of the Recent European and west 
African Cardiidae (Mollusca, Bivalvia). Gloria 
Maris. 28: 49-86. 

WAGNER, G. R, 1994, Homology and the mecha- 
nisms of development. Pp. 274-299, in: в. к. 
HALL, ed.. Homology. The Hierarchical Basis of 
Comparative Biology New York, Academic Press. 

WELLER, S., 1907, A report on the Cretaceous pa- 
leontology of New Jersey. Geological Survey of 
New Jersey, Paleontology Series, 4: 1071 pp. 

Revised ms. accepted 15 Jan. 1998 

APPENDIX 1 

Material examined. Numbers in parentheses 
indicates number of specimens examined. 

Pleuriocardia eufaulense (Conrad, 1860): 
ANSP 19597 (1, holotype), 36491 (7); 
AMNH 45040 (1), 45041 (1), 45071 (1); 
FMNH 18647 (2); USNM 20847 (1). 



CARDIID PHYLOGENY: EUCARDIIDS AND PERUCARDIA 



59 



Granocardium (Granocardlum) carolinum (Or- 
bigny, 1844): Data from Orbigny (1844). 

Granocardium (Granocardium) kuemmeli 
(Weiler, 1907): USNM 21126 (1, holo- 
type); AMNH 45042 (1 ), 45043 (1 ), 45044 
(1), 45045 (1), 45046 (1), 45047 (1), 
45048 (1); ANSP 36475 (5); YPM 
IP025574(1). 

Granocardium (Ethmocardium) whitei (Dal I, 
1900): USNM 315529 (1, holotype), 
USNM 2871 (1 ); AMNH 9402 (1 ), 27846 
(1); ANSP 36948 (20); YPM IP032009 
(1), IP.032010 (50), IP.032636 (20), 
IP032662 (20), IP.031422 (50). 

Profragum praecurrens (Stoliczka, 1871): 
GSI 1060 (1, plaster cast of cotype), 
1061 (1, plaster cast of cotype); UNC 
15564(20). 

Indocardium blanfordi Chiplonkar & Badve, 
1976: MNHN 9665 (2). Additional data 
from Chiplonkar & Badve (1976). 

Austrocardium acuticostatum (Orbigny, 
1842): PUDG 162 (7); MNHN 5697 (1, 
plaster cast of lectotype). 

Perucardia brueggeni Olsson, 1944: PR! 
3732 (1, hypotype), 4827 (1, cotype), 
4827a (1, paratype), 4828 (1, paratype), 
4829 (1, paratype), 4830 (1, cotype), 
4831 (1, paratype). 

Loxocardium obliquum (Lamarck, 1805): 
ANSP 6269 (1), 6970 (1), 7667 (5); 
FMNH PE3642 (144), PE3606 (2), 
PEÍ 7386 (7). 

Hedecardium waital<iense (Suter, 1907); 
DSIRGS 10837(3). 

Agnocardia dissidepictum (Woodring, 1925): 
USNM 352819 (1, holotype); ANSP 
11035(1). 

Orttiocardium porulosum (Solander, 1766); 
ANSP 6266 (4); AMNH 3091 (1); FMNH 
UC 24932 (5); YPM IP006880 (1). 

Sawl<insia matleyi Cox, 1941;NHM L74121 
(1, holotype), NHM L74764 (1, hypo- 
type), L 741 13(1, hypotype), L 74763(1, 
hypotype); NMB G 14089 (1, hypotype), 
NMB G 14091 (1, hypotype), NMB G 
14093 (1, hypotype), NMB G 14094 (1, 
hypotype); UWIGM 1152 (3), 1154 (1). 

Sciiedocardia hatclietigbeense (Aldrich, 
1886); USNM 638802 (1, syntype), 
645087 (1, syntype); ANSP 5420 (1), 
8687(1), 8756(3). 

Plagiocardium granulosum (Lamarck, 1805); 
ANSP 6268 (14), 7663(1). 

Parvicardium (Papillicardium) ettieridgei 
(Tremlett, 1950): NHM L 80479 (1, holo- 
type). 

Parvicardium (Parvicardium) triangulatum 



(Laubrière, 1881); Data from Laubrière 

(1881). 
Goniocardium raciiitis (Deshayes, 1829): 

ANSP 12429 (6); FMNH PE3624 (2). 
Avicularium aviculare (Lamarck, 1 805): ANSP 

6279 (3). 
Byssocardium emarginatum (Deshayes, 

1829); IRSNBI.G. 10591 (4). 

APPENDIX 2 

A. Taxa represented by a non-type species or 
a post-Eocene species. 

(1 ) ¡Hedecardium. The only Eocene species 
are /-/. co///ns/ Marwick, 1960, and /-/. brunneri 
(Hector, 1886). Although these two species 
are identifiable as ¡Hedecardium. the material 
is fragmentary and the hinge is unknown 
(Marwick, 1944). The type species, the Oligo- 
cène ¡H. waitaf<iense (Suter, 1907), is known 
from well-preserved specimens (Marwick, 
1944; Beu & Maxwell, 1990) and is chosen to 
represent this taxon. 

(2) PapiHicardium. The type species is the 
Middle Miocene to Recent Papillicardium pa- 
pillosum (Poli, 1791). The Eocene P. 
ef/?enc/ge/ (Tremlett, 1950) is chosen to repre- 
sent Papillicardium. 

(3) Parvicardium. The type species is the 
Recent Parvicardium siculum (Sowerby, 
1841). The Eocene species Parvicardium tri- 
angulatum (Laubrière, 1881) is selected to 
represent this taxon. 

(4) Criocardium. The type species is 
Cardium (Criocardium) dumosum Conrad, 
1871. Cardium kuemmeli Weiler, 1907, is 
used to represent Criocardium, because there 
is more and better preserved material. In 
erecting С kuemmeli, Weiler (p. 586) stated 
that "the species exhibits clearly the charac- 
teristics of the subgenus Criocardium." Weiler 
also stated that numerous specimens of this 
species were already in the collections of the 
USNM, labeled Cardium dumosum, the type 
species of Criocardium. 

(5) Pleuriocardia. The type species is Pieu- 
riocardia kansasense (Meek, 1871). Pleurio- 
cardia eufaulense (Conrad, I860) is used 
to represent Pleuriocardia because this is 
the most common species in the subfamily 
with an abundance of well-preserved ma- 
terial. 

(6) Austrocardium. Freneix & Grant-Mackie 
(1978) erected Austrocardium as a monotypic 
genus, type species A. acherontis Freneix & 
Grant-Mackie, 1978. Schneider (1992) found 
that Cardium acuticostatum Orbigny, 1842, 
belonged in Austrocardium. Austrocardium 



60 



SCHNEIDER 



acuticostatum is chosen to represent Austro- 
cardium because the material of A. acuti- 
costatum is better preserved than that of A. 
acherontis; A. acherontis would be scored 
identically to A. acuticostatum, except that the 
states for its posterior margin and shape of 
anterior cardinal are unl<nown. 

(7) Loxocardium. The type species is the 
Eocene Loxocardium formosum (Deshayes, 
1858). This is a relatively rare species. By far 
the most common species of Loxocardium is 
L. obliquum (Lamarck, 1805), for which I was 
able to examine over 100 specimens. 

(8) Agnocardia. The type species is the 
Eocene Agnocardia claibornense (Aldrich, 
1911). This species is l<nown from only a few 
broken valves. Vokes (1984, 1989) reported 
that the hinge of this species was unknown. 
After examination of specimens (including the 
types) of all the western hemisphere species of 
Agnocardia [A. sorrentoensis (Иаппа, 1927), 
A. glebosum (Conrad, 1848), A. acrocome 
(Dall, 1900), A. spinosifrons yokes, 1984, A. 
dissidepictum (Woodring, 1925), A. cinderel- 
lae (Maury, 1917) and A. pessoae (Maury, 
1924); A. rectispina (Koenen, 1893) from the 
Early Oligocène of Germany is the only other 
species of Agnocardia that I know of] it was 
decided that the best material of Agnocardia is 
actually the youngest (Late Pliocene) species 
A. dissidepictum. All species of Agnocardia 
would be coded identically for the characters 
considered herein. 

B. Reasons for not including taxa with al- 
leged Cretaceous to Eocene members. 

(1-3) Cardium, Bucardium, and Acanttio- 
cardia (Acantiiocardia). Many authors have 
described species of Cretaceous cardiids as 
belonging to these taxa. However, Keen 
(1951, 1969, 1980) and Popov (1977) re- 
jected all Cretaceous species of Cardium, Bu- 
cardium, and A. {Acanthocardia). Most of 
these species belong to Austrocardium, the 
rest to Pleuriocardia. 

(4) Vepricardium. Keen (1969, 1980) gave 
the range of Vepricardium ( Vepricardium) as 
Paleocene to Recent, and was followed by 
Popov (1977) and Kafanov & Popov (1977). I 
have found that alleged Paleogene species 
are either Ortliocardium, Agnocardia or inde- 
terminate. 

(5) Papyridea. I have found that all alleged 
Eocene Papyridea are species of Parvi- 
cardium. Keen (1969, 1980) states that the 
stratigraphie range of Papyridea is Miocene to 
Recent. 



(6) Trigoniocardia. A number of Eocene 
species have been variously classified as 
Trigoniocardia. Cardium {Trigoniocardia?) 
Colosseum Cox, 1941, Cardium (Anttiocardia) 
[sic] avonum Richards, in Richards & Palmer 
1953, and Cardium (Trigoniocardium) [sic] 
protoaliculum Richards, in Richards & 
Palmer, 1953, are species of Sawkinsia. 
Palmer & Brann (1965) classified the latter 
two species as Trigoniocardia (Americardia). 
Keen (1969, 1980) and Kafanov & Popov 
(1977) reject pre-Oligocene records of Trigo- 
niocardia and Americardia. 

(7) Fragum. Many Cretaceous species 
have been classified as Fragum. Most of 
these species belong to Profragum, the rest to 
Pleuriocardia. Alleged Eocene species of 
Fragum are indeterminate or belong to one of 
the following: Papillicardium, Parvicardium, 
Loxocardium, or Goniocardium. Keen (1969, 
1 980) and Kafanov & Popov (1 977) reject pre- 
Oligocene records of Fragum. 

(8) Europicardium. The type species is the 
Miocene to Pliocene Europicardium multi- 
costatum (Brocchi, 1814). Popov (1977) lists 
one Eocene species of Europicardium, 
Cardium stilpnaulax Cossmann, 1886. The 
type figures of С stilpnaulax in Cossmann 
(1886) shows it to have the shell shape, wide 
concave ribs, hinge, and ornamentation of Or- 
thocardium. However, the species figured as 
С stilpnaulax in Cossmann & Pisarro (1906) 
has the shell shape and ornamentation of Eu- 
ropicardium. Given the unsettled taxonomic 
and stratigraphie status of this taxon, it was 
decided not to include it in the analysis. 

(9) Dinocardium. Laevicardium {Dinocar- 
dium) cubensis Kojumdgieva & de la Torre, 
1982, Late Eocene of Cuba, is indeterminate. 

(10) Tridacna. Collignon (1949) described 
Tridacna besairiei as coming from the Maas- 
trichtian (later redescribed as Danian [Col- 
lignon, 1968]) of Madagascar. However, the 
provenance of this specimen is dubious; it 
probably is no older than Miocene (Schneider, 
1998). 



APPENDIX 3 

Synonymy of Criocardium Conrad, 1871, 
with Granocardium Gabb, 1869. 

Gabb (1869) erected Granocardium for 
some Late Cretaceous species of cardiids. 
Gabb (p. 266) described Granocardium as fol- 
lows: 



CARDIID PHYLOGENY: EUCARDIIDS AND PERUCARDIA 



61 



Shell nearly equilateral, usually longer than wide; 
valves closed all round; surface ornamented by two 
series of radiating hbs; large ribs bearing spines, tu- 
bercles, or grains, and smaller ribs occupying the 
interspaces between the larger, and granulate. 

As stated in the text, Gabb recognized the pri- 
mary spines to be on top of ribs, not between 
them. However, he did not perceive that one 
side of these larger ribs was homologous with 
a single smaller rib, and that the spine-bearing 
tops of the larger rib were homologous with the 
interspaces. Gabb assigned the species 
Cardium productumSo\NerbY 1832, С mouto- 
n/anum Orbigny, 1844, С caro//num Orbigny, 
1844, C. tippanum Conrad, 1858, and С sa- 
bulosum Gabb, 1869, to Granocardium. No 
type species was designated. In contrast to 
Gabb's definition of Granocardium, on all of 
these species the "smaller" ribs do not bear 
spines. Spines are present between the 
"smaller" ribs, or between the "smaller" ribs 
and the "larger" ribs. 

Stoliczka (1871: 207-8) felt that Gra- 
nocardium was a junior synonym of Trachy- 
cardium: 

. . . the species forming the subgenus [Grano- 
cardium] are said to be characterized by the inter- 
mediate ribs being granulate. Such can be seen on 
both ends of the shell of C. órbita for instance, 
which is a Traciiycardium: I don't see, therefore, the 
necessity for a new sub-genus. 

Cardium órbita is considered a species of the 
Trachycardiine Vasticardium (Fischer-Piette, 
1977; Vidal, 1997). No species of Trachy- 
cardiinae has "two series of radiating ribs" or 
"intermediate ribs." Stoliczka's statement 
above does not make sense in light of the 
morphology of either trachycardiines or 
Gabb's species of Granocardium. Stoliczka 
was at least consistent, classifying Gabb's 
Granocardium species as Traciiycardium. 

Apparently unaware of Gabb's (1869) erec- 
tion of Granocardium, Conrad (1871) erected 
Criocardium as a subgenus of Cardium, and 
described Criocardium as "Multiradiate; inter- 
stices spinose, ribs smooth; anterior lateral 
tooth long and prominent." Although it is un- 
clear what Conrad meant by "multiradiate" 
(numerous ribs? — this describes the vast ma- 
jority of cardiids; or, multiple types of ribs, as in 
Gabb's [1869] deschption of Granocardium?), 
Conrad correctly noted ("interstices spinose, 
ribs smooth") that the spines are between ribs, 
not on top of them. Conrad placed Cardium 



dumosum Conrad, 1871, and Cardium raulin- 
eanum Orbigny, 1844, in Criocardium. A type 
species was not designated. Stoliczka (1871) 
thought that Criocardium was little different 
from Granocardium, and therefore also con- 
sidered Criocardium a junior synonym of 
Traciiycardium. Stoliczka did designate С du- 
mosum as the type species of Criocardium. 
Stewart (1 930) designated Cardium carolinum 
as type species of Granocardium. Stewart did 
not discuss Criocardium. 

Stephenson's (1 941 ) descriptions of the or- 
namentation of С carolinum and С dumosum 
are accurate. Stephenson reached the same 
conclusions as I, regarding Criocardium as a 
junior synonym of Granocardium. 

With Granocardium and Criocardium incor- 
rectly described, and Criocardium erected 
without knowledge of Granocardium, these 
two genus-level names have since been used 
capriciously. Keen (1969, 1980) attempted to 
differentiate the two by defining Granocar- 
dium as having "intercalary ribs 2 to 3" and 
Criocardium as having "intercalary ribs tend- 
ing to be single rows of small spines between 
ribs." However, Cardium carolinum's orna- 
mentation varies across the surface of the 
shell, as on many species that have been as- 
signed to Granocardium. On the anterior and 
posterior slopes of the shell of С carolinum, 
most rows of spines are of primary spines, 
with an occassional row of secondary spines. 
The central slope of the shell bears only rows 
of secondary spines. Therefore, the number 
of intercalary ribs on Granocardium varies 
from or 1 on the anterior and posterior 
slopes to 30 consecutive "intercalary" ribs 
across the central slope of the shell. Cardium 
carolinum has rows of secondary spines be- 
tween ribs, which Keen used to define Crio- 
cardium. On Cardium dumosum, there are 
both intercalary ribs and rows of secondary 
spines. 

Given the foregoing taxonomic and mor- 
phologic confusion, I recommend that all 
cardiids with the following morphologic fea- 
tures be considered Granocardium, with Crio- 
cardium considered a subjective junior syn- 
onym; 

Shell quadrate to ovate. Ribbing consists 
entirely of regularly spaced ribs across entire 
shell surface. Ribs narrow, smooth-topped, 
solid underneath, and project beyond rib in- 
terspaces. Rows of spines in interspaces be- 
tween ribs. Spines of two different sizes 
(termed primary and secondary), but spines 



62 SCHNEIDER 

within a single row all of one size. Spines тагу spines raised higher than other inter- 
within a single row connected by a raised spaces. Spines in microstructural continuity 
thread, but raised thread never present with- with shell. Concentric sculpture and cross- 
out spines. Interspaces that bear rows of pri- striae absent. 



MALACOLOGIA, 1998, 40(1-2): 63-112 

A NEW GENUS AND FIVE NEW SPECIES OF MUSSELS (BIVALVIA, MYTILIDAE) 
FROM DEEP-SEA SULFIDE/HYDROCARBON SEEPS IN THE GULF OF MEXICO 

Richard G. Gustafson^*, Ruth D. Turner^, Richard A. Lutz\ & Robert C. Vrijenhoek^ 

ABSTRACT 

Five new species of modioliform mussels in the family Mytilidae are described from material 
collected at sulfide/hydrocarbon seeps in the Gulf of Mexico. New definitive taxa, placed in the 
subfamily Bathymodiolinae, include the genus Tamu and the species Tamu fisheri from hydro- 
carbon seeps on the Louisiana Continental Slope, Bathymodiolus heckerae from brine seeps at 
the base of the West Florida Escarpment in the eastern Gulf of Mexico, and Bathymodiolus 
brooksi from the West Florida Escarpment site and from hydrocarbon seeps at Alaminos Canyon 
in the western Gulf of Mexico. An additional two new mussel species, which exhibit combinations 
of morphological characters unlike any existing mytilid genus but for which molecular data are 
equivocal, are provisionally placed in the genera Bathymodiolus and Idas, respectively. These 
are: "Bathymodiolus" childressi from hydrocarbon seeps at Alaminos Canyon and the Louisiana 
Continental Slope, and "Idas" macdonaldi (in the subfamily Modiolinae) from hydrocarbon seeps 
on the Louisiana Continental Slope. 

Key words: Mytilidae, deep-sea, sulfide seeps, hydrocarbon seeps, Bathymodiolinae. 



INTRODUCTION 

Modioliform mussels in the family Mytilidae 
are conspicuous members of many deep-sea 
hydrothermal vent and cold-water methane/ 
sulfide seep environments. A common feature 
of these mussels is their dependence on sul- 
fide-oxidizing or methanotrophic symbionts 
(Fisher, 1990; Cavanaugh, 1992). The first 
vent mussel described was Bathymodiolus 
thermophilus Kenk & Wilson, 1985, which oc- 
curs at hydrothermal vents on the Galápagos 
Rift and the East Pacific Rise (EPR). Recently 
described species are: B. platifrons Hashi- 
moto & Okutani, 1994; B. japonicus Ha- 
shimoto & Okutani, 1994; B. adulcidos Hashi- 
moto & Okutani, 1994; and B. septemdierum 
Hashimoto & Okutani, 1994, from vent and 
cold seep sites around Japan; B. brevier 
Cosel, Métivier & Hashimoto, 1994, and B. 
elongatusCosel, Métivier & Hashimoto, 1994, 
from vent sites in the south Pacific; and B. 
puteoserpentis Cosel, Métivier & Hashimoto, 
1994, from the Snake Pit site on the Mid-At- 
lantic Ridge. In addition, the small mussel Idas 
washingtonia (Bernard, 1978) occurs at hy- 



drothermal vents on the Juan de Fuca Ridge 
in the north-eastern Pacific (Juniper et al., 
1992) and Amygdalum politum (Verrill & 
Smith, in Verrill, 1880), a small thin-shelled 
mytilid, occurs near cold water hydrocarbon 
seeps on the Louisiana Continental Slope 
(Turner, 1985). 

As yet undescribed modioliform mussels 
were reported from hydrothermal vents or 
cold-seeps in the Pacific Ocean at Guaymas 
Basin (Turner, 1 985), Middle Valley (Juniper et 
al., 1992), the Mariana Back-Arc Basin 
(Hessler & Lonsdale, 1 991 ), and the Mid-Oki- 
nawa Trough (Hashimoto et al., 1995); and in 
the Atlantic Ocean at the South Barbados ac- 
cretionary prism (Jollivet et al., 1990) and on 
the Mid-Atlantic Ridge at 37°50'N ("Menez 
Gwen" site), 37°17'N ("Lucky Strike" site), 
29°N ("Broken Spur" site), and 1 4°45'N (Cosel 
etal., 1997). 

An allozyme survey by Craddock et al. 
(1995) identified several additional modio- 
liform taxa from sulfide/hydrocarbon seeps in 
the Gulf of Mexico. A subsequent analysis of 
these specimens for DNA sequences from a 
region of the mitochondrial Cytochrome с Ox- 



^ Institute of Marine and Coastal Sciences, P. O. Box 231 , Rutgers University New Brunswick, New Jersey 08903, USA 
^Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts 02138, USA 

'Present Address; National Oceanic and Atmospheric Administration, National Marine Fisheries Service, Northwest Fish- 
eries Science Center, Conservation Biology Division, 2725 Montlake Blvd. E., Seattle, Washington 98112-2097 



63 



64 



GUSTAFSON ETAL 



TABLE 1 . New species and type localities of modioliform mussels from the Gulf of Mexico. 



New species 



Location 



Latitude Longitude Depth (m) 



Bathymodiolus heckerae 
Bathymodiolus brooksi 
Bathymodiolus brooksi 
"Bathymodiolus" childressi 
"Bathymodiolus" childressi 
"Bathymodiolus" childressi 
Tamu fisheri 
Tamu fisheri 
"Idas" macdonaldi 



West Florida Escarpment 


26°02.2' N 
84°54.5' W 


3314 


Alaminos Canyon 


26°21.3' N 
94°29.7' W 


2222 


West Florida Escarpment 


26°02.2' N 
84°54.5' W 


3314 


Bush Hill, Louisiana Continental 


27°46.9' N 


546 


Slope 


91°30.4' W 




Brine Pool-NR 1, Louisiana 


27°43.4' N 


650 


Continental Slope 


91°16.6' W 




Alaminos Canyon 




2222 


26°21.3N, 94°29.7' W 






Bush Hill. Louisiana Continental 


27°46.9' N 


546 


Slope 


91°30.4' W 




Near Garden Banks-386, 


27°50' N 


650 


Louisiana Continental Slope 


92°10' W 




Near Garden Banks-386, 


27°50' N 


650 


Louisiana Continental Slope 


92°10' W 





idase Subunit-I (COI) gene corroborated the 
discrete nature of these taxa (W. R. Hoeh, 
pers. comm., unpublished data). 

Herein, we describe five of the mytilid 
species identified in Craddock et a!. (1995) 
from the Gulf of Mexico (Table 1, Fig. 1). Fol- 
lowing the suggestion of Soot-Ryen (1955), 
characters used for classification of these 
new mytilid species have been taken from the 
shell or from easily visible parts of the 
anatomy, such as muscles, gill, and mantle 
margins. Of special importance to classifica- 
tion in the Mytilidae is the comparative place- 
ment of the retractor muscles of the foot and 
byssus (Soot-Ryen, 1955; Knudsen 1970). 
However, where deemed important, taxo- 
nomic characters associated with the internal 
anatomy, such as the course taken by the di- 
gestive tract, have been included. 



MATERIALS AND METHODS 
Specimens 

Mussel specimens were collected during 
dives of the DSV ALVIN (A) and DSRV JOHN- 
SON SEA-LINK-I (JSL) (Tables 1 -7) and sub- 
sequently prepared as described in Craddock 
et al. (1995). Additional specimens were pro- 
vided by Colleen M. Cavanaugh (Harvard 
Univ.), James J. Childress (Univ. California - 
Santa Barbara), Charles R. Fisher (Pennsyl- 
vania State Univ.), Ian R. MacDonald (Texas 
A& M Univ.), and Craig R. Smith (Univ. Hawaii 
- Manoa). 



Holotypes and a series of paratypes are de- 
posited in the Academy of Natural Sciences of 
Philadelphia (ANSP). Additional paratypes 
are deposited in the following institutions: 
United States National Museum of Natural 
History, Washington, D.C. (USNM); Museum 
of Comparative Zoology, Harvard University 
(MCZ); Houston Museum of Natural Science, 
Houston, Texas (HMNS), Museum National 
d'Histoire Naturelle. Paris (MNHN), and Rut- 
gers University (RU). Catalogue numbers and 
other pertinent information concerning holo- 
types and paratypes are summarized in Ap- 
pendix 1. 

Shell and anatomical features of specimens 
of the following species were examined for this 
report: Bathymodiolus thermophilus and B. 
puteoserpentis from their respective type lo- 
calities; paratypes of Benthomodiolus abys- 
sicola (Knudsen, 1 970) borrowed from ZMUC; 
Idas argenteus Jeffreys, 1876, from the 
Tongue of the Ocean (TOTO) east of Andres 
Island in the Bahama Islands; Idas washingto- 
nia from South Cleft hydrothermal vent on the 
Juan de Fuca Ridge off southern British Co- 
lumbia and from whale bone in the Santa 
Catalina Basin off California; Adipicola sp. 
from Middle Valley on the Juan de Fuca Ridge; 
and undescribed deep-sea mussels from Mar- 
iana Back-Arc Basin in the Pacific and Lucky 
Strike on the Mid-Atlantic Ridge. 

Small shells examined by scanning elec- 
tron microscopy were air dried, glued to stubs, 
coated with approximately 400 À of gold/pal- 
ladium, and viewed on an Hitachi S-450 scan- 
ning electron microscope. Drawings of shells 



NEW DEEP-SEA MUSSELS 



65 




FIG. 1 . Location of submersible dive sites in the Gulf of Mexico where rnussels were collected. 



and tissues were made either freehand or 
with the aid of a camera lucida. 

Morphological Terminology 

The "horizontal branchial septum" is a thin, 
membranous horizontal shelf separating in- 
current and excurrent chambers, posterior to 
the posterior adductor (commonly extends 
from the ventral side of posterior adductor to 
the base of the excurrent siphon). The "valvu- 
lar siphonal membrane" is an extension of the 
branchial septum formed by fusion of right 
and left mantle lobes ventral to the excurrent 
siphon and extending a variable distance into 
the pedal-byssal gape; a small centrally 
placed papilla is sometimes present at the an- 
terior end of the valvular siphonal membrane. 

Morphometries 

Shell measurements used to statistically 
discriminate among the five new species 
were: L = length of valve; H = height of valve; 
W = width of valves, G = length of the liga- 
ment; and A = anterior length or the distance 
from the anterior shell margin to an imaginary 
line drawn vertically from the anterior edge of 
the beak or umbonal bulge (Fig. 2). Measure- 
ments were made with hand-held calipers 
(±0.1 mm). All analyses were performed on 
Iog10 transformations of the original vari- 
ables. Multivariate analyses were performed 
on standardized variables with Varimax rota- 



tion using the statistical computer program 
JMP 3.0.2 (SAS Statistics Inst., Inc, Raleigh, 
North Carolina). 



SYSTEMATIC SECTION 

Family Mytilidae 

Subfamily Bathymodiolinae Kenk & Wilson, 
1985 

Type genus; Bathymodiolus Kenk & Wilson, 
1985 

Revised Diagnosis: Shell smooth, modioli- 
form, with subterminal umbones; adult hinge 
edentulous, juvenile hinge with small den- 
ticulations anterior and posterior of ligament; 
posterior byssal retractors divided into ante- 
rior and posterior portions with separate in- 
sertion points on the adult shell producing 
separate muscle scars; intestine short, either 
straight or with a very short recurrent loop; 
demibranchs of hypertrophied ctenidia thick 
and fleshy, inner and outer demibranchs of 
equal length, filaments broadly thickened. 
Ctenidia associated with symbiotic bacteria. 

Remarks: As originally described this subfam- 
ily contained the single genus Bathymodiolus 
(Kenk & Wilson, 1985). Eight members of this 
subfamily have been previously described: 
B. thermophilus, B. brevier, B. elongatus, B. 
puteoserpentis, B. platifrons, B. japonicus, B. 
aduloides, and B. septemdierum (Kenk & Wil- 
son, 1985; Hashimoto & Okutani, 1994; Cosel 



66 



GUSTAFSONETAL 




FIG. 2. Diagram depicting measurements taken and generalized shell characters. A, anterior length (distance 
from anterior shell margin to anterior edge of umbo); AA, anterior adductor: APR. anterior portion of poste- 
rior byssal-pedal retractor; AR, anterior byssal-pedal retractor; H, shell height; L, shell length; G, ligament 
length; PA, posterior adductor; PL, pallia! line; PPR, posterior portion of posterior byssal-pedal retractor; W, 
width of shell valves. 



etal., 1994). The current contribution adds the 
genus Tamu and the species T. fisheri, B. 
heckerae, and B. brooks! to the subfamily. 

All members of this subfamily have hyper- 
trophied gills associated with symbiotic bacte- 
ria that reside either within certain cells termed 
"bacteriocytes" or on the gill surface (Fisher, 
1990: Fisher et al., 1993; Cavanaugh, 1992; 
Cavanaugh et al., 1987; СМ. Cavanaugh, 
pers. comm.). The simplified alimentary sys- 
tem, hypertrophied gills, and symbiosis with 
sulfide-oxidizing or methanotrophic bacteria, 
indicative of a different feeding mechanism in 
this group, separates members of this sub- 
family from all other known mytilids. 

Bathymodiolus Kenk & Wilson. 1985 

Bathymodiolus LePennec et al. 1983: 70; 
Le Pennée & Hily, 1984: 517; Laubier & Des- 
bruyères, 1984: 1507; Smith, 1985: 1068 
[nomen nudum]. 

Bathymodiolus Kenk & Wilson, 1985: 255 
(type species, by original designation, Bathy- 
modiolus thermophilus Kenk & Wilson, 1985). 

Revised Diagnosis: Shell large (maximum 
size greater than 90 mm), smooth, modio- 
liform, with sub-terminal umbones; adult hinge 
edentulous, juvenile hinge with small denticu- 
lations anterior and posterior of ligament (Figs. 
3-5); posterior byssal retractors divided into 



posterior and anterior portion, retractor scars 
separate; labial palp suspensors and pedai re- 
tractors present; demibranchs of ctenidia thick 
and fleshy; filaments broadly thickened, with 
reduced ventral food grooves, containing in- 
tracellular bacterial symbionts; intestine 
straight without recurrent loop; rectum enters 
ventricle anterior to the auricular ostia. 

Remarks: The manuscript name Bathy- 
modiolus was introduced as a nomen nudum 
by LePennec et al. (1983: 70) and subse- 
quently appeared in Le Pennée & Hily (1984), 
Laubier & Desbruyères (1984), and Smith 
(1985; publication date. May) prior to its valid 
introduction, under the rules of the Inter- 
national Code of Zoological Nomenclature 
(ICZN), by Kenk & Wilson (1985; publication 
date, 9 July). 

The extremely reduced pedal gape of B. 
thermophilus appears to be a derived charac- 
ter, absent in other species referred to this 
genus (Hashimoto & Okutani, 1994; Cosel et 
al., 1994, 1997). Bathymodiolus brevior, B. 
elongatus, B. puteoserpentis (Cosel et al., 
1994), and "Bathymodiolus" childressi have 
been referred to Bathymodiolus on a provi- 
sional basis. The final systematic placement 
of these species, and others placed in Bathy- 
modiolus, must await complete morphological 
analyses and molecular studies on the entire 
group of deep sea mytilids. 



NEW DEEP-SEA MUSSELS 



67 



Bathymodiolus thermophilus Kenk & Wilson, 
1985 Figures 3-5 

Bathymodiolus thermophilis (sic) Laubier & 
Desbruyères, 1984: 1510 [nomen nudum]. 

Bathymodiolus thermophilus Smith, 1985 
(May): 1068 [nomen nudum]. 

Bathymodiolus thermophilus Kenk & Wil- 
son, 1985 (9 July): 255, figs. 2-13 (type local- 
ity, "Mussel Bed" hydrothermal vent, Galápa- 
gos Rift, 0°47.89'N; 86°9.21'W in 2495 m, 
ALVIN Dive 879; holotype USNM 803661). 

Description: Shell large, up to 180 mm long, 
modioliform, with sub-terminal umbones, ellip- 
tical in juveniles, arcuate in older specimens. 
Ventral shell margin nearly straight in young 
specimens, slightly concave in specimens 
larger than 10 cm. Adult hinge edentulous, ju- 
venile hinge with small denticulations anterior 
and posterior to ligament. Posterior byssal re- 
tractors divided, retractor scars separate; sep- 
arate pedal retractors prominent; slender 
labial palp suspensors extend anteriorly from 
anterior retractors to support the musculahzed 
labial palps. Ventral palliai line with a dorsally 
directed concavity in byssal region about one- 
third of the distance from the anterior end. 
Inner fold of mantle lobes fused in postero- 
ventral and antero-ventral midline creating 
valvular siphonal membrane, with papilla, and 
an extremely reduced pedal gape. Dorsal 
edges of ascending lamellae attached to mus- 
cular longitudinal ridges on surfaces of mantle 
lobe and visceral mass. Horizontal branchial 
septum, extending from the base of the excur- 
rent siphon and the ventral side of the poste- 
rior adductor, separates incurrent and excur- 
rent chambers posteriorly. Inner and outer 
demibranchs essentially equal-sized, thick 
and fleshy, filaments broadly thickened, with 
reduced ventral food grooves. Ctenidia con- 
tain intracellular symbiotic bacteria. Muscular- 
ized inner palps long and slender, attached 
over most of their length to visceral mass, ex- 
tending farther posteriorly than smaller mus- 
cularized outer palps. Intestine straight with- 
out recurrent loop; intestine/rectum enters 
ventricle anterior to the position of the auricu- 
lar ostia. 

Remarks: The manuscript species name Ba- 
thymodiolus thermophilis (sic) was introduced 
as a nomen nudum by Laubier & Desbruyères 
(1984) and as B. thermophilus by Smith 
(1 985; publication date. May) prior to the valid 



description of this species, under the rules of 
the ICZN, by Kenk & Wilson (1985; publica- 
tion date, 9 July). 

Kenk & Wilson (1985) described Bathy- 
modiolus as having a small pedal gape result- 
ing from extensive ventral fusion of the inner 
folds of the mantle lobes. This feature is pres- 
ent in the type species B. thermophilus, but is 
lacking in other described members of this 
genus (Hashimoto & Okutani, 1994; Cosel et 
al., 1994), as well as in all other known 
mytilids. As pointed out in Kenk & Wilson 
(1985: 260), the dorsal ends of the ascending 
lamellae are attached to muscular longitudinal 
ridges on the surfaces of the mantle lobes and 
the visceral mass. These muscular longitudi- 
nal ridges are also unique to B. thermophilus 
and were not evident in any other mussel ex- 
amined for this report. 

The hinge of B. thermophilus was originally 
described as edentulous (Kenk & Wilson, 
1985). However, in specimens of B. ther- 
mophilus smaller than about 10 mm there are 
up to 25 "vertical striations" or denticles im- 
mediately posterior of the ligament and about 
6 denticles located immediately below the 
umbones (Fig. 3-5). Other deep-sea mussel 
species described herein (Figs. 6-28) also 
have hinge denticulations as juveniles (Figs. 
8-10, 18-20, 23, 25-27). These denticula- 
tions are lost in adult members of the genus 
Bathymodiolus 

Although Bathymodiolus was described as 
lacking ventral food grooves on the ctenidia 
(Kenk & Wilson, 1985), we observed reduced 
food grooves in all specimens of B. ther- 
mophilus we examined. Food grooves were 
first described in B. thermophilus by Le Pen- 
née et al. (1983), Le Pennée & Hily (1984), 
and Fiala-Médioni et al. (1986). 

Kenk & Wilson (1 985) described the perios- 
tracum of Bathymodiolus as "hirsute"; mean- 
ing hairy, bristly or shaggy. However, these 
"periostracal hairs" are probably of byssal ori- 
gin (Bottjer & Carter, 1 980; Ockelmann, 1 983) 
and not of taxonomic value. The original de- 
scription of Bathymodiolus described the 
labial palps as "small," whereas the labial 
palps of B. thermophilus specimens we ex- 
amined, from the type-locality and elsewhere, 
were large and muscular. 

Range: This species appears confined to the 
area of hydrothermal vent activity on the 
Galápagos Rift and along the EPR at 9° to 
1 0°N, 1 1 °24'N and 1 3°N (Table 2). In addition. 



GUSTAFSON ETAL 




FIG. 3. Bathymodiolus thermophilus Kenk & Wilson. Juvenile hinge line of specimen 4.5 mm in length. 
FIG. 4. Bathymodiolus thermophilus Kenk & Wilson. Hinge denticles, located immediately posterior to liga- 
ment in juvenile specimen 4.5 mm in length. 

FIG. 5. Bathymodiolus thermophilus Kenk & Wilson. Hinge denticles, located immediately below the umbo 
in juvenile specimen 4.5 mm in length. 



preliminary comparison of mtDNA CO! se- 
quences between B. thermophilus from the 
type locality and mussels collected from 17°S 
on the EPR revealed essentially no differ- 
ences (R.C. Vrijenhoek, unpublished data). 

Bathymodiolus heckerae Turner, 
Gustafson, Lutz & Vrijenhoek, new species 
Figures 6-13 

This species, known since 1984, has been 
referred to in literature concerning seep and 
vent biology but was never formally de- 
scribed. The following is a list of these refer- 
ences. 

"Mussel" - Pauli et al., 1984: 965, fig. 2 [mus- 
sels visible in habitat photo]. 



"Mussels" - Florida Escarpment Cruise Par- 
ticipants, 1984: 32, fig. 1 [mussels visible 
in habitat photo]. 

"Large mussel" - Turner & Lutz, 1984: 60, 
figs. 1 (site #9 = Florida Escarpment, dia- 
gram of mussel shell), 5, 6, [mussels vis- 
ible in habitat photo], 8 (left) [micrograph 
of prodissoconch]. 

"Large, elongate mussels" - Turner, 1985: 
29, figs. 4B-C, 6. 

"Mytilid" - Southward, 1985: 673. 

"Mytilid mussel" - Pauli et al., 1985: 710. 

"Large mussels," "large golden-brown my- 
tilids" - Hecker, 1985: 465, 466, figs. 2, 
4, 5, 6 [mussels visible in habitat photos]. 

"Large mussels" - Grassle, 1986: 338. 

"Seep mussels," "Florida Escarpment mus- 
sel" - Cavanaugh et al., 1987: 346, 347, 



NEW DEEP-SEA MUSSELS 
TABLE 2. Specimens of Bathymodiolus thermophilus examined. 



69 











Number and condition of 


Dive 


Date 


Depth 


Latitude; Longitude 


specimens 


ALVIN Dives 


Galápagos Rift 








887 


12 Feb. 1979 


2488 


00°48.5'N 


;86°09.1'W 


1 - shell & tissue 


983 


30 Nov. 1 979 


2457 


00°48.2'N 


:86°13.4'W 


2 - shell, 7 - shell & tissue 


2223 


28 May 1990 


2503 


00°47.9N 


; 86°09.2'W 


42 - shell 


2224 


29 May 1990 


2461 


00°48.2N 


;86°13.5'W 


35 - shell 


ALVIN Dives 


East Pacific Rise 


11°N 






2225 


3 June 1990 


2515 


11°24.9'N; 103°47.3'W 


15- shell, 2 -shell & tissue 


2226 


4 June 1990 


2515 


11°24.9'N; 103°47.3'W 


63 - shell 


ALVIN Dives 


East Pacific Rise 


13°N 






2228 


6 June 1990 


2630 


12°48.6'N; 103°56.5W 


14 -shell 


2229 


7 June 1990 


2630 


12°48.6'N; 103°56.5'W 


51 - shell, 1 - shell & tissue 


ALVIN Dives 


East Pacific Rise near 9°N- 


-10°N 




2350 


31 March 1991 


2585 


09°30.9'N 


104°14.5'W 


4 - shell 


2351 


1 April 1991 


2550 


09°50.rN 


104°17.4'W 


3 - shell 


2352 


2 April 1991 


2567 


09°33.5N 


104°14.1'W 


47 - shell 


2354 


4 April 1991 


2527 


09°47.7N 


104°17.1'W 


8 - shell 


2356 


6 April 1991 


2556 


09°40.9'N 


104°15.8'W 


3 - shell 


2358 


8 April 1991 


2578 


09°30.9'N 


104°14.6'W 


3 - shell & tissue 


2359 


9 April 1991 


2564 


09°30.9'N 


104°17.7'W 


6 -shell 


2368 


19 April 1991 


2539 


09°51.1N 


104°17.5'W 


2 -shell 


2498 


6 March 1992 


2525 


09°50.5'N 


104°17.5'W 


4 - shell & tissue 



TABLE 3. Specimens of Bathymodiolus heckerae examined. 











Number and condition of 


Dive 


Date 


Depth 


Latitude; Longitude 


specimens 


ALVIN Dives 


Gulf of Mexico - 


West Florida Escarpment 




1343 


9 March 1984 


3270 


26°03'N 


84°54'W 


14 - shell & tissue 


1344 


10 March 1984 


3270 


26°03N 


84°56'W 


1 - shell 


1346 


12 March 1984 


3286 


26°03'N 


84°54'W 


1 - shell & tissue 


1753 


14 Oct. 1986 


3277 


26°02.4N 


84°54.2'W 


16 -shell 


1754 


15 Oct. 1986 


3303 


26°02.4'N 


84°55.3'W 


4 - shell; 6, shell & tissue 


1755 


16 Oct. 1986 


3300 


26°01.5'N 


84°55.3'W 


14 - shell, 2 - shell & tissue 


1756 


17 Oct. 1986 


3243 


26°0rN 


84°55'W 


27 -shell 


1758 


20 Oct. 1 986 


3266 


26°01.8'N 


84°54.9'W 


4 - shell 


2196 


26 March 1990 


3314 


26°02.4'N 


84°54.4'W 


91 - shell, 17- shell & tissue 


2197 


29 March 1990 


3314 


26°02.2'N 


84°54.5W 


60 - shell 


2542 


3 June 1992 


3313 


26°01.8'N 


84°54.6'W 


49 - shell, 40 -shell & tissue 



TABLE 4. Specimens of Bathymodiolus brooksi examined. 



Dive 



Date 



Depth 



Latitude; Longitude 



Number and condition of 
specimens 



ALVIN Dives. Gulf of Mexico 
2209 11 April 1990 

2211 13 April 1990 

2535 22 May 1992 

ALVIN Dives, Gulf of Mexico 
1343 9 March 1984 

2196 26 March 1990 

2542 3 June 1992 



Alaminos Canyon 
2340 26°21.1'N;94°30.3'W 

2222 26°21.3N;94°29.7'W 

2220 26°21.1'N;94°29.5W 

West Florida Escarpment 
3270 26°03'N;84°54'W 

3314 26°02.4'N;84°54.4'W 

3313 26°01.8'N;84°54.6'W 



18 -shell 

65 - shell, 20 - shell & tissue 

6 - shell & tissue 

1 - shell & tissue 

1 -shell 

4 - shell, 3 -shell & tissue 



70 



GUSTAFSONETAL 



TABLE 5. Specimens of "Bathymodiolus" childressi examined. 



Dive 



Date 



Depth 



Latitude; Longitude 



Number and condition of 
specimens 



JOHNSON SEA LINK-I Dives, Gulf of Mexico - Louisiana Continental Slope - Bush Hill 
1877 27 Sept. 1986 548 27°46.9'N; 91°30.4'W 5 - shell & tissue 

3108 31 Aug. 1991 548 27°46.9'N; 91°30.4'W 3 - shell & tissue 

31 29 15 Sept. 1 991 546 27°46.9'N: 91 °30.4'W 1 1 9 - shell, 59 - shell & tissue 

JOHNSON SEA LINK-I Dives, Gulf of Mexico - Louisiana Continental Slope - Green Canyon-272 
3133 17 Sept. 1991 737 27°41.3N; 91°32.5'W 4 - shell 

3137 19 Sept. 1991 723 27°41.rN; 91°32.2'W 44 - shell, 8 -shell & tissue 

JOHNSON SEA LINK-I Dives, Gulf of Mexico - Louisiana Continental Slope - Brine Pool NR-1 
3145 27 Sept. 1991 650 27°43.4N; 91°16.6W 29 - shell 

ALVIN Dives, Gulf of Mexico - Alaminos Canyon 
2211 13April1990 2222 26°21.3'N; 94°29.7'W 31 - shell, 8 - shell & tissue 



TABLE 6. Specimens of Tamu fisheri examined. 



Dive 



Date 



Depth 



Latitude; Longitude 



Number and condition of 
specimens 



JOHNSON SEA LINK-I Dives, Gulf of Mexico - Louisiana Continental Slope 

3108 31 Aug. 1991 548 27°46.9'N; 91°30.4'W 

3129 15 Sept. 1991 546 27°46.9'N; 91°30.4W 

JOHNSON SEA LINK-I Dives, Gulf of Mexico - Louisiana Continental Slope 

3131 16 Sept. 1991 701 27°50N; 92°10W 

3149 29 Sept. 1991 650 27°50'N; 92°10'W 

MCZ No. 296151 (Texas A & M University, Louisiana Slope, Cruise #85-6-5, Trawl #5) 

L2787 (right valve) 

L2788 (left valve) 

L2789 (left valve) 
MCZ No. 296152 (Texas A & M University, Louisiana Slope, Cruise #85-6-5, Trawl #10) 

L2742 (right valve) 

L2743 (left valve) 

L2744 (left valve) 

L2745 (left valve) 



Bush Hill 

6 - shell, 3 - shell & tissue 

3 - shell & tissue 
Near Garden Banks-386 

1 - single valve 

6 - shell 



TABLE 7. Specimens of "Idas" macdonaldi examined. 



Dive 



Date 



Depth Latitude; Longitude 



Number and condition of 
specimens 



JOHNSON SEA LINK-I Dives, Gulf of Mexico - Louisiana Continental Slope 

3149 29 Sept. 1991 650 27°50'N; 92°10W 4 - shell, 6 - shell & tissue 



fig. 1a-b [micrographs of bactehocyte 

and symbiotic bacterium]. 
'Mussels (cf. Bathymodiolus) - Hook & Gol- 

ubic, 1988: 348, fig. 1 [mussels visible in 

habitat photos], fig. 2. 
"Mytilid bivalve," "seep mussel" - Gary et al., 

1989:411. 



"Deep-sea mussel, cf. Bathymodiolus" - 
Hook & Golubic, 1990:240. 

"Mytilid" - Petrecca & Grassle, 1990: 281. 

"West Florida Escarpment mussel (com- 
mon)" - Craddock et al., 1991 : p. 302. 

"Florida Escarpment mussel" - Dahlhoff & 
Somero, 1991:475 (table 1). 



NEW DEEP-SEA MUSSELS 



71 





В 



D 




FIG. 6. Bathymodiolus heckerae Turner, Gustafson, Lutz & Vrijenhoek. Holotype, ANSP A1 8846. A, anterior 
view; B, posterior view; C, dorsal view; D, ventral view; E, lateral view of right valve; F, lateral view of left 
valve. 



72 



GUSTAFSON ETAL 




2.5 cm 



FIG. 7. Bathymodiolus heckerae Turner, Gustafson, Lutz & Vrijenhoek. External views of a growth series of 
shells illustrating ontogenetic change in shape. 



"FL mytilid" - Cavanaugh, 1992: 316. 
"Bathymodiolus-like mussels" - Hook & Gol- 

ubic, 1992: 120. 
"Seep mytilid Va" - Fisher, 1993: 609. 
"Deep-sea mussel (an undescribed new 

genus similar to Bathymodiolus)" - Hook 

&Golubic, 1993:81. 
"SM Va" - Fisher et al., 1993: 278, 284. 
"FL/Va" - Craddock, et al., 1995: 479-483. 
"Seep Mytilid Va" - Nelson & Fisher, 1995: 

table 3. 

Types: Holotype ANSP AI 8846 from ALVIN 
Dive 1343 along the base of the West Florida 
Escarpment in the eastern Gulf of Mexico at 
26°03N; 84°54'W, in 3270 m. Paratypes are 
from ALVIN Dive 1754 at 26°02.4'N: 
84°55.3'W in 3303 m (USNM); ALVIN Dive 
1755 at 26°01.5'N; 84°55.3'W in 3300 m 
(MOZ); ALVIN Dive 2196 at 26°02.4'N: 
84°54.4'W in 3314 m (ANSP 400772;, USNM, 
HMNS, MNHN); ALVIN Dive 2197 at 
26°02.2'N; 84°54.5'W in 3314 m (HMNS); and 
ALVIN Dive 2542 at 26°01.8'N; 84°54.6'W in 
3314 m (ANSP 400771 , 400773; MNHN). 



Shell Morphology: Shell large, up to 190 mm 
long, modioliform, thin, fragile, essentially 
equivalve, elongately elliptical. Anterior mar- 
gin sharply rounded; posterior margin broadly 
rounded; ventral margin straight in young 
specimens, with a slight ventral concavity in 
medium sized specimens, concavity more 
pronounced in larger specimens; dorsal mar- 
gin broadly convex, more or less straight over 
span of the ligament (Figs. 6, 7, 11, 12). Um- 
bones often eroded; prosogyrate; subtermi- 
nal, positioned between 6% and 16% of the 
length of the shell from anterior end. An indis- 
tinct, raised, broadly rounded ridge extends 
from umbonal region to posterior-ventral mar- 
gin. 

External sculpture lacking; surface smooth 
except for concentric growth lines; fine radial 
lines in periostracum extending from umbo to 
ventral margin, most prominent posteriorly; 
and fine radial periostracal corrugations along 
the ventral margin in the region of the byssal 
gape. Shell dull-white, periostracum straw- 
yellow to light-brown in young specimens, 
older specimens have dark-brown perios- 



NEW DEEP-SEA MUSSELS 



73 




FiG. 8. Bathymodiolus heckerae Turner, Gustafson, Lutz & Vrijenhoek. Juvenile hinge line of specimen 7.5 

mm in length. 

FIG. 9. Bathymodiolus heckerae Turner, Gustafson, Lutz & Vrijenhoek. Hinge denticles located immediately 

posterior of the ligament in juvenile specimen 7.5 mm in length. 

FIG. 10. Bathymodiolus heckerae Turner, Gustafson, Lutz & Vrijenhoek. Hinge denticles located immediately 

below the umbo in juvenile specimen 7.5 mm in length. 



tracum that becomes straw-yellow peripher- 
ally. Periostracum of older specimens some- 
times marked by irregularly shaped dark 
brown pigment patches, overlain by numer- 
ous byssal thread attachment plates. Interior 
off-white, predominately nacreous. 

Ligament opisthodetic, parivincular, ex- 
tending posteriorly from umbones to occupy 
from 32% to 49% of dorsal margin. Adult 
hinge edentulous, except for small posteriorly 
directed projection of anterior hinge margin 
beneath ligament's anterior end; hinge some- 
what thickened below and anterior to umbo. 
Juvenile hinge with about 15 denticles imme- 



diately posterior to ligament and approxi- 
mately 10 denticles located immediately 
below umbones (Figs. 8-10). Hinge denticles 
become obsolete in specimens greater than 
18 mm in length. 

Muscle Scars: Muscle scars and palliai line in- 
distinct. Anterior adductor scar rounded but 
truncated posteriorly; located ventral and par- 
tially anterior to umbo in small specimens, en- 
tirely in front of umbo in medium and large 
specimens. Posterior adductor scar round to 
oblong, usually contiguous with small siphonal 
retractor scar ventrally and posterior portion of 



74 



GUSTAFSON ETAL 



posterior byssal-pedal retractor scar dorsally. 
Anterior retractor scar located within upper ex- 
tremity of umbonal cavity directly beneath 
umbo. Posterior byssal retractors form two 
scars with very large intervening gap, anterior 
one obliquely elliptical, directly beneath or 
slightly anterior of postehor end of ligament in 
small specimens, well antenor of postehor end 
of ligament in medium and large specimens, 
second one elliptical, parallel to antero-poste- 
rior axis of shell and located antero-dorsally to 
and bordering posterior adductor scar (Fig. 
12). Palliai line distant from shell margin, ex- 
tending from postero-ventral edge of anterior 
adductor scar to postero-ventral edge of pos- 
terior adductor, curving slightly upwards and 
then downwards to form slight indentation in 
byssal gape region at about one-quarter to 
one-third of distance from anterior, end. Small 
siphonal retractor scar located at postehor end 
of ventral palliai line, usually but not always 
contiguous with posterior adductor (Fig. 12). 



Selected Measurements (in 


mm): 










anterior 






length 


tieight 


width 


length 


Dive 




110.6 


36.0 


28.1 


~ 


A 1343 


Holotype 
ANSP 


75.2 


27.8 


22.3 


9.7 


A 1754 


Paratype 
USNM 


134.2 


43.0 


32.8 


155 


A 1755 


Paratype 
MCZ 


98.0 


33,3 


25.0 


13.8 


A 21 96 


Paratype 
HMNS 


84.5 


27.0 


24.0 


8.2 


A 21 96 


Paratype 
MNHN 


148.0 


47.4 


36.1 


16,7 


A 21 96 


Paratype 
Rutgers 


22.6 


11.4 


7.8 


1,8 


A2196 


Paratype 
MNHN 


387 


17.5 


13.8 


3,2 


A2197 


Paratype 
HMNS 


102.0 


34.0 


25.5 


11,5 


A 2542 


Paratype 
Rutgers 


99.0 


36.5 


24.8 


10,5 


A 2542 


Paratype 
ANSP 


132.5 


45.0 


31.7 


16,6 


A 2542 


Paratype 
ANSP 


122.9 


39.7 


29.8 


16.1 


A 21 96 


Paratype 
ANSP 


148.1 


41.1 


37.3 


23.0 


A2196 


Paratype 
HMNS 


79.2 


26.8 


21.6 


7.2 


A2196 


Paratype 
USNM 


164,0 


47.0 


41.7 


18.4 


A 2542 


Paratype 
Rutgers 



Internal Morphology 

Musculature: Main features of musculature 
evident from previous description of muscle 



scars and illustrated in Figure 13. Posterior 
byssal retractors divided into two widely di- 
vergent main bundles that attach separately 
to shell, a posterior portion inserting along an- 
tero-dorsal edge of postehor adductor and an 
anterior portion inserting below and anterior to 
ligament's posterior end. Posterior portion of 
posterior byssal retractor long and slender re- 
sulting in an elongate and quite narrow region 
of shell attachment. Pedal retractors large 
and prominent, arising from dorso-lateral sur- 
face of foot mass and passing posteriorly 
along lateral aspect of anterior byssal retrac- 
tors to become integrated with antenor and 
lateral region of anterior portion of posterior 
byssal retractors at point of shell attachment. 
Siphonal retractors integrated with palliai 
musculature, although there does appear to 
be a siphonal retractor scar on the shell. An- 
terior retractors long and slender, arising from 
dorso-lateral aspect of byssal-pedal mass 
and passing anteriorly to insert in antero-dor- 
sal extremity of umbonal cavity. Pair of slen- 
der labial palp suspensors extend forward as 
branches of anterior retractors to attach to 
shell just behind and adjacent to anterior ad- 
ductor. Posterior adductor rounded, anterior 
adductor rounded: one-half the size of poste- 
rior adductor. 

Foot and Byssus: Foot long, thick; shape in 
preserved specimens variable, dependent on 
degree of contraction. Byssal strands gray to 
brown, wide, flat, unornamented. Byssal 
gland extending down foot behind byssal 
groove, without extension dorsal to origin of 
anterior retractors. 

Mantle and Mantle Cavity: Connections be- 
tween edge of ascending lamellae and sur- 
face of mantle lobes and visceral mass weak 
or lacking, resulting in incomplete separation 
of incurrent and excurrent chambers. Lacking 
muscular longitudinal ridges for attachment of 
ascending lamellae to mantle lobes and vis- 
ceral mass (see Kenk & Wilson, 1985: 260). 
Ventral edges of inner mantle lobes not un- 
usually thickened or muscular. Excurrent 
tubuliform siphon short, not capable of exten- 
sion beyond perimeter of shell, lacking inter- 
nal diaphragm in specimens examined. Hori- 
zontal branchial septum incomplete; fusion of 
inner mantle immediately below excurrent 
siphon forming short horizontal shelf, not di- 
rectly attached to ventral edge of posterior ad- 
ductor. Incurrent and excurrent chambers not 
completely separated posterior of posterior 
adductor; posterior end of gill axes attached 



NEW DEEP-SEA MUSSELS 



75 



Bathymodiolus brooksi (X1 ) 




50 mm 



'Idas" macdonaldi (X1 0) 




"Bathymodiolus" childressi (XI ) 



Tamu fisheri (X2) 





FIG. 11. Bathymodiolus heckerae, B. brooksi, "Bathymodiolus" childressi, Tamu fisheri, and "Idas" mac- 
donaldi. Inset outlines of a graded series of shell outlines illustrating change in shape with increase in size. 
Only one specimen of "Idas" macdonaldi is illustrated. Dotted lines connect the relative positions of the an- 
terior edge of the umbones in specimens of different size. Note scale bar and magnifications. 



to ventral surface of horizontal branchial sep- 
tum. Short extension as valvular siphonal 
membrane joins right and left mantle lobes, 
extending anteriorly only a short distance into 
pedal gape; small central papilla on anterior- 
most ventral extension of valvular siphonal 
membrane extends anteriorly into pedal gape. 
Pedo-byssal gape extensive; incurrent aper- 
ture extending from anterior end of valvular 
siphonal membrane to posterior edge of ante- 
rior adductor. 

Ctenidia: Demibranchs thick, short; approxi- 
mately equal-sized, both demibranchs extend 
anteriorly to same degree; ascending lamel- 
lae slightly shorter than descending. Ventral 
edges of demibranchs with poorly developed 
food grooves; dorsal food grooves present in 
deep folds just below junction of ascending 
lamellae and areas of attachment to mantle 
lobes and visceral mass. Filaments wide, 
fleshy; ctenidia and filaments light-brown. Dis- 
tal interlamellar junctions lacking; descending 
and ascending portion of each filament con- 



nected apically to one-quarter height of demi- 
branch; every 2nd to 6th filament is "principal 
filament" [see Atkins, 1937: text fig. 18, type 
B(1 b)] with septum rising to one-third height of 
demibranch. A single posterior "tubular con- 
nection" (see Kenk & Wilson, 1985) between 
free edges of ascending lamellae and gill 
axes sometimes present, indiscernible in 
some individuals. 

Labial Palps: Paired labial palps greatly mod- 
ified from typical filter-feeding type, appearing 
to function as sorting area for material gath- 
ered by foot rather than ctenidia. Base of 
inner and outer palp pair widely separated; 
ctenidia lie lateral of labial palps in preserved 
specimens. Mouth situated at basal mid-point 
of anterior end of inner pair of labial palps, far- 
ther posterior than typical for mytilids. Inner 
palp pair placed posteriorly, large and muscu- 
lar, elongately triangular. Outer pair of palps 
more anterior, triangular, muscular, but 
smaller than inner pair. Oral groove on inner 
surface of both pair of palps, bordered by pli- 



76 



GUSTAFSONETAL 



Bathymodiolus brooksi (X1 ) 




50 mm 



Bathymodiolus heckerae (X1) 



"Idas" macdonaldi (X10) 





"Bathymodiolus" childressi (XI ) 



Tamu fisheri (X2) 





FIG. 12. Bathymodiolus heckerae, B. brooksi, "Bathymodiolus" childressi, Tamu fisheri, and "Idas" mac- 
donaldi. Diagrams of left-lateral view of shell illustrating generalized location of muscle scars, palliai line and 
ligament. Lighter shading anterior and posterior to ligament in diagram of "Idas" macdonaldi indicates loca- 
tion of adult hinge denticles. Note scale bar and magnifications. 



cations, running from near tip of proboscid- 
like extensions to mouth. Outer surfaces of 
palps smooth, non-plicate. 

Digestive System: Alimentary tract straight 
with no recurrent loop, situated directly on 
body mid-line. Intestine leaves posterior end 
of stomach and traverses short distance pos- 
teriorly, merging with rectum; rectum enters 
extreme antero-ventral aspect of pericardium 
and ventricle, anterior to the level of the auric- 
ular openings into the ventricle. 

Remarks: Bathymodiolus heckerae lacks 
both the extensive mid-ventral mantle fusion 
and the muscular longitudinal ridge in the 
mantle cavity, supporting the ascending 
lamellae, which are diagnostic characters of 
B. thermophilus. Bathymodiolus heckerae dif- 
fers from B. brooksi in having a more arcuate 
shape, a greater relative shell length anterior 
to the umbo (A/L), larger and more prominent 



pedal retractors, and a smaller height to 
length ratio at a given length (Fig. 28). It dif- 
fers from "Bathymodiolus" childressi in having 
umbones more distant from the anterior, a 
less robust shell, widely separated posterior 
byssal retractors and associated scars, and a 
central papilla on the anterior rim of the valvu- 
lar siphonal membrane. 

Relationship with B. brevier, B. elongatus, 
and B. puteoserpentis (which were placed in 
this genus only provisionally) is difficult to as- 
sess since we know little about the internal 
anatomy of these species (Cosel et al., 1 994), 
although the recently reported presence of 
two recurrent loops in the intestine of B. 
puteoserpentis (Cosel et al., 1997) distin- 
guishes this species from B. heckerae and 
other mussels examined in this report. Bathy- 
modiolus heckerae differs from these three 
species in being much more arcuate and 
elongated (Cosel et al., 1994). The shell 
shape of adult B. heckerae is also much more 



NEW DEEP-SEA MUSSELS 77 

Bathymodiolus brooksi (X 1 ) " Idas" macdonaldi (X 1 0) 




Bathymodiolus heckerae (X1 ) 

PR 




AR 



LPS 




Sri PPR 



"Bathymodiolus" childressi (X1 ) 



Tamu fisher! (X2) 




50 mm 




FIG. 13. Bathymodiolus heckerae, B. brooksi, "Bathymodiolus" childressi, Tamu fisheri, and "Idas" mac- 
donaldi. Foot and retractor muscle masses as viewed from a left-lateral orientation. Anterior is to the left. Note 
scale bar and magnifications. AR, anterior byssal-pedal retractor; APR, anterior portion of posterior byssal 
retractor; B, byssus; F, foot; LPS, labial palp suspensor; PPR, posterior portion of posterior byssal retractor; 
PR, pedal retractor. 



arcuate than any of the four Bathymodiolus 
species (platifrons, japonicus, aduloides, and 
septemdierum) from deep-sea sites off 
Japan. Bathymodiolus heckerae also differs 
from B. platifrons in having subterminal um- 
bones (located between 6% and 16% of the 
anterior end of the shell) in comparison to the 
terminal umbones of B. platifrons (Hashimoto 
& Okutani, 1994). 

In a protein electrophoretic study, Craddock 
et al. (1995) showed that B. heckerae (as 
FL/Va) and B. thermophilus (as MB/Bt) had no 
shared alleles at 17 of 26 gene loci and that 
these two species had a Nei's genetic dis- 
tance (D) of 1.085 (Nei, 1978). Nei's genetic 
distance between B. heckerae, from the West 
Florida Escarpment site, and the two popula- 
tions of B. brooksi from the West Florida Es- 
carpment and Alaminos Canyon sites were 
0.528 and 0.719, respectively. These genetic 
distances are within the range of values for 



species-level separation. Bathymodiolus 
heckerae was more highly divergent in pair- 
wise comparisons with "Bathymodiolus" chil- 
dressi (D = 2.188 and 2.086 for Bush Hill and 
Alaminos Canyon samples), T. fisheri (D = 
1.983), and "Idas" macdonaldi (D = 2.556) 
(Table 8; Craddock et al., 1995). 

Analysis of a 246 bp region of the mtDNA 
COI gene showed a sequence divergence of 
14.7% between B. heckerae and B. brooksi, 
and 17.6% to 18.7% between B. heckerae 
and "Bathmodiolus" childressi (Table 8; W. R. 
Hoeh, unpublished data). Percent sequence 
divergence between B. heckerae and T. fish- 
eri was 52.2%, and 44.9% between B. heck- 
erae and "Idas" macdonaldi (Table 8). These 
levels of allozymic and mtDNA divergence 
support separate species status for B. heck- 
erae, as well as separation at the generic 
level from T. fisheri and "Idas" macdonaldi. 

Two genetically (Cavanaugh, 1992; Ca- 



78 



GUSTAFSONETAL. 



TABLE 8. Genetic distance matrix. Nei's (1 978) unbiased genetic distance (above diagonal) based on 
26 allozyme loci (from Craddock et al., 1995). Percent sequence divergence (below diagonal) for 246 
bp of mitochondrial CO! (W. R. Hoeh, unpublished data). Site and Operational Taxonomic Unit (OTU) 
designations as in Craddock et al. (1995). la, Ib = "Bathymodiolus" childressi; II, Vb = Bathymodiolus 
brooksi; ill = Tamu fisheri; IV = "Idas" macdonaldi; Va = B. heckerae; BH = Bush Hill, Louisiana 
Continental Slope; AC = Alaminos Canyon; GB = Garden Banks. Louisiana Continental Slope; FL = 
West Florida Escarpment. 



Site/OTU 


BH/la 


AC/lb 


AC/II 


GB/III 


GB/IV 


FL/Va 


FL/Vb 


BH/la 


— 


0.042 


1.507 


2.209 


2.656 


2.188 


2.531 


AC/lb 


0.83 


— 


1.531 


2.138 


2.570 


2.086 


2.434 


AC/II 


17.16 


17.16 


— 


1.992 


5.688 


0.719 


* 


GB/III 


48.74 


47.91 


50.28 


— 


1.859 


1.983 


2.552 


GB/IV 


44.95 


43.37 


41.85 


37.97 


— 


2.556 


3.258 


FL/Va 


17.63 


18.73 


14.73 


52.22 


44.95 


— 


0.528 


FL/Vb 


17.16 


17.16 


0.00 


50.28 


41.85 


14.73 


- 



*Some minor allozyme differences may exist but they remain to be adequately resolved. 



vanaugh et aL, 1992) and morphologically 
distinct (Cavanaugh et al., 1987) bactena are 
found within gill bacteriocytes of B. heckerae. 
One of these is a large coccus, about 1 .6 am 
in diameter, wWh stacked internal membranes 
typical of Type I methanotrophs and the other 
is a smaller coccus or rodshaped cell, about 
0.4 um in diameter, without internal mem- 
branes. Stable carbon isotope ratios, meth- 
anol dehydrogenase activity, and the pres- 
ence of a gill symbiont with stacked internal 
membranes indicate that B. heckerae relies 
on its methanotrophic symbionts to some de- 
gree as a source of carbon and energy (Ca- 
vanaugh et al., 1987; Cary et al., 1989). 

Many but not all specimens of B. heckerae 
harbor a commensal polynoid polychaete 
Branchipolynoe seepensis Pettibone, 1986, 
within the mantle cavity. A second polychaete, 
the nautiliniellid Laubierus mucronatus Blake, 
1993, has also been described from the man- 
tle cavity of B. heckerae (Blake, 1993). An ad- 
ditional nautiliniellid Flascarpia alvinae Blake, 
1993, is present at the West Florida Escarp- 
ment site but its supposed bivalve host has 
not been determined (Blake, 1993). 

An electrophoretic analysis of B. heckerae 
at this site (Craddock et al., 1991, 1995) re- 
vealed the presence of a single individual of a 
morphologically distinct congeneric mussel. 
Subsequently, eight additional specimens of 
this congener B. brooksi (described herein) 
were identified. Other faunal components of 
this site include the vestimentiferan Escarpia 
laminata Jones, 1985: the bresiliid shrimp 
Alvinocaris muricola Williams, 1988; the ne- 
olepetopsid limpet Paralepetopsis floridensis 
McLean, 1990; an undescribed vesicomyid bi- 
valve, a coiled archaeogastropod, a large 



white turrid gastropod, serpulid polychaetes, 
galatheid crabs, anemones, holothuhans, 
ophiuroids, and zoarcid fish (Pauli et al., 
1984; Hecker, 1985). Newly settled В. heck- 
erae are often found attached by byssal 
threads within the eroded apices of the un- 
named small coiled archaeogastropods which 
themselves are found crawling on the adult 
mussel shells at this site (Turner & Lutz, 1 984; 
Turner, 1985). The small prodissoconch I and 
large prodissoconch II of B. heckerae sug- 
gests a planktotrophic mode of larval devel- 
opment (Turner & Lutz, 1984). 

Etymology: The specific name honors Dr. Bar- 
bara Hecker who was among the first scien- 
tists to describe the cold-water seep fauna of 
the West Florida Escarpment. The working 
designation "Seep Mytilid Va" was given to 
this species. 

Range: Known only from cold-water methane/ 
sulfide seeps at the base of the West Florida 
Escarpment in the eastern Gulf of Mexico 
near 26°02'N and 84°55'W, in depths from 
3243 to 3314 m (Table 3). 

Bathymodiolus brooksi Gustafson, Turner, 
Lutz & Vrijenhoek, new species 
Figures 11-15 

This species, known since 1990, has been 
referred to in literature concerning seep and 
vent biology but was never formally de- 
scribed. The following is a list of these refer- 
ences. 

"Mussels" (in part) - Brooks et al., 1990: 
1772. 



NEW DEEP-SEA MUSSELS 



79 





D 



y.,«^.^, m - 



■^|s«^ 



\ ... ^ 



.5 cm 




FIG. 14, Bathymodiolus brooksi Gustafson, Turner, Lutz & Vrijenhoek. Holotype, ANSP A18847. A, anterior 
view; B, posterior view; C, dorsal view; D, ventral view; E, lateral view of right valve; F, lateral view ot left 
valve. 



80 



GUSTAFSON ETAL. 








2.5 cm 



FIG. 15. Bathymodiolus brooksi Gustafson, Turner, Lutz & Vrijenhoek. External views of a growth series of 
shiells illustrating ontogenetic change in shape. 



"Alaminos Canyon more common mussel" - 
Craddocketal., 1991:302. 

"West Florida Escarpment mussel (one indi- 
vidual)" - Craddock et al., 1991 : 302. 

"Alaminos Canyon sp. A" - Fisher et al., 1 991 : 
134A. 

"Seep mytilid II," "Seep mytilid Vb" - Fisher, 
1993:609. 

"Seep Mytilid 11," "SM II" - Fisher et al., 1993: 
278, 280-287, fig. 1 [mussels in habitat 
photo], figs. 2, 3 [micrographs of symbi- 
otic bacteria in gills]. 

"AC/II, FL/Vb" - Craddock, et al., 1995: 
479-483. 

"Seep Mytilid 11" - Nelson & Fisher, 1995: 
134, table 3. 

Types: Holotype ANSP AI 8847 from ALVIN 
Dive 2211 in the western Gulf of Mexico at a 
hydrocarbon seep in Alaminos Canyon at 
26°21 .3'N; 94°29.7'W in 2222 m. A number of 
paratypes (ANSP 400775, USNM, MCZ, 
HMNS, MNHN) are from the same dive and 
locality. Additional paratypes are from ALVIN 
Dive 2209 in Alaminos Canyon at 26°21 .1 N; 
94°30.3'W in 2340 m (ANSP 400774, USNM, 
MCZ, HMNS) and from the base of the West 
Florida Escarpment in the eastern Gulf of 
Mexico from ALVIN Dive 2196 at 26°02.4'N: 
84°54.4'W in 3314 m (ANSP 400777), and 



ALVIN Dive 2542 at 26°01.8'N; 84°54.6'W in 
3313 m (ANSP 400776, USNM, HMNS). 

Shell Morphology: Shell large, up to 180 mm 
long, modioliform, elongate, elliptical, thin and 
fragile, essentially equivalve. Anterior margin 
moderately rounded: posterior margin broadly 
rounded; ventral margin straight in young 
specimens, with slight ventral concavity in 
medium sized specimens, concavity more 
pronounced in larger specimens: dorsal mar- 
gin very broadly convex, more or less straight 
over span of the ligament (Figs. 11, 12, 14, 
15). Umbones of largest specimens eroded; 
prosogyrate; subterminal, positioned within 
anterior one-tenth. An indistinct, raised, 
broadly rounded ridge extends from umbonal 
region to posterior-ventral margin. 

External surface sculpture lacking, smooth 
except for concentric growth lines, fine radial 
lines in periostracum extending from umbo to 
ventral margin, and fine radial periostracal 
corrugations in the median ventral area. Shell 
dull-white beneath dark-brown to straw-yel- 
low periostracum. Periostracum often marked 
by irregularly shaped dark brown pigment 
patches, overlain by numerous byssal thread 
attachment plates. Interior off-white, predomi- 
nately nacreous. 

Ligament opisthodetic, parivincular, ex- 



NEW DEEP-SEA MUSSELS 



81 



tending posteriorly from umbones to occupy 
from 41% to 59% of dorsal margin. Adult 
hinge edentulous, except for posteriorly di- 
rected projection of anterior hinge margin be- 
neath anterior end of ligament, hinge thick- 
ened below and anterior to umbo. Hinge 
denticles absent in smallest specimen (36 
mm length) observed. 

Muscle Scars: Anterior adductor scar rounded 
but truncated posteriorly, located below and 
partially anterior to umbo, distant from antero- 
ventral margin. Posterior adductor scar round, 
contiguous with small siphonal retractor scar 
ventrally and posterior portion of posterior 
byssal retractor scar dorsally. Anterior retrac- 
tor scar located in posterior portion of umbonal 
cavity. Posterior byssal retractors form two 
scars with large intervening gap; anterior one 
elliptical, directly beneath or slightly anterior of 
posterior end of ligament; second one ellipti- 
cal, parallel to antero-postehor axis of shell 
and located antero-dorsally to and bordering 
posterior adductor scar (Fig. 12). Palliai line 
distant from shell margin, extending from pos- 
tero-ventral edge of anterior adductor scar to 
posterior adductor, curving slightly upwards 
and then more strongly downwards to form an 
indentation in byssal gape region at about 
one-quarter to one-third of distance from ante- 
rior; small siphonal retractor scar located at 
posterior end of ventral palliai line, usually but 
not always contiguous with posterior adductor. 



Measurements (in mm): 












anterior 






length 


height 


width 


length 


Dive 




121.3 


46.8 


35,4 


~ 


A2211 


Holotype 
ANSP 


152.0 


60.3 


45.8 


12,6 


A 2211 


Paratype 
MCZ 


142.2 


54.4 


39.7 


11,3 


A 2211 


Paratype 
USNM 


125.9 


48.6 


44.5 


9,0 


A 2211 


Paratype 
MNHN 


40.0 


20.3 


13.0 


2.7 


A2211 


Paratype 
ANSP 


171.0 


64.9 


49.0 


10.5 


A 2209 


Paratype 
MCZ 


132.7 


48-4 


36.0 


12.7 


A 2209 


Paratype 
MCZ 


116.4 


44.6 


30,5 


9.3 


A 2209 


Paratype 
MCZ 


141.4 


51.0 


38,9 


11.3 


A 2209 


Paratype 
ANSP 


166.0 


61.8 


44,0 


14,4 


A 2209 


Paratype 
Rutgers 


132.3 


54.4 


40,3 


9,4 


A2211 


Paratype 
MNHN 



146,0 


49.5 


42.0 


12.5 


A 2209 


Paratype 
Rutgers 


143.4 


55.5 


42.0 


13.0 


A 2209 


Paratype 
HMNS 


106.3 


42.2 


34.7 


8.8 


A2211 


Paratype 
Rutgers 


855 


35.7 


24,6 


50 


A2196 


Paratype 
ANSP 


127.7 


55.4 


40,1 


9.0 


A 2542 


Paratype 
USNM 


117.5 


42.4 


30.0 


60 


A 2542 


Paratype 
HMNS 


88.2 


36.7 


28.6 


5.2 


A 2542 


Paratype 
ANSP 



Internal Morphology 

Musculature: Main features of musculature 
evident from previous description of muscle 
scars and Figure 13. Posterior byssal retrac- 
tors divided into two widely divergent main 
bundles that attach separately to shell, a pos- 
terior portion inserting along postero-dorsal 
edge of posterior adductor and an anterior 
portion attaching to shell just below ligament's 
posterior end. Posterior pedal retractors very 
thin, arising from antero-dorsal part of foot, 
passing lateral to anterior retractors and in- 
serting on shell anterior and lateral to poste- 
rior portion of posterior byssal retractors. 
Siphonal retractors integrated with palliai 
musculature. Anterior retractors arising from 
dorso-lateral section of byssal-pedal mass 
and passing anteriorly to insert in antero-dor- 
sal extremity of umbonal cavity. Pair of slen- 
der labial palp suspensors extend forward as 
branches of anterior retractors to attach to 
shell just behind and adjacent to anterior ad- 
ductor. Posterior adductor oblong; anterior 
adductor round in cross-section, about one- 
half size of posterior adductor. 

Foot and Byssus: Foot long, thick; shape in 
preserved specimens variable, dependent on 
degree of contraction. Byssal strands light to 
dark brown, wide, flat, unornamented. Byssal 
gland extending down foot behind byssal 
groove, without extension dorsal to origin of 
anterior byssal retractors. 

Mantle and Mantle Cavity: Connections be- 
tween edge of ascending lamellae and sur- 
face of mantle lobes and visceral mass weak 
or lacking, resulting in incomplete separation 
of incurrent and excurrent chambers. Lacking 
muscular longitudinal ridges for attachment of 
ascending lamellae to mantle lobes and vis- 
ceral mass (see Kenk & Wilson, 1985: 260). 



82 



GUSTAFSONETAL. 



Ventral edges of inner mantle lobes thick- 
ened, muscular. Excurrent tubuliform siphon 
capable of slight extension beyond perimeter 
of shell, lacking internal diaphragm in speci- 
mens examined. Horizontal branchial septum 
incomplete; fusion of inner mantle immedi- 
ately below excurrent siphon forms short hor- 
izontal shelf, not directly attached to ventral 
edge of posterior adductor. Incurrent and ex- 
current chambers not completely separated 
posterior of posterior adductor; posterior end 
of gill axes attach to ventral surface of hori- 
zontal branchial septum. Short extension as 
valvular siphonal membrane joins right and 
left mantle lobes, extending anteriorly a short 
distance into pedal gape; small central papilla 
on valvular siphonal membrane extending an- 
teriorly into pedal gape. Pedo-byssal gape ex- 
tensive; incurrent aperture extending from an- 
terior end of valvular siphonal membrane to 
posterior edge of anterior adductor. 

Ctenidia: Demibranchs approximately equal- 
sized, thick, short; ventral edges with poorly 
developed food grooves; dorsal food grooves 
present in deep folds just below junction of as- 
cending lamellae and areas of attachment to 
mantle lobes and visceral mass. Filaments 
wide, fleshy; ctenidia and filaments light- 
brown. Distal interlamellar junctions lacking; 
descending and ascending portion of each fil- 
ament connected apically to one-quarter 
height of demibranch; every 2nd to 5th fila- 
ment is "principal filament" (see Atkins, 1937: 
text fig. 18, type В [lb]) with septum rising to 
greater than one-third height of demibranch. 
Lacking "tubular connections" (see Kenk & 
Wilson, 1985) between free edges of ascend- 
ing lamellae and gill axes. 

Labial Palps: Paired labial palps broadly trian- 
gular, thick, muscular; inner pair more poste- 
rior than outer pair, but not markedly so; pli- 
cate ventral to oral groove on inner surface of 
inner palp and dorsal to oral groove on inner 
surface of outer palp; outer palp surfaces 
smooth. Mouth situated in normal anterior po- 
sition at basal junction of inner and outer 
palps. Antero-ventral portion of demibranchs 
situated between inner and outer palps coin- 
cident with plicate palp surfaces. 

Digestive System: Alimentary tract essentially 
straight, without recurrent loop, situated di- 
rectly on body mia-line. Intestine leaves pos- 
terior end of stomach and traverses posteri- 
orly ventral to pericardium to a level just 



posterior to ventricle's mid-point; rectum en- 
ters pericardium and ventricle from below at 
mid-point of ventricle, but anterior to level of 
auricular openings. 

Remarks: Although specimens of B. brooksi 
from the West Florida Escarpment were more 
variable in shell shape than those from 
Alaminos Canyon, overall morphological dif- 
ferences between these were minor. Crad- 
dock et al. (1995) identified a single unique 
individual (with the OTU label FL/Vb; B. 
brooksi) among 94 specimens of FL/Va (B. 
heckerae) from this site. Once aware of the 
existence of a genotypically unique individual 
in this collection, visual examination of the 
voucher shell collection readily identified the 
lone individual. Although this one specimen 
appeared to differ genetically from all other 
deep-sea mussels examined by Craddock et 
al. (1995), analysis of additional specimens of 
FL/Vb (B. brooksi) collected from this site in 
1993 showed that these new FL/Vb samples 
did not differ from AC/II (B. brooksi from 
Alaminos Canyon), indicating that B. brooksi 
is present both at Alaminos Canyon and the 
West Florida Escarpment sites (Table 8). In 
addition, analysis of mt DNA COI sequences 
revealed that the new FL/Vb specimens from 
West Florida Escarpment were identical with 
B. brooksi from Alaminos Canyon (AC/II) 
(Table 8; W. R. Hoeh, unpublished data). 

Bathymodiolus brooksi lacks both the ex- 
tensive ventral mantle fusion and the muscu- 
lar longitudinal ridge in the mantle cavity, sup- 
porting the ascending lamellae, that are 
characteristic of B. thermophilus. Bathymodi- 
olus brooksi differs from B. heckerae in having 
a more anteriorly located umbo, a less arcu- 
ate ventral shell margin, and relatively thin 
pedal retractors. In addition, the height to 
length ratio of B. brooksi is normally greater 
than B. heckerae at a given length (Fig. 28). 
Bathymodiolus brooksi differs from "Bathy- 
modiolus" childressi in having widely sepa- 
rated anterior and posterior portions of the 
posterior byssal retractors, whereas posterior 
byssal retractors are separated into multiple 
bundles with a single muscle scar in "Bathy- 
modiolus" childressi. Bathymodiolus brooksi 
has a central papilla on the anterior margin of 
the valvular siphonal membrane, which is 
missing in "Bathymodiolus" childressi. In B. 
brooksi, the intestine is straight and the rec- 
tum enters the ventricle anterior to the auricu- 
lar ostia; whereas in "Bathymodiolus" chil- 
dressi, the intestine has a very short recurrent 



NEW DEEP-SEA MUSSELS 



83 



loop and the rectum enters the ventricle pos- 
terior to the auricular ostia. In addition, B. 
brooksi differs from "Bathymodiolus" chil- 
dressi in having a more elongate, more slen- 
der and less tumid shell shape. 

Bathymodiolus brooksi differs from B. pla- 
tifrons in having subterminal umbones (within 
3% to 10% of the anterior) in comparison to 
the terminal position of the umbo in B. pla- 
tifrons. The relative height of the posterior por- 
tion of the shell is much less in B. brooksi (H/L 
ranges from 0.34 to 0.51 ) than in B. platifrons 
(H/L range; 0.50 to 0.68) and B. japonicus 
(H/L range; 0.51 to 0.61). Bathymodiolus 
brooksi differs from B. adulcidos in having a 
straight, unlooped intestine and a central 
papilla on the valvular siphonal membrane. A 
central papilla on the valvular siphonal mem- 
brane is also lacking in B. septemdierum 
(Hashimoto & Okutani, 1994). 

Relationship between B. brooksi and B. 
brevier, B. elongatus, and B. puteoserpentis is 
difficult to assess since we know little about 
the internal anatomy of the latter three 
species (Cosel et al., 1994), although the re- 
cently reported presence of two recurrent 
loops in the intestine of B. puteoserpentis 
(Cosel et al., 1997) distinguishes this species 
from B. brooksi and other mussels examined 
in this report. Bathymodiolus brevior, B. elon- 
gatus, and B. puteoserpentis are much wider 
relative to their length than is B. brooksi; the 
ratio of width over length for B. brooksi ranges 
from 0.25 to 0.35, whereas these ratios in B. 
brevior, B. elongatus, and B. puteoserpentis 
are greater than 0.35. 

The protein electrophoretic study of Crad- 
dock et al. (1 995) showed that B. brooksi from 
Alaminos Canyon (designated as AC/II) and 
B. thermophilus (designated as MB/Bt) had 
no shared alleles at 17 of 26 gene loci and 
that these two species had a Nei's genetic dis- 
tance (D) of 1 .280. Nei's genetic distance be- 
tween B. brooksi from Alaminos Canyon and 
B. heckerae from the West Florida Escarp- 
ment site was 0.719 (Craddock et al., 1995; 
see Table 8). These genetic distances are 
within the range of values for species-level 
separation. Bathymodiolus brooksi was more 
highly divergent in pairwise comparisons with 
"Bathymodiolus" childressi (D - 1.507 and 
1.531 for Bush Hill and Alaminos Canyon 
samples), T fisheri (D = 1.992), and "Idas" 
macdonaldi (D = 5.688) (Table 8; Craddock et 
al., 1995). Bathymodiolus brooksi shared only 
8 to 9 of 26 alleles with "Bathymodiolus" chil- 
dressi, only 4 of 26 alleles with T. fisheri, and 



only 1 of 26 with "Idas" macdonaldi (Craddock 
et al., 1995). Since most congeneric group- 
ings of animals have Nei's D values less than 
2.0 (Nei, 1987), these results support generic 
separation of T. fisheri and "Idas" macdonaldi 
from B. brooksi. 

Analysis of a 246 bp region of the mtDNA 
COI gene showed a sequence divergence of 
14.7% between B. brooksi and B. heckerae, 
and 17.1% between B. brooksi and " Bathy- 
modiolus" childressi (Table 8; W. R. Hoeh, un- 
published data). Percent sequence diver- 
gence between B. brooksi and T. fisheri was 
50.3%, and 41.8% between B. brooksi and 
"Idas" macdonaldi (Table 8). These levels of 
allozymic and mtDNA divergence support 
separate species status for B. brooksi, as well 
as separation at the generic level from T fish- 
eri and "Idas" macdonaldi. 

General features of the Alaminos Canyon 
hydrocarbon/brine seep sites are presented in 
Brooks et al. (1990). Simultaneous occur- 
rence of sulfur-oxidizing and methanotrophic 
bacterial symbionts in gill tissue, as well as 
the presence of two morphological types of 
symbionts visible in transmission electron mi- 
crographs of the gill tissue, suggests that B. 
brooksi harbors both thiotrophic and methan- 
otrophic bacterial symbionts within its gill bac- 
teriocytes (Fisher et al., 1993). Specimens of 
this species from the West Florida Escarp- 
ment site also harbor two morphologically dis- 
tinct bacterial endosymbionts (C. M. Ca- 
vanaugh, pers. comm.). 

Bathymodiolus brooksi shares the Alaminos 
Canyon site with the methanotrophic mussel 
"Bathymodiolus" childressi, two species of 
vestimentiferan tubeworms, a white shrimp, 
and galatheid crabs (Brooks et al., 1 990). This 
species shares the West Florida Escarpment 
site with B. heckerae. Other West Florida Es- 
carpment site fauna are described in the re- 
marks section for B. heckerae. 

Etymology: The specific name honors Dr. 
James M. Brooks, Texas A & M University, 
who has been one of the driving forces behind 
exploration of deep-sea hydrocarbon/brine 
seeps in the Gulf of Mexico. The working des- 
ignation "Seep Mytilid 11" was given to this 
species from Alaminos Canyon and "Seep 
Mytilid Vb" to members of this species from 
the West Florida Escarpment. 

Range: Known from hydrocarbon seeps at 
Alaminos Canyon in the western Gulf of Mex- 
ico in depths from 2222 to 2340 m and from 



84 



GUSTAFSON ETAL 



cold-water methane/sulfide seeps at the base 
of the West Florida Escarpment in the eastern 
Gulf of Mexico near 26°02'N; 84°55'W in 
depths from 3270 to 3314 m (Table 4). 

"Bathymodiolus" childressi Gustafson, 
Turner, Lutz & Vrijenhoek, new species 
Figures 11-13, 16-20 

This species, known since 1985, has been 
referred to in literature concerning seep and 
vent ecology but was never formally de- 
scribed. The following is a list of these refer- 
ences. 

"Mytilid (large, brown)" - Turner, 1985; 29 
(Louisiana Slope). 

"Undescribed mussel" - Childress et al., 
1986: 1306, fig. 2 [micrographs of gill fil- 
ament and symbiotic bacteria]. 

"Mytilid" - Grassle, 1986: 339. 

"Undescribed mytilid" - Fisher et al., 1986: 
SA. 

"Mussels" - Brooks et al., 1987a: 498. 

"Mussels," "Mytilidae undescribed" - Brooks 
etal., 1987b: 1138, 1139. 

"Seep mussels," "symbiont-containing mytilid 
bivalve" Gary et al., 1988: 78, 79. 

"Undescribed hydrocarbon-seep mussels" - 
Fisher et al., 1987: 59, figs, la, lb, 2a, 
3a, 3c [micrographs of gill filaments, bac- 
teriocytes, symbiotic bacteria]. 

"Mussels from Louisiana hydrocarbon seeps" 
- Hook & Golubic, 1988: 361 -362. 

"Mussel" - Kennicutt et al., 1 988a: 44, figs. 1 , 
2 [mussels visible in habitat photos]. 

"Mussel" - Kennicutt et al., 1988b: 1639. 

"Undescribed seep mussel" - Page et al., 
1988: 192A. 

"Undescribed mussel (Mytilidae)" - Brooks et 
al., 1989:2. 

"Methane-oxidizing mussel," "Bathymodiolus- 
like," "seep mussels" - MacDonald et al., 
1989: 235, figs. 3C and 3D [mussels vis- 
ible in habitat photos]. 

"Mussels," "Mytilidae sp." - Wade et al., 
1989: 19, 22. 

"Bathymodiolus n. sp." - MacDonald et al., 
1990a: 1096, figs. 3, 4 [mussels visible in 
habitat photos]. 

"Seep mussel (Bathymodiolus n. sp.: Mytili- 
dae)" - MacDonald et al., 1990b: 248, 
fig. 4 [mussels visible in habitat photos]. 

"Methanotrophic mussels" - MacDonald et 
al., 1990c: 15, figs. 2a-c [mussels visible 
in habitat photos]. 

"Mussels" - Alper, 1990a: 536, fig. p. 537 
[mussels visible in habitat photo]. 



"Mussels" - Alper, 1990b: 23, figs. pp. 22, 26, 

28 [mussels visible in habitat photos]. 
"Undescribed seep mussel" - Page et al., 

1990:251. 
"Louisiana seep mussel" - Dahlhoff & 

Somero, 1991:475 (table 1). 
"Bathymodiolus sp." - Waren & Ponder, 

1991:54. 
"Alaminos Canyon less common mussel" - 

Craddock et al., 1991:302. 
"Alaminos Canyon sp. B" - Fisher et al., 

1991: 134A. 
"Bathymodiolus sp., undescribed" - Ko- 

chevar et al., 1992: 389, fig. 4 [micro- 
graphs of gill filament and symbiotic bac- 
teria]. 
"Bathymodiolus sp., undescribed" - Lee et 

al., 1992:99. 
"Louisiana seep mussel" - Kennicutt et al., 

1992:298. 
"Seep Mytilid la" - Fisher & Childress, 1992: 

223, fig. 2 [micrographs of bacteriocytes, 

symbiotic bacteria]. 
"LA mytilid" - Cavanaugh, 1992: 316. 
"Seep mytilid la," "Seep mytilid lb" - Fisher, 

1993:609. 
"SM la, SM lb" - Fisher et al., 1 993: 278, 280. 
"Seep Mytilid la" - Gustafson & Lutz, 1994: 

80, figs. 4.1, 4.2 [micrographs of prodis- 

soconch I and II]. 
"BH/la, AC/lb" - Craddock et al., 1995: 

479-483. 
"Seep Mytilid la," "Seep Mytilid lb" - Nelson & 

Fisher, 1995: 133-134, table 3. 
"Seep mytilid la" - Lee & Childress, 1995: 

137. 
"Seep Mytilid la" ~ Nix et al., 1995: 605, 606, 

609 613. 
"Seep mytilid la" - Lee & Childress, 1996: 

373. 
"Seep Mytilid la" Kochevar & Childress, 

1996: tables 1,2. 

Types: Holotype ANSP A18848 from JOHN- 
SON SEA-LINK-I Dive 3129, Bush Hill hydro- 
carbon seep, 27°46.9'N; 91°30.4'W, about 
210 km south southwest of Grand Isle, 
Louisiana in 546 m. The type-locality is on the 
Louisiana Continental Slope between Blocks 
184 and 185 in the Green Canyon offshore 
petroleum leasing area. Several paratypes 
(ANSP 400778, MCZ, HMNS, MNHN) are 
from the same locality. Additional paratypes 
are from JOHNSON SEA LINK-I Dive 3137 at 
27°41.1'N; 91°32.2'W in 723 m (Green 
Canyon-272) (MCZ, HMNS, MNHN); JOHN- 
SON SEA LINK-I Dive 3145 at 27°43.4'N; 
91°16.6'W in 650 m (Brine Pool NR-1) 



NEW DEEP-SEA MUSSELS 



85 




FIG. 16. "Bathymodiolus" childressi Gustafson, Turner, Lutz & Vrijenhoek. Holotype, ANSP A18848. A, ante- 
rior view; B, posterior view; C, dorsal view; D, ventral view; E, lateral view of right valve; F, lateral view of left 
valve. 



86 



GUSTAFSONETAL 






Чк. 





2.5 cm 



■■"•IP- '"^^ 



FIG. 17. "Bathymodiolus" childressi Gustafson, Turner, Lutz & Vrijenhoek. External views of a growth series 
of shells illustrating ontogenetic change in shape. 



(USNM, MCZ); and ALVIN Dive 2211 at 
26°21.3'N; 94°29.7'W in 2222 m (Alaminos 
Canyon) (ANSP 400779, USNM, HMNS, 
MNHN). 

Shell Morphology: Shell large, up to 120 mm 
long, modioliform, thin and fragile, essentially 
equivalve, elliptical in immature specimens, 
becoming increasingly arcuate in larger, old 
specimens (Figs. 11, 12, 16, 17). Anterior 
margin narrowly rounded; posterior margin 
broadly rounded; ventral margin straight to 



slightly concave in small specimens, becom- 
ing increasingly concave in larger specimens; 
dorsal margin convex (Fig. 11). Umbones 
often eroded; prosogyrate; nearly terminal to 
slightly subterminal; prodissoconch I from 100 
to 110 um in length; prodissoconch II reddish, 
385 to 404 um in length. An indistinct, raised, 
broadly rounded ridge or keel extends from 
the umbonal region to the postero-ventral 
margin. 

External sculpture lacking, surface smooth 
except for concentric growth lines and fine ra- 



NEW DEEP-SEA MUSSELS 



87 




FIG. 18. "Bathymodiolus" childressi Gustafson, Turner, Lutz & Vrijenhoek. Juvenile hinge line of specimen 
4.5 mm in length. Scale bar = 0.5 mm. 

FIG. 19. "Bathymodiolus" childressi Gustafson, Turner, Lutz & Vrijenhoek. Hinge denticles located immedi- 
ately posterior of the ligament in juvenile specimen 4.5 mm in length. 

FIG. 20. "Bathymodiolus" childressi Gustafson, Turner, Lutz & Vrijenhoek. Hinge denticles located immedi- 
ately below the umbo in juvenile specimen 4.5 mm in length. 



dial periostracal corrugations in the median 
ventral area. Shell dull-white beneath a dark- 
brown to straw-yellow periostracum. Antero- 
dorsal portion of shell variably eroded de- 
pending on age and collection site. Interior 
off-white, predominately nacreous. 

Ligament opisthodetic, parivincular, extend- 
ing posteriorly from umbones to occupy 38% 
to 58% of dorsal margin. Adult hinge edentu- 
lous, thickened below and anterior to umbo. 
Juvenile hinge with 8 to 9 denticles immedi- 
ately posterior to ligament and with 4 to 5 den- 
ticles located immediately below umbones 



(Figs. 18-20). Hinge denticles obsolete in 
specimens greater than 11 mm in length. 

Muscle Scars: Muscle scars and palliai line in- 
distinct. Anterior adductor scar oblong, below 
and posterior to the umbo; posterior adductor 
scar round, contiguous dorsally with single 
posterior byssal-pedal retractor scar; anterior 
retractor scar located in posterior portion of 
umbonal cavity; posterior byssal retractors 
forming continuous scar extending from di- 
rectly beneath posterior end of ligament to an- 
tero-dorsal edge of posterior adductor scar 
(Fig. 12). Ventral palliai line straight, well 



88 



GUSTAFSON ETAL 



inset, paralleling the ventral shell nnargin and 
extending from postero-ventral edge of ante- 
rior adductor scar to posterior adductor. 

Selected measurements (in mm): 

anterior 
length height width length Dive 

88.7 46.1 37.7 - JSL3129 Holotype 

ANSP 

83.3 43.3 29.6 1.1 JSL3129 Paratype 

MNHN 

73.4 39.5 30.0 3.8 JSL3129 Paratype 

ANSP 

67.6 36.5 29.3 2.6 JSL3129 Paratype 

Rutgers 
86.1 44.3 36.5 2.1 JSL3137 Paratype 

HMNS 
123.6 58.4 46.0 4.5 JSL3145 Paratype 

USNM 
118.5 53.3 46.0 2.4 JSL3145 Paratype 

MCZ 
45.9 23.4 20.5 0.2 A 2211 Paratype 

HMNS 

56.7 30.2 25.2 1.3 A 2211 Paratype 

Rutgers 

63.5 32.6 28.6 2.7 A 2211 Paratype 

ANSP 
106.8 48.9 41.5 2.3 JSL3145 Paratype 

USNM 
94.1 45.5 39.4 4.2 JSL3137 Paratype 

Rutgers 
78.4 39.6 28.5 1.5 JSL3129 Paratype 

HMNS 

90.6 45.5 37.6 2.5 JSL3137 Paratype 

MNHN 
61.4 30.7 28.1 1.1 JSL3137 Paratype 

MNHN 

Internal Morphology 

Musculature: Although the posterior byssal 
retractors form one continuous muscle scar in 
each valve (see description above, Fig. 12), 
posterior byssal retractors are subdivided into 
six main muscle bundles (Fig. 13). Posterior 
pedal retractors small, thin, arising from an- 
tero-dorsal portion of the foot mass and pass- 
ing lateral to anterior bundle of posterior 
byssal retractors. Siphonal retractors not evi- 
dent. Anterior retractors arising just ventral to 
origin of anterior portion of posterior byssal re- 
tractors on dorsal surface of byssal-pedal 
mass and passing anteriorly to insert in pos- 
terior portion of umbonal cavity (Fig. 13). 
Paired labial palp suspensors slender, ex- 
tending forward as branches of anterior re- 
tractors to attach just behind and adjacent to 
anterior adductor. Posterior adductor oblong; 
anterior adductor small, round in cross-sec- 
tion. 



Foot and Byssus: Foot thick; shape in pre- 
served specimens variable, dependent on de- 
gree of contraction. Byssal strands light-to 
dark-brown, wide, flat, unornamented. Byssal 
gland extending down foot behind byssal 
groove. 

Mantle and Mantle Cavity: Connections be- 
tween edge of ascending lamellae and surface 
of mantle lobes and visceral mass weak or 
lacking, resulting in incomplete separation of 
incurrent and excurrent chambers. Lacking 
muscular longitudinal ridges for attachment of 
ascending lamellae to mantle lobes and vis- 
ceral mass (see Kenk & Wilson, 1985: 260). 
Ventral edges of inner mantle lobes thickened 
and muscular. In life, excurrent tubuliform 
siphon capable of moderate extension beyond 
end of shell. Lacking horizontal branchial sep- 
tum between incurrent and excurrent cham- 
bers; incurrent and excurrent chambers not 
physically separated posterior to the posterior 
adductor. Posterior end of gill axes attach to 
inner wall of fused inner mantle lobes just ven- 
tral to excurrent siphon. Short valvular sipho- 
nal membrane joins right and left lobes, ex- 
tending anteriorly a short distance into pedal 
gape; anterior edge of valvular siphonal mem- 
brane smooth, lacking central papilla. Pedo- 
byssal gape extensive; incurrent aperture ex- 
tending from anterior end of valvular siphonal 
membrane to posterior edge of anterior ad- 
ductor. 

Ctenidia: Demibranchs approximately equal- 
sized, tall, fleshy; ventral margins with well- 
developed food grooves; dorsal food grooves 
in deep folds just below the junction between 
the ascending lamellae and both the mantle 
lobes and the visceral mass. Ctenidia off- 
white; filaments thin for the group examined in 
this report, but broader than typical for 
mytilids. Distal interlamellar junctions lacking; 
descending and ascending portion of each fil- 
ament connected apically to one-quarter 
height of demibranch; every 2nd to 6th fila- 
ment is a "principal filament" (see Atkins, 
1937: text fig. 18, type B[1b]) exhibiting short 
interlamellar septum extending dorsally to a 
slight degree. Lacking "tubular connections" 
(see Kenk & Wilson, 1985) between free 
edges of ascending lamellae and gill axes. 

Labial Palps: Paired labial palps greatly mod- 
ified from the typical filter-feeding type, ap- 
pearing to function as sorting area for mater- 
ial gathered by the foot rather than the 



NEW DEEP-SEA MUSSELS 



89 



ctenidia. Base of inner and outer palp pair 
widely separated. Inner pair placed farther 
posteriorly, large and muscular with long pro- 
boscid-like extension of far posterior end. 
Mouth situated at basal mid-point of anterior 
end of inner pair of labial palps, farther poste- 
rior than typical for mytilids. Outer pair of 
palps more anterior, triangular, muscular, but 
smaller than inner pair with shorter proboscid- 
like extension. 

Digestive System: Stomach and direct intes- 
tine situated left of the mid-line; rectum on 
mid-line posterior to entry into ventricle. Intes- 
tine leaves posterior end of stomach and tra- 
verses a short distance posteriorly to the left 
of the mid-line; intestine/rectum with a very 
short recurrent loop, which turns in a clock- 
wise direction when viewed dorsally, just prior 
to turning upwards to enter the ventral aspect 
of the ventricle just posterior to the auricular 
ostia. 

Remarks: "Bathymodiolus" childressi pos- 
sesses a combination of morphological char- 
acters not seen in any previously described 
deep-sea mytilid genus; however, genetic dis- 
tance measures (Nei's D and percent se- 
quence divergence for 246 bp of the mtDNA 
COI gene) do not clearly separate this 
species from other members of the genus Ba- 
thymodiolus. So as to avoid erecting a new 
mono-specific genus, this species is provi- 
sionally placed in Bathymodiolus. Specimens 
of "Bathymodiolus" childressi previously des- 
ignated Seep Mytilid la (Louisiana Continental 
Slope) and lb (Alaminos Canyon) appear 
identical in all particulars and are here re- 
garded as conspecific. 

"Bathymodiolus" childressi differs from all 
other species referred to Bathymodiolus in 
having multiple separation of the posterior 
byssal retractors (similar to what is seen in 
Modiolus), a single posterior byssal retractor 
scar, and a rectum that enters the ventricle 
posterior to the level of the auricular ostia. 
"Bathymodiolus" childressi differs from B. 
heckerae and B. brooksi in having a more an- 
teriorly located umbo, a recurrent intestinal 
loop, and lacking a papilla on the valvular 
siphonal membrane. "Bathymodiolus" chil- 
dressi differs from all other Bathymodiolus 
species, except B. platifrons, in having the 
umbo located at the extreme anterior end of 
the shell, in an almost terminal position. Al- 
though superficially similar to B. platifrons, 
"Bathymodiolus" childressi differs from B. 



platifrons in having a single posterior byssal 
retractor scar, a rectum that enters the ventri- 
cle posterior to the level of the auricular ostia, 
a recurrent intestine, and lacking a papilla on 
the valvular siphonal membrane (Hashimoto 
&Okutani, 1994). 

The protein electrophoretic study of Crad- 
dock et al. (1995) showed that "Bathymodio- 
lus" childressi (designated as AC/lb and 
BH/la) and B. heckerae (designated as 
FL/Va) had pairwise Nei's D values of 2.086 
and 2.188, whereas comparison of these two 
populations of "Bathymodiolus" childressi with 
B. brooksi (designated as AC/II) yielded D val- 
ues of 1 .531 and 1 .507, respectively. Pairwise 
comparison of the two "Bathymodiolus" chil- 
dressi populations and B, thermophilus (des- 
ignated as MB/Bt) yielded Nei's D values of 
1.831 and 1.833 (Craddock et al., 1995; Table 
8). These genetic distances straddle the 
range of values for species-level separation 
and are not sufficient evidence to support 
erection of a new genus for "Bathymodiolus" 
childressi. 

The two populations of "Bathymodiolus" 
childressi were more highly divergent in pair- 
wise comparisons with T fisheri (D = 2.209 
and 2.138), and "Idas" macdonaldi (D = 2.656 
and 2.570) (Table 8; Craddock et al., 1995). 
Since most congeneric groupings of animals 
have Nei's D values less than 2.0 (Nei, 1987), 
these results support generic separation of T. 
fisheri and "Idas" macdonaldi from "Bathy- 
modiolus" childressi 

Analysis of a 246 bp region of the mtDNA 
COI gene showed a sequence divergence of 
17.6% to 18.7% between "Bathymodiolus" 
childressi and B. heckerae, and 17.2% be- 
tween "Bathymodiolus" childressi and B. 
brooksi (Table 8; W. R. Hoeh, unpublished 
data). Sequence divergence between "Bathy- 
modiolus" childressi and T fisheri ranged from 
47.9% to 48.7%. Similar values for "Bathy- 
modiolus" childressi and "Idas" macdonaldi 
ranged from 43.4% to 45.0% (Table 8). These 
levels of mtDNA divergence support separate 
species status for "Bathymodiolus" childressi, 
and separation at the generic level from T 
fisheri and "Idas" macdonaldi. 

"Bathymodiolus" childressi occurs over a 
depth range of at least 1670 m, which is not 
remarkable considering that Knudsen (1970) 
recorded at least 15 abyssal and hadal bi- 
valves with depth ranges greater than 2000 m 
and numerous other deep-sea bivalves with 
similar or greater vertical distributions are on 
record (references in Allen, 1983). 



90 



GUSTAFSON ETAL 



"Bathymodiolus" childressi from both the 
Louisiana Continental Slope and Alaminos 
Canyon contain methanotrophic symbionts in 
their gills (Fisher, 1993), which provide a 
source of carbon and energy to the host mus- 
sel via oxidation of environmental methane 
(Childress et al., 1986; Fisher et al., 1987). In- 
tracellular bacteria are limited to bacteriocytes 
within the gill filaments and have internal 
membrane structures typical of Type I 
methanotrophs (Childress et al., 1986; Fisher 
et al., 1987). Analysis of 16S rRNA gene se- 
quence data reveals the presence of only a 
single bacterial species in "Bathymodiolus" 
childressi (Cavanaugh, 1992). 

The labial palp suspensors of "Bathymodio- 
lus" childressi provide support for the large 
labial palps. Although rare in the Mytilidae in 
general, similar muscles occur in the deep sea 
mytilids Dacrydium ockelmanni Mattson & 
Waren, 1977 (mislabelled "pedobyssal retrac- 
tors"), D. angulare Ockelmann, 1983 ("labial 
palp suspensors") and B. thermophilus ("labial 
palp muscles") (Kenk & Wilson, 1985), as well 
as in B. heckerae and B. brooksi described in 
this report. 

The fine scale distribution of "Bathymodio- 
lus" childressi at hydrocarbon/brine seeps on 
the Louisiana Continental Slope is signifi- 
cantly correlated with methane concentra- 
tion (MacDonald et al., 1989). Living mussels 
occur in clusters near gas vents, around areas 
of general fluid discharge where seeping brine 
may be a carrier of methane (MacDonald et 
al., 1989, 1990a), and around brine-filled de- 
pressions on the sea-floor where the density of 
brine (up to 3.5 times normal seawater) traps 
methane in close proximity to oxygen laden 
seawater (MacDonald et al., 1990c). Although 
"Bathymodiolus" childressi form discrete beds 
on soft sediments and among carbonate 
outcrops, they also occur on and among 
clumps of the vestimentiferan tubeworm La- 
mellibrachia sp. (MacDonald et al., 1 989). Two 
other species of mussel, T fisheri and "Idas" 
macdonaldi co-occur with "Bathymodiolus" 
childressi at some sites on the Louisiana 
Continental Slope, but they are far less com- 
mon and were only recently recognized 
(Fisher & Childress, 1992; I. R. MacDonald, 
pers. comm.). Other fauna associated with 
"Bathymodiolus" childressi at Louisiana Conti- 
nental Slope sites include the trochid gastro- 
pod Cataegis meroglypta McLean & Quinn, 
1987; the nerite gastropod Bathynerita nati- 
coidea Clarke, 1989; the shrimp Alvinocaris 
stactophila Williams, 1988; and the crabs 



Rochinia crassa (A. Milne Edwards, 1879), 
Benthochascon schmitti Rathbun, 1931, and 
Munidopsis sp. (MacDonald et al., 1989, 
1990a, с). 

Published information on communities at 
Alaminos Canyon are scanty but we know 
that "Bathymodiolus" childressi shares this 
site with the mussel B. brooksi, vestimen- 
tiferan tubeworms, galatheid crabs, and 
swarms of white shrimp. 

Numerous, round, white-rimmed, egg cap- 
sule scars (or the egg capsules themselves) 
are often found on the posterior and postero- 
dorsal portion of the shell of "Bathymodiolus" 
childressi from Bush Hill, Green Canyon, and 
Brine Pool NR-1. These capsules are de- 
posited by Bathynerita naticoidea (C. R. 
Fisher, pers. comm.). 

Micrographs depicting the prodissoconchs I 
and II of "Bathymodiolus" childressi have been 
published in Gustafson & Lutz (1 994: figs. 4.1 , 
4.2). The prodissoconch I length of 100 to 110 
um, the prodissoconch II length of 385 to 404 
um and the sculpture of concentric growth 
lines on the prodissoconch II are consistent 
with characteristics indicative of planktotro- 
phic development (Gustafson & Lutz, 1994). 

Etymology: The specific name honors Dr. 
James J. Childress, University of California - 
Santa Barbara, whose seminal work on the 
physiology of this species revealed its re- 
liance on a methane-based symbiosis with in- 
tracellular bacteria (Childress et al., 1986). 
The working designation "Seep Mytilid la" was 
given to this species from the Louisiana seeps 
and "Seep Mytilid lb" to members of this 
species from Alaminos Canyon. 

Range: Known from the northern Gulf of Mex- 
ico on the Louisiana Continental Slope in 546 
to 737 m and from the western Gulf of Mexico 
at Alaminos Canyon in 2222 m (Table 5). 

Tamu Gustafson, Turner, Lutz & Vrijenhoek, 
new genus 

Type species: Tamu fisheri Gustafson, Turner, 
Lutz & Vrijenhoek, new species. 

Description: Shell smooth, modioliform, with 
sub-terminal umbones; adult hinge edentu- 
lous, juvenile hinge with small denticulations 
anterior and posterior to ligament; posterior 
retractors divided into anterior and posterior 
portions, posterior retractor scars separate; 
small pedal retractors present; mantle open 
ventrally; demibranchs of ctenidia hypertro- 



NEW DEEP-SEA MUSSELS 



91 



phied and fleshy, filaments broadly thickened, 
with well-developed ventral food grooves; 
symbiotic bacteria associated with external 
gill surfaces; intestine with a short recurrent 
loop beneath the ventricle, rectum entering 
ventricle anterior to the auricular ostia. 

Remarks: Tamu possesses a combination of 
morphological characteristics not seen in any 
existing mytilid genus (Table 9) and exhibits 
genetic distance measures (Nei's D and per- 
cent sequence divergence for 246 bp of the 
mtDNA COI gene) that clearly separate the 
type species from the genus Bathymodiolus 
(Table 8). Comparison of Tamu with existing 
genera is hampered by the fact that most 
deep-sea mytilid genera have been described 
without benefit of anatomical studies; in many 
cases, surviving type specimens consist of 
shell material only. Tamu differs from Bathy- 
modiolus in having thickened gills that contain 
symbiotic bacteria in "pockets," open to the 
mantle cavity; by its relatively small size; and 
by the absence of palp suspensors. Tamu dif- 
fers from Idas and Adipicola in having poste- 
rior byssal retractors that are divided into an- 
terior and posterior portions and in loosing the 
hinge denticulations at maturity. Tamu further 
differs from Idas (as represented by putative I. 
argenteus, the type species, and I. washing- 
tonia) in having thickened versus filamentous 
gills, lateral versus medial placement of the 
pedal retractors (relative to the posterior 
byssal retractors), and outer and inner demi- 
branchs of equal length. Tamu further differs 
from Adipicola (as represented by Adipicola 
sp. from the Middle Valley hydrothermal vent 
site on the Juan de Fuca Ridge in the north- 
west Pacific) in having separate pedal retrac- 
tors that are not integrated with the posterior 
byssal retractors. Tamu differs from other 
deep-sea mytilid genera (Amygdalum, Ben- 
thomodiolus, and Dacrydium) in having thick- 
ened ctenidia versus filamentous ctenidia. In 
addition, the outer demibranchs are only one 
half the length of the inner demibranchs in 
Benthomodiolus and Dacrydium, whereas 
outer and inner demibranchs are of equal size 
in Tamu. Palp suspensors are absent in 
Tamu, but present in both Benthomodiolus 
(type species) and Dacrydium (Ockelmann, 
1983). 

Nei's genetic distance based on 26 al- 
lozyme loci between T. fisheri and members 
of the genus Bathymodiolus, ranged from 
1.983 to 3.305 (Craddock et al. 1995; Table 
8). These Nei's D values are outside the 



range of those for most congeneric groupings 
of animals (Nei, 1987). Percent sequence di- 
vergence for a 246 bp region of the mtDNA 
COI gene ranged from 47.9% to 52.2% be- 
tween T fisheri and members of the genus 
Bathymodiolus. Tamu fisheri and "Idas" mac- 
donaldi were somewhat closer related, with a 
pairwise Nei's D value of 1 .859 and a CO! se- 
quence divergence of 38% (Table 8). 

The generic name derives from the abbrevi- 
ation for Texas A& M University (TAMU). Mem- 
bers of the Geochemical and Environmental 
Research Group at Texas A & M University 
have been instrumental in the discovery and 
exploration of numerous hydrocarbon/brine 
seeps on the Louisiana and Texas Continental 
Slope where many of these mussel taxa were 
first discovered. 

Tamu fisheri Gustafson, Turner, Lutz & 
Vrijenhoek, new species 
Figures 11-13,21-23 

This species, known since 1991, has been 
referred to in literature concerning seep and 
vent biology but was never formally de- 
scribed. The following is a list of these refer- 
ences. 

"Seep mytilid III" - Fisher, 1993: 609. 
"Seep mytilid III" - Gustafson & Lutz, 1994: 

81 , fig. 4.3 [micrograph of prodissoconch 

II]. 
"GB/III" - Craddock et al., 1995: 479-483. 
"Seep mytilid III" - Nelson & Fisher, 1995: 

table 3. 
"Seep mytilid III" - Kochevar & Childress, 

1996: tables 1, 2. 

Types: Holotype ANSP AI 8849 from JOHN- 
SON SEA-LINK-I Dive 3108 at Bush Hill hy- 
drocarbon seep at 27°46.91N; 91°30.36'W, 
210 km south southwest of Grand Isle, 
Louisiana in 548 m. The type-locality is be- 
tween Blocks 184 and 185 in the Green 
Canyon offshore petroleum leasing area in 
the Gulf of Mexico on the Louisiana Continen- 
tal Slope. Five paratypes (ANSP 400780, 
400781 ; USNM, MCZ) are from the same dive 
and locality. Additional paratypes are from 
JOHNSON SEA-LINK-I Dives 3131 and 3149 
at approximately 27°50'N; 91°10'W in 701 
and 650 m, respectively (ANSP 400782; 
MCZ, HMNS). 

Shell Morphology: Shell small, length no 
greater than 60 mm. Modioliform, thick and 
sturdy, essentially equivalve. Anterior margin 



92 



GUSTAFSONETAL 



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NEW DEEP-SEA MUSSELS 



93 




В 



Wf 









FIG. 21. Tamu fisheri Gustafson, Turner, Lutz & Vrijenhoek. Holotype, ANSP AI 8849. A, anterior view; B, 
posterior view; C, dorsal view; D, ventral view; E, lateral view of right valve; F, lateral view of left valve. 



94 



GUSTAFSON ETAL. 







1.0 cm 





FIG. 22. Tamu fisheri Gustafson, Turner, Lutz & Vrijenhoek. External views of a growth series of shells illus- 
trating ontogenetic change in shape. 




FIG. 23. Tamu fisheri Gustafson, Turner, Lutz & Vri- 
jenhoek. Remnants of juvenile hinge denticles lo- 
cated immediately posterior of the ligament in juve- 
nile specimen 16.9 mm in length. 

sharply rounded; posterior margin broadly 
rounded, becoming angular dorsally; ventral 
margin straight, very slightly concave in re- 
gion of byssal gape in largest specimens; dor- 
sal margin very tDroadly convex (Figs. 11. 12, 
21, 22). Shell length greater than twice the 
height. Umbones often eroded; prosogyrate; 
subterminal, positioned within the anterior 
one-twentieth. Prodissoconch II red, 460 itm 
in length. A raised, broadly rounded ridge ex- 
tends from the umbonal ridge to the posterior- 
ventral margin. 

External sculpture lacking, surface smooth 



except for concentric growth lines and very 
fine radial periostracal corrugations in the me- 
dian ventral area. Shell dull-white beneath 
dark-brown to straw-yellow periostracum. An- 
tero-dorsal portion of periostracum and shell 
variably eroded depending on age and collec- 
tion site. Interior polished, off-white, predomi- 
nately nacreous. 

Ligament opisthodetic, parivincular, ex- 
tending posteriorly from the umbones to oc- 
cupy from 37% to 50% of the dorsal margin. 
Adult hinge edentulous, thickened below and 
anterior to the umbo. Juvenile hinge with den- 
ticles immediately posterior of the ligament 
and immediately below the umbones (Fig. 
23). Hinge denticles obsolete in specimens 
greater than 17 mm in length. 

Muscle Scars: Anterior adductor scar oblong, 
positioned at an oblique angle near the antero- 
ventral margin, below the umbo. Posterior ad- 
ductor scar round, contiguous with small 
siphonal retractor scar ventrally and posterior 
portion of posterior byssal-pedal retractor scar 
dorsally. Anterior retractor scar located within 
upper extremity of umbonal cavity directly be- 
neath umbo. Posterior byssal retractors form 
two scars with a moderate gap between them; 
anterior scar obliquely elliptical, directly be- 
neath the posterior end of the ligament, poste- 



NEW DEEP-SEA MUSSELS 



95 



rior scar elliptical, parallel to the antero-poste- 
rior axis of the shell and located antero-dor- 
sally to and bordering the posterior adductor 
scar (Fig. 12). Ventral palliai line prominent, 
extending from the median posterior aspect of 
the anterior adductor scar to the posterior ad- 
ductor, curving slightly upwards and then 
downwards to form an indentation in the 
byssal gape region at about the mid-point of 
the antero-posterior axis; small siphonal re- 
tractor scar located at posterior end of ventral 
palliai line contiguous with posterior adductor. 

Measurements (in mm): 

anterior 
length height width length Dive 

53.5 23.8 17.6 - JSL3108 Holotype 

ANSP 
46.8 21.4 16.2 2.2 JSL3108 Paratype 

Rutgers 
50.0 21.9 17.0 2.8 JSL3108 Paratype 

USNM 
51.4 21.0 18.5 1.9 JSL3108 Paratype 

ANSP 

48.8 20.6 16-1 2.2 JSL3108 Paratype 

ANSP 

49.6 20.5 16.2 2.0 JSL3108 Paratype 

USNM 
31.6 14.1 10.1 2.0 JSL3149 Paratype 

HMNS 

33.9 15.2 12.3 2.0 JSL3149 Paratype 

Rutgers 
33.9 15.9 10.6 1.7 JSL3149 Paratype 

MCZ 
37.0 16.3 13.3 2.9 JSL3149 Paratype 

ANSP 

Internal Morphology 

Musculature: Main features of musculature 
evident from previous description of muscle 
scars and Figure 13. Posterior byssal retrac- 
tors separated into posterior and anterior por- 
tions, each consisting of two main muscle bun- 
dles, that attach separately to the shell; the 
posterior portion inserting along the postero- 
dorsal edge of the posterior adductor and the 
anterior portion inserting just below and pos- 
terior to the posterior end of the ligament. 
Pedal retractors very slender, arising from an- 
tero-dorsal portion of foot, passing lateral to 
the anterior retractors and inserting lateral to 
posterior portion of the posterior byssal retrac- 
tors. Siphonal retractors indistinct, originating 
in inner mantle margin around the excurrent 
siphon and attaching along postero-ventral 
edge of the posterior adductor. Anterior retrac- 
tors arising from dorso-lateral portion of the 
foot mass and passing anteriorly to insert in 
the antero-dorsal extremity of the umbonal 



cavity. Labial palp suspensors not evident. 
Posterior and anterior adductor rounded. 

Foot and Byssus: Foot long, thick; shape in 
preserved specimens variable, dependent on 
degree of contraction. Byssal strands few to 
profuse, gray to light-brown, thin, flat, unorna- 
mented. Byssal gland extending down foot 
behind byssal groove, without extension dor- 
sal to origin of anterior retractors. 

Mantle and Mantle Cavity: Connections be- 
tween edge of ascending lamellae and sur- 
face of mantle lobes and visceral mass weak 
or lacking, resulting in incomplete separation 
of incurrent and excurrent chambers. Lacking 
muscular longitudinal ridges for attachment of 
ascending lamellae to mantle lobes and vis- 
ceral mass (see Kenk & Wilson, 1985: 260). 
Ventral edges of inner mantle lobes not thick- 
ened and muscular. Excurrent siphonal open- 
ing small, tubuliform siphon capable of mod- 
erate extension beyond perimeter of shell, 
lacking internal diaphragm. Fusion of inner 
mantle immediately below excurrent siphon 
forms short, incomplete, horizontal branchial 
septum between incurrent and excurrent 
chambers; incurrent and excurrent chambers 
not completely separated posterior of poste- 
rior adductor; posterior ends of gill axes at- 
tach to underside of horizontal branchial sep- 
tum. Short valvular siphonal membrane joins 
right and left lobes, extending anteriorly a 
short distance into pedal gape; anterior edge 
of valvular siphonal membrane smooth, lack- 
ing central papilla. Pedo-byssal gape exten- 
sive; incurrent aperture extending from ante- 
rior end of valvular siphonal membrane to 
posterior edge of anterior adductor. 

Ctenidia: Lamellae of unequal height; as- 
cending lamellae two-thirds height of de- 
scending, resulting in inner and outer demi- 
branchs forming short-armed W-shaped gill 
when viewed in cross-section. Demibranchs 
unequal in length; inner demibranch slightly 
longer anteriorly than outer. Demibranchs hy- 
pertrophied, thick, short; ventral edges have 
well-developed, recessed food grooves; dor- 
sal food grooves present in deep folds just 
below junction of ascending lamellae and 
areas of attachment to mantle lobes and vis- 
ceral mass. Filaments broad, moderately 
fleshy; ctenidia and filaments white. Distal in- 
terlamellar junctions lacking; lamellae joined 
apically to approximately one-half height of 
descending and three-quarter height of as- 
cending lamellae; "principal filaments" (see 
Atkins, 1937: text fig. 18, type B[1b]) lacking. 



96 



GUSTAFSON ETAL. 



TABLE 10. Means (mm) and standard errors (in parentheses) of mensural characters in five new species 
of seep mytilids from the Gulf of Mexico. N = sample size; L = shell length; H = shell height; W = width of 
shell valves; A = anterior length; and G = ligament length (see Fig. 2). 



Species 


Site 


N 


L 


H 


W 


A 


G 


Bathymodiolus 


West Florida 


236 


90.6(2.8) 


31.2(0.8) 


24.2 (0.6) 


10.7(0.4) 


38.0(1.2) 


heckerae 


Escarpment 














Bathymodiolus 


Alaminos 


75 


115.1 (3.5) 


46.1 (1.2) 


34.7(1.0) 


8.3 (0.3) 


58.8(1.8) 


brooksi 


Canyon 














Bathymodiolus 


West Florida 


5 


100.0(9.6) 


40.4(4.1) 


29.9 (2.7) 


5.8 (0.9) 


40.7(6.1) 


brooksi 


Escarpment 














"Bathymodiolus" 


Alaminos 


29 


54.7(1.3) 


29.5 (0.8) 


24.3 (0.7) 


1.5(0.1) 


27.5 (0.8) 


childressi 


Canyon 














"Bathymodiolus" 


Bush Hill 


91 


78.6(0.9) 


40.2 (0.4) 


32.2 (0.4) 


2.5(0.1) 


36.1 (0.5) 


childressi 
















"Bathymodiolus" 


Brine Pool 


27 


107.7(3.1) 


50.1 (1.2) 


40.7(1.3) 


3.6(0.2) 


49.7(1.5) 


childressi 


NR-1 














Tamu fisheri 


Bush Hill 


13 


37.9 (3.2) 


16.7(1.3) 


13.0(1.1) 


2.1 (0.1) 


18.0(1.7) 


"Idas" mac- 


Garden Banks- 


5 


11.8(0.9) 


5.8(0.5) 


6.0 (0.4) 


0.6(0.1) 


4.1 (0.4) 


donaldi 


386 















Lacking "tubular connections" (see Kenk & 
Wilson, 1985) between free edges of ascend- 
ing lamellae and gill axes. 

Labial Palps: Paired labial palps short, broad, 
flat, triangular; inner surfaces plicate, outer 
surfaces smooth; bases of inner and outer 
pair coincident; both pairs in normal anterior 
position, without proboscid-like extensions. 
Outer pair of palps larger, up to twice the size 
of inner pair. Mouth situated normally, at the 
basal junction of inner and outer palps. Ex- 
treme anterior portions of gill placed between 
inner and outer palps coincident with plicate 
palp surfaces. 

Digestive System; Alimentary system well de- 
veloped for the group; stomach and direct in- 
testine located on body mid-line. Intestine 
leaves posterior end of stomach and passes 
posteriorly down midline ventral to ventricle; 
short recurrent loop to the right begins imme- 
diately below posterior end of ventricle; recur- 
rent intestine passes anteriorly on right side. 
Rectum turns to the mid-line and enters ex- 
treme antero-ventral portion of ventricle ante- 
rior to the auricular openings. 

Remarks; Some characters that separate T 
fisheri and other deep-sea mytilids have been 
previously discussed in the remarks section 
for the genus description. The small adult size 
of T. fisheri and the bifurcation of both poste- 
rior and anterior portions of the posterior 
byssal retractors further differentiate this 
species from "Bathymodiolus" childressi, B. 
brooksi, and B. heckerae. Conversely, T fish- 



eri is much larger than the largest specimens 
of "Idas" macdonaldi (Table 10). Tamu fisheri 
has a short recurrent intestinal loop similar to 
"Bathymodiolus" childressi, but in contrast to 
the straight intestine present in most species 
of Bathymodiolus. 

Tamu fisheri is rare at both Bush Hill and the 
site near Garden Banks, in contrast to the 
much more abundant "Bathymodiolus" chil- 
dressi. Fauna associated with T fisheri at 
Bush Hill are discussed in the remarks section 
for "Bathymodiolus" childressi. The site near 
Garden Banks is "extremely oily," but lacking 
in "major community development (stunted 
tube worms, isolated bivalves)" (I. R. Mac- 
Donald, pers. comm.). The new mussel "Idas" 
macdonaldi is also found at the site near Gar- 
den Banks. Tamu fisheri has an association 
with sulfur-oxidizing symbiotic bacteria on the 
surface of the gills (C. R. Fisher, pers. comm.). 
These bacteria express high activities of the 
enzyme ribulose biphosphate carboxylase/ 
oxygenase. Two specimens of T. fisheri, in- 
cluding the holotype, contained an unidenti- 
fied commensal polynoid polychaete within 
the mantle cavity. 

Round, white-rimmed, egg capsule scars 
identical to those commonly deposited by the 
snail Bathynerita naticoidea on the shell of 
"Bathymodiolus" childressi (C. R. Fisher, pers. 
comm.) were found on the postero-dorsal por- 
tion of one shell of T fisheri from Bush Hill. 
Gustafson & Lutz (1994; fig. 4.3) illustrate the 
prodissoconch II of T fisheri (designated 
"Seep Mytilid III") with a length of approxi- 
mately 460 um, and a surface sculpture of 



NEW DEEP-SEA MUSSELS 



97 



concentric growth lines alone, which is con- 
sistent with characteristics indicative of plank- 
totrophic development. 

Etymology: The specific name honors Dr. 
Charles R. Fisher of The Pennsylvania State 
University, who has provided us with many of 
the specimens examined in this report and 
who has done a great deal of the seminal work 
on the physiology of these symbiotic mussel 
taxa. The working designation "Seep Mytilid 
III" was given to this species from the Loui- 
siana Continental Slope cold-water seeps. 

Range: Known only from hydrocarbon seeps 
at Bush Hill in Green Canyon and from a site 
within Garden Banks petroleum lease block 
386 on the Louisiana Continental Slope in the 
northern Gulf of Mexico in depths from 546 to 
650 m (Table 6). 

Subfamily Modiolinae 

Type genus: Modiolus Lamarck, 1799 

Idas Jeffreys, 1876 

Idas Jeffreys, 1876: 428 (type species, by 
monotype, Idas argenteus Jeffreys, 
1876, non Idas Mulsant, 1876). 

Idasola Iredale, 1915: 340 (unnecessary re- 
placement name for Idas Jeffreys, 1876: 
428, non Mulsant, 1876 [Waren, 1991: 
116]). 

(For further synonymy, see Dell 1987:25). 

Revised Diagnosis: Shell small (8 to 22 mm 
maximum length), modioliform, rhomboidal to 
oblong, smooth, umbones subterminal; pe- 
riostracum light-yellow to brownish-yellow; 
prodissoconch reddish-brown; ligament ex- 
tending along most of postero-dorsal margin; 
fine hinge denticulations present anterior and 
posterior to ligament. Posterior retractors un- 
divided; posterior retractor scars continuous 
with posterior adductor scar. Separate pedal 
retractors present. All of the species assigned 
to this genus occur in deep-water and are 
commonly collected in association with 
sunken organic matter, including wood, whale 
bone, and fish skeletons. 

Remarks: Waren (1991: 116) presented con- 
vincing evidence, based on the requirements 
of the ICZN, for the maintenance of Jeffrey's 
name Idas in contrast to the replacement 
name Idasola of Iredale (1 915). Waren (1 991 ) 
also synonymized Idas and Adipicola, stating 



that he could not see why Dell (1987) distin- 
guished between these two genera. Waren 
(1991: 116) presumed that Dell based his 
generic distinction on the presence or ab- 
sence of "crenulated areas along the hinge 
line," which Waren (1991) considered to be a 
juvenile character, lost with growth in adult 
Adipicola but retained in adult Idas due to the 
latter's smaller size at maturity. In support of 
Warén's (1991) position, hinge denticulations 
were also present in all juvenile specimens of 
the species described in this report, being re- 
tained only in adult "Idas" macdonaldi, the 
smallest species examined. However, Dell 
(1987) also pointed out that in Idas the pedal 
retractor is associated with the posterior 
byssal retractor, whereas there is no sign of a 
separate pedal retractor in Adipicola. 

Other anatomical differences have not been 
studied in the type specimens of these genera 
(type specimens consist of shells only); how- 
ever, analyses for this report of the anatomy in 
putative I. argenteus (the type species of the 
genus), I. washingtonia, and Adipicola sp. 
(see Materials and Methods section for source 
material) revealed further differences between 
these two genera. Specimens of I. argenteus 
and I. washingtonia have outer demibranchs 
that are only one-half the length of the inner 
demibranchs, whereas specimens of Adipi- 
cola sp. have outer demibranchs equal in size 
to the inner demibranchs. In addition, Adipi- 
cola sp. have thick fleshy gills, whereas spec- 
imens of I. argenteus and I. washingtonia have 
thin, filamentous gills and "Idas" macdonaldi 
have moderately thickened but still essentially 
filamentous gills. These anatomical observa- 
tions argue against placing Idas and Adipicola 
in synonymy. 

Idas differs from Bathymodiolus, Bentho- 
modiolus, and Tamu in having undivided pos- 
terior byssal retractors (Dell, 1987), medial 
versus lateral placement of the pedal retrac- 
tors (relative to the position of the posterior 
byssal retractors), and hinge denticulations 
anterior and posterior of the ligament in adult 
specimens. Idas further differs from Bathy- 
modiolus and Tamu in its small adult size and 
in having thin filamentous ctenidia, the outer 
demibranchs of which are only one-half the 
length of the inner demibranchs (as exempli- 
fied by I. argenteus and I. washingtonia). Idas 
further differs from Bathymodiolus in lacking 
palp suspensors (as exemplified by I. argen- 
teus, I. washingtonia, and "Idas" macdonaldi). 

Idas differs from Dacrydium in having sepa- 



98 



GUSTAFSONETAL 



rate posterior pedal retractors (in I. argenteus, 
I. washingtonia, and "Idas" macdonaldi), um- 
bones located some distance from the ante- 
rior end, and in lacking palp suspensors. 

"Idas" macdonaldi Gustafson, Turner, Lutz 
& Vrijenhoek, new species 
Figures 11-13, 24-27 

Types: Holotype ANSP AI 8850 from JOHN- 
SON SEA-LINK-I Dive 3149 at 27°50'N; 
92°1 0'W, in 650 m in the Gulf of Mexico on the 
Louisiana Continental Slope near Garden 
Banks block 386 offshore petroleum leasing 
area. Two paratypes (ANSP 400783, 400784) 
and 6 additional specimens (Rutgers) are 
from the same dive and locality. 

Shell Morphology: Shell small, less than 15 
mm long, modioliform, sturdy and stout, 
translucent, essentially equivalve. Anterior 
margin sharply rounded: posterior margin 
broadly rounded: ventral margin straight but 
with concave indentation in region of byssal 
gape, indentation more pronounced in longest 
specimens; dorsal margin broadly convex, 
more or less straight over the span of the lig- 
ament (Figs. 11, 12, 24). Umbones often 
eroded; prosogyrate; subterminal, positioned 
within anterior one-twentieth. Raised, broadly 
rounded external ridge extends from umbonal 
region to posterior-ventral margin. 

External sculpture lacking, surface smooth 
except for concentric growth lines. Shell dull- 
white beneath straw-yellow periostracum. An- 
tero-dorsal portion of periostracum variably 
eroded, periostracum sometimes lacking on 
dorsal three-quarters. Interior off-white, pre- 
dominately nacreous. 

Ligament opisthodetic, parivincular, ex- 
tending posteriorly from the umbones to oc- 
cupy from 31% to 37% of dorsal margin. Adult 
hinge thickened below and anterior to um- 
bones, with 12 to 28 denticles immediately 
posterior to ligament and 9 to 1 9 denticles im- 
mediately below umbones on a thickened 
boss (Figs. 25-27). 

Muscle Scars: Muscle scars and palliai line in- 
distinct. Anterior adductor scar round, some- 
what truncated posteriorly, positioned near 
antero-ventral margin, below umbo. Posterior 
adductor scar round, contiguous with poste- 
rior byssal-pedal retractor scar dorsally. Ante- 
rior byssal retractor scar located within upper 
extremity of umbonal cavity directly beneath 
umbo. Elongated posterior byssal-pedal re- 



tractor scar not divided; parallel to antero-pos- 
terior axis of shell; posterior end of muscle 
scar bordering posterior adductor scar antero- 
dorsally, anterior end terminating below pos- 
terior hinge denticles (Fig. 12). Ventral palliai 
line straight without dorsal concavity, extend- 
ing from postero-ventral aspect of anterior ad- 
ductor scar to postero-ventral edge of poste- 
rior adductor. 

Measurements (in mm): 

anterior 
length hieight width length Dive 

10.6 4.9 5.1 - JSL3149 Holotype 

ANSP 
9.9 4.8 4.5 - JSL3149 Paratype 

ANSP 
11.2 5.3 4.8 - JSL3149 Paratype 

ANSP 
9.9 5.0 5,3 0.7 JSL3149 Specimen 

Rutgers 
11.2 5.4 5.6 0.5 JSL3149 Specimen 

MCZ 
13.4 5.8 6.2 8 JSL3149 Specimen 

Rutgers 
6.6 3.7 3.3 - JSL3149 Specimen 

Rutgers 
8 4 4.0 3.6 — JSL3149 Specimen 

USNM 
8.2 4.3 3.8 - JSL3149 Specimen 

HMNS 



Internal Morphology 

Musculature: Main features of musculature 
evident from previous description of muscle 
scars and Figure 13. Postenor byssal retrac- 
tors continuous, not divided into posterior and 
anterior portions; attaching to shell from an- 
tero-dorsal edge of posterior adductor to just 
posterior of and below ligament's posterior 
end. Separate pedal retractors located medi- 
ally, between posterior byssal retractors, par- 
tially obscured when viewed from a lateral as- 
pect; becoming integrated with posterior 
byssal retractors at point of shell attachment. 
Anterior retractors arising from dorso-lateral 
aspects of foot mass and extending anteriorly 
to attach to shell in antero-dorsal extremity of 
umbonal cavity. Labial palp suspensors not 
evident. Posterior adductor rounded, anterior 
adductor slightly oblong. 

Foot and Byssus: Foot thick; shape in pre- 
served specimens variable, dependent on de- 
gree of contraction. Byssal strands white to 
light-brown, thin, flat, unornamented. Purple 
tinted byssal gland extending down foot be- 



NEW DEEP-SEA MUSSELS 



99 





В 








2.5 mm 




FIG. 24. "Idas" macdonaldi Gustafson, Turner, Lutz & Vrijenhoek. Holotype, ANSP A18849. A, dorsal view; 
B, ventral view; C, lateral view of right valve; D, lateral view of left valve. 



100 



GUSTAFSONETAL 




FIG. 25. "Idas" macdonaldi Gustatson, Turner, Lutz & Vrijenhoek. Juvenile hinge line of specimen 10.4 mm 
in length. 

FIG. 26. "Idas" macdonaldi Gustafson, Turner, Lutz & Vrijenhoek. Hinge denticles located immediately pos- 
terior of the ligament in juvenile specimen 10.4 mm in length. 

FIG. 27. "Idas" macdonaldi Gustafson, Turner, Lutz & Vrijenhoek. Hinge denticles located immediately below 
the umbo in juvenile specimen 10.4 mm in length. 



hind byssal groove; extending laterally and 
slightly dorsal to origin of anterior retractors. 

Mantle and Mantle Cavity: Connections be- 
tween edge of ascending lannellae and surface 
of mantle lobes and visceral mass weak or 
lacking, resulting in incomplete separation of 
incurrent and excurrent chambers. Lacking 
muscular longitudinal ridges for attachment of 
ascending lamellae to mantle lobes and vis- 
ceral mass (see Kenk & Wilson, 1985: 260). 
Ventral edges of inner mantle lobes not thick- 
ened and muscular. Excurrent siphon little 
more than a simple slit with short extensible 
collar, not capable of extension beyond 



perimeter of shell. Unusual internal diaphragm 
occludes ventral two-thirds of excurrent 
siphonal opening, attached dorsally to slender 
muscular bridge that connects side walls of in- 
ternal opening approximately two-thirds of dis- 
tance from the siphon floor. Lacking horizontal 
branchial septum; incurrent and excurrent 
chambers not separated posterior of posterior 
adductor. Posterior end of gill axes attach to 
inner wall of fused inner mantle lobes just ven- 
tral to exhalent siphon. Short valvular siphonal 
membrane joins right and left mantle lobes, 
extending anteriorly a short distance into 
pedal gape; anterior edge of valvular siphonal 
membrane smooth, lacking central papilla. 



NEW DEEP-SEA MUSSELS 



101 



Pedo-byssal gape extensive; incurrent aper- 
ture extending from anterior end of valvular 
siphonal membrane to posterior edge of ante- 
rior adductor. 

Ctenidia: Lamellae of unequal heigfit; as- 
cending lamellae two-thirds to three-quarters 
height of descending, resulting in inner and 
outer demibranchs forming short-armed W- 
shaped gill. Demibranchs unequal; outer 
demibranchs shorter anteriorly, approximately 
90% to 95% the length of the inner demi- 
branchs. Status of food grooves not deter- 
mined due to poor preservation. Ctenidia fila- 
mentous to moderately thickened; filaments 
off-white in color. Distal interlamellar junctions 
lacking; lamellae joined apically to approxi- 
mately one-third height of gill; "principal fila- 
ments" (see Atkins, 1937: text fig. 18, type В 
[lb]) lacking. Lacking "tubular connections" 
(see Kenk & Wilson, 1985) between free 
edges of ascending lamellae and gill axes. 

Labial Palps: Paired labial palps short, thick- 
ened, broadly triangular; inner surfaces pli- 
cate, outer surfaces smooth; bases of inner 
and outer pair coincident; both pairs in normal 
anterior position, without proboscid-like ex- 
tensions. Outer pair of palps larger, up to 
twice the size of inner pair. Mouth situated 
normally, at the basal junction of inner and 
outer palps. 

Digestive System: Alimentary system well de- 
veloped for group; stomach and direct intes- 
tine located slightly to left of body mid-line. In- 
testine leaves posterior end of stomach and 
passes posteriorly left of mid-line and ventral 
to ventricle; very short recurrent loop to the 
right begins before ventricle's mid-point; re- 
current intestine then passes beneath ventri- 
cle to right side of mid-line and proceeds an- 
teriorly for a short distance. Rectum then 
returns to mid-line and enters floor of ventricle 
anterior to auricular openings and about one- 
fifth of distance from ventricle's anterior. 

Remarks: "Idas" macdonaldi possesses a 
combination of morphological features not 
seen in any described genus of mytilid mus- 
sel. So as to avoid erecting a new mono-spe- 
cific genus, this species is provisionally 
placed in Idas. Although most morphological 
features place "Idas" macdonaldi in the genus 
Idas, the ctenidial structure is radically differ- 
ent from that seen in other species of this 
genus. In "Idas" macdonaldi, the outer demi- 
branchs extend to 90% to 95% the length of 



the inner demibranchs and are moderately 
thickened. However, examination of adult I. 
argenteus (type species of Idas) collected at 
The Tongue of The Ocean (TOTO) in the 
North Atlantic, revealed filamentous outer 
demibranchs that are only half the length of 
the inner demibranchs. Long, thick outer 
demibranchs have not been previously re- 
ported for the genus Idas. Reduced outer 
demibranchs were also observed in I. wash- 
ingtonia from the South Cleft hydrothermal 
vent site on the Juan de Fuca Ridge and in I. 
washingtonia from whale bone in the Santa 
Catalina Basin. Type specimens of I. argen- 
teus (type material consists of shell only) and 
I. washingtonia were not examined for this 
feature. 

Reduced outer demibranchs have also 
been observed in Dacrydium ockelmanni 
(Mattson & Waren, 1977) and in paratypes of 
Benthomodiolus abyssicola (Knudsen, 1970; 
see Discussion below). Other morphological 
characters of "Idas" macdonaldi correspond 
with those of the genus Idas, although speci- 
mens of "Idas" macdonaldi are larger than 
most other known species of this genus. 

Several features of "Idas" macdonaldi serve 
to distinguish this species from other mussels 
described herein; small size, rhomboidal 
shape, unseparated posterior byssal retrac- 
tors, and lack of palp suspensors (although the 
latter are also lacking in T fisheri). No previous 
records of Idas or Adipicola from the Gulf of 
Mexico exist. Other Atlantic species of Idas 
and Adipicola include I. argenteus, A. simp- 
soni (Marshall, 1900) and A. pelágica (Wood- 
ward, 1854). Although listed as arising in the 
Recent geological period in Moore (1969), 
Idas has been recorded from the Miocene of 
northern Germany (Janssen, 1972; I. ligni- 
cola) and the Cretaceous of Egypt (Abbass, 
1962; I. faragi and I. nakadyi). 

"Idas" macdonaldi differs from I. coopingeri 
(Smith, 1 885) (reported from deep-water sites 
off Australia), I. japónica (Habe, 1 976) (from off 
Japan and New Zealand), I. argenteus, and I. 
washingtonia in having the umbones located 
in an almost terminal position; the anterior 
length (A) of the shell occupies the anterior 3% 
to 7% of the shell in "Idas" macdonaldi, the an- 
terior 16% in I. coopingeri, the anterior 10% to 
14% in I. japónica, the anterior 12% to 20% in 
I. argenteus, and the anterior 23% to 33% in I. 
washingtonia (Dell, 1987). "Idas" macdonaldi 
further differs from I. japónica in having a less 
narrow and elongate shell and in having the 
pedal and posterior byssal retractors almost at 



102 



GUSTAFSON ETAL 



TABLE 1 1 . Correlation matrix of mensural characters (log^^ transformed) from five new species of mytilids 
from the Gulf of Mexico. The PC-1 and PC-2 columns represent loadings of each character on the first 
two, Varimax rotated, principal component axes. PC-1 plus PC-2 explained 98.97% of the variance in 
these five characters. L = shell length; H = shell height; W = width of shell valves; A = anterior length; and 
G = ligament length. 



Variable 



H 



W 



G 



PC-1 



PC-2 



L 
H 
W 
A 

G 



1 .0000 



0.9425 


0.9297 


0.7170 


0.9821 


0.8507 


0.5136 


1.0000 


0.9842 


0.4811 


0.9565 


0.9670 


0.2358 




1.0000 


0.4516 


0.9450 


0.9750 


0.2043 






1 .0000 


0.6497 


0.2614 


0.9649 








1 .0000 


0.8845 


0.4302 



right angles to the plane of the anterior byssal 
retractors (the posterior and anterior retractors 
are essentially in the same plane in I. japónica) 
(Dell, 1987). 

"Idas" macdonaldi differs from I. ghisottii 
(Waren & Carrozza, 1990), from the Mediter- 
ranean Sea, in having a more rhomboidal and 
less elongate shell shape and in maintaining 
hinge denticulations anterior of the ligament 
up to adult size. "Idas" macdonaldi differs from 
I. indica (Smith, 1904), from off the Andaman 
Islands, in having a smooth shell surface and 
more anteriorly located umbones. Myrina 
modiolaeformis Sturany, 1896, was placed in 
Idas by Dell (1987); however, Waren (1991) 
questioned whether this species really be- 
longs in Idas. This species has not been found 
since the original description and its system- 
atic placement is uncertain. Narrow, elongate 
specimens described as Idas dalli Smith, 
1885, from off Culebra Island, West Indies, 
also apparently do not belong in Idas, accord- 
ing to K. W. Ockelmann, as reported in Dell 
(1987). 

The largest paratype of "Idas" macdonaldi 
was found attached by byssal threads to the 
external shell surface of a specimen of the 
vesicomyid bivalve Vesicomya cordata Boss, 
1968. Other specimens were "found intersti- 
tially in a mass of pea-sized carbonate rubble" 
(I. R. MacDonald, pers. comm.). Other fauna 
at this "extremely oily" site, which "lacked 
major community development," are T fisheri, 
"Bathymodiolus" childressi, stunted tube- 
worms, and isolated vesicomyid bivalves (I. 
R. MacDonald, pers. comm.). Two specimens 
of "Idas" macdonaldi contained a single large 
unidentified polynoid polychaete within the 
mantle cavity. These polynoids have been for- 
warded to Dr. James Blake for taxonomic de- 
scription. 

Etymology: The specific name honors Dr. Ian 
R. MacDonald of the Geochemical and Envi- 
ronmental Research Group at Texas A & M 



University, who is responsible for the collec- 
tion, preservation, and forwarding of this new 
species. The working designation "Seep 
Mytilid IV" was given to this species from the 
Louisiana Continental Slope cold-water 
seeps. 

Range: Known only from the northern Gulf of 
Mexico on the Louisiana Continental Slope in 
the vicinity of Garden Banks block 386 off- 
shore petroleum leasing area in 650 m (Table 
7). 



MORPHOMETRIC ANALYSIS 

The new mytilid species fall into three dis- 
crete size classes (Table 10). The two Bathy- 
modiolus species and "Bathymodiolus" chil- 
dressi were generally large, although 
differences in size existed among samples 
within two of the species. Tamu fisheri was in- 
termediate in size and "Idas" macdonaldi was 
small. Principle components analyses pro- 
ceeded from a correlation matrix (Table 11) of 
the five characters illustrated in Figure 2. The 
first principal components axis (PCI) repre- 
sented covariates of overall size (L, W, H, and 
G). Length of the shell anterior to the beak 
(character A) loaded highly on PC2. 

The five species of mussels separated rea- 
sonably well according to the PCI and PC2 
axes (Fig. 29). The two Bathymodiolus 
species found at the West Florida Escarp- 
ment site, although similar in size, can be dis- 
criminated because the anterior length (A) of 
B. heckerae is proportionally larger than in B. 
brooksi. Similarly, B. brooksi and "Bathymodi- 
olus" childressi at the Alaminos Canyon site 
can be discriminated because the anterior 
length (A) of B. brooksi is greater than in "Ba- 
thymodiolus" childressi, at a given size. Adult 
specimens of the three species found along 
tfie Louisiana Continental Slope sites can be 
discriminated easily because of their non- 



NEW DEEP-SEA MUSSELS 



103 



65 г 


"Idas" macdonaldi 






- 




Y = 0.554 


0006X 


nññ 


i 

со 








0.45 








035 
n ос 


■ 







specimens of the three species found along 
the Louisiana Continental Slope sites can be 
discriminated easily because of their non- 
overlapping size distributions; ''Bathymodio- 
lus" childressi being largest, T. fisheri be\ng in- 
termediate, and '4das'' macdonaldi being 
smallest (Table 10). 



DISCUSSION 



0.45 



0.65 г 




Tamu fisheri 






- 




Y = 478 


0001X 


0.55 


- J^ 


-^ 








0.45 








0.35 

n 9C 


■ 











0.65 


" Bathymodiolus" childressi 




055 
0.45 
0.35 

n 9C 


1 . 


Y = 0589-0.001X 


Oí 

1 

■& 

I 


i 



Bathymodiolus brooksi 






0-65 


Bathymodiolus 


hec 


/селае 






Y = 1.021X-°2== 




055 


- "^ 












n> 




iggj^ 












0) 










0.45 


^&Qo 




en 

Ф 




^&a.*> 


,° 


T 




caSçtS^è?^^'-'^ 


Q 




О.ЗЬ 


^ <^аРга& 


tS^&Ä Otf> 






Hü^^O^i 


yg^^gfffc;^<J О О 






■ 


^^°V^^^■S^-^^ 




0.25 







50 100 150 200 

Length (mm) 



FIG. 28. Plots of the ratio of height to length against 
length for "Idas" macdonaldi, Tamu fisheri, "Bathy- 
modiolus" childressi. Bathymodiolus brooksi, and 
Bathymodiolus heckerae. 



Prior to the discovery of the species de- 
scribed in this study, mytilid mussel genera 
with representatives in the deep sea (defined 
as those whose range extends below 600 m) 
included Adiplcola, Amygdalum, Bathymodio- 
lus, Benthomodlolus, Crenella, Dacrydium, 
Idas, Modiolus, and Musculus (Clarke, 1962; 
Knudsen, 1979; Dell, 1987; Kenk & Wilson, 
1985). Of these genera, only Bathymodiolus 
was known to contain endosymbiotic bacteria 
in specialized gill cells (Felbeck et al., 1981; 
Cavanaugh, 1983; Fiala-Médioni, 1984), al- 
though a mussel species retrieved from whale 
bone on the deep-sea floor and referred to /. 
washingtonia was reported to "host" chemo- 
autotrophic bacteria (Smith et al., 1989), and 
two mussels from the Middle Valley hydro- 
thermal vent on the northern Juan de Fuca 
Ridge referred to /. washingtonia and Adipl- 
cola sp. respectively, were reported to have 
bacteria associated with the microvillar sur- 
face of the gill cells (Juniper et al., 1 992). With 
the exception of "Idas" macdonaldi, the mus- 
sel species described in this study, possess 
fleshy, thickened gills, similar to B. thermo- 
philus. Gills of this type are thought to indicate 
the presence of a bacterial association 
(Fisher, 1990). Both B. brooksi anä В. heck- 
erae harbor two distinct populations of en- 
dosymbiotic gill bacteria (one having the mor- 
phology of a type I methanotroph and the 
other resembling a sulfide oxidizing bac- 
tehum); B. thermophilus (sulfide-oxidizing en- 
dosymbiont) and '^Bathymodiolus" childressi 
(methanotrophic endosymbiont) have only 
one symbiont (Childress et al., 1986; Ca- 
vanaugh et al., 1 987; Fisher et al., 1 991 ; Ca- 
vanaugh, 1 992; Cavanaugh et al., 1 992; С M. 
Cavanaugh, pers. comm.). Tamu fisheri ap- 
parently has an association with bacteria on 
the surface of the gill (C. R. Fisher, pers. 
comm.). 

Anatomical characters used to separate the 
new species herein described from each 
other and from previously described Bathy- 
modiolus species are summarized in Table 
12. Cosel et al. (1994) were not able to inves- 



104 



GUSTAFSONETAL. 



2п 



1- 



PC2 -1 



-2- 



-3 



-4 



Bathymodiolus 
heckerae 



Тати 
fisherí 




Bathymodiolus 
brooksi 



"Idas" 
macdonaldi 



"Bathymodiolus" 
childressi 



-4 



-3 



-2 



-1 



PC1 

FIG. 29. Scatter plots of the first two principle components (PC1 and PC2) for shell measurements of all avail- 
able specimens. Ellipses encompass 95% confidence limits for each species. Bathymodiolus heckerae = (x), 
Bathymodiolus brooksi (Alaminos Canyon = D; West Florida Escarpment = ■), "Bathymodiolus" childressi 
= (+), Tamu fisheri = (L), and "ldas"macdonaldi = (Y). 



Bathymodiolus by Hashimoto & Okutani 
(1994) and Cose! et a!., (1994), as well as the 
species of Bathymodiolus herein described, 
lack the extensive ventral mantle fusion and 
the prominent longitudinal muscular ridge for 
attachment of the ascending lamellae to the 
mantle, diagnostic of the type species B. ther- 
mophilus (Kenk & Wilson 1985). In most 
species of Bathymodiolus, the intestine is 
more or less straight, lacking a recurrent loop, 
whereas a short or very short recurrent in- 
testinal loop is present in B. aduloides, "Ba- 
thymodiolus" childressi, T. fisheri, and "Idas" 
macdonaldi. The rectum enters the ventricle 
in "Bathymodiolus" childressi at a point poste- 
rior to the level of the auricular ostia, whereas 
in other Bathymodiolus species the rectum 
enters the ventricle at a point anterior to the 



level of the auricular ostia (Table 1 2). The pos- 
terior byssal retractors are separated into 
separate anterior and posterior portions in Ba- 
thymodiolus, but not in "Bathymodiolus" chil- 
dressi. 

The affinities of the new deep-sea mytilid 
taxa described herein to existing deep-sea 
mytilids, including B. thermophilus, are not at 
all certain. The genera Amygdalum, Crenella, 
and Musculus all have typically filamentous 
filibranch gills and shell characters which sep- 
arate them from the other genera under dis- 
cussion. Modiolus also has typically filamen- 
tous gills. Relationships with Benthomodiolus, 
Dacrydium, and Adipicola are more problem- 
atical. Major anatomical characters of these 
deep-sea genera are summarized in Table 9. 

Recently, the validity of two primary diag- 



NEW DEEP-SEA MUSSELS 



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GUSTAFSONETAL. 



nostic characters that have been used to sep- 
arate the smaller of these deep-sea mytilid 
taxa, the presence or absence of "periostracal 
hairs" and "vertical hinge striations," have 
come under question. The so-called perios- 
tracal hairs considered by some to be a diag- 
nostic character of Idas, Benthomodiolus 
(Dell, 1987), and some other mytilids may not 
be of periostracal ohgin (Bottjer & Carter, 
1980), but may merely be byssal gland secre- 
tions laid down over the exterior of the normal 
periostracum by the foot, as suggested by 
Ockelmann (1983). A scanning electron mi- 
croscopic examination of "periostracal hairs" 
on small specimens of several species de- 
scribed herein suggests that the hairs on the 
surface of these shells are of byssal origin. 
Likewise, the vertical hinge denticles, thought 
to be a diagnostic character of Idas and of 
some Adipicola (Dell, 1987), are a character 
common to most juvenile modioliform mus- 
sels. These hinge denticulations are main- 
tained in adult Idas and in some species of 
Adipicola as a consequence of their small size 
(Waren, 1991). In the present study, small 
specimens of every species examined had 
hinge denticles both in front of and behind the 
hinge ligament. With the exception of "Idas" 
macdonaldi, these denticles were absent in 
adult specimens. 

We have examined paratypes, on loan from 
the Zoologisk Museum, University of Copen- 
hagen, of Benthomodiolus abyssicola (Knud- 
sen, 1970), the type species of Benthomodio- 
lus. Although the intestine has a short 
recurrent loop and the posterior retractors are 
divided in this small mussel (17.2 mm maxi- 
mum length) from 3270 to 3670 m in the Gulf 
of Panama, there are no hinge denticulations 
even in the smallest specimens, the gills are 
thin and filamentous as in typical filter-feed- 
ers, and the outer demibranchs are incom- 
plete, extending forward only to the middle of 
the inner demibranchs. These characters lead 
us to reject a close relationship between Ben- 
thomodiolus and the five new species de- 
scribed herein. Kenk & Wilson (1985) came to 
the same conclusion concerning a relation- 
ship between Benthomodiolus and Bathy- 
modiolus. 

The genus Dacrydium consists of small 
(about 5 mm maximum size) "nest-building" 
neotenous deep-sea mussels that lack sepa- 
rate pedal retractors, but have reduced outer 
demibranchs, unseparated posterior retrac- 
tors, a long recurrent intestinal loop, labial 
palp suspensors, and provincular and juvenile 



hinge teeth that persist throughout the ani- 
mal's life (Mattson & Waren, 1977; Ockel- 
mann, 1983). This combination of characters, 
although similar in some respects, distin- 
guishes Dacrydium from the five new species 
described herein. 

Several species of small deep-sea mussels 
referred to the genus Modiolus (Verco, 1908; 
Pelseneer, 1911; Prashad, 1932) may ulti- 
mately be placed in one or the other of the 
above discussed genera. Recently, Modiolus 
willapaensis Squires & Goedert, 1991, was 
described from Late Eocene deposits repre- 
senting ancient subduction-related methane 
seeps in southwestern Washington, USA 
(Goedert & Squires, 1 990; Squires & Goedert, 
1991). This species apparently did not obtain 
lengths greater than 27 mm. Although super- 
ficially resembling seep mussels described in 
this study, no internal features of the shell 
(hinge denticulations or muscle scars) were 
observed in the articulated fossils and there- 
fore relationship of M. willapaensis with extant 
seep mussels cannot be determined. Simi- 
larly, fossil M. exbrocchii exbrocchii Sacco 
have been described from Miocene (Torton- 
ian) deposits in Italy, in association with other 
mollusks, such as Lucina, characteristic of 
seep environments (Moroni, 1966). 

Although some anatomical features of B. 
heckerae and B. brooksi (extensive ventral 
pedo-byssal gape and lack of muscular at- 
tachment ridge for ascending lamellae), "Ba- 
thymodiolus" childressi (multiple posterior 
byssal retractors, short recurrent loop of in- 
testine and position of rectum relative to the 
ventricle) and "Idas" macdonaldi (complete 
outer demibranchs and relatively large size) 
differ from that seen in the respective type 
species of these genera, we hesitate in erect- 
ing additional deep-sea mytilid genera for 
these species. On the other hand, the level of 
genetic divergence (Craddock et al., 1995) 
and the unique combination of anatomical 
features in T. fisheri (bifurcate posterior and 
anterior portions of the posterior byssal re- 
tractors, short recurrent loop of intestine, and 
lack of palp suspensors) argue for generic 
level differentiation of this species. 



ACKNOWLEDGMENTS 

We thank the pilots and crew of the AT- 
LANTIS ll/ALVIN and the SEWARD JOHN- 
SON/JOHNSON SEA-LINK-I, for their techni- 



NEW DEEP-SEA MUSSELS 



107 



cal expertise and hospitality. We also thank 
those individuals who graciously supplied us 
with specimens: C. M. Cavanaugh, Harvard 
University; J. J. Childress, University of Cali- 
fornia at Santa Barbara; С R. Fisher, Penn- 
sylvania State University (NOAA/NURC at 
UNCW); I. R. MacDonald, Texas A & M Uni- 
versity; and C. R. Srлith, University of Hawaii. 
Particular thanks go to those scientists, too nu- 
merous to name, who helped collect and 
process specimens at sea, and to С Craddock 
for diligent hard work with allozyme studies of 
these mussels that initially revealed this diver- 
sity of new species and W. R. Hoeh for sharing 
preliminary (unpublished) COI mtDNA se- 
quences. This is contribution No. 97-06 of the 
Institute of Marine and Coastal Sciences, Rut- 
gers University, and New Jersey Agricultural 
Experiment Station Publication No. D/32104- 
2-97, supported by New Jersey State funds 
and NSF Grants OCE-83-10891, OCE-87- 
1 6591 , and OCE-92-1 7026 to RAL and OCE- 
89-17311, OCE-93-02205, OCE-96-33131 to 
RCV and RAL and NIH Grant PHSTW00735- 
01 to RCV and RAL. 



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Revised ms accepted 18 February 1998 



APPENDIX 1 

The ID#, location and museum catalog 
numbers of the mussel holotypes and 
paratypes. The holotypes and a series of 
paratypes are deposited in the Academy of 
Natural Sciences of Philadelphia (ANSP). Ad- 
ditional paratypes are deposited in the follow- 
ing institutions: United States National Mu- 
seum of Natural History, Washington, D.C. 
(USNM): Museum of Comparative Zoology, 
Harvard University (MCZ); Houston Museum 
of Natural Science, Houston, Texas (HMNS), 
Museum National d'Histoire Naturelle, Paris 



(MNHN), and Rutgers Univerisity (RU). 
MNHN and RU do not assign catalog num- 
bers to their collections. 



Bathymodiolus heckerae 
ID # Location 



A 1343 
A 1 754-3 
A 1755-13 
A 21 96-8 
A2196 
A 2196-1 
A 21 96-40 
A 21 97-33 
A 2542-40 
A 2542 
A2196 
A2196-17 
A 21 96-56 
A 2542-13 



Holotype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 



Bathymodiolus booksi 
ID # Location 



-13 

-7 

-22 



A 2211 
A 2211 
A2211 
A2211 
A2211 
A 2209-11 
A 2209-20 
A 2209-14 
A 2209 
A 2209-2 
A2211-6 
A 2209-9 
A 2209-1 8 
A 221 1-36 
A2196 
A 2542-7 
A 2542-60 
A 2542 



Holotype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 



ANSP 

USNM 

MCZ 

HMNS 

MNHN 

RU 

MNHN 

HMNS 

ANSP 

ANSP 

ANSP 

HMNS 

RU 

MNHN 



ANSP 

MCZ 

USNM 

MNHN 

ANSP 

MCZ 

MCZ 

MCZ 

ANSP 

RU 

MNHN 

RU 

HMNS 

RU 

ANSP 

USNM 

HMNS 

ANSP 



"Bathymodiolus" childressi 
ID # Location 



JSL3129 
JSL3129 
JSL3129 
JSL 3129-61 
JSL 31 37-39 
JSL 3145-41 
JSL 3145-23 
A 221 1-39 
A 2211 -44 
A 2211 
JSL 3145-37 



Holotype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 
Paratype 



ANSP 

MNHN 

ANSP 

RU 

HMNS 

USNM 

MCZ 

HMNS 

RU 

ANSP 

USNM 



Cat# 

AI 8846 
880270 
316977 
45307 



45306 

400773 

400771 

40072 

45299 



Cat. # 

A 18847 
319676 
88-268 

400775 
316973 
316975 
316974 
400774 



45300 

400777 
880269 
84302 
40076 



Cat. # 
AI 8848 

400778 

45303 
880272 
316978 
45308 

400779 
880271 



112 



GUSTAFSONETAL. 



JSL 31 37-27 


Paratype RU 




JSL 3149-4.3 


Paratype MCZ 


45301 


JSL3129-112 


Paratype HMNS 


45305 


JSL3149 


Paratype ANSP 


400782 


JSL3137 


Paratype MNHN 










JSL3137 


Paratype MNHN 




"Idas" macdonaldi 










ID# 


Location 


Cat. # 


Tamu fisheri 


















JSL3149 


HolotypeANSP 


AI 8850 


ID# 


Location 


Cat. # 


JSL3149 


Paratype ANSP 


400784 


JSL 3108 


HolotypeANSP 


AI 8849 


JSL3149-11.6 


Paratype ANSP 


400783 


JSL 3108-1 


Paratype MCZ 




JSL3149-12.2 


Paratype RU 




JSL 3108-3 


Paratype USNM 


880273 


JSL 3149-12.3 


Paratype MCZ 


316980 


JSL 3108 


Paratype ANSP 


400780 


JSL 3149-12.4 


Paratype RU 




JSL 3108 


Paratype ANSP 


400781 


JSL 3149 


Paratype RU 




JSL 3108-11 


Paratype USNM 


880274 


JSL3149-11.2 


Paratype USNM 


880275 


JSL 3149-1.3 


Paratype HMNS 


316979 


JSL3149-11.6 


Paratype HMNS 


45304 


JSL 3149-3.3 


Paratype RU 











MALACOLOGIA, 1998, 40(1-2): 113-229 



PROTOBRANCHIA (MOLLUSCA: BIVALVIA) CHILENOS RECIENTES Y 

ALGUNOS FÓSILES 

María VillarroeP José Stuardo^ 



RESUMEN 

Se estudian 15 especies de protobranquios recientes de Chile continental, 5 especies antar- 
ticas y 7 fósiles. De un total de 35 especies recientes citadas para la costa chilena y antartica, 
se aceptan sólo las 27 siguientes: Nucula austrobenthalis, N. (Л/.) falklandica. N. (N.) fernan- 
densis. N. (N.) interflucta. N. (N.) pisum, Ennucula eltanini. E. grayi. E. puelcha. Nuculana {Sac- 
cella) cuneata. N. {Borissia) inaequisculpta. Propeleda longicaudata. Tindariopsis sulculata, 
Silicula patagónica. S. rouchi. Yoldia {Aequiyoldia) eightsi. Yoldiella chilenica, Y. ecaudata, Y. 
granula, Y. indolens. Malletia chilensis. M. magellanica. M. patagónica. M. inaequalis. Malletiella 
sorror. Tindaria virens. T. salaria, y Acharax macrodactyla. Se agrega a esta lista la especie 
nueva: Nucula (N.) pseudoexigua, encontrada en el Estrecho de Magallanes. Se amplía la dis- 
tribución de la especie antartica Propeleda longicaudata al Estrecho de Magallanes. 

Se da especial énfasis a la descripción de las partes blandas, junto a los caracteres de la con- 
cha utilizados tradicionalmente en el estudio de los moluscos. 

Se estudió las siguientes características y estructuras morfológicas externas e internas: 
tamaño, forma y ornamentación de la concha: charnela, dientes charnelares y ligamento; manto 
y musculatura palea!: sifones, tentáculo sifonal, glándula hipobranquial y ctenidios: pie, muscu- 
latura pedal, visceral y aductores: boca, palpos labiales, tentáculo del palpo y lámelas del palpo; 
esófago, estómago, tiflosoles, divertículos digestivos, intestino y recto: corazón, glándula pe- 
ricárdica: ríñones; ganglios supraesofágicos, cerebro-pleurales, pedales y viscerales: y gó- 
nadas. Se considera, además, la información disponible sobre la distribución y ecología de las 
especies chilenas. En un estudio comparativo general, se corrobora el valor de las partes 
blandas en la diferenciación de categorías superiores dentro de la clase, pero con el limitado 
conocimiento que se tiene de ellas y debido al escaso número de especies estudiadas, su valor 
a nivel específico es todavía impreciso. Por otra parte, la complejidad observada en algunas de 
las estructuras estudiadas permitió sugerir modificaciones en la interpretación filogenética de 
ellas, especialmente en el caso de la estructura del estómago, la posición del corazón y la es- 
tructura de los sifones. 

Se consideran válidas las familias Nuculidae, Nuculanidae, Sareptidae, Tindariidae, Siliculi- 
dae, Malletiidae. y Acharacidae. 

Se trata a las especies fósiles con un criterio taxonómico similar al de las especies recientes 
y se compila una lista de alrededor de 54, efectuando y/o sugiriendo los cambios genéricos 
apropiados, cuando las descripciones e ilustraciones lo permitían. Como resultado del material 
colectado en distintas zonas fosilíferas se describen en detalle las especies siguientes: Ennu- 
cula araucana, E. ¿nogalis?, E. lebuensis, E. valdiviana, Propeleda medinae, Tindariopsis ele- 
gans, y Malletia volckmanni. Por último se discute la distribución geográfica y batimétrica de las 
especies recientes estudiadas. 



EXPANDED ENGLISH ABSTRACT 

The classification of the subclass Protobranchia followed here considers the families Nuculi- 
dae, Nuculanidae, Siliculidae, Sareptidae, Malletiidae, and Tindariidae in the order Nuculoida, 
and the family Acharacidae in the order Solemyoida. We also follow the separatation of Malleti- 
idae from Nuculanidae, further justifying it on anatomical grounds. 

Fifteen protobranch species of Recent distribution in continental Chile, five Antarctic, and 
seven fossil species were studied. Out of a total of 35 species cited for the coast of Chile and 
Graham Land in Antarctica, only the following 27 are here accepted as valid: Nucula austroben- 

' Facultad de Biología. Universidad Michoacana de San Nicolás de Hidalgo, Valle de Huetamo 30. Valle Quieto, Morelia, С 
P. 58066, Michoacán, México; rnvmelo@zeus.ccu.umtch.mx. 

^Departamento de Oceanografía, Facultad de Ciencias Naturales y Oceanografía, Universidad de Concepción, Chille, 
Casilla 2407, Concepción, Chile. 

113 



114 VILLARROEL&STUARDO 

thalis Dell, 1990: Nucula {Nucula) falklandica Preston, 1912: Nucula (Nucula) fernandensis V\- 
llarroel, 1971 : Nucula (Nucula) interflucta Marincovich, 1973: Nucula [Nucula) pisum Sowerby I, 
1833: Ennucula eltaninlDeW. 1990: Ennucula gray! {ä'Orblgny, 1846): Ennucula puelcha (ä'Or- 
bigny, 1842); Nuculana (Saccella) cunéala (Sowerby I, 1833): Nuculana (Borissia) inaequis- 
cu/pia (Lamy, 1906): Propeleda longicaudataJh\e\e, 1912: Tindariopsis sulculata {Gou\6, 1852): 
Silicula patagónica Dali, 1908: Silicula rouchi Lamy, 1911; Yoldia [Aequiyoldia) eights! (Jay, 
1839); Yoldiella chilenica (Dall, 1908); Yoldiella ecaudata (Pelseneer, 1903); Yoldiella granula 
(Dali, 1908); Yoldiella indolens (Dall, 1908); Malletia chllensis oes Moulins, 1832; Malletia ma- 
gellanica Smith, 1 875; Malletia patagónica Mabille & Rochebrune, 1 889: Malletia inaequalis Dall, 
1 908: Malletiella sorrorSooi Ryen, 1 959; Tindaria virens (Dall, 1 890): Tindaria salaria Dall, 1 908; 
and Acharax macrodactyla (Mabille & Rochebrune, 1 889). Nucula (N.) pseudoexigua Villarroel 
& Stuardo, a new species from the Strait of Magellan is described. The Antarctic species Pro- 
peleda longicaudata Jh\e\e, 1912, is reported for the first time from the Strait of Magellan. 

A diagnosis for every taxonomic category and a detailed description for every species are 
given, including the shell features traditionally utilized, as well as the soft parts. Most features 
having so far been studied only on a few species of the subclass, allow a comparative analysis 
with the Chilean representatives, summarized as follows. 

(1) Size varies within the different families. Living nuculids are in general smaller than nucu- 
lanaceans and solemyaceans. The largest size found in the Chilean Nuculidae reaches 20.6 mm 
length in Ennucula grayi. whereas among Nuculanidae and Malletiidae, a maximum measured 
length of 51.0 mm was found in Malletia chllensis. A Chilean fossil of this genus measured 60 
mm. 

(2) The studied species fall within the three known basic forms: nuculoid, nuculanoid, and sole- 
myoid (Fig. 61). 

(3) No comprehensive study of hinge tendencies within each family has been attempted: such 
study would possibly permit to examine affinities and divergencies at lower taxonomic ranks. 

(4) The study of the ligament in specific taxa should be used to test the validity of prevailing 
models and interpretations. So far, the study of the ligament in Nuculidae and Nuculanidae has 
followed Owen's (1 959) interpretation of an external or lamellar layer connected with the mantle 
margins, and another internal, fibrous layer connected to the isthmus of the mantle. A resilifer or 
chondrophore interrupts the two teeth series, and is directed anteriorly in Nucula and Ennucula 
(Fig. ЗА, cdr), is more or less straight in Yoldia (Fig. 129), and is directed posteriorly in Nuculana 
(Fig. 3). Previously, Stempell (1898a) demonstrated that the ligament in Malletia can be divided 
in anterior, central and posterior parts, the central part corresponding to the resilium (inner layer 
of the ligament), and the anterior and posterior parts with an external origin. Thus, such similar 
differentiation in Nuculidae, Nuculanidae and Malletiidae, suggested that the resilium of internal 
position in Nucula and Nuculana. had migrated to become external in Malletiidae, without diss- 
apearing. An intermediate stage in its position is observed in Tindariopsis. as was shown by 
Stempell (1898a). 

Relevance is given to the novel and most stimulating interpretation on the evolution of the lig- 
ament in the bivalves advanced by Waller (1990). He questions the traditional model of an am- 
phidetic primary ligament of three layers, and proposes a protobranch stem group from which 
two major types of ligament for the bivalves evolved. 

(5) Variation in number and size of hinge teeth does not allow to use them as taxonomic fea- 
tures of generic or suprageneric value, but size and form may sometimes offer specific taxo- 
nomic value, as noted by Knudsen (1970) and Villarroel (1971). 

(6) The palps are very similar in the Nuculacea and Nuculanacea, but their homology with the 
Solemyidae is not well known. The palps in Solemya are not interpreted as doubled palps ap- 
pendixes of other protobranchs: the palps sheets would be reduced to simple ridges (Fig. 1 1 ) in 
the edge of the furrow that joins the mouth with the appendixes (Figs. 15-17)(Ridewood, 1903; 
Morse, 1913; Yonge, 1939; Reid, 1980). 

The appendix or palp tentacle on the external sheet of every palp considered by Drew (1901) 
be equivalent of a pair of hypertrophiated fold (Figs. 10, 12, other figs., tp) differ in position ac- 
cording to family (Fig. 61 ). in the Nuculanacea, the palp appendix is located on the terminal por- 
tion of the external palp sheet (e.g.. Fig. 5, Silicula rouchi: Fig. 77, Nuculana (S.) cuneata: Fig. 
90, Nuculana {B.) inaequisculpta). in the Nuculidae, the palp appendix is displaced to the end, 
because behind it there is an additional, non-extensible structure termed the "palp caecum," 
which represents a pair of hypertrophiated folds (Stasek, 1965). 

The proximal end of the palp appendix is linked with the surface of the palp external sheets and 
the palp caecum (Fig. 10, bp); its musculature is fused with the posterior foot retractor. Stasek's 
(1961) observation of this feature in Лс/7а was corroborated, without exception, in every species 
studied. Nevertheless, in almost all the cases, the appendix was found in different degrees of con- 
traction, preventing recognition of specific differences (Figs. 4 and 62, 74 and 76, tp). 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 1 1 5 

(7) In a general comparative analysis, the value of the soft parts in the differentiation of the 
higher categories within the subclass, is corroborated: however, due to the limited available 
knowledge of many internal structures and the few studied species, their taxonomic role at the 
specific level cannot be always ascertained. On the other hand, the complexity observed in some 
of the internal morphological parts permitted us to set forth complementary interpretations on 
their possible phylogenetic value, particularly in the case of the stomach, the position of the 
heart, and the configuration of the various types of siphons. 

Although stomach morphology has been described for species of Nucula. Nuculana and Mal- 
letia. a comparison became necessary, resulting in the identification of a new caecum and 
changes in the interpretation of the features observed by previous authors. In fact, its study in 
the available species allowed the conclusion that there is not one basic type or "Gastroproteia," 
as proposed by Purchon (1956, 1959), but three. These are: 

Type la. Common to the genera Nucula and Ennucula and characterized by several (three or 
four) ciliary sorting areas and a wide extension of the typhlosole (Figs. 18-32, 60). 

Type lb. Common to the genera of Nuculanidae and Malletiidae and characterized by three cil- 
iary sorting areas and a small extension of the minor typhlosole (Figs. 33-56, 60). 

Type Ic. Common to the genera of Solemyidae and Nucinellidae and characterized by the ab- 
sence of distinct sorting areas and lack of typhlosoles. 

It is not difficult to differentiate the internal and external features recognized in the stomach of 
Nuculacea and Nuculanacea. The dorsal hood is smaller in Nuculanacea than in Nuculacea, and 
the three ducts that communicate the stomach with the digestive diverticula are also different in 
these two superfamilies (Figs. 18-56, 60). 

Similar differences were found in the ciliary sorting areas and the number of folds. For in- 
stance, the three additional sorting areas as^ , as^ and as'^ described by Purchon (1 956), although 
not present in all species, can also be used in interspecific differentiation. Thus, the first one was 
found only in Nucula {Nucula) pisum {F\g. 21) and Ennucula puelcha (Figs. 29-31), but not in the 
other studied species of these genera: the second sorting area was found presenting different 
sizes in Nucula (Nucula) pisum. Nucula (Nucula) fernandensis. and Ennucula puelcha. being 
largest in the latter. The third above named sorting area was not observed in the studied Nucu- 
lacea, and none were found in the studied Nuculanacea. Such differences do not back Purchon's 
(1987b) generalization that one description can embody all of them (Fig. 60). 

Undoubtedly, the complexity of the gastric shield with its biggest modification in Propeleda and 
Malletia is larger in Nuculanacea than in Nuculidae and Solemyidae, but presently it is difficult to 
establish generic or specific differences. On the other hand, folding of the typhlosoles entering 
the style-sac has shown specific constancy in the studied species of Nucula and Ennucula. De- 
velopment of the typhlosoles in Nuculanacea shows a different pattern. 

(8) Attention has also been given to the number of loops observed in the gastric and medium 
intestine with a pattern of coiling, which according to Heath (1937) is specific, with minimal in- 
traspecific variation as observed in Nucula (Nucula) pisum and Nucula (Nucula) pseudoexigua 
(Figs. 63-67). It begins on the side of the stomach and continues anteriorly in some species al- 
most reaching the mouth. It turns then dorsally to the esophagus and continues posteriorly above 
the stomach, or continues ventrally to form the coils prior to its final turn backwards. 

Heath (1937) was the first to demonstrate that in Nuculacea the intestine does not extend for- 
wards as much as in Nuculanacea. He associated the species of Nucula and Acila with life in 
shallow water in the case of simple coiling and life in deep water in the case of complex coiling. 
However, the many coils in the Chilean species of Nucula and Ennucula is not associated with 
depth, and a high degree of coiling was also described by Knudsen (1970) in various abyssal 
species of Nucula, Ennucula and Brevinucula. He, furthermore, found a large number of coils in 
species of Nuculanidae-species of Spinula with 1 , 6 and 7 coils: species of Ledella with 1 , 4 and 
5 coils: and Phaseolus with two. Thus, there seem to be two tendencies within the nuculanids: 
one with a high number of coils in the above-named genera, and another with only one coil in 
Nuculana. Propeleda. Yoldia and Yoldiella. 

The species of the genera Neilonella. Tlndaha, Tindariopsis and Malletia always have only one 
coil and show no variation with depth. 

Schileyko (1 989) observed that the number of coils is associated to the quality of the nutrients 
rather than the depth. This observation explains why Nucula (N.) fernandensis. collected at shal- 
low depth in a sandy sustratum had a large number of coils. Schileyko (1989) proposed six ten- 
dencies in the pattern of coils. 

Although there is no clear functional relationship between number of coils and life habits, there 
seems to be a clear association between coiling and shell volume for species of some genera. 
Such a relationship is observed in short but inflated species of Nucula. Ennucula. Spinula and 
Ledella, all of which have an intestine with more than 3 or 4 coils. On the other hand, species of 
genera with a flat, elongate shape, such as Malletia. have almost always only one coil. Excep- 



1 1 6 VILLARROEL & STUARDO 

tions of inflated species with only one coil within the genus Nuculana may be explained by the 
anterior position of the intestine, typical of nuculanaceans. 

(9) The phylogenetic value of the relationship between position of the heart and rectum sug- 
gested by Pelseneer (1888, 1911) for the bivalves, seems to be applicable to the evolution of the 
Protobranchia, as well. In fact, species of Nuculidae, recognized as the more primitive family, 
have a heart located dorsal to the rectum (Nucula, Ennucula) or surrounding it {Nucula próxima), 
whereas in more specialized families of Nuculanacea, the heart may be found surrounding the 
rectum (Nuculanidae) or located underneath (Malletiidae) (Figs. 58, 59). Thus, the studied 
species of Nuculana. Propeleda. Silicula, Yoldiella and Yoldia had without exception a heart sur- 
rounding the rectum (Figs. 76, 78, 85, 89). In the species of Malletia. Tindaria. and Tindariopsis, 
the heart can be positioned ventral to the rectum {Malletia chilensis and Tindaria virens; Figs. 92, 
95) or surrounding it {Malletia patagónica and Tindariopsis sulculata: Figs. 81 , 82). 

According to Owen (1959; fig. 7) in So/emya the heart surrounds the rectum. 

(10) The structure of the siphons in the Nuculanacea seems to indicate clearly differentiated 
morphological adaptations. Yonge (1939, 1957), based on species of Nuculanidae and Malleti- 
idae, recognized three different types of fusion for the walls of the siphonal tubes correlated with 
length (Fig. 57a-c): (a) with both siphons fused by tissue; (b) with the exhalant siphon closed, 
and ciliary junctions completing the inhalant siphon; and (c) with ciliary junctions completing both 
siphons. 

Our study of the Chilean species and the information provided by Knudsen (1970), Filatova & 
Schileyko (1985), and Allen (1985), allow us to propose the following five additional types (Fig. 
57 d-h); (d) siphons united dorsally and ventrally only by ciliary junctions; (e) Exhalant siphon 
open dorsally and ventrally; with or without a variable number of tentacles or papillae along the 
margin of the mantle corresponding to the inhalant siphon; (f) with exhalant siphon only, closed 
ventrally; mantle margins corresponding to the inhalant siphon serrated; (g) Exhalant siphon only 
partially separated from the inhalant one; and (h) Siphons only dorsally united. 

To study the precise type of union, examination of several specimens was required; however, 
it was often difficult to differentiate a close ciliary junction from a tissular one, and we risk possi- 
ble confusion in some cases. In fact, we agree with Drew (1899), Pelseneer (1911), and Heath 
(1937) in that a fusion by tissue, due to its ontogenetic origin, keeps a line of fusion indicated by 
a medial ventral line which breaks easily when pressed by a dissecting instrument. For species 
not examined by us. we trusted the descriptions. 

Coupling our observations with those by Knudsen (1 970), Allen (1 963), Allen & Sanders (1 973, 
1982), and Sanders & Allen (1977), we are permitted to establish the following relationships 
among the genera of Nuculanacea (genera in parenthesis indicate that description of the siphons 
is not sufficiently detailed to be certain of the type of union); 

Fusion of type a. Observed in species of Malletia. Yoldia. Yoldiella, {Spinula?), {Ledella), Jupi- 
teria. Lembulus. and Nuculana. 

Fusion of type b. Observed in species of Yoldia. Yoldiella. {Spinula?). {Ledella), and Nucu- 
lana. 

Fusion of type с Observed in species of Neilonella. Malletia, Nuculana, {Phaseolus), Tindari- 
opsis. and Propeleda: however, in this last genus the ventral borders are divergent. 

Fusion of type d. Observed in species of Neilonella and Tindaria. 

Fusion of type e. Observed in species of Sarepta. 

Fusion of type f. Observed in species of Tindaria. 

Fusion of siphons in Nuculanacea does not follow definite evolutionary lines, and to under- 
stand their adaptive significance will require both ecological and functional studies. Pelseneer 
(1911) noticed the presence of the siphonal tentacle generally on the left in species of Yoldia and 
Nuculana. Stempell (1899) found it indistinctly on one side or the other in Yoldiella ecaudata. but 
mainly on the right side in Malletia chilensis. Yonge (1939) located it in general mainly to the right, 
but in the species here studied it was indistinctly found on one side or the other; the same was 
observed by Knudsen (1970) in abyssal and hadal species. 

(11) Regarding geographic distribution, the study of the Chilean protobranchs has demon- 
strated that the extraordinary wide distribution recorded for some species is doubtful, and this is 
probably also the case of species from other geographic regions with purported very wide distri- 
bution. For instance, the identification of species of Nucula in Chile with a wide interregional dis- 
thbution may be erroneous, as we have established for Nucula exigua Sowerby I, 1833; Nucula 
carlottensis Dall, 1897; Nucula declivis Hinds, 1843; Ennucula colombiana (Dali, 1908); and Nu- 
culana callimene (Dall, 1908). In other cases, the distribution may appear wide due to a wrong 
synonymy as in the case of Malletia chilensis. mistakingly recorded up to Magellan. 

Table 2 indicates the existence of two faunistic groups of Protobranchia (also acknowledged 
for bivalves in general by Woodward, 1851 -1856; Soot-Ryen, 1959; Stuardo, 1964, 1988), with 
a limited overlapping of species. In fact, only the species Nucula {Nucula) pisum. Ennucula grayi. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



117 



and Ennucula puelcha present a wider distribution witlnin tlie two recognized "Provinces," 
whereas Malletia chilensis and Tindariopsis sulculata cover limits that may be considered tran- 
sitional zones. 

This table also helps to demonstrate possible interspecific relationships. For instance, mor- 
phological affinities among Nucula [Nucula] pisum. N. (Л/.) fernandensis, N. (Л/.) interflucta. and 
N. (N.) falklandica seem to be the result of allopatric radiation, the first being the stem from which 
the other two radiated. The fossil record of N. (N.) pisum supports this conclusion (Philippi, 
1887). 

Ennucula grayi ana E. puelcha seem to be sympatric species, or may correspond to only one. 

(12) Little is known of the ecology of the Chilean species, as they have been studied in some 
detail only in two places in central Chile: Bahía Concepción (this study) and Bahía Valparaíso 
(Ramohno, 1968). 

Three species are present at Bahía Concepción: Nucula (Nucula) pisum. Nuculana (Saccella) 
cuneata. and Malletia chilensis. The first two were found living mainly in sandy-mud, whereas 
Malletia usually lives in mud, difference that agree with Ramorino's observations (1968) at the 
Bahía Valparaiso. Ennucula grayi, which lives at Valparaiso, is not found at the Bahía Concep- 
ción, probably due to the seasonal environmental variations in temperature, salinity and oxygen 
(Ahumada & Chuecas, 1 979). Abundance of the three reported species is neither comparable to 
the values reported for Valparaiso, as discussed in the taxonomic part under each species. 

(13) Regarding distribution in depth, all the species listed in Table 2 have an extended range 
of bathymétrie distribution, as is well known for the group; however, following the bathymétrie di- 
vision of the oceans (Hedgpeth, 1957), there is only one intertidal species: Nucula (N.) inter- 
flucta. from Iquique, and only one abyssal species: Tindaria salaria collected off Islas Salas y 
Gomez. All the other are sublittoral or sublittoral-bathyal species, in general, the sublitoral con- 
tains the better known Chilean fauna of protobranchs: the abyssal fauna and that of the oceanic 
islands remain to be collected and studied. 

(14) The Chilean fossil protobranchs have not been recently reviewed, and their taxonomic 
status is rather poorly known. However, a revision of the literature yielded about 50 species de- 
scribed for the Paleozoic, Mesozoic, and Cenozoic. The collections available to us allowed the 
detailed description of only five species belonging to the genera Ennucula, Propeleda. Tindari- 
opsis. and Malletia. For the remaining species, we confirm or suggest the appropriate generic 
changes when the description and illustrations permitted it. 

Key Words: Protobranchia, Chilean, Antarctic, taxonomy, anatomy, distribution, Nuculoida, 
Solemyoida. 



INTRODUCION 

En el estudio de los moluscos es de 
aceptación general que los protobranquios 
constituyen el grupo más primitivo entre los 
bivalvos. Tal conclusión se ha alcanzado por 
el estudio de las partes blandas, estructuras 
cuyo valor filogenético se postula como fun- 
damental en la clasificación de este complejo 
grupo, y de los bivalvos en general (Yonge, 
1959). 

A pesar de su primitivismo, los protobran- 
quios presentan una mezcla de estructuras 
especializadas, resultado de una gran ra- 
diación observable tanto en las especies re- 
cientes (en particular en formas de la fauna 
abisal), como en las especies fósiles. En ellos 
el pie es todavía una suela plana; los cteni- 
dios, aún cuando deben considerarse gran- 
des, no dominan todavía la cavidad del manto, 
yacen en lo que se considera una posición 
primitiva, posterior y sus filamentos per- 
manecen triangulares; entre los órganos 



paléales, son los palpos labiales más que los 
ctenidios, los que colectan el alimento. Es por 
ello que la clasificación de los protobranquios 
debe considerar fundamentalmente el estudio 
detallado de sus partes blandas. 

No todos los caracteres utilizados en la 
clasificación taxonómica tienen el mismo 
valor filogenético ya que, en general, los bi- 
valvos muestran un grado de evolución en 
mosaico con muchos ejemplos de conver- 
gencia (Morton y Yonge, 1964), al cual los 
protobranquios no escapan. Esta podría ser 
una de las razones de la prevalencia de una 
clasificación simplificada de este grupo hasta 
la década de los años sesenta, que conside- 
raba sólo a unas pocas familias. Sin em- 
bargo, el estudio de las formas abisales y sus 
adaptaciones funcionales, ha permitido am- 
pliar la clasificación de los protobranquios 
para incluir a nuevas familias y reforzar así la 
importancia que en esta nueva clasificación 
tienen las partes blandas (Alien y Hannah, 
1986). 



118 



VILLARROEL & STUARDO 



De acuerdo a estos planteamientos los ob- 
jetivos más importantes del presente estudio 
fueron dos. En primer lugar, realizar el estudio 
taxonómico de casi todas las especies chile- 
nas conocidas, considerando una combi- 
nación de caracteres tanto de la concha como 
de las partes blandas; en segundo lugar, lle- 
var a cabo el estudio anatómico comparativo 
de las distintas especies de protobranquios 
encontradas. Esto, permitió la evaluación de 
algunos caracteres anatómicos considerados 
en la clasificación y en la evolución del grupo, 
esperándose que sea este aspecto de la re- 
visión, lo que estimule mayores investiga- 
ciones. 

El estudio anatómico permitió, además, 
discutir la interpretación de estructura y fun- 
ción de los órganos más importantes. 

Finalmente, se logró compilar una sinopsis 
de todas las especies fósiles chilenas conoci- 
das, proyectando los resultados del análisis 
taxonómico-anatómico realizado con las es- 
pecies actuales, a la interpretación de ellos. 
Sin embargo, el deficiente conocimiento ta- 
xonómico previo, el escaso número de es- 
pecies fósiles chilenas disponibles y, en 
menor grado, la falta de literatura, permitió 
sólo un estudio parcial de ellas. 

Antecedentes Históricos Sobre La 
Clasificación de los Protobranquios 

Hay escasos estudios sobre los protobran- 
quios de Chile, aunque los catálogos sobre la 
fauna de moluscos de este pais han compi- 
lado las especies descritas incluyendo oca- 
sionalmente comentarios taxonómicos y 
sinonimias. Estudios que junto a la identifi- 
cación consideran datos sobre profundidad, 
substrato y abundancia relativa son los de 
Hupé (1854), Smith (1881), Mabille y Roche- 
brune (1889), Stempell (1898a), Dalí (1908a, 
1909)y Soot-Ryen (1959). 

Dos trabajos taxonómicos importantes son: 
el de Ramorino (1968) que incluye, además, 
estudios de densidad en los fondos de la 
Bahía de Valparaíso, y el de Marincovich 
(1973) sobre moluscos intermareales de 
Iquique, que describe una nueva especie de 
Nucula. 

Otros autores han examinado diversas es- 
pecies de protobranquios chilenos en estu- 
dios faunísticos de gran extensión latitudinal. 
Entre ellos destacan: el de Hertlein y Strong 
(1940) sobre especies de la costa de México 
y América Central; el catálogo de Carcelles y 



Williamson (1951) sobre los moluscos de la 
provincia Magallánica; las monografías de 
Keen (1 958, 1 971 ) y OIsson (1 961 ) sobre mo- 
luscos de la Provincia Panameña; los de 
Soot-Ryen (1951), Powell (1951), y Dell 
(1964, 1990) sobre fauna Antartica, y el de 
Bernard (1983) sobre bivalvos del Pacífico 
Oriental. Respecto de los moluscos del Pací- 
fico central, Rehder (1 980) describió a un pro- 
tobranquio entre los moluscos de la Isla de 
Pascua. 

Coan y Scott (1997) presentan el estado 
taxonómico actual de los protobranquios en 
su inventario de los bivalvos marinos del 
Noreste del Océano Pacífico, basados en el 
examen de material tipo de colecciones de 
varios museos y toda la literatura publicada. 

Las investigaciones sobre anatomía del 
grupo son escasas. De todas las especies 
chilenas, sólo tres han sido anteriormente es- 
tudiadas en detalle: Malletia chilensis, Tinda- 
riopsis sulculata (Stempell, 1898a; Heath, 
1937), y Nucula {Nucula) fernandensis Villa- 
rroel, 1971, lo cual refleja el estado del 
conocimiento sobre la anatomía de los mo- 
luscos chilenos en general. La descripción 
anatómica de Petrasma atacama Kuznetzov 
y Schileyko, 1984, designada por estos au- 
tores para la zona peruano-chilena, por la la- 
titud que ellos señalan (7°41'N; 79°47'W) co- 
rresponde a Ecuador. 

Por otra parte, la importancia de los estu- 
dios anatómicos en la clasificación de los pro- 
tobranquios ha sido incorporada en las con- 
tribuciones de Pelseneer (1 891 ,1911), Davies 
(1933), Yonge (1939), Alien (1954, 1978, 
1 985), Purchon (1 956, 1 959, 1 978, 1 987a), Fi- 
latova (1958, 1976), Morton (1963, 1967), 
Stasek (1963), Savitskii (1969a, 1969b, 
1 974), Alien y Sanders (1 973, 1 982), Sanders 
y Allen (1973, 1977), Schileyko (1983, 1985, 
1989), Filatova y Schileyko (1984, 1985), y 
Allen y Hannah (1986, 1989). 

La fauna de bivalvos fósiles chilenos, des- 
crita en su mayoría por Philippi (1887, 1899), 
no ha vuelto a ser revisada y los nombres 
propuestos originalmente se usan todavía en 
trabajos de índole puramente estratigráfica, 
tales como los recopilados por Steinmann 
(1856-1929), Wiickens (1904), Fuenzalida 
(1938, 1942), Tavera (1942, 1956, 1960), 
Tavera y Veyl (1958) y otros. Zinsmeister 
(1984) describió un género y tres especies 
nuevas para el Eoceno Superior, Formación 
La Meseta, Isla Seymour, Península Antartica 
y Stinnesbeck (1986), una subespecie y dos 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



119 



especies nuevas de la Formación Ouiriquina 
(Maastrichtiano) de Chile Central. 

A partir de la propuesta inicial de Neumayr 
(1 884), quien basándose en los caracteres de 
la concha incluyó este taxón junto a los Ar- 
cacea en el orden Taxodonta, la clasificación 
de los protobranquios ha combinado las inter- 
pretaciones filogenéticas de paleontólogos y 
neontólogos. 

La historia geológica de los protobranquios 
y su filogenia, comenzó a ser discutida en de- 
talle, combinando estas tendencias, por Сох 
(1959). Con postehoridad, McAlester (1964) 
en un estudio de los Nuculoides del Paleo- 
zoico temprano, y considerando los trabajos 
anatómicos de especies recientes, concluyó 
que dentro de los protobranquios existe una 
radiación evolutiva primaha en dos grupos 
distintos, representados por las formas nucu- 
loides y nuculanoides, asignándole a cada 
una el rango de superfamilia: Nuculacea y 
Nuculanacea, respectivamente. 

Estos antecedentes fueron considerados 
por Newell (1965, 1969) para proponer la 
separación de la subclase de los protobran- 
quiados en dos categorías diferentes: los 
Palaeotaxodonta Korobkov, 1954, y los 
Cryptodonta Neumayr, 1884, en contraste a 
clasificaciones más conservadoras (Yonge, 
1939; Purchon, 1959, 1978). Newell se basó 
en que trabajos modernos en el género Sole- 
mya. tendían a demostrar numerosas diferen- 
cias morfológicas en la concha entre Nucu- 
loides y Solemyoides, las que sumadas a una 
larga histoha geológica que no evidenciaba 
su origen común, sugería dos líneas evoluti- 
vas completamente diferentes. 

La clasificación de Newell (1969) fue modi- 
ficada por Salvini-Plawen (1980), quien al 
igual que Nevesskaya et al. (1971) sugiere 
considerar las subclases como superórdenes, 
proponiendo además el nombre de Ctenidio- 
branchia Salvini-Plawen, 1980, en lugar de 
Palaeotaxodonta Korobkov, y Palaeobranchia 
Iredale, 1939, en vez de Cryptodonta Neu- 
mayr. Incluye a estos superórdenes en la sub- 
clase Pelecypoda Goldfuss, 1820, con- 
siderando al orden Nuculida Dalí, 1 889, dentro 
de los Ctenidiobranchia y a los órdenes Sole- 
myida Dalí, 1889, y Praecardiida Newell, 
1965, dentro de los Palaeobranchia. 

Schileyko (1983) considera al superorden 
Protobranchia conformado por los órdenes 
Solemyioda y Nuculida 

Alien y Hannah (1986) reactualizaron la 
subclase Protobranchia Pelseneer, 1889, di- 



vidiéndola en los órdenes Solemyoida, y Nu- 
culoida y a esta última en dos superfamilias: 
Nuculoidea y Nuculanoidea. 

Waren (1989) demostró que la superfamilia 
Nuculanoidea debería ser asignada a H. 
Adams y A. Adams, 1858, y no a Gray, 1824, 
como concluyeran Alien y Hannah (1986). 
También la distribución de familias propuesta 
por estos autores fue criticada por Maxwell 
(1988), quien justificadamente, sugiere en 
phmer lugar, la división de la familia Nuculi- 
dae en dos subfamilias (Nuculinae Gray, 
1824, y Nuculominae Maxwell, 1988), y 
luego, USÓ la familia Sareptidae Stoliczka, 
1871, en reemplazo de Yoldiidae, a cuyas 
subfamilias Yoldiinae Habe, 1977, y Yoldielli- 
nae Alien y Hannah, 1986, agrega la subfa- 
milia Sareptinae Stoliczka, 1871. El género 
Sareptó A. Adams, 1860, es incluido por Alien 
y Hannah (1 986) en la subfamilia Yoldiellinae, 
lo que con los antecedentes existentes con- 
sideramos justificado. Por otra parte, la sepa- 
ración de los Nuculidae propuesta por 
Maxwell nos parece un carácter filogenético 
importa tte, susceptible de complementarse 
con caracteres anatómicos, como se ha in- 
tentado desarrollar en este trabajo. 

Convencidos de la necesidad de profun- 
dizar el estudio anatómico de las partes 
blandas en este grupo y por su trascendencia 
taxonómica mantenemos para la subclase el 
nombre Protobranchia Pelseneer, 1889, pre- 
firiéndolo a la proposición reciente de Palaeo- 
taxodonta Korobkov (Carter, 1990). 

Carter (1990) resume una clasificación 
para el orden Solemyoida que incluye a las 
superfamilias Solemyoidea "H. Adams y A. 
Adams, 1857 [1840]" (con la familia Solemy- 
idae y las subfamilias Solemyinae y Clino- 
pisthinae Pojeta, 1988, fósil) y la superfamilia 
Nucinelloidea Vokes, 1956, con las familias 
Nucinellidae y Manzanellidae Chronic, 1952 
(fósil). 

El género Acharax Dalí, 1908, es incluido 
en los Solemyinae por las características de 
ligamento afín a Solenomya. 

Considerando a las especies discutidas en 
este trabajo, la clasificación aquí seguida, es 
la siguiente: 

Clase Bivalvia Linné, 1758 
Subclase Protobranchia Pelseneer, 1889 
Orden Nuculoida Dalí, 1889 
Superfamilia Nuculacea Gray, 1824 
Familia Nuculidae Gray, 1824 
Subfamilia Nuculinae Gray, 1824 



120 



VILLARROEL & STUARDO 



Subfamilia Nuculominae Maxwell, 1988 
Superfamilia Nuculanacea H. Adams y A. 

Adams, 1858 
Familia Nuculanidae H. Adams y A. Adams, 

1858 
Subfamilia Nuculaninae H. Adams y A. 

Adams, 1858 
Subfamilia Ledellinae Allen y Sanders, 1982 
Familia Siliculidae Allen y Sanders, 1 973 
Familia Sareptidae Stoliczka, 1871 
Subfamilia Sareptinae Stoliczka, 1871 
Subfamilia Yoldiellinae Allen & Hannah, 1986 
Familia Malletiidae H. Adams y A. Adams, 

1858 
Familia Tindariidae Verrill & Bush, 1897 
Orden Solemyoida Dall, 1889 
Superfamilia Solemyacea Gray, 1840 
Familia Acharacidae Scarlato y Starobogatov, 

1979 



MATERIALES Y MÉTODOS 
Materiales Examinados 

Especies Actuales: De un total de 27 es- 
pecies aquí aceptadas para Chile, se estudia- 
ron 20, de las cuales 1 5 son continentales y 5 
antarticas. Las áreas de recolección se repre- 
sentan en los Mapas 1 y 2. 

En la lista de especies incluida en la Tabla 
2, se han marcado con un asterisco aquellas 
de las que no se obtuvieron ejemplares, y con 
interrogante, aquellas otras citadas cuya 
presencia se considera improbable. Las es- 
pecies restantes fueron identificadas en 
muestras depositadas en las colecciones de 
bivalvos del Museo del Departamento de 
Zoología, Universidad de Concepción, Chile 
(MZUC), provenientes de las expediciones, 
donaciones y recolecciones siguientes, cuyas 
abreviaciones se utilizan en el texto: 

(1 ) Expedición Mar-Chile I, entre Coquimbo 
(29''57'24"S) y el extremo S de la Isla de 
Chiloé (42°55'S), Febrero-Marzo 1960 (M. 
Ch. I.). 

(2) Expedición Mar-Chile II, entre la fron- 
tera con el Perú (18 28'S) y Punta Patache 
(2048'S), Julio 1962 (M.Ch. II). 

(3) Crucero 69-5 del buque "Hero", de la Na- 
tional Science Foundation, realizado entre el 
Estrecho de Magallanes (53 30'S y el Archi- 
piélago Madre de Dios (50' 9'30"S), 1 8 de Oc- 
tubre a 5 de Noviembre 1969 ("Hero" 69-5). 

(4) Material proporcionado por el Instituto 



de Fomento Pesquero, Chile, proveniente de 
uno de sus cruceros frente a la costa centro- 
norte chilena (IFOP-01), Noviembre 1964. 

(5) Muestras de la Bahía de Valparaíso en- 
viadas por la Estación de Biología Marina de 
Montemar, Departamento de Oceanología, 
Universidad de Chile, Valparaíso. 

(6) XlXa Expedición Antartica Chilena, Di- 
ciembre 1964-Enero 1965 (Ant. XIX). 

(7) XXIIa Expedición Antartica Chilena. Di- 
ciembre 1967-Enero 1968 (Ant. XXII). 

(8) Operación Centolla, Mayo 1962 (Op. 
Centolla). 

(9) Muestreo cuali y cuantitativo en la Bahía 
de Concepción, Febrero 1968 y Diciembre- 
Enero 1969. 

Especies Fósiles: Las muestras estudiadas 
abarcan, tanto la mayoría de las formaciones 
marinas que afloran en las Provincias de 
Concepción y Arauco, como también las de 
algunas de las Provincias de Santiago y Co- 
quimbo (Mapa 1 ). Fueron proporcionadas por 
el Profesor Lajos Biró (O.E. P.D.), del Labora- 
torio de Paleontología de la Universidad de 
Concepción. 

(1) Lo Valdés, 14 al 31 de Enero de 1964. 

(2) Navidad, 1 a 4 de Noviembre de 1968. 

(3) Tubul, Noviembre de 1965 y visitas es- 
porádicas posteriores. 

En colectas efectuadas por el autor princi- 
pal en Coquimbo, Tongoy (Prov. Coquimbo), 
Cajón del Fierro-Baños del Flaco (Prov. de 
Colchagua), Cocholgüe, Lirquén, San Vi- 
cente, Tumbes y Quinquina (Prov. de Con- 
cepción) no se encontraron protobranquios 
fósiles. Algunas muestras adicionales prove- 
nientes de Navidad, se examinaron en la Es- 
cuela de Geología de la Universidad de Chile, 
Santiago. 

Las muestras estudiadas sólo cubren cor- 
tos tramos del tiempo transcurrido desde el 
Paleozoico Superior (Carbonífero-Pérmico), 
piso más antiguo en que se han encontrado 
protobranquios hasta el presente (Tabla 1). 

Aunque el número de fósiles revisados en 
las distintas colecciones ascendió a más de 
10,000 ejemplares, sólo 140 individuos, 742 
valvas y 32 moldes internos son protobran- 
quios correspondientes a las siete especies 
fósiles analizadas. 

En la colección de fósiles de R. A. Philippi 
(1887, 1899) existente en el Museo Nacional 
de Historia Natural en Santiago, no se encon- 
tró ningún protobranquio. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



121 




MAPA 1. Localidades principales mencionadas en el texto agrupadas de acuerdo a su latitud aproximada. 
Main geographic references cited in the text, grouped according to their approximate latitude. 



122 



VILLARROEL & STUARDO 



Islas 

Georglas del Sgr 




ICXr 90 8 и 7Cr 6Cr 50" 40 30 20 

MAPA 2. Principales localidades Antárticas mencionadas en el texto. Main Antarctic localities cited in the text. 



Métodos 

En las citas sinonímicas de las especies se 
señalan aquellas que incluyen descripciones 
anatómicas con la abreviación (anat.). 

Las muestras de especies actuales con 
partes blandas fueron conservadas en alco- 
hol al 75%. Entre los fósiles, no siempre se tu- 
vieron ejemplares completos y conchas origi- 
nales, por lo que fue necesario efectuar 
algunas determinaciones utilizando conchas 
incompletas, moldes externos, internos e/o 
impresiones. 

Los términos técnicos usados en las des- 
cripciones de las especies son los usuales 
(e.g., Arnold, 1 965) para definir los caracteres 
de la concha. La observación de estas es- 
tructuras y las disecciones de las partes 



blandas teñidas con rojo neutro diluido en al- 
cohol, se efectuaron utilizando un microsco- 
pio estereoscópico Zeiss. 

En el estudio de las partes blandas se 
hicieron cortes histológicos, para precisar la 
interpretación de los ciegos estomacales. En 
la lista de especies estudiadas, aparte de las 
especies marcadas con asterisco (*), cuya 
existencia en Chile es dudosa, no se estudió 
la anatomía interna de Silicula patagónica, ni 
de Yoldiella indolens. 

Las dimensiones de la concha medidas en 
cada especie fueron: longitud, altura y espe- 
sor y se efectuaron en la forma representada 
en las Figuras 1y 2. Debido a la gran varia- 
bilidad de las medidas observadas no se cal- 
cularon índices. 

El material estudiado y su procedencia se 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



123 



TABLA 1. Ubicación cronológica de las localidades de donde 
provienen las colecciones revisadas. En todas se han mencionado 
protobranquios fósiles, pero en este estudio se encontraron sólo en las 
marcadas con asterisco (*). Las edades referidas a localidades distin- 
tas se agrupan de acuerdo a otros autores. Chronological location of 
the studied samples of fossil protobranchs (*). Strata and localities 
arranged according to various authors. 



Período 



Época 



Localidades 



Cuaternario 



Terciario 



Cretácico 



Jurásico 



Pleistocene 



Plioceno 



Mioceno Inferior 
Eoceno 

Eoceno Inferior 
Paleoceno Superior 
Superior 



Inferior 



Superior 



Coquimbo 
Tongoy 
Tubul* 
Coquimbo 
Tongoy 
Tubul* 
Navidad* 
Isla Seymour 
Boca Lebu 
Boca Lebu 
Quiriquina 
San Vicente 
Lirquén 
Cocholgüe 
Tumbes 
Lo Valdés* 
Baños del Flaco 
Rio Maitenes 
Cajón del Fierro 
Lo Valdés' 
Baños del Flaco 
Río Maitenes 
Cajón del Fierro 



indican en detalle después de la sinonimia de 
cada especie. En cada una de las muestras 
se señala el número de ejemplares completos 
estudiados (ej), y/o el número de valvas (v), 
su ubicación lateral izquierda o derecha (i o d) 
y el tamaño máximo y mínimo. Si la abre- 
viación ej va acompañada de s, significa que 
se trata de ejemplares completos, pero 
secos. Si la abreviación ej va sola, indica que 
se trata de una muestra conservada en alco- 
hol. En el caso de los fósiles los moldes inter- 
nos se abrevian mi. 

Para cada muestra se indica también en 
orden continuado: No. de Museo (colección 
del Museo del Departamento de Zoología de 
la Universidad de Concepción, MZUC o de la 
Colección de Paleontología, DGUC), nombre 
de la expedición y de la estación en que fue 
obtenida (si la hubiere), posición geográfica, 
tipo de substrato y profundidad (expresada en 
m). Las referencias a los tipos de substrato 
fueron tomadas directamente de las etique- 



tas. En el caso de los fósiles, se incluye tam- 
bién indicaciones de edad y naturaleza de las 
rocas en que se encontraron. 

En las Figuras 1 a 3 se ilustran los carac- 
teres de la concha; en las restantes, se han 
representado solamente las estructuras de la 
concha y de las partes blandas que se dis- 
cuten en el texto; se hace referencia a ellas, 
cuando se estimó necesario. 

Las conchas de las especies de pequeño 
tamaño se lavaron con jabón suave y se 
limpiaron durante un minuto en un vibrador 
Bransonic 220. Luego se montaron en grafito 
coloidal sólido en isopropanol al 20%. Se 
metalizaron con oro en un sistema SPUTER 
S 150 coater y se fotografiaron con el micro- 
scopio de barrido Siemen ETEC Autoscan U- 
1 en el Laboratorio de Microscopía Elec- 
trónica de la Dirección de Investigación de la 
Universidad de Concepción. Las especies de 
mayor tamaño se fotografiaron con un micro- 
scopio estereoscópico Cari Zeiss Modelo IV, 



124 



VILLARROEL& STUARDO 



provisto de una cámara Carl Zeiss С 35 para 
microfotografía. Los dibujos de las partes 
blandas se hicieron con una cámara clara 
Carl Zeiss. Todos los dibujos, excepto las fi- 
guras 3, 9-12, 66, 75, 80 y 95 fueron hechos 
a escala y las medidas se expresan en cada 
caso en mm o en décimas de mm. 

La numeración tanto de dibujos como de 
fotografías es consecutiva y se designan 
como figuras (Figs.). En el caso de las fo- 
tografías se indica el número de Museo de la 
muestra, el tamaño del ejemplar o el aumento 
utilizado y su procedencia. 

En el caso de las especies fósiles, se nu- 
mera en forma consecutiva las especies de 
las cuales se revisó material. 

Abreviaciones Empleadas 



ct 

a 

aa 

ada 

adp 

an 

ар 

apt 

api 

as (1-4) 

b 

bp 

cav p 
ccp 
ccv 
cd 

cdr 

con 

cp 

cp' 

cq 

es 

dch 
dd 

dd^ 

dd^' 

dd ^^ 

dd^'3' 

ddg 



ctenidio 

aurícula 

aorta anterior 

aductor anterior de la concha 

aductor posterior de la concha 

ano 

ápice 

aorta posterior 

área plegada (FAde otros autores) 

área de selección (SA de otros au- 
tores) 

boca 

ciego del palpo 

cavidad pericárdica 

conectivo cerebro pedal 

conectivo cerebro visceral 

capuchón dorsal (DH de otros au- 
tores) 

condróforo 

escultura concéntrica 

ciego posterior 

entrada ciego posterior 

cinturón quitinoso 

cinturón de separación del estó- 
mago y saco del estilo 

dientes charnelares 

conductos de los conductos diges- 
tivos 

conducto del divertículo digestivo 
derecho 

entrada del ducto digestivo dere- 
cho al estómago 

conductos de los divertículos di- 
gestivos izquierdos 

entrada de los divertículos en el 
estómago 

divertículos digestivos 



deg 


dientes del escudo gástrico 


div 


escultura divergente 


dm 


músculo dorsal medio 


dp 


disco pedal 


dq 


dientes quitinosos 


dva 


escultura divaheada 


e 


esófago 


e' 


entrada del esófago 


eg 


escudo gástrico 


es 


estatocisto 


est 


estómago 


esc 


escutelo 


esp 


espesor 


fl 


filamento del palpo 


g 


gónada 


gib 


glándula del biso 


gl h 


glándula hipobranquial 


gse 


ganglio supraesofágico 


gp 


ganglio pedal 


gv 


ganglio visceral 


h 


altura 


i 


intestino 


iaa 


impresión aductor anterior 


lap 


impresión aductor posterior 


im 


intestino medio 


iv 


intestino visceral 


1 


longitud 


le 


lámela externa del palpo 


lig 


ligamento (int = interno: ext = ex 




terno) 


li 


lámela interna del palpo 


Ip 


lámina del palpo 


Ipl 


línea paleal 


lun 


lúnula 


mbr 


músculo branquial 


mi 


músculo interior del palpo 


mm 


músculos medios 


mp 


músculos paléales 


ms 


músculos sifonales 


msp 


membrana suspensora del palpo 


nbr 


nervio branquial 


npa 


nervio paleal anterior 


npl 


nervio del palpo 


npp 


nervio paleal posterior 


o' 


entrada al estómago 


P 


pie 


per 


pehcardio 


pl 


palpo labial 


pm 


papilas del manto 


pr 


perióstraco 


PP 


músculos protractores pedales 


rad 


escultura radial 


r 


recto 


ret 


escultura reticulada 


ri 


riñon 


rm 


músculos retractores del manto 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



125 



ra músculo retractor pedal anterior 

rpp músculo retractor pedal posterior 

(Ф) 

rs músculos retractores sifonales 

s sifón 

se saco del estilo 

sex sifón exhalante 

si surco intestinal 

si' continuación del surco intestinal 
del estómago 

sin sifón inhalante 

sp seno paleal 

sol surco oral lateral 

tm tentáculos del manto 

tma tiflosol mayor (TY de otros autores) 

tme tiflosol menor (TY' de otros au- 
tores) 

tp tentáculo del palpo 

tpd talón pedal 

ts tentáculo sifonal 

um umbo 

V ventrículo 

vm músculo ventral medio 



taxonomía de los 
protobranquiados 
chilenos recientes 

Clase Bivalvia (Lamellibranchiata) 

Linné, 1758 

Subclase Protobranchia Pelseneer, 1889 

Diagnosis 

Bivalvos con pie sagital y longitudinalmente 
surcado, suela con márgenes papilados; fila- 
mentos branquiales simples, generalmente 
aplanados, no reflejados, con manojos de ci- 
lios abfrontales; sin glándula del biso, pero 
con una glándula pedal (o "bisal") en la quilla 
del pie que no produce biso. 

Clave Para Las Familias Y Géneros 
De Protobranquios Chilenos 
Recientes Y Fósiles 

1 . Concha de forma variable con el extremo 
posterior no alargado. Sin seno paleal. Animal 
sin sifones 2 

1'. Concha oval, oblonga o alargada; ex- 
tremo posterior generalmente más largo y a 
menudo rostrado. Con seno paleal general- 
mente presente. Tubos sifonales parcial o to- 
talmente unidos 4 

2. Concha alargada, soleniforme; entre- 
abierta. Perióstraco sobrepasando los bordes 



de las valvas. Charnela sin dientes. Liga- 
mento externo. Bordes del manto unidos en 
su parte media. Palpos labiales muy pe- 
queños. Ctenidios muy grandes ocupando un 
tercio de la cavidad paleal .... Acharacidae 

Acharax 

2'. Concha corta, ovalada, subthangular o 
redondeada; no entreabierta. Perióstraco no 
sobrepasando los bordes de las valvas. Char- 
nela provista de numerosos dientes. Bordes 
del manto libres. Palpos labiales y ctenidios 
casi del mismo tamaño Nuculidae.3 

3. Márgenes internos de las valvas crenu- 
lados (tamaño hasta 5 mm) Nucula 

3'. Márgenes internos de las valvas lisos 
(tamaño hasta 20.6 mm) Ennucula 

4. Ligamento externo o parcialmente in- 
terno. Corazón ventral al recto o atravesado 
por él. Tamaño a grande 5 

4'. Ligamento interno. Corazón atravesado 
por el recto. Tamaño pequeño, mediano o 
grande Nuculanidae ... 7 

5. Ligamento externo 6 

5'. Ligamento parcialmente interno; su 

parte externa alojada en una cavidad poste- 
rior a los umbos. Sifón exhalante completo; 
inhalante abierto ventralmente . . . Ledellinae 
(hasta 13.3 mm) Tlndariopsis 

6. Concha más o menos veneriforme, in- 
flada, de umbos prominentes. Sin seno 
paleal. Sifones formados sólo por unión de 
papilas o repliegues del manto. .Tindahidae 
(hasta 6 mm) Tindaria 

6'. Concha ovalada, comprimida lateral- 
mente, de umbos bajos. Con seno paleal. Si- 
fones unidos, cerrados o abiertos ventral- 
mente . .Malletiidae (hasta 51 mm) . Malletia 

7. Concha más o menos rostrada. Extremo 
posterior generalmente realzado por una 
quilla 8 

7'. Concha redondeada. Extremo posterior 
sin quilla Yoldiidae. 10 

8. Ornamentación formada por costillas 
concéntricas. Charnela provista de dientes 
chevronados (en "v") . . . .Nuculaninae ... 9 

8'. Sin ornamentación concéntrica. Char- 
nela provista de dientes lamelares muy obli- 
cuos Siliculidae (hasta 12 mm) 

Sllicula 

9. Rostro romo, muy largo, bicarinado 
(hasta 18.9 mm) Propeleda 

9'. Rostro corto no carinado (hasta 12.5 
mm) Nuculana 

1 0. Concha de regular tamaño, entreabierta 
posteriormente. Seno paleal profundo. Con- 
dróforo triangular .Yoldiinae (hasta 35.5 mm) 

Yoldia 



126 



VILLARROEL & STUARDO 



10'. Concha muy pequeña, cerrada es- 
trechamente. Seno paleal poco profundo. Sin 
condróforo Yoldiellinae (hasta 12 mm) 

Yoldiella 



Orden Nuculoida Dalí, 1889 

Superfamilia Nuculacea Gray, 1824 

Los mismos caracteres de la familia. 

Familia Nuculidae Gray, 1824 

Diagnosis 

Concha equivalva, hasta 50 mm de longitud 
(30 mm en las especies chilenas), subtriangu- 
lar u oval. Valvas inequilaterales; parte poste- 
rior corta, a menudo truncada, la anterior más 
larga; extremo redondeado. Umbo opistogiro. 
Lúnula casi siempre cordiforme. General- 
mente sin escutelo; sólo algunas veces existe 
un escutelo o un pseudo-escutelo bien de- 
finido. Prodisoconcha lisa. Escultura, si la hay, 
formada por estrías concéntricas, concéntri- 
cas y radiales, radiales bifurcadas, o modifi- 
caciones y combinaciones de las anteriores. 
Margen ventral interno liso o crenulado. Inte- 
rior nacarado. Placa de la charnela general- 
mente fuerte, curvada o acodada en el medio; 
condróforo bordeado por una serie anterior y 
otra posterior de dientes taxodontos. No hay 
ligamento externo; resilium interno. Línea 
paleal entera. Bordes del manto libres. Pie vo- 
luminoso. Aductores grandes, subiguales. 
Glándula hipobranquial sobre la pared de la 
cavidad suprabranquial. Corazón sobre el 
recto. Palpos labiales muy grandes, cada uno 
con un largo apéndice tentacular. Estómago 
(en las especies chilenas) con o sin un ciego 
dorsal posterior; al menos con dos áreas de 
selección distintas. Eje de los ctenidios de 
posición oblicua o vertical con filamentos sim- 
ples, que dividen la cavidad paleal en una gran 
cámara inhalante anterior y una pequeña cá- 
mara exhalante posterior. Ganglio visceral 
más pequeño que el cerebral. Sin órgano sen- 
sorial en el manto anterior. Sin sifones. 

Distribución 

Los representantes de esta familia viven en 
la actualidad en todos los mares, tanto en 
aguas someras como profundas, en fondos 
que van desde grava y arena gruesa hasta 
sedimento fino. Algunas especies son de 
aguas tropicales, pero la mayoría de ellas se 
encuentran en aguas templadas y boreales 
(Hertlein y Strong, 1940). 



Observaciones 

Un resumen de algunas especies de Nu- 
culidae recientes descritas y/o citadas para 
Chile fue publicado por Villarroel (1 971 ). 

Subfamilia Nuculinae Gray, 1824 

Con una capa superficial de finos prismas 
radiales, de sección rectangular. 

Género Nucula Lamarck, 1 799 

Nucula Lamarck, 1799:87. Especie tipo por 
monotipia; Arca nucleus Linné, 1 758 (Hertlein 
y Strong, 1940). 

Diagnosis 

Concha oval o subthangular, sólida; escul- 
tura lisa o concéntrica con estrías radiales 
finas, anchas y aplastadas, a menudo difíciles 
de ver en la parte media de la concha, pero 
distintas cerca del borde ventral de ella en 
donde forman un margen crenulado; interes- 
pacios angostos, cerca de 1/10 del ancho de 
las estrías. Eje del condróforo, oblicuo, di- 
rigido anteriormente. Borde del manto liso, sin 
papilas. 

Subgénero Nucula s. s. (= Lamellinucula 
Schenck, 1944) 

Concha oval o subtriangular, truncada; es- 
cultura lisa o concéntrica, generalmente con 
estrías radiales y margen crenulado; placa de 
la charnela en ángulo; dientes proximales 
junto a un condróforo relativamente pequeño; 
ligamento oblicuo. 

Especies encontradas en Chile: 

1. Nucula (Л/.) falklandica Preston, 1912 

2. Nucula (N.) fernandensis Villarroel, 
1971 

3. Nucula (N.) interflucta Marincovich, 
1973 

4. Nucula (Л/.) pisum Sowerby I, 1833 

5. Nucula (N.) pseudoexigua, sp. nov. 

De las especies encontradas en Chile con- 
tinental, sólo Nucula {Nucula) interflucta no 
fue estudiada. Esta es la más pequeña de las 
especies chilenas y la única que habita en la 
zona intermareal. No ha sido registrada de 
otras partes. 

Nucula polynesica Rehder, 1980, descrita 
para la Isla de Pascua, es una especie con 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



127 



aparentes afinidades a la fauna del Pacífico 
Central. 

Dell (1990) describió a Nucula austroben- 
thalis con un amplio rango de distribución en 
las profundidades antarticas ubicadas al Sur 
de los 56 S en 3519-4209 m. 

Clave Para las Especies 
de Nucula Estudiadas 

1. Escultura de la concha conspicua, for- 
mada por costillas concéntricas que general- 
mente se interrumpen en algún punto de su 
curso, y por estrías radiales. Estómago con 
un ciego posterior. Especie de la región ma- 
gallánica . . . . N. (N.) pseudoexigua sp. nov. 

Г. Escultura de la concha inconspícua de 
apariencia lisa, formada por estrías concéntri- 
cas y radiales débiles. Estómago con o sin 
ciego posterior 2 

2. Concha casi orbicular. Estómago con un 
ciego posterior. Especie de las Islas Juan Fer- 
nández N. {N.) fernandensis 

2'. Concha alargada antero-ventralmente 
3 

3. Concha con la región anterior elevada. 
Márgenes internos de las valvas crenulados. 
Estómago con un ciego posterior. Especie de 
la región magallánica . . . .Л/. (Л/.) falklandica 

3'. Concha con la región dorsal anterior 
semitruncada. Estómago sin ciego posterior. 
Sólo los márgenes ventrales internos de las 
valvas son crenulados. Especie de amplia 
distribución en Chile N. (Л/.) pisum 

Se han citado otras tres especies dudosas 
para Chile. Nucula exigua Sowerby I, 1833, 
registrada entre el Golfo de California y Perú, 
ha sido citada para el Estrecho de Maga- 
llanes por Dalí (1 908) y otros autores (Hertlein 
y Strong, 1 940; Soot Ryen, 1 959). Nucula de- 
clivis Hinds, 1843, otra especie con distribu- 
ción muy similar a la anterior, fue también 
citada por Dalí (1 908) para el Estrecho de Ma- 
gallanes. Soot-Ryen (1959) comentando la 
improbabilidad de que estos dos nucúlidos se 
encuentren en Chile, sugirió que las identifi- 
caciones en cuestión, pudieran pertenecer a 
una forma de otra especie, N. carlottensis 
Dalí, 1897, que parecería estar ampliamente 
distribuida a lo largo de la costa oeste de 
América. 

Ningún otro autor ha fundamentado esta 
sugerencia que consideramos también du- 
dosa. En consecuencia, la inclusión de estas 
tres especies en la fauna malacológica 
chilena no se justifica. 



Nucula (Л/.) falklandica Preston, 1912 
Figs. 1,27, 28, 68, 69, 102, 103 

Nucula falklandica Preston, 1912: 637, lám. 
21, fig. 3 (Loe. tipo: Islas Falkland); Carcelles 
y Williamson, 1951: 322; Powell, 1960:169; 
Dell, 1964: 139, fig. 1 (17). Dell, 1990: 5, figs. 

8 y 9. 

Nucula minúscula Melvill y Standen, 1907: 
113 (пол Pfeffer, 1886). 

Material Estudiado 

9 ejemplares (ej) у 20 valvas (v). MZUC. 
Procedencia: (1) 1 ej, 2.5 mm (No. 4548), Op. 
Centolla, Est. 2, E. de Magallanes, Bahía In- 
útil; fango con abundantes restos de conchas, 
46 m. (2) 3 ej, 2.5-3 mm (No. 4553), Op. Cen- 
tolla, Est. P5M6, E. de Magallanes, Bahía In- 
útil; fango con algas, esponjas, briozoos y 
conchas, 46 m. (3) ej, y 20 v, 1-2 mm (No. 
4662) "Hero" 69-5, Est. 210, E. de Maga- 
llanes, Bahía Corbeta Papudo (Guarello) 
(50°21'17"S; 74°43'25"W), fango amarillo 
verdoso, 500 m. 

Descripción 

Concha: Concha pequeña (hasta 3 mm de 
longitud), semiovalada, blanca, de aspecto 
vitreo. Prodisoconcha más blanca y opaca 
que el resto de la concha. Perióstraco amarillo 
muy pálido. Umbos ubicados en el tercio pos- 
terior de la concha, ligeramente abultados. 
Margen dorsal anterior arqueado y notoria- 
mente elevado en su región media, lo que le 
da a la concha un aspecto de truncamiento 
dorso anterior; margen ventral redondeado; 
margen dorsal posterior elevado. Extremo 
posterior, levemente truncado. Ornamen- 
tación reticulada, formada por líneas radiales 
finas y densas que cubren toda la superficie 
de la concha, pero se hacen poco visibles 
sobre los umbos. Líneas de crecimiento dis- 
tribuidas irregularmente, aumentando su den- 
sidad hacia el margen ventral. Superficie in- 
terna de las valvas lisa, transparentando la 
reticulación externa. Todo el margen interior 
de la concha finamente crenulado. Charnela 
arqueada, con dientes poco numerosos, muy 
poco curvados hacia arriba: 3 a 7 anteriores y 
2 a 4 posteriores. (Dell, 1964, cita a un ejem- 
plar del Museo Británico de 3.6 x 3.3 mm con 

9 dientes anteriores y 5 posteriores.) Primeros 
dos dientes anteriores próximos al condró- 
foro, distintos en posición y forma de los que 
les siguen. Impresiones de los músculos 



128 



VILLARROEL & STUARDO 



aductores iguales, alargadas verticalmente. 
Otras impresiones musculares no visibles. 

Anatomía Interna: Disco pedal con incisiones 
cortas y largas, dando un aspecto dentado. 
Glándula hipobranquial voluminosa, de as- 
pecto granular con pequeñas gotas de apa- 
riencia oleaginosa. Palpo alargado, con ten- 
táculo muy ancho. Ctenidios con filamentos 
externos de forma triangular muy aristada; fi- 
lamentos internos más largos que los exter- 
nos, no aristados. Corazón con aurículas y 
ventrículo globosos. Estómago con área de 
selección (as) con menos de 12 repliegues. 
Ciego posterior del estómago muy notorio 
como en N. (N.) pseudoexigua y N. (Л/.) fer- 
nandensis. Intestino corto con no más de dos 
vueltas. 



Observaciones 



restos de conchas: y ejemplares pequeños y 
valvas sueltas hasta 500 m de profundidad, 
en fango. Parece presentar gran tolerancia 
batimétrica, pero esta especie es aparente- 
mente poco abundante. 

Nucula (N.) fernandensis Villarroel, 1971 
Figs. 23-26, 99-101 

Nucula femandens/s Villarroel, 1971: 159- 
171: Cekalovic y Artigas, 1981: 80. Nucula 
(Linucula) fernandensis Villarroel, Bernard, 
1983: 10. 

Material Estudiado 

Serie tipo (Villarroel, 1971): MZUC (Loe 
Tipo: Islas Juan Fernández). MZUC No. 
10387. Paratipos: No. 4577, 4580, 10295, 
10296, 10297, 10298, 10299, 10300. 



Aunque ninguno de los ejemplares estudia- 
dos alcanza el tamaño del ejemplar tipo (3.6 
mm, fide Dell, 1964), es posible encontrar en 
ellos todos los rasgos de la concha que ca- 
racterizan a esta especie. 

En la descripción original, Preston (1912) 
Incluyó una figura que ha sido considerada 
poco representativa por autores posteriores, 
sin embargo, Dell (1964) publicó una figura del 
tipo en vista interna que permite reconocerla 
fácilmente. Una vista externa e interna de la 
especie y dibujos de la concha y de su ana- 
tomía se dan en las Figuras 1 , 27, 28, 68 y 69. 

Tanto la concha como las partes blandas 
permiten diferenciar fácilmente a esta es- 
pecie de las otras. Es particularmente intere- 
sante, el que en esta especie aparezca un 
ciego en el estómago, igual al descrito en N. 
{N.)fernandensls y N. (N.) pseudoexgua. su- 
giriendo una posible relación filogenética. 

Distribución Geográfica 

La especie se conocía previamente sólo de 
las Islas Falkland (Preston, 1912: Dell, 1964): 
Oreadas del Sur y Península Antartica (Dell. 
1990). El material estudiado permite extender 
su distribución al Estrecho de Magallanes y 
Bahía Inútil. 

Habitat 

Las muestras estudiadas cubren toda el 
área de dispersión de la especie. Se encon- 
traron ejemplares grandes viviendo en pro- 
fundidades hasta de 46 m, en fango con 



Descripción 

Concha: Concha pequeña (hasta 4.5 mm de 
longitud), redondeada, de perióstraco ama- 
rillo pálido. Umbos anchos y abultados, de su- 
perficie lisa, sin ornamentación, general- 
mente erosionados. Prodisoconcha blanca. 
Escultura formada por líneas radiales finas, 
que cubren completamente la concha: en al- 
gunos ejemplares son visibles en la región 
posterior sólo con fuerte aumento: líneas con- 
céntricas débiles, irregularmente distribuidas, 
más densas hacia el margen ventral: con 
finísimas líneas divergentes, superpuestas a 
las radiales, sólo en la región anterior y pos- 
terior, como en N. (N.) pisum. Región poste- 
rior delimitada por líneas radiales algo más 
fuertes que en el resto de la concha. Condró- 
foro angosto. Dientes pequeños, anchos, ob- 
tusos (no agudizados): los anteriores varían 
entre 8 (ejemplares de menor tamaño) y 12 
(mayor tamaño): los posteriores varían entre 
4 y 6 en los mismos casos. Impresiones 
de los aductores desiguales, el anterior de 
mayor altura que el posterior. Impresiones de 
los músculos dorsal medio y ventral medio, 
continuas, ubicadas bajo un condróforo. Im- 
presiones puntiformes no alineadas: dos de 
ellas más marcadas. 

Anatomía Interna: Manto, glándula del biso, 
corazón, ganglios y musculatura pedal apa- 
rentemente similares a los de N. sulcata, N. 
rugosa y Acila castren si s y como en N. (Л/.) 
pisum. Riñon semejante al de N. nucleus. 
Músculos dorsal medio y ventral medio, jun- 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



129 



tos, situados aproximadamente debajo del 
condróforo. Haces musculares que fijan la 
masa visceral a la concha, separados y des- 
iguales, ubicados en una línea curva, concor- 
dando con las impresiones que se observan 
en la cara interna de las valvas. Aductores an- 
terior y posterior aproximadamente del mismo 
grosor, el posterior de sección más oval que el 
anterior. 

Boca situada junto al aductor anterior. Pal- 
pos alargados, más altos en la región poste- 
rior junto al tentáculo. 

Branquias grandes, de filamentos del- 
toídeos (tendiendo a lo triangular), siendo la 
rama externa de cada filamento de tamaño 
aproximadamente igual a la mitad de la rama 
interna. 

Estómago de gran tamaño, la mitad de su 
altura corresponde al saco del estilo, que 
puede aparecer ensanchado o alargado de- 
pendiendo del grado de contracción del pie. 
Capuchón dorsal terminando sobre el lado 
izquierdo en un ciego digitiforme. Región 
dorso-lateral izquierda a la entrada del esó- 
fago, con cuatro pliegues. Con un gran saco 
(ciego) de posición dorsal a la región de se- 
lección del lado derecho, cuyo extremo se 
dirige posteriormente a la izquierda: sin 
repliegues en su interior. Tiflosol menor ex- 
tendiéndose desde la proximidad de la aber- 
tura del esófago, rodeando el área de selec- 
ción, hasta el saco del estilo. No existen otras 
áreas de selección. Aberturas de los di- 
vertículos digestivos situadas una bajo el esó- 
fago, ligeramente a la derecha, las otras dos 
sobre el lado izquierdo del estómago. Los 
conductos que nacen de las dos aberturas 
más próximas al esófago se dirigen hacia el 
lado derecho; el tercero lo hace hacia la 
izquierda. Intestino muy largo, con un enro- 
llamiento notable y un tiflosol dorsal. A conse- 
cuencia del enrollamiento tan acentuado, el 
esófago y el estómago se hallan desplazados 
considerablemente hacia la izquierda. 

Observaciones 

La presencia en esta especie de un ciego 
estomacal no conocido o descrito anterior- 
mente, nos lleva a sugerir el valor que este 
carácter podría tener en la separación de es- 
pecies del género Nucula. Este ciego no se 
encontró en N. (N.) pisum. 

Distribución Geográfica 

Conocida sólo de la localidad tipo: frente a 
las Islas Juan Fernández (33 35'S; 



78' 31 '2"W): en arena fina, entre 220 y 280 m 
de profundidad. 

Nucula (N.) pisum Sowerby I, 1833 
Figs. 4, 21,22, 62-64, 97, 98 

Nucula pisum Sowerby I, 1833: Nucula fig 
23 (Feb.); Sowerby I, in Broderip & Sowerby 
1833; 198 (13 March) (Localidad tipo; Val- 
paraíso); Hanley, 1843: 172, lám. 20, fig. 23 
d'Orbigny, 1846: 625; Hupé, 1854: 340; Han- 
ley, 1856: 376, lám 20 fig. 12; Hanley, 1860 
153, lám. 229, fig. 133; Sowerby II, 1870: Nu 
cula lám. 4, fig. 24; Philippi, 1887: 190, lám 
41 , fig. 25 (Fósil en la Hacienda de la Cueva) 
Dalí, 1909; 250; Hertlein y Strong, 1940; 387 
Carcelles, 1950; 73; Soot-Ryen, 1959; 12, 
lám. 1 , figs. 1 , 2; Powell, 1 960, 5: 1 70. 

Linucula pisum {Sowerby), Dell, 1964; 144, 
lám. 2, figs. 7, 8; Ramorino, 1 968: 1 83, lám. 1 , 
fig. 4, lám. 4, fig. 2. 

Nucula (Linucula) pisum Sowerby, Bernard, 
1983; 10. 

Material Estudiado 

450 ejemplares (ej) y 8 valvas (v); MZUC. 
Procedencia: (1) 14 ej, 1.2-4.1 mm (No. 
4653), Bahía Mejillones, Punta Cuartel (cerca 
Pta. Angamos); arena, 2-3 m. (2) 61 ej, 2-5 
mm (No. 4604), Coquimbo, Bahía La He- 
rradura (29^ 57'S; 71 22'W). (3) 3 ej, 6 v. 
2.8-3.5 mm (No. 4594), M.Ch.l, Est. 1, frente 
a Coquimbo (29'57.4'S; 71 22.4'W); fango 
conchífero, 82-88 m. (4) 1 ej s, 2.4 mm (No. 
4590). M. Ch. I, Est. 20-21 , al S de Coquimbo 
(31 51.5'S; 71 35'W); restos de conchas. 88 
m. (5) 1 50 ej, 1 .5-4 mm (No. 4735), Bahía de 
Valparaíso (33 S); fango, 200 m. (6) 20 ej s, 
2-3.4 mm (No. 4675), M. Ch.l, Est. 39, Chile 
central (34 08.4'S; 72'02.5'W); fango-arena, 
90 m. (7) 185 ej, 2.3-4 mm (No. 4683-4685, 
4688, 4690, 4693, 4698, 4699, 4701, 4718, 
4721, 4722, 4725, 4728), draga van Veen, 
Bahíade Concepción (36'S); fango, 10-27m. 
(8) 7 ej s, 2.5-3.8 mm (No. 4596), M. Ch. I, Est. 
68, frente a Arauco (37 06'S; 73"38'W); arena 
gruesa-roca y "cascajo", 58 m. (9) 1 ej s, 2.7 
mm (No. 4595), M. Ch. I. Est. 77, al S de Lebu 
(38 16'S; 73"41'W); fango, arena fina, 
120-160 m. (10) 4 ej, 2-3 mm (No. 4737), M. 
Ch. I, Est. 79, al S de Lebu (38°16'S; 
74''06'W): fango-arena fina, 110 m. (11) 1 ej, 2 
mm(No. 4681),M.Ch. I, Est. (117) X 1, Golfo 
de Concorvado (42'55'S; 72"55'W); arena- 
fango-cantos, 190 m. (12) 3 ej, s, 2.2-3.3 mm 
(No. 4549), Op. Centolla, Est. P5M2, draga 



130 



VILLARROEL & STUARDO 



Petersen 0.1 m^, E. de Magallanes, Bahía Inú- 
til (53'30'S; 6949'W); fango calcáreo, abun- 
dantes conchas, 46 m. (13)3ej2.4-3mm(No. 
4550), Op. Centolla, Est. P4M2, draga Pe- 
tersen 0.1 m^, E. de Magallanes, Bahía Inútil 
(53°30'S; 69°49'W); fango calcáreo con con- 
chas, 52 m. (14) 2 ej, 2v, 2.6-2.7 mm (No. 
4551), Op. Centolla, Est. P4M1, draga Pe- 
tersen 0.1 m^, E. de Magallanes, Bahía Inútil 
(53°30'S; 69°49'W); fango calcáreo con con- 
chas, 52 m. (15) 3 ej, 2.9-3 mm (No. 4739), 
Op. Centolla, Est. P5M6, draga Petersen 0.1 
m , E. de Magallanes. Bahía Inútil (53''30'S; 
69°49'W); fango con algas, esponjas, brio- 
zoos y conchas, 46 m. (16) 6 ej, 2.5-3 mm 
(No. 4554), Op. Centolla, Est. P5M5, draga 
Petersen 0.1 m^, E. de Magallanes, Bahía Inú- 
til (53'30'S; 69°49'W); fango calcáreo con 
conchas, 46 m. 

Descripción 

Concha: Concha pequeña (hasta 5 mm de 
longitud), subtrígona, oblicua y semiinflada, 
de aspecto vitreo, a veces con viso nacarado. 
Prodisoconcha frecuentemente blanca, muy 
prominente. Perióstraco crema o anaranjado, 
generalmente cubierto en las regiones ante- 
rior y posterior con depósitos de color rojizo. 
Umbos posteriores poco elevados. Bordes 
dorsal anterior y ventral levemente curvados; 
dorsal posterior extremadamente corto y 
curvo. Extremo anterior muy largo y arqueado, 
posterior casi truncado. Ornamentación de 
líneas radiales finas, visibles por transparen- 
cia, que nacen en los umbos y cubren toda la 
superficie; en el área lunular y escutelar se ob- 
servan sólo con fuerte aumento. Estrías de 
crecimiento distribuidas irregularmente, más 
notorias hacia el borde dorsal o anterior y pos- 
terior; interrumpen a las radiales originando 
una aparente ornamentación reticulada. 
Areas lunular y escutelar más brillantes que el 
resto de la concha, cubiertas densamente con 
finas líneas divergentes. Margen ventral in- 
terno crenulado. Charnela con 7 a 14 dientes 
anteriores y 3 a 7 posteriores, según la talla 
del individuo; los dientes son aguzados y cur- 
vados hacia afuera. Condróforo piriforme, pe- 
queño, dirigido anteriormente formando un 
ángulo casi recto con la corrida de dientes 
posteriores. Impresión del aductor anterior 
subcircular; la del posterior alargada vertical- 
mente. Impresiones de los músculos medio- 
dorsal y medio-ventral contiguas, ubicadas 
muy cerca de la charnela, por delante del con- 



dróforo. Impresiones punctiformes cercanas a 
la charnela. La mayor situada a mitad de 
camino entre el aductor anterior y la impresión 
de los músculos medios; el resto, próximas a 
las impresiones de los músculos medios 

Anatomía Interna: Bordes del manto lisos sin 
papilas. Glándula del biso grande. Glándula 
hipobranquial voluminosa cubriendo más de 
la mitad de las branquias y parte del palpo. 
Lámelas del palpo más altas en su parte 
media. Ctenidios grandes con sus ramas di- 
rigidas anteriormente. Filamentos bran- 
quiales delgados y numerosos, con ambas 
ramas prolongándose sobre el eje; la rama 
externa es aflechada. Corazón con aurículas 
grandes; ventrículo alargado. Area de selec- 
ción del estómago con pocos pliegues (no 
más de 10). Con sólo un área plegada (¿área 
de selección?) sobre la entrada del esófago. 
Intestino, relativamente largo, con pocas 
vueltas (no más de tres); su distribución varía 
individualmente, pero conserva un plan ge- 
neral, en forma de 8. 

Observaciones 

El tipo de N. (Л/.) pisum fue examinado por 
Dell (1964), y transferido al género Linucula, 
subgénero propuesto por Marwick (1931) 
para algunas especies fósiles neoze- 
landesas. Dell (1956) describió las primeras 
especies vivientes de Nueva Zelandia y dis- 
cutiendo una de ellas, concluyó que la escul- 
tura divergente tan peculiar a estas especies, 
su restricción geográfica a Nueva Zelandia y 
la historia del grupo durante el terciario, per- 
mitían considerarlo como un género. Dell 
(1964) al discutir nuevamente la posición de 
Linucula, fundamentó el género en la combi- 
nación de los siguientes caracteres; "Margen 
crenulado, a menudo extendiéndose alrede- 
dor de las valvas; radiales bien marcadas; es- 
cultura divergente sobre la lúnula y el es- 
cutelo y falta de hinchamiento." Maxwell 
(1988), siguiendo a Dell (1964), lo considera 
digno de rango genérico. 

El estudio de la concha de N. (N.) pisum y 
de N. (Л/.) fernandensis mostró (Villarroel, 
1971), que ambas especies presentan los 
caracteres descritos por Dell (1956, 1964) 
para el género Linucula y que, en consecuen- 
cia, este último se diferenciaría del género 
Nucula sólo por la presencia de las líneas 
finísimas que cruzan a las radiales en la 
lúnula y escutelo, dando la impresión de di- 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



131 



vergencia. Sin embargo, Villarroel (1971) 
considera que el valor taxonómico de estas 
líneas parece relativo, ya que además de 
constatar diferencias en estas dos especies 
en la charnela y en la forma y disposición de 
los distintos órganos, N. (N.) fernandensls 
presenta un ciego posterior en el estómago 
que existe también en N. (Л/.) pseudoexigua y 
N. (Л/.) falklandica. pero no en N. (N.) pisum. 
Este ciego podría corresponder a un carácter 
filogenético importante, pero ésto podrá ser 
valorado sólo cuando se estudie la anatomía 
de las especies neozelandesas de Linucula. 

La variación en el número y forma de los 
dientes no permite utilizarlos como caracteres 
de valor genérico o supragenérico, ya que 
varía considerablemente con el crecimiento 
en una misma especie y aún en individuos del 
mismo tamaño; sin embargo, la forma y el 
tamaño de los dientes presentan a menudo 
valor específico, como lo han hecho notar al- 
gunos autores (Knudsen, 1970: Villarroel, 
1971). 

En esta especie es común encontrar epi- 
zoos tubícolas sobre las valvas, los que se 
ubican preferentemente en las áreas dorsal 
anterior y posterior, además de, o en lugar de 
los depósitos de color rojizo que la caracteri- 
zan. 

Distribución Geográfica 

Bahía de Mejillones (Antofagasta) a Estre- 
cho de Magallanes. 

La distribución de N. (Л/.) pisum. que hasta 
hace poco sólo se conocía para la localidad 
tipo de Valparaíso, fue ampliada por Ramo- 
rino (1968) hacia el S hasta Chiloé. El abun- 
dante material aquí estudiado permite, sin 
lugar a dudas, extender su distribución por el 
N, hasta Bahía Mejillones (Antofagasta) y 
hacia el S, hasta el Estrecho de Magallanes y 
Bahía Inútil. Las localidades de recolección 
estudiadas permiten, además, demostrar la 
continuidad de su distribución entre Antofa- 
gasta y el Golfo de Corcovado, pero no exis- 
ten datos que permitan asegurar tal con- 
tinuidad desde el Golfo de Corcovado hasta 
el Estrecho de Magallanes. Esa zona ha sido 
muy pobremente muestreada. 

Habitat 

Esta especie se encuentra en un amplio 
rango de distribución vertical, desde 8 a 200 
m, en fondo arenoso, arena fangosa y fango 
arenoso. 



Se encontró gran diferencia de densidad de 
N. (N.) pisum, al comparar los datos 
obtenidos por Ramorino (1968) en la Bahía 
de Valparaíso, con los logrados en la Bahía 
de Concepción. En esta última, la profundi- 
dad máxima de rastreo fue de 50 m (no exis- 
ten profundidades mayores), encontrándose 
N. (N.) pisum sólo entre 10 y 27 m con una 
densidad de aproximadamente 30 ejem- 
plares/m^. En cambio, en la Bahía de Val- 
paraíso se rastreó hasta los 200 m, encon- 
trándose la densidad mínima (465/m^) en 
zona arenosa entre 20 y 50 m y una máxima 
(848 ejemplares/m^) en fango arenoso entre 
51 y 80 m. 

Ambas coinciden, sin embargo, al 
demostrar la mayor densidad en un substrato 
de fango arenoso. 

Nucula (N.) pseudoexigua sp. nov. 

Figs. 18-20,65-67, 104-106 

Material Estudiado 

9 ejemplares (ej) y 7 valvas (v); MZUC. 
Procedencia: (1) 1 ej, 4v, 2.5-4 mm (No. 
10304, 10305, Paratipos), "Hero" 69-5, Est. 9 
(201), Confluencia Canales Trinidad y Con- 
cepción (50"9'55"S: 74 43'75"W); arena y 
grava, 390-460 m. (2) 7 ej, 2.3-5.1 mm (No. 
10306, 10308, Paratipos), "Hero" 69-5, Est. 
57, (50"0'50"S; 74'=14'10"W): fango, 223 m. 
(3) 1 ej s, 3.5 mm (No. 10293, Holotípo), 3v 
3.2-3.5 mm (No. 10307, Paratipos), "Hero" 
69-5, Est. 211, Canal Sarmiento (51 12'S: 
74 9'W): fango, 500 m. 

Localidad Tipo 

Canales del sur de Chile entre 50'9'S; 
7443'W y 51°12'S; 74 9'W; 223 a 500 m de 
profundidad. 

Descripción 

Concha: Concha pequeña (hasta 5.1 mm de 
longitud), suborbicular, débilmente globosa, 
blanca, translúcida de aspecto vitreo con viso 
nacarado. Prodísoconcha blanca, opaca, lisa. 
Perióstraco amarillo verdoso claro. Umbos 
poco prominentes. Borde dorsal anterior ar- 
queado y formando un ángulo con el borde 
ventral curvado; borde posterior suavemente 
arqueado, no truncado. Ornamentación de las 
valvas formada por costillas concéntricas, 
fuertes, espaciadas regularmente, cuyadirec- 



132 



VILLARROEL & STUARDO 



ción no cambia sobre las áreas dorsales; son 
más débiles sobre la lúnula y en algunos ejem- 
plares se interrumpen en uno o dos puntos de 
su curso aparentando una bifurcación. Hay 
estrías radiales finísimas y densas sobre las 
concéntricas, que tienden a desaparecer 
hacia los extremos anterior y posterior. Lúnula 
delimitada por un surco débil. Areas dorsales 
con finas líneas microscópicas divergentes 
que cruzan a las radiales y las concéntricas. 
Superficie interna de las valvas lisa, trans- 
parentando la ornamentación externa; mar- 
gen ventral interno crenulado. Dientes de la 
charnela fuertes, agudizados, curvados débil- 
mente hacia afuera; se cuentan 7 a 12 anteri- 
ores y 4 a 7 posteriores, según la talla del in- 
dividuo; en la valva derecha, el diente 
posterior al condróforo tiene una base equiva- 
lente a dos dientes juntos. 

Anatomía Interna: Disco pedal con incisiones 
bien marcadas en sus bordes, los que apare- 
cen parcialmente divididos. Glándula hipo- 
branquial grande, cubriendo más de la mitad 
de la branquia. Palpos con un surco lateral 
externo notorio y tentáculo grande. Branquias 
con filamentos internos y externos casi 
¡guales. Cavidad pericárdica ubicada detrás 
del condróforo. Corazón simétrico con el ven- 
trículo alargado y globoso y las aurículas 
trilobuladas en su unión con los ventrículos. 
Estómago grande, con el área de selección 
mayor provista de numerosos repliegues 
(hasta 18); área de selección en la entrada 
del esófago (as^) muy desarrollada; ciego 
posterior del estómago, grande. Intestino 
largo, con dos surcos (tiflosoles), y no menos 
de cuatro vueltas. 

Observaciones 

Nucula (N.) pseudoexigua se caracteriza 
por su ornamentación de costillas concéntri- 
cas bien marcadas y difiere de N. semiornata 
d'Orbigny, 1846, del Atlántico, la especie que 
más se le parece, porque estas costillas no 
cambian de dirección abruptamente. En N. 
semiornata se observa un cambio de direc- 
ción en las estrías concéntricas, tan notorio 
como en N. exigua Sowerby I, 1833, una es- 
pecie tropical circunscrita a la Provincia 
Panameña. 

Probablemente sea esta nueva especie la 
que condujo a error a Dalí (1908a) al citarla 
como N. exigua para el Estrecho de Maga- 
llanes; difiere de esta última principalmente 
por las costillas concéntricas que no sufren 
cambio de dirección sobre la lúnula y el es- 



cutelo, y por el menor inflamiento de las val- 
vas. 

Distribución Geográfica 

Conocida sólo de la localidad tipo. 

Habitat 

La mayor densidad de esta especie se en- 
contró a una profundidad de 223 m en subs- 
trato de fango, disminuyendo entre 390 y 460 
m en substrato de arena y grava; su menor 
abundancia se halló a 500 m, en substrato de 
fango. 

Subfamilia Nuculominae Maxwell, 1988 

Sin prismas radiales. 

Género Ennucula Iredale. 1931 

Ennucula Iredale. 1931; 202, 231. Especie 
tipo designación original; Nucula obliqua 
Lamarck, 1819. 

Diagnosis 

Concha subovalada a oval-alargada, mo- 
deradamente inflada; sin ornamentación ex- 
terna conspicua, sólo provista de líneas de 
crecimiento. Margen ventral de las valvas 
liso. Condróforo notablemente oblicuo. Mar- 
gen del manto provisto de papilas. 

Especies encontradas en Chile; 

1. Ennucula grayi {d'Orb\gny, 1846) 

2. Ennucula puelcha {аЮгЬ\дпу. 1842) 

3. Ennucula eltaniniDe\\.^990 

Las revisiones de bivalvos chilenos re- 
cientes (Soot-Ryen, 1959; Dell, 1964, 1990). 
han concluido que existen cuatro especies de 
Ennucula en Chile; E. colombiana. E. puelcha, 
E. grayi y E. eltanini. 

Ennucula colombiana (Dalí, 1908a) fue 
descrita originalmente de Panamá, Colombia 
y Ecuador entre 29.5 y 401 brazas y citada 
también en el S de Chile, en 1 22 y 1 94 brazas 
(224.5 y 357 m) y en la costa W de la Pata- 
gonia, 51 '1 2'S en 258 brazas (51 6 m). Su dis- 
tribución en la parte S de Sudamérica fue 
mantenida por autores subsecuentes (Hert- 
lein y Strong, 1940; OIsson, 1961 y Dell, 
1 964), pero Ramorino (1 968) puso estas citas 
en duda al considerarlas como correspondi- 
entes a probables ejemplares juveniles de E. 
grayi. 

La revisión de abundante material del área 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



133 



magallánica permite concluir que existen ahí 
sólo tres especies de Ennucula: E. eltanini, E. 
grayi. y E. pueicha. Los juveniles de las dos úl- 
timas especies son fácilmente diferenciables; 
sin embargo, la conclusión de Ramorino 
(1968) de que los juveniles de E. grayi co- 
rrespondan a la especie E. colombiana Dalí 
(1908), no se justifica, ya que son los juveniles 
de E. puelctia los que se asemejan más a la 
descriptción de Dalí y a las figuras de OIsson 
(1961: lám. 1, fig. 3, За). Parece poco proba- 
ble que, de existir E. colombiana en la zona de 
Magallanes, se haya escapado al intenso 
muestreo de que ha sido objeto esa zona. 

Dell (1 990) describió la pequeña especie E. 
eltanini, de 4.1 x 3.2 mm, para la zona del Es- 
trecho de Magallanes y Oeste de Tierra del 
Fuego entre 307 y 544 m. Esta especie se 
diferencia fácilmente de E. grayi y E. pueicha 
por la prominencia de sus umbos y su pe- 
queño condróforo. 

La descripción y distribución de las dos es- 
pecies estudiadas se discute a continuación. 

Clave Para las Especies de 
Ennucula Estudiadas 

1. Concha subovalada, inflada; margen 
dorsal anterior no elevado; lúnula plana, sub- 
cordada. Impresiones de los aductores cons- 
picuas, sobre un área cóncava. Borde ante- 
rior del manto generalmente sin papilas; si las 
hay, sólo se las encuentra dorsal y anterior- 
mente al aductor; bordes posteriores con pa- 
pilas mameliformes E. grayi 

1'. Concha oval-alargada, poco inflada; 
margen dorsal anterior y área lunular de las 
valvas, elevadas. Impresiones de los aduc- 
tores poco visibles y ubicadas en un área 
plana. Bordes del manto con papilas, las an- 
teriores mameliformes y las posteriores digiti- 
formes E. pueicha 

Ennucula grayi {d'Orblgny, 1846) 
(Figs. 8, 70, 71, 73, 107-109) 

Nucula obligua Lamarck, Sowerby I, 1833; 
Nuculai\g. 21, non Lamarck, 1819; Hanley, 
1860; 156-157 lám. 229, fig. 150. 

Nucula gray/ d'Orbigny, 1846; 625; Hupé, 
1854; 304; Sowerby II, 1870; Nucula lám. fig. 
13. Mabille y Rochebrune, 1889; H112; Dalí, 
1909; 250; Hertlein y Strong, 1940; 385. 

Nucula tanneri DaW. 1908a; 219, 367 (Loe 
tipo; Estrecho de Magallanes en 369 brazas) 
Hertlein y Strong, 1 940; 388; Carcelles, 1 950 
73; Carcelles y Williamson, 1951 ; 322. 

Ennucula grayi (d'Orbigny), Soot-Ryen 



1959; 13, lám. 1, fig. 3; Dell, 1964; 142, lám. 
2, figs. 3-6; Linse, 1997; 45. 

Nucula {Leionucula) grayi d'Orbigny, 
Bernard, 1983; 10. 

Material Estudiado 

85 ejemplares (ej) y 50 valvas (v); MZUC. 
Procedencia; (1 ) 1 v i, 1 4 mm (No. 4600), Exp. 
M. Ch. I, Est. 21-22, al S de Coquimbo 
(31''5rS; 71°40'30"W); fango-arena, 
130-200 m. (2) 1 ej, 16 mm (No. 4736), Bahía 
de Valparaíso (33 'S); fango. (3) 1 v i, 20.6 mm 
(No. 4564); IFOP 01, Est. 57, frente a lloca 
(34"56'54"S; 72 19'30"W), 94 m. (4) 6 v, 
16-17 mm (No. 4598 Exp. M. Ch. I, Est. 69, 
frente a Coronel (37''06'S; 73'38'W); roca, 
96-100 m. (5) 1 ej s, 16 mm (No. 4599), Exp. 
M. Ch. I, Est. 79, al S de Lebu (38^1 6'S; 
74^06'W); fango-arena fina, 110 m. (6) 13 v, 
14-18 mm (No. 4676), Exp. M. Ch. I, Est. 77, 
Chile austral (38"1 6'S; 73°41 'W); fango-arena 
fina, 120-160 m. (7) 1 ej s, 17 mm (No. 4567), 
Exp. M. Ch. I, Est. 90, Chile austral (39 03'S; 
73 5rW); "cascajo", 1 74 m. (8) 1 ej, 2 v, 2-3.5 
mm (No. 4738). "Hero" 69-5, Est. 210, draga 
Petersen 0.1 m^, Bahía Corbeta Papudo 
(Guareno) (50"21'17"S; 75"17'25"W); fango 
amarillo verdoso, 70-78 m. (9) 23 ej, 2.5-4 
mm (No. 4555), "Hero" 69-5, Est. 56, 
(51-0'50"S; 74 14'10"W); fango fino, 221 m. 
(10) 10 ej, 2-8 mm (No. 4615), "Hero" 69-5, 
Est. 213 (51 27'30"S; 74 03'W); fango, 722 
m. (1 1 ) 40 ej, 24 V, 2-1 5 mm (Nos. 461 7, 461 9, 
4621), "Hero" 69-5, Est. 280. draga Petersen 
0.1 m^, E. de Magallanes (53'17'18"S; 
7048'36"W); fango-arenoso, 180-210 m. 
(1 2) 2 ej. 1 4 mm (No. 4628), "Hero" 69-5, Est. 
280 В. draga Petersen 0.1 m^, E. de Maga- 
llanes (53 17'18"S; 7048'36"W); fango con 
muy poca arena, 178,5 m. (13)3ej, 12-1 4 mm 
(No. 4629), "Hero" 69-5. Est, 280 C, draga Pe- 
tersen 0.1 m^. E. de Magallanes (53 17'18"S; 
70'48'36"W); fango con muy poca arena, 1 79 
m. (14) 3 ej, 3v, 13-14 mm (No. 4606). "Hero" 
69-5, Est. 279 C, draga Petersen 0.1 m^, E. de 
Magallanes (53=1 5'S; 70 50'18"W); fango, 
156 m. 

Descripción 

Concha: Concha de regular tamaño (hasta 
20.6 mm de longitud), gruesa subovalada, in- 
flada, de color blanco amarillento, opaca. Pe- 
rióstraco brillante, con bandas concéntricas 
irregulares de color oliva claro, que se alter- 
nan con bandas más oscuras y aumentan su 
tono hacia el borde ventral, llegando hasta 



134 



VILLARROEL & STUARDO 



pardo negruzco. Con depósitos de un material 
oscuro en la región dorsal, que pueden llegar 
a cubrir la concha completamente. Umbos in- 
flados, amplios, ubicados en el tercio posterior 
de la concha; ápices opistogiros. Borde dorsal 
anterior suavemente arqueado y casi el doble 
más largo que el posterior, que es recto; már- 
genes anterior, ventral y posterior redondea- 
dos. Ornamentación formada por estrías de 
crecimiento que, al cruzar el borde del es- 
cutelo se dirigen en forma oblicua hacia los 
ápices y estrías radiales tenues e irregu- 
larmente dispuestas, visibles con mayor faci- 
lidad en la parte ventral y en los individuos 
jóvenes. Lúnula subcordada, plana junto a los 
ápices, delimitada por una línea más clara en 
el perióstraco; escutelo no delimitado. Interior 
de las valvas blanco verdoso, nacarado con 
brillo iridiscente, rara vez de color verde. Serie 
de dientes de la charnela formando un ángulo 
casi recto. Condróforo ancho. Impresiones de 
los aductores muy profundas y ubicadas en la 
mayor curvatura producida por el inflamiento 
de las valvas. Impresión de los músculos 
medios una más arriba que la otra. Impre- 
siones puntiformes dispersas. 

Anatomía Interna: Borde anterior del manto 
sin papilas; si existen son pequeñas, poco no- 
torias y sólo ubicadas dorsal y anteriormente 
al aductor; borde posterior con papilas 
mameliformes. Palpos generalmente más an- 
chos en la región media. Corazón con aurícu- 
las globosas; origen de la aorta anterior ale- 
jado del recto, junto a la aurícula. Estómago 
como en E. puelcha. 

Observaciones 

Ennucula grayi se presenta generalmente 
cubierta con depósitos oscuros color rojizo en 
la región dorsal principalmente. Las muestras 
de la zona sur se caracterizaron por la fre- 
cuencia de un epizoo Hidroídeo que cubría 
las valvas, ubicándose preferentemente en la 
región dorsal y en la ventral anterior. 

Esta especie fue la que presentó el mayor 
tamaño entre los nucúlidos estudiados (20.6 
mm de longitud). 

Las diferencias de esta especie con E. 
puelcha se discuten en las observaciones de 
esta última. 

Distribución Geográfica 

Desde 45' Lat S en la Costa Atlántica al Es- 
trecho de Magallanes y la costa de Chile, 
hasta Coquimbo (31 ''51 'S) hacia el N. 



Ramorino (1968) concluyó que las citas de 
Ennucula savatieri y Nucula cardara Dalí, 
1916, de San Diego por Parker (1964), eran 
sinónimos de E. grayl, lo que le permitió ex- 
tender la distribución de esta especie hasta 
América Central y California. No existiendo 
mayor información taxonómica que lo justi- 
fique, tales citas nos parecen dudosas. 

Habitat 

Las muestras estudiadas cubren toda el 
área de dispersión conocida de esta especie 
en la costa chilena, desde 31 '51'S; 71°40'W 
(al S de Coquimbo) hasta el Estrecho de Ma- 
gallanes, en profundidades de 94 hasta 722 m 
en substrato de fango arenoso, presentando 
una mayor abundancia entre 180 y 221 m. 

Ennucula puelcha (d'Orbigny, 1 842) 
(Figs. 29-32, 72, 110-112) 

Nucula puelcha d'Orbigny, 1842; 162 (Loe. 
tipo; Bahía San Blas, Patagonia); d'Orbigny, 
1 846; 644, lám. 84, figs. 24-26; Hanley, 1 860; 
156, lám. 230, fig. 149; Sowerby II, 1870, Nu- 
cula lám. 1, sp. 7 Figueiras y Sicardi, 1968; 
258. 

Nucula uruguayensis Smith, 1880; 320 
(Loe. tipo; Río de la Plata); Smith, 1885; 229, 
lám. 18, fig. 12-12b; Pilsbry, 1897; 9; Smith, 
1915; 97; Carcelles, 1994; 26; Figueiras y 
Sicardi, 1968; 258. 

Nucula savatieri Mabille y Rochebrune, 
1889; H112, lám. 8, fig. 2a-c (Loe. tipo; Canal 
Beagle.); Dali, 1908a; 367, lám, 18, fig. 11; 
Hertlein y Strong, 1940; 387; Carcelles, 1950; 
73, lám. 3, fig. 62; Carcelles y Williamson, 
1951; 323. 

Nucula pigafettae Dalí, 1908a; 219, 368 
(Loe. tipo; Estrecho de Magallanes); Hertlein 
y Strong, 1940; 386; Carcelles y Williamson, 
1951; 322. 

Nucula agujana Dalí, 1908a; 370, lám. 10, 
figs. 6, 7 (Loe. tipo; Punta Agujas, Perú). 

Nucula (?) agujana Dalí, Hertlein y Strong, 
1940; 384. 

Nucula fe//ppone/ Marshall, 1929; 6, lám. 4, 
figs. 10-12 (Río de la Plata; en estómago de 
Micropogon undulatus Linné). 

Nucula {Ennucula) puelcha d'Orbigny, 
Schenck, 1939; 30, lám. 8, figs. 5-8. 

Ennucula savatieri Mabille y Rochebrune, 
Soot-Ryen, 1959; 13. 

Ennucula puelcha (d'Orbigny), Dell, 1964; 
141. 

Nucula (Leionucula) puelcha d'Orbigny, 
Bernard, 1983; 10. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



135 



Material Estudiado 

34 ejemplares (ej) y 15 valvas (v); MZUC. 
Procedencia: (1) 1 ej, 10 mm (No. 4603), M. 
Ch. I, Est. 51, Chile central (34 56'S; 
72'14'W): fango-arena, 50 m. (2) 1 ej, 10 mm 
(No. 4602), M. Ch. I, Est. 77, Chile central 
(38°16'S; 73^ 41 'W); fango-arena fina, 80 m. 
(3) 9 V, 14.4-16.2 mm (No. 4566), M. Ch. I, 
Est. 96, al S de Mehuín, Valdivia (39 59'55"S: 
74^01 '7"W); arena gruesa-cantos, 260-295 
m. (4) 1 ej, 5 mm (No. 4601), M. Ch. I, Golfo 
de Ancud (42 55'S; 72 55'W); arena-fango- 
cantos, 190 m. (5) 4 ej, 4.6-10.5 mm, 1v, 4.5 
mm (Nos. 4645, 4654), "Hero" 69-5, Est. 56, 
Puerto Bueno, Canal Sarmiento (51 0'50"S; 
74 14'10"W): fango, 221 m. (6) 1 ej, 10 mm 
(No. 4608), "Hero" 69-5. Est. 279 С, E. de Ma- 
gallanes (53"15'S; 70 50'3"W); arena fina 
con piedrecillas, 156 m. (7) 10ej,4v, 10.3-12 
mm (Nos. 461 8, 4622), "Hero" 69-5. E. de Ma- 
gallanes (53-17'18"-53 18'40"S; 70'48'36"- 
70"42'20"W); fango arenoso, 180-210 m. (8) 
4 ej, 5-8 mm (No. 4635), "Hero" 69-5, Est. 
280 В. E. de Magallanes (53-17'18"S; 
70^48'36"W); fango arenoso, 178, 5 m. (9) 1 
ej, 2v, 5 mm (No. 4638), "Hero" 69-5, Est. 
244(27), E. de Magallanes (53"03'3"S; 
7r46'36"W). 

Descripción 

Concha: Concha de regular tamaño (hasta 
16.2 mm de longitud), subovalada, alargada 
en sentido antero-posterior, poco inflada, 
blanca. Perióstraco brillante, bandeado de 
tono oliva claro, rara vez pardo negruzco en 
su margen ventral: su color aumenta de in- 
tensidad en los adultos (algunos ejemplares 
poseen depósitos de color ferruginoso sobre 
la región dorsal). Umbos poco abultados con 
ápices levemente opistogiros. Borde dorsal 
anterior más largo que el posterior, elevado: 
borde anterior truncado, formando un ángulo 
con el borde ventral: bordes restantes re- 
dondeados. Ornamentación de las valvas for- 
mada por leves estrías de crecimiento, más 
aparentes hacia el margen ventral: estrías ra- 
diales tenues e irregularmente dispuestas, 
más conspicuas en la parte ventral y en indi- 
viduos jóvenes. Lúnula de color más claro 
que el resto de la concha, levemente elevada, 
delimitada por una banda clara del periós- 
traco. Escutelo delimitado por un surco débil. 
Interior de las valvas generalmente verde in- 
tenso. Condróforo angosto. Impresiones de 
los aductores poco marcadas y ubicadas 
sobre un área casi plana. Impresiones de los 



músculos medios una al lado de la otra. La 
mayoría de las impresiones puntiformes se 
encuentran agrupadas cercanas al aductor 
anterior. 

Anatomía Interna: Bordes anterior y posterior 
del manto con papilas; las anteriores como 
botones y las posteriores digitiformes. Palpos 
generalmente más anchos en la región pos- 
terior junto al tentáculo. Corazón con aurícu- 
las cónicas: origen de la aorta anterior cer- 
cana al recto. Estómago con el área de 
selección mayor (as) muy grande, con innu- 
merables repliegues. Otras áreas de selec- 
ción muy desarrolladas, especialmente as^ 
que cubre el lado izquierdo y dorsal de la en- 
trada del esófago. Con una vuelta en la región 
gástrica del intestino. 

Observaciones 

Ennucula puelcha se différencia de E. grayi 
por una menor convexidad y menor razón es- 
pesor/longitud de las valvas, una lúnula ele- 
vada, por poseer papilas en el borde del 
manto tanto en su borde anterior como poste- 
rior, y el ohgen de la aorta anterior junto al 
recto. Además, no alcanza nunca colores tan 
oscuros como E. grayi y sobre su superficie 
no se encontraron epizoos. 

Según Dell (1964) tanto E. puelcha como 
E. grayi deberían considerarse como sub- 
especies de una especie polítipica, dada el 
amplia área de superposición conocida para 
ambas especies y el número de formas (es- 
pecies) descritas que han pasado a la sino- 
nimia de la una y de la otra. Dell señala tam- 
bién que estudios de especies vivientes de 
Ennucula a nivel mundial, han mostrado que 
en cualquier área faunística es raro encontrar 
más de una especie. 

Tal apreciación parece respaldada con el 
estudio de algunas partes de la concha, pero 
para precisar criterios definitivos de politipia 
es necesario considerar también el estudio 
comparativo de las partes blandas y la 
ecología de cada especie. Por el momento 
las diferencias indicadas justifican su sepa- 
ración. 

Las vueltas de la región gástrica del in- 
testino fueron consideradas por Yonge (1 939) 
características de la familia Nuculanidae, 
como consecuencia de una mayor actividad: 
sin embargo, las encontramos también en 
Nucula (N.) fernandensis y en Ennucula 
puelcha, entre las especies de la familia Nu- 
culidae aquí estudiadas (Figs. 24,30). Si la 



136 



VILLARROEL & STUARDO 



función postulada por Yonge es correcta, este 
carácter indicaría que las especies nom- 
bradas son también muy activas, aunque 
hasta este momento es más cauto sugerir so- 
lamente que, este carácter se encuentra pre- 
sente en algunas especies tanto de Nucu- 
lacea como de Nuculanacea, sin precisar una 
función determinada. 

Distribución Geográfica 

Desde el Estrecho de Magallanes a Río 
Grande do Sul por el Atlántico y hasta Punta 
Aguja, Perú, por el Pacífico. 

Habitat 

Las muestras estudiadas cubren sólo parte 
del área de dispersión de esta especie. En- 
nucula puelcha es muy poco abundante; se 
encontró desde los 34'56'S (Chile central) 
hasta el Estrecho de Magallanes, entre 50 y 
295 m de profundidad, en sustrato de fango 
arenoso. Su mayor densidad se obtuvo entre 
180 y 210 m de profundidad. En las muestras 
del Estrecho de Magallanes se halló junto a 
E. grayi. Tlndaria virens y Yoldiella chilenica. 

Con anterioridad E. puelcha ha sido re- 
gistrada en fondos de fango (como E. pigafet- 
tae Dalí y E. agujana Dalí) en profundidades 
que varían entre 77 y 1036 brazas (139 m y 
186.4 m, respectivamente). Originalmente 
fue descrita sobre bancos de arenas someras 
que se descubren con la marea baja. 

Superfamilia Nuculanacea H. Adams y A. 
Adams, 1858 

Descripción 

Concha algo alargada posteriormente, 
equivalva, inequilateral; parte anterior corta, 
redondeada y convexa, parte posterior ge- 
neralmente más larga que la anterior; extremo 
angosto y a menudo rostrado. Apices orto u 
opistogiros. Ligamento interno o externo. Inte- 
rior aporcelanado, rara vez nacarado. Char- 
nela acodada o casi recta, con o sin condró- 
foro. Generalmente con seno paleal. Con o sin 
glándula hipobranquial. Bordes del manto 
más o menos unidos. Aductor anterior más 
grande que el posterior. Ctenidios de posición 
horizontal, más o menos angostos, sujetos en 
toda su extensión. Corazón atravesado por el 
recto o ventral a él. 



Nuculanidae H. Adams y A. Adams, 1858 
(= Ledidae H. Adams y A. Adams, 1858) 

Descripción 

Concha alargada, rara vez entreabierta an- 
teriormente. Ligamento generalmente in- 
terno, proyectado a veces hacia el margen 
dorsal, llegando a ser parcialmente externo. 
Interior aporcelanado. Línea paleal con seno 
paleal. Sifones desarrollados; por lo general, 
el exhalante forma un tubo completo y el in- 
halante es abierto ventralmente. Glándula 
hipobranquial pequeña, a veces, ausente. 
Corazón atravesado por el recto. 

Los representantes recientes de esta fa- 
milia viven en la actualidad en todos los 
mares y a distintas profundidades, prefe- 
rentemente en fondos blandos. 



Observaciones 

Algunos autores utilizaron esta familia bajo 
el nombre de Ledidae, pero a pesar de que 
como fuera demonstrado por Bowen y Hep- 
pell (1966), Ledidae H. Adams y A. Adams, 
1858, tiene 10 meses de prioridad sobre Nu- 
culanidae, el nombre aceptado generalmente 
para esta familia ha sido Nuculanidae. lo que 
valida su conservación bajo los términos de 
Artículo 40(a) del Código Internacional de 
Nomenclatura Zoológica. 

Subfamilia Nuculaninae H. Adams 
y A. Adams, 1858 

Diagnosis 

Concha alargada, dorsoventralmente an- 
gosta, generalmente fuerte; escultura concén- 
trica bien definida; rostro formado por exten- 
sión del margen posterodorsal cóncavo; umbo 
anterior; margen posteroventral cuando es 
sinuoso no es profundo; lumen de los sifones 
generalmente entero; intestino generalmente 
con una vuelta simple a la derecha del cuerpo. 

Género Nuculana Link, 1807 

Nuculana Link, 1807; 155. Especie tipo por 
monotipia; Arca rostrata Bruguiére, 1789, ex 
Chemnitz MS; = Arca pernula Müller, 1779. 

Leda Schumacher, 1 81 7; 55, 1 72, 1 73, lám. 
19, fig. 4. 551. Especie tipo por monotipia: 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



137 



Arca rostrata Bruguière, 1789, ex Chemnitz 
MS, ^ Arca pernula Müller, 1789. 

Otros sinónimos propuestos por Alien y 
Hannah (1986) son: Exocholeda Iredale, 
1939; Kamaleda Iredale, 1939; Zygonoleda 
Iredale, 1939; Eptoleda Iredale, 1939; 
Thestyieda Iredale, 1929; Scaeoleda Iredale, 
1929; Politoleda Hertlein y Strong, 1940; 
Costelloleda Hertlein y Strong, 1940; Robaia 
Habe, 1958. 

Diagnosis 

Concha con la parte posterior más o menos 
larga, a menudo arqueada y aguzada o re- 
dondeada; parte anterior más corta, elevada 
y redondeada; por lo general con orna- 
mentación concéntrica. Apices pequeños 
opistogiros. Ligamento interno; cartílago del 
ligamento corto, colocado bajo el vértice, a 
veces dirigido oblicuamente hacia atrás. Si- 
fones completamente unidos o al menos en 
parte. Seno paleal pequeño, poco profundo. 

Observaciones 

Dell (1955) aclaró la confusión que ha exis- 
tido en la literatura sobre el uso del nombre 
Nuculana con preferencia a Leda. Plantea 
que Leda Schumacher, 1817, es un nombre 
sustituto para Nucula Lamarck, 1799, y en 
consecuencia no es válido. Por otra parte, 
Nuculana Link, 1807, tiene 10 años de priori- 
dad y parece un nombre legalmente válido, 
conclusión aceptada por muchos investi- 
gadores, por ejemplo. Grant y Gale (1931), 
Prashad (1 932), Сох (1 940), Hertlein y Strong 
(1940), Fletcher (1945), Soot-Ryen (1959). 

Savitskii (1969a) analiza la problemática 
del género Nuculana y agrega detalles de las 
razones que han creado tanta confusión. 
Entre ellas señala que se estableció el género 
Leda Schumacher, 1817, con la especie tipo; 
Arca rostrata Bruguiére, 1789, ex Chemnitz 
ms, la cual Hanley (1860) presentó como un 
sinónimo de Arca pernula Müller, 1 779. Lo an- 
terior no solo demuestra phoridad, sino que 
también sinonimia. Además, Hanley (I860) al 
mismo tiempo aclaró que Arca rostrata Mon- 
tagu, 1803, era diferente de Arca rostrata 
"Chemnitz, 1784." 

Verrill y Bush (1897) al revisar los Ledidae 
y Nuculidae de la costa del Atlántico de Esta- 
dos Unidos aceptan como especie tipo para 
el género Leda a Arca rostrata "Montagu" y 



propusieron limitar el género Leda a las es- 
pecies Leda pernula (Müller); L. cuspidata 
Gould; Leda caudata Donovan, y L. tenuiscu- 
lata (Couthouy), y otras. Esto último Savitskii 
(1969) lo invalida por las notables diferencias 
entre estas especies y la citada por Verrill y 
Bush (1897). 

Savitskii (1969) propone agrupar a las Nu- 
culana en dos grupos probables de sub- 
géneros, el Grupo I, Nuculana Link, 1 807, con 
la especie tipo Arca pernula Müller, 1 779, con 
los tres subgéneros; Nuculana s.S., The- 
styieda Iredale, 1929, y Poroleda Hutton, 
1893, y el Grupo II, Leda Schumacher emend. 
Verrill y Bush, 1897 con la especie tipo Arca 
rostrata "Montagu, 1803," para seguir usando 
el nombre de Leda que ha sido empleado por 
tanto tiempo, con tres subgéneros; Saccella 
Woodring, 1925, Lembulus Risso, 1826, ex 
Leach ms, y Borissia Slodkewitch, 1938. Su 
agrupación nos permite separar muy bien a 
las especies de Nuculana y Propeleda aqui 
estudiadas. 

Especies Estudiadas; 

1 . Nuculana (Saccella) cuneata (Sowerby 
I, 1833) 

2. Nuculana (Borissia) inaequisculpta 
(Lamy, 1906) 

Además de N. (S.) cuneata descrita origi- 
nalmente para Valparaíso, y de N. (ß.) inae- 
quisculpta aparentemente restringida a la 
Península de Palmer, Antartica y archipiéla- 
gos vecinos, se han citado impropiamente 
para Chile otras dos especies recientes. Nu- 
culana (Saccella) acuta Conrad, 1832, de la 
costa atlántica estadounidense, citada tam- 
bién por Dalí (1909) para California, Golfo de 
Panamá y región al S de Valparaíso, es una 
especie diferente que no se encuentra en la 
costa oeste de las Americas (Hertlein y 
Strong, 1940) y no puede ser considerada un 
sinónimo de N. (S.) cuneata (Sow/erby), como 
Dalí concluyera. 

Nuculana {Saccella) callimene Dalí es otra 
especie descrita originalmente del Golfo de 
Panamá y mencionada también para Tomé, 
Chile. Sin embargo, como se discute más 
adelante, el registro de Tomé corresponde a 
N. (S.) cuneata. La presencia de N. callimene 
en Chile es dudosa y su validez debe ser 
confirmada, en primer lugar, por un estudio 
de su variación y anatomía, en la localidad 
tipo. 



138 



VILLARROEL & STUARDO 



Clave para las Especies de 
Nuculana Estudiadas 

1. Conclna con un rostro corto. Ornamen- 
tación formada por costillas concéntricas 
fuertes que cubren toda la concha . . . N. (S.) 

cuneata 
^'. Concha no rostrada. Ornamentación for- 
mada por costillas concéntricas débiles sólo 
en la parte central de la concha . . . N. (B.) 

inaequisculpta 

Subgénero Sacce//a Woodring, 1925 

Sacce//a Woodring, 1925: 15. Especie tipo 
por desiginación original Arca fragllis De- 
shayes, 1858, ex Chemnitz ms, = Leda com- 
mutata Philippi, 1844. Nuevo nombre para 
Ledina Sacco, 1898, (Dec.) non Ledina Dalí, 
1898 (Abril) 

Diagnosis 

Concha elongada-ovada con un angosto (o 
agudo) rostro y una más o menos marcada 
quilla posteroumbonal, típicamente con es- 
cultura de prominentes costillas marginales. 
Seno paleal más profundo que en Jupiteha. 
(Savitskii, 1969; Maxwell, 1988) 

Nuculana (S.) cuneata (Sowerby I, 1833) 
Figs. 7, 42,43, 77-79, 115-118 

Nucula cuneata Sowerby I, 1833: fig. 15 
(Feb): Sowerby I, in Broderip y Sowerby I, 
1833: 198 (13 March) (Loe. tipo: Valparaíso); 
Reeve, 1841: 111, lám 85, fig. 15: Philippi, 
1860: 158; Philippi, 1887: 190, lám. 41, fig. 4. 

Leda cuneata (Sowerby), d'Orbigny, 1846: 
546; Hupé, 1854: 307; Hanley, 1860; 128, 
lám. 228, figs. 92, 93; Sowerby II, 1871, 
Laeda lám. 6, fig. 35a, b. 

Nuculana cuneata Sowerby, Hertlein y 
Strong, 1 940; 403, lám. 1 , fig. 20; Soot-Ryen, 
1959: 14. 

Leda {Jupiteha) callimene Dalí, 1 908a: 372, 
lám. 1 7, figs. 3, 4 (ex parte Tomé, Chile, en 1 4 
brazas). 

Leda callimene, Dalí, 1909: 250 (ex parte); 
Zetek, 1918:37. 

Nuculana callimene (Dalí), Carcelles y 
Williamson, 1 951 ; 324 (ex parte). 

Nuculana (Saccella) callimene Dalí, 
Hertlein y Strong, 1940; 393, lám. 1, fig. 13 
(ex parte); Keen, 1958; 18, fig. 8; Olsson, 
1961; 64, lám. 1, figs. 7a, b (ex parte); Keen, 
1 971 ; 29, fig. 21 ; Bernard, 1 983; 1 2. 



Nuculana (Saccella) cuneata Sowerby, 
Ramohno, 1968: 189, lám. 1,figs. 3, 8, lám. 4, 
fig. 3 (ex parte); Bernard, 1983; 12. 

Material Estudiado 

241 ejemplares (ej) y 5833 valvas (v); 
MZUC. Procedencia; (1 ) 48 ej, 92 ej s, 571 9 v, 
4-11 mm (No. 4562), M. Ch. I, Est. 1, Punta 
Tortuga, Coquimbo (29°57'24"S; 71°4'22"W); 
fango, conchilla, 82 m. (2) 83 ej s, 6-11 mm 
(No. 4680), M. Ch. I, Est. 2, Punta Tortuga, Co- 
quimbo (29^57'24"S; 71 24'48"W); fango, 
conchilla, roca, 122 m. (3) 4 v, 2-8 mm (No. 
4589), M. Ch. I, Est. 19, zona Norte (31° 
51'54"S; 71°42'42"W); fango, 169 m. (4) 2 v, 
4-6 mm (No. 4592), M. Ch. I, Est. 20, zona 
Norte (31°51'30"S; 71"35'W); conchilla, 200 
m. (5) 22 V, 3-9 mm (No. 4584), M. Ch. I, Est. 
37, Valparaiso (33'06'S; 71 47'W); fango, 135 
m. (6) 1 ej s, 7 mm (No. 4572), M. Ch. I, Est. 
74, frente a Punta Talca (33' 25'S; 71 '43'W); 
fango, 52 m. (7) 7 ej, 4 v d, 4-7 mm (No. 4734), 
Bahía de Valparaíso (33 S). (8) 3 ej s, 4-8 mm 
(No. 4678), M. Ch. I, Est. 39, Chile central 
(34°8'24"S; 72''2'30"W); fango, arena, 90 m. 
(9) V i, 3-4 mm (No. 4587), M. Ch. I, Est. 40, 
Chile central (34°6'48"S; 72°30'W); arena, 28 
m. (1 0) 7 ej, 5-9 mm (No. 4591 ), M. Ch. I, Est. 
41, Chile central (34 56'S; 72 9'W); arena, 
fango, trozos de roca, 1 60 m. (1 1 ) Restos de v 
(No. 4574), IFOP 01, Est. 61, frente a Ca- 
rranza (35'38'S; 72 39'W); conchilla, 107 m. 
(12) 3 v d, 4 V i, 5-8 mm (No. 4585), M. Ch. I, 
Est. 64, frente a Bahía Concepción (36'32'S; 
73 21 'W); fango, 125 m. (13)4vi, 5vd, 5-8 
mm (No. 4573), IFOP 01, Est. 73, frente a 
Dichato (Punta Носа y Tumbes) (36'32'S; 
72 57'W); 76 m. (14) 47 v, 3-8 mm (Nos. 
4687, 4689, 4696, 4706, 4708, 4710, 4712, 
471 4, 4726, 4729), draga van Veen, Bahía de 
Concepción; fango, 16-23 m. (15) 7 ej, 12 v, 
3-6 mm (Nos. 4557, 4559, 4560), Golfo de 
Arauco (37 13'S; 73 1 9'W): tango arenoso, 
60-65 m. (1 6) Restos de v (No. 4679), M. Ch. 
I, Est. 77, zona Sur (38 1 6'S; 73 '41 'W); tango, 
arena fina, 120-160 m. (17) 4 v, 4-6 mm (No. 
4558), M. Ch. I, Est. 108, al S de Mehuin, Val- 
divia (40 54'S; 73 56'W); fango, 1 36 m. (1 8) 1 
V, 5 mm (No. 4571 ), IFOP 01 , Est. 31 frente a 
Islas Juan Fernández (33 ■35'S; 78 31 '1 2"W); 
arena, 220-280 m. 

Descripción 

Concha: Concha de regular tamaño (hasta 
11.5 mm de longitud), subtriangular, gruesa. 



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139 



blanca. Perióstraco blanco, ocre o amari- 
llento. Umbos inflados con los ápices adya- 
centes, débilmente opistogiros. Márgenes re- 
dondeados. Parte posterior poco alargada, 
suavemente cóncava; extremo curvado. Or- 
namentación formada por numerosas costi- 
llas concéntricas, separadas por surcos sub- 
iguales, más densas en la base; cubren toda 
la concha, excepto en un angosto espacio 
cercano a la carena radial dorso-posterior, 
donde son casi obsoletas. Con un surco débil 
que se extiende desde los umbos hasta la 
base del margen anterior. No hay lúnula ni es- 
cutelo, pero la carena radial marcada y el 
área dorsal posterior plana forman un pseu- 
doescutelo con finas costillas longitudinales. 
Interior de las valvas blanco arcilloso. Char- 
nela acodada con dientes fuertes, sólidos; la 
serie posterior con 2 ó 3 dientes menos que la 
anterior y separada de ella por un condróforo 
triangular, profundo, ubicado directamente 
bajo los ápices. Línea paleal bien marcada, 
seno paleal poco profundo, aguzado hacia 
atrás. Impresiones de los aductores pe- 
queñas, bien marcadas y distintas; la anterior 
de doble tamaño que la posterior. Impre- 
siones de los músculos medios, adyacentes, 
bein marcadas, ubicadas bajo y ligeramente 
anterior al condróforo. 

Anatomía Interna: Manto uniforme con un no- 
table repliegue en todo su borde libre. Pie 
posteriormente muy geniculado. Glándula 
hipobranquial grande. Palpos labiales tan lar- 
gos como los ctenidios con pliegues anchos y 
con su extremo posterior alargado en un fila- 
mento. Tentáculo del palpo relativamente pe- 
queño; su inserción es muy anterior a la 
lámela del palpo. Ctenidios con filamentos 
gruesos y triangulares. Cavidad pericárdica 
bastante grande; origen de la aorta posterior 
junto a la unión del ventrículo con la aurícula. 
Estómago con sólo un área de selección (as). 
Riñon grande, poco lobulado. Sifones unidos 
en parte; inhalante incompleto. 

Observaciones 

Después de haber observado más de 1000 
valvas de una de las muestras procedentes 
de Coquimbo, y de compararlas con las de 
otras localidades chilenas, se llega a la con- 
clusión de que en Chile existe una sola es- 
pecie de Nuculana que corresponde a N. (S.) 
cuneata. En la mayoría de las muestras se 
observan dos extremos de variación: uno co- 
rresponde a ejemplares con la concha pro- 



porcionalmente más alta y el umbo más in- 
flado y el otro a conchas proporcionalmente 
más bajas con umbos menos inflados. La 
comparación de varias series de conchas de 
distintas localidades, demostró una grada- 
ción de forma que une a ambos extremos. 
Además, al hacer mediciones de una sub- 
muestra obtenida por cuarteo desde la mues- 
tra mayor que contiene alrededor de 6000 
ejemplares (Punta Tortuga, Coquimbo; fango 
conchífero, 82 m), se constató que todos, sin 
excepción, presentaban: (1) la misma dis- 
posición de las costillas concéntricas, las que 
se hacen más densas a medida que se acer- 
can al margen ventral; (2) una carena dorsal 
posterior que delimita un área que semeja a 
un escutelo; y (3) en la región anterior un débil 
surco que nace en el umbo y termina en el 
margen ventral. La anatomía y el interior de la 
concha no mostraron tampoco mayores dife- 
rencias. Probablemente fue este tipo de 
variación poblacional, lo que llevó a Dalí 
(1908a) a identificar a ejemplares de Tomé 
con la especie Nuculana callimene (Dalí, 
1908) del Golfo de Panamá. 

Los dos extremos de variación se muestran 
en las Figuras 117 y 118; esta última muestra 
un ejemplar que coincide con la figura y des- 
cripción de la especie de Dalí, lo que sugiere 
que fueron ejemplares de este tipo los estu- 
diados por él. Por otra parte, no hay referen- 
cias de que Dalí haya visto ejemplares de N. 
(S.) cuneata al hacer la descripción de N. ca- 
llimene o que haya considerado su existen- 
cia. A juzgar por las medidas del tipo y de 
otros ejemplares dados por Dalí (1908a) y 
OIsson (1961) el tamaño de esta especie 
(15-16 mm) parece mucho mayor que el en- 
contrado en los ejemplares más grandes de 
las muestras chilenas (11.5 mm), y en estas 
últimas son muy pocos los ejemplares que 
tienen la relación longitud-alto de N. ca- 
llimene. Es factible que se trate de dos es- 
pecies alopátricas. 

Ramorino (1968) basándose en una infor- 
mación proporcionada por el fallecido Dr. 
Joseph Rosewaterdel United States National 
Museum comenta que "Л/. (Saccella) cuneata 
es muy parecida en su aspecto general a N. 
{Saccella) callimene (Dalí, 1908), y que las 
posibles diferencias fundamentales estarían 
dadas por la cantidad de dientes charnelares 
y el radio G/A (la razón espesor/altura), 
aunque las tallas comparadas no son equiva- 
lentes." Efectivamente, el número de dientes 
anteriores y posteriores del ejemplar tipo 
(15.5 mm de longitud) es de 26 y 20, respec- 



140 



VILLARROEL & STUARDO 



tivamente, mientras que el promedio de 11 
ejemplares medidos por Ramorino con un 
tamaño (longitud) variable entre 5.96 y 9.60 
mm fue de 1 a 1 7 dientes anteriores y 8 a 1 5 
dientes posteriores. Ejemplares de Coquimbo 
de 11 mm de longitud presentaron un máximo 
de 18 dientes anteriores y 16 dientes pos- 
teriores, lo que corrobora y confirma que en 
ésta como en otras especies el número de 
dientes varía con la talla. 

Es notable, sin embargo, que en la vista in- 
terior de un ejemplar del USNM de 15.5 mm 
(¿el Holotipo?) del Golfo de Panamá dada por 
OIsson (1 961 : lám. 1 , fig. 7a) se cuentan sólo 
17 dientes en la serie anterior y 19 (¿20?) en 
la serie posterior. 

Distribución Geográfica 

Desde Mejillones (23'S) hasta el S de Val- 
divia (40-54'S) y alrededor de las Islas Juan 
Fernández (33 35'S). 

Habitat 



Subgénero ßonss/a Slodkewitsch, 1938. 

Borissia Slodkewitsch, 1938: 78, 86. Es- 
pecie tipo por designation original: Nuculana 
(Borissia) alferovi Slodkewitsch, 1938. Mio- 
ceno de Tyushev del Este de Kamchatka; 
Kafanov y Savitskii, 1995: 87. 

La posición taxonómica de Borissia fue dis- 
cutida ampliamente por Savitskii (1978, fide 
Kafanov y Savitskii, 1995). 



Diagnosis 

Concha oblonga-ovada, marcadamente 
convexa: casi subequilateral. Margen poste- 
rior de la valva más amplio que el anterior. 
Umbos protruidos. Escultura externa en la 
forma de costillas amplias, bajas y con- 
torneadas. Costillas dispuestas a través de 
toda la superficie, excepto el área posterior o 
limitadas a un triángulo umbonal. Líneas de 
crecimiento transversas en áreas separadas 
(Kafanov y Savitskii. 1995). 



Las muestras estudiadas cubren toda el 
área de dispersión conocida. Se encontraron 
en profundidades entre 28 y 200 m, en subs- 
trato de fango arenoso y frente a las Islas 
Juan Fernández entre 220 y 280 m de pro- 
fundidad, en arena. 

Esta especie presenta su mayor abundan- 
cia entre Coquimbo y Valparaíso, dismi- 
nuyendo hacia el S donde llega a ser más o 
menos rara. En N. (S.) cuneataal igual que N. 
(N.) pisum. y M. chilensis, se encontraron 
diferencias de densidad al comparar los datos 
obtenidos por Ramorino (1968) en la Bahía 
de Valparaíso, con los logrados en la Bahía 
de Concepción. En esta última se obtuvo una 
densidad de 10 ejemplares/m^ (promedio de 
10 muestras) en sustrato de fango entre 16 y 
23 m, valor levemente inferior al obtenido por 
Ramorino (1968) entre 20 y 50 m de profun- 
didad, en la Bahía de Valparaíso, igual a 15 
ejemplares/m^ en fondo de fango. 

Por otra parte, los datos de este autor indi- 
can una mayor densidad en fango arenoso 
entre 1 21 y 200 m, en cambio en las muestras 
de las localidades que aquí se estudiaron, se 
encontró la mayor densidad entre 82 y 122 m 
en fango y fango conchífero. 

Con anterioridad, N. (S.) cunéala había 
sido citada en fondo de arena gruesa y grava 
entre 14 y 45 brazas (Sowerby I, in Broderip y 
Sowerby I, 1833). 



Nuculana {B.) Inaequisculpta (Lamy, 1906) 
Figs. 37, 38, 90, 121. 122 

Yoldia inaequisculpta Lamy, 1906: 125, fig. 
3 (Localidad tipo: Oreadas del Sur.): Lamy, 
1910: 314: Lamy, 1911: 29, lám. 1, fig. 23; 
Carcelles, 1953: 209, lám. 5, fig. 99. 

Nuculana {sub gen.?) inaequisculpta 
(Lamy), Soot-Ryen, 1951:6. 

Nuculana (s. I.) inaequisculpta (Lamy), 
Powell, 1960: 170; Dell, 1964: 144. 

¿Malletia Sabrina Иеа\еу?, Nicol, 1966: 17, 
lám. 1 . figs. 3, 5, non Malletia Sabrina Hedley, 
1916. 

Nuculana Inaequisculpta (Lamy), Egorova, 
1991:44, fig. 2. 

Material Estudiado 

14 ejemplares (ej) y 1 valva (v). MZUC. 
Procedencia: (1) 1 ej, 3 mm (No. 4556), Ant. 
XXII, Estrecho de Bransfield (62'58'6"S; 
60 40'6"W); fango arenoso, 60 m. (2) 1 ej s, 2 
mm (No. 4540), Ant. XXII, Est. 17, E. de 
Bransfield (62 58'6"S; 6040'6"W); fango 
arenoso, 93 m. (3) 1 v erosionada (No. 4520), 
Ant. XIX, Bahía Foster, Isla Decepción 
(62 59'24"S; 60 34'W), 160 m. (4) 1 ej, 5 mm 
(No. 451 7), Ant. XXII, Est. 50, E. de Bransfield 
(62 28'36"S; 59 40'30"W); fango, 123 m. (5) 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



141 



4 ej, 5.9-12.5 mm (No. 4529). Ant. XXII, Est. 
19, E. de Bransfield (62°29'24"S; 
59°39'24"W); fango, 70 m. (6) 1 ej, 12 mm 
(No. 4537), Ant. XXII, Est. 35, E. de Bransfield 
(62 29'S; 5942'36"W); arena y fango, 48 m. 
(7) 2 ej, 5-10.1 mm (No. 4510), Ant. XIX, E. 
de Bransfield (63 12'S; 58 35'W); 135-150 
m. (8) 4 ej, 8.5-9 mm (No. 4518), Ant. XIX, 
Bahía Margarita, frente Islas Jenny y Adelaida 
(67°50'S; 68"45'S); 150 m. 

Descripción 

Concha: Concha de regular tamaño (hasta 
12.5 mm de longitud), oval truncada, semi- 
rectangular, no rostrada; delgada y frágil, 
blanca. Bordes redondeados, excepto el pos- 
terior que es levemente truncado y oblicuo. 
Perióstraco de color variable, blanco a ama- 
rillo verdoso o pardo claro. Umbos poco 
prominentes, ligeramente anteriores; ápices 
rectos. Ornamentación de la concha formada 
por finas costillas concéntricas, poco ele- 
vadas, que dejan espacios subiguales entre 
ellas; bien marcadas en la región central de la 
concha; casi imperceptibles hacia los ex- 
tremos anterior y posterior. Área comprendida 
entre la línea que une los ápices cpn la base 
del extremo posterior aplanada. Áreas dor- 
sales anterior y posterior elevadas, surcadas 
finamente por la continuación de las costillas 
concéntricas que se dirigen hacia los ápices. 
Resilium cordado, casi completamente in- 
terno; sólo una parte muy pequeña se ubica 
externamente por delante y detrás de los 
ápices. Interior de las valvas blanco brillante. 
Línea paleal visible, con un seno paleal pe- 
queño, no mayor que la impresión del aductor 
posterior. Charnela acodada, dientes fuertes 
de base ancha, de mayor tamaño en el centro 
de cada serie anterior y posterior, muy suave- 
mente curvados hacia arriba: serie anterior 
con 2 ó 3 dientes más que la posterior. Im- 
presiones de los aductores de la concha de- 
siguales; anterior más marcada y de doble 
tamaño que la posterior. 

Anatomía Interna: Manto con un repliegue 
fuerte, cercano al borde ventral, que se en- 
gruesa a medida que se acerca al extremo 
posterior, donde sufre uno o más repliegues 
sobre sí mismo. Pie casi recto, muy poco 
geniculado; disco pedal con crenulaciones 
poco notorias. Glándula hipobranquial au- 
sente. Palpos labiales de regular tamaño, muy 
surcados; tentáculos más o menos del mismo 



tamaño que el palpo. Un par de repliegues 
hipertrofiados en la base del tentáculo. Cteni- 
dios apegados al techo de la cavidad del 
manto, de filamentos gruesos. Cavidad peri- 
cárdica pequeña; corazón de aurículas y ven- 
trículos tubulosos, éste último atravesado por 
el recto. Estómago con saco del estilo corto. 
Sifones bien desarrollados, pero pequeños; 
sólo el exhalante es cerrado, el inhalante está 
formado únicamente por repliegues del manto 
que se unen débilmente. 

Observaciones 

Dell (1964) ha hecho notar que en N. (S.) 
inaequisculpta la concha "tiene algo de Ma- 
lletiidae, aunque la charnela esté interrum- 
pida por un condróforo bien desarrollado y la 
escultura sea más bien de un Nuculanidae." 

Las variaciones de la forma de la concha 
fueron dibujadas por Egorova (1991). 

El estudio anatómico de esta especie, es- 
pecialmente en lo que se refiere a la posición 
del corazón con respecto al recto, la forma y 
posición de los sifones, y la disposición ge- 
neral de los órganos en la cavidad del manto, 
permiten incluirla sin lugar a dudas en los Nu- 
culanidae. 

El par de repliegues hipertrofiados obser- 
vados en la base del tentáculo del palpo de 
esta especie (Fig. 90) podría corresponder en 
función con "la pequeña extensión (flap) de la 
lámela interna del palpo que rodea a la base 
del apéndice" representada por Yonge (1939; 
fig. 35, po) en Nuculana minuta, Yoldlella lu- 
cida, y Malletia obtusata. 

Distribución Geográfica 

Oreadas del Sur, Shetland del Sur, Georgia 
del Sur, Archipiélagos de Palmer y Estrecho 
de Bransfield, Bahía Rybiy Khvost, Océano 
Indico (Antartica). 

Habitat 

Nuculana (S.) inaequisculpta es una es- 
pecie antartica muy poco abundante. En las 
muestras estudiadas, fue encontrada desde 
el Estrecho de Bransfield (62-S) hasta Bahía 
Margarita, frente a las Islas Jenny y Adelaida 
(67'S), en profundidades de 48 a 160 m con 
substrato de fango y fango arenoso. Presentó 
su mayor densidad y tamaño en substrato de 
fango a 70 m de profundidad. Egorova (1 991 ) 
la encontró entre 20 y 150 metros. 



142 



VILLARROEL & STUARDO 



Con anterioridad esta especie fue encon- 
trada a profundidades mayores a las aquí ex- 
puestas. Dell (1 964) la cita de las Oreadas del 
Sur entre 244 y 344 m y en el Archipiélago de 
Palmer entre 160 y 335 m de profundidad. 

Género Propeleda Iredale. 1924 

Propeíeda Iredale, 1924: 181. Especie tipo 
por designación original: Leda ensicula 
Angas, 1877. Reciente de Australia: figurada 
por Hedley (1914: lám. 78, figs. 15, 16). 

Diagnosis 

Concha con un rostro largo y truncado: 
condróforo. oblicuo y angosto, dirigido hacia 
atrás: dientes de la charnela casi paralelos al 
borde. 



Propeleda longicaudataJb\e\e, 1912 
(Figs. 33-36, 74-76, 113, 114). 

Propeleda longicaudataJh\e\e, 1912: 229, 
lám. 17, fig. 22 (Loe. tipo: Estación de Gauss, 
Mar de Davis, Antartica.): Iredale. 1924: 186: 
Powell, 1951: 77; Powell, 1960: 170; Dell, 
1964: 146: Nicol, 1966: 13, lám. 2, figs. 2, 4. 

Poroleda longicaudata (Thiele), Hedley, 
1916: 18. 

Nuculana (Poroleda) longicaudata (Hed- 
ley), Soot-Ryen, 1951:5. 

Propeleda longicaudata (Thiele, 1912), 
Linse, 1997: 46. 

Material Estudiado 

35 ejemplares (ej) y 41 valvas (v); MZUC. 
Procedencia: (1) 1 ej, 18.2 mm (No. 4506). 
Ant. XIX, Bahía Margarita entre Islas Jenny y 
Adelaida (67 50'S: 68 45'W): cantos 
grandes, 150 m. (2) 1 ej, 1.2 mm (No. 4507). 
Ant. XXII, Est. 28, Isla Greenwich, Shetland 
del Sur (62"28'42"S; 59 38'30"W): fango 
arenoso, 93 m. (3) 14 ej, 9-18 mm (Nos. 
4502, 4508, 4511, 4514), Ant. XIX, E. de 
Bransfield (63"12'S: 58"35'W); arena y 
piedrecillas, 135-150 m. (4) 8 ej, 41 v, 7-13 
mm (Nos. 4610, 4627, 4642), "Hero" 69-5, 
Est. 201 (9), Confluencia Canales Concep- 
ción y Trinidad (50-9'55"S; 74 43'25"W); 
fango, 390-460 m. (5) 11 ej, 10-13.5 mm 
(Nos. 4646, 4652), "Hero" 69-5, Est. 56, 
Puerto Bueno, Canal Sarmiento (51 0'50"S: 
7414'10"W): fango, 215-220 m. 



Descripción 

Concha: Concha de regular tamaño (hasta 
18.85 mm de longitud), sólida, muy compri- 
mida, muy inequilateral; alargada posterior- 
mente, con un rostro curvado hacia arriba; 
opaca, blanca. Perióstraco delgado, amarillo 
verdoso a pardo claro. Umbos inconspicuos 
con ápices opistogiros ubicados en el tercio 
anterior. Márgenes convexos (redondeados), 
excepto el dorsal posterior que es cóncavo y 
se eleva gradualmente a medida que se 
aproxima al margen posterior. Ornamen- 
tación formada por dos fuertes carenas (qui- 
llas) que nacen en el ápice y corren hasta 
el borde posterior, separándose paulatina- 
mente: hay, además, costillas concéntricas 
muy densas sobre los umbos que disminuyen 
a medida que se aproximan al margen ventral 
y cambian su dirección abruptamente sobre 
las quillas dirigiéndose hacia arriba; con 1 a 5 
cóstulas complementarias sobre las quillas. 
Lúnula alargada, con numerosas estrías muy 
finas, continuación de las concéntricas, que 
se dirigen oblicuamente hacia el ápice. Inte- 
rior de las valvas blanco con brillo aporce- 
lanado; con una carena posterior. Charnela 
acodada con dientes laminares alargados 
muy numerosos; los postenores duplican en 
número a los anteriores. Base de los dientes 
proximales, de lados muy desiguales, for- 
mando prolongaciones laminares muy acen- 
tuadas. Resilium parcialmente externo y divi- 
dido, con la parte anterior de mayor tamaño 
que la posterior. Línea paleal poco visible; 
seno paleal del mismo tamaño que la impre- 
sión del aductor posterior. Impresiones de los 
aductores muy desiguales: la anterior re- 
dondeada, algo alargada verticalmente, la 
posterior de forma oval ubicada en la mitad 
de la parte posterior. 

Anatomía Interna: Parte ventral del extremo 
posterior del manto reflejado hacia el interior; 
con 6-8 pequeños lóbulos. Pie grande. Glán- 
dula hipobranquial pequeña. Palpos labiales 
de tamaño regular, con un fuerte tentáculo. 
Ctenidios muy alargados de filamentos pro- 
longados y gruesos. Ventrículo y aurículas 
alargadas, el primero atravesado por el recto. 
Estómago grande, con repliegues adicionales 
al área de selección mayor, pero separados 
de ésta (se asemejan a los de Tindaria virens. 
en la que son la continuación de los pliegues 
del área mayor); ciego dorsal muy surcado. 
Sifones incompletos, comunicados, formados 



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143 



por un repliegue interno, posterior, que se 
abre ventralmente; en la parte interna del re- 
borde posterior del manto hay dos proyec- 
ciones laterales en la base de los sifones. 

Observaciones 

El material estudiado permite corroborar la 
afirmación de Hedley (1916) y Powell (1951), 
de que los ejemplares de mayor tamaño de P. 
longicaudata tienden a ser proporcionalmente 
más angostos que los de menor tamaño; 
asimismo, el rostro tiende a alargarse despro- 
porcionadamente al resto de la concha. 

Las características anatómicas de esta es- 
pecie no son muy diferentes a las observadas 
en las especies del género Nuculana. De 
hecho. P. longicaudata presenta solamente el 
cuerpo más alargado. 



piares viejos ampliamente aplastado, margen 
posteroventral puede ser sinuoso; placa de la 
charnela bien desarrollada; ligamento interno 
y/o externo: intestino posterior con diversas 
configuraciones; músculos aductores, aproxi- 
madamente ¡guales en tamaño; sifones ge- 
neralmente combinados para formar un 
lumen común; palpos por lo general con rela- 
tivamente pocos pliegues (<30) (Alien y 
Sanders, 1982). 

Género r/ndar/ops/s Verrill y Bush, 1897 

Tindariopsis Verrill y Bush, 1897: 59. Es- 
pecie tipo por designación original: Malletia 
{Tindaria) agathida Dalí, 1889. St. Kitts, en 
687 brazas (1236.6 m) y al E de Tobago, In- 
dias occidentales, en 880 brazas (1584 m). 



Distribución Geográfica 

Mar de Bellinghausen, Mar de Davis, Tierra 
Adelaida, Mar de Ross, Archipiélago de 
Palmer, Oreadas del Sur, Shetland del Sur, 
Georgia del Sur, Costa Knox, Tierra Princesa 
Elizabeth (Thiele, 1912: Hedley, 1916; Soot- 
Ryen, 1951; Powell, 1951; Dell, 1964). Estre- 
cho de Bransfield y Estrecho de Magallanes. 
Especie probablemente circumantártica. 

Habitat 

Las muestras estudiadas cubren sólo en 
parte el área de dispersión de la especie. En 
las muestras procedentes del Archipiélago de 
Palmer, se halló esta especie en profundi- 
dades de 93 a 150 m, en substrato de fango 
arenoso, arena y "piedrecillas." En el Estre- 
cho de Magallanes fue encontrada viviendo 
en profundidades de 215 a 460 m en fango. 

Con anterioridad P. longicaudata había sido 
encontrada en profundidades mayores entre 
487 y 51 2 m (Powell, 1 951 ), entre 1 00 y 1 080 
m (Dell, 1964), y entre 64 y 1180 m (Linse, 
1997). 

Subfamilia Ledellinae Alien y Sanders, 1982 

Concha robusta, moderadamente inflada, 
veneriforme u ovalada, con o sin rostro, es- 
cultura concéntrica generalmente presente, 
ocasionalmente con estrias radiales; umbo 
aproximadamente central; margen dorsal 
posterior convexo, margen ventral en ejem- 



Diagnosis 

Concha con un rostro corto, definido por un 
lomo y un surco radial. Surco ligamental ex- 
terno, posterior a los ápices, bien marcado. 
Hay una pequeña ranura bajo el ápice para 
una parte especializada del ligamento, que in- 
terrumpe la charnela. 



Observaciones 

Tindariopsis fue propuesto originalmente 
como un subgénero de Tindaria Bellardi, 
1875, de la familia Malletiidae, sin que se 
conocieran sus características anatómicas. 
Verrill y Bush (1897) señalaron que "si tiene 
sifón y seno paleal podría formar un género 
distinto y ser referido a Malletinae." El estudio 
anatómico de la especie Tindariopsis sulcu- 
lata (Gould, 1852), referida a este género, 
demostró que caracteres tales como el 
corazón atravesado por el recto y la presen- 
cia de seno paleal y sifones no completa- 
mente unidos, permitirían incluir a Tindariop- 
sis tanto en la familia Nuculanidae como 
Malletiidae. Sin embargo, la inserción del li- 
gamento parcialmente externo y un rostro for- 
mado por proyección del margen posterior de 
la concha, llevó a Alien y Sanders (1982) y 
Alien y Hannah (1986) a proponer reunir los 
géneros Ledella y Tindanopsis en la subfa- 
milia Ledellinae, separándolos de otros Nu- 
culánidos. 

Entre los caracteres anatómicos estudia- 
dos en las especies incluidas en este trabajo. 



144 



VILLARROEL & STUARDO 



un rasgo interno que caracteriza a Tlndariop- 
sis es la presencia de un corazón atravesado 
por el recto. 

Tindariopsis sulculata 
(Gould, 1852, ex Couthouy MS) 
(Figs. 39-41, 80-82, 157-159) 

Nucula sulculata "Couthouy," Gould, 1852: 
424; Atlas, 1860, lám. 37, fig. 539a-e (Loe. 
tipo: Bahía Orange, Patagonia.): Johnson, 
1964: 155. 

Leda lugubris A. Adams, 1856: 49 (Loe. 
tipo: ?): Smith, 1881: 39: Mabille y Roche- 
brune, 1889: H113. 

Leda su/cü/afa ("Couthouy"), Hanley, 1860: 
129; Mabille y Rochebrune, 1889: H1 13; 
Stempeil, 1 897: 1 7-28; Stempell, 1 898a: 343, 
lám. 22. figs. 1, 5-8, 10, 11, lám. 23, figs. 19. 
21 , lám. 24, figs. 23-26. 28-31 , lám. 25, figs. 
33-38,40,41,43 (Anat.). 

Leda orangica Mabille y Rochebrune. 1 889: 
H1 13, lám. 8, fig. 3 (Loe. tipo: Bahía Orange). 

Tindaria [Tindariopsis) sulculata ("Cou- 
thouy"), Dalí, 1908a: 390; Hertlein y Strong, 
1940: 425; Soot-Ryen. 1959: 16; Powell, 
1960: 171. 

Tindaria sulculata {''Couibouy"), Dalí, 1909: 
251. 

Tindariopsis ? su/cü/aía ("Couthouy"), Dell, 
1964: 149. 

Material Estudiado 

23 ejemplares (ej) y 76 valvas (v); MZUC. 
Procedencia: (1) 1 ej s., 8 mm (No. 4588), M. 
Ch. I, Est. 51, Chile central (34 56'S; 
72°14'W);fangoyarena, 50m.(2) 1 ejs., 10.8 
mm, 1 V d., 4.8 mm (No. 4664), M. Ch. I, Est. 
76, Chile austral (38^1 6'S; 73 39'W): fango y 
arena fina, 66 m. (3) 8 ej s., 4-10 mm (No. 
4586), M. Ch. I, Est. 91 , Chile austral (39 03'S: 
73"39'W); arena fina compacta, 71 m. (4) 1 v 
i, 6 v d., 4-11 mm (No. 4561), M. Ch. I, Est. 
(117) X-1, Golfo de Corcovado (42'55'S; 
72''55'W); arena, fango y "piedras". 1 90 m. (5) 
2 V i, 3 v d., 5-8 mm (No. 4623), "Hero" 69-5, 
Est. 206, draga Petersen О, 1 m^, Caleta Hen- 
derson (50 16'42"S; 74 48'28"W); fango con 
grava fina, 30 m. (6) 7 ej, 8-1 3 mm, 3 v d, 2 v 
i, 11-13 mm (No. 4640), "Hero" 69-5, Est. 58, 
Puerto Bueno (50"59'S; 74 13'W); fango con 
carbón, vidrios quebrados y escorias, parece 
algo negruzco, 18 m. (7) 25 v d, 7.5-13 mm, 
21 V i, 11-13 mm (No. 4624), "Hero" 69-5, 
Bahía Isthmus, Península Zach (52 10'S; 



73 37'W): fango, 32-40 m. (8) 5 ej, 4.5-13 
mm, 1 V d, 1 1 mm (Nos. 4607 y 4631 ), "Hero" 
69-5, E. de Magallanes, frente a Punta Arenas 
(53"1 7'S-53 1 8'40"S; 70 48'36"W-70°42' 
20"W); fango, 180-210 m. (9) 1 v d, 10 mm 
(No. 4644), "Hero 69-5, Est. 227, E. de Maga- 
llanes (53"14'42"S-53 14'54"S; 70 53' 
1 2"W-70°53.30"W); fango, 1 05 m. (1 0) 1 ej s, 
1 0.8 mm, 1 v, 4.8 mm (No. 4649), "Hero" 69-5, 
Est. 48, E. de Magallanes, Bahía Fortescue 
(53 41'40"S; 72 0'45"W); grava con muchas 
algas rojas, 18 m. 



Descripción 

Concha: Concha de tamaño mediano (hasta 
13.3 mm de longitud), triangular, alargada 
posteriormente, inflada, muy gruesa, blanca. 
Perióstraco delgado, pardo claro amarillento 
a casi negro. Umbos pequeños, ligeramente 
antenores, con ápices levemente prosogiros. 
Margen posterior y dorsal anterior oblicuos, 
casi rectos: márgenes anterior y ventral re- 
dondeados; dorsal posterior ligeramente cón- 
cavo, elevado en su extremo y generalmente 
aguzado. Ornamentación formada por costi- 
llas concéntricas (3-4 por mm) sobrepuestas 
unas a otras y muy poco curvadas; no llegan 
a los márgenes anterior ni posterior. Líneas 
de crecimiento más notorias en las regiones 
anterior y posterior, formando surcos que in- 
terrumpen a las concéntricas. Pequeña lúnula 
y escutelo delimitados por un leve surco que 
señala el término de las costillas concéntri- 
cas; con líneas de crecimiento muy finas. In- 
terior de las valvas blanco, aporcelanado; con 
un área solevantada por un espesamiento de- 
trás de la impresión del aductor anterior. 
Charnela acodada; dientes numerosos, hasta 
14 anteriores y 19 posteriores, ligeramente 
curvados hacia arriba. Línea paleal bien mar- 
cada; seno paleal casi cuadrangular, no 
mayor que la impresión del aductor posterior; 
notorio por un engrosamiento de la concha. 
Impresiones de los aductores desiguales; an- 
terior redonda; posterior ovalada. Hay tam- 
bién una impresión lineal única, oblicua, que 
sale por debajo de la ranura ligamentaria y 
llega hasta la cercanía de la impresión del 
aductor anterior. 

Anatomía Interna: Bordes del manto lisos. No 
hay glándula hipobranquial. Palpos labiales 
muy grandes con tentáculo pequeño. Cteni- 
dios muy pequeños. Corazón de ventrículo y 



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145 



aurículas globosos, atravesado por el recto. 
Estómago con un área de selección (as) sim- 
ple, cuyos repliegues sufren sólo una leve 
flexión; sin área de selección complemen- 
taria. Sifones pequeños, completamente 
unidos, pero abiertos ventralmente. 

Observaciones 

La ornamentado de la concha de T. sulcu- 
lata es muy similar a la de la especie fósil T. 
elegans, que se trata posteriormente. Difiere 
de ella por la menor longitud y por la trun- 
cación de su extremo posterior. 

Distribución Geográfica 

Desde 34^S (Chile Central) hasta 35 41'S 
(E. de Magallanes), Islas Falkland y Río de la 
Plata, Argentina. 

Habitat 

Las muestras estudiadas de esta especie 
cubren toda el área de dispersión de la costa 
del Pacífico. Se encontró en profundidades 
de 18 a 210 m en substrato de fango, fango 
arenoso, fango con escoria, arena fina y en 
grava con algas rojas. 

Con anterioridad, T. sulculata había sido 
encontrada entre 13 y 300 m en fondo de 
arena gruesa con algo de fango (Soot-Ryen, 
1959). 

Familia Siliculidae Alien y Sanders, 1973 

Concha alargada, extremadamente com- 
primida, entreabierta, sin escutelo; umbo pe- 
queño, difícilmente visible a nivel del margen 
dorsal; placa de la charnela débil, dientes 
alargados, laminares; ligamento opistodético, 
interno, oblicuo; con sifones, el margen ven- 
tral del sifón inhalante formado por adhesión 
y no por fusión; láminas branquiales externas 
de la mitad del tamaño de las internas; boca 
ubicada muy posterior al músculo aductor; 
única vuelta del intestino posterior al lado 
derecho, o a la derecha e izquierda del 
cuerpo (Alien y Sanders, 1973). 

Género S/7/cu/a Jeffreys, 1879 

S/7/ca/a Jeffreys, 1879: 574, lám. 45, fig. 6, 
6a. Especie tipo por monotopia: Silicula fra- 
g/7/s Jeffreys, 1879. 



Diagnosis 

Concha frágil, lisa, comprimida; muy in- 
equilateral, soleniforme, truncada atrás y re- 
dondeada adelante; umbo en el tercio ante- 
rior, pequeño, obtuso. Condróforo oblicuo, 
dirigido posteriormente. Resilium casi total- 
mente interno, la parte externa obsoleta. 
Línea de la charnela casi recta; dientes lame- 
lares, transversales; serie posterior más 
alargada; con menor número de dientes que 
la anterior. Seno paleal de profundidad varia- 
ble. 

Especies estudiadas: 

1. Silicula patagónica DaW. 1908 

2. Silicula rouchi Lamy, 1 91 

Además de la especie S. patagónica arriba 
señalada, Carcelles y Williamson (1951) han 
incluido también a S. fragilis Jeffreys, 1879, 
del Hemisferio Norte, en una lista de la fauna 
malacológica de las regiones Magallánica y 
Patagónica. La presencia de esta especie en 
el Hemisferio Sur es improbable. 

Con objeto de completar el conocimiento 
de los caracteres anatómicos del género se 
incluye en esta revisión el estudio de la es- 
pecie antartica S. rouchi Lamy, 1910. 

Clave Para Las Especies 
De Silicula Estudiadas 

1. Concha con el extremo posterior re- 
dondeado; presenta su mayor altura junto a 
los umbos. Umbos abultados. Tamaño hasta 
8 mm de longitud S. patagónica 

1'. Concha con el extremo posterior trun- 
cado; presenta su mayor altura cerca del ex- 
tremo. Umbos pequeños. Tamaño hasta 12 
mm de longitud S. rouchi 

Silicula patagónica Dalí, 1908 
Fig. 130 

Silicula (Phaseolus) patagonicus Dalí, 
1908a: 392 (Loe. tipo: costa W Patagonia, 
51 2'S). 

Silicula patagónica Dalí, Carcelles y 
Williamson, 1951: 324; Soot-Ryen, 1959: 14; 
Alien y Sanders, 1973: 283, fig. 23. 

Material estudiado 

1 ejemplar (ej) y 2 valvas (v); MZUC. Proce- 
dencia: (1 ) 1 ej, 5.7 mm (No. 4651 ), "Hero" 69- 



146 



VILLARROEL & STUARDO 



5. Est. 56, Puerto Bueno, Canal Sarmiento 
(51 =0'50" S; 74°1 4'1 0"W); fango, 221 m. (2) 2 
V, 8 mm (No. 4659), "Hero" 69-5, Est. 201, 
Confluencia Canales Trinidad y Concepción 
(50^9'55" S; 7443'25"W); fango, 460 m. 



1951: 6; Carcelles, 1953: 208; Powell, 1958: 
1 71 ; Powell, 1 960: 1 71 ; Dell, 1 964: 1 47: Nicol, 
1966: 15, lám. 1, figs. 1, 7; Allen y Sanders, 
1973: 284, figs. 25-27; Egorova, 1982: 56, 
figs. 242-244; Dell, 1990: 16, fig. 13. 



Descripción 

Concha: Concha muy semejante a S. rouchi, 
pero más pequeña (hasta 8.4 mm), con el ex- 
tremo posterior menos truncado y menos alto 
y el borde dorsal posterior más recto. 

Anatomía Interna: Caracteres anatómicos 
muy semejantes a los de S. rouchi. 



Observaciones 

La comparación anatómica de S. patagó- 
nica con S. rouchi no estableció diferencias 
significativas. Aunque el ejemplar estudiado 
de S. patagónica era más pequeño que los de 
S. rouchi. (probablemente un juvenil), se con- 
sidera que la conclusión anterior es válida, no 
así en el caso de la concha donde se encon- 
traron diferencias que correspondían a la 
descripción original. 

Pese a esto, es indudable que ambas es- 
pecies necesitan una revisión basada en una 
mayor cantidad de ejemplares. 

Distribución Geográfica 

Conocida sólo desde Canal Sarmiento 
(51 °02'30" S; 74 08'30"W) hasta la confluen- 
cia de los Canales Trinidad y Concepción 
(59 = 9'55"S; 74°43'25"W). 

Habitat 

Silicula patagónica parece ser una especie 
muy rara, ya que se encontró sólo un ejem- 
plar vivo a 221 m de profundidad y 2 valvas a 
460 m, en substrato fangoso. Con anteriori- 
dad, se conocía sólo de la localidad tipo 
donde fue colectada entre 223-544 m de pro- 
fundidad en fango (Dell, 1990). 

Silicula rouchi Lamy, 1911 
Figs. 5, 14,48,49. 126 

Silicula rouchi Lamy, 1911: 394 (Loe. tipo: 
Tierra Alejandro I); Lamy, 1911: 30-1, lám. 1, 
figs. 24, 25: Hedley, 1916: 18; Soot-Ryen, 



Material Estudiado 

9 ejemplares (ej); MZUC. Procedencia: (1) 
7 ej, 9-11.2 mm (Nos. 4500, 4508, 4509, 
4515), Ant. XIX, Est. 2, E. de Bransfield 
(63"12'S; 58 35'W); fango, 135-150 m. (2) 1 
ej roto (No. 4546), Ant. XXII, Est.22, draga 
Petersen 0.1 m^. Isla Greenwich, Shetland 
del Sur (62° 28'30"S; 59 39'24"W); fango, 
196 m. (3) 1 ej, 12 mm (No. 4523), Ant. XXII, 
Est. 56, draga Petersen 0.1 m^. Isla Green- 
wich, Shetland del Sur, (62°25'48"S; 
59°37'W); fango, 244 m. 

Descripción 

Concha: Concha de regular tamaño (hasta 1 2 
mm de longitud), blanca, oblonga, alargada, 
comprimida lateralmente, delgada, frágil; en- 
treatDÍerta anteriormente. Parte anterior corta, 
semicircular; parte posterior más alargada. 
Borde dorsal recto: posterior oblicuamente 
truncado, formando casi un ángulo con el 
borde ventral. Perióstraco verdoso a pardo 
claro amarillento, con bandas más oscuras. 
Umbos ubicados en el tercio anterior; poco 
prominentes, de ápices agudos y levemente 
prosogiros. Ornamentación muy fina, for- 
mada por líneas de crecimiento muy densas; 
en la región anterior hay líneas radiales muy 
tenues, difícilmente observables en la zona 
adyacente a los umbos; en la región posterior 
existen dos o más surcos finísimos. Interior 
de las valvas de color blanco, aporcelanado, 
brillante. Ligamento casi totalmente interno 
dividido externamente en una parte anterior y 
otra posterior a los umbos. Línea paleal muy 
débil; seno paleal pequeño, ubicado inmedia- 
tamente debajo de la impresión del aductor 
posterior y no más grande que ella. Impre- 
siones de los aductores poco notorias. 

Anatomía Interna: Manto con pliegues y lobu- 
laciones pequeñas, poco numerosas en la 
región posterior. Píe grande, muy geniculado. 
Sin glándula hipobranquíal. Palpos labiales 
relativamente pequeños con surcos grandes; 
tentáculo del palpo con una base diferenciada 
de la lámina del palpo que llega hasta la pro- 
ximidad de la boca. Ctenidios alargados, ubi- 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



147 



cados en el techo de la cavidad del manto; fi- 
lamentos triangulares con un gran poro la- 
teral. Corazón tubular, delgado, atravesado 
por el recto. Estómago grande con repliegues 
complementarios a la gran área de selección 
(as). Intestino corto en forma de "S". Con un 
solo tubo sifonal. Tentáculo del sifón, largo y 
fino, ubicado sobre el lado izquierdo. 

Observaciones 

Algunos ejemplares presentan adheren- 
cias de color pardo rojizo sobre los umbos y 
los bordes anteriores. 

Los ctenidios de los protobranquios han 
sido descritos tradicionalmente como no re- 
flejados; sin embargo, en Silicula rouchi se 
observa un esbozo de reflejo de filamento ex- 
terno (Fig. 5), correspondiendo en parte, a la 
condición hipotética intermedia postulada por 
Yonge (1959), entre la condición protobran- 
quial y la condición filibranquial (Morton y 
Yonge, 1964). 

Distribución Geográfica 

Antartica: Shetland del Sur, Archipiélago de 
Palmer, Isla Alejandro, Tierra del Kaiser Wil- 
helm II, Tierra Adelaida, Tierra del Rey Jorge 
V, Tierra Oates y Mar de Ross (Dell, 1 964). 

Habitat 

Las muestras estudiadas cubren sólo en 
parte el área de dispersión de la especie. En 
el Estrecho de Bransfield se la encontró en 
profundidades de 135 y 150 m, en substrato 
de fango; en la Isla Greenwich de las Shet- 
land del Sur, en 1 96 y 244 m, en fango. Se en- 
contró un mayor número de ejemplares en la 
primera localidad mencionada. 

Con anterioridad, S. rouchiiue encontrada 
en fondos de fango entre 160 y 355 m, en 
fondo de fango y cantos entre 278 y 500 m y 
en fondo de diatomeas en 720 y 826 m (Dell, 
1964). En el Mar de Ross se encontró entre 
311 y 1153 m (Dell, 1990). 

Familia Sareptidae Stoliczka, 1871 
Diagnosis 

Concha generalmente frágil, marcada- 
mente comprimida, ovalada o alargada, ge- 
neralmente extendida posteriormente; puede 
o no ser rostrada, puede o no estar entre- 
abierta; lisa o con finas líneas concéntricas de 



crecimiento; margen posterodorsal recto o 
convexo, raramente cóncavo; series de dien- 
tes de la charnela anterior y posterior inte- 
rrumpidos; ligamento interno y/o externo 
puede estar ubicado en un condróforo; sifo- 
nado (Alien y Hannah, 1986). 

Subfamilia Sareptinae Stoliczka, 1871 

Diagnosis 

Concha moderadamente grande, comph- 
mida, alargada, ligeramente entreabierta an- 
terior y posteriormente, levemente rostrada; 
escultura concéntrica fina, ocasionalmente 
con estrías oblicuas o radiales; ligamento en 
su mayor parte interno; sifones fusionados 
ventralmente, lumen completo. 

Género Уо/сУ/а Möller, 1842 

Yoldia Möller, 1842; 91. Especies citadas; 
"V; árctica, Nucula árctica Gray" y 'T angu- 
laris nob.. Nue. Myalis Couth.?" Especie tipo 
por designación posterior (ICZN Opinion 769 
en 1966); Yoldia hyperborea Torell, 1859 
(Nombre No. 1706), = Nucula hyperborea 
Gould, 1 841 , ex Lovén ms {fide Coan y Scott, 
1997; 22). 

Diagnosis 

Algo similar a Nuculana. pero con la con- 
cha más delgada, subovada, débilmente ros- 
trada, generalmente entreabierta posterior- 
mente. Sin ornamentación; sólo con líneas de 
crecimiento. Charnela formada por dos senes 
subiguales de pequeños dientes en forma de 
"v" invertida; condróforo grande, ubicado 
simétricamente entre las dos hileras de dien- 
tes. Sifones largos. Seno paleal profundo y 
amplio; el ápice en forma de "U" ancha. 

Observaciones 

Una discusión acerca de la designación de 
la especie tipo de Yoldia ha sido hecha por 
Grant y Gale (1 931 ) y resumida por Hertlein y 
Strong (1940), quienes dan también una 
sinonimia detallada. 

Subgénero Aequiyoldia Soot-Ryen, 1951 

Aequiyoldia Soot-Ryen, 1951: 6. Especie 
tipo por designación original: Yoldia subae- 
qfu/7atera//s Smith, 1875. 



148 



VILLARROEL & STUARDO 



Diagnosis 

Conclia casi equilateral, débilmente ros- 
trada. Charnela con escasos dientes, casi en 
igual número a cada lado; condróforo triangu- 
lar y amplio. Márgenes del manto casi siempre 
con tentáculos solamente sobre los sifones. 

Observaciones 

Soot-Ryen (1951) creó este subgénero 
para las especies antarticas "que no están es- 
trechamente relacionadas a las especies 
meridionales de Yoldia s. str," justificando su 
separación "en la apariencia general, los 
pocos dientes y algunas diferencias en la 
anatomía." Además de los dientes, la única 
caracteristica anatómica que parece impor- 
tante es la distribución de las papilas o ten- 
táculos en los bordes del manto, por sobre los 
sifones, como se indica en la diagnosis. 

Yoldia {Aequiyoldia) eightsi {Jay. 1839, ex 

Couthouy MS) 

Figs. 44-46,87-89, 128-129 

Nucula eightsii Jay, 1839, ex Couthouy MS: 
113, lám. 1 , figs. 12, 13 (Loe. tipo: no indicada) 
(E. Coan, 1995, comunicación personal): 
Couthouy, in Jay, 1839 {fide Bernard, 1983). 

Yoldia sp. n. Woodward, 1854: 270, fig. 182 
(Loc. tipo: no indicada). 

Leda {Yoldia) eightsii (Jay, 1839, ex 
Couthouy MS), Hanley, 1860: 142, fig. 164. 

Leda {Yoldia) woodward! Hanley, 1860: 
140-141, pi. 226, figs. 17, 22 (sin localidad). 

Yoldia woodwardi Hanley, Sowerby II, 
1871: Yoldia lám. 1, fig. 2a, b; Pelseneer, 
1903: 10; Lamy, 1906: 19; Lamy, 1910: 393; 
Lamy, 1911 : 29; Melvill y Standen, 1914: 127; 
Carcelles, 1950: 74; Carcelles y Williamson, 
1951:325; Bernard, 1983: 13. 

Yoldia cl woodwardi Иап\еу, Linse, 1997: 
46 

Yoldia eightsii (Jay, 1839, ex Couthouy 
MS), Sowerby II, 1871; lám. 5, sp. 26: Smith, 
1 902; 21 1 ; Hedley, 1911:3; Melvill у Standen, 
1914: 127; Carcelles у Williamson, 1951:325. 

Yoldia kerguelensis Thiele у Jaeckel, 1 931 : 
207, lám. 8, fig. 65; Gaillard, 1974: 6. 

Yoldia subaequilateralis Smith, 1875: 73; 
1879: 187, lám. 9, fig. 18; 1885: 242; 1902: 
211; Gaillard, 1974:6. 

Yoldia {Aequiyoldia) subaequilateralis 
Smith, Soot-Ryen, 1951: 6; Powell, 1957: 
114; 1960: 170. 



Yoldia {Aequiyoldia) woodwardi Hanley, 
Soot-Ryen, 1951: 7, lám. 1, figs. 1-6; Car- 
celles, 1953: 208; Soot-Ryen, 1959: 15; Pow- 
ell, 1960: 171; Bernard, 1983: 13. 

Yoldia {Aequiyoldia) eightsii {Jay, 1839, ex 
Couthouy MS), Soot-Ryen, 1951: 6; Car- 
celles, 1953:208. 

Yoldia {Aequiyoldia) eightsi {Jay, 1839, ex 
Couthouy MS). Dell, 1963: 247, fig. 1; Dell, 
1964: 146; Nicol, 1966: 11, lám. 1, figs. 6, 8; 
Rabarts y Whybrow, 1979: 177, figs. 3-5, 
8-10, 14a, b, 15c, b; Bernard, 1983: 13; Dell, 
1990: 10, figs. 2, 5. 

Material Estudiado 

259 ejemplares (ej) y 1 valva (v); MZUC. 
Procedencia: (1 ) 31 ej, 1 -31 .5 mm (No. 4503), 
Ant. XIX, Est. 16, Isla Decepción (62 ■59'24"S; 
60 34W); fango, 97 m. (2) 4 ej, 22-30 mm (No. 
4504), Ant. XIX, Est. 10, Bahia Chile, Puerto 
Soberanía (62°30'S; 59 41'W); fango, 25 m. 
(3) 17 ej, 4.5-31.8 mm (No. 4530), Ant. XXII, 
Est. 37, draga Petersen 0.1 m^. Isla Green- 
wich, Shetland del Sur (62 28'24"S; 
59°41'24"W); fango arenoso, 33 m. (4) 13 ej, 
4.5-31.4 mm, (No. 4531) Ant. XXII, Est. 36, 
draga Petersen 0.1 m , Isla Greenwich, 
(62 28'42"S; 59 42'24"W); tango 33 m. (5) 1 
ej, 32.5 mm (No. 4532) Ant. XXII, Est. 34, 
draga Petersen 0.1 m^. Isla Greenwich, 
(62"29'S; 5942'6"W); tango arenoso, 38 m. 
(6) 16 ej, 12.5-26 mm (No. 4533), Ant. XIX, 
Est. 10, Bahía Chile, Calefón Iquique, Isla 
Greenwich (62 30'S; 59 41'W); fango y can- 
tos, menos de 10 m. (7) 1 ej, 28 mm (No. 
4534), Ant. XXII, Est. 40, draga Petersen 0.1 
m^. Isla Greenwich (62 29'6"S; 59 40'30"W); 
fango arenoso, 44 m. (8) 1 ej, 24 mm (No. 
4535), Ant. XXII, Est. 31, draga Petersen 0.1 
m^. Isla Greenwich (62 29'6"S; 59'41'W); 
fango arenoso, 39 m. (9) 2 ej, 31.7-32.5 mm 
(No. 4536), Ant. XXII, Est. 35, draga Petersen 
0.1 m^. Isla Greenwich (62^^29'S; 5942' 
36"W); fango arenoso, 48 m. (10) 1 ej, 28.4 
mm (No. 4538), Ant. XXII, Est. 29 draga Pe- 
tersen 0.1 m^ Isla Greenwich (62"29'30"S; 
59 40'6"W); fango arenoso, 49 m. (11) 1 ej, 12 
mm (No. 4539), Ant. XXII, Est. 39, draga Pe- 
tersen 0.1 m^. Estrecho de Bransfield 
(62 •28'54"S; 59°41 '1 8"W); tango arenoso, 54 
m. (12) 2 ej, 17 y 19.5 mm (No. 4541), Ant. 
XXII, Est. 17, draga Petersen 0.1 m^, E. de 
Bransfield (62 58'6"S; 60 40'6"W); arena 
fina, fango, 93 m. (13) 5 ej, 3-5.5 mm (No. 
4542), Ant. XXII, Est. 26, draga Petersen 0.1 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



149 



m^, Isla Greenwich, (62°28'22"S; 59°38' 
12"W); fango, 90 m. (14) 1 ej 35.5 mm (No. 
4543), Ant. XXII, Est. 38, draga Petersen 
0.1 m^, Isla Greenwich (62 28'36"S; 59 41' 
36"W); arena, fango, 33 m. (1 5) 1 61 ej, 5.5-30 
mm (No. 4544), Ant. XIX, Bahía Chile, Puerto 
Soberanía, (62" 30'S; 59-4rW); fango, más o 
menos 25 m. (16) 1 v d, 13.3 mm (No. 4661), 
Base Antartica A. Prat. (17) 2 ej, 13.8 y 32.7 
mm (No. 4505), Ant. XIX, Bahía Margarita 
frente a Islas Jenny y Adelaida (67'50'S- 
68'45'S); cantos glaciales, 150 m. 



Descripción 

Concha: Concha de regular tamaño (hasta 
35.5 mm de longitud), subovalada, compri- 
mida, gruesa, entreabierta anteriormente, 
blanca. Parte anterior ligeramente más larga 
que la posterior que es algo aguzada; bordes 
redondeados; el dorsal posterior levemente 
cóncavo, a veces anormalmente exagerado. 
Perióstraco amarillo verdoso en los juveniles 
a pardo oscuro en los ejemplares de mayor 
tamaño, más oscuro hacia el margen ventral; 
ocasionalmente con bandas concéntricas 
más oscuras. Umbos muy poco abultados, 
generalmente erosionados. Apices pequeños, 
opistogiros. Ornamentación formada por es- 
trías de crecimiento finas y líneas radiales 
tenues, más notorias en los extremos anterior 
y posterior. Condróforo triangular. Resilium 
casi totalmente interno, dividido externamente 
en una parte anterior y otra posterior al 
condróforo, siendo la anterior de mayor 
tamaño. Interior de las valvas blanco, brillante, 
engrosado dorso posteriormente. Charnela 
formada por dos series subiguales de dientes 
fuertes, poco numerosos (hasta 12); la 
anterior con uno o dos dientes más que la pos- 
terior. Línea paleal débil; seno paleal subre- 
dondeado anteriormente, profundo, alcan- 
zando hasta la altura del condróforo; 
posteriormente agudo. Impresión de los mús- 
culos sifonales pequeña y débil, ventral y pos- 
terior a la impresión del aductor. 

Anatomía Interna: Manto de bordes gruesos 
especialmente sobre los sifones, con pe- 
queñas papilas en la región anterior y poste- 
rior. Pie angosto, levemente geniculado. 
Masa visceral muy grande. Cavidad pe- 
ricádica desplazada mucho más atrás del 
condróforo. Láminas del palpo muy angostas; 
tentáculo del palpo largo. Glándula hipobran- 
quial pequeña. Estómago muy alargado con 



el área de selección mayor (as) dividida en 
dos regiones con diferente orientación de los 
pliegues ciliados; hay una área plegada adi- 
cional (¿área de selección?) sobre ella. Si- 
fones firmemente unidos. 



Observaciones 

Yoldia (A.) eightsies el protobranquiado de 
mayor tamaño existente en aguas antarticas. 

Ejemplares de las muestras de Puerto 
Soberanía e Isla Decepción, presentan una 
concavidad dorsal posterior notoria por efecto 
de un crecimiento defectuoso, fenómeno ob- 
servado por Dell (1963) al revisar el tipo. La 
comparación anatómica entre ejemplares 
que presentaban esta concavidad y otros nor- 
males no arrojó diferencias. 

La sinonimia de esta especie fue aclarada 
por Dell (1963). 

Peck y Bullough (1993) calcularon el incre- 
mento anual de crecimiento de Y. (A.) eights! 
basados en una población de la Isla Signy, 
Antartica, en alrededor de 5 mo. Las edades 
para los individuos más grandes de la 
población (35 mm de largo) fueron calculados 
en ± 65 años. A los especímenes de 43 mm 
les calcularon 120 años. Estos mismos au- 
tores encontraron que en las zonas expues- 
tas predominan los juveniles, lo cual explican 
se deba al efecto abrasivo de los iceberg 
sobre los bancos de Yoldia y a la inhibición 
del asentamiento de larvas por las altas den- 
sidades de individuos. 

Otros autores como Davenport (1989), 
Rabarts (1970), y Nolan y Clarke (1993) en- 
contraron tasas de crecimiento similares 
usando tres técnicas diferentes. 



Distribución Geográfica 

Yoldia {A.) eightsi es una especie amplia- 
mente distñbuida en la Antartica (Dell, 1 990). 
Se la ha citado para las Islas Falkland, Geor- 
gia del Sur, Oreadas del Sur, Shetland del 
Sur, Islas Sandwich del Sur, Archipiélago de 
Palmer, Mar de Bellinghausen y Mar de Ross. 
Aunque considerada una especie con proba- 
ble distribución circunantártica (Dell, 1964; 
Nicol, 1966), Yoldia (A.) eightsi ha sido en- 
contrada con una distribución en parches 
alrededor del continente. Tierra del Fuego, 
Sur de Chile, hasta las Islas Kerguelen (Dell, 
1990). 

Rabarts y Whybrow (1979) aseveran que 



150 



VILLARROEL & STUARDO 



Yoldia (A.) woodwardi es simpátrica con 
Yoldia (A.) eights! en las Islas Falklands y en 
Tierra del Fuego. 

Habitat 



Yoldia lucida Lovén, 1846 (ICZN Opinión 
1306, en 1985); ilustrada como Portlandia lu- 
cida Lovén, por Sars, 1878: 37, lám. 4, figs. 
8a., 8b; Schileyko, 1985; 171; Waren, 1978; 
214; 1989; 226. 



En las muestras estudiadas fue encontrada 
en Isla Decepción, Archipiélago de Palmer, y 
Shetland del Sur en substrato de fango y can- 
tos a menos de 10 m de profundidad; en 
fango arenoso entre 25 y 97 m y entre cantos 
glaciales en 1 50 m; en el Mar de Ross entre 4 
y 55 m. 

Con anterioridad, esta especie fue colec- 
tada entre 50 y 87 m de profundidad en fon- 
dos de cantos pequeños, arena con cantos, y 
arcilla arenosa con algas y cantos (Soot- 
Ryen, 1951), en fondos de arena entre 144 y 
161 m de profundidad, arena verde, fango y 
conchas entre 135 y 144 m, en fango verde 
entre 244 y 344 m y en fondo rocoso entre 
200 y 728 m (Dell, 1964). 

Su rango total va de 4-824 m, pero es 
mucho más común en profundidades inferio- 
res a los 100 m (Dell, 1990). 

Yoldia (Aequiyoldia) eightsi cava relativa- 
mente poco comparada con otras especies 
de Yoldia (Davenport, 1989). Se alimenta 
principalmente de material orgánico presente 
en las capas superficiales de los sedimentos 
(Yonge, 1939; Davenport, 1988). 

Subfamilia Yoldiellinae Alien y Hannah, 1986 



Diagnosis 

Concha pequeña, generalmente compri- 
mida, ovalada o elíptica, ocasionalmente con 
un rostro mal definido, no entreabierta; lisa, o 
con escultura muy fina; ligamento anfidético, 
en gran parte interno; sifones de estructura 
variada, seno sifonal pequeño; intestino con 
configuraciones diversas (Alien y Hannah, 
1986). 

La atribución de esta subfamilia como 
Yoldiellidae Alien, 1978, y Yoldiellinae Alien, 
1985, ha sido decretada nomina nuda. 
porque no hay suficientes caracteres para 
separlas de otras familias/subfamilias. Entre 
los autores que han seguido atribuyendo in- 
correctamente a la subfamilia está Oliverio 
(1993). 



Diagnosis 

Concha pequeña, frágil, ovalada, general- 
mente cuneiforme; cerrada o muy ligera- 
mente entreabierta. Perióstraco satinado, 
iridiscente. Ligamento parcialmente externo; 
la parte interna, que es relativamente grande, 
interrumpe el margen de la charnela más o 
menos completamente y ocupa una ranura 
simple, generalmente delimitada por un lomo 
en la superficie inferior de la línea de la char- 
nela. Seno paleal relativamente pequeño, 
generalmente indistinto. Sifones delgados y 
unidos sólo hasta la mitad de su longitud. 

Especies Estudiadas 

1 . Yoldiella ecaudata (Pelseneer, 1 903) 

2. Yoldiella chilenica{Da\\, 1908) 

3. Yoldiella indolens (DaW, 1908) 

Dalí (1 908a) describió para Chile cuatro es- 
pecies de Yoldiella. como Yoldia: Y. granula 
del Estrecho de Magallanes, Y. indolens, Y. 
chilenica. y Y. infrequens de la zona de los 
canales al N del Estrecho de Magallanes. 
Ninguna de estas especies fue ilustrada ori- 
ginalmente, por lo que se presentan aquí por 
primera vez fotografías de V. chilenica y Y. in- 
dolens. Yoldiella infrequens podría conside- 
rarse definitivamente como un sinónimo de 
lindarla virens Dalí, 1889, ya que así lo de- 
muestran su descripción y las observaciones 
del tipo efectuadas por Soot-Ryen (1959). 

Se incluye en este estudio a la especie Y. 
ecaudata (Pelseneer, 1903) de aguas antarti- 
cas. 

Waren (1978, 1989) y Schileyko (1985) han 
hecho intentos basados en el análisis de las 
partes blandas para dilucidar la problemática 
de las especies atribuidas a este género. 
Desgraciadamente la calidad del material que 
estudiamos no nos permitió corroborar las ob- 
servaciones hechas por ellos. 

Clave Para las Especies de 
Yoldiella Estudiadas 



Género Yoldiella Verhll y Bush, 1897 

Yoldiella Verrill y Bush, 1897; 55, figs. 3, 4, 
11 , 14. Especie tipo por designación original; 



1 . Concha ovalada 2 

1' Concha subtriagular; hasta de 5.25 mm 

de longitud Y. indolens 

2. Concha muy inequilateral, con el ex- 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



151 



tremo posterior alargado, dorsalmente recto y 
con un débil escutelo. Hasta de 1 2 mm de lon- 
gitud y. chilenica 

2' Concha ligeramente equilateral, ambos 
extremos levemente aguzados: sin escutelo. 
Hasta de 3.5 mm de longitud . . .Y. ecaudata 

Yoldiella ecaudata (Pelseneer, 1903) 
(Figs. 83-86, 125) 

Leda ecaudata Pelseneer, 1903: 22, figs, 
77, 78 (Loe. tipo: Gaussberg y Archipiélago 
de Palmer): Thiele, 1912: 229, fig. 20, 20a. 

Yoldiella ecaudata (Pelseneer), Soot-Ryen, 
1951: 5; Carcelles, 1953: 208: Powell, 1960: 
170; Dell, 1964: 145; Egorova, 1982: 55, figs. 
234-237; Dell, 1990: 12, figs. 15, 16. 

Material Estudiado 

29 ejemplares (ej) y 3 valvas (v); MZUC. 
Procedencia: (1)1 ej, 3.2 mm (No. 4575), Ant. 
XXII, Est. 61, draga Petersen 0.1 m^ I. 
Greenwich, Shetland del Sur (62'"28'6"S; 
59 30'48"W): fango, 188 m. (2) 2 ej, 1.5-3 
mm (No. 4545), Ant. XXII, Est. 22, draga Pe- 
tersen 0.1 m^, I. Greenwich, Shetland del Sur 
(62'^28'S: 59 39'24"W): fango, 1 96 m. (3) 1 ej, 
3.4 mm (No. 4569), Ant. XXII, Est. 48, draga 
Petersen 0.1 m^, I. Greenwich, Shetland del 
Sur (62 28'12"S; 59'40'6"W); fango arenoso, 
73 m. (4) 2 ej, 3.1-3.3 mm (No. 4576), Ant. 
XXII, Est. 50, draga Petersen 0.1 m^, I. 
Greenwich, Shetland del Sur, (62=28'36"S; 
59"40'30"W): fango, 123 m. (5) 1 ej, 2.5 mm 
(No. 4568), Ant. XXII, Est. 50, draga Petersen 
0.1 m^, I. Greenwich, Shetland del Sur 
(62''28'36"S: 59 40'30"W); fango, 123 m. (6) 
2 ej, 3.5 mm (No. 4228), Ant. XXII, Est. 59, 
draga Petersen 0.1 m^, I. Greenwich, Shet- 
land (62 28'36"S; 59"41'36"W); fango, 70 m. 
(7) 1 ej s, 3.1 mm (No. 4527), Ant. XXII, Est. 
37, draga Petersen 0.1 m^, I. Greenwich, 
Shetland del Sur (62 28'24"S; 5941 '24"W): 
fango arenoso, 33 m. (8) 1 ej, 2.5 mm (No. 
4525), Ant. XXII, Est. 41, draga Petersen 0.1 
m^, I. Greenwich, Shetland del Sur (62" 
27'12"S: 59 37'36"W), fango arenoso, 220 m. 
(9) 1 ej, 2 mm, 3 v, 2.5-3 mm (No. 4522), Ant. 
XXII, Est. 51, draga Petersen 0.1 m^, I. 
Greenwich, Shetland del Sur (62°28'48"S; 
59'40'36"W): fango, 79 m. (10) 1 ej que- 
brado, 3.5 mm (No. 4521), Ant. XXII, Est. 20, 
draga Petersen 0.1 m^, I. Greenwich, Shet- 
land del Sur (62'29'S; 59"39'42"W); fango, 
61 m. (11) 1 ej, 3.5 mm (No. 4570), Ant. XXII, 
Est. 29, draga Petersen 0.1 m^, I. Greenwich, 
Shetland del Sur (62'29'30"S; 5940'6"W); 



fango arenoso, 49 m. (12) 1 ej, 2 mm (No. 
4524), Ant. XXII, Est. 30, draga Petersen 0.1 
m^, I. Greenwich, Shetland del Sur (62"30'S; 
59'40'6"W): fango, 60 m. (13) 13 ej, 2-3 mm 
(Nos. 4501, 4513, 4516), Ant. I, Est. 2, E. de 
Bransfield (63"12'S; 58"35'W); fango, arena, 
"piedrecillas," 135-150 m. (14) 1 ej, 2 mm 
(No. 4519), Ant. I, Est. 1, I. Decepción, Bahía 
Foster; fango, arena y cantos pequeños, 
160 m. 



Descripción 

Concha: Concha muy pequeña (hasta 3.5 
mm de longitud), oval, ligeramente equila- 
teral, con los extremos levemente aguzados. 
Perióstraco amarillo blanquecino, presen- 
tando, a veces, bandas más oscuras. Umbos 
prominentes de ápices levemente opisto- 
giros, adyacentes. Sin ornamentación, pero 
con finas líneas de crecimiento irregular- 
mente distribuidas. Interior de las valvas 
blanco brillante. 

Anatomía Interna: Manto sobresaliendo de 
las valvas en algunos ejemplares, con un 
repliegue largo que rodea al margen ventral, 
y varios pequeños junto a los sifones. Glán- 
dula hipobranquial poco notoria. Palpos labia- 
les de regular tamaño, con tentáculo fuerte. 
Ctenidios anchos, con numerosos filamentos. 
Cavidad pehcárdica relativamente grande: 
corazón atravesado por el recto: aurículas y 
ventrículo globosos: estómago con saco del 
estilo pequeño: área de selección mayor con 
numerosos pliegues. Sifones unidos aparen- 
tando un sifón único. Tentáculo sifonal largo, 
sobre el lado izquierdo. 



Observaciones 

En algunos ejemplares el pie se encontró 
extendido fuera de las valvas y dirigido hacia 
atrás. 



Distribución Geográfica 

Antartica: desde 62 28'S a 70 'S; Gauss- 
berg y Archipiélago de Palmer (Dell, 1964). 
Parece tener una amplia distribución en 
aguas alrededor de la península Antartica. 
Descrita para el mar de Bellinghausen 
(desde 80'O a 92'0) ha sido posteriormente 
colectada en la Estación Gauss (90 E) del 
Mar de Davis y de la Península Antartica 
(Dell, 1990). 



152 



VILLARROEL&STUARDO 



Habitat 

Las muestras estudiadas cubren sólo una 
parte del área de dispersión de la especie. Se 
encontraron ejemplares en la Isla Greenwich, 
Shetland del Sur, en profundidades de 60 a 
196 m en substrato de tango arenoso; en 
Bahía Foster, Isla Decepción, en 160 m en 
fango con arena y cantos, y en el Estrecho de 
Bransfield entre 135 y 150 m, en fango con 
arena y cantos pequeños. Parece ser una es- 
pecie abundante. 

Con anterioridad, Y. ecaudata había sido 
colectada entre 278 y 500 m de profundidad 
fuera del Mar de Ross (Dell, 1964). En el Mar 
de Ross, se encuentra en profundidades 
entre 362 y 891 m con un único muestreo 
conocido a 2525 m (Dell, 1990). 

Yoldiella chilenica (Dalí, 1908) 
Figs. 123, 124 

Yoldia ( Yoldiella) chilenica Dalí, 1 908a: 380 
(Loe. tipo: Canal Sarmiento (51 '52'S; 73' 
41 'W); en fango, entre 348 y 258 brazas 
(626.4 y 464.4 m); Hertlein y Strong, 1940: 
416. 

Portlandia {Yoldiella) chilenica (Dalí), Car- 
celles y Williamson, 1951 : 325. 

Yoldiella chilenica (Dalí), Soot-Ryen, 1959: 
15. 

Yoldiella {Yoldiella) chilenica (Dalí), 
Bernard, 1983: 14. 

Yoldia cf. chilenica (Dalí), Linse, 1997: 46. 

Material Estudiado 

109 ejemplares (ej) y 541 valvas (v); 
MZUC. Procedencia: (1) 3 ej s., 3.5-5 mm 
(No. 4582), M. Ch. I, Est. X-3, Golfo de Ancud 
(42"S;73"W); fango, arena fina, 264 m. (2) 25 
V, 1.5-7 mm (No. 4658), "Hero" 69-5, Est. 
210, draga Petersen 0.1 m^. Bahía Corbeta 
Papudo (50"21'17"S; 75'17'25"W): fango 
amarillo pardo, 70-78 m. (3) 17 ej, 4-7 mm 
(No. 4648), "Hero" 69-5, Est. 56, Puerto 
Bueno, Canal Sarmiento (5rO'50"S; 74" 
14'10"W); fango, 221 m. (4) 5 ej, 3 mm, 4 v, 
3-8.5 mm (No. 4632), "Hero" 69-5, Est. 211, 
Canal Sarmiento (51"12'S; 74 9'W); fango, 
480 m. (5) 1 ej, 1 .5-7 mm (No. 461 6), "Hero" 
69-5, Est. 213, Canal Sarmiento (51 27' 
30"S; 74°03'W); fango, 722m. (6) 3 ej, 7-7.5 
mm, 10 V, 3-8 mm (No. 4625), "Hero" 69-5, 
Est. 279 С, draga Petersen 0.1 m^, E. de Ma- 



gallanes (53°15'S; 70°50'18"W); fango, 156 
m. (7) 2 ej, 6.5-7 mm, 10 ej, 1.5-2.1 mm, 10 
V, 1.5-2 mm, 16 v, 5-6.5 mm (No. 4630), 
"Hero" 69-5, Est. 280 C, draga Petersen 0.1 
m^ E. de Magallanes (53 15'18"S; 70^48' 
18"W); tango, 179 m. (8) 4 ej, 7-7.5 mm, 10 
V, 3-8 mm (No. 4634), "Hero" 69-5, Est. 280, 
E. de Magallanes (5317'18"S: 70''48'36"W); 
fango, 175 m. (9) 2 ej, 7 mm, 4 ej, 1.5-1.7 
mm, 16 V, 3.5-7.5 mm (No. 4633), "Hero" 
69-5, Est. 280 B, E. de Magallanes (53° 
17'18"S: 70°48'18"W); tango, 178 m. (10) 
422 V, 3-8.6 mm (No. 4609), "Hero" 69-5, E. 
de Magallanes, frente a Punta Arenas 
(53°17'18"S; 70'48'36"W): tango, 180-210 
m. (11) 40 ej, 3-7 mm (No. 4620), "Hero" 69- 
5, frente a Punta Arenas, E. de Magallanes 
(53 17'18"S-53 18'40"S;70' 48'36"W- 
70 42'20"W);fango, 180-210 m. (12)9ej, 28 
V, 4-5 mm (No. 4612), "Hero" 69-5, Est. 201 
(9), Confluencia Canales Concepción y Trini- 
dad, (50"9'55"S: 74"43'25"W): fango, 460 m. 

Descripción 

Concha: Concha pequeña (hasta 1 1 .5 mm de 
longitud), oval, alargada posteriormente, 
blanca, inequilateral, la parte anterior más 
corta y redondeada. Borde dorsal posterior 
ligeramente recto. Perióstraco amarillo pálido 
a amarillo verdoso y con bandas de tono más 
oscuro, de ancho y distribución variables. 
Prodisoconcha diferenciada. Sin ornamen- 
tación, pero con líneas de crecimiento muy 
finas. Escutelo débilmente impreso con los 
márgenes de las valvas elevados. Ligamento 
oscuro, anfidético. Interior de las valvas 
blanco, aporcelanado, muy brillante. Seno 
paleal amplio y corto, redondeado hacia ade- 
lante. Serie de dientes anteriores general- 
mente con dos dientes más que los posterio- 
res. 

Observaciones 

No presenta diferencias anatómicas muy 
características que la separen de Y. ecaudata 
(deschta anteriormente), excepto que en esta 
última, el manto sobrepasa el margen de las 
valvas. 

Distribución Geográfica 

Desde el Golfo de Ancud (42 S: 73 W) 
al Estrecho de Magallanes (53 17'18"S; 
70 48'36"W). 



Habitat 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 

Observaciones 



153 



Con anterioridad, Y. chilenica se conocía 
sólo de la localidad tipo en el Canal Sarmiento. 

En las muestras estudiadas se encontró en 
el Golfo de Ancud a una profundidad de 264 m, 
en substrato de arena fina y en el Estrecho de 
Magallanes en profundidades entre 70 y 722 
m, en substrato fangoso. Su mayor densidad 
se observó entre 1 80 y 21 m de profundidad. 

Es una especie muy abundante en los fon- 
dos fangosos del Estrecho de Magallanes. Se 
la encuentra viviendo preferentemente junto a 
Tindaria virens y Ennucula grayi. 

Yoldiella indolens (Dalí, 1908) 
Fig. 127 

Yoldia (Yoldiella) indolens Dalí, 1908a: 381 
(Loe. tipo: Costas del S. de Chile, Canal 
Messier (4841 'S; 74 24'W-48 '9'S; 74° 
36'W); 194 brazas (349.2 m), fango); Hertlein 
y Strong, 1940:417. 

Yoldia indolens (Dalí), Carcelles y William- 
son, 1951:325. 

Material Estudiado 

2 ejemplares (ej) y 18 valvas (v); MZUC. 
Procedencia: (1 ) 1 ej, 2 mm, 4 v, 1 .3-1 .4 mm 
(No. 4520), "Hero" 69-5, Est. 280-C draga Pe- 
tersen 0.1 m^ E. de Magallanes (53 '15'18"S; 
70''48'36"W); fango, 179 m. (2) 1 ej, 2 mm, 6 
V, 1.8-2.2 mm (No. 4626), "Hero" 69-5, Est. 
280-B, draga Petersen 0.1 m^, E. de Maga- 
llanes (53 17'18"S; 70 48'36"W); tango, 178 
m. 3) 1 8 V, 1 .5-2 mm (No. 4643), Hero" 69-5, 
Est. 210, draga Petersen 0.1 m^. Bahía Cor- 
beta Papudo (Guarello), (50 21'17"S; 
75°17'25"W); tango, 70-78 m. 

Descripción 

Concha: Concha muy pequeña (hasta 5.25 
mm de longitud), oval, inflada, translúcida; in- 
equilateral con el lado anterior más corto. Ex- 
tremos redondeados, el posterior con un débil 
ángulo superior. Perióstraco oliváceo, opaco, 
con 2 ó 3 bandas angostas más oscuras de 
distribución variable. Umbos amplios, abulta- 
dos. Sin ornamentación. Interior de las valvas 
aporcelanado. Seno paleal pequeño. Dientes 
anteriores y posteriores en número igual. 

Anatonia Interna: Partes blandas aparente- 
mente como en Y. ecaudata. 



El color blanquecino opaco de algunas val- 
vas de esta especie pequeña, sugiere un cam- 
bio de aspecto por alteración de la concha al 
enterrarse en el fango. Además, por efecto del 
desgaste, algunas se ven equilaterales, su- 
giriendo las características de la especie Y. 
granu/a descrita por Dalí (1908); sin embargo, 
estas valvas no presentan el diente distinto a 
los otros, mientras que en otras se constatan 
focos de calcificación incipiente. 

Aunque los ejemplares estudiados no al- 
canzan el tamaño del ejemplar tipo (5.25 
mm), se observan en ellos todos los rasgos 
de la concha que caracterizan e esta especie. 

Distribución Geográfica 

Estrecho de Magallanes entre 53°15'S y 
53°17'S. 



Habitat 

Con anterioridad, Y. indolens se conocía 
sólo de la localidad tipo en el Canal Messier, 
en substrato de fango a 349 m de profundi- 
dad. En las muestras estudiadas se encontró 
en el Estrecho de Magallanes en profundi- 
dades entre 70 y 1 79 m en sustrato fangoso. 



Familia Malletiidae H. Adams 
y A. Adams, 1858 

Diagnosis 

Concha redondeada, alargada o veneri- 
forme, a veces posteriormente aguzada o 
truncada; equivalva; inequilateral o equila- 
teral. Charnela casi recta, con dientes más o 
menos numerosos; serie anterior con un 
número menor de dientes que la serie poste- 
rior. Ligamento externo, alargado, promi- 
nente, opisto o anfidético, o parcialmente in- 
terno, corto y alojado en una cavidad de las 
valvas. Apices orto u opistogiros. Con o sin 
seno paleal. Glándula hipobranquial grande. 
Corazón ventral al recto o atravesado por él. 
Ctenidios con un poro ventral. Sifones sepa- 
rados ventralmente o unidos por manojos de 
cilios o por tejido. 

Los representantes recientes de esta fa- 
milia viven en todos los mares, preferente- 
mente en aguas profundas y fondos blandos. 



154 



VILLARROEL & STUARDO 



Observaciones 

El rango taxonómico de la familia Malleti- 
idae ha sido muy discutido. Este taxón fue 
descrito originalmente como subfamilia de 
Nuculanidae por H. Adams y A. Adams (1 858) 
y elevada de rango por autores posteriores, 
quienes la separaron de los Nuculanidae 
esencialmente por la presencia de un liga- 
mento externo. Se sugería, así, dar importan- 
cia filogenética primaria a la utilización de la 
posición del ligamento en la clasificación de 
los protobranquios recientes y fósiles, inclu- 
yendo a la familia fósil Ctenodontidae, princi- 
palmente paleozoica. Sin embargo, Yonge 
(1939, 1959) al realizar un estudio anatómico 
y funcional de los protobranquios, concluyó 
que las características de Malletia y otros 
géneros incluidos tradicionalmente en esta fa- 
milia no justificaban su separación, ya que no 
pasaban de ser nuculánidos especializados 
para vivir de preferencia en los fondos blandos 
de profundidad, donde la competencia es es- 
casa. Este modo de vida estaría demostrado 
por una concha de apariencia delicada y más 
o menos comprimida lateralmente. Además, 
no serían diferentes, ya que mostrarían la 
misma anatomía básica y las mismas adapta- 
ciones encontradas en todos los represen- 
tantes vivientes de la familia Nuculanidae. 
Agregó, que el ligamento externo de Malletia 
no tendría mayor peso para indicar relación 
filogenética que el complejo total de una mor- 
fología y caracteres adaptatives esencial- 
mente idénticos, por lo que sugirió reunir 
ambas familias. La validez de estos argumen- 
tos parecía irrefutable y así fue considerado 
subsecuentemente por algunos autores. 

McAlester (1964), junto con reconocer el 
valor de las conclusiones de Yonge de que las 
diferencias en el modelo del ligamento no in- 
dican una divergencia filogenética primaría de 
los géneros nuculoides, hizo notar la falta de 
conocimiento sobre la morfología de otros 
géneros externamente lígamentados, que no 
se parecen mucho a Malletia. Concluyó, que 
un mayor estudio podría descubrir que estas 
formas son fundamentalmente diferentes 
tanto a Malletia como a otros nuculánidos 
vivientes, lo que fue corroborado con pos- 
terioridad por Sanders y Alien (1 985). Sin em- 
bargo, el estudio anatómico comparativo de 
especies pertenecientes a los géneros Mal- 
letia, Tindaria, y Tindariopsis y las descrip- 
ciones de las partes blandas de Neilonella y 
otras especies de Malletia y Tindaria dadas 
por Knudsen (1970), sugerían la utilización de 



caracteres adicionales para la diferenciación 
taxonómica de estos grupos, tales como las 
vueltas del intestino, la estructura de los si- 
fones, la disposición de las áreas de selec- 
ción del estómago y la posición del corazón 
en relación al recto. Como ya ha sido discu- 
tido, sólo el último de estos caracteres parece 
encerrar valor taxonómico a nivel de familia, 
ya que mientras las especies estudiadas de 
los géneros Nuculana, Propeleda (Nucu- 
lanidae), Silicula (Siliculidae), Yoldia y Yol- 
diella (Sareptidae) tienen un corazón atrave- 
sado por el recto, especies de los géneros 
Malletia (Malletiidae), Tindaria (Tindariidae), y 
Tindariopsis (Nuculanidae) tienen el corazón 
ventral al recto o atravesado por él. 

La estructura de los sifones y del estómago 
parece presentar tendencias evolutivas múlti- 
ples (algunas de las cuales es necesario es- 
tudiar mejor) cuyo valor taxonómico es difícil 
de precisar. Así por ejemplo, Malletia pre- 
senta sifones completamente unidos y cerra- 
dos o abiertos ventralmente, mientras que en 
los otros géneros de Malletiidae y Nucu- 
lanidae, pueden estar separados o unidos 
parcial o totalmente y ventralmente abiertos, 
en parte o por completo. Las vueltas del in- 
testino, pueden tener también algún valor ta- 
xonómico como lo ha sugerido Knudsen 
(1970). Sin embargo, sólo el estudio de un 
número mayor de especies de cada género 
permitirá en último término sancionar el valor 
de estos caracteres. 

Las especies chilenas con estas carac- 
terísticas están incluidas en los géneros: Ma- 
lletia. Tindaria, Tindariopsis, y Malletiela. Este 
último representado sólo por M. sorror Soot- 
Ryen, 1959: 18, lám. 1, figs. 4, 5. "Albatross" 
Est. 2791 , costas SW de Chile en 677 brazas 
= 1218.6 m, es conocido sólo en la localidad 
tipo. Esta especie no se halló en las muestras 
estudiadas. 

Género Malletia des Moulins, 1832 

Malletia des Moulins, 1832: 85. Especie 
tipo por monotipia: Malletia chilensis des 
Moulins, 1832. 

Diagnosis 

Concha de tamaño mediano, oval, com- 
primida lateralmente, alargada: posterior- 
mente aguzada o redondeada; por lo general 
bastante delgada. Lisa o concéntricamente 
estriada. Interior subnacarado. Charnela con 
la serie posterior de dientes separada de la 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



155 



anterior. Ligamento externo, alargado, promi- 
nente. Seno palea! grande y profundo. Si- 
fones, completamente unidos, cerrados o 
abiertos ventralmente. 

Especies Estudiadas 

1 . Malletia chilensis des Moulins, 1 832 

2. Malletia patagónica Mabille y Roche- 
brune, 1889 

Otras tres especies recientes han sido des- 
critas para Chile: 

M. inequalis Dalí, 1908: M. magellanica 
(Smith, 1875); y M. /7yades/ Mabille y Roche- 
brune, 1889. La validez de algunas de estas 
especies se discute más adelante. 

Clave Para las Especies Chilenas 
de Malletia 

1 . Extremo posterior aguzado . M. magella- 
nica 

1'. Extremo posterior redondeado o algo 
truncado 2 

2. Extremo posterior redondeado: anterior 
más o menos truncado M. chilensis 

2'. Extremo anterior redondeado: posterior 
algo truncado 3 

3. Parte anterior mucho más larga que la 
posterior. Borde dorsal anterior redondeado. 
Sin escutelo M. inequalis 

3'. Parte anterior más corta o igual. Bordes 
dorsal anterior y posterior casi rectos. Con es- 
cutelo M. patagónica 

Malletia chilensis oes Moulins, 1832 
(Figs. 17, 50-53, 56, 91. 92, 133, 146, 147) 

Malletia chilensis des Moulins, 1832: 85, 
lám, 1 , figs. 1 -8; H. Adams y A. Adams, 1 858: 
549, lám. 126, figs. 6, 6a: Chenu, 1862: 181, 
fig. 913; Kolbelt, 1881: 372, lám. 109, fig. 3; 
Tryon, 1884: 249, lám. 126, fig. 34 (expl. en 
lám. 126 como Yoldia {Malletia) chilensis); Fis- 
cher, 1 886: 987. lám. 1 7, fig. 22: Verrill y Bush, 
1 897: 56, 60, fig. 9; Stempell, 1 898a: 343, lám. 
22, figs. 2, 3, 4, 9, 1 2; lám. 23. figs. 13-17; lám. 
24, fig. 32 (Anat.); Stempell, 1902: 219: Dall, 
1 909: 251 ; Carcelles y Williamson, 1 951 : 322; 
Soot-Ryen, 1959: 16, figs. 1, b; Franc, 1960: 
2074, fig. 1731; Dell, 1964: 148; Ramorino, 
1968: 191. lám. 1,fig. 1, lám. 4, fig. 1. 

Malletia {Malletia) chilensis des Moulins, 
Hertlein y Strong, 1940; 421; Bernard, 1983: 
10 

Solenella noms// So we rby I, 1833: 197 (Lo- 



calidad tipo: Valparaíso); Reeve, 1841: 48, 
lám. 30, 4 figs.; Hanley, 1843: 17, fig. 8; Han- 
ley, 1856?; 337; d'Orbigny, 1846; 543; Wood- 
ward, 1851-1856:270, lám. 17, fig. 22; Hupe, 
1854: 306; Deshayes, 1839; 270; 1850: lám. 
34, figs. 5, 6, 7; Hanley, 1860: 164, lám. 226, 
figs. 1, 2 (var. brevlor); Sowerby II, 1870; 
Solenella lám. 1 , figs. 2a, b. 

Material Estudiado 

126 ejemplares (ej) y 53 valvas (v); MZUC. 
Procedencia: (1 ) 23 ej, 4.5-51 mm (No. 4733), 
Bahía de Valparaíso (33 S); fango, 45-100 m. 
(2) 1 ej s, 21 .5 mm, 1 v rota, 1 9 mm (No, 4665) 
M. Ch. I, Est. 49, Chile central (34'56'S; 
72°1 4'W) ; fango, arena, "rocas", 1 50 m. (3) 20 
ej, 12-26 mm, 11 ej s, 11-13 mm, 20 v, 
18.6-25 mm (Nos. 4666, 4667, 4672, 4673), 
M. Ch. I, Est. 51, Chile central (34"36'S; 
72^1 4'W); fango, arena, 50 m. (4) 2 ej s. 31 -39 
mm (No. 4671), Barra Rio Carampague, 
Arauco (37°20'S); arena, 1 m. (5) 15 ej, 6-22 
mm (Nos. 4682, 4686, 4691, 4692, 4694, 
4695, 4697), draga van Veen, Bahía de Con- 
cepción (36 S); fango, 20-27 m. (6) 84 ej, 
9-32 mm, 17 v, 15-16 mm (Nos. 4700, 4702, 
4705, 4707, 4709, 4711, 4713, 4715-4717, 
4719, 4720, 4723, 4724, 4730, 4731), Bahía 
de Concepción (36 S); fango, 10-35 m. (7) 8 
ej s, 18-21 mm (No. 4669), M. Ch. I, Est. 76, 
Chile austral (38'16'S; 73'39'W); fango, 
arena fina, 60 m. (8) 1 ej s, roto, 21 mm (No. 
4668), M. Ch. I. Est. 93, Chile austral (39 '58'S; 
7345'W); fango, arena fina, 86 m. (9) 4 v d, 7 
V i, 21 -26 mm (No. 4670), M. Ch. I, Canal De- 
sertores, Sur de Chile (42 24'S; 72^34'W); 
fango, arena fina, 240 m. (10) 11 ej s, 20-24 
mm, 4 V, 22-25 mm (No. 4563), M. Ch. I, corte 
X-2, Est. 51, Canal Desertores, Sur de Chile 
(42°24'S; 72'=34'W); fango, arena fina, 240 m. 

Descripción 

Concha: Concha de gran tamaño (hasta 51 
mm de longitud), blanca, oblonga, compri- 
mida, entreabierta, delgada, generalmente in- 
equilateral. Márgenes redondeados; el dorsal 
anterior casi recto. Perióstraco de color varia- 
ble: amarillo, verde oliva o pardo, general- 
mente en bandas. Umbos pequeños, ge- 
neralmente erosionados; ápices agudos; 
anteriores en los ejemplares grandes, poste- 
riores en los pequeños. Ornamentación de la 
concha formada por estrías radiales muy 
tenues y escasas en la región anterior, y por 
dos carenas muy débiles en la región poste- 



156 



VILLARROEL & STUARDO 



rior. Ligamento de la misma longitud que la 
serie posterior de dientes. 

Interior de las valvas blanco mate o 
plomizo, algunas veces algo nacarado. Char- 
nela casi recta; con 3 a 7 dientes anteriores 
como nudosidades y 14 a 40 posteriores, 
aguzados: los dientes posteriores cuadripli- 
can en número, a los anteriores. La placa que 
sustenta los dientes anteriores se prolonga 
hasta el nivel del aductor, formando una 
quilla. Línea paleal bien marcada. Seno 
paleal amplio, profundo, sobrepasando al 
umbo; de contorno algo irregular, con el borde 
anterior casi recto; oblicuo con respecto a la 
vertical al eje anteroposterior que pasa por el 
umbo; borde inferior más o menos coales- 
cente con la línea paleal; borde superior ge- 
neralmente interrumpido por la impresión del 
aductor, continuando más allá de ésta. 

Anatomía Interna: Papilas tentaculiformes bí- 
fidas o trífidas, poco numerosas sobre los 
bordes dorso anteriores del manto; hay nu- 
merosos tentáculos ramificados sobre los 
bordes dorso posteriores y posteriores del 
manto. Tentáculo del palpo muy largo, dos 
veces la longitud de la lámina; con un fila- 
mento laminar. Ctenidios pequeños; filamen- 
tos con un poro ventral. Corazón ventral al 
recto; ventrículo globoso. Area de selección 
mayor del estómago con repliegues diver- 
gentes que encierran otra área plegada, per- 
pendicular a los pliegues inferiores. 

Sifones largos, grandes, completamente 
unidos. Tentáculo sifonal ubicado en el lado 
derecho o izquierdo. 



Observaciones 

La comparación anatómica de ejemplares 
provenientes de Valparaíso y Concepción, y 
otros colectados en Valdivia y Chiloé con dife- 
rente coloración del perióstraco, no demostró 
diferencias. Los ejemplares de las muestras 
australes presentan un color pardo oscuro con 
bandas más claras, a diferencia del tono pre- 
dominantemente verdoso encontrado en las 
poblaciones del centro y norte de Chile. 

El mayor tamaño alcanzado por los ejem- 
plares de la Bahía de Concepción fue de 32 
mm, en contraste a los de Bahía de Valparaíso 
que alcanzan un tamaño hasta de 51 mm, 
siendo el mayor tamaño entre las especies es- 
tudiadas. Estas différencias de tamaño y color 
sugieren extremos de variación clinal. 

Ramorino (1968) realizó un estudio de la 



variación de la concha en ejemplares de M. 
chilensisäe Bahía de Valparaíso, donde hace 
ver que las descripciones de Soot-Ryen de 
ejemplares del área de Chiloé asignadas a M. 
inequalis Dalí, 1908a (una especie del Estre- 
cho de Magallanes), no muestran diferencias 
con los de Valparaíso. Aún cuando Ramorino 
no examinó ejemplares de esta especie en 
otras localidades, concluye que M. inequalis 
debería, en consecuencia, ser considerada 
como sinónimo de M. chilensis. 

Abundante material examinado prove- 
niente de Chiloé, y su comparación con pobla- 
ciones de diferentes localidades de la zona 
central y Valparaíso, demuestran que efecti- 
vamente se trata de una sola especie que cor- 
responde a M. chilensis. Sin embargo, la con- 
clusión de Ramorino (basada sólo en la 
identificación de Soot-Ryen) de que esta es- 
pecie es igual a M. inequalis no se justifica, 
mientras no se ilustre y se estudie en detalle el 
tipo de esta última y se compare con muestras 
del Estrecho de Magallanes, la localidad tipo. 
Además, las características dadas por Dalí 
para M. inequalis son diferentes de M. chilen- 
sis como se demuestra en la clave adjunta. 

Es factible, en consecuencia, que en el 
área magallánica existan al menos tres es- 
pecies diferentes; M. inequalis. M. patagó- 
nica, y M. magellanica a menos que la 
primera demuestre ser sinónimo de una de 
las otras dos. Mientras ésto no se com- 
pruebe, sólo se justifica incluir en la sinonimia 
de M. chilensis a M. inequalis Soot-Ryen, 
1959 (non Dalí). 

Malletia magellanica y M. patagónica son 
especies tan diferentes de M. chilensis que no 
puede pensarse en sinonimizarlas con esta úl- 
tima o entre sí. Malletia hyadesi Mabille y 
Rochebrune, 1889. especie también descrita 
del Estrecho de Magallanes, ha sido consi- 
derada como un sinónimo de M. magellanica 
Mabille y Rochebrune por Dalí (1908a) 
(aunque es obvio que se refiere a M. patagó- 
nica de Mabille y Rochebrune) y como sinó- 
nimo de M. patagónica Mabille y Rochebrune 
por Hertlein y Strong (1940); desgraciada- 
mente, sin discusión alguna. Malletia hyadesi 
se diferencia de todas las otras especies, por 
presentar la charnela más corta y por la posi- 
ción de las inserciones musculares (muy 
abajo la anterior y muy anterior la posterior). A 
no ser que se demostrara que se trata de un 
ejemplar anómalo o que las impresiones mus- 
culares han sido dibujadas sólo en parte (pre- 
cisar límites de las impresiones musculares es 
a veces difícil), no se justifica que se identi- 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



157 



fique con M. patagónica. Hasta que ello pueda 
demostrarse, se propone considerarla sólo 
como un probable sinónimo de esta última. 

Distribución Geográfica 

Desde Coquimbo (30'S) hasta el Canal De- 
sertores (42°S). 

Habitat 

Las muestras estudiadas cubren la mayor 
parte del área de dispersión de esta especie 
y fueron colectadas en profundidades que 
varían entre 1 y 240 m, en substrato de fango 
con arena fina. 

Malletia chilensis (al igual que N. (Л/.) pisum 
y N. (S.) cuneata) parece presentar grandes 
diferencias de densidad si se comparan los 
datos publicados por Ramorino (1968) para la 
Bafiía de Valparaíso, con los obtenidos en la 
Bahía de Concepción. En esta última se ob- 
tuvo una densidad de 30 ejemplares/m^ 
(promedio de 7 muestras) en substrato de 
fango entre 20 y 27 m. Este valor es muy in- 
ferior al calculado por Ramorino (1968) entre 
20 y 50 m en la Bahía de Valparaíso que fue 
de 1373 ejemplares/m^, en fondo arenoso 
entre 51 y 80 m de profundidad. En los fondos 
de fango arenoso de la Bahía de Concepción 
no se encontró M. chilensis. 

Malletia patagónica Mabille y 

Rochebrune. 1889 

Fig. 91 

Malletia patagónica Mabille y Rochebrune, 
1889: H 114, lám. 8. fig. 1 (Loe. tipo: Punta 
Arenas); Hertlein y Strong, 1940: 424: Car- 
celles, 1950: 74, lám. 3, fíg. 65; Carcelles y 
Williamson, 1951: 324; Dell, 1964: 148 

? Malletia hyadesl Mabille y Rochebrune, 
1889: H 114, lám. 7, fig. 8 (Loe. tipo: Punta 
Arenas). 

Malletia magallanica Smith (non M. magal- 
lanica [Smith, 1875]), Dali, 1908a: 383 (E. de 
Magallanes). 

Malletia [Malletia) patagónica Mabille y 
Rochebrune, Bernard, 1983; 10. 

Material Estudiado 

1 ej, 33.5 mm (No. 4636), "Hero" 69-5, Est. 
280 A, E. de Magallanes (53 17'18"S; 70°48' 
36"W), fango con muy poca arena, 177 m. 
MZUC. 



Descripción 

Concha: Concha de tamaño mediano (hasta 
42 mm de longitud), elíptica, gruesa, entre- 
abierta, algo comprimida, inequilateral; parte 
posterior más larga, oblicuamente truncada. 
Márgenes redondeados, excepto el dorsal 
posterior que es casi recto. Perióstraco pardo 
amarillento. Umbos conspicuos. Concha sin 
ornamentación. Estrías de crecimiento dis- 
tribuidas irregularmente. Ligamento de la 
misma longitud que la serie de dientes poste- 
riores. Escutelo muy largo. 

Interior de las valvas rosado o blanco con 
manchas amarillas. Charnela corta, con 10 
dientes anteriores y 29 posteriores; los pos- 
teriores triplican en número a los anteriores. 
Línea paleal muy poco marcada: seno paleal 
pequeño, estrecho, con el borde antehor re- 
dondeado, subcircular; borde superior inte- 
rrumpido por la impresión del aductor, conti- 
nuando más allá de éste. 

Anatomía Interna: Borde dorsal posterior del 
manto con tentáculos simples. Tentáculo del 
palpo corto, casi la mitad del tamaño de la 
lámina, originándose en el extremo posterior 
de ella; con un músculo fuerte que lo une a la 
masa visceral: con filamento laminar. Cora- 
zón atravesado por el recto: ventrículo y au- 
rículas muy angostas y aplastadas. Sifones 
pequeños, cortos. Tentáculo sífonal a la 
derecha del sifón. 



Observaciones 

Después de su hallazgo original, esta es- 
pecie fue encontrada por la expedición del 
"Albatross" (Dali, 1908a) en distintos puntos 
del Estrecho de Magallanes, cercanos a la lo- 
calidad tipo. Desgraciadamente, ella fue iden- 
tificada erróneamente por Dalí (1908a) como 
M. magellanica Mabille y Rochebrune. 1889, 
aunque es obvio que en la discusión de esta 
especie se refiere a M. patagónica. Malletia 
magellanica es una especie creada por Smith 
(1 875), y sólo citada, pero no descrita por Ma- 
bille y Rochebrune (1889). También la locali- 
dad original citada por Dalí para M. magella- 
nica es la de M. patagónica. 

Esta especie se diferencia fácilmente de 
las otras presentes en esa zona, por su forma 
elíptica y los bordes dorsales anterior y pos- 
terior casi rectos. 

Es importante hacer resaltar que, además 
de Malletia gigantea Smith, ésta es la única 



158 



VILLARROEL&STUARDO 



otra especie de Malletia conocida en la que el 
corazón es atravesado por el recto. 



Distribución Geográfica 

Estrecho de Magallanes (53^01'S-53°17' 
18"S; 68°13'W-70°48'36"W). 

Habitat 

La muestra estudiada fue obtenida cerca 
de Punta Arenas, la localidad tipo, a una pro- 
fundidad de 177 m en fango, con muy poca 
arena. Con anterioridad, Dalí (1908a) la citó 
del Estrecho de Magallanes entre 56.7 m y 
664.2 m en fondos de arena, fango verde y 
fango de diatomeas. 

Familia Tindariidae Verrill y Bush, 1897 

Diagnosis 

Concha ovalada, robusta; escultura con- 
céntrica, ocasionalmente con líneas radiales; 
placa de la charnela fuerte con dientes en 
forma de "v" invertida bien desarrollados, con- 
tinuos bajo el umbo; umbos grandes, ortogiro 
o prosogiro; ligamento externo, más elongado 
posteriormente que anteriormente; faltan ver- 
daderos sifones; abertura inhalante posterior 
rodeada por papilas alargadas; palpos relati- 
vamente pequeños con pocos surcos; in- 
testino con una vuelta simple a la derecha del 
cuerpo; puede penetrar en el manto (Sanders 
y Allen, 1977). 

Género r/ndará Bel lardi, 1875 

Tindaria Bellardi, 1 875; 28. Especie tipo por 
monotipia; T. arató Bellardi, 1875. (= Deminu- 
cula Iredale, 1931). 

Diagnosis 

Concha pequeña, ovalada, redondeada o 
veneriforme; inflada, gruesa. Sin orna- 
mentación o formada sólo por costillas con- 
céntricas de desarrollo variable. Umbos abul- 
tados; ápices prosogiros. Charnela más o 
menos interrumpida bajo el umbo; dientes de 
la serie posterior muy curvados; la serie ante- 
rior con dientes fuertes, cortos y rectos. Sin 
seno paleal; abertura exhalante formada sólo 
por papilas del borde del manto; con o sin 
sifón inhalante. Palpos grandes. 



Observaciones 

Este género se encuentra representado en 
Chile por T. salaria (Dalí, 1908a) conocida 
sólo frente a las Islas Salas y Gómez, la lo- 
calidad tipo, en 1142 brazas (2055.6 m) de 
profundidad, y por T. virens (Dalí, 1 889), la es- 
pecie aquí tratada. 

Tindaria virens (Dalí, 1890) 
Figs. 52, 54, 55,93-96, 119, 120 

Malletia {Tindaria) virens Dalí, 1890; 254, 
lám. 13, fig. 3 (Loe. tipo; Costa Oeste de 
Chile, 48 9'S-51 52'S, entre 122 y 449 
brazas de profundidad). 

Tindaria virens Dalí, Dalí, 1908a; 389; 
Hertlein y Strong, 1940; 428 (Cit.); Clarke, 
1 961 ; 371 ; Carcelles y Williamson, 1 951 ; 323; 
Bernard, 1983; 11. 

Yoldia (Yoldiella) infrequens Dal I, 1908a: 
219,381. 

Tindaria c\. virens Dall, Linse, 1997; 47 



Material Estudiado 

247 Ejemplares (ej) Y 1 29 valvas (v) ; MZUC 
Procedencia; (1 ) 7 ej s, 1 .9-4.2 mm, 4 v ¡, 5 v 
d, 3-4.3 mm (N. 4597), M. Ch. I, Est. X-3, 
Golfo de Ancud (42 'OO'S; 73 'OO'W); fango, 
arena fina, 264 m. (2) 11 ej, 3.1 -5 mm, 2 ej s., 
4.5-6 mm, 6 v, 5.5-2 mm (Nos. 4611, 4642, 
4660), "Hero" 69-5, Est. 9 (201), Confluencia 
Canales Concepción y Trinidad, (50'9'55"S; 
74 43'25"W); arena, grava, etc., 460 m. (3) 5 
ej, 3.2-4.3 mm, 30 v d, 10 v i, 2-4.4 mm (N. 
4657), "Hero" 69-5, Est. 210, draga Petersen 
0.1 m^. Bahía Corbeta Papudo (50 21'17"S; 
75'17'25"W); fango amarillo verdoso, 70-78 
m. (4) 5 ej, 4 v, 4.2-5.2 mm (No. 4647), "Hero" 
69-5, Est. 56, Puerto Bueno, Canal Sarmiento 
(51"0'50"S; 74 14'10"W); fango, 236 m. (5) 
181 ej, 2.8-5.1 mm, 39 v s, 2.2-5.4 mm (No. 
4650), "Hero" 69-5, Est. 57, Puerto Bueno, 
Canal Sarmiento (51°0'50"S; 74°14' 
1 0"W); fango, 223 m. (6) 30 ej, 3.6 mm, 20 v s, 
2-5.5 mm (No. 4614), "Hero" 69-5, Est. 213, 
Canal Sarmiento (51"27'30"S; 74 3'W); 
fango, 722 m. (7) 6 ej, 2-3 mm, (No. 4637), 
"Hero" 69-5, Est. 243 (26), draga Petersen 0.1 
m^, E. de Magallanes (53 3'S; 71 •33'12"W); 
fango, 151 m. (8) 11 v s, 2-5 mm (No. 4639), 
"Hero" 69-5, Est. 244 (27), draga Petersen 0.1 
m^ E. de Magallanes (53"3'3"S; 71°46' 
36"W); fango, 184 m. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



159 



Descripción 

Concha: Concha pequeña (hasta 6 mm de 
longitud), de contorno triangular, gruesa, in- 
flada; inequilateral, con el lado anterior más 
corto que el posterior; blanca. Perióstraco 
amarillo verdoso a pardo claro, rara vez con 
bandas. Prodisoconcha blanca. Umbos li- 
geramente anteriores, elevados, de ápices 
ortogiros. Márgenes redondeados, excepto el 
dorsal posterior que es oblicuo, casi recto, 
formando un margen posterior angular. Orna- 
mentación de la concha formada por costillas 
concéntricas generalmente muy regulares, 
notorias aun sobre la prodisoconcha. Sin 
lúnula ni escutelo. 

Interior de las valvas blanco, con brillo 
aporcelanado. Charnela acodada con nu- 
merosos dientes en forma de "v" invertida; los 
posteriores (hasta 18) en mayor número que 
los anteriores (hasta 13). Línea paleal difícil- 
mente visible. Impresiones de los aductores 
ovaladas, a veces de tono oscuro; la anterior 
alargada en sentido vertical, de doble tamaño 
que la posterior que es alargada en sentido 
horizontal. No se observan otras impresiones 
musculares. 

Anatomía Interna: Manto de bordes lisos, 
más delgado sobre los sifones. Pie grande, 
fuerte; disco pedal crenulado. Glándula hipo- 
branquial grande, cubre por completo los 
ctenidios. Palpos labiales muy grandes; ten- 
táculo del palpo fuerte, del mismo tamaño 
que los ctenidios. Ctenidios grandes de posi- 
ción horizontal; filamentos subthangulares. 
Corazón ventral al recto. Estómago grande 
con repliegues adicionales al área de selec- 
ción mayor. Intestino relativamente corto (1 
vuelta). Sifones parcialmente unidos en su 
parte interna por un tabique formado por dos 
mitades no fusionadas. Tentáculo del sifón 
pequeño, fino, ubicado más abajo y a la 
derecha del sifón. 

Observaciones 

Clarke (1 961 ) identificó a esta especie en la 
fauna abisal de la Costa del Congo Belga, 
basándose en 1 2 ejemplares obtenidos por el 
"Vema" a 1675 brazas; sin embargo, una 
diferencia encontrada entre éstos y los parati- 
pos de T. virens por él examinados, fue la 
presencia de dientes un poco más fuertes, 
dispahdad que supone de escaso valor taxo- 
nómico. Es de esperar que el estudio ana- 



tómico comparativo de ejemplares de un área 
tan distante al área tipo, logre precisar si se 
trata de la misma especie o no. 



Distribución Geográfica 

Desde el Golfo de Ancud (42°S; 73°W) al 
Estrecho de Magallanes (53''S; 71°46'W). 
Con anterioridad, T. virens era conocida sólo 
de la localidad tipo, costa oeste de Chile 
(48"09'S-51°52'S). 

Habitat 

En las muestras estudiadas esta especie 
se encontró en profundidades de 70 a 460 m, 
en substrato de fango. Su mayor densidad se 
observó en 236 m de profundidad. 

Orden Solemyoida Dalí, 1889 

Paleotaxodontos con charnela sin dientes o 
con dientes taxodontos subumbonales sepa- 
rados de los dientes laterales anteriores por 
un espacio edentado; concha equivalva alar- 
gada anterior o anteroventralmente; huella 
muscular del aductor posterior reducida o 
ausente; perióstraco grueso; branquias 
grandes, anchas, cubriendo todo el cuerpo; 
proboscis del palpo ausente o muy pequeña; 
palpos pequeños, triangulares, sin surcos; 
aparato digestivo simple reducido o ausente 
(Alien y Hannah, 1986; Pojeta, 1988). 

Superfamilia Solemyacea Gray, 1840 

Concha pequeña a grande, entreabierta; 
anterior a anteroventralmente alargada, sin 
dientes; músculo aductor posterior más pe- 
queño que el anterior, con una huella muscu- 
lar arqueada o recta desde el aductor ante- 
rior, indicando la unión del integumento a la 
masa visceral y continúa con las huellas de 
los músculos del pie. Ligamento variable con 
o sin ninfas o condróforos. Con una extensa 
fusión ventral del manto; lumen del tubo di- 
gestivo estrecho o ausente. 

Observaciones 

La inclusión de las familias Solemyidae y 
Acharacidae entre los protobranquios se ha 
basado en la estructura de los ctenidios 
(Pelseneer, 1888, 1911; Yonge, 1939; Сох, 



160 



VILLARROEL & STUARDO 



1959). Sin embargo, Newell (1969) consi- 
derando las grandes diferencias morfológicas 
observadas y la antigüedad de Solemyidae y 
los nuculoideos (Nuculacea y Nuculanacea). 
considera que, aunque ambos grupos han 
ocupado nichos ecológicos similares, no han 
alcanzado paralelismo alguno en la concha. 
Tampoco hay evidencia paleontológica de que 
hayan sido derivados el uno del otro, ni están 
conectados por formas intermedias, aunque 
Alien y Sanders (1 969) y Alien (1 978) han pos- 
tulado un ancestro actinodontiano común. Ro- 
jeta (1 988) ha indicado evidencia de la evolu- 
ción de este grupo a partir de la familia 
"nuculoide" Ctenodontidae. De la misma ma- 
nera Yonge (1939), Purchon (1956), Alien y 
Sanders (1 969) y Alien (1 978) han comentado 
que las similahdades anatómicas de los Sole- 
myidae indican claramente una derivación de 
un tronco común con los nuculoideos (Fig. 
61 ). Allen (1 985) también ha discutido la mor- 
fología más primitiva de los Solemyoidea y 
analizado sus adaptaciones morfológicas a 
los sedimentos blandos, incluyendo el signifi- 
cado funcional de su aparato digestivo muy 
reducido y el papel de las bacterias quimoau- 
totróficas (Felbeck et al., 1981, 1983: Cava- 
naugh, 1983: Reid y Brand, 1986) en los bac- 
teriocitos, similares a los descritos para las 
Calyptogena de las fuentes hidrotermales 
(Fiala-Médioni y Motivier, 1986: Childress et 
al., 1987: Stuardo y Valdovinos, 1988). 

Familia Acharacidae Scarlato y 
Starobogatov, 1979 

Scarlato y Starobogatov (1979) crearon la 
familia Acharacidae y la superfamilia Achara- 
coidea, caracterizándolas por la ausencia 
total de un ligamento interno y un ligamento 
externo reforzado por ninfas. 

Estudios detallados de la anatomía de las 
partes blandas de especies de Acharax 
pueden apoyar o rechazar esta separación. 
Desde el punto de vista de la microestructura 
de la concha y del ligamento. Carter (1990), 
considera al género Acharax dentro de una 
subfamilia Solemyinae: sin embargo, preferi- 
mos seguir a otros autores que consideran a 
Acharacidae una buena familia, mientras no 
hayan mayores contribuciones anatómicas al 
grupo. 

Género Acharax DaW, 1908 

Acharax Dalí, 1908b: 364. Especie tipo por 
designación original: Solemya johnsoni Dalí, 
1908b: 364. 



Diagnosis 

Concha alargada, oval o subrectangular, 
comprimida o circular en sección transversal: 
ligamento opistodético, completamente ex- 
terno: visible internamente sólo donde cruza 
el espacio entre los márgenes de las valvas. 
Ninfas sin reborde de sustentación ("prop") 
[Traducción descripción original]. 

Observaciones 

Dalí (1908b) incluyó en su subgénero 
Acharax a dos especies del Sur de Chile: 
Solemya patagónica Srr\\\b. 1885, y S. macro- 
dactila Mabille y Rochebrune, 1889, su- 
giriendo que la primera parecería ser un 
ejemplar anómalo y que la segunda podría 
ser, en consecuencia, sólo un sinónimo. 

Acharax patagónica (Smith, 1885) fue des- 
crita de la costa oeste de la Patagonia 
(52 45'30": 73 46'W, en 245 brazas = 441 m) 
basado en un único ejemplar, caracterizado 
por un engrosamiento dorsal. Baratiní (1951) 
citó también a esta especie para Uruguay, 
sobre la base de ejemplares procedentes de 
la desembocadura del Río de la Plata: sin em- 
bargo, en un estudio de la fauna uruguaya, 
Figueiras y Sicardi (1968). al refehrse a S. 
patagónica comentan que encontraron en 
esa zona "especímenes de este género que 
indudablemente pertenecen a otra especie." 

Acharax macrodactyla (Mabille y Roche- 
brune, 1889) fue descrita originalmente para 
la Bahía Orange y citada por Dalí (1908b) 
hasta el norte de Chiloé. 

Dell (1 995) quien informa haber examinado 
recientemente material del sur de Su- 
damérica, concluye al igual que Dalí (1908b) 
que Acharax macrodactyla no puede ser 
diferenciada de Acharax patagónica y que 
esta última es muy afín a A. johnsoni (Dalí, 
1891) registrada desde Puget Sound, Wash- 
ington, a Perú. 

En el material estudiado se encontraron 4 
valvas pequeñas y un ejemplar minúsculo de 
una especie no descrita de este género. 

Acharax sp. 
Figs. 6, 9, 13, 131, 132 

Material Estudiado 

1 ej, 2.7 mm, 2 v, 8.1 mm, 2 v, 3,2 mm (No. 
4613), "Hero" 69-5, Est. 213, Canal 
Sarmiento (51 27.5'S: 74 03'W): fango, 722 
m. MZUC. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



161 



Descripción 

Concha: Concha de tamaño muy pequeño 
(Inasta 8.1 mm de longitud), alargada, del- 
gada, lisa, blanca; muy inequilateral. Bordes 
dorsal anterior y ventral paralelos; extremos 
redondeados, el posterior más bajo que el an- 
terior. Perióstraco grueso, de color pardo os- 
curo, con franjas radiales más oscuras, casi 
negras, que nacen del umbo y se prolongan 
en procesos digitiformes más allá del borde 
de la concha, dejando espacios entre ellas, 
equivalentes a su mitad. Las franjas están 
provistas de costillas que se hacen más noto- 
rias hacia el extremo de las digitaciones. (En 
los ejemplares más pequeños, menores de 
2.7 mm de longitud, el perióstraco café muy 
claro no sobresale de los bordes de la con- 
cha, sino que está doblado hacia el intehor de 
ella; las franjas radiales apenas se insinúan y 
la concha es transparente.) 

Umbos en el tercio posterior de la concha, 
poco prominentes; ápices inconspicuos. Liga- 
mento externo, ancho, ubicado muy posterio- 
rmente en una cavidad formada por el borde 
de las valvas. Interior de las valvas blanco, 
opaco, sin ornamentación. Impresiones de 
los aductores desiguales; posterior pequeña, 
ovalada, ubicada bajo el ligamento; impresión 
anterior más grande, alargada, ubicada dor- 
salmente cerca del margen. 

Anatomía Interna: Bordes del manto libres, 
subperiféricos (sin llegar a los bordes de la 
concha); el posterior con 8 lóbulos, de los 
cuales los 3 inferiores son de mayor tamaño 
que el resto. Glándula hipobranquial muy de- 
sarrollada, cubierta totalmente por los cteni- 
dios. Palpo pequeño de forma triangular, sin 
apéndices; su parte ventral posterior (corres- 
pondiente al tentáculo del palpo) como una 
lengüeta corta y ancha. Ctenidios grandes, 
ocupando casi la mitad de la cavidad paleal; 
inequilaterales respecto al eje ctenidial, con la 
parte superior de mayor tamaño que la infe- 
rior. 

Observaciones 

El examen del palpo labial en Acharax sp. 
(Figs. 6, 9, pl), mostró diferencias conside- 
rables con respecto al de Solemya togafa des- 
crito e ilustrado por Yonge (1939), ya que no 
existe el subapéndice del tentáculo del palpo. 
Sin embargo, la falta de este subapéndice en 
Acharax sp. podría deberse a un carácter ju- 
venil, dado el pequeño tamaño del ejemplar 
estudiado. Fue imposible determinar la posi- 



ción exacta del corazón con respecto al recto. 
Parece ser infeñor a él, aunque White (1942) 
describe el ventrículo rodeando al recto en 
Solemya velum Say, del hemisferio Norte. 

Distribución Geográfica 

Canal Sarmiento (51"27.5'S; 74'^03'W). 

Habitat 

Fue encontrada a 722 m de profundidad, 
en un substrato de fango con gran contenido 
de materia orgánica. 

Especie aparentemente escasa. 



SINOPSIS TAXONÓMICA DE LAS 
ESPECIES FÓSILES 

Los representantes más antiguos de los 
protobranquios fósiles encontrados en Chile 
provienen del Paleozoico Superior (Car- 
bonífero-Pérmico); sin embargo, la historia 
geológica de este grupo se remonta práctica- 
mente a los orígenes de los bivalvos, a 
comienzos del Paleozoico. 

Rojeta y Runnegar (1985) han discutido la 
evolución temprana de este grupo (como Pa- 
leotaxodonta), y hacen ver que ya en el Or- 
dovícico se conocen a lo menos tres docenas 
de géneros y cientos de especies. Entre 
otros, los denominados prenucúlidos se han 
encontrado a comienzos del Ordovicico, y 
una de las interpretaciones propuestas (Run- 
negar y Bentley, 1983) han colocado a Poje- 
tala, uno de los primeros bivalvos conocidos, 
con los "paleotaxodontos" prenucúlidos. De 
ser esto correcto, significa que el origen de 
los protobranquios puede trazarse desde el 
Cámbrico temprano al Ordovicico. Tironucula 
tiene dientes tan simples como Pojetala y 
similares impresiones musculares umbonales 
(Morris y Fortey, 1976; Rojeta y Runnegar, 
1985) y se propone que formas como Tironu- 
cula pueden haber sido intermedias entre los 
nuculoides y los actinodontoides (Rojeta, 
1978). 

Pese a que la clasificación supragenérica 
de los "paleotaxodontos" Ordovícicos se en- 
cuentra en revisión, se distinguen dos am- 
plios morfogrupos; (a) aquellos en los que las 
conchas son casi equidimensionales en lon- 
gitud y altura; y (b) aquellos en los que la con- 
cha es significativamente más larga que alta. 
Según Rojeta y Runnegar (1985), estos mor- 
fogrupos muestran, aparentemente, la di- 



162 



VILLARROEL & STUARDO 



vision de los primeros "paleotaxodontos" en 
formas de Wpo-Nucula y de Wpo-Nuculana. En 
opinion de estos autores, hay también con- 
siderable evidencia paleontológica sugiriendo 
que los Solemyidae se derivaron de los "pa- 
leotaxodontos," probabilidad documentada 
por especies del Ordovícico (e.g. Paleosole- 
mya ordovicicus Rojeta y Runnegar, 1985). 
De este modo, la separación de los órdenes 
Nuculoida y Solemyoida, dentro de la sub- 
clase Protobranchia, punto de vista compar- 
tido en este trabajo, parece más probable que 
la separación de los Solemyidae como un 
orden de una subclase Cryptodonta. 

En Chile, sólo los Nuculidae de los géneros 
Nucula y Ennucula están representados por 
especies fósiles. Una única especie asignada 
al género Acila por Tavera (1942) es un 
nomen nudum. 

El número de especies fósiles chilenas 
referidas al género Nucula es muy grande, 
pero sólo un número reducido de ellas han 
sido lo suficientemente bien descritas como 
para permitir su identificación. Entre éstas, al- 
gunas no se han vuelto a encontrar desde su 
descripción y otras pertenecen ahora a 
géneros diferentes. Todas provienen del 
Mesozoico y Cenozoico. 

Especies adscritas con anterioridad al 
género Nucula pertenecen al género Ennu- 
cula si se considera la falta de ornamentación 
radial, margen ventral liso y gran inclinación 
del condróforo. Se trata de especies meso- 
zoicas y cenozoicas. 

Los representantes más antiguos de los 
Nuculanidae pertenecen al Silúrico (De- 
chaseaux, 1952), pero los fósiles chilenos 
asignados a ella provienen del Mesozoico y 
Cenozoico. 

Sólo para los géneros Nuculana. Australo- 
portlandia. Propeleda y Tindariopsis se han 
descrito representantes fósiles chilenos. 

Hay muy pocas especies fósiles referidas 
al género Nuculana (^ Leda) en Chile, 
aunque se conocen muchas citas de es- 
pecies identificadas (pero no descritas) sólo a 
nivel genérico. Por otra parte, se han descrito 
especies de Nucula, que por su forma po- 
drían corresponder a este género, como se 
indica en la lista de nomina dubia. 

Hasta ahora ninguna especie fósil chilena 
parece haber sido asignada al género Pro- 
peleda en la literatura revisada, pero las es- 
pecies de Philippi (1887) Nucula medinae. N. 
darwini, y N. dorbigny pueden ser referidas a 
este género, por poseer un rostro largo y trun- 



cado, condróforo oblicuo y angosto, dirigido 
hacia atrás, y dientes de la charnela casi 
paralelos al borde. De ellas se estudió sólo 
Nucula medinae sobre la base de fragmentos 
de la concha y moldes. 

Kafanov y Savitskii (1 995) en su revisión de 
los taxa de un grupo genérico de la familia 
Nuculanidae registrados en depósitos Ceno- 
zoicos del Pacífico Noroccidental proponen 
incluir a Propeleda Iredale, 1924 (= Lamelli- 
leda Cotton, 1930), en la subfamilia Poroledi- 
nae Scarlato y Starobogatov, 1979, lo cual 
Maxwell (1988) había considerado de valor 
dudoso. 

No se han mencionado especies fósiles 
pertenecientes al género Tindariopsis en la 
literatura consultada, pero es indudable que 
Nucula elegans Hupé, 1854, debe incluirse 
en él. 

De los Yoldiidae se encontró descrita solo 
una especie, Yoldia levitestata Stinnesbeck, 
1987. 

La familia Malletiidae es, sin duda, la de ori- 
gen más reciente entre los protobranquios 
(McAlester, 1964), y está representada por 
especies principalmente Cenozoicas y Re- 
cientes. 

Las especies chilenas fósiles de Malletiidae 
pueden referirse a los géneros Australoneiloy 
Malletia. Las dos especies de este último 
género encontradas en Chile, se incluyen 
aquí en el subgénero Neilo H. Adams y A. 
Adams, 1852, caracterizado por poseer una 
concha con ornamentación concéntrica y 
forma arcoide. Según Hertlein y Strong 
(1940), este subgénero ha sido citado del 
Cretácico Superior al Reciente de la Patago- 
nia, del Helvetiano, Mioceno Inferior de Fran- 
cia y del Oligoceno Superior al Reciente en 
Nueva Zelandia. A esto hay que agregar el 
registro del Mesozoico de Neilo (Neilo) 
quiriquinae Stinnesbeck, 1986, de la Forma- 
ción Quiriquina, Maastrichtiano y los del 
Cenozoico de Chile. 

La familia Solemyidae, que está represen- 
tada en las especies chilenas recientes por el 
género Acharax, se conoce por una sola es- 
pecie fósil incluida con propiedad en el 
género Solemya. 

Se conocen especies de Solemya desde el 
Paleozoico al Reciente (Carbonífero y posi- 
blemente Silúrico a Reciente, según Hertlein 
y Strong, 1940). La única especie chilena 
conocida, fue descrita para el Piso de Navi- 
dad (Mioceno Inferior). 

Por otra parte, esta compilación ha mos- 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



163 



trado también el enorme número de especies 
que, por deficiencias de descripción y figuras, 
se hace necesario considerar como nomina 
dubia y, por ellos, se incluyen con los nu- 
culánidos en igual condición, al final de esta 
sinopsis. 

Las especies que sobre la base de sus des- 
cripciones y figuras pueden ser consideradas 
en el género Nucula. no estaban represen- 
tadas en las colecciones estudiadas. En cada 
caso, se incluye a las referencias bibliográ- 
ficas consultadas, las localidades conocidas y 
el rango estratigráfico. 

Especie Paleozoica 
Nuculana bellistriata Stevens? 

Nuculana bellistriata Stevens, Brüggen, 
1950: 11 (Huentelauquen): Hoffstetter et al., 
1956: 149 (Huentelauquen; NW Prov. Acon- 
cagua 31'40'S y Prov. Coquimbo 31=30'S) 
(Capas de la desembocadura del Choapa, 
Carbonífero Sup. o Pérmico Inf.). 

Especies Mesozoicas 

Pertenecientes al Cretácico según Philippi 
(1887) en su obra sobre fósiles Terciarios y 
Cuartarios donde incluye 161 moluscos del 
Cretácico. 

Nucula ceciliana (d' Orbigny, 1842) 

Mactra ceciliana d' Orbigny, 1 842: 1 26, lám. 
15, figs. 5, 6; 1850: 235: Philippi, 1887: 142, 
lám. 32, fig, 8 (Isla Quinquina). 

Nuculana ceciliana (d' Orbigny), Wiickens, 
1904: 228, 272, 277, lám. 19, fig. 5 
(Quiriquina: 25 ejemplares; Tomé: 100 ejem- 
plares; San Vicente: 6 ejemplares); Tavera, 
1942: 587 (Piso de Quiriquina). Cretácico Su- 
perior. 

Nucula {Leionucula) ceciliana (d' Orbigny), 
Stinnesbeck, 1 986: 1 62, lám. 1 , fig. 1 -3 (For- 
mación Quiriquina, Maastrichtiano). 

Nucula albertina d' Orbigny, 1850: 243; 
Philippi, 1887: 194, lám. 31, fig. 8 (Cretácico 
de Puerto del Hambre (Port Famine), Or- 
ange). 

Nucula apiana Philippi, 1 887: 1 93, lám. 41 , 
fig. 19 (Cretácico de Tumbes). 

Observaciones 

La comparación de las descripciones e ilus- 
traciones de Nucula albertina d'Orbigny y N. 



apicina Philippi demuestran, que éstas son 
sólo sinónimos de N. ceciliana d'Orbigny, co- 
rroborando la conclusión de Wiickens (1904), 
quien comparó un gran número de ejem- 
plares. 

Nucula compressiuscula Philippi, 1899 

Nucula compressiuscula Philippi, 1899: 61 , 
lám. 26, fig. 11 (Portezuelo del Tinguiririca; 
Jurásico Superior-Cretácico Inferior). 

Nucula discors Philippi, 1887 

Nucula discors Philippi, 1 887; 1 89, lám. 41 , 
fig. 23 (Provincia de Arauco). 

Nucula patagónica PhlWppl, 1887 

Nucula patagónica Ph\\\pp\, 1887; 191, lám. 
41 , fig. 8 (Terciario de Santa Cruz, Argentina); 
von Ihering, 1899: 15 (Patagoniano Inferior y 
Medio): Ortmann, 1900: 379; Ortmann, 1902: 
80-82, lám. 25, fig. 7a, b (Desembocadura 
Río Santa Cruz, Lago Pueyrredón, Ar- 
gentina); Fuenzalida, 1942: 412, 413, 423, 
424 (Patagoniano Inferior, Medio y Superior y 
cf. en los Estratos de Boquerón); Tavera, 
1942: 607 (Piso de Navidad en Arauco); Fe- 
ruglio, 1949; 100, 128, 156, 253 (cf. en 
Juliense. Comodoro Rivadavia y Patago- 
niense, Argentina y Chile, Boquerón); Hoff- 
stetter et al., 1 956: 44 (Estratos de Boquerón, 
Eoceno y Paleoceno). 

Nucula tricésima von Ihering, 1897: 243, 
lám. 4, fig. 21, lám. 5, fig. 27. 

Observaciones 

Ortmann (1902) designó como sinónimo de 
esta especie a Nucula tricésima von Ihering, 
1897, del Superpatagónico, sobre la base de 
una serie de 20 ejemplares y un molde in- 
terno. De ellos, uno presenta las característi- 
cas de N. tricésima y otros, más o menos las 
de N. patagónica Philippi, existiendo además, 
una serie de individuos intermedios. 

Fuenzalida (1942), insistió posteriormente 
en las diferencias señaladas por von Ihering 
(1907): mayor altura con relación al ancho 
(espesor o longitud?) en N. tricésima y mayor 
número de dientes en la serie anterior ("pos- 
terior") de la charnela (11 a 13 en Л/. patagó- 
nica y 15 a 17 en Л/. tricésima). No obstante 
estas diferencias, N. tricésima podría repre- 



164 



VILLARROEL & STUARDO 



sentar un sinónimo de N. patagónica, ya que 
las características comparadas por estos au- 
tores varían de acuerdo al tamaño de los 
ejemplares. 



Rango Estratigráfico 



Neocomiano 
(1964). 



(Berriasiano Inferior). Biró 



Nucula oi/a//e/ Philippi, 1887 

Nucula o\/a//e/ Philippi, 1887: 186, lám. 41, 
fig. 12 (Tumbes); Neuman, 1892: 111 
(Tumbes). 

A/ucL//apus/7/a Philippi, 1899 

Nucula pusilla Philippi, 1899: 61 lám. 24, 
fig. 12 (Portezuelo del Tinguiririca); Klohn, 
1960: 52 (cf. Formación Baños del Flaco, en 
el faldeo occidental del Valle Barroso, Prov. 
Santiago. Valanginiano). 

Ennucula ¿nogalis ? (Philippi, 1899) 
(Figs. 140, 141) 

Nucula nogalis Philippi, 1899: 62, lám. 28, 
fig. 9 (Loe. Tipo: Nogales, al N del Agua de los 
Pajaritos). 

Nucula sp. Biró, 1 964: 54 (Lo Valdés, Berri- 
asiano Inferior). 

Material Estudiado 

1 V i, 1 5 mm de longitud, 1 1 .4 mm de altura, 
4 mm espesor, (V/132), Lo Valdés, Prov. de 
Santiago. 1964. Depto. Geociencias Universi- 
dad de Concepción. 

Descripción 

Concha de regular tamaño (15 mm de lon- 
gitud), ovalada, inflada; lado posterior ex- 
tremadamente corto y cóncavo, casi recto: 
anterior largo y convexo. Bordes dorsal y ven- 
tral redondeados. Umbos abultados. Orna- 
mentación de la valva formada por estrías 
concéntricas finas y densas en número de 
6-7 por mm. No existe lúnula ni escutelo. 

Observaciones 

El único ejemplar estudiado, citado por Biró 
(1964) como Nuculasp., es de tamaño menor 
que el descrito por Philippi (1899), y muestra 
alguna diferencia en el contorno de la concha, 
atribuible probablemente a una quebradura 
dorsal. 



Distribución Geográfica 

Nogales (Prov. Aconcagua), Lo Valdés 
(Prov. Santiago). 

Nuculana amuhensis rostrata 
Stinnesbeck, 1986 

Nuculana amuriensis rostrata Stinnesbeck, 
1986: 163, lám. 1, figs. 4-6 (Formación Quin- 
quina, Maastrichtiano). 

Nuculana cuneiformls Stinnesbeck, 1986 

Nuculana cuneiformis Stinnesbeck, 1986: 
164, lám. 1, figs. 7-9 (Formación Quiriquina, 
Maastrichtiano). 



Neilo (Neilo) quiñquinae SWnnesbecK 1986 

Neilo {Neilo) quiriquinae Stinnesbeck, 
1986: 167, lám. 1, figs. 15, 16 (Formación 
Quiriquina, Maastrichtiano). 



Especies Cenozoicas (Terciario) 

Nucula (Nucula) pisum Sowerby I, 1833 

Л/иса/а p/sum Sowerby I, 1833: 198 (Véase 
sinonimia para especie reciente). 

Observaciones 

Nucula (Л/.) pisum. descrita como especie 
reciente, fue citada por Philippi (1887) del Ter- 
ciario de Coquimbo, Caldera, La Cueva, Navi- 
dad, Lebu, Valdivia y Chiloé y del Cuaternaho 
de Mejillones del Sur, Caldera, Coquimbo y 
Cáhuil. Sin embargo, aunque algunas de 
estas localidades han sido estudiadas con 
posterioridad, no se han encontrado otros 
ejemplares de esta especie. 

Nucula semiornata D'Orbigny, 1846 

Nucula semiornata d'Orbigny, 1846: 624, 
lám. 84, figs. 27-29; von Ihering, 1907; Fuen- 
zalida, 1942: 404 (cf. al Terciaho de Maga- 
llanes); Feruglio, 1949: 156, 196, 253 (Pata- 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



165 



goniense, Entrerriense y Actual; Estratos de 
Loreto; Sierra de Carmen Silva); Hoífstetter et 
al., 1956: 202 (Formación Loreto, Oligoceno 
(y/o) Eoceno Sup. ?), Magallanes, 53'7'S). 

Nucula (Leionucula) palmen 
Zinsmeister, 1984 

Nucula [Leionucula) palmen Zinsmeister, 
1984: flg. ЗА, В (Isla Seymour, Antartica, Eo- 
ceno); Stilwell у Zinsmeister, 1992: 47 (Isla 
Seymour, Antartica). 



EnnL/CL//a araucana (Philippi, 1887) 
Figs. 142, 143 

Nucula araucana Philippi, 1887: 191, lám. 
41, figs, 7, 7b (Lebu y ¿Navidad? Terciario); 
Grzybowsky, 1892: 614, 631 (Terciario de Ta- 
lara, Perú); Tavera 1942: 602, 607, 612, 627 
(Piso de Navidad, Mioceno de Arauco); Fen- 
ner y Wenzel, 1942: 1004 (Piso de Navidad); 
Feruglio, 1949: 156, 240, cf. (Tierra del 
Fuego, Magallanes y Navidad); Hoffstetter et 
al. 1956: 306, 243 (Ranquil, Prov. Arauco y 
Navidad); Tavera y Veyl, 1958: 160. 



Material Estudiado 

2 ejemplares (ej), 1 valva (v) y 1 molde in- 
terno (mi). DGUC. Procedencia: (1) 1 ej 12 
mm de longitud, 9 mm altura, 5.8 mm de es- 
pesor, con sólo la capa interna de la concha y 
con una perforación de 1.6 mm de diámetro; 
1 V d, 17 mm de longitud, 13 mm altura, ca. 
8.7 mm de espesor, con su molde interno; 
fragmentos de valvas, una de ellas alcanzaría 
20 mm de longitud. (T/16), Tubul, 24. X. 1969. 
(2) 1 ej ca. 15 mm de longitud, ca. 13 mm al- 
tura, con una perforación de 2.3 mm (T/17), 
Tubul, 11.x. 1970. (3) 1 impresión de una v i, 
17 mm longitud, 12 mm altura, con 21 dientes 
anteriores y 8 posteriores (T/1 8), Tubul, 1 1 . X. 
1970. 



Descripción 

Concha de regular tamaño (hasta 20 mm 
de longitud), triangular. Umbos prominentes. 
Bordes redondeados, excepto el posterior 
que es casi recto, formando un ángulo con el 
margen ventral. Líneas de crecimiento más 
notorias en la región ventral, donde originan 
costillas concéntricas irregularmente dis- 



tribuidas. Lúnula bien delimitada, casi plana; 
escutelo poco notorio. Charnela con 21 dien- 
tes anteriores y 8 posteriores (contados en la 
impresión de una valva de 17 mm de longi- 
tud). 

Observaciones 

Se distingue de E. valdiviana (Philippi, 
1887) y E. lebuensis (Philippi, 1887) por su 
contorno triangular y por el ángulo que forma 
el borde posterior con el borde ventral. 

El ejemplar de "Navidad", descrito por 
Philippi (1887, lám. 41, fig. 7 b), sin medidas 
y que consideró una "variedad", parece co- 
rresponder a un ejemplar de esta especie. 
Este material no se encuentra en las colec- 
ciones existentes en el Museo Nacional de 
Historia Natural, Santiago. 

Distribución Geográfica y 
Rango Estratigráfico 

Ennucula araucana Philippi ha sido encon- 
trada en los afloramientos del Piso de Navi- 
dad, en (Mioceno Inferior) Navidad (Prov. 
Santiago), Arauco, Ranquil, Lebu (Prov. 
Arauco), e Isla Mocha, ¿Tierra del Fuego? 
(Eoceno-Plioceno) (Prov. Magallanes), en los 
afloramientos Plio-Pleistocénicos de Tubul y 
en Talara, Perú (no se especifica Piso). 

Ennucula lebuensis (Philippi, 1887) 
Figs. 138, 139 

Nucula lebuensis Philippi, 1887: 191, lám. 
41, fig. 5 (Loe. tipo: Lebu, Terciario); Tavera, 
1942: 602, 604, 612, 626, 627 (Piso de Navi- 
dad en Arauco y Ranquil y Oligoceno del 
Perú); Fenner y Wenzel, 1942: 1004 (Piso de 
Navidad); Feruglio, 1949: 302: 2: 250 (Navi- 
dense); Hoffstetter et al., 1956:243,245,306. 

Material Estudiado 

(1) 2 moldes internos. 19 mm longitud, 13.7 
mm altura, 8.7 mm espesor; 19 mm longitud, 
14 mm altura, 10 mm espesor (T/1 9), Tubul, 
24.x. 1969. DGUC. 

Descripción 

Concha de regulartamaño (hasta 26 mm de 
longitud), ovalada, ligeramente comprimida; 
muy inequilateral. Bordes redondeados. Al- 



166 



VILLARROEL & STUARDO 



tura del extremo posterior, igual a la mitad de 
la altura máxima de la concha. Umbos poco 
prominentes: ápices aplastados, líneas de 
crecimiento irregularmente distribuidas, débil- 
mente visibles. Lúnula plana, lanceolada. 

Observaciones 

Como lo hiciera notar Philippi (1887) esta 
especie, en comparación a E. valdiviana, se 
caracteriza por su forma elíptica y su extremo 
posterior poco elevado. 

Al igual que en el caso de otras especies, el 
material tipo de Philippi parece haberse per- 
dido y no se encuentra en las colecciones del 
Museo Nacional de Historia Natural, Santiago. 

Distribución Geográfica y 
Rango Estratigráfico 

Piso de Navidad, Mioceno Inferior, en 
Arauco, Ranquil y Lebu: Plio-Pleistoceno de 
Tubul (Prov. de Arauco) y Oligoceno del Perú 
(sin localidad). 

Ennucula valdiviana (Philippi, 1887) 
Figs. 134-137 

Nucula valdiviana Philippi, 1887:190, lám. 
41, fig. 22 (Localidad tipo: Llancahue, Boca 
del Río Rapel, Terciario): Javera, 1942: 619 
(Piso de Navidad). 

Material Estudiado 

1 ejemplar (ej), 4 valvas (v) 1 molde interno 
(mi). DGUC. Procedencia: (1 ) 1 ej, 1 7 mm lon- 
gitud, 10.5 mm altura, 7.2 mm espesor (sólo 
capa interna de la concha), 1 v de 19.5 mm 
longitud, 12.9 mm altura, 1 resto de valva 
(tiene 21 dientes anteriores) (T/13), Tubul, 
24.X.1969.(2)2v, 15.7 mm longitud, 14.2 mm 
altura (T/14) Tubul, 7. X. 1968. (3) 1 v d, 19.5 
mm de longitud, 1 3 mm, dientes anteriores 1 9, 
(MV/1 ), Tubul, 1 0. I. 1 971 . (4) 1 mi de aproxi- 
madamente 1 6 mm de longitud, 1 2 mm altura, 
7 mm espesor (T/15), Tubul, 24.X.1969. 

Descripción 

Concha de regular tamaño (hasta 30 mm 
de longitud), elíptica, débilmente globosa: 
muy inequilateral, en la parte posterior muy 
corta. Bordes redondeados: extremos ante- 
rior y posterior levemente rostrados: la altura 
de este último es casi 2/3 de la altura máxima 
de la concha. Umbos poco prominentes. Or- 



namentación de las valvas formada por finas 
estrías concéntricas y líneas radiales poco 
notorias. Lúnula y escutelo alargado y bien 
delimitados. Serie anterior con 19 dientes en 
un ejemplar de 1 9.5 mm de largo. 

Observaciones 

Esta especie es más o menos frecuente en 
el Plio-Pleistoceno de Tubul. Se la encuentra 
con la concha original bien conservada, en la 
que se distingue la capa de nácar caracterís- 
tica de los Nuculidae. También se encuentra 
en moldes internos. Las líneas radiales no 
fueron descritas por Philippi, pero el resto de 
los caracteres están en perfecta concordan- 
cia con su descripción. 

La característica más notable para diferen- 
ciarla de E. lebuensis, es la relación altura ex- 
tremo posterior/altura máximo de la concha, 
igual a 2/3 en E. valdiviana y a 1/2 en E. 
lebuensis. 

El material estudiado por Philippi no se en- 
cuentra en las colecciones del Museo Nacio- 
nal de Historia Natural, Santiago. 

E. valdiviana es fácil de reconocer por su 
forma alargada. 

Distribución Geográfica y 
Rango Estratigráfico 

Ennucula valdiviana ha sido encontrada en 
los afloramientos del Piso de Navidad (Mio- 
ceno Inferior), Boca del Río Rapel (Prov. de 
Santiago), Tubul (Prov. de Arauco) y Llan- 
cahue (Prov. de Valdivia). 

Nuculana errazür/z/ (Philippi, 1887) 

Nucula errazurizi Philippi, 1887: 189 lám. 
41, fig. 11 (Terciario de Lebu): Fuenzalida, 
1942: 404 (cf. al Terciario de Magallanes). 

Leda errazurizi (Philippi), Ortmann, 1900: 
378: Ortmann, 1902: 84, 85, lám. 26, figs. За, 
b (Desembocadura Río Santa Cruz, Cañón 
cerca Cerro Oveja, Rio Chico, Arroyo Gio, 
Lago Pueyrredón: Argentina); Feruglio, 1949: 
156, (Terciario Tierra del Fuego y Punta Are- 
nas en general) Estratos de Boquerón: Hoff- 
stetter et al., 1956: 44, 222, (Boquerón, Eo- 
ceno (y Paleoceno?) 52''30'-54 S). 

Nuculana oxyrrhyncha (Philippi, 1887) 

Nucula oxyrrhyncha Philippi, 1887: 190 
lám. 41, fig. 21 (Terciario de Lota, Lebu y 
Navidad): Brüggen, 1950: 44 (Algarrobo, 
Lebu, Rumena Quidico, Navidad). 



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167 



Leda oxyrrhyncha (Philippi), Ortmann, 
1900: 378; Ortmann, 1902: 83, lám. 26, figs. 
2a, b (Desembocadura Río Santa Cruz, Ar- 
royo Gio.); Fuenzalida, 1942: 412, 413, 424 
(Patagoniano): Tavera, 1942: 592, 593. 594, 
599, 626, 627 (Piso Boca Lebu, Millongue) 
Oligoceno del Perú): Feruglio, 1949: 156. 
234, 237, 240 (Navidad, Boquerón, Lebu, Mi- 
llongue): Hoffstetter et al., 1956: 40, 44, 95, 
227, 228, 243: Tavera y Veyl, 1958: 160, lám. 
1, fig. 2a (Formación Ranquil en Isla Mocha): 
non Jaworski, in Steinmann 1922: 114, 117, 
lám. 4, figs. 7a-e. 

Observaciones 



tos de concha; 1 mi, 1 5 mm longitud, sólo visi- 
ble dorsalmente; 1 mi 8 mm longitud, 3 mm al- 
tura: 1 mi 1 2 mm longitud, 5 mm altura, (P/1 .), 
Pique Pilpilco, Curanilahue en arenisca dura. 

Descripción 

Concha de regular tamaño (hasta 15 mm 
de longitud) delgada, alargada, comprimida, 
rostrada posteriormente. Bordes redondea- 
dos; dorsal posterior cóncavo. Umbos poco 
abultados. Ornamentación de las valvas for- 
mada por costillas concéntricas finas y den- 
sas, 10 por mm. No hay lúnula ni escutelo. 



La cita de esta especie por Tavera (1942) 
para el Oligoceno del Perú, basada probable- 
mente en Leda oxyrrhyncha Jaworski, 1922, 
es errónea, ya que las figuras de la especie 
de Jaworski son muy diferentes a las de 
Philippi (1 887), y parecen corresponder a otra 
especie. 

Jupitena (Surojupiteria) dissensa Stilwell y 
Zinsmeister, 1992 

Jupitena {Surojupiteria) dissensa Stilwell y 
Zinsmeister, 1992: 48 (Terciario Inferior. Isla 
Seymour, Antartica). 

Australoportlandia antárctica 
Zinsmeister, 1984 

Australoportlandia antárctica Zinsmeister, 
1984: 1504, fig. 3F, G (Formación La Meseta, 
Eoceno, Isla Seymour, Antartica); Stilwell y 
Zinsmeister, 1992: 50 (Formación La Meseta, 
Eoceno, Isla Seymour, Antartica). 

Propeleda medinae (Philippi, 1887) 

Nucula medinae Philippi, 1887: 188, lám. 
41 , fig. 24 (Loe. tipo: Boca del Río Rapel, Ter- 
ciario); Fenner y Wenzel, 1942: 1003 (Punta 
del Fraile y Ranquil, Piso de Navidad; Mi- 
llongue, Piso Millongue, Prov. de Arauco). 

Leda medinae (Philippi), Tavera, 1 942: 595, 
596, 599 (Piso de Millongue); Feruglio, 1949; 
44 (Algarrobo, Rumena Ouidico, Navidad); 
Hoffstetter et al., 1956: 227 (Eoceno de Mi- 
llongue). 

Material Estudiado 

4 moldes internos (mi) y fragmentos de con- 
cha; DGUC. Procedencia: 1 mi, 11 mm longi- 
tud. 5 mm altura; pedazo de mi con fragmen- 



Observaciones 

En el aspecto externo, la semejanza de 
esta especie fósil con la especie reciente an- 
tartica P. longicaudata es notable. 

Distribución Geográfica y 
Rango Estratigráfico 

Propeleda medinae se ha encontrado en 
los afloramientos del Piso de Navidad (Mio- 
ceno Inferior), en Boca del Río Rapel (Prov. 
Santiago), Punta del Fraile y Ranquil (Prov. 
de Arauco), y en el Piso de Millongue (Eoceno 
Superior y parte del Eoceno Medio), en Mi- 
llongue (Prov. Arauco) y en Algarrobo y Ru- 
mena Ouidico (Prov. Santiago). 

Propeleda c/anv/n/ (Philippi, 1887) 

Nucula darwini PblWppl, 1887: 188, lám. 41, 
fig. 17 (Terciario de Lebu); Fenner y Wenzel, 
1942: 1004 (cf. al Piso de Navidad); Feruglio, 
1949: 302; 2: 237, 240, 250 (Fauna de Mi- 
llongue, Piso de Navidad). 

Leda darwini (Philippi), Fenner y Wenzel, 
1942: 1016 (Puente Río Pilpilco, Estero Pata 
Vacas); Hoffstetter et al., 1956: 227, 243 (Mi- 
llongue). 

Propeleda dorbigny (Philippi, 1 887) 

Nucula dorbigny Philippi. 1887: 188, lám. 
41, fig. 10 (Lebu). 

Leda D'Orbigny (Philippi), Fenner y Wen- 
zel, 1942: 1004, 1016 (Piso Millongue en Mi- 
llongue, Puente Río Pilpilco, Estero Pata 
Vacas, Puente Río Trongol, Río Curanilahue). 

Leda D'Orbigny (Philippi), Tavera, 1942: 
526, 596, 599, 626 (Piso Millongue y Oligo- 



168 



VILLARROEL & STUARDO 



ceno del Perú); Hoffstetter et al., 1956: 
227. 

Leda олЬ/длу (Philippi), Feruglio, 1949: 237 
(Millongue). 

Tindariopsis elegans (Hupé, 1 854) 
Figs. 2, 148-156 

Nucula elegans Hupé, 1854: 305, lám. 5, 
fig. 7 (Loe. tipo: Coquimbo, Eoceno): Philippi, 
1887: 189, lám. 31, fig. 6 (Terciario de Tubul); 
Möricke y Steinmann, 1895: 230, 240 (Tubul, 
Coquimbo): Fenner y Wenzel, 1942: 1004 
"var angusta.'' (Piso Navidad): Hoffstetter et 
al., 1956: 84, 243 (Pliocene de Coquimbo. 
Paleoceno-Mioceno de Navidad). 

Leda elegans (Hupé), Tavera, 1942: 614 
(Pliocene y Cuaternario de Arauco): Feruglio, 
1949: 230, 240 (Capas Terciarias de Tubul y 
Piso Navidad). 

Nuculana elegans (Hupé), Frassinetti y Co- 
vacevich, 1995 (Plioceno Superior de Isla 
Guamblín, Archipiélago de los Chonos, Sur 
de Chile). 

Material Estudiado 

137 ejemplares (ej), 736 valvas (v) y 24 
moldes internos (mi); DGUC, Procedencia: 
(1) 13 ej, 5-13 mm, 185 v s, 6-15 mm (T/10), 
Canal Los Patos, Arauco, I. 1964. (2) 3 ej, 
12-13.5 mm. 6 v s, 8-12 mm (T/7) Tubul. 
7.x. 1968. (3) 10 ej, 5-11.5 mm, 40 v s, 5-14 
mm (T/8) Tubul. 7. X. 1968. (4) 4 ej. 4-14 mm. 

20 v s, 9-1 2.5 mm (T/9) Tubul, 1 0.X.1 968. (5) 
5 ej, 10-13 mm, 10 v s, 14.5-11.5 mm (T/2) 
Tubul, 10.x. 1968. (6) 17 V s, 6-10 mm (T/4), 
Tubul, 10.x. 1968. (7) 35 v s, 7-12 mm (T/5) 
10.x. 1968. (8) 9 ej, 7-15 mm, 66 v s, 4-14.5 
mm (T/3) Tubul, 17. X. 1968. (9) 5 ej, 6.3-13.6 
mm, 88 v s, 4.7-14.8 mm (T/8) Tubul, 
24. XI. 1968. (10) 50 ej, 3-13 mm, 216 v s, 
4.7-13.5 mm (T/1) Tubul, 24. X. 1969. (11) 17 
mi, 9-11.5 mm (T/11) Tubul, 24. X. 1969. (12) 

21 ej, 8-13.5 mm, 7 mi, 4-8.5 mm, 70 v s, 
4-13.5 mm (T/12) Tubul, 11. X. 1970. 

Descripción 

Concha de tamaño mediano (hasta 15 mm 
de longitud), gruesa, elíptica, inflada. Umbos 
anteriores con ápices prosogiros. Bordes re- 
dondeados; el dorsal y el ventral posterior 
tienden a ser rectos; extremo posterior trun- 
cado. Ornamentación formada por costillas 
concéntricas sobrepuestas, densas (3.5 por 
mm) y flectadas sobre la carina posterior. 
Lúnula y escutelo débilmente delimitados. 



Seno paleal amplio. Impresiones de los aduc- 
tores desiguales: la anterior redondeada y la 
posterior ovalada. 

Observaciones 

En T. elegans, como en otros bivalvos 
(Waller, 1967), existe gran variación en la 
forma y escultura de las valvas por efecto de 
un mayor o menor grado de abrasión post- 
mortem, antes o después de la fosilización. 
Efectivamente, algunos ejemplares (Figs. 
1 52, 1 54, 1 55) presentan en la región anterior 
sólo costillas concéntricas, sin que se distin- 
gan las costillas sobrepuestas que caracteri- 
zan a esta especie. Otros, (Fig. 153) que han 
sufrido mayor desgaste, exhiben la parte pos- 
terior lisa, dejando ver un surco carinal y ase- 
mejándose a Nucula ambiyrryncha Philippi, 
1887. Sin embargo, algunos individuos (mu- 
estra 1) presentan parte del pehóstraco, que 
se observa plegado, contándose más o me- 
nos 10 finísimos pliegues por costilla de la 
concha. 

El seno paleal de esta especie es poco pro- 
fundo, pero nunca tan angular como el figu- 
rado por Philippi (1887; lám. 31, fig. 6). 

Tindariopsis elegans es uno de los bivalvos 
más abundantes en los estratos de Tubul, 
Arauco, y fue recientemente redescrita del 
Plioceno Superior de Isla Guamblín (44° 
47'45" S; 75" 05'15" W) (Francinetti y Cov- 
acevich, 1995). Parece muy afín a la especie 
reciente T. sulculata en lo que se refiere a la 
ornamentación y forma general, diferencián- 
dose por su rostro más largo y truncado, 
menor convexidad de las valvas, mayor den- 
sidad de costillas concéntricas y mayor am- 
plitud del seno paleal. 

De 137 ejemplares completos y 753 valvas 
examinados, 20 resultaron con perfora- 
ciones, generalmente en el centro de la valva, 
producidas por un depredador. En general, su 
asociación faunística, por la presencia de 
pectínidos, se puede comparar con la aso- 
ciación magallánica actual. 

Distribución Geográfica y 
Rango Estratigráfico 

Ha sido encontrada en los afloramientos 
del Eoceno y Plioceno de Coquimbo (Prov. 
Coquimbo), Paleoceno y Mioceno de Navidad 
(Prov. Santiago), Plioceno y Pleistocene de 
Arauco y Tubul (Prov. Arauco), Plioceno su- 
perior de Isla Guanblín, Archipiélago de los 
Chonos, Sur de Chile. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



169 



Yoldia levitestata Stlnnesbeck, 1986. 

Yoldia levitestata Stinnesbeck, 1986: 165, 
lám. 1, figs. 10, 11 (Formación Quinquina, 
Maastrichtiano). 

Observaciones 

Aparentemente hay sólo dos especies in- 
determinadas referidas a este género, una 
del Pliocene de la Isla Mocha (Tavera y Veyl, 
1958), y la otra, aún de determinación 
genérica dudosa, del Pliocene de Valparaíso 
(Tavera, 1960). 

El género Yoldia, tiene un rango estratigrá- 
fico probable desde el Eoceno al Reciente, 
aunque ha sido citado también del Car- 
bonífero (Hertlein y Strong, 1 940) y del Maas- 
trichtiano. 

Yoldiella leurovata Stilwell y 
Zinsmeister, 1992 

Yoldiella leurovata Stilwell y Zinsmeister, 
1992: 51 (Eoceno tardío de la Formación La 
Meseta, Isla Seymour, Antartica). 

Australoneilo ross/ Zinsmeister, 1984 

Australoneilo rossi Zinsmeister, 1984: 
1 503, figs. ЗН-К (Isla Seymour, Antartica, Eo- 
ceno). Stilwell у Zinsmeister, 1992: 51 

Solenomya antárctica Philippi, 1887 

Solenomya antárctica Philippi, 1887: 179, 
lám. 42, fig. 5 (Loe. tipo: Boca del Río Rapel); 
Tavera, 1942: 602, 626 (Piso Navidad); Fe- 
ruglio, 1949: 241 (Piso Navidad). 

Solemya peteri Zinsmeister, 1 984 

So/emyapeíen Zinsmeister, 1984: 1505, fig. 
3L (Formación La Meseta, Eoceno. Isla Sey- 
mour, Antartica). Stilwell y Zinsmeister, 1992: 
52 (Terciario Inferior Isla Seymour, Antartica). 



Especies Mesozoicas y Cenozoicas 

Nucula {Lelonucula) nova Wiickens, 1991 

Nucula nova Wiickens, 1911:5, lám. 1 , figs. 
4a, 4b, 5 (Mesozoico); Fuenzalida, 1942: 414, 
424 (Terciario Islas Seymour, Patagoniano In- 
ferior); Feruglio, 1949: 156 (Boquerón); Hoff- 
stetter et al., 1956: 44 (Eoceno y Paleoceno 
de Boquerón, región Magallánica). 



Nucula {Lelonucula) nova Wiickens, Zins- 
meister, 1984: 1501, figs. 3C-E (Isla Sey- 
mour, Antartica, Eoceno); Stilwell y Zinsmeis- 
ter, 1992: 47 (Terciario Inferior Isla Seymour, 
Antartica). 

Malletia {Neilo) pencana (Philippi, 1887) 

Nucula pencana Philippi, 1887: 185, lám. 
41 , fig. 5 (Cretácico de Hualpén); Steinmann, 
1892: 111 (Hualpén). 

Malletia pencana (Philippi), Wiickens, 
1904: 230, 269, 272, 278 (Quinquina); Wet- 
zel, 1930: 75; Tavera, 1942: 587, 619 (Piso 
Quiriquina; Pilpilco, Antihuala, Piso de Navi- 
dad); Feruglio, 1949: 266, 303 (Estratos 
Cerro Dorotea); Hoffstetter et al., 1956: 64, 
303 (Estratos Cerro Dorotea, Crét. Sup. 
Maastrichtiano Ultima Esperanza, 51°2'18"S; 
Capas de Quiriquina Crét. Sup. Maastrich- 
tiano). 

Neilo (Neilo) pencana (Philippi), Stinnes- 
beck, 1986: 166 lám. 1 , figs. 12-14. 

Neilo beu/Stilwell y Zinsmeister, 1992 

Neilo beul Stilwell у Zinsmeister, 1992; 52 
(Terciario Inferior Isla Seymour, Antartica). 

Neilo maxwe/// Stilwell у Zinsmeister, 1992 

Neilo maxwelli StWvjeW у Zinsmeister, 1992; 
52 (Terciario Inferior Isla Seymour, Antartica). 

Malletia (Neilo) voickmanni (Ph\\'\pp\, 1887) 
Figs. 144, 145 

Nucula voickmanni. Philippi, 1887: 188, 
lám. 41 , fig. 9 (Loe. tipo: Tubul y Lebu, Tercia- 
rio): Tavera, 1 942: 606, 612 (Piso de Navidad, 
Patagónico y Magallánico); Fuenzalida, 1 942: 
404 (Terciario de Magallanes); Feruglio, 
1949: 156 (Piso Navidad). 

Malletia voickmanni (Philippi), Tavera, 
1942; 602, 604, 612, 619 (Piso Navidad en 
Ránquil); Wiickens, 1904; 278 (Terciario); 
Brüggen, 1950: 45 (Punta del Fraile, Arauco). 

Malletia i/o/c/cmann/ (Philippi), Hoffstetter et 
al., 1956: 243, 245, 306 (Piso de Ránquil, 
Mioceno de Arauco 37'30'S); Feruglio, 1949: 
240 (Terciario de Magallanes). 

Material Estudiado 

1 V d, 46 mm longitud, 24 mm altura (N/1). 
Terciario de Navidad. 15.1.1968. DGUC. De 
esta valva falta la parte ventral posterior y no 
se puede observar su interior, por estar unida 



170 



VILLARROEL & STUARDO 



a una arenisca arcillosa, gris de grano fino, 
bien cementada. 

Descripción 

Concha de gran tamaño (46 mm de longi- 
tud), oval-oblonga, inflada, posteriormente 
algo rostrada. Umbos poco prominentes. Bor- 
des, anterior y dorsal-anterior, redondeados; 
dorsal-posterior y posterior casi rectos, con 
una ligera concavidad. Ornamentación for- 
mada por costillas concéntricas regulares (1 
por mm), que cambian de dirección sobre dos 
carenas débiles que nacen desde el ápice y 
separándose un poco terminan en la unión 
del borde ventral con el posterior; en el área 
comprendida entre estas carenas y el borde 
dorsal posterior, las costas se flectan hacia el 
ápice. Existe un escutelo muy alargado y an- 
gosto que encierra al ligamento. 

Observaciones 

A juzgar por la naturaleza de la roca en la 
que se encontró, M. volckmanni vivía en 
fondo fangoso; las especies actuales de este 
género viven en substrato similar. 

Distribución Geográfica y 
Rango Estratigráfico 

Malletia volckmanni ha sido encontrada en 
los afloramientos del Piso de Navidad (Prov. 
de Santiago) (Mioceno Inferior), Tubul, Rada 
Ranquil, Punta del Fraile (Provincia de 
Arauco), y en los Pisos Patagónico (Ar- 
gentina) y Magallánico, Eoceno-Plioceno 
(Prov. Magallanes). 

OTRAS REFERENCIAS A 
NUCULA y NUCULANA 

(1) Especies fósiles indeterminadas, referi- 
das al género Nucula, han sido mencionadas 
para diferentes niveles estratigráficos por los 
siguientes autores: 

Nucula sp. Steinmann, 1892: 10 (Piso de 
Navidad;¿Quiriquina?). 

Nucula sp. Biese-Nickel, 1942: 443, 460, 
442, (Cretácico al S de Copiapó, Caliza de 
Pabellón alfa 30-35 m. Caliza de Nantoco 
ß 250-300 m. Kinmeridgiano y Neocomiano). 

Nuculasp. Fuenzalida, 1942: 404 (Terciario 
de Magallanes). 

Nucula sp. Fenner y Wenzel, 1942: 1003, 



1004, 1018 (Piso de Navidad, Ranquil, Punta 
del Fraile; Quebrada el Molino, Arauco). 

Nucula sp. Tavera, 1 956: 208 (Cretácico In- 
ferior de Copiapó; Totoralillo; Barremiano-Ap- 
tiano). 

Nucula sp. Segerstróm, 1959: 8 (Hauteri- 
viano Superior, Formación Totoralillo). 

Nucula sp. Galli y Dingman, 1 962: 31 (Piso 
Lotharingiano y Sinemuriano del Liásico, For- 
mación Longacho. Tal vez una especie dis- 
tinta). 

(2) Especies fósiles chilenas indetermi- 
nadas referidas al género Nuculana han sido 
mencionadas para diferentes niveles estrati- 
gráficos por los siguientes autores: 

Nuculana sp. Biese-Nickel, 1942: 442 
(Cretácico Inferior al S de Copiapó, Caliza 
Pabellón alfa 30-35 m). 

Nuculana sp. Tavera, 1942: 599, 602 (Piso 
Millongue y Piso Navidad). 

Nuculana sp. Fenner y Wenzel, 1942: 
1004, 1016 (Lorcura, Terciario carbonífero de 
Arauco, Piso de Navidad). 

Nuculana sp. Tavera, 1956: 208 (Cretácico 
Inferior de Copiapó). 

Nuculana sp. Corvalán, 1959: 47 (Hauteri- 
viano Superior de Vallenar y Barremiano de 
las Ventanas, (28'30'S, 70'^52'W; Chañar 
Quemado, 28^21 'S, 70'52'W). 

Nuculana sp. Segerstróm, 1959a: 9, "una 
nueva especie" (Jurásico Inferior, Formación 
Lautaro, ribera oeste del Río Copiapó). 

Nuculana sp. Segerstróm, 1959b: 8 (Hau- 
teriviano Superior, Formación Totoralillo, To- 
toralillo). 

Nuculana sp. Levi, 1960: 246, "aff. Leda 
sthatlssima Geotsche (La Calera)." 

Nuculanasp. Zinsmeister, 1984: 1504 (For- 
mación La Meseta, Eoceno, Isla Seymour, 
Antartica). 

Nuculana spp. Biró, 1964: 57, 58 (Forma- 
ción Lo Valdés, Titoniano Superior). 

Nomina Dubia 

Las especies que se incluyen en la lista ad- 
junta, no están lo suficientemente bien de- 
scritas ni ilustradas como para permitir pre- 
cisar su posición genérica, y en algunos 
casos, aún su posición a nivel de familia. 

Nuculidae? 

Nucula andina Philippi, 1899: 60, lám. 26, 
fig. 8 (Portezuelo del Tinguiririca). De género 
dudoso. 



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171 



Nucula arcaeformis Philippi, 1887: 187, 
lám. 41, fig. 18 (Cretácico en Hualpén); Stein- 
mann et al., 1892: 111: Wiickens, 1904: 271 
(Piso Quiriquina). Probablemente una Barba- 
tia. 

Nucula? cornuta Philippi, 1887: 186, 1агл. 
41, flg. 20 (Cretácico de Tumbes): Wiickens, 
1904: 271 , 272 (Piso Ouiriquina). De posición 
taxonómica incierta. 

Nucula hualpensisPM\pp\, 1887: 187, lám. 
41, fig. 3 (Cretácico de Hualpén). Podría ser 
Malletiidae. 

Nucula largillierti ö'Orblgny, 1842: 128, lám. 
15, figs. 9, 10; Hupé, 1854: 304; Philippi, 
1887: 187. lám. 31, fig. 7 (Cretácico Isla 
Quiriquina). D'Orbigny, 1846: lám. 5, figs. 5, 6, 
describe aparentemente a esta especie como 
Tellina largillierti. 

Nucula? quisquilla Philippi, 1899: 60, lám. 
24, fig. 9 (Portezuelo de Tinguiririca). No 
parece ser un protobranquio. 

Nucula? quiriquinae Philippi, 1887: 185, 
lám. 41, fig. 6 (Cretácico Isla Ouiriquina); 
Steinmann et al., 1892; 111; Wiickens, 1904: 
271, 272 (Piso Ouiriquina). En apariencia un 
nuculanáceo, pero de posición genéhca 
incierta. 

Nucula subcarinata Philippi, 1899: 59, lám. 
26, fig. 6 (Portezuelo del Tinguiririca). De 
género dudoso. 

Nucula subradiata Philippi, 1899: 59, lám. 
26, fig. 5. Probablemente un nuculanáceo. 
Sin localidad. 

Nucula? tinguiriricana Philippi, 1899: 60, 
lám. 26, fig. 7. Probablemente un nuculaná- 
ceo. Sin localidad. 

Nucula triangula Philippi, 1899: 60, lám. 26, 
fig. 1 (Portezuelo del Tinguiririca). De género 
dudoso. 

Nucula barros! Philippi, 1 887: 191, lám. 41 , 
fig. 14 (Boca Río Rapel); Steinmann et al., 
1892: 23 (Piso Ouiriquina); Wiickens, 1904: 
271. ¿Un venérido? 

Nucula lauta Philippi, 1887: 189, lám. 31, 
fig. 2 (Lebu); Brüggen, 1950: 44. No parece 
un protobranquio. Probablemente pertenezca 
a otro orden. 

Nuculanidae? 

Nucula andina Philippi, 1887: 60, lám. 26, 
fig. 8 (Portezuelo del Tinguirihca). Podría ser 
una Nuculana. 

Nucula angusta Philippi, 1887: 186, lám. 
41, fig. 13 (Cretácico de Algarrobo); Stein- 
mann et al., 1892: 111 (Algarrobo). 



Leda angusta (Philippi), Fuenzalida, 1942: 
412, 413, 423 (Boquerón, Patagoniano, Piso 
Concepción); Renner y Wenzel, 1942; 1004, 
(Arauco); Feruglio, 1949: 156 (Costa austral, 
Seno Skyring, parte superior estratos Bo- 
querón); Hoffstetter et al., 1956: 44 (Estratos 
Boquerón, 52'30'-54-S, Eoceno [y Paleo- 
ceno ?]). De género dudoso; su rango estrati- 
gráfico muy amplio necesita ser revisado. 

Leda minuta Wiikens? non Nuculana minu- 
ta (Müller, 1776), Tavera, 1942: 587, cf. (en 
Pilpilco y Antihuala); Feruglio, 1 949: 301 , 302 
(Senoniano Patagonia austral, Salaman- 
quense del subsuelo de Comodoro Riva- 
davia). Posiblemente una Nuculana. Nucu- 
lana minuta (Müller) es una especie reciente 
de amplia distribución en el hemisferio norte, 
siendo conocida desde el Ártico hasta el 
Canal Inglés y la Bahía de Fundy, en el Atlán- 
tico, y en el Pacífico hasta California y Japón 
(Tebble, 1966). 

Nucula lunularis Philippi, 1899; 62, sin fig. 
(Loe. tipo: Portezuelo del Tinguiririca). Philippi 
(1899), menciona que el único ejemplar 
usado para describir esta especie, se ex- 
travió, razón por la cual no la ilustró. Por la 
descripción original se podría considerar 
como un posible nuculanáceo. 

Nucula ambiyrryncha Philippi, 1887: 190, 
lám. 41, fig. 3 (Terciario de Rapel). Probable- 
mente una Nuculana. 

Nucula sanctaemariae Philippi, 1887: 188, 
lám. 41, fig. 2 (Terciario Isla Santa María); 
Fuenzalida, 1942: 425 (Estero Vitracic, 
Península Brunswick). 

Leda sanctamariae (Philippi), Feruglio, 
1949: 302; 2: 156, 250 (Loreto, Cabo 
Domingo Sunday); Hoffstetter et al., 1956: 
202 (Oligoceno (y/o Eoceno Sup.?), Forma- 
ción Loreto, región Magallánica (51 '30'- 
54 'S). Probablemente una Nuculana. 

Nomina Nuda 

Acila brueggeni Tavera, 1942: 599 (Piso 
Boca Lebu y Piso Millongue); Feruglio, 1949: 
237-239 (Millongue, Prov. Arauco, 37 30'S, 
Eoceno); Hoffstetter et al.. 1956: 227. 

Acila bruggeni Fenner y Wenzel, 1942: 
1016, 1003 (Pino Huacho). No existe de esta 
especie descripción ni figura. 

DISCUSIÓN Y CONCLUSIONES 

La clasificación de la subclase Proto- 
branchia aquí aceptada comprende a las fa- 



172 



VILLARROEL & STUARDO 



milias Nuculidae, Nuculanidae, Siliculidae, 
Sareptidae, Tindariidae y Malletiidae dentro 
del orden Nuculoida y la familia Acharacidae 
dentro del orden Solemyoida. 

Los estudios de McAlester (1964), Knud- 
sen (1970), Allen y Hannah (1986), Maxwell 
(1988), y Coan y Scott (1997), sugieren la 
conveniencia de mantener a la familia Malleti- 
idae separada de Nuculanidae, en la que ha 
sido incluida por otros autores. El presente 
estudio ha intentado corroborar tal sepa- 
ración, basado especialmente sobre carac- 
teres anatómicos de las partes blandas (e.g., 
corazón atravesado por el recto o general- 
mente bajo él; intestino con una sola vuelta). 

De un total de 35 especies recientes des- 
critas y/o citadas para la costa de Chile se 
aceptan 28, de las cuales Propeleda longi- 
caudata era conocida con anterioridad sólo 
de aguas antarticas y Nucula pseudoexigua 
corresponde a una especie nueva. 

Las cuatro especies de Malletiidae acep- 
tadas en este trabajo, podrían corresponder 
quizá sólo a dos, si las diferencias reconoci- 
das para las distintas especies, sobre todo de 
aquellas que no han vuelto a encontrarse 
después de su descripción original, resultan 
ser sólo el resultado de variación o anormali- 
dades. 

Pese a que se ha elevado de rango al taxón 
Tindariopsis Verrill y Bush escrito original- 
mente como subgénero, su posición es 
incierta y podría corresponder solo a un 
sinónimo de Neilonella Dalí. 

La mayoría de los caracteres anatómicos 
de la concha o de las partes blandas conoci- 
dos para los protobranquios es el resultado 
del estudio de sólo algunas especies y no 
existen trabajos en que se analice de manera 
general la relación de los diversos caracteres. 
Su análisis, en el caso de las especies chile- 
nas, nos permite puntualizar las siguientes 
relaciones con las generalizaciones del grupo. 

(1 ) El tamaño de las distintas familias de los 
protobranquios es variable. Los nucúlidos 
vivientes, en general, son más pequeños que 
los nuculanáceos y solemiáceos; el menor 
tamaño adulto conocido, igual a 600 |.i fue 
registrado por Moore (1977) para Condylonu- 
cula cynthiae y se conoce un máximo de 49 a 
50 mm de largo en Acila divaricata (Hinds) del 
Japón. Las especies chilenas no hacen ex- 
cepción a los límites conocidos; por ejemplo, 
el mayor tamaño encontrado fue igual a 20.6 
mm de longitud en Ennuca/a gray/ (d'Orbigny, 
1846). En Nuculanidae y Malletiidae el mayor 



tamaño medido fue de 51 mm de longitud en 
Malletia chilensis, aunque se ha descrito un 
fósil chileno de este mismo género que al- 
canza a 60 mm, y se conoce una especie re- 
ciente de Kerguelen Malletia gigantea (Smith 
1875) que mide 62 mm. 

(2) Se pueden distinguir tres formas bási- 
cas: nuculoide (elevada y corta), nuculanoide 
(elevada y larga) y solemyoide (larga), repre- 
sentadas en las Figuras 1, 3, 131 y 132. Las 
especies asignadas a las distintas familias, 
caen dentro de estas tres formas fundamen- 
tales, con distintos grados de variación adap- 
tativa (Fig. 61). En Solemyacea {Acharax, 
Figs. 131-132; Solemya) la parte anterior del 
umbo es generalmente más larga, al contrario 
de lo que ocurre en Nuculanacea, en donde la 
parte posterior es generalmente igual a (e.g., 
especies de Neilonella) o mayor que la ante- 
rior (e.g., Nuculana. Silicula. Yoldia, Yoldiella, 
Ledella. Malletia. excepto en M. inequalis. 
Figs. 113-130, 133, 144-158). 

(3) No se ha hecho un estudio comparativo 
de la forma y variación de la charnela, dentro 
de cada familia y su evolución ha seguido 
líneas evolutivas diferentes, donde, sin em- 
bargo, el conocimiento alcanzado no permite 
precisar afinidades y divergencias. 

(4) Merece alguna discusión el ligamento 
por la importancia que ha revestido en la 
clasificación de los bivalvos en general, pero 
su estructura en los protobranquios es to- 
davía problemática (Stempell, 1898a; Dalí, 
1908a; Trueman, 1952, 1969; Owen, 1959; 
Waller, 1990). 

Tradicionalmente la posición del ligamento 
se ha descrito: interna en Nuculidae, Siliculi- 
dae y algunos Nuculanidae: parcialmente in- 
terna en algunos Nuculanidae y Malletiidae; 
predominantemente externa en algunos Mal- 
letiidae: externa y/o interna en Tindariidae. 
Pero, esta generalización se complica al con- 
siderar el origen de las dos capas del liga- 
mento descrito por Trueman (1952, 1969) y 
Owen (1959). 

Según Owen (1959), el ligamento de Nu- 
cula y Nuculana está formado por una capa 
externa, denominada también lamelar (divi- 
dida en una capa externa anterior y otra pos- 
terior), conectada con los márgenes del 
manto, y otra interna o fibrosa, conectada por 
el istmo del manto, que corresponde a capas 
similares del ligamento primario de los bi- 
valvos (Yonge, 1957; Trueman, 1969). Esta 
característica puede aplicarse, en general, a 
todos los Nuculidae y Nuculanidae y va 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



173 



acompañada por el desarrollo variable de un 
resilífero o condróforo, que interrumpe a las 
dos series de dientes y está dirigido hacia 
adelante en Nucula y Ennucula (Fig. ЗА, cdr); 
es más o menos recto en Yoldla (Fig. 129) y 
dirigido hacia atrás en Nuculana (Fig. 3). 

En los otros géneros la diferenciación de la 
parte externa e interna del ligamento, es difí- 
cil de precisar macroscópicamente y plantea 
interrogantes difíciles de responder sin estu- 
dios histoquímicos y de microscopía elec- 
trónica (pero véase a Waller, 1990). 

Owen (1 959) describió una estructura simi- 
lar a la de Nucula y Nuculana (con un liga- 
mento considerado de tipo amfidético, alivin- 
cular) en el ligamento de Solemya parkinsoni 
Smith (considerado de tipo opistodético y 
transversal), en la cual, la parte anterior de la 
capa externa se extiende a lo largo de la línea 
charnelar, y la capa interna queda desplazada 
bajo la posterior de la externa (Fig. 3C). Mal- 
letia. presenta según Trueman (1969) un liga- 
mento externo opistodético y parivincular; 
pero, si el ligamento externo observado en 
Malletia fuera similar a la estructura del liga- 
mento en Solemya. podría corresponder al de 
la capa externa del ligamento, lo que signifi- 
caría que la capa externa (el resilium) habría 
desaparecido como lo sugiere Dalí (1 890). Sin 
embargo, McAlester (1 964), basado en Stem- 
pell (1898a), concluye que, en los Malletiidae 
como en los Ctenodontidae fósiles, las áreas 
de inserción del ligamento no muestran esta 
separación de las capas, y por el contrario, 
conservan el tipo más corriente en los bi- 
valvos, en los cuales la capa externa e interna 
están unidas para formar un ligamento ex- 
terno prominente. Desgraciadamente, McAl- 
ester no comenta mayormente el trabajo de 
Stempell, ya que éste no solamente refuta a 
Dalí, sino que demuestra que el ligamento de 
Malletia puede dividirse en tres partes: ante- 
hor, central y posterior, con la central corres- 
pondiendo al resilium (capa interna del liga- 
mento) y la anterior y posterior con un mismo 
origen. De este modo, la equivalencia de la 
diferenciación de las capas del ligamento 
hecha por Owen y Stempell, parece corres- 
ponder exactamente en Nuculidae, Nucu- 
lanidae y Malletiidae, sugiriendo que el 
resilium de posición interna en Nucula y Nu- 
culana, ha emigrado para hacerse externo en 
Malletiidae, sin desaparecer. Un estado inter- 
medio en la posición del resilium se observa 
en Tindariopsis como lo muestra también 
Stempell. 



A diferencia de estos autores Schileyko 
(1983), basado en la observación de series 
morfológicas, considera que ha habido una 
penetración gradual del ligamento externo en 
el espacio entre las dos valvas, lo que ha sido 
acompañado con la formación del resilifer. 
Las razones de este cambio serían: (1) Las 
posibilidades de aumento de volumen de la 
sustancia elástica del resilium más que del 
ligamento externo. (2) El ligamento interno 
proporciona un refuerzo concentrado, en 
cambio el externo distribuye el esfuerzo a 
todo el largo. (3) El ligamento externo impide 
el desarrollo de los umbos y (4) El ligamento 
interno está aislado de la influencia de los fac- 
tores externos negativos y no se lo puede 
dañar sin destruir la concha. 

En el caso de los Solemyoida se han des- 
crito tres posiciones del ligamento: anfidético 
principalmente interno en Solemya. opis- 
todético interno en Petrasma y opistodético 
completamente externo en Acharax. La 
evolución del ligamento en Solemyoida 
parece, en consecuencia, seguir líneas para- 
lelas al de los Nuculoida. 

En una interpretación novedosa y funda- 
mentada sobre la evolución del ligamento en 
los bivalvos. Waller (1990) cuestiona el mo- 
delo anfidético de tres capas del ligamento 
phmaho, aduciendo que éste quizá no era 
así: que las tres capas no necesariamente 
corresponden a las tres capas de la concha y 
que el primer tipo de ligamento fue opis- 
todético. Concluye que en los protobranquios 
el ligamento lamelar no se diferencia en dos 
subcapas como en otras subclases; no pre- 
senta ninguna relación especial a ninguna 
capa externa de la concha (que carece de 
una capa prismática columnar) y, en el hecho, 
es secretado sobre las partes adyacentes de 
ella, pudiendo haberse originado como mate- 
rial de reparación de la concha. En los Nucul- 
idae, el resilium consiste de una parte media 
no calcificada y una parte lateral calcificada. 
La parte media no calcificada es continua en 
sus lados anterior y posterior con el ligamento 
lamelar sin evidencia física de un límite que lo 
separe de las regiones vecinas. Esto llevó a 
Waller (1 990) a postular que el resilium es ya 
sea ligamento primario o que ha invadido se- 
cundariamente la región central. 

De estos sistemas más simples de liga- 
mento presentes en todos los Protobranchia, 
salvo por los Solemyidae, se habrían origi- 
nado dos tipos principales de ligamento pre- 
sentes en los bivalvos actuales. 



174 



VILLARROEL&STUARDO 



(5) La variación en el número y forma de los 
dientes en Nuculoidea no permite utilizarlos 
como caracteres de valor genérico o supra- 
genérico, ya que varía considerablemente 
con el crecimiento en una misma especie y 
aún en individuos del mismo tamaño; aunque 
conservando constante la relación: número 
de dientes anteriores/número de dientes pos- 
teriores (Savitskii, 1969a). Sin embargo, la 
forma y el tamaño de los dientes presentan a 
menudo valor específico, como lo han hecho 
notar algunos autores (Knudsen, 1970: Villa- 
rroel, 1971). 

(6) Los palpos son muy semejantes en los 
Nuculacea y Nuculanacea. pero su homología 
con los Solemyidae aun no se conoce bien. En 
Solemya se interpretan como apéndices del 
palpo no pareados de los otros protobran- 
quios, y las láminas estarían reducidas a sim- 
ples lomos (Fig. 11) en los bordes del surco 
que une a la boca con estos apéndices (Figs. 
15-17) (Ridewood, 1903: Morse, 1913: 
Yonge, 1939: Reid, 1980). 

El apéndice o tentáculo del palpo sobre la 
lámina externa de cada uno de los palpos, 
considerado por Drew (1901) equivalente de 
un par de repliegues hipertrofiados (Figs. 10, 
1 2, y siguientes, tp) cambia su posición según 
la familia (Fig. 61). En los Nuculanacea, el 
apéndice del palpo está ubicado sobre la por- 
ción terminal de la lámela externa del palpo 
(e.g., Fig. 5, Silicula rouchi: Fig, 77, Nuculana 
(S.) cunéala: Fig. 90, Nuculana {B.) inaequis- 
culpta). En cambio en los Nuculidae está des- 
plazado al extremo, ya que detrás de él hay 
una estructura adicional, no extensible, de- 
nominada "ciego del palpo," que según 
Stasek (1965) también representa un par de 
repliegues hipertrofiados. 

El apéndice del palpo se une en su extremo 
proximal con la superficie externa de la 
lámina del palpo y con el ciego del palpo (Fig. 
10, bp): su musculatura pasa a fusionarse 
con el retractor posterior del pie. Estas obser- 
vaciones efectuadas inicialmente en Adía por 
Stasek (1961) fueron corroboradas, sin ex- 
cepción, en cada una de las especies aquí 
estudiadas. Sin embargo, en la mayoría de 
los casos, los apéndices se encontraron en 
distintos grados de contracción, impidiendo 
establecer diferencias específicas (Figs. 4 y 
62, 74 y 76, tp). 

(7) De las estructuras internas estudiadas, 
sólo estómago e intestino, la posición del 
corazón y los sifones permiten extrapolar 
conclusiones generalizabas al grupo. 

Aunque la morfología del estómago ha sido 



descrita en detalle para especies de Nucula, 
Nuculanay Malletia (Stempell, 1898a: Health, 
1937: Yonge, 1939: Graham, 1949: Owen, 
1956: Purchon, 1956), se hace necesaria una 
descripción comparativa de los Nuculacea y 
Nuculanacea sobre la base de las especies 
estudiadas. Esta comparación incluye la iden- 
tificación de una estructura nueva (ciego pos- 
terior), y cambios en la interpretación de las 
estructuras observadas por autores prece- 
dentes, a los que hemos tratado de designar, 
siguiendo la nomenclatura más usada. 

El tamaño y apariencia externa del estó- 
mago es similar en Nuculacea y Nucu- 
lanacea, pero en Solemyacea es extraordi- 
nariamente pequeño, apenas una dilatación 
(Yonge, 1939: Owen, 1961; Purchon, 1987b) 
(Figs. 13, 18-56) o puede faltar (Reid, 1980, 
en Solemya sp.). Su posición, que se aprecia 
mejor en las Figuras 13, 14, 71 y 79, varía 
como lo hiciera ver Yonge, por efecto de una 
mayor o menor extensión del pie en el mo- 
mento de fijar al animal. La separación de 
este órgano del resto del cuerpo es relativa- 
mente fácil en este grupo (excepto en los 
Solemyidae), porque a diferencia de los fili- 
branquios y eulamelibranquios, está fijo débil- 
mente a los órganos y tejidos adyacentes, lo 
que Yonge (1939) interpreta como resultado 
de la acción de thturación muscular que debe 
realizar el estómago. 

La estructura del estómago en Nuculacea y 
Nuculanacea ha sido dividida en una región 
superior, glandular, llamada estómago propia- 
mente tal y una región alargada que se ex- 
tiende ventralmente en el pie, denominado 
saco del estilo (Figs. 1 8-56, se). Según Yonge 
(1939), Graham (1949), y Purchon (1956), 
esta parte es homologa con el saco del estilo 
de los otros bivalvos. 

La estructura del estómago en los Solemy- 
acea, posee los caracteres normales internos 
básicos, incluyendo un capuchón dorsal y un 
escudo gástrico (Owen, 1961). Yonge (1939: 
fig. 38) ha diferenciado interiormente tres re- 
giones, las que no nos fue posible observar 
en Acharax {F\g. 13, est.), debido al pequeño 
tamaño del ejemplar estudiado. 

Purchon (1956, 1959) caracterizó el estó- 
mago de todos los protobranquios como 
pertenecientes a un único tipo denominado 
por él "tipo de estómago 1 o Gastroproteia." El 
examen de este órgano en las especies chile- 
nas y antarticas estudiadas permite concluir 
que no existe sólo un tipo básico de estómago, 
sino que éste puede subdividirse de acuerdo 
a las ilustraciones de la Figura 60. Aceptando 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



175 



las relaciones que guardan entre si los tipos 
de estómagos encontrados o descritos en la 
literatura pertinente, y que la familia Nucinelli- 
dae forma parte de los protobranquios como lo 
demuestran Alien y Sanders (1 969) es posible 
distinguir al menos tres tipos básicos: 

Tipo la. Común a los géneros de Nucula y 
Ennucula (Nuculidae) y caracterizado por 
varias áreas de selección (tres a cuatro) y una 
gran extensión del tiflosol menor. 

Tipo Ib. Común a los géneros de Nucu- 
lanidae y Malletiidae y caracterizado por tres 
áreas de selección y una pequeña extensión 
del tiflosol menor. 

Tipo le. Común a los géneros de Solemyi- 
dae y Nucinellidae y caracterizado por la 
ausencia de áreas de selección distintas y 
ausencia de tiflosoles. 

La diferenciación de las partes reconocidas 
interna y externamente en Nuculacea y Nu- 
culanacea, no es difícil y como ha sido indi- 
cado por diversos autores para otras es- 
pecies, en las aquí estudiadas el estómago 
propiamente tal presenta regiones pardo os- 
curas externamente lisas (quitinosas, verde 
oscuro en preparaciones) y otras claras, 
amarillas, entre las anteriores, ambas fácil- 
mente distinguibles. La entrada del esófago 
está ubicada anteriormente y un poco hacia la 
izquierda en Nuculacea, y dorsoanterior- 
mente en Nuculanacea. 

En Nuculidae el estómago presenta dor- 
salmente un capuchón, que muestra en su in- 
terior dos pliegues (lomos) longitudinales, y 
se curva hacia la izquierda terminando en un 
ciego digitiforme (Figs. 20-32, cd). En Nucu- 
lanacea, este capuchón es pequeño y está 
ubicado dorsalmente a la izquierda (Figs. 33- 
56, cd). AI igual que en Nuculidae es recorrido 
por dos pliegues (lomos) que están situados 
transversalmente. 

Los tres conductos (Fig. 18-56; dd, o dd\ 
dd^, dd^) que comunican al estómago con los 
divertículos digestivos que lo rodean, entran 
uno por la izquierda (dd^) y dos por la derecha 
(dd\ dd^), Dos de ellos (dd^ y dd^) están en 
comunicación con la masa izquierda de los di- 
vertículos, y el tercero (dd'^), con la masa de 
divertículos del lado derecho, como puede 
observarse en los esquemas adjuntos. La 
posición de estos conductos es diferente en 
Nuculacea y Nuculanacea. En los primeros, 
los orificios de los conductos dd^ y dd^ se ubi- 
can más o menos simétricamente a los lados 
o bajo la entrada del esófago, sobre áreas 
planas (Figs. 18-32). En Nuculanacea, en 
cambio, el conducto dd^ se encuentra ubi- 



cado generalmente sobre un surco, bajo la 
entrada del esófago (Figs. 33-56), y los otros 
dos (dd^ y dd^), se abren sobre surcos que 
corren entre pliegues, dirigidos hacia el esó- 
fago en un bolsillo denominado as"* (Figs. 36, 
41,44). 

Las denominadas áreas de selección del 
estómago, son igualmente importantes en la 
diferenciación taxonómica de los Nuculacea y 
Nuculanacea. El área de selección mayor as, 
presente en Nuculacea y Nuculanacea, des- 
crita por Graham (1949) en Nucula hanleyi, 
mostró en el material estudiado variaciones 
interespecíficas en cuanto al número de 
repliegues y a la orientación de éstos. 

La variación observada en el número y 
tamaño de los repliegues, en Nucula y Ennu- 
cula (Nuculacea), se representa en las Figu- 
ras 18-31. En las figuras siguientes (Figs. 
32-56), se muestra la variación en los Nucula- 
nacea, cuyos pliegues aparecen de tamaño 
mucho mayor y con orientaciones distintas. 
Sin embargo, no parece haber modelos que 
representen a todas las especies de un gé- 
nero (compare Figs. 37, 38 y Figs. 42, 43 ilus- 
trando a dos especies distintas de Nuculana). 

Después de Graham (1949), Purchon 
(1956) describió en Nucula nucleus (Linné, 
1758), tres áreas adicionales denominadas 
as\ as^ y as"^, que pueden o no estar pre- 
sentes en las distintas especies. En conse- 
cuencia, la presencia y distribución de dichas 
áreas también parece servir como un buen 
carácter específico. Así por ejemplo, as^ se 
encontró sólo en Nucula (Nucula) pisum (Fig. 
21 ) y en Ennucula puelcha (Figs. 29-31 ) y no 
en las otras especies estudiadas de este 
género; as^ se encontró presentando dife- 
rente tamaño en Nucula (Nucula) pisum. Nu- 
cula (Nucula) fernandensis y Ennucula 
puelcha. siendo mayor en esta última. En 
cambio, as'^, no se observó en ninguna de las 
especies de Nuculanacea estudiadas. 

En una posición que corresponde a esta úl- 
tima área de selección (as^), existe un gran 
saco (ciego), de posición dorsal a la región de 
selección mayor "as", sin repliegues en su in- 
terior, cuyo extremo se dirige posteriormente 
a la izquierda, Villarroel (1971) describió este 
ciego en Nucula (Nucula) fernandensis (Figs. 
23-26, cp). Se encuentra también en Nucula 
(Nucula) pseudoexigua, sp. nov., y Nucula 
(Nucula) falklandica (Figs. 18-20 y 27-28, 
cp). 

Purchon (1956) describió también un área 
plegada en Nucula nucleus Linné, que Owen 
(1956: fig. 2) denominó tracto de expulsión 



176 



VILLARROEL & STUARDO 



("rejection tract") en Nucula sulcata Bronn. 
Esta área fue descrita, además, en Nucula la- 
yardi por Dinamani (1967: fig. 1) pero no fue 
encontrada por Graham (1949) en Nucula 
hanleyi Winckwortli. En el caso de las es- 
pecies chilenas se observó en Nucula (Nu- 
cula) fernandensis y Ennucula puelcha (Figs. 
26, 32, api), pero no se encontró en Nucula 
{Nucula) pisum, o Nucula (Nucula) pseudo- 
exigua, sp. nov. 

En los nuculanáceos estudiados, no exis- 
ten las áreas as\ as^, as^, pero en cambio se 
encuentra también en el tracto de expulsión 
un área selectiva adicional denominada "as"*" 
por Purchon (1956: fig. 3 de Nuculana minuta 
[Müller]), considerada con anteriohdad por 
Yonge (1 939) como un ciego (Figs. 36, 41 , 42, 
49, 50, api, as4). Según Purchon (1956). 
estas áreas pueden haberse derivado de un 
área de selección, pero no tendrían en la ac- 
tualidad función selectiva. 

Aparte de las áreas ya descritas, se encon- 
tró una aparente área de selección pequeña 
en Malletia chilensis y Propeleda longicau- 
data {F\gs. 36, 50. 56, as?). 

Las diferencias indicadas existentes entre 
los estómagos de Nuculacea y Nuculanacea 
no apoyan la generalización de Purchon 
(1987b) de que son básicamente compara- 
bles y que una sola deschpción puede englo- 
barlos (Fig. 60). 

Además de las áreas de selección, y de 
aquellas ya descritas en que se abren los 
conductos de los divertículos digestivos, en el 
interior del estómago existe una tercera parte, 
revestida por una pared quitinosa que deja 
libre sólo las áreas de selección, y un surco 
que une el estómago con el saco del estilo. 

La pared quitinosa forma un amplio cinturón 
alrededor del estómago, y presenta su mayor 
complejidad en Propeleda y Malletia. donde 
se observan modificaciones pectinadas cerca 
del área de selección mayor (as), y dientes en 
el escudo (Figs. 36, 56, dq y deg). 

Es indudable que la complejidad del es- 
cudo gástrico es mayor en Nuculanacea que 
en Nuculidae y Solemyidae, pero en la actua- 
lidad, es difícil juzgar su valor como carácter 
de diferenciación genérica o específica. 
Según Yonge (1939), el escudo de los proto- 
branquios sería homólogo con el de los otros 
moluscos. 

La parte inferior del estómago o saco del 
estilo en Nuculacea y Nuculanacea, longitud 
y diámetro que alcanza en algunos géneros. 
Es indudablemente más largo en Yoldia (Fig. 
44) que, por ejemplo, en Silicula (Fig. 48), Nu- 



culana (Figs. 37, 42), Malletia (Fig. 50) y Tin- 
darla (Figs. 52, 55); y entre los nucúlidos, más 
largo en Ennucula (Fig. 29) que en Nucula 
(Figs. 18-28). Hay dos repliegues ciliados o 
tifíeseles a lo largo de la pared anterior del 
saco del estilo, que dejan entre ellos el lla- 
mado "surco intestinal." Los dos tiflosoles 
fueron denominados originalmente tiflosol 
mayor y tiflosol menor por Graham (1949), 
nombres que continuaron siendo utilizados 
por Owen (1956) y Purchon (1956), aunque 
parte del tiflosol menor ha sido denominado 
también "pliegue derecho" (right fold, Owen, 
1956) y "lomo о reborde longitudinal" (longitu- 
dinal ridge, Purchon, 1956). 

Ventralmente, en la unión del saco del es- 
tilo con el intestino, ambos tiflosoles dan ori- 
gen a numerosos repliegues longitudinales 
que corren a lo largo de este último (Fig. 73, 
im). Su número varía específicamente, como 
se pudo constatar en las especies estudiadas 
de Nucula y Ennucula. 

Al llegar al estómago ambos tiflosoles se 
separan. En Nuculacea, el tiflosol menor se 
dirige hacia atrás y rodea gran parte del área 
de selección mayor, pudiendo terminar en el 
lado derecho cerca de la abertura esofágica, 
como ocurre en Ennucula puelcha (Fig. 32, 
tme), Nucula nuc/eus (Linné, 1758) (Purchon, 
1956: fig. 2) y en Nucula /7an/ey/ Winckworth 
(Graham, 1949: fig. 8); о seguir por sobre la 
abertura esofágica y entrar en el capuchón 
dorsal, en Nucula {Nucula) fernandensis (Fig. 
26), Nucula sulcata Bronn (Purchon, 1956) y 
Nucula layardi {D'\narr\an\, 1967: fig. 1). 

Dinamani (1967) ha sugerido que la exten- 
sión de este tiflosol hasta el capuchón dorsal 
representaría una modificación única en los 
Nuculacea, ya que podría también conside- 
rarse que dicho tiflosol está interrumpido por 
el repliegue que divide las dos partes del es- 
tómago, haciendo terminar el tiflosol dentro 
del saco del estilo mismo y no en el capuchón 
dorsal. De acuerdo con ésto, el lomo que se 
extiende en el estómago sería sólo una parte 
del pliegue que nace del capuchón dorsal. 
Desgraciadamente, este autor no hizo co- 
mentarios con respecto al recorrido del tiflosol 
menor en Nuculanacea. En este grupo, a 
diferencia de Nuculacea, no circunda el área 
de selección posteriormente, sino que sólo 
parcialmente en la parte anterior, acom- 
pañando al surco intestinal como se ha ob- 
servado en Propeleda longicaudata y Malletia 
chilensis (Figs. 36, 56, tme), y como lo ilus- 
trara Purchon (1956: fig. 3) en Nuculana mi- 
nuta (Müller). 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



177 



(8) De interés ha resultado la observación 
del número de vueltas en los denominados in- 
testino gástrico y medio de diversas especies 
y sus interpretaciones. 

Según Yonge (1939), la porción correspon- 
diente al intestino gástrico se extiende en la 
base del pie, por lo que cuando éste es pro- 
yectado hacia afuera se estiraría formando 
una sola vuelta. 

Las vueltas en esta región del intestino 
fueron consideradas por Yonge (1939) carac- 
terísticas de la familia Nuculanidae, como 
consecuencia de una mayor actividad; sin 
embargo, ellas se encuentran también en Nu- 
culidae, como ocurre en Nucula (Nucula) fer- 
nandensis y Ennucula puelcha entre las es- 
pecies aquí estudiadas (Figs. 24, 30). Si la 
función postulada por Yonge es correcta, este 
carácter indicaría que las especies nom- 
bradas son también muy activas, aunque 
como se argumenta a continuación, hasta 
este momento es más cauto sugerir sola- 
mente que este carácter se encuentra pre- 
sente en algunas especies de las dos fami- 
lias, sin precisar una función determinada. 

Desde la base del pie, el intestino corre 
dorsalmente a la pared dorsal del estómago y 
luego se vuelve anteriormente. El intestino 
medio es de diámetro variable y presenta un 
patrón de ordenación de sus vueltas especí- 
fico (Heath, 1 937: figs. 2, 3, 6, 8, y siguientes), 
con una variación intraespecífica aparente- 
mente mínima en las especies estudiadas 
(e.g. Nucula {Nucula) pisum). Comienza so- 
bre o junto al estómago, y se continúa anteri- 
ormente en algunas especies, hasta alcanzar 
cerca de la boca. Luego, pasa dorsalmente a 
corta distancia del esófago, y continúa por 
sobre el estómago a la parte dorsal posterior 
del cuerpo, o bien, se vuelve ventralmente 
para formar las vueltas ya mencionadas. 

Heath (1937) fue el primero en demostrar 
que en los Nuculacea el intestino no se ex- 
tiende tan adelante como en Nuculanacea, lo 
que el considera una condición primitiva. 
Describió el número de vueltas en varias es- 
pecies de Nucula y Acila, asociando un tipo 
simple de pocas vueltas con aguas someras, 
y el enrollamiento más complejo como típico 
de animales que viven a grandes profundi- 
dades. 

Un número elevado de vueltas se observó 
también en las especies chilenas estudiadas 
de Nucula y Ennucula, aunque no existe 
ninguna relación con la profundidad; ha sido 
mencionado por Knudsen (1970) en nu- 
merosas especies abisales de los géneros 



Nucula. Ennucula y Brevinucula. Además, 
este autor describe especies de algunos 
géneros de la familia Nuculanidae que pre- 
sentan, también, un número elevado de 
vueltas. Así, ocurre en especies de Spinula 
con 1 , 6 y 7 vueltas, de Ledella con 1 , 4 y 5 
vueltas y de Phaseolus con dos vueltas. 

En consecuencia, parecería que en Nucu- 
lanidae hay dos tendencias, una que corres- 
ponde a un enrollamiento acentuado en es- 
pecies de los géneros ya mencionados 
(¿tendencia paralela a Nuculidae?); y la otra, 
representada especialmente por los géneros 
Nuculana, Propeleda. Yoldia y Yoldiella, con 
especies en la que existe una sola vuelta; 
¿cual es especializada y cual primitiva? 

Los géneros Neilonella. lindarla, Tindari- 
opsls y Malletia presentan siempre una sola 
vuelta. En estos grupos tampoco existe una 
relación de un mayor número de vueltas con 
la profundidad. 

Schileyko (1989) después de revisar 
muchas especies de aguas someras y abi- 
sales llega a la conclusión que el alarga- 
miento del intestino, que se da indistinta- 
mente en varias familias de protobranquios, 
se debe más bien a la calidad de las partícu- 
las útiles a la alimentación que a la profundi- 
dad. Encontró que las especies presentes en 
la fosa Kurilo-Kamchatka, donde existe abun- 
dancia de sustancias nutritivas, no presentan 
el intestino alargado. Esto explicaría el por 
qué Nucula (Nucula) fernandensis, que vive 
en fondos arenosos, con pocas sustancias 
nutritivas, tenga un intestino más largo que 
las otras Nucula estudiadas, cuyos habitats 
son más nutritivos (limo-arcilla). 

Schileyko (1989) agrupa a los protobran- 
quios en seis grupos de variantes de la 
topografía del intestino: 

(a) Se conserva una vuelta en el lado dere- 
cho del cuerpo (Schileyko, 1989: fig. 8, Nu- 
cula tenuis) 

(b) Se conserva una vuelta en el lado dere- 
cho del cuerpo, pero la vuelta se alarga 
muchísimo. Algunas veces penetra en la hoja 
derecha del manto (algunos Tindariidae) 
(Schileyko, 1989: fig. 8, Tindaria callisti- 
formis). 

(c) Se conserva la disposición del intestino 
en el lado derecho, pero el número de vueltas 
aumenta hasta 5-11 (Ledellidae, en parte) 
(Schileyko, 1989: fig. 8, Bathyspinula oceá- 
nica). Nucula próxima, de 10 m de profundi- 
dad, tiene tres vueltas; la especie cercana N. 
cancellata de 3834 m de profundidad tiene 
ocho vueltas (Alien, 1978: fig. 10). En esta 



178 



VILLARROEL & STUARDO 



misma publicación Allen menciona las mis- 
mas relaciones dentro del género Yoldiella, 
pero representa (Alien, 1978: fig. 11) dife- 
rentes géneros; el género Yoldiella perte- 
nece, probablemente, al Yoldiella sp. L, pero 
V^ sp. К se debe trasladar a otro género (Ob- 
servación hecha por Schileyko, 1986, en 
Schileyko, 1989). 

(d) Las vueltas (una o unas) se encuentran 
tanto a la derecha como a la izquierda y se 
pasan de un lado a otro por detrás del estó- 
mago (Pristigloma nitens, Pseudotindaria, 
Ledellina) (Schileyko, 1989: fig. 8, Ledellina 
olivácea). 

(e) Todas las vueltas se enrrollan casi hori- 
zontalmente encima del estómago (Pristi- 
gloma alba, Microgloma) o alrededor de él 
{Setigloma) (Schileyko, 1989: fig. 8, Seti- 
gloma japónica). 

(f) Las vueltas se emplazan en diferentes 
superficies sin ninguna predominancia a la 
derecha o a la izquierda (Lametilidae) (Schi- 
leyko, 1 989: fig. 8, Lametila abyssorum [como 
"Lametyla"]. no la de Alien y Sanders, 1973: 
fig. 33). 

De estas seis variaciones propuestas por 
Schileyko (1989) en las especies chilenas se 
presentaron solo las tres primeras: (1) Con 
una vuelta en el lado derecho en: Silicula 
rouchi {F\g. 14); Nuculana (S.) cunéala (Figs. 
78, 79); Tindariopsis sulculata (Figs. 81, 82); 
Yoldiella ecaudata (Fig. 84); Yoldiella chi- 
lenica (Fig. 86); Yoldia (Aequiyoldia) eightsi 
(Fig. 89); Tindaria virens (Figs. 95, 96). (2) Se 
conserva una vuelta en el lado derecho del 
cuerpo, pero la vuelta se alarga muchísimo o 
forma dos vueltas en: Nucula (N.) pisum (Fig. 
64); Ennucula gray i (Fig. 71); y Propeleda 
longicaudata (Fig. 76). (3) Se conserva la dis- 
posición del intestino en el lado derecho, pero 
el número de vueltas aumenta en: Nucula (N.) 
fernandensis: Nucula (Л/.) pseudoexigua (Fig. 
66); y Ennucula puelcha (Fig. 73). 

Parece existir una relación entre especies 
muy anchas, pero cortas de Nucula y Ennu- 
cula. Spinula y Ledella y un número superior 
a 3 ó 4 vueltas. Por el contrario, géneros ca- 
racterizados por especies aplastadas y largas 
presentan casi siempre una sola vuelta, 
aunque de longitud y forma variable (e.g., 
Malletia). 

Sin embargo, las excepciones demos- 
tradas por el género Nuculana que contiene 
especies bastante anchas, pero con una sola 
vuelta, sugiere tendencias que aún en el caso 
de Propeleda, Yoldia, Yoldiella, Malletiidae, y 



otros géneros, podrían explicarse mejor por la 
posición adelantada del intestino, como lo 
propone Heath (1937). Waren (1978: figs. 1- 
7) muestra como la configuración de las 
vueltas del intestino pueden vahar según el 
grado de compresión de la masa visceral. 

(9) El valor filogenético de la posición del 
corazón en relación al recto, sugehdo por 
Pelseneer (1888, 1911) para todos los bi- 
valvos, parece poder aplicarse también a la 
evolución de este órgano dentro de los proto- 
branquios. Familias reconocidas como más 
primitivas (Nuculidae), presentan un corazón 
dorsal al recto o envolviendo al recto (atra- 
vesado por él), mientras que en familias más 
especializadas (Nuculanidae, Malletiidae), el 
corazón puede estar envolviendo al recto 
(Nuculanidae) o bajo él (Malletiidae) (Figs. 
58, 59). 

Efectivamente, se observó que en las es- 
pecies de Nucula y Ennucula aquí estudiadas 
(Nuculidae), el corazón es dorsal al recto, al 
igual que en la especie europea Nucula nu- 
cleus (Linné) (Figs. 63, 65, 67, 71, 73), pero 
diferente a N. próxima, en laque White (1942) 
describió al ventrículo atravesado por el recto. 
A este respecto, es igualmente importante 
mencionar que según Drew (1 901 ), en N. del- 
phinodonta el corazón rodea al recto durante 
su desarrollo y solamente llega a ser dorsal a 
él, cuando el animal alcanza su madurez sex- 
ual. En consecuencia, en Nuculidae se cono- 
cen dos tipos de posición del corazón en 
relación al recto: dorsal a él y envolviéndolo. 

En las especies estudiadas de los géneros 
Nuculana. Propeleda, Silicula, Yoldiella, y 
Yoldia, el corazón se observó envolviendo al 
recto y no existen en la literatura citas de 
otras especies de estos géneros en que se 
presente en una posición distinta (Figs. 76, 
78, 85, 89). En las de los géneros Malletia, 
Tindaria, y Tindariopsis el corazón puede ser, 
ventral al recto (Malletia chilensis y Tindaria 
virens: Figs. 92, 95) o estar envolviéndolo 
(Malletia patagónica y Tindariopsis sulculata; 
Figs. 81, 82). El corazón también parece 
estar envolviendo al recto en M. gigantea 
(Smith, 1875) (White, 1942). 

Según Owen (1959: fig. 7), en Solemya 
(Solemyidae) el corazón está envolviendo al 
recto. Desgraciadamente, no se ha descrito 
su posición en el género Acharax y, en la es- 
pecie de este género estudiada por nosotros, 
no pudo establecerse debido al tamaño re- 
ducido del ejemplar estudiado. 

(10) La plasticidad de la estructura sifonal 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



179 



en el proceso adaptative frente a condiciones 
ambientales diferentes, parece ser otra de las 
tendencias que esta marcando la diferen- 
ciación de especies entre los nuculanáceos, 
pero sin una secuencia filogenética clara. Es- 
tructuralmente, los sifones representan la 
hipertrofia de las regiones posteriores de los 
márgenes del manto que rodean las aber- 
turas exhalante e inhalante y de los músculos 
paléales asociados. 

Yonge (1 939, 1 957) basado en especies de 
Nuculanidae y Malletiidae señaló tres formas 
diferentes de fusión de las paredes de los 
tubos sifonales. que supuso correlacionadas 
con el largo de los sifones: 

1, con ambos sifones fusionados por teji- 
dos (tercera forma de Schileyko. 1983): 

2, sifón exhalante cerrado, con unión ciliar 
completando sólo el sifón inhalante (segunda 
forma de Schileyko, 1983): 

3, con unión ciliar completando ambos si- 
fones (Fig. 57a-c) (primera forma de Schi- 
leyko, 1983). 

El estudio de las especies chilenas aquí 
tratadas y el de las especies abisales y há- 
dales de protobranquios realizado por Knud- 
sen (1970), Schileyko (1983), y Alien (1985), 
permite ampliar las tres formas fundamen- 
tales de Yonge a ocho (Fig. 57a-h), agre- 
gando a las anteriores aquellas que presen- 
tan: 

4, sifones unidos dorsal y ventralmente 
solo por uniones ciliares (Fig. 57d): 

5, sifón exhalante abierto dorsal y ventral- 
mente, ya sea con un número variable de ten- 
táculos o papilas en el margen del manto 
(correspondiente al sifón inhalante), o sin 
ellos (margen liso. Fig, 57f): 

6, sifón exhalante solamente, cerrado ven- 
tralmente (cuarta forma de Schileyko, 1983), 
con el margen del manto correspondiente al 
sifón inhalante aserrado (Fig. 57e): 

7, sifón exhalante solo parcialmente sepa- 
rado del inhalante (Fig. 57g) y 

8, sifones unidos sólo dorsalmente (Fig. 
57h). 

La proposición de Yonge (1957) de que la 
formación de los sifones comenzó con el en- 
samble de cilios de los bordes opuestos del 
manto, seguido por la fusión secuencial de 
los tejidos, es convincente en opinión de 
Schileyko (1983) y Alien (1985). Schileyko 
(1983) agrega que cuando existe la unión 
ciliar como una especie de cremallera, la ca- 
pacidad de conducción es mayor que cuando 
existe un tubo que la limita. 



La diferenciación entre unión ciliar y tisular 
es difícil, al extremo de que, en las especies 
aquí estudiadas en las que se examinaron 
detalladamente los sifones, solo se pudo con- 
cluir si existía o no unión completa, sin pre- 
cisar su origen ciliar o histológico. Se arriesga 
así una posible confusión de ambas, puesto 
que según Drew (1899) la fusión mediante 
tejido, por su origen ontogénico, conserva 
una línea de unión indicada por un surco en la 
línea media ventral (Pelseneer, 1911: Heath, 
1 937), que se rompe con cierta facilidad al ser 
presionada con un instrumento de disección. 
Precisar la unión, requirió casi siempre el 
examen de muchos ejemplares. La consta- 
tación definitiva debería hacerse mediante 
cortes histológicos e idealmente con micros- 
copía de barrido. 

En suma, se encontró que el sifón exha- 
lante es un tubo completo, y el inhalante está 
formado aparentemente por unión ciliar en los 
Nuculanidae-A/ucu/ana (Saccella) eunesta 
(Fig. 77): Nuculana (Borissia) inaequisculpta 
(Fig. 90): Propeleda longicaudata (Figs. 75, 
76): Tindañopsis sulculata (Fig. 80): y el Tin- 
dariidae- T"/ndará virens (Figs. 94-96). En 
cambio, ambos sifones forman un tubo 
verdadero en: Yoldia {Aequiyoldia) eightsi 
(Sareptidae, Figs. 87-89); Silicula rouchi {S\\\- 
culidae, Fig. 5): Yoldiella ecaudata (Nucula- 
nidae): y Malletia chilensis (Malletiidae, Fig. 
12). 

Estas observaciones, sumadas a las des- 
cripciones de Knudsen (1970). Alien (1963), 
Alien y Sanders (1973, 1982), y Sanders y 
Alien (1977), permiten establecer las siguien- 
tes relaciones entre géneros de Nuculanacea 
y estado de fusión de los sifones: 

Fusión de tipo a. Observada en especies 
de los géneros Malletia. Yoldia. Yoldiella, 
(¿Spinula?). (Ledella), y Nuculana. 

Fusión de tipo b. Observada en especies 
de los géneros Yoldia. Yoldiella. {¿Spinula?). 
{Ledella), y Nuculana. 

Fusión de tipo с Observada en especies 
de los géneros Neilonella, Malletia. Nuculana. 
{Phaseolus), Tindariopsis, y Propeleda. En 
este último género, sin embargo, los bordes 
ventrales son divergentes. 

Fusión de tipo d. Observada en especies 
de los géneros Neilonella y Tindaha. 

Fusión de tipo e. Observada en especies 
del género Sarepta (Knudsen. 1970). 

Fusión de tipo t. Observada en especies 
del género Tindaña. 

La descripción de los sifones en los 



180 



VILLARROEL & STUARDO 



géneros incluidas en paréntesis, no es lo su- 
ficientemente detallada como para precisar el 
tipo de unión. 

En Ledella kermadecensis. Knudsen 
(1970), describió un solo sifón con dos aber- 
turas, mientras que en las especies Yoldiella 
ecaudata y Silicula rouchi aquí estudiadas y 
en Spinula oceánica Filatova, S. tasmanica 
Knudsen, S. vityasi Filatova, estudiadas por 
este mismo autor, existe un solo tubo sifonal, 
no pudiendo establecerse si corresponde so- 
lamente a un sifón exhalante o a una fusión 
de los dos sifones. 

Filatova y Schileyko (1 984) agregan una im- 
portante observación en cuanto a la estructura 
del sifón. Ellos encontraron que las paredes 
del único sifón de los Nuculanidae (Ledellinae 
y Spinulinae) pueden contener parénquima o 
hemolinfa. Con el primer carácter ellos sepa- 
ran la subfamilia Ledellinae con los géneros 
Bathyspinula Filatova, 1958; Ledellina Fila- 
tova y Schileyko (1984); y Ledella Verrill y 
Bush, 1897. Con un sifón de paredes huecas 
con hemolinfa caracterizan a Parayoldiellinae 
Filatova, 1971, con los géneros Parayoldlella 
Filatova, 1971, e Intercalarla Filatova y Schi- 
leyko, 1984. 

Además estos autores concluyen que la 
diferencia en la estructura del sifón hace que 
su alargamiento y movimiento sea también 
diferente. El sifón provisto de parénquima se 
puede alargar poco, pero se puede encorvar, 
en cambio el otro tipo es hidráulico y si bien 
se puede alargar mucho y funcionar como 
una válvula peristáltica, no se puede doblar o 
encorvar tan fácilmente. Desgraciadamente 
no hicimos cortes de los sifones que observa- 
mos, pero seria interesante hacerlo para 
todas las especies que aquí se presentan. 

Filatova y Schileyko (1984) encuentran una 
correlación entre la longitud de los sifones y la 
presencia de un rostro en la concha que les 
proporciona protección, pero que limita la 
movilidad del sifón. 

La fusión de los sifones dentro de los Nu- 
culanacea no parece seguir líneas evolutivas 
definidas. Efectivamente, aún cuando la pre- 
sencia de sifones ha sido acompañada de 
una reducción del tamaño de las branquias y 
que, como lo sugiriera Yonge (1 939), el grado 
de unión de los sifones podría estar correla- 
cionado con su largo, no parecen haber otras 
relaciones funcionales claras. Será difícil pre- 
cisarlas, mientras no se conozcan en detalle 
los hábitos de las distintas especies. 

Pelseneer (1911) observó la presencia de 



un tentáculo sifonal generalmente a la 
izquierda en especies de Yoldia y Nuculana, 
mientras que fue encontrado indistintamente 
a un lado u otro por Stempell (1899) en 
Yoldiella ecaudata y por Filatova y Schileyko 
(1984) en Ledellina y Bathyspinula. Stempell 
(1899) lo encontró de preferencia a la 
derecha en Malletia chllensls. Yonge (1 939) lo 
ubica de preferencia a la derecha, pero en las 
especies aqui estudiadas — Nuculana (S.) 
cunéala, Yoldia (Aequiyoldia) eightsi. lindarla 
virens. Yoldiella ecaudata. y Malletia chilensls 
se encontró indistintamente a un lado u otro 
(Figs. 77, 85, 89. 96, ts). 

En las especies abisales y hádales des- 
chtas por Knudsen (1 970), el tentáculo sifonal 
se encontró en un número igual de especies, 
tanto a la derecha como a la izquierda. 

No todas las especies de Nuculana pre- 
sentan tentáculo sifonal y a este respecto nos 
parece interesante la ausencia de tentáculo 
en la única especie descrita hasta ahora para 
las ventilas hidrotermales, Nuculana grassiei 
Alien, 1993. El autor de la especie lo rela- 
ciona a un desarrollo pobre del sistema 
nervioso y quizás a una preadaptación para 
vivir en sedimento con bastante material bac- 
teriano en la superficie. 

(11) Respecto de la distribución geográfica, 
el estudio de los protobranquios chilenos, ha 
demonstrado, que la distribución extraordi- 
nariamente amplia de algunas especies de 
protobranquios es dudosa y éste, probable- 
mente, es el caso de muchas otras en otras 
regiones biogeográficas. Así ocurre con es- 
pecies de Nucula de supuesta amplia dis- 
tribución geográfica en Chile, pero errónea- 
mente identificadas, como ya se estableció 
para Nucula exigua Sowerby I, 1833; Nucula 
carlottensis Dalí, 1897; Nucula declivis Hinds, 
1843; Ennucula colombiana (Dalí, 1908a); y 
Nuculana callimene (Dalí, 1908a). 

En otros casos, la distribución geográfica 
aparece amplia, por la sinonimización equí- 
voca de especies distintas, como ocurrió con 
Malletia chilensls. cuya distribución se había 
establecido erróneamente hasta Magallanes. 

En la Tabla 2 se ha representado el rango 
de la distribución de las especies estudiadas, 
en 10 columnas, que incluyen a las siguientes 
áreas geográficas; 

1. Islas Juan Fernández — Islas Salas y 
Gómez 

2. Perú 

3. Arica — Mejillones 

4. Coquimbo — Valparaíso — Constitución 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



181 



5. Talcahuano — Canal de Chacao 

6. Isla de Chiloé — Península de Taitao 

7. Golfo de Penas — Estrecho de Maga- 
llanes 

8. Tierra del Fuego — Islas Falkland 

9. Argentina 
10. Antartica 

La Tabla 2 demuestra la existencia de los 
dos grupos faunísticos reconocidos para los 
bivalvos (Woodward 1851-1856; Soot-Ryen, 
1959; Stuardo, 1964, 1988), con una limitada 
sobreposición de especies. En el hecho, solo 
las especies Nucula (N.) pisum. Ennucula 
grayi. y E. puelcha presentan una distribu- 
ción amplia dentro de las dos provincias, 
mientras que Malletia chilensis y Tindariopsis 
sulculata se extienden dentro de límites 
que podrían considerarse zonas de transi- 
ción. Todas las especies restantes están cir- 
cunscritas a los límites conocidos tradicional- 
mente para las dos unidades faunísticas, de 
origen subtropical y subantártico, respectiva- 
mente. 

Las especies antarticas, salvo Propeleda 
longicaudata, no llegan al extremo sur de Su- 
damérica (Tabla 2). Por otra parte, son pocas 
las especies de protobranquios que se ex- 
tienden al Atlántico, reforzando la impresión 
de Stuardo (1 964, 1 988) de que debe tratarse 
de precisar la diferencia ambiental entre la 
fauna de elementos magallánicos del Atlán- 
tico y del Pacífico. 

La Tabla 2 muestra también posibles rela- 
ciones interespecíficas. Por ejemplo, las rela- 
ciones morfológicas entre Nucula (Nucula) 
pisum. N. (A/.) fernandensis. y N. (Л/.) falk- 
landica parecen ser el resultado de una ra- 
diación alopátrica de especies en las que N. 
(A/.) pisum correspondería a la especie an- 
cestral de la cual las otras dos se derivaron, 
separándose hacia los extremos de disper- 
sión de la primera. El registro fósil de esta es- 
pecie (Philippi, 1887) parece corroborar lo an- 
terior. 

Ennucula grayi y E. puelcha son dos es- 
pecies simpátricas muy parecidas, pero 
cuyas relaciones entre sí y con respecto a las 
especies de Ennucula de áreas vecinas del 
Pacífico o del Atlántico son todavía oscuras. 
Podrían corresponder a una sola especie. 

(12) De la ecología de estas especies, se 
sabe poco excepto por las indicaciones de 
sustrato que se dan en las descripciones. 

Solo en dos lugares de la costa de Chile se 
han estudiado en detalle; Bahía de Concep- 
ción (este estudio) y Bahía de Valparaíso 



(Ramorino, 1968). Los datos son resumidos 
aquí brevemente. 

Se han encontrado sólo tres especies en la 
Bah ía de Concepción ; Nucula ( Nucula) pisum. 
Nuculana {Saccella) cuneata. y Malletia chi- 
lensis. de las cuales Nucula y Nuculana se en- 
contraron viviendo preferentemente en fango 
arenoso, mientras que Malletia fue encon- 
trada preferentemente en fango, diferencias 
que coinciden con las observaciones de 
Ramorino (1968) en la Bahía de Valparaíso. 
La especie Ennucula grayi que vive también 
en los fondos de la Bahía de Valparaíso no se 
encuentra en la Bahía de Concepción, proba- 
blemente debido a las vahaciones ambien- 
tales estacionales tan extremas conocidas en 
esta última (Ahumada y Chuecas, 1979). La 
abundancia de las otras tres especies tam- 
poco es comparable a la que Ramorino (1 968) 
encontró en Valparaíso como se ha discutido 
bajo cada una de estas especies. 

Las relaciones de las distintas especies a 
distintos tipos de fondos se ha resumido en la 
distribución de cada especie. En general, son 
pocas las que se encuentran vivas en fondos 
con sedimentos gruesos; la mayoría habita 
siempre en fondos de arena y fango, o en 
mezclas de ambos. Esto no difiere de lo des- 
crito para otros protobranquios. pareciendo 
haber una relación estrecha entre las carac- 
terísticas del sedimento y la forma y actividad 
del animal. Como lo ha demostrado Alien 
(1 954) para las especies británicas de Nucula 
y Nuculana. variaciones de forma dentro de la 
misma especie pueden también ser conse- 
cuencia de la variación del sustrato. (Ver dis- 
cusión sobre longitud del intestino.) 

(13) El número de especies de protobran- 
quios que habitan grandes profundidades 
(2358-7000 m) es considerable, a juzgar por 
la lista dada por Knudsen (1970; tabla 1), 
Schileyko (1989). Sin embargo, siguiendo la 
división batimétrica de los océanos, entre los 
protobranquios chilenos, habría una sola es- 
pecie intermareal (i); Nucula (N.) interflucta. 
descrita para Punta Morro, Iquique, encon- 
trada en limo arenoso negro entre guijarros y 
cantos rodados de una playa protegida y una 
sola especie abisal (a. Tabla 2); lindarla 
salaria, colectada frente a las Islas Salas y 
Gómez. Todas las demás son sublitorales (s, 
Tabla 2) o sublitorales y batiales al mismo 
tiempo (s-b, Tabla 2). 

La distribución gradual batimétrica de las 
especies chilenas representa en parte (litoral- 
abisal) a las observaciones de Schileyko 



182 



VILLARROEL & STUARDO 



TABLA 2. Distribución geográfica y batimétrica de los protobranquios chilenos y de algunos antarticos; a = 
abisal: b = batial; i = intermareal; s = sublitoral. 

Geographic and batimetric distribution of Chilean and some Antarctic protobranchs; a = abyssal: b = 
bathyal: i = intertidal: s = sublitoral. 







Areas geográficas 








Prof (m) 


Distr. 


Especies 


1 2 3 


4 


5 


6 


7 


8 


9 


10 


vert. 


Nucula pisum 


X 


X 


X 


X 


X 








8- 


-200 


s 


N. fernandensis 


X 
















120- 


-280 


s 


N. falklandica 










X 


X 






46- 


-500 


s-b 


N. interflucta 


X 




















i 


N. pseudoexigua 










X 








223- 


-500 


s-b 


Ennucula gray! 




X 


X 


X 


X 


X 


X 




92- 


-744 


s-b 


E. puelcha 


X X 


X 


X 


X 


X 


X 


X 




139- 


-210 


s 


Nuculana cuneata 


X X 


X 


X 












28- 


-280 


s 


N. inaequisculpta 
















X 


48- 


-304 


s 


Propeleda longicaudata 










X 






X 


93- 


-1080 


s-b 


Sllicula patagónica 










X 








219- 


-460 


s-b 


S. rouchí 
















X 


135- 


-720 


s-b 


Yoldia eights'! 
















X 


25- 


-728 


s-b 


Yoldiella ecaudata 
















X 


33- 


-891 


s-b 


Y. granula 










X 








110 


s 


Y. chilenica 








X 


X 








70- 


-722 


s-b 


Y. indolens 










X 








70- 


-349 


s 


Malletia ctiilensis 




X 


X 


X 










1- 


-240 


s 


M. magellanica 










X 








36- 


-58 


s 


M. patagónica 










X 




- . 




57- 


-664 


s-b 


M. inaequalis 










X 








56- 


-110 


s 


Malletiella sorror 






X 












1219 


s-b 


Tindaria virens 








X 


X 








70- 


-808 


s-b 


T. salaria 


X 
















2055 


a 


Tindahopsis sulculata 




X 


X 


X 


X 


X 


X 




13- 


-300 


s 


Acharax patagónica 










X 








441 


s-b 


A. macrodactyla 








X 




X 






36- 


-664 


s-b 



(1989) (litoral hasta ultraabisal) y que la 
mayor parte de los taxa de profundidad tienen 
representantes de poca profundidad. 

Respecto a la distribución en profundidad 
de Malletia chilensis. parece extraño que 
Ramorino (1968) la encontrara como máximo 
hasta solo 102 m, probablemente por limita- 
ciones de muestreo. Como se desprende de 
los datos resumidos en la Tabla 2, esta es- 
pecie y todas las otras tienen un rango de 
distribución batimétrica mucho mayor. 

De esta síntesis también se desprende 
que tanto el conocimiento de las especies 
sublitorales de protobranquios chilenos como 
el de las especies batiales parece adecuado, 
pero el de las especies abisales que viven 
frente a estas costas es prácticamente nulo. 
Se deben hacer esfuerzos para cono- 



cer mejor tanto la fauna de moluscos abisales 
como la de invertebrados en general. Parece 
igualmente pobre el conocimiento de la fauna 
de protobranquios en las islas oceánicas 
chilenas, sobre todo de las islas Juan Fer- 
nández y Pascua (Rapa Nui). 

(14) Como se demuestra en este trabajo, 
las especies de protobranquios fósiles no han 
sido estudiadas recientemente, y su cono- 
cimiento taxonómico deja mucho que desear. 
Sin embargo, la revisión de la literatura ha 
permitido compilar y reubicar taxonómica- 
mente un total de alrededor de 50 especies 
del Paleozoico, Mesozoico y Cenozoico. Del 
mismo modo, la obtención de muestras per- 
mitió redescribir en detalle cinco especies de 
los géneros Ennucula. Propeleda. Tindariop- 
sis y Malletia. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



183 



SINOPSIS DE LOS PROTOBRANQUIOS 

RECIENTES DESCRITOS O CITADOS 

PARA CHILE CON INCLUSIÓN DE LAS 

ESPECIES ANTÁRTICAS ESTUDIADAS 

(A = especies antarticas; * = especies 

no vistas; 

? = especies cuya presencia es improbable) 

FAMILIA NUCULIDAE 

A *Nucula austrobenthalis Dell, 1 990 

? Nucula declivis Hinds, 1843 

? Nucula exigua (forma de carlottensis?. fide 

Soot-Ryen, 1958) 
? Nucula carlottensis Dalí, 1897 
Nucula (A/.) falklandica Preston, 1912 
Nucula (N.) femanc/ens/s Vil I arroe I, 1971 
Nucula (N.) interflucta Maúncovlch, 1973 
Nucula (/V.) pisum G.B. Sowerby I, 1833 
Nucula (N.) pseudoexigua. sp. nov. 
? Ennucula colombiana (Dalí, 1908) 
"Ennucula eltanini Dell, 1 990 
Ennucula grayi (d'Orbigny, 1 846) 
Ennucula puelcha (d'Orbigny, 1 842) 

FAMILIA NUCULANIDAE 

Nuculana (Saccella) cunéala (G. B. Sowerby 

I, 1833) 
? Nuculana (S.) callimene (Dalí, 1908) 
A Nuculana (Borissia) inaequisculpta (Lamy, 

1906) 
A Propeleda longicaudata Thiele, 1912 
Tindariopsis sulculata (Gould, 1852, ex 

Couthouy ms) 

FAMILIA SILICULIDAE 
Silicula patagónica Dalí, 1 908 
? Silicula fragf/y/s Jeffreys, 1879 
A Silicula rouchi Lamy, 1911 

FAMILIA SAREPTIDAE 

A Yoldia (Aequiyoldia) eightsi (Jay, 1839, ex 

Couthouyms) 
Yoldiella chilenica (Dalí, 1908) 
A Yoldiella ecaudata (Pelseneer, 1903) 



* Yoldiella granula (Dalí, 1 908) 
Yoldiella indolens (Dalí, 1908) 

FAMILIA MALLETIIDAE 
Malletia chilensisóes Moulins, 1832 
*Malletia magellanica Smith, 1875 
Malletia patagónica Mabille y Rochebrune, 
1889 

* Malletia inaequalis Dalí, 1908 
*Malletiella sorror Soot-Ryen, 1959 

FAMILIATINDARIIDAE 
Tindaria virens Dalí, 1890 

* lindarla salaria Dalí, 1908 

FAMILIAACHARACIDAE 
lAcharax patagónica [SrciAh, 1885) 
*Acharax macrodactyla (Mabille y Roche- 
brune, 1889) 



AGRADECIMIENTOS 

Agradecemos al Dr. George M. Davis por 
haber revisado el manuscrito onginal y ani- 
marnos a actualizarlo. Al Dr. Eugene V. Coan 
por su crítica y cuidadosa revisión, comenta- 
rios, sugerencias y por la literatura enviada. A 
la Biól. Sandra Rubio por la captura del MS. A 
la dibujante Lourdes Espinoza por el entin- 
tado de algunas figuras. Al Laboratorio de Mi- 
croscopía Electrónica de la Dirección de In- 
vestigación de la Universidad de Concepción. 
Al Dr. E. López por la revisión de estilo. Al Dr. 
Alan R. Kabat y Raye Germon por permitirnos 
revisar los tipos de Dalí en el Museo Smithso- 
niano. A la Geól. Irina Musina por las traduc- 
ciones del ruso al español. A la Coordinación 
Científica de la Universidad Michoacana 
cuyos proyectos CICH 5.5 y 7.11 hicieron 
posible terminar la revisión bibliográfica. A 
todos aquellos que nos tuvieron la paciencia 
de soportar muchas revisiones al MS, nue- 
stros más sinceros agradecimientos 



184 



VILLARROEL & STUARDO 




FIG. 1. Nucula (N.) falklandica. Valva izquierda esquematizando los tipos de ornamentación de la concha. 

Left valve showing the types of shell ornamentation. 

A, B, C, tipos de costillas concéntricas que fueron observadas en Tindaria virens, Nuculana (S.) cuneata y 

Tindariopsis sulculata, respectivamente. A, B, C, types of concentric ribs observed on T. virens. N. (S.) 

cuneata, and T. sulculata, respectively. 

D, crenulación del borde interno (género: Nucula). D, crenulation of the inner margin (genus: Nucula). 

FIG. 2. Tindariopsis elegans. Vista dorsal mostrando escutelo, ligamento, lúnula y medidas de espesor y lon- 
gitud. Dorsal view showing escutcheon, ligament, lunule and measurements for width and length. 

FIG. 3. Esquema de la valva derecha de un nuculanáceo, destacando las impresiones musculares, dientes 
de la charnela y ligamento. Right valve outline in nuculanaceans, showing muscle scars, hinge teeth and li- 
gament. (A) Charnela de un Nuculidae. Nuculid hinge. (B) Charnela de Malletiay Tindaria. Hinge in Malletia 
y Tindaria. (C) Charnela de un Solemyidae. Hinge in solemyids. (D) Tipos de dientes más característicos en 
las especies estudiadas. Characteristic hinge teeth in the studied species. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



185 




FIG. 4. Nucula (N.) pisum. Vista lateral izquierda de la cavidad del rлanto mostrando la disposición de los 
órganos en un Nuculidae. Parte de la glándula hipobranquial se ha omitido para señalar el ctenidio. Left lat- 
eral view of mantle cavity showing internal organs in Nuculidae. Part of hypobranchial gland omitted to show 
ctenidia. 

FIG. 5. Silicula rouchi. Vista lateral izquierda mostrando la disposición de los órganos en la cavidad del 
manto y cavidad pericárdica de un nuculanáceo. Left lateral view showing internal organs of mantle cavity 
and pericardial cavity in Nuculanacea. 

FIG. 6. Acharaxsp. Vista izquierda de la cavidad del manto, indicando la disposición de los órganos de un 
Solemyidae. Left view of mantle cavity showing internal organs in Solemyidae. 



186 



VILLARROEL & STUARDO 

cav p 




ada 




FIG. 7. Nuculana (S.) cuneata. Vista izquierda del manto, mostrando la disposición de los músculos del 
manto y de los sifones. Left view of mantle showing arrangement of mantle muscles and siphons. 

FIG. 8. Ennucula grayi. Musculatura del pie y músculos aductores. Foot musculature and adductors. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



187 




FIG. 9. Acharaxsp. Vista externa del palpo labial izquierdo. External view of left labial palp. 

FIG. 10. Acila castrensis. Superficie lisa del palpo en la que se indican las comentes ciliares (modificada de 

Stasek, 1961; fig. 5). Palp surface showing ciliary currents (modified from Stasek, 1961, tig. b). 

FIG 11. Solemya togata. Vista externa del palpo labial izquierdo (según Yonge, 1939; fig. 34; modificada). 

External view of left labial palp (modified from Yonge, 1939; fig. 34). 

FIG 12 Yoldia ensifera. Superficie lisa del palpo en la que se indican las comentes ciliares (según Stasek, 

1965; fig. 3). Palp surface showing ciliary currents (after Stasek, 1965; fig. 3). 

FIG. 13. Acharaxsp. Aparato digestivo. Digestive system. 

FIG. 14. Silicula rouchi. Aparato digestivo y su relación con el sistema nervioso. Digestive system in relation 

to nervous system. 



188 



VILLARROEL & STUARDO 




FIGS. 15-17. Relación de la lámela del palpo derecho con la boca, en Acila, Yoldia y Malletia. Right palp 
lámela showing relationship to mouth in Acila, Yoldia y Malletia. 

FIG. 15. Acila castrensis. Las caras yuxtapuestas de las lamelas han sido separadas. La dirección del 
movimiento ciliar se indica sobre las lámelas izquierdas; los pliegues se han indicado en las derechas (según 
Stasek, 1961 : fig. 4). Separated juxtaposed parts of palp lamellae. Ciliary movement shown in right lamella 
(after Stasek, 1961: fig. 4). 

FIG. 16. Yoldia ensifera. Las corrientes ciliares se indican al lado derecho (según Stasek, 1965: fig. 2). Cil- 
iary currents shown on right side (after Stasek, 1965: fig. 2). 

FIG. 17. Malletia chilensis. Nótese la presencia de surcos ciliados en el ensanchamiento del canal oral la- 
teral. View of ciliated grooves on embayment of lateral oral canal. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



189 




FIGS. 18-20. Nucula (Л/.) pseudoexigua. Estómago. Vistas derecha, anterior e izquierda. Stomach in right, 

anterior and left views. 

FIGS. 21 -22. Nucuia (Л/.) pisum. Estómago. Vistas derecha e izquierda. Stomach. Right and left views. 



190 



VILLARROEL & STUARDO 

1""" cd 



as"^ 




FIGS. 23-26. Nucula (N.) fernandensis. Estómago. Vistas derecha, izquierda, anterior e interior. Stomacii. 
Right, left, anterior and internal views. 

FIGS. 27-28. Nucula (N.) falklandica. Estómago. Vistas derecha y posterior. Stomach. Right and posterior 
views. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 

.2 



191 





FIGS. 29-32. Ennucula puelcha. Estómago. Vistas derecha, izquierda, interior y anterior. Stomach. Right, 
left, interior and anterior views. 



192 



VILLARROEL& STUARDO 




FIGS. 33-35. Propeleda longicaudata. Estómago. Vistas izquierda, anterior y derecha. Stomach. Left, an- 
terior and right views. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 

:d 



193 




as? 





FIG. 36. Propeleda longicaudata. Vista interior del estómago. Stomach, interna! view. 

FIGS. 37-38. Nuculana (В.) inaequisculpta. Estómago. Vistas anterior e izquierda. Stomach. Anterior and 



left views. 



194 



VILLARROEL & STUARDO 




FIGS. 39-41. Tindariopsis sulculata. Estómago. Vistas derecha, izquierda y anterior. Stomach. Right, left 
and anterior views. 

FIGS. 42-43. Nuculana (S.) cuneata. Estómago. Vistas anterior e izquierda. Stomach. Antenor and left 
views. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



195 




rj°^' ^i'"^^. ^"'^'^ {Aequiyoldia) eightsi. Estómago. Vistas anteriores, izquierda y posterior Stomach An- 
terior, lett and posterior views. 

Ief?^ewl"^^' ^'"^"'^ '°'"'^'' ^^'^'^^З^- ^'^^^^ anterior, derecha e izquierda. Stomach. Antenor, nght and 



196 



VILLARROEL & STUARDO 




FIGS. 50, 51 , 53. Malletia chilensis. Estómago. Vistas derecha y posterior (se indica línea de corte), anterior 
e izquierda. Stomach. Right, posterior (showing incision line), anterior and left views. 

FIGS. 52, 54, 55. Tindaria virens. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



197 




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FIG. 57. Tipos de unión entre sifones, observados en ios géneros de Nuculanacea. (a) Ambos sifones fu- 
sionados por tejido; (b) Sifón exhalante cerrado, inhalante abierto ventralmente; (c) Ambos sifones abiertos 
ventralmente; (d) Sifones abiertos dorsal y ventralmente; (e) Sifón exhalante cerrado; región correspondi- 
ente al inhalante con bordes aserrados; (f) Sifón exhalante abierto ventralmente o dorsal y ventralmente; 
región del sifón inhalante con bordes tentaculados o lisos. Fusion types in the genera of Nuculanacea. (a) 
Both siphons fused by tissue; (b) exhalant siphon closed, inhalant open ventrally; (c) both siphons open ven- 
trally; (d) siphons open dorsally and ventrally; (e) exhalant siphon closed; part corresponding to inhalant 
siphon with serrated margins; (f) exhalant siphon, ventrally or dorsally and ventrally opened; inhalant siphon 
area with tentacles or smooth margins. 

FIGS. 58, 59. Esquema diagramático de una sección transversal de la cavidad pericárdica y el recto y vista 
dorsal de la relación corazón-recto en la cavidad pericárdica, que muestra las modalidades fundamentales 
observadas en los géneros estudiados. Schematic transversal section of pericardial cavity and rectum dor- 
sally showing the relationship heart-rectum and arrangements observed in the studied genera. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



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FIGS. 62-64. Nucula (Л/.) pisum. 

FIG. 62. Vista lateral izquierda. Left lateral view. 

FIG. 63. Vista dorsal rлostrando tracto digestivo, divertículos digestivos, corazón y glándula hipobranquial 
derecha. Dorsal view showing; digestive tract, digestive diverticula, heart and right hypobranchial gland. 

FIG. 64. Vista lateral izquierda mostrando aparato digestivo, sistema nervioso y glándula del biso. Left lat- 
eral view showing digestive tract, nervous system and byssal gland. 



202 



VILLARROEL& STUARDO 




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FIGS. 65-67. Nucula (N.) pseudoexigua. 

FIG. 65. Vista lateral izquierda de la cavidad del manto y cavidad pericárdica. Left lateral view of mantle and 

pericardial cavity. 

FIG. 66. Vista lateral derecha del intestine. Muy aumentada. Enlarged nght lateral view of intestine. 

FIG 67 Vista lateral izquierda, mostrando aparato digestivo, sistema nervioso y cavidad pencárdica con 
corazón y riñon. Left lateral view showing digestive tract, nervous system, pencardial cavity, heart and kid- 
ney. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



203 




FIGS. 68-69. Nucula (Л/.) falklandica. 

FIG. 68. Vista lateral izquierda. Left lateral view 

FIG. 69. Vista lateral izquierda del tracto digestivo, ctenidia y sistema nervioso. Left lateral view of the di- 
gestive tract, ctenidia and nervous system. 



204 



VILLARROEL & STUARDO 



cav 





FIGS. 70-71 . Ennucula grayi. 

FIG. 70. Vista lateral izquierda del manto. Left lateral view of mantle. 

FIG. 71. Vista lateral izquierda mostrando aparato digestivo, sistema nervioso y glándula del biso. Left lat- 
eral view shiowing digestive tract, nervous system and byssal gland. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 205 

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FIG. 72. Ennucula puelcha. Vista lateral izquierda de la cavidad paleal. Left lateral view of palliai cavity. 

FIG. 73. Ennucula grayi. Vista dorsal mostrando tracto digestivo, corazón, glándula hipobranquial y muscu- 
latura pedal. Dorsal view showing digestive tract, heart, hypobranchial gland and pedal musculature. 



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PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 207 

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FIGS. 77-79. Nuculana (S.) cuneata. 

FIG. 77. Vista lateral izquierda mostrando los órganos de la cavidad paleal, divertículos digestivos izquier- 
dos, estómago, cavidad pericárdica y corazón. Left lateral view showing organs of the palliai cavity, left di- 
gestive diverticula, stomach, pericardial cavity and hearth. 

FIG. 78. Vista dorsal mostrando tracto digestivo, corazón, riñon y ctenidio derecho. Dorsal view showing di- 
gestive tract, heart, kidney and right ctenidia. 

FIG. 79. Vista lateral izquierda mostrando aparato digestivo, sistema nervioso y lámela del palpo derecho. 
Left lateral view showing digestive tract, nervous system and right palp lámela. 



208 



VILLARROEL & STUARDO 
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FIGS. 80-82. Tindariopsis sulculata. 

FIG. 80. Vista lateral izquierda de la cavidad paleal con parte del manto. Left lateral view of palliai cavity with 

part of mantle. 

FIG. 81 . Vista dorsal del aparato digestivo y corazón. Dorsal view of fieart and digestive tract. 

FIG 82 Vista lateral izquierda mostrando aparato digestivo, sistema nervioso y musculatura pedal anterior 

y visceral. Left lateral view showing digestive tract, nervous system, anterior and visceral pedal musculature. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 

lig 



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FIGS. 83-84. Yoldiella ecaudata. 

FIG. 83. Vista lateral izquierda. Left lateral view. 

FIG. 84. Vista lateral izquierda de los órganos de la cavidad del manto. Pie y sifón extendidos. Left lateral 

view of the mantle cavity. Foot and extended siphons. 



210 



VILLARROEL&STUARDO 



mm 




sex 



gse 




FIGS. 85-86. Yoldiella chilenica. 

F.G. 85. Vista lateral izquierda de la cavidad del rлar.to. Left lateral view of mantle cav,t, 

fo'es' ^;^iS:^;:^Sng^d-S^^^^^^ '^'^ ^^' -^-^ — ° V detalle de los , 

y uigesrive tract, part of the nervous system and detail of siphons. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 

mm 

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FIGS. 87-89. Yoldia (Aequiyoldia) eightsi. 

FIG. 87. Vista lateral izquierda. Parte del manto se ha omitido para mostrar el palpo. Left lateral view. Part 
of mantle omitted to sfiow palp. 

FIG. 88. Vista dorsal del corazón y recto. Dorsal view of the heart and rectum. 

FIG. 89. Vista lateral izquierda mostrando aparato digestive, sistema nervioso, aparato circulatorio (la au- 
rícula izquierda ha sido omitida para mostrar el riñon), ctenidios y sifones. Left latera! view showing diges- 
tive tract, nervous system, heart (left auricle omitted to show the kidney), ctenidia and siphons. 



212 



VILLARROEL& STUARDO 




FIG. 90. Nuculana (В.) inaequisculpta. Vista lateral izquierda mostrando la cavidad del manto. Left lateral 

view showing mantle cavity. 

FIG. 91 . Malletia patagónica. Vista lateral izquierda. Left lateral view. 

FIG. 92. Maletia chilensis. Vista lateral izquierda mostrando la cavidad del manto. Left lateral view showing 

mantle cavity. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



213 



gse^/S 




"Sin 



FIGS. 93-96. Tindaria vlrens. 

FIG. 93. Vista lateral izquierda mostrando las gónadas y parte del manto. Left lateral view showing gonads 
and part of mantle. 

FIG 94 Vista lateral izquierda mostrando cavidad del manto, sifones, musculatura pedal y gandíos cere- 
bral y visceral. Left lateral view showing mantle cavity, siphons, pedal musculature, cerebral and visceral 
ganglia. 
FIG. 95. Vista dorsal del tracto digestivo y corazón. Dorsal view of digestive tract and heart. 

FIG 96 Vista lateral izquierda mostrando: aparato digestivo, sistema nervioso y glándula del biso. Vista 
frontal del sifón. Lett lateral view showing digestive tract, nervous system and byssal gland. Frontal view of 
siphon. 



214 



VILLARROEL & STUARDO 




FIGS. 97, 98. Nucula (Л/.) pisum. 

FIG. 97. Valva derecha (MZUC 4550), 20X, Bahía Inútil, Estrecho de Magallanes. Right valve (MZUC 4550), 
20X, Inutil Bay, Magellan Strait. 

FIG. 98, Vista dorsal del mismo ejemplar, 28X. Dorsal view of the same specimen, 28X 

FIGS. 99-101. Nucula (Л/,) fernandensis. 

FIG. 99. Valva derecha (MZUC 10388), 18X, Islas Juan Fernández. Right valve (MZUC 10388), 18X, Juan 
Fernandez Islands, 

FIG. 100. Valva izquierda (MZUC 10387. paratipo). 16.5X, Islas Juan Fernández. Left valve (MZUC 10387, 
paratype), 16.5X, Juan Fernandez Islands. 

FIG. 101. Vista dorsal (MZUC 10387. paratipo), 22X, Islas Juan Fernández, Dorsal view (MZUC 10387 
paratype), 22X, Juan Fernández Islands, 

FIGS. 102, 103. Nucula (N.) falklandica. 

FIG. 1 02. Valva derecha (MZUC 4662), 41 X, Estrecho de Magallanes. Right valve (MZUC 4662). 41 X, Ma- 
gellan Strait. 

FIG. 103. Vista dorsal del mismo ejemplar. 41 X. Dorsal view of same specimen. 41 X. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



215 




FIGS. 104-106. Nucula pseudoexigua. 

FIG. 104. Vista dorsal (MZUC 10304, paratipo). 28X. Confluencia Canales Trinidad y Concepción. Dorsal 
view (MZUC 10304. paratype). 28X. Confluence of Concepción and Trinidad channels. Valva izquierda del 
mismo ejemplar (MZUC 10304, paratipo), 25X, Left valve of same specimen (MZUC 10304), 25X. 

FIG. 105. Vista dorsal (MZUC 10293, Holotype), 20X, Canal Sarmiento. Dorsal view (MZUC 10293, Holo- 
type), 20X, Sarmiento Channel. Paratype. 

FIG. 1 06. Vista interior de valva izquierda (MZUC 1 0304), 1 8X, Confluencia Canales Concepción y Trinidad. 
Internal view left valve. (MZUC 10304), 18X, Confluence of Concepción and Trinidad Channels. 

FIGS. 107-109. Ennuculagrayi. 

FIG. 107. Vista dorsal (MZUC 4617). 14 mm. Estrecho de Magallanes. Dorsal view (MZUC 4617), 14 mm, 
Magellan Strait. 

FIG. 1 08. Vista interna (MZUC 461 7), 1 5 mm. Estrecho de Magallanes. Internal view (MZUC 461 7), 1 5 mm, 
Magellan Strait. 

FIG. 109. Valva derecha del ejemplar anterior. Right valve of same specimen. 



216 



VILLARROEL & STUARDO 




120 



122 



FIGS. 110-112. Ennucula puelcha 

FIG. 110. Valva derecha, vista interna (MZUC 
4565). 17.7 mm, Mar Chile II Est. 24. Right valve, 
internal view (MZUC 4565), 17.7 mm, Mar Chile II 
Est. 24. 

FIG. 111. Vista externa del mismo ejemplar, Estre- 
cho de Magallanes. External view of same speci- 
men, Magellan Strait. 

FIG. 112. Vista dorsal del mismo ejemplar. Dorsal 
view of same specimen. 

FIGS. 113, 114. Propeleda longicaudata. 

FIG. 1 1 3. Vista dorsal (MZUC 461 0), 9 mm. Conflu- 
encia Canales Concepción y Trinidad. Dorsal view 
(MZUC 4610), 9 mm. Confluence of Concepción 
and Trinidad Channels. 

FIG. 114. Vista lateral del mismo ejemplar. Lateral 
view of same specimen. 

FIGS. 115-118. Nuculana (S.) cuneata. 

FIG. 115. Vista lateral (MZUC 4706), 8 mm. Bahía 
Concepción. Lateral view (MZUC 4706), 8 mm, 
Concepción Bay. 



FIG. 116. Vista dorsal del mismo ejemplar. Dorsal 
view of same specimen. 

FIG. 117. Valva izquierda (MZUC 4562), 112 mm. 
Punta Tortuga. Coquimbo. Left valve (MZUC 4562), 
112 mm. Tortuga Point, Coquimbo. 

FIG. 118. Valva izquierda (MZUC 4562), 11 mm. 
Punta Tortuga, Coquimbo. Left valve (MZUC 4562), 
11 mm. Tortuga Point, Coquimbo. 

FIGS. 119, 120. Tindaria virens 

FIG. 119. Vista dorsal (MZUC 4650), 4.4 mm. Es- 
trecho de Magallanes. Dorsal view (MZUC 4650), 
4.4 mm, Magellan Strait. 

FIG. 120. Vista lateral del mismo ejemplar. Lateral 
view of same specimen. 

FIGS. 121, 122. Nuculana (ß.) inaequisculpta 

FIG. 121. Vista dorsal (MZUC 4537), 1 2 mm. Estre- 
cho de Bransfield. Dorsal view (MZUC 4537), 12 
mm, Bransfield Strait. 

FIG. 122. Vista lateral del mismo ejemplar. Lateral 
view of same specimen. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



217 




FIG. 123. Yoldiella chilenica Valva derecha e izquierda (MZUC 4633), 14X. Estrecho de Magallanes. Right 
and left valve (MZUC 4633), 14X, Magellan Strait. 

FIG. 124. Yoldiella chilenica Vista dorsal (MZUC 4633), 12X, Bahía Corbeta Papudo. Dorsal view (MZUC 
4633), 12X, Corbeta Papudo Bay. 

FIG. 1 25. Yoldiella ecaudata Interior y exterior de valva izquierda (MZUC 4228), 1 7X y 26X, Isla Greenwich, 
Shetland del Sur. Interior and exterior of left valve (MZUC 4228), 17X and 26X, Greenwich Island, South 
Shetland. 

FIG. 126. Silicula rouchi Interior y exterior de valva derecha (MZUC 4509), 17X y 15X, Estrecho de Brans- 
field. Interior and exterior of right valve (MZUC 4509) 1 7X y 1 5X, Estrecho de Bransfield. Vista dorsal (MZUC 
4509), 15X, Estrecho de Bransfiel. Dorsal view (MZUC 4509), 15X, Bransfiel Strait. 



218 



VILLARROEL & STUARDO 



127 




128 




129 




130 





N 



с 




FIG. 127. Yoldiella indolens Valva derecha (MZUC 4520), 2 mm, Estrecho de Magallanes. Right valve 
(MZUC 4520), 2 mm, Magellan Strait. 

FIGS. 128, 129. Yoldla {Aequiyoldia) eightsi 

FIG. 128. Valva izquierda (MZUC 4503), 20.5 mm. Isla Decepción. Left valve (MZUC 4503), 20.5 mm, De- 
cepción Island. 

FIG. 129. Vista interna del mismo ejemplar. Internai view of same specimen. 

FIG. 130. Silicula patagónica Valva izquierda (MZUC 4659), 8 mm, Confluencia Canales Trinidad y Con- 
cepción. Left valve (MZUC 4659), 8 mm. Confluence of Trinidad and Concepción Channel. 

FIGS. 131, 132. Acharaxsp. 

FIG. 131. Valva derecha (MZUC 4613), 8.1 mm, Canal Sarmiento. Right valve (MZUC 4613), 8.1 mm. 
Sarmiento Channel. 

FIG. 132. Vista interna del mismo ejemplar. Internal view of same specimen. 

FIG. 133. Malletia chilensis. Vista de un ejemplar con las partes blandas (MZUC 4707), 30 mm. Bahía de 
Concepción. Specimen with soft parts (MZUC 4707), 30 mm, Concepción Bay. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



219 




147 



145 



FIGS. 134-137. Ennucula valdíviana. 

FIG. 134. Valva derecha (MV/1), 19.5 mm, Tubul. 
Right valve (MV/1 ), 1 9.5 mm, Tubul. 

FIG. 135. Vista dorsal (T/13), 17 mm, Tubul. Dorsal 
view (T/13), 17 mm, Tubul. 

FIG. 136. Vista lateral del ejemplar anterior. Lateral 
view of same specimen. 

FIG. 137. Vista de la charnela del ejemplar de Fig. 
134. Hinge of specimen in Fig. 134. 

FIGS. 138, 139. Ennucula lebuensis. 

FIG. 138. Vista lateral de un molde interno (T/19), 
19 mm, Tubul. Lateral view of internal mold (T/19), 
19 mm, Tubul. 

FIG. 139. Vista dorsal del mismo. Dorsal view of 
same mold. 

FIGS. 140, 141. Ennucula ¿nogal is? 

FIG. 140. Vista dorsal de una valva izquierda 
(V/1 32), 1 5 mm. Lo Valdés. Dorsal view of left valve 
(V/132), 15 mm, Lo Valdés. 



FIG. 141. Vista lateral de la valva anterior. Lateral 
view of same valve. 

FIGS. 142, 143. Ennucula araucana. 

FIG. 142. Esquema de una vista dorsal. Drawing in 
dorsal view. 

FIG. 143. Valva derecha (T/16), 17 mm, Tubul. 
Right valve (T/16), 17 mm, Tubul 

FIGS. 144, 145. Malletia {Nello) volckmanni. 

FIG. 144. Vistas dorsal (N/l), 46 mm, Navidad. Dor- 
sal view (N/l), 46 mm. Navidad. 

FIG. 145. Vista lateral del mismo ejemplar. Lateral 
view of same specimen, 

FIGS. 146, 147. Malletia chilensis. Vista lateral e in- 
terna de la valva izquierda (MZUC 4733), 26 mm, 
Bahía Valparaíso. Lateral and interior view, left 
valve (MZUC 4733), 26 mm, Valparaiso Bay. 



220 



VILLARROEL & STUARDO 



150 



151 




155 



158 



159 



FIGS. 148-156. Tindariopsis elegans. 

FIG. 148. Valva izquierda (T/2), Tubul. Left valve (T/2), Tubul. 

FIG. 149. Vista dorsal (T/1), 11 mm, Tubul. Dorsal view (T/1), 11 mm. Tubul. 

FIG. 1 50. Valva derecha (T/3), 1 1 mm. Tubul. Right valve (T/3). 1 1 mm, Tubul. 

FIG. 151. Valva izquierda (T/1), 10.5 mm, Tubul. Left valve (T/1), 10.5 mm, Tubul. 

FIG. 1 52. Valva derecha (T/1 2), 8 mm, Tubul. Right valve (T/1 2), 8 mm. Tubul. 

FIG. 1 53. Valva izquierda (T/1 ). 9 mm, Tubul. Left valve (T/1 ), 9 mm, Tubul. 

FIG. 154. Valva izquierda (T/3) 10 mm. Tubul. Left valve (T/3), 10 mm, Tubul. 

FIG. 1 55. Valva izquierda (T/8), 1 3.5 mm, Tubul. Left valve (T/8), 1 3.5 mm, Tubul. 

FIG. 1 56. Valva izquierda (T/1 ). 8.5 mm. Tubul. Left valve (T/1 ), 8.5 mm. Tubul. 

FIGS. 157-159. Tindariopsis sulculata. 

FIG. 1 57. Vista lateral (MZUC 4631 ), 8 mm, Estrecho de Magallanes. Lateral view (MZUC 4631 ), 8 mm, Ma- 
gellan Strait. 

FIG. 158. Vista dorsal del mismo ejemplar. Dorsal view of same specimen. 

FIG. 1 59. Vista de la charnela (MZUC 4631 ), 1 mm. Estrecho de Magallanes. Hinge (MZUC 4631 ), 1 mm, 
Magellan Strait. 



PROTOBRANCHIA CHILENOS RECIENTES Y ALGUNOS FÓSILES 



221 



LITERATURA CITADA 

ADAMS, A., 1856, Descriptions of thirty-four new 
species of bivalve molluscs {Leda. Nucula and 
Pythina) from the Cumingian Collection. Pro- 
ceedings of the Zoological Society of London, for 
1856:47-53. 

ADAMS, H. y A. ADAMS. 1 858, The genera of Re- 
cent Mollusca. Vol. 2. London [pp. 541 -572, pis. 
129-132, Jan. 1858] 

AHUMADA, R. y L. CHUECAS, 1979, Algunas ca- 
racterísticas hidrográficas de la Bahía de Con- 
cepción (36 40'S: 73'02'W) y áreas adyacentes. 
Chile. Gayana Miscelánea. 8: 1 -56. 

ALLEN, J. A., 1954, A comparative study of the 
British species of Nucula and Nuculana. Journal 
of the Mahne Biological Association of the United 
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Revised ms. accepted 9 March 1998 



MALACOLOGIA. 1998, 40(1-2): 231 -250 

THE LAND SNAIL FAUNA OF A SQUARE KILOMETER PATCH OF RAINFOREST 

IN SOUTHWESTERN CAMEROON: HIGH SPECIES RICHNESS, 

LOW ABUNDANCE AND SEASONAL FLUCTUATIONS 

A. J. de Winter & E. Gittenberger 

Institute of Evolutionary and Ecological Sciences, University of Leiden, c/o National Museum of 

Natural History P. O. Box 9517, NL 2300 RA Leiden, 

The Netherlands: sbu2eg@rulsfb.leidenuniv.de 

ABSTRACT 

Systematic sampling of a single square km patcti of rather acidic, undisturbed, fairly uniform 
Cameroonian rainforest during two different rainy seasons yielded 97 species of land snails, be- 
longing to at least 12 families. Up to 45 species were collected wittiin a single sampling site of 
20 m < 20 m during a single visit, and up to 51 during two visits in different seasons. This might 
be the world's highest sympatric land snail diversity reported to date. Variation in species com- 
position among the sampling sites appeared to be largely random, and not due to geographic or 
ecological replacement. Three (super)families make up 86% of the species, the carnivorous 
Streptaxidae (34%) being the most diverse. Overall snail abundance was rather low, and many 
species were rare. Of 64% of the species, the abundance was less than 1% of all specimens 
(2,654) collected. A substantial difference was observed in overall snail abundance between the 
two sampling periods. About 27% of the species were uniquely found in one of the two sampling 
periods, and many species differed more than 50% in relative abundance between these sea- 
sons. At least 27% of the species were largely or completely arboreal, and 19% were found to 
live both on the ground and in the vegetation: 46% of the species appear to be confined to the 
ground, and of 7% insufficient information was available. Major adult shell dimensions (height or 
diameter) range between approximately 1 and 165 mm, but the vast majority (74%) of species 
has adult shells smaller than 10 mm. The shell height:diameter ratio distribution is bimodal, but 
differs from those previously reported for other faunas by relatively many "globose" (H/D 0.8-1 .2) 
and very tall (H/D 2.8-4.4) shells. The distribution of neither shell size nor shell shape differed 
between ground-dwelling and (partly) arboreal species. 

Key words: Gastropoda, Africa, species diversity, biodiversity, species abundance, shell size, 
shell shape, vertical distribution, seasonal variation. 



INTRODUCTION 

Tropical rainforests in Africa and elsewhere 
are severely threatened by commercial timber 
logging and both slash-and-burn and cash 
crop agriculture. Huge areas of forest have al- 
ready been degraded or have disappeared 
before information could be obtained about 
their biodiversity and ecology. Originally, 
closed forests covered large parts of 
Cameroon. During the period 1980-1990 ap- 
proximately 140.000 ha (0.6%) were de- 
stroyed or degraded annually, and some 40% 
of the original forest cover now remains 
(Dixon et al., 1996). In view of the poor eco- 
nomic conditions of the country, there seems 
to be little hope that this trend will change in 
the near future. Detailed data on the biodiver- 
sity and ecology of undisturbed forest faunas 
are therefore urgently needed. This informa- 
tion would enable comparisons with various 



types of degraded forest, enabling, for exam- 
ple, conservation planning and evaluation of 
the usefulness of future reforestation from the 
viewpoint of biodiversity restoration. The lack 
of knowledge of the effects of disturbance on 
biodiversity is most apparent for inverte- 
brates, including gastropods. 

Land snails are a poorly studied group in 
tropical forests, including those of western 
Africa. Mainly on the basis of tentative eco- 
logical reasoning, Solem (1984) asserted that 
in rainforests land snails are "generally nei- 
ther diverse nor abundant." Recent studies 
have challenged the universality of this state- 
ment with respect to species diversity (De 
Winter, 1992, 1995: Emberton, 1995: Tatters- 
field. 1996). 

The present study describes the land snail 
diversity in a single square km patch of undis- 
turbed rainforest in southwestern Cameroon 
in some detail, in order to obtain baseline data 



231 



232 



DE WINTER & GITTENBERGER 



for future research in this and other tropical 
forest regions. Data from disturbed forests in 
this region will be given in additional papers. 
This study is carried out within the frame- 
work of the Tropenbos Cameroon Programme 
(TCP), which was established in 1992 by the 
Cameroonian Ministry of Environment and 
Forests (MINER) and the Dutch Tropenbos 
Foundation. The general objective of this mul- 
tidisciplinary programme is to develop meth- 
ods and strategies for the management of nat- 
ural forests enabling sustainable, that is, 
ecologically sound, socially acceptable, and 
economically viable, production of timber and 
other products and services (Foahom & 
Jonkers, 1992). The TCP study area (Fig. 1) 
covers 1 91 6 km^, and coincides with two adja- 
cent concessions of a Dutch timber company. 



THE STUDY AREA 

The 1 km X 1 km patch of undisturbed rain- 
forest studied ("block i2". as indicated on the 
prospection map of the timber company) is lo- 
cated about 15 km S of Lolodorf (about 
3 06'N, 10 44'E: Figs. 1, 2). Block 12 com- 
prises the relatively low and flat southwestern 
part of the so-called Biboo-Minwo catchment, 
a study region of с 7.7 km^ with an altitude 
between about 420 and 720 m located in the 
transition zone between the western lowlands 
and the eastern, more mountainous, part of 
the TCP area (Waterloo et al., 1997). Within 
block 12, elevations range from approximately 
420 m in the western and central parts to ap- 
proximately 480 m in the eastern fringes. 

The geology reflects the erosion of the Pre- 
cambrian shield, the region being dissected 
by streams and small rivers into undulating 
plains and remaining hills with bedrock con- 
sisting of acid gneisses. The soils are moder- 
ately to well drained, with clay and sand con- 
tents of about 35% and 45% in the topsoil 
(upper 0-10 cm), respectively. The topsoil is 
poor in nutrients (total nitrogen 0.25-0.5%, 
organic carbon 4-8%, available phosphorous 
12-26 ppm), and very strongly to extremely 
acidic, with pHíHjO) between 5 and 3.5 (Van 
Gemerden & Hazeu, in press). Small to very 
large (up to 5 m high), flat-topped rock out- 
crops mainly occur in the eastern and south- 
western parts of block i2. 

Southwest Cameroon forms part of the 
Guineo-Congolian domain of dense and 
humid evergreen rainforests. The study site 
lies within the Biafran Atlantic district, the flora 



of which is rich in Caesalpiniaceae (Letouzey, 
1985). In these forests, four vegetational lay- 
ers can be distinguished, with gradual transi- 
tions. The crowns of the emergent trees, 
sometimes surpassing 60 m in height, consti- 
tute the highest level and cover 20-30% of 
the ground surface. Canopies of mature trees 
of 25-40 m high form the second layer, cov- 
ering 60-80% of the floor surface. The third 
layer of shrubs and small trees may reach 
3-6 m, and the remaining layer of herbs is 
less than 1 m high. The foliage of the latter 
two layers covers 40-60% of the floor sur- 
face. Lianas are abundant in the canopy and 
in natural gaps. 

The vegetation of the region, including that 
of block 12, may be classified as very old sec- 
ondary forest, with perhaps true virgin forest 
on the steeper hill slopes (Van Gemerden & 
Hazeu, in press). The sheer size of the trees 
indicates that it has been left in peace for some 
centuries. According to Letouzey (1968) the 
region was subjected to extensive forest clear- 
ing by man in the 18th century. Letouzey's 
(1968) conclusion was based on historical re- 
search, as well as on the common occurrence 
of the tree Lophira alata ("Azobé"), the seeds 
of which germinate best under light conditions. 
His view seems to be in agreement with the 
presence in block i2 of a few truly giant Ceiba 
pentandra (with buttresses about 7 m wide), a 
tree more typical of young secondary forests 
and arable land. Preliminary data of M. P. M. 
Parren (pers. comm.) show a substantial tree 
diversity (diameter at breast height >10 cm) 
of about 125 species ha V The area is rela- 
tively rich in valuable timber species, of which 
especially Lophira alata and others such as 
Pterocarpus soyauxii ("Padouk") and Entan- 
dropiiragma utile ("Sipo") are exploited. 

The climate is equatorial. The area receives 
about 2,100 mm precipitation annually, with 
distinctly wet periods in September-Novem- 
ber and in April-May. There is a relatively dry 
period between December and March, when 
the monthly rainfall is well below 100 mm. 
Mean maximum daily precipitation is as high 
as 115 mm. Relative humidities are high 
throughout the year, with mean minimum and 
maximum monthly values of about 70% and 
96%, respectively. The air temperature is little 
variable over the year (mean 24.6'C), with 
minimum monthly values of approximately 
23 С in August and maximum values of ap- 
proximately 26 С in March. The wind direction 
is predominantly W-SW, and wind speeds are 
generally low (less than 4 m s^^); high wind 



CAMEROONIAN RAINFOREST LAND SNAIL DIVERSITY 



233 



Tropenbos Programme study area 

■^^ Approx. location of Block i2 
• Village 




FIG. 1. The location of the square km forest site studied ("block 12") within the area covered by the Tropen- 
bos Cameroon Programme. 



speeds can occur during thunderstorms (cli- 
matic data, partly extrapolated, from Waterloo 
etal., 1997). 

Although there is variation among the sites 
sampled in such characteristics as slope incli- 
nation and exposition, presence or absence 
of rock outcrops, and tree species, the overall 
nature of block i2 appeared to be fairly homo- 
geneous: rivers are less than 5 m wide, and 
altitude differences are 60 m at most. During 
the first visit in 1 995, the area was still virtually 
undisturbed, and the canopy closed, except 
for some natural gaps. However, in Febru- 
ary/March 1996 most of the region, including 
block i2, was selectively logged with an inten- 
sity of about 1 tree ha \ Since the logging ac- 
tivities took place shortly before or during this 
visit, we assumed that logging could not yet 
have affected our results, especially since dis- 
turbed sites were avoided. 



MATERIAL AND METHODS 
Sampling 

Sampling took place in two periods, August 
29-October 6, 1995, and March 21 -April 12, 
1 996, further referred to as "1 995" and "1 996." 
Each sampling period was early in one of the 
two rainy seasons. 

Collections were made within patches of 20 
m X 20 m that were marked with poles (called 
"sampling sites", "stations", or "plots" in this 
paper). Stations on rock boulders were con- 
siderably smaller than 20 m x 20 m. In all sites, 
the actual ground surface thoroughly sampled 
covered only a small part of the entire site. 

In each sampling site, the forest floor was 
searched for 60 min. In this period samples of 
leaf-litter and a few mm of topsoil were also 
taken from several microhabitats that seemed 



234 



DE WINTER & GITTENBERGER 



to be favourable for snails, such as beside 
logs and between roots of trees where dead 
organic material accumulates. Approximately 
four litres of litter from each station were 
sieved in a large cotton bag in which half way 
down a sieve of 15 mm mesh was secured. 
The coarse material was searched for larger 
species on the spot (in small portions on a 
plate), and the material that passed the sieve 
was bagged and dried. The volume of the 
bagged litter varied substantially, depending 
on the amount of decomposed matter relative 
to intact surface leaves and twigs on the for- 
est floor. Litter on top of the rock boulders was 
often more decomposed and contained more 
humus than that on the forest floor proper. 

At many sampling plots, the understorey 
vegetation (about 3/4 m to 3 m high) was sys- 
tematically beaten over an open, inverted um- 
brella. The snails spotted in the umbrella were 
picked out, and the remaining leaves, twigs 
and fine material were bagged for later exam- 
ination. In addition, the trunks of trees were 
carefully searched for about 30 min. The floor 
was searched by the senior author, whilst the 
understorey vegetation and tree trunks were 
generally sampled by E.-J. Semengue, a well- 
trained and dedicated local worker. 

Because there is only low, herbaceous veg- 
etation on the horizontal top surface of the 
rock boulders, both persons engaged in hand 
picking and litter sampling on the rock surface 
for 60 min. Also some non-boulder sites were 
incompletely (only the floor or the vegetation) 
sampled due to various logistic reasons 
(Table 1). In principle, sites visited in 1995 
were sampled again in 1996. However, due to 
logging activities in 1996 a number of sites 
sampled in 1995 were disturbed, and new 
plots were chosen. The exact boundaries of a 
previously visited plot were not always easy to 
determine, because the demarcation poles 
had been removed after the first visit. In order 
to emphasize that the position of a plot visited 
for the second time is likely to deviate some- 
what from that during the first visit, each sam- 
ple was given a unique station number. In 

1995, 16 sites were studied (including those 
on rock boulders), whilst 20 sites (including 
the ones sampled also in 1 995) were visited in 

1996. The approximate location of the sam- 
pling plots is indicated in Figure 2. Table 1 pro- 
vides details of each station. 

In addition, snail shells were extracted from 
eight litter samples taken for hydrological 
studies in May 1996 and kindly provided by M. 
Ruppert. Each of these samples consisted of 



all the leaf-litter present on a floor surface 
quadrate of 50 cm x 50 cm. The quadrates 
were placed randomly with respect to litter 
quantities within a flat patch of 50 m x 50 m 
forest floor, but spots with larger pieces of 
dead wood were avoided. The litter was dried 
in a stove, passed through a 15 mm mesh 
sieve, and the snails from the coarse fraction 
were removed. The fine fraction was retained 
and further dealt with as described below. 

Analysis of Samples 

Some months after collecting, the volume 
of the retained fraction of the floor and boulder 
litter samples was measured. Then the litter 
was passed through three sieves (5 mm, 
2 mm, and 0.5 mm). The finest fraction was 
discarded after the first three bags were ex- 
amined, because it proved to contain no mol- 
luscs. From the coarse fraction snails were 
picked out by eye, whilst the remaining frac- 
tions were systematically searched in small 
portions under a stereo-microscope. 

The bagged material from the vegetation 
was treated in the same manner, but the vol- 
ume was not measured. 

Because of the considerable time interval 
between collecting and searching of the floor 
litter samples, the distinction between empty 
shells and shells that contain a dried-in animal 
proved to be difficult, especially because oc- 
casionally live specimens were observed with 
strongly eroded shells. In this hot, humid and 
acidic environment the decomposition of most 
empty shells (the heavy ones of some Acha- 
tinidae perhaps excluded) probably takes less 
than two months (De Winter, unpublished ob- 
servations). We therefore decided not to dis- 
tinguish between live specimens and empty 
shells in most of the analyses of species di- 
versity and abundance. The relatively few 
snails spotted in the field were included in the 
data obtained from the litter, since direct 
searching took place at the same spots where 
the litter samples were taken. All snails en- 
countered alive were preserved in ethanol in 
order to obtain material for future anatomical 
studies; this collection also served to infer in- 
formation on the species' preferred habitat. 

The snails collected from the tree-trunks 
proved to belong to the same species as 
those collected from the understorey vegeta- 
tion, and were therefore added to these. 

In the field no empty shells were found in 
the vegetation, probably because deceased 
animals will usually drop to the floor. Virtually 



CAMEROONIAN RAINFOREST LAND SNAIL DIVERSITY 



235 



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CAMEROONIAN RAINFOREST LAND SNAIL DIVERSITY 



237 




D82 П83 

D75 




FIG. 2. The approximate location of the sampling 
sites within the square km forest area studied. 
Open squares: sites sampled once, either in 1995 
or 1996; closed squares: sites sampled in both 
years. See Table 1 for further details. The dashed 
line indicates the boundaries of a 9 ha plot used for 
forestry studies. 



all shells extracted from the vegetation litter 
samples were in a fresh condition and pre- 
sumably caught alive. 

Although in some groups (e.g., most Strep- 
taxidae), it is possible to distinguish between 
adult and juvenile shells by the morphology of 
the aperture, most species encountered have 
an undetermined shell growth, and many can 
reproduce before reaching their maximum 
shell size (e.g., Subulinidae). Therefore, we 
did not distinguish between adult and juvenile 
specimens in the analyses. 

Analysis of Diversity Patterns 

The study is of a qualitative rather than a 
quantitative nature. Although searching time 
was standardized, and sampling took place 
within sites not exceeding 0.04 ha, results 
from different sites are not directly compara- 
ble for various reasons. Firstly, due to the het- 
erogeneous structure of the environment, 
floor litter sampling was not at random, but 
concentrated on spots that, subjectively, 
seemed to be favourable for land snails. Sec- 
ondly, in view of the small overall number 
of specimens found, and the high proportion 
of rare species, the presence or absence of 
many species often seemed to be of a sto- 
chastical rather than a systematic nature. 
Thirdly, numbers of live specimens obtained, 
especially of arboreal species, often varied 



greatly between days, and even within days. 
This seemed to be due to variation in climatic 
conditions, especially humidity and tempera- 
ture, rather than to ecological differences be- 
tween sites. Differences in circadian activity 
patterns of the species may also have had an 
effect; nocturnal species are more likely to be 
found early in the morning. In view of these 
limitations, elaborate statistical analyses of 
our data with respect to both species compo- 
sition and abundance appeared to be of little 
value. However, data were sufficient to detect 
some general trends. 

The measures of diversity used in this study 
are overall species richness (S), and Whit- 
taker's index /, which is the total number of 
species recorded (S) divided by the mean 
number of species per site (a), providing a 
measure of diversity difference among sites 
(Magurran, 1988; Cameron. 1992). If /equals 
1 , sites have identical faunas, and higher val- 
ues indicate increasing differentiation. High 
values of / can result from geographical or 
ecological replacement of taxa, or from 
chance effects due to sampling error. These 
patterns can be distinguished by comparing 
the variance of sites per species to the maxi- 
mum variance possible for the same values of 
S and a., as explained in Cameron (1992). If 
the achieved variance is low, replacement ef- 
fects will be more important than chance ef- 
fects, and vice versa. 



Identification and Taxonomy 

The vast majority of the species were clas- 
sified according to shell characters only, 
except for the urocyclid slug-like taxa {Zoni- 
tarion. Verrucarion), of which one adult speci- 
men per sample, if available, was dissected. 
This means that the estimates of the numbers 
of species might be conservative; additional 
cryptic species may be present, especially 
among the shelled Urocyclidae. In view of the 
small size and overall homogeneous nature 
of the area studied, it seems improbable that 
the number of species was overestimated as 
the result of intraspecific variation in shell 
characters. 

The taxonomy and distribution of most land 
snails in Cameroon and elsewhere in western 
Africa are poorly known. Most names used in 
this study are provisional. The use of "cf," in a 
name merely serves to point out a resem- 
blance to a described species. Virtually all ju- 
venile shells could be assigned to a species 



238 



DE WINTER & GITTENBERGER 



by careful comparison of spire dimensions 
and sculpture, especially of the embryonic 
whorls. A few juvenile shells that could not be 
matched with adult specimens of species al- 
ready recognised were treated as separate 
species. Most species were assigned to 
known genera, but it should be kept in mind 
that many of these probably comprise a het- 
erogeneous assemblage of species that are 
more or less similar in shell characters. The 
anatomy of species described from western 
Africa, including type species of genera, is 
generally not or insufficiently known. 



RESULTS 

Faunal Composition 

Table 2 lists the 97 species recognised in 
this study, 34 of which are probably previously 
described, 22 seem to be new to science, and 
41 are of unclear status. A substantial portion 
of the latter group might be undescribed as 
well. The distributions of all 34 described 
species, as well as of a fair number of the re- 
maining ones, extend well beyond the Biboo- 
Minwo region. 

The species found in this study belong to at 
least 12 families, two of which are Proso- 
branchia Mesogastropoda, the remaining Pul- 
monata (Soleolifera and Stylommatophora) 
(Table 3). The family assignment of some 
species is at best tentative in the absence of 
anatomical data. 

The fauna is dominated by three (super)- 
families, the Streptaxidae (33 species), the 
Achatinoidea (27 species, the majority being 
subulinids), and the Helicarionoidea (23 spe- 
cies). Together they constitute 86% of the 
species observed. The Streptaxidae are car- 
nivores, the other two are vegetarians sensu 
lato, as far as is known. 

Streptaxids were both surprisingly speciose 
and abundant, comprising 33 (34%) of the 
species observed and 29% of all individuals 
collected. Gulella (Paucidentina) sp. 1 was 
the most common species in this study, con- 
tributing about 10% of all specimens found 
and present in virtually all sites. Streptaxidae 
were comparatively less diverse and less 
abundant in the collections from the vegeta- 
tion (25% of the species, 1 8% of the individu- 
als) than in those from the forest floor (35% of 
the species and 33% of the individuals). 



Species Diversity and Abundance 

Of the 97 species recorded from the entire 
100 ha area, 80 were found in 1995, nine of 
which were not encountered again in 1 996. Of 
the 88 species observed in 1 996, 1 7 were not 
found in 1995. High species richness was 
also found in smaller areas. An intensively 
studied subarea of 300 m x 300 m (13 sites 
sampled, 6 of which sampled in both seasons; 
Fig. 2), one of several 9 ha plots marked in 
the field for forestry studies and used by us for 
orientation, yielded 83 species, 67 of which 
were obtained in 1995, and 74 in 1996. 

Species diversity and abundance data of 
the sampling sites are summarized in Table 1 . 
The complete data table of the species and 
numbers of specimens per station will be de- 
posited in the archives of the National Mu- 
seum of Natural History, Leiden. The highest 
diversity found during a single visit (in 1 995) of 
a 20 m X 20 m sampling site (Sta022) was 45 
species, which represents 56% of all species 
found in 1995 and 46% of the total fauna ob- 
served in both seasons. Unfortunately, this site 
was disturbed in 1996 and could not be re- 
sampled. Instead, a seemingly similar site ap- 
proximately 25 m to the east (Sta068) was 
sampled; together these two sites yielded 57 
species, or 59% of the total number of species 
observed in block 12. The "revisited" stations 
comprised five plots, of which both the floor 
and the vegetation were sampled, and three 
rock boulder sites (Table 1, Fig. 2). The total 
number of species found during both sampling 
periods varied between 27 and 51 (mean 42.2) 
species among the floor-plus-vegetation plots, 
and between 29 and 39 (mean 33.3) species 
among the boulder sites. 

The diversity patterns were quantitatively 
analysed for stations of which both the floor 
and the vegetation were sampled, as well as 
for collections from the major habitat types 
(floor, vegetation, rock boulders) separately 
(Table 4). 

The floor-plus-vegetation sites (eight in 
1995, 16 in 1996, including five "revisited" 
plots) yielded 95 of the 97 species observed 
(76 in 1995, 86 in 1996). For both years, the 
Whittaker's index /indicates substantial varia- 
tion in species diversity between the stations. 
The proportion of the maximum possible vari- 
ance achieved for stations per species was 
not indicative of significant replacement of 
species (cf. values given in Cameron, 1992; 
Tattersfield, 1996). Whittaker's index values 



TABLE 2. List of 97 land snail species recorded in one square km of rainforest in SW. Cameroon, with num- 
bers of specimens collected in 1 995 and 1 996. Species are ordered according to total number of specimens 
collected. Tentative type of habitat (vertical distribution) is indicated as A (arboreal), F (floor-dwelling), I ("indif- 
ferent") or ? (unknown). In the absense of anatomical data for most species, the Charopidae/Punctidae are 
united in the superfamily Punctoidea, the Subulinidae/Ferussaciidae are grouped with the Achatinidae in the 
Achatinoidea, and the Euconulidae, Urocyclidae and related (sub) families in the Helicarionoidea. If possi- 
ble, the tentative family assignment is also indicated. 







Number 


Number 






SPECIES 


FAMILY 


1995 


1996 


Total 


Habitat 


Gulella {Paucidentina) sp. 1 


Streptaxidae 


142 


128 


270 


F 


Pseudopeas sp. 2 


Achatinoidea/Subulinidae 


93 


61 


154 


F 


Trochozonites cf. pilosus d'Ailly 


Helicarionoidea/Urocyclidae 


91 


40 


131 


1 


Zonitarion semimembranaceus 


Helicarionoidea/Urocyclidae 


71 


47 


118 


A 


(Martens) 












Afropunctum sp. 


Helicarionoidea/Euconulidae 


43 


72 


115 


A 


Dictyoglessula sp. 


Achatinoidea/Subulinidae 


54 


52 


106 


F 


Philalanka ci. dellcatula Thiele 


Punctoidea 


20 


62 


82 


A 


Pseudopeas sp. 3 


Achatinoidea/Subulinidae 


31 


48 


79 


A 


Trochozonites sp. 2 


Helicarionoidea/Urocyclidae 


15 


63 


78 


A 


Thapsia cf. troglodytes (Morelet) 


Helicarionoidea/ Urocyclidae 


42 


30 


72 


1 


Gulella bolocoensis Ortiz & Ortiz 


Streptaxidae 


38 


26 


64 


F 


Cyathopoma n.sp. 


Cyclophoridae 


48 


14 


62 


F 


?Endodontoid n.gen. n.sp. 2 


Punctoidea 


32 


30 


62 


F 


Kaliella sp. 


Helicarionoidea/Euconulidae 


39 


23 


62 


1 


Trochozonites cf. bifilaris (Dohrn) 


Helicarionoidea/Urocyclidae 


36 


14 


50 


I 


Gulella fea/ Germain 


Streptaxidae 


35 


14 


49 


F 


Nesopupa bisulcata (Jickeli) 


Vertiginidae 


26 


20 


46 


F 


Curve IIa s p. 1 


Achatinoidea/Subulinidae 


27 


13 


40 


F 


Ptychotrema (Ennea) silvática 


Streptaxidae 


28 


12 


40 


F 


Pilsbry 












Ischnoglessula sp. 1 


Achatinoidea/Subulinidae 


20 


17 


37 


1 


Pseudopeas sp. 1 


Achatinoidea/Subulinidae 


16 


21 


37 


1 


Plleata sp. 1 


Achatinoidea/Subulinidae 


9 


25 


34 


F 


Gulella {Avakubia) acuminata 


Streptaxidae 


12 


22 


34 


A 


Thiele 












Pseudoglessula sp. 


Achatinoidea/Subulinidae 


13 


20 


33 


F 


Curve IIa s p. 2 


Achatinoidea/Subulinidae 


12 


21 


33 


F 


Trochozonites sp. 4 


Helicarionoidea/Urocyclidae 


25 


8 


33 


F 


Achatina iostoma (Pfeiffer) 


Achatinoidea/ Achatinidae 


28 


2 


30 


1 


Micractaeon koptawelilense 


Achatinoidea/? Ferussaciidae 


9 


21 


30 


F 


(Germain) 












Gudeella'sp. 1 


Helicarionoidea/Urocyclidae 


5 


25 


30 


1 


Maizaniella (Spirulozania) n.sp. 


Maizaniidae 


14 


15 


29 


F 


Gulella {Pupigulella) pupa Thiele 


Streptaxidae 


15 


14 


29 


1 


Subulona sp. 


Achatinoidea/Subulinidae 


9 


19 


28 


F 


Streptostele sp. 3 


Streptaxidae 


10 


14 


24 


F 


Ptychotrema {Ennea) cf. aillyi 


Streptaxidae 


7 


16 


23 


A 


Adam 












Afroguppya sp. 1 


Helicarionoidea/Euconulidae 


14 


9 


23 


F 


Ischnoglessula sp. 2 


Achatinoidea/Subulinidae 


15 


7 


22 


A 


Gulella (Avakubia) cf. 


Streptaxidae 


11 


11 


22 


A 


avakubiensis Pilsbry 












Ptychotrema cf. columellahs 


Streptaxidae 


11 


10 


21 


F 


(Martens) 












Alllya s p. 1 


Aillyidae 


20 


1 


21 


F 


Maizaniella ( Macromaizaniella) 


Maizaniidae 


12 


8 


20 


F 


preussi (Martens) 












Gulella cf. suturalis Degner 


Streptaxidae 


9 


10 


19 


A 


Ptychotrema (Excisa) duseni 


Streptaxidae 


4 


15 


19 


F 


(d'Ailly) 












Aillya sp. 2 


Aillyidae 


19 





19 


F 


Ptychotrema ( Ennea) cf. 




10 


8 


18 


1 


perforatum (d'Ailly) 


Streptaxidae 


8 


10 


18 


A 


Edentulina libehana (Lea) 


Streptaxidae 


4 


12 


16 


F 


Gulella (Costigulella) n.sp. 


Streptaxidae 


12 


4 


16 


1 


Prositala cf. butumbiana 


Punctoidea 










(Martens) 










(continued) 



240 

TABLE 2. (Continued) 



DE WINTER & GITTENBERGER 







Number 


Number 






SPECIES 


FAMILY 


1995 


1996 


Total 


Habitat 


?Endodontoicl n.gen. n.sp. 1 


Punctoidea 


7 


8 


15 


F 


Afroguppya s p. 2 


Helicarionoidea/Euconulidae 


5 


10 


15 


F 


Trochozonites sp. 7 


Helicarionoidea/Urocyclidae 


8 


6 


14 


A 


Trochozonites sp. 8 


Helicarionoidea/Urocyclidae 


6 


7 


13 


A 


Gulella (Avakubia) n.sp. 


Streptaxidae 


4 


8 


12 


A 


Trochozonites sp. 1 


Helicarionoidea/Urocyclidae 


11 


1 


12 


A 


Callistoplepa sliuttlewortiii 


Achatinoidea/Achatinidae 


5 


6 


11 


1 


(Pfeiffer) 












Gulella (Conogulella) sp. 


Streptaxidae 


3 


8 


11 


1 


Streptostele sp. 2 


Streptaxidae 


4 


7 


11 


F 


Pupisoma sp. 


Vertiginidae 


3 


7 


10 


1 


Gulella cf. germaini Connolly 


Streptaxidae 





9 


9 


F 


Streptostele sp. 1 


Streptaxidae 


4 


5 


9 


F 


Gulella (Paucidentina) sp. 2 


Streptaxidae 


2 


6 


8 


F 


Pileata s p. 2 


Achatinoidea/Subulinidae 


5 


1 


6 


F 


Sinistrexcisa cameruniae 


Streptaxidae 





6 


6 


F 


De Winter. Gomez & Prieto 












Trochozonites sp. 6 


Helicarionoidea/Urocyclidae 


2 


4 


6 


A 


Gonaxis camerunensis (d'Ailiy) 


Streptaxidae 


2 


3 


5 


F 


Pseudoveronicella sp. 


Veronicellidae 





5 


5 


1 


Archachatina margínala 


Achatinoidea/Achatinidae 


2 


2 


4 


1 


(Swainsson) 












Pseudachatina cf. downesii 


Achatinoidea/Achatinidae 





4 


4 


A 


(Gray) 












Subulina sp. 


Achatinoidea/Subulinidae 


2 


2 


4 


A 


Pseudopeas sp. 4 


Achatinoidea/Subulinidae 





4 


4 


? 


Gulella (Paucidentina) cf. 


Streptaxidae 


2 


2 


4 


1 


con/ca (Martens) 












Ptychotrema (Ennea) cf. 


Streptaxidae 


1 


3 


4 


F 


complicatum (Martens) 












Gudeella sp. 2 


Helicarionoidea/Urocyclidae 





4 


4 


F 


Verrucanon sp. 


Helicarionoidea/Urocyclidae 


3 


1 


4 


A 


Trochozonites sp. 9 


Helicarionoidea/Urocyclidae 





4 


4 


A 


Trochozonites sp. 1 


Helicarionoidea/Urocyclidae 





4 


4 


A 


Gulellal Ennea spec. 


Streptaxidae 


1 


2 


3 


9 


Edentulina martensi (Smith) 


Streptaxidae 


2 


1 


3 


F 


Streptostele sp. 5 


Streptaxidae 





3 


3 


F 


Trochozonites cf. adansoniae 


Helicarionoidea/Urocyclidae 





3 


3 


A 


(Morelet) 












Trochozonites sp. 5 


Helicarionoidea/Urocyclidae 


2 


1 


3 


F 


Ischnoglessula sp. 3 


Achatinoidea/Subulinidae 





2 


2 


A 


Pseudopeas ci. fea/ Germain 


Achatinoidea/Subulinidae 





2 


2 


F 


Gulella cf. fernandensis 


Streptaxidae 


2 





2 


F 


Ortiz & Ortiz 












Streptostele sp. 4 


Streptaxidae 


1 


1 


2 


F 


Trachycystis cf. iredalei 


Punctoidea 


2 





2 


A 


(Preston) 












Trochozonites sp. 3 


Helicarionoidea/Urocyclidae 


1 


1 


2 


A 


Archachatina camerunensis 


Achatinoidea/Achatinidae 


1 





1 


A 


d'Ailiy 












Lignus solimanus (Morelet) 


Achatinoidea/Achatinidae 


1 







A 


Leptocala mollicella (Morelet) 


Achatinoidea/Achatinidae 


1 







1 


Kempioconcha sp. 


Achatinoidea/Subulinidae 


1 







F 


Opeas sp. 


Achatinoidea/Subulinidae 





1 




? 


?Ferussaciidae/Subulinidae sp. 


Achatinoidea 





1 




? 


Gulella n.sp. 


Streptaxidae 





1 




? 


Ptychotrema (Parennea) n.sp. 


Streptaxidae 


1 







F 


?Gonaxis spec. 


Streptaxidae 


1 







7 


?Endodontoid n. gen. n. sp. 3 


Punctoidea 





1 




? 


Zonitarion sp. 1 


Helicarionoidea/Urocyclidae 





1 




F 


Totals 




1,362 


1,292 


2,654 





CAMEROONIAN RAINFOREST LAND SNAIL DIVERSITY 



241 



TABLE 3. Systematic list of (super)families and species numbers of land snails found in one square km of 
rainforest in soutfiwestern Cameroon and their tentative vertical distribution. 





No. Species 




VERTICAL DISTRIBUTION 




Taxon 


Floor 


Arboreal 


"Indifferent" 


Unknown 


PROSOBRANCHIA 












MESOGASTROPODA 












Cyclophoridae 


1 


1 


— 


— 


— 


Maizaniidae 


2 


2 


— 


— 


— 


PULMONATA 












STYLOMMATOPHORA 












Vertiginidae 


2 


1 


— 


1 


— 


Achatinoidea 


27 


11 


7 


6 


3 


Achatinidae 


7 


— 


3 


4 


— 


Subulinidae 


18 


10 


4 


2 


2 


?Ferussaciidae 


2 


1 


— 


— 


1 


Streptaxidae 


33 


20 


6 


4 


3 


Punctoidea 


6 


2 


2 


1 


1 


Aillyidae 


2 


2 


— 


— 


— 


Helicarionoidea 


23 


6 


12 


5 


— 


Euconulidae 


4 


2 


1 


1 


— 


Urocyclidae 


19 


4 


11 


4 


— 


GYMNOMORPHA 












SOLEOLIFERA 












Veronicellidae 


1 


— 


— 


1 


— 


TOTALS 


97 


45 


27 


18 


7 



for samples from the floor and vegetation sep- 
arately are somewhat greater than for floor- 
plus-vegetation plots, whilst those for the 
boulder sites are smallest. 

Most species occurred in low numbers 
(Table 2). Both in 1995 and 1996, 64% of the 
species were represented by less than 1% of 
all specimens obtained, about one third took 
up 1-5%, and only a few species were more 
common. 

Snail abundance was generally low. Collec- 
tions from all stations in 1995 and 1996 to- 
gether yielded 2,654 specimens. There was 
considerable variation among plots and habi- 
tats (forest floor, vegetation, boulder) in the 
number of specimens collected (Table 4). 
Boulder sites tended to yield more individuals 
than sites on the forest floor proper, but these 
differences disappear if abundance is ex- 
pressed as snails per litter volume. The 
greater number of specimens collected from 
rock boulders might be at least partly due to 
the greater volume of boulder litter sampled, 
because boulder litter was generally more de- 
composed, and thus finer, than that on the for- 
est floor. Numbers of snails collected from the 
arboreal habitats also varied greatly, which 
seemed to be strongly dependent on weather 
conditions. 

The eight litter samples from 0.25 m^ (50 
cm X 50 cm) floor quadrates collected in 1 996 



give an impression of the magnitude and vari- 
ation of snail density, species richness, and 
amount of leaf-litter per surface unit of forest 
floor (Table 5). The data illustrate some char- 
acteristic features of this forest: (1) the vari- 
ability in the amount of (partly decomposed) 
litter on the forest floor; (2) the low abundance 
of snails (12-52 snails/m^ of forest floor, 8- 
20 shells/I sieved litter); (3) the low speci- 
mens;species ratio; and (4) the high species 
diversity. Comparison of the abundance data 
of these randomly taken samples (Table 5) 
with those provided in Table 1 and Table 6 
suggests that the average snail density per 
surface unit of forest floor is generally lower 
than appears from the data of the 0.04 ha 
sites, which are based on choice litter taken 
from seemingly favourable microhabitats. 

Differences Between Sampling Periods 

The total number of specimens found in 
both seasons was about the same (1,362 in 
1995, 1,292 in 1996), but, due to the greater 
number of sites sampled in 1996, mean num- 
ber of specimens per site was considerably 
smaller than in 1 995 (Table 4). The total num- 
ber of species found in 1995 (80) was smaller 
than in 1996 (88). Mean number of sites per 
species was relatively greater in 1995 than in 
1996. 



242 



DE WINTER & GITTENBERGER 



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CAMEROONIAN RAINFOREST LAND SNAIL DIVERSITY 



243 



TABLE 5. Snails from a 0.5 m x 0.5 m floor surface 
quadrat, witfi tfie number of species and speci- 
mens, the volume of sieved litter, and the number oi 
specimens per litre and per m^. 





Number 


Number 


Litter 


Shells/ 






of 


of 


vol. 


litre 


Shiells/ 




species 


shiells 


(litres) 


of litter 


m^ 


Sample 












1 


10 


13 


0.9 


14.4 


52 


2 


5 


6 


0.3 


20.0 


24 


3 


2 


3 


0.25 


12.0 


12 


4 


4 


5 


0.25 


20.0 


20 


5 


4 


4 


0.5 


8.0 


16 


6 


4 


4 


0.35 


11.4 


16 


7 


4 


4 


0.25 


16.0 


16 


8 


6 


7 


0.4 


17.5 


28 


Totals 


22 


46 


3.2 


— 


— 


Mean 


4.9 


5.7 


0.4 


13 


23 



For many species, the number of speci- 
mens per species varied considerably be- 
tween the two sampling periods (Table 2). 
Histograms of species frequencies ordered 
according to decreasing relative abundance 
(% of total specimens) describe a hollow 
curve both for 1 995 and 1 996, but the ranking 
order of the species in 1 995 differed consider- 
ably from that in 1 996 (Fig. 3). More than one- 
fourth (26) of the species was found uniquely 
either in 1 995 or in 1 996. Of 25 of the species 
found in both seasons, the relative abun- 
dance differed 50% or more between years. 
Achatina iostoma, for instance, was repre- 
sented in 1 995 by three adult shells and 25 ju- 
veniles of about 20-30 mm, whilst in 1996 
only two adult specimens were encountered. 
Of Trochozonites cf. pilosus and T. cf. bifilaris 
only clearly juvenile shells were observed in 



the 1996 samples, whereas both adults and 
juveniles occurred in much larger numbers in 
1 995. Only one out of 40 specimens of the two 
Aillya species found was collected in 1996. 
Such data are suggestive of a life cycle of one 
year or less. The relative abundance of 46 
species differed less conspicuously between 
years. 

For both floor and boulder sites, the ab- 
solute number of individuals found per site 
was generally higher in 1995 than in 1996. 
However, the mean number of species in the 
floor sites did not differ between the two sam- 
pling periods, whilst in the boulder sites mean 
species richness was much greater in 1995 
(Table 4). This general trend was also ob- 
served by comparisons of the eight sites that 
were sampled in both seasons. The number 
of individuals per species in the floor samples 
was significantly lower in 1996 than in 1995, 
whereas these ratios were the same in the 
boulder sites (Table 1). 

Standardized per litter volume, the median 
number of specimens in 1 995, calculated over 
all floor and boulder litter samples, was signif- 
icantly higher than in 1 996 (Table 6; one-tailed 
Mann-Whitney test, Z = 3.92, P = 4.5 x 10-^), 
as was the median number of species (Table 
6; one-tailed Mann-Whitney test, Z- 3.12, P = 
0.91 X 10'^). The larger total number of 
species found in 1996 might be due to the 
larger number of sites sampled, and the al- 
most double total volume of (sieved) floor lit- 
ter taken in that year, increasing the chance of 
finding new, rare species. 

Values of Whittaker's index /for 1995 and 
1996 (Table 4) indicate that differences in 
species diversity among sites were greater in 
1996 than in 1995. This might well be related 



12-1 



'4 1 996 
Vo 1 995 




FIG. 3. Relative abundance (% of the total number of specimens collected in each season) of 97 land snail 
species in 1995 and 1996, ordered according to decreasing abundance in 1995. 



244 



DE WINTER & GITTENBERGER 



TABLE 6. Gastropod diversity and abundance in litter samples taken from the forest floor and from rock boul- 
der in 1995 and 1996, expressed as number of specimens or species per litre of sieved litter. 





Median 


Range 


Nsamples 


Total litter volume 


Total specimens 


Specimens/litre 












1995 


49.3 


22.2-88.2 


15 


19.75 


1009 


1996 


21.1 


9.2-61.2 


20 


36.2 


899 


Species/litre 












1995 


15.3 


7.7-25.4 


15 






1996 


10.6 


5.0-18.4 


20 







to the lower number of specimens per station 
in 1996 (Table 4), and thus partly result from 
sampling error. 

Vertical Distribution 

The fauna appeared to be stratified with 
species confined to the ground, species con- 
fined to arboreal habitats, and species inhab- 
iting both levels. A majority of 45 species 
(46%) were classified as floor dweller (F), on 
evidence that live specimens were almost ex- 
clusively found on the forest floor and on boul- 
ders, or because specimens of (minute) 
species commonly found in the floor litter 
were never obtained from the vegetation. This 
class includes seven species that were nor- 
mally encountered on the floor, but of which 
the odd specimen was found in samples from 
the vegetation. Species of which live speci- 
mens were only found in the vegetation at 3/4 
m or more above the ground (27 species, 
28%) were considered to have arboreal habits 
(A), assuming that the relatively few shells 
found on the forest floor were from deceased 
animals that had dropped to the ground. The 
remaining snails that were regularly found 
alive (18 species, 19%), were classified as 
"indifferent" (I). Information on the vertical dis- 
tribution of some uncommon species could be 
derived from nearby undisturbed forest sites 
not covered in this report. Of seven species 
(7%) insufficient information was available. 
The tentative vertical distribution of the indi- 
vidual species is listed in Table 2. 

All major families have representatives in 
the three classes (F, A, I) recognised (Table 
3), only the Achatinidae have no true floor- 
dwelling species. The majority of the Subulin- 
idae and Streptaxidae species are ground 
dwellers, whilst of the Urocyclidae signifi- 
cantly more species have arboreal habits. 

The upper, horizontal surface of the large 
rock boulders constitutes a special habitat. 
Five to 15 m^ of horizontal rock surface 
yielded up to 31 species during a single visit 



(Table 4). Despite intensive searches, snails 
were never observed on the steep flanks of 
the 3-5 m high outcrops. Although these 
rocks are virtually devoid of higher vegetation, 
a relatively significant proportion of the shells 
found in the litter belongs to arboreal species. 
There are usually one or more spots where 
the woody understorey vegetation grows 
against the flanks of the boulder, often at- 
tached to it by climbers. Possibly some arbo- 
real species migrate between the vegetation 
and the rock habitat, the microclimates of 
which might resemble each other. 

The occurrence of a limited number of 
species, such as Cyathopoma n. sp., Pty- 
chotrema (Ennea) silvática, Gulella bolocoen- 
sis. Gulella (Costigulella) n. sp., and Gulella 
(Pupigulella) pupa, might be associated with 
the presence of bare rock, but none were con- 
fined to the giant boulders. 

Shell Size and Shape 

Shell height (H) and diameter (D) were 
measured from an "average" adult specimen 
of each of 86 species, (semi-)slugs and 
species known by only juvenile shells being 
excluded. H ranges between 0.8 and 1 65 mm, 
D between 0.9 and 94 mm. Figure 4 gives the 
distributions of H and D. Major shell dimen- 
sion (H or D) of 32 species (37%) is less than 
5 mm, and of another 32 species (37%) be- 
tween 5 and 10 mm. Shells of eight species 
(9%) measure between 10 and 20 mm, and 
those of 14 species (16%) are larger than 20 
mm, four of which have adult shell heights ex- 
ceeding 90 mm. 

Ground-dwelling species did not differ in 
major shell dimension (H or D) from the arbo- 
real (two-tailed Mann-Whitney test, Z = 1.12, 
P = 0.26), "indifferent" (Z = 1.64, P = 0.10), or 
arboreal plus "indifferent" species (Z = 1 .65, P 
= 0.10). 

We examined the shell shape distribution of 
the floor-dwelling, arboreal and "indifferent" 
species separately, as well as that of these 



CAMEROONIAN RAINFOREST LAND SNAIL DIVERSITY 



245 



% 35 - 




<1 1-3 3-5 5-10 10-20 20-50 >50 

Shell Height (mm) 



All (N=82) 




04 08 12 16 20 24 28 32 36 40 44 



Floor (N=40) 




)4 8 12 16 2 2.4 2 8 3 2 3 6 4 44 




Arboreal (N=25) 



<1 1-3 3-5 5-10 10-20 20-50 >50 

Shell Diameter (mm) 

FIG. 4. Shell height (upper graph) and shell diame- 
ter (lower graph) distributions of 86 land snail 
species found within one square km of Cameroon- 
ian rainforest. 



three groups together (Fig. 5). All distributions 
in Figure 5 are bimodal, due to relatively many 
species with "globose" (H/D 0.8-1.2) and 
moderately tall to very tall shells (H/D > 1.6). 
Of 82 species, H:D ratios were calculated, ex- 
cluding six slug-like species (two Zonitarion, 
one Verrucarion. one Pseudoveronicella. and 
two Aillya), and nine species with unknown 
vertical distributions or with only juvenile 
shells available. The H:D ratio distribution of 
the floor-dwelling species did differ from nei- 
ther that of the arboreal species (two-tailed 
Mann-Whitney test, Z = 1.26, P - 0.21), nor 
that of the "indifferent" species (Z = 1 .01 , P = 
0.31) or the arboreal and "indifferent" species 
together (Z= 1.42, P = 0.15). 



DISCUSSION 
Species Richness 

The malacofauna of this small patch of acid 
rainforest was found to be extremely rich in 




04 08 12 16 2 2.4 28 32 36 40 44 

Shell Height : Diameter ratio 

FIG. 5. Shell height:diameter ratio distributions of 
82 land snail species found within one square km of 
Cameroonian rainforest (upper graph), as well as of 
the floor-dwelling, arboreal and "indifferent" species 
separately. 



species. Although comparisons with other 
studies are hampered by a lack of standardis- 
ation with respect to area size and sampling 
methods, this Cameroonian area might well be 
the globally most species-diverse locality 
known with respect to land molluscs. The rich- 
est site reported so far is Waipipi Reserve, 
Manakau Peninsula, New Zealand. Solem et 
al. (1981) reported 60 species from this 4 ha 
site, and a total number of 72 native species 
from a surrounding area of approximately 50 x 
1 5 km (but see Emberton (1 985) for somewhat 
lower numbers). Other species-rich sites (all 
approx. 4 ± 2 ha) include Pine Mountain, Ken- 
tucky, U.S.A., where L. Hubricht collected 44 
species, and a patch of lowland rainforest near 
Manombo Village, Fianarantsoa Province, 
Madagascar, where 52 species were found 
(both sites described in Emberton, 1995). Tat- 
tersfield (1997) reported 50 species from 27 



246 



DE WINTER & GITTENBERGER 



plots of 40 m X 40 m each in Kakamega For- 
est, an area of approximates 265 km^ in west- 
ern Kenya, the richest of which yielded 33 
species. In this paper, we report 97 species in 
100 ha of rainforest, 83 species within a 9 ha 
subarea, up to 45 in a sampling site of 20 m x 
20 m during a single visit, and up to 51 species 
in sites sampled twice. In all cases, the actual 
floor surface sampled is much smaller than 
0.04 ha. Up to 10 species were found in litter 
from a 0.5 m X 0.5 m plot. 

In view of the large proportion of rare 
species, it is likely that the actual number of 
species will even be greater than 97, Several 
parametric and non-parametric methods have 
been developed to estimate the actual species 
richness in similar situations, based on the fre- 
quency of rare species in a sampling program. 
According to Colwell & Coddington (1995) the 
Chao-2 and second-order Jackknive estima- 
tors provide the least biased estimates of true 
species richness for small numbers of sam- 
ples. Both estimators are based on presence- 
absence data, and take into account the num- 
ber of species that occur in only one or in two 
samples. These two methods were applied to 
all stations in 1 995 (8) and 1 996 (1 6) of which 
both the forest floor and vegetation were sam- 
pled. The total number of species observed in 
these plots was 95. The Chao-2 and second- 
order Jackknive estimates are 107 and 110 
species, respectively. Subtracting the two 
species found in the remaining samples, there 
may be at least 105-108 species present in 
this 100 ha area, especially since these non- 
parametric estimators usually underestimate 
the true species richness (Colwell & Codding- 
ton, 1995). 

Possible Explanations for the High 
Species Diversity 

Of the factors favouring high land snail di- 
versity that were discussed by Solem (1984), 
three might be involved in the situation de- 
scribed here: leaf-litter characteristics, lack of 
disturbance for prolonged periods of time, and 
stable moisture supply. 

Leaf-litter associated parameters are likely 
to be important for the high species diversity 
observed. The majority of species found are 
floor dwellers, but since leaf-litter occurs also 
patchily on the understorey vegetation above 
the forest floor, these factors might also affect 
certain arboreal taxa. With more than 125 
species of trees per ha, the composition and 



architecture of litter deposits are obviously 
highly variable. Leaf-litter is unequally distrib- 
uted on the forest floor, and thicker litter accu- 
mulations seemed to contain more individuals 
and species than spots with thin litter de- 
posits, as was also found by Solem et al. 
(1 981 ) in New Zealand. Even in tropical ever- 
green forests trees periodically shed their 
leaves, but not synchronised like in temperate 
regions (e.g.. Medway, 1972; HIadik, 1978). 
Thus, thickness, distribution and composition 
of litter layers are dynamic in both space and 
time. The great variety in size, shape and firm- 
ness of the leaves, combined with differential 
decomposition rates by spot differences in mi- 
croclimate, moisture and soil conditions, po- 
tentially provides a wide array of microhabi- 
tats supporting a high land snail diversity of 
vegetable matter and fungi consumers, and 
associated predator species. These factors 
might partly be involved in the apparent sea- 
sonality of the snail fauna observed that might 
otherwise not be expected in an evergreen 
forest. 

There are only few published reports sup- 
porting the view that litter parameters are re- 
lated to land snail species diversity, for exam- 
ple, those by Solem et al. (1981) on New 
Zealand, and by Getz & Uetz (1994) on North 
American forests. Solem's (1984) assertion 
that rainforests have negligible litter deposits 
and. therefore, support a little diverse land 
snail fauna certainly does not hold for the 
forests of western Africa. 

The fauna of this small area is also diverse 
in taxa above the species level, and seems to 
include few species that are closely related 
(as judged largely from conchological charac- 
ters). The species belong to a considerable 
number of (sub)genera. Several of the larger 
generic entities used here are actually com- 
posed of various, as yet largely unnamed, dis- 
tantly related genera. For example, anatomi- 
cal studies have revealed that Trochozonites, 
the most speciose genus found, is an artificial 
taxon embracing at least four groups of 
species, despite their similarity in shell char- 
acters (Ortiz de Zarate, 1951). Local specia- 
tion therefore seems to have contributed little 
to the high species richness observed. It is 
much more probable that this land snail fauna 
gradually accumulated in the area, possibly 
over long periods of time. 

In the dry and relatively cold glacial periods, 
the size of the African forest belt was much re- 
duced to a small number of discrete areas. 



CAMEROONIAN RAINFOREST LAND SNAIL DIVERSITY 



247 



The study area is situated within such a puta- 
tive Pleistocene forest refugium (Maley, 
1996). Whether this is in any way related to 
the high actual species richness can only be 
investigated by comparison with other areas, 
both within and outside the hypothesized refu- 
gia. 

Absence of stress periods by prolonged 
droughts probably favours high species diver- 
sity, because the moisture regime determines 
the possible activity pehods of land snails 
(Solem et al., 1981). Even in the driest peri- 
ods of the year the study area receives up to 
80 mm precipitation per month (Waterloo et 
al, 1997). According to Solem (1984) rain- 
forests suffer from too much rain, which 
causes leaching of nutrients, and are there- 
fore little diverse in land snails. 

If the proportion of arboreal species in this 
fauna is truly greater than in other faunas, this 
might also be a factor contributing to the high 
species diversity. Waipipi Reserve in New 
Zealand had only 1 4 out of 60 species with ar- 
boreal habits, including several which live 
both on the floor and in the vegetation (Solem 
et al., 1 981 : Solem & Climo, 1 985). There ap- 
pear to be hardly any published data on 
the number of arboreal species in other fau- 
nas, however. Most studies appear to have 
adopted sampling techniques that underesti- 
mate the numbers of arboreal taxa present. 

Diversity Pattern and Sampling Error 

The analysis of the data suggests that the 
diversity of this fauna is essentially sympatric, 
because no indication of geographic or eco- 
logical replacement of species was found. 
There are no obvious barriers to dispersal; the 
forest cover is homogeneous, and the 
streams in the study area are 5 m wide at 
most. However, the concept of sympatric di- 
versity is difficult to apply (De Winter, 1995: 
Emberton, 1995). This holds especially for 
rainforests, where it is almost impossible to 
find "restricted habitats with a homogeneous 
set of dominant plant species" (Solem, 1980). 
Although the low overall density of snails in 
this area is undoubtedly an effect of the low 
pH and the low mineral content of the soil, the 
actual numbers of live collected snails 
seemed to be very much dependent on 
weather conditions. The greatest numbers of 
live specimens were obtained during damp, 
warm conditions, as occur after heavy rains in 
the night and early morning followed by hot. 



sunny weather. After several days without 
precipitation rather few live snails were found, 
but during rain sampling was also less suc- 
cessful. 

Dry conditions especially had a negative ef- 
fect on the numbers of (semi)arboreal snails 
collected, due to problems in finding the sites 
where the snails hide. Solem et al. (1 981 ) re- 
ported that some shelled arboreal taxa seal 
themselves firmly to the vegetation duhng dry 
periods, and in hindsight it seems possible 
that we not always applied enough force to 
shake these from their resting sites. Other 
species, notably slug-like taxa, probably 
seek shelter in holes and fissures of tree 
trunks. 

The effect of climatic conditions is best il- 
lustrated by considering the data of the most 
diverse plot, Sta022, where 45 species were 
collected during a single visit. The richness of 
this plot was due to an exceptionally large 
number of specimens and species collected 
from the vegetation during optimal weather 
conditions as deschbed above. The snail 
numbers found in the vegetation were much 
greater than on the floor, and the number of 
species found in both habitats was the same 
(Table 1). The number of species collected 
from the floor was not excessive, and several 
relatively common species were not repre- 
sented. Under favourable conditions and by 
taking greater leaf-litter samples, it should be 
possible to find perhaps as much as 75% of 
the entire malacofauna within a single 0.04 ha 
plot. 

Thus, in view of high proportion of the total 
fauna that can be found in a few square meter 
of forest, sampling error — resulting from the 
large proportion of rare species, the low over- 
all snail abundance, and the varying weather 
conditions during sampling — has very likely 
had a significant effect. The differences in 
species composition found among the sites 
sampled in the same season, as indicated by 
the values of Whittaker's /, are therefore likely 
to be inflated. Geographic replacement of taxa 
also would seem unlikely in view of the small 
size and overall homogeneous nature of the 
study area. Sampling needs to be done at a 
much finer scale in order to detect differences 
in microhabitat preferences among species. 
Sampling error constitutes a serious problem 
for quantitative studies in these forests. Timed 
searching, as recently advocated by Ember- 
ton et al. (1996), does not seem to solve the 
problem, because it will inevitably result in 



248 



DE WINTER & GITTENBERGER 



overlooking even more species, especially the 
tiniest ones. 

Streptaxid Diversity 

The very large proportion of carnivorous 
species (all Streptaxidae) in a land snail fauna 
is a remarkable phenomenon, which is unique 
to the Afrotropical region as far as known. In 
the Manakau Peninsula, New Zealand, only 
four out of 72 species are carnivores, all be- 
longing to the Rhytididae (Solem et al., 1 981 ). 
The rainforest fauna of Manombo Reserve, 
Madagascar, has eight (15%) streptaxid spe- 
cies. Substantial proportions of Streptaxidae 
have been reported for much larger areas 
elsewhere in Africa, such as the former Bel- 
gian Congo (Pilsbry, 1919) and East Africa 
(Kenya, Tanzania and Uganda: Verdcourt, 
1 983). On a smaller geographic scale the pro- 
portion of streptaxid species seems to vary 
greatly. Tattersfield (1996) found nine (18%) 
streptaxids out of 50 land snail species in 
Kakamega Forest in Kenya, whilst in eastern 
Tanzania the proportion of Streptaxidae in- 
creased with altitude from about one fourth of 
the species below 500 m to 46% at a single 
station at 1 000 m, taking up to one third of the 
collected individuals (Emberton et al., 1997). 

The conspicuous radiation of the Streptaxi- 
dae contributes substantially to the species 
diversity here and elsewhere in tropical Africa. 
Maybe these carnivorous snails occupy a 
segment of the ecological space filled by non- 
molluscan invertebrates outside the Ethiopian 
region. However, any data supporting this 
speculation are completely lacking. At pres- 
ent, no satisfactory explanation for this high 
proportion of carnivorous snails can be of- 
fered. 

Emberton et al. (1 997) surmised that "surely 
many of these streptaxid species must take 
nonmolluscan prey". However, in the course of 
six months of fieldwork in Cameroon, various 
streptaxid species have been only found feed- 
ing on other land snails or (in one occasion) 
their eggs. These incidental observations 
show that at least some species are not selec- 
tive with respect to the species and size of their 
prey. Edentulina libehana, for example, was 
found to attack some ten species of snails and 
semi-slugs (including observations from sites 
in Cameroon not described in this report), 
some up to twice its size. However, the con- 
siderable size-range of the streptaxids in this 
fauna (adult shell height 1 .5-37.4 mm) is sug- 
gestive of quite some variation in feeding 



habits. Theoretically, Streptaxidae could live 
as scavengers on carrion, because at least 
two reports (Berry, 1963; Aiken, 1981) claim 
that some species feed in captivity on (mam- 
malian) liver. 

Shell Size and Shape 

The malacofauna of block i2 occupies an 
enormous shell size range, but the vast ma- 
jority of the species are rather small. Ember- 
ton (1995) provided shell size distributions of 
three diverse sympatric faunas, using shell di- 
ameter as an index of shell size. The shell di- 
ameter distribution reported here strongly 
resembles that found in the Manombo rainfor- 
est, Madagascar. The proportion of "minute 
species" (sensu Emberton, 1995; D between 
0.5-5 mm) is virtually identical (66%), and in 
both faunas giant species (D > 40 mm) are 
represented. The other two faunas (Pine 
Mountain, U.S. A, and Waipipi Reserve, New 
Zealand) have very different size distribu- 
tions. In New Zealand, 85% of the species are 
minute, and the remaining species are all 
smaller than 10 mm. In the U.S.A., giant 
species are lacking, and minute taxa consti- 
tute only 40% of the total fauna, the remaining 
species being approximately evenly distrib- 
uted among the size classes. 

Peake (1968) found in Solomon Island rain- 
forests that ground-dwelling snails have a 
much more restricted shell-size range with 
generally smaller shells than arboreal or 
partly arboreal species. Here we observed 
that shells of species regularly exceeding 50 
mm in height occur only in the arboreal and 
"indifferent" taxa. However, giant species (all 
Achatinidae) constitute a minor proportion of 
the total fauna, and shell dimensions of floor- 
dwelling and (partially) arboreal taxa were not 
different statistically. 

The shape distribution of land snail shells 
was analysed by Cain (1977, 1978a, b, 1980) 
for a number of faunas. He observed that in 
most faunas species have shells that are ei- 
ther clearly higher than wide or wider than 
high, comparatively few having shells with ap- 
proximately equal height and width. Cain 
(1978b; 219) suggested that species with 
high-spired shells tend to forage on vertical 
surfaces, and hence occur especially on rock 
faces and in trees; taxa with low-spired shells 
were hypothesized to feed more commonly 
on horizontal surfaces, and species with 
shells of about equal height and width to show 
little preference. 



CAMEROONIAN RAINFOREST LAND SNAIL DIVERSITY 



249 



The distribution of H:D ratios of the shells 
found in this study deviates from those in the 
three sympatric faunas discussed by Ember- 
ton (1995). There are relatively many high- 
spired species, even more than in Madagas- 
car, including some species in the 4.0-4.4 
class, which is absent in Emberton's material. 
This is mainly due to the large proportion of 
subulinid species in the area studied. Another 
remarkable characteristic of this fauna is the 
very large proportion of shells in the 0.8-1.2 
("globose") class, and the apparent deficit of 
species in the 1.2-1. 6 class. In the other three 
sympatric faunas, as well as in most large- 
scale faunas studied by Cain, the shell shape 
distribution is characteristically bimodal due to 
a deficit of globose-shelled snails. Most glo- 
bose-shelled species are helicarionoids, es- 
pecially of the heterogeneous genus Tro- 
chozonites, the 13 members of which have 
pyramidal shells, and tend to have arboreal 
habits, comprising only one true floor-dwelling 
species. 

Cain (1978a) reported a relatively high pro- 
portion of globose species in the Helicostyli- 
nae of the Philippines and the Papuininae of 
the New Guiñean area, most of which are ar- 
boreal species in rainforests. Emberton 
(1995) found arboreal species in a Madagas- 
can rainforest to be globose rather than high- 
spired. Thus, perhaps there is some tendency 
in rainforest areas for globose-shelled 
species to have arboreal habits. 

The suggestion that there might be a corre- 
lation between shell shape and preferred 
habitat has received experimental support for 
some British species (Cain & Cowie, 1978; 
Cameron, 1978, 1981; Cook & Jaffar, 1984), 
but does not seem to hold for high-spired 
Malagasy snails (Emberton, 1 995), nor for the 
species studied here. Differences in shell 
shapes between geographically separate fau- 
nas generally appear to have a stronger taxo- 
nomic bias, like the great diversity of the high- 
spired Subulinidae in tropical Africa. 



ACKNOWLEDGEMENTS 

Many people directly or indirectly involved 
in the Tropenbos Cameroon Project provided 
invaluable support during fieldwork by the first 
author. Special thanks are due to Wyb 
Jonkers and Wim van Driel (Wageningen 
Agricultural University, TCP) for allowing to 
use the infrastructure, transport and other fa- 
cilities of the project; to Barend van Gemer- 



den, Gerard Hazeu and Maarten Waterloo 
(Winand Staring Centre, Wageningen) and 
Marc Parren (Wageningen Agricultural Uni- 
versity) for providing data on the vegetation, 
soil, hydrology, and tree diversity, respec- 
tively, and for helpful discussions; to Martin 
Zogo (TCP, Kribi) for arranging the necessary 
permits and the shipment of the collections; 
and to Eric-Joel Semengue (Ebom) for being 
an excellent guide, an ardent collector, and 
pleasant company during six months of field 
work. The manuscript benefited from the con- 
structive criticism of three referees. The fig- 
ures in this paper were prepared by Eric 
Bosch (National Museum of Natural History, 
Leiden). This study was funded by the Nether- 
lands Foundation for the Advancement of 
Tropical Research (NWO-WOTRO). 



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Revised ms. accepted 2 January 1998 



MALACOLOGIA, 1998, 40(1-2): 251 -266 

CYTOCHROME OXIDASE l-BASED PHYLOGENETIC RELATIONSHIPS AMONG 

THE POMATIOPSIDAE, HYDROBIIDAE, RISSOIDAE AND TRUNCATELLIDAE 

(GASTROPODA: CAENOGASTROPODA: RISSOACEA) 

George M. Davis\ Thomas Wilke\ Christina Spolsky\ Chi-Ping Qiu^, Dong-Chuan Qiu^, 
Ming-Yi Xia^, Yi Zhang^, & Gary Rosenberg^ 

ABSTRACT 



The Gondwanian-derived Asian pomatiopsid radiation is taxonomically complex, diversity-rich, 
and widely deployed geographically This Asian branch of the family has coevolved with such 
human trematode parasites as Schistosoma and Paragonimus: it is ideally suitable for studying 
patterns and processes of evolution over 1 00 million years. Cytochrome с oxidase subunit I gene 
sequences are used here to elucidate taxonomic relationships from the subspecies to familial 
level. In Chinese literature, pomatiopsid taxa have been classified in the Hydrobiidae: what are 
the genetic relationships between Hydrobia and allied taxa classified as pomatiopsid? 

Sixteen sequences, ranging in length from 578 to 645 nucleotides, are aligned from 11 species 
of nine genera assigned to seven families, four of which are rissoacean. Five different phyloge- 
netic analyses are concordant: (1) the pomatiopsid taxa are in one distinct ciade, the other ris- 
soaceans form a second clade: (2) truncatellids are more closely allied to the hydrobiids than to 
the pomatiopsids: (3) the rissoid Setia is part of the truncatellid-hydrobiid clade; (4) two sub- 
species of Oncomelania are clearly divergent: (5) triculine taxa appear divergent from poma- 
tiopsine taxa. However, the Tricula sp. node is weakly supported. 

Individuals of a population differ by an average of 0.005 = 0.004 nucleotide differences/site: 
the subspecies of Oncomelania differ by 0.148 ± 0.004; the two species of Hydrobia differ by 
0.162 (range of 0.161 - 0.163); the triculine genera Tricula and Gammatricula differ by 0.132 
(range of 0.130 - 0.133); the pomatiopsid subfamilies Pomatiopsinae and Triculinae differ by 
0.179 ± 0.020: the families Hydrobiidae and Pomatiopsidae differ by 0.267 ± 0.016. Non-ris- 
soacean and rissoacean taxa differ by 0.274 ± 0.023. 

Key words: systematics, cytochrome с oxidase subunit I, CO!, gene sequences, phylogeny, 
Rissoacea, Pomatiopsidae, Hydrobiidae. Truncatellidae, Rissoidae, China. Jamaica. Bulgaria, 
Denmark. 



INTRODUCTION 

This study is one of a series (reviewed in 
Davis, 1992) aimed at understanding the ori- 
gin and evolution of the freshwater snail fam- 
ily Pomatiopsidae in Asia. There are com- 
pelling reasons to pursue such studies: (1) 
The family is ideally suited for in-depth studies 
of biogeography and evolution. The family is 
of Gondwanian origin with genera found in 
South Africa, South America, northern India, 
and Australia. Davis (1979) hypothesized an 
introduction of early pomatiopsids from the 
northeastern Indian Plate into northern Burma 
and western China with subsequent distribu- 
tion throughout southern China, Japan, and 
the Philippines reaching North America via 



Bering Strait. (2) Pomatiopsids are ideal for 
studying patterns and processes of evolution 
over the past 100 million years. The family is 
taxon rich and widely deployed geographi- 
cally. A series of anatomical studies on poma- 
tiopsid taxa have yielded a rich database of 
characters and character-states enabling the 
establishment of testable phylogenetic hy- 
potheses of the evolution of the family. Each 
phylogeny is tested with the addition of data 
from a newer study. The latest phylogeny 
(Davis, 1992) has not falsified the previous 
phylogenies. These phylogenies are mapped 
on area cladograms testing and reinforcing 
the biogeographic hypothesis. (3) A diverse 
array of Asian pomatiopsids are important in- 
termediate hosts of human trematode para- 



^ Academy of Natural Sciences of Philadelphia, 1900 Benjamin Franklin Parkway. Philadelphia. Pennsylvania 19103. U.S.A.: 

davis@say.acnatsci.org. 

^Chinese National Center for Systematic Medical Malacology. Chinese Academy of Preventive Medicine. 207 Rui Jin Er Liu, 

Shanghai 200025. Peoples Republic of China 

^Sichuan Institute of Parasitic Diseases. Chengdu 610041 Sichuan. People's Republic of China 



251 



252 



DAVIS ETAL. 



sites. These studies are essential to study co- 
evolution of the blood parasite Schistosoma 
with prosobranch snails. Three genera of the 
Pomatiopsidae — Oncomelania, Neothcula 
and Robertsiella — are involved in the trans- 
mission of the human blood fluke Schisto- 
soma in China, the lower Mekong River, and 
Malaysia. The schistosome occurring in 
China is also distributed in Japan, Taiwan, the 
Philippines and Sulawesi. The genus Schisto- 
soma is, as are the Pomatiopsidae, of Gond- 
wanian origin; one branch of the Schistosoma 
clade has coevolved with Asian Pomatiopsi- 
dae, with genera distributed in two subfami- 
lies, the Pomatiopsinae and Thculinae (re- 
viewed in Davis, 1980, 1992). (4) Molecular 
data are essential to test the phylogenetic re- 
sults based on anatomy. Allozyme data have, 
to the limited degree they have been applied, 
reinforced the phylogenetic hypotheses on 
the relationships of key genera in the afore- 
mentioned subfamilies (Davis et al., 1994); 
that is, the phylogenies based on allozymes 
and anatomical data are congruent. They 
have been useful to clarify subspecific status 
of populations of Oncomelania hupensis in 
China (Davis et al., 1995). But with the need 
to include numerous taxa for phylogenetic 
analysis, the ability to use allozyme data ef- 
fectively decreases. We have found that mito- 
chondrial gene sequences are ideally suited 
for testing phylogenetic relationships based 
on anatomical data. We have established that 
cytochrome b sequences are useful to deter- 
mine patterns of divergence at the population 
and subspecies level within the genus On- 
comelania (Spolsky et al., 1996). 

There are a number of questions that this 
study was designed to answer: (1 ) Are the Hy- 
drobiidae and Pomatiopsidae truly divergent 
separate families? From Davis (1979) onward 
we have argued that, on the basis of anatomy 
and patterns of development, the Hydrobiidae 
and Pomatiopsidae are highly divergent. This 
is an important question because up to the 
present, Chinese workers and others around 
the world have insisted on including the Po- 
matiopsidae within the Hydrobiidae and thus 
believe that some hydrobiids transmit schisto- 
somes (Maiek & Little, 1971; Brandt, 1974; 
Liu et al., 1974; Liu, 1979; Brown, 1980 (re- 
vised to use Pomatiopsidae in 1994); Kang, 
1984, 1986; MaIek, 1985). Davis (1979, 1980, 
1992) has shown that the Hydrobiidae are not 
found in India, China or southeast Asia; fur- 
ther, no hydrobiid transmits Schistosoma. 

Understanding the patterns of divergence 
of these two families is important to under- 



standing the origin and coevolution of ris- 
soacean snails with Schistosoma. One pur- 
pose of this paper is to present additional ev- 
idence that the two families are distinct and 
divergent. 

(2) On the basis of anatomical data, there 
are two distinct subfamilies of the Pomatiopsi- 
dae; the Pomatiopsinae and Triculinae. Al- 
lozyme data reinforced the confamilial status 
of the two generic groupings but did not un- 
equivocally serve to demonstrate two distinct 
subfamilies as anatomical data did (Davis et 
al., 1994). Would the cytochrome с oxidase 
subunit I (COI) gene sequences serve to 
clearly demonstrate family and subfamily- 
level generic groupings? 

(3) Would the Truncatellidae (represented 
here by only one species) be more closely re- 
lated to the Hydrobiidae or to the Pomatiopsi- 
dae? Davis (1979) and Ponder (1988) consid- 
ered the Truncatellidae to be closely related to 
the Pomatiopsidae on the basis of anatomical 
data. Analyses of 28S rRNA sequences in- 
volving one species of Hydrobiidae, nine 
species of two genera of Truncatellidae, and 
one species of Pomatiopsidae (Rosenberg et 
al., 1997) placed the Hydrobiidae as an out- 
group to a cluster consisting of two branches; 
one solitary branch included some of the trun- 
catellid taxa; the second branch subdivided 
into two groups, one including the remaining 
truncatellid taxa, the other the pomatiopsid 
species. What would the COI sequence data 
tell us? 

(4) Would COI data support the conclusion 
based on allozyme data (Davis et al., 1995) 
that Oncomelania hupensis hupensis and O. 
hupensis robertsoni are distinct subspecies? 



METHODS 



Taxa Studied 



Pomatiopsidae; Triculinae; Gammatricula 
chinensis Davis, Liu & Chen, 1990; Triculasp. 

Pomatiopsidae; Pomatiopsinae; Oncome- 
lania hupensis hupensis (Gredler, 1881); On- 
comelania hupensis robertsoni Bartsch, 
1946. 

Hydrobiidae; Hydrobiinae; Hydrobiacl pon- 
tieuxini Radoman, 1973; Hydrobia neglecta 
Muus, 1963. 

Rissoidae; Setia turhculata Monterosato, 
1884. 

Truncatellidae: Truncatella pulchella (Pfeif- 
fer, 1839). 



CYTOCHROME OXIDASE-I-BASED RISSOACEAN PHYLOGENY 



253 



TABLE 1 . Localities and collecting information for the specimens studied. 



Taxa; Preparation # 



Localities 



Catalog* 



PomatiopsidaeTriculinae 
Gammatricula chinensis 
414/415/416 

Tricula sp. 
453/454 



Pomatiopsidae: Pomatiopsinae 
Oncomelania hupensis 

hupensis 93/96 
Oncomelania hupensis 

robertsoni 45/48 



Hydrobiidae 
Hydrobia cf. pontieuxini 

346/347/351 
Hydrobia neglecta 
435/436/439 

Rissoidae 
Setia turhculata 
474/476/477 

Truncatellidae 

Truncatella pulchella 
479-480 



China, Zhejiang Province, Kaiwa Co, 

Tong Cun Town, Bai Keng Village; 

118 15'47"E,29 = 00'05"N 
China, Sichuan Province, Dayi County; 

Tian Gong Mia Township; Huang Ba Village; 

117'23'16"E,30-35'26"N 



China, Hubei Province, Han Yang County; 

1 14^01 '01 "E,30"34'08"N 
China, Yunnan Province; Dali City, 

Da Jin Ping, Zi Ran Village; 

100°12'04"E, 25°27'06"N 



Bulgaria, 1 km W of Nessebar; 

27 71'73"E. 42 65'99"N 
Denmark, Punen Island, Odense Fjord; 

10 32'E, 55 30'N 



Bulgaria, 1 km W of Nessebar; 
27 71'73"E. 42 65'99"N 



Jamaica, W of Falmouth; 
77°39'46"W, 18 29'46"N 



ANSP 400351 
ZAMIPM0136 

ANSP 400352 



ANSP 375731 
CIPD 0349 

ANSP 400353 
ANSP 400354 

ANSP 400355 

ANSP 400356 



Four molluscan taxa were used as out- 
groups: (1) the polyplacophoran Katharina tu- 
nicata (Wood, 1815), the sequence for which 
was obtained from GenBank (accession num- 
ber U09810); (2) the cerithiacean Cerithium 
atratum (Born, 1778) (Harasewych et al., 
1997); (3) the muricacean Stramonita haema- 
stoma (Linnaeus, 1767) (GenBank accession 
number U86330, under the name Thais): and 
(4) the rissoacean Setia turriculata studied in 
this paper. 

Locality data are given in Table 1 . Oncome- 
lania hupensis hupensis. O. hupensis robert- 
soni and T. pulchella were brought to the USA 
alive, G. chinensis and Tricula sp. were pre- 
served in 100% methanol, H. cf. pontieuxini 
and hi. neglecta were preserved in 70% 
ethanol, and S. turriculata was frozen. Imme- 
diately prior to isolation of DNA, the living 
specimens of Oncomelania and Truncatella 
were quick-frozen at -80'C. 

DNA Preparation 

The methods used for preparing DNA from 
individual snails were described by Spolsky et 
al. (1996), with the following modifications. Al- 
cohol-preserved specimens of Gammatricula, 



Tricula and Hydrobia were soaked 5 min each 
in two changes of 300 |.il of ice-cold exchange 
buffer before being placed in lysis buffer. 
Ethanol precipitation and washing were re- 
peated and the final DNA pellet redissolved in 
25 |il of water. 

The quality of DNA was determined by 
electrophoresis through a 1% agarose gel in 
TBE. DNA concentration was determined 
using a HoeferTKOlOO fluorometer. 

DNA Amplification 

PCR was used to amplify a fragment of the 
mitochondrial COI gene using the primer pair 
C0F14 (forward: 5' GGTCAACAAATCATA- 
AAGATATTGG 3') and COR722 (reverse: 5' 
TAAACTTCAGGGTGACCAAAAAAYCA 3'). 
C0F14 is identical to primer LCO1490 as 
described by Folmer et al. (1994), while 
COR722 is a modification of Folmer et al. 
(1994) primer HC021 98. 

Each PCR reaction mixture, in a total vol- 
ume of 50 ц1, contained 20-1 00 ng of genomic 
DNA, 2.5 units of cloned Pfu DNA polymerase 
(Stratagene), 200 цМ of each dNTR 20-40 
pmol of each primer, 20 цд of BSA, and 5 ,ul of 
10X Pfu reaction buffer. PCR amplifications 



254 



DAVIS ETAL. 



were performed using an M-J Research PTC- 
100 thermal controller with the following cy- 
cling conditions: initial 1 min 30 sec at 95"C, 
followed by 40 cycles of 1 min at 95", 1 min 20 
sec at 47°C, and 1 min 1 sec incremented by 
1 sec per cycle at 73'C. After a final 5 min at 
74°C, reactions were held at 4°C. 

Amplified DNA products were separated by 
electrophoresis through a 1% low melting 
point agarose gel in TAE buffer. The band cor- 
responding to a fragment of the correct size 
was cut out, and the DNA purified using either 
Microcon-100 microconcentrators (Amicon) 
after digesting the agarose with agarase or di- 
rectly with Wizard PCR preps (Promega). 
DNA concentration was determined on a Hoe- 
fer TKO100 fluorometer. 

Sequencing 

Sequences of the COI fragment were de- 
termined by manual cycle sequencing, using 
the Thermo Sequenase radiolabeled termina- 
tor cycle sequencing kit (Amersham) accord- 
ing to their protocol. 

Each reaction mixture contained 40-60 ng 
of purified PCR product, 4 units of Thermo Se- 
quenase DNA polymerase, 2 ц1 of reaction 
buffer, 4 pmol of either C0F14 or COR722 
primer in a total reaction volume of 20 ¡.il. One 
fourth of the reaction mixture was aliquoted to 
each of four dideoxynucleotide-specific termi- 
nation mixes containing the four dNTPs at 7.5 
цМ each plus, for each termination, 0.1 5 pmol 
of one of the four ^^P-labelled ddNTPs at a 
specific activity of 1500 C/mmole. Cycling 
conditions consisted of 30 cycles of 60 sec at 
95'C, 60 sec at 51 С and 75 sec at 72 С for 
the forward primer and 30 cycles of 60 sec at 
95°C, 60 sec at 56 С and 75 sec at 72"C for 
the reverse primer. Four |liI of stop solution 
were added after cycling and samples were 
stored frozen until ready to use. 

Before loading, the samples were heated 5 
minutes at 75 'C and 3 ц\ of each loaded im- 
mediately on the gel. Reaction products for 
each primer were run on three separate gels: 
2.5 h on an 8% Long Ranger gel (PMC), 4 h 
on a 6% gel, and 7.5 h on a 5% gel at a con- 
stant power of 37.5 Watts, providing complete 
sequences for both strands. 

Data Analyses 

COI sequences for each individual were as- 
sembled and edited using ESEE 3.0s (Cabot 
& Beckenbach, 1989). ESEE was also used 



to align our sequences with sequences ob- 
tained from GenBank and the literature. 

A distance matrix was computed using 
DNADIST of PHYLIP version 3.57 (Felsen- 
stein, 1989, 1993). Maximum likelihood trees 
were generated using DNAML (PHYLIP 3.57). 
Twenty repetitions, with randomized input 
order and optimization by global branch re- 
arrangement, were run for each analysis. 
Bootstrap estimates (1,000 replicates) were 
made using program SEQBOOT, in conjunc- 
tion with DNAML and CONSENSE. Parsi- 
mony analyses were done using Hennig86 
(Farris, 1 988) and PAUP 3.0s with branch and 
bound searching (Swofford, 1993). In analy- 
ses using PAUP, terminal nucleotides not 
present in all sequences were trimmed from 
the analyses: using DNAML, all 645 nu- 
cleotide positions were included. 

We performed five different phylogenetic 
analyses to satisfy different conditions and 
compare among methods: (1) DNAML with 
the polyplacophoran Katharina and the rissoid 
Setia as outgroups: (2) As the polypla- 
cophoran was not much more distant from the 
ingroup taxa than was Setia, we used Setia as 
the outgroup in a maximum likelihood analy- 
sis: (3) Also with Sei/a as the outgroup, we ran 
Hennig86 (256 variable sites: 220 informative 
sites): (4) We subsequently added the two 
Caenogastropoda: these two taxa are better 
outgroups (i.e., within Gastropoda but outside 
Rissooidea) than either Katfiarina or Setia. To 
our knowledge, there are no data available for 
other hssoacean taxa that might serve as out- 
groups. For this set of taxa, we computed a 
maximum likelihood tree as follows: first, we 
empirically determined the optimal transi- 
tion/transversion ratio (ratio which minimizes 
the likelihood measure: we then used the op- 
timal ratio, 1.3 in this case, in an exhaustive 
DNAML analysis (20 iterations, global branch 
swapping): (5) we also computed parsimony 
trees for the same set of taxa, using a 1:1 
transition: transversion ratio. 



RESULTS 

Sequence alignments for 16 sequences, 
ranging in length from 578 to 645 nucleotides, 
are shown in Table 2. Individuals with identical 
sequences (414, 415: 474, 476, 477: 346, 
347; 435, 436, 439; and 453, 454) were com- 
bined for alignment and subsequent anal- 
yses. A single nucleotide at position 57 is 
missing from the Cerithium sequence; we pu- 



CYTOCHROME OXIDASE-I-BASED RISSOACEAN PHYLOGENY 



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258 



DAVIS ETAL. 



tatively assign this deletion to a compression- 
based misreading of sequence in a GC-rich 
region. 

Felsenstein's distance matrix of sequence 
divergence, based on data in Table 2, is given 
in Table 3. Individuals of a population differed 
by nucleotide divergence values of 0.005 ± 
0.004 (N = 5). The subspecies of Oncomela- 
nia hupensis differed by 0.148 ± 0.004 (N = 
4). The two species of Hydrobia differed by 
0.162 (range 0.161 - 0.163). The genera Tric- 
ü/a vs. Gammaincu/a differed by 0.132 (range 
of 0.130 - 0.133). The subfamily Pomatiopsi- 
nae vs. the Triculinae differed by 0.179 ± 
0.020 (N = 12). The families Hydrobiidae vs. 
Pomatiopsidae differed by 0.267 ± 0.01 6 (N = 
21). The non-rissoacean outgroup snail taxa 
differed from the rissoaceans by 0.274 ± 
0.023. 

The unrooted maximum likelihood tree with 
the polyplacophoran as outgroup is given in 
Figure 1. Replacement of Katharina by Setia 
as the outgroup does not change the topology 
of the remaining tree. From these trees the 
following are clear: (1) The pomatiopsid taxa 
are one distinct clade; the other rissoaceans 
form a second distinct clade: (2) The trun- 
catellids are more closely allied to the hydro- 
biids than to the pomatiopsids: (3) The rissoid 
SetIa is part of the Truncatellidae-Hydrobiidae 
clade (except in Fig. 2, where it is the out- 
group); (4) The two subspecies of Oncomela- 
nia are clearly divergent: (5) The triculine taxa 
appear divergent from the pomatiopsine taxa. 
However, the triculine node is only weakly 
supported (54% bootstrapping value). 

The Hennig86 analysis using SetIa as out- 
group yielded two equally parsimonious trees 
with a length of 517, a consistency index of 
0.66 and a retention index of 0.74. The Nelson 
consensus tree is shown in Figure 2. The po- 
matiopsids are in one clade, the hydrobiids 
and truncatellids in another. The results are 
the same as in the maximum likelihood analy- 
sis except that the position of Tricula is unre- 
solved: there is a trifurcation in the pomatiop- 
sid clade with Tricula not unequivocally within 
a triculine clade (it is in one of the alternative 
Hennig trees). 

The trees obtained using Stramonita and 
Ceritlilum as outgroups are given in Figures 3 
and 4. The maximum likelihood analysis (Fig. 
3) yields a tree for the ingroup taxa similar to 
that in Figure 1 except that Tricula is a sister 
taxon to Oncomelania rather than to Gamma- 
tricula. The PAUP-based parsimony analyses 
(Fig. 4) again clearly define two major clades, 



a Pomatiopsidae clade and a Truncatellidae- 
Hydrobiidae clade. The analysis produced 
two shortest trees of 974 steps: the set of four 
next shortest trees required one additional 
step: the latter were not included in computing 
the Adams consensus tree. The two shortest 
trees differed in their placement of Setia within 
the hydrobiid clade, thus resulting in a con- 
sensus tree with a trifurcation in this clade. 



DISCUSSION 

Taxonomic decisions should not be made 
on the basis of molecular distance coefficients 
alone (Davis, 1994), but on anatomical, cyto- 
logical and developmental data within an eco- 
logical context. Thus, the COI data presented 
here must be examined in light of the avail- 
able anatomical data and the patterns of evo- 
lution evidenced in the clades shown here. 
The data provide a beginning of showing rela- 
tionships: there are insufficient hydrobiid, 
truncatellid and rissoid genera and species in- 
volved in this study to strongly support dis- 
crete hssoid, truncatellid, and fiydrobiid 
clades. The data are, however, sufficient to 
answer our questions and provide the basis 
for predictions concerning family relationships 
indicated here. 

The hydrobiids and pomatiopsids are dis- 
tinct clades. The genetic data coupled with 
anatomical data reviewed in Davis (1979, 
1980, 1992) show that these clades are 
greatly divergent. The COI sequence data 
strongly support the existence of a pomatiop- 
sid clade separate from the hydrobiids. 

The distinctiveness of the pomatiopsid 
clade is further evidenced by the grouping of 
the Rissoidae and Truncatellidae with the Hy- 
drobiidae within one clade. Thus, a second 
question is answered: the Truncatellidae, by 
these data, are more allied genetically with 
the Hydrobiidae than with the Pomatiopsidae. 
However, the truncatellid branch is weakly 
supported, so additional data are required. 
Davis (1979) and Ponder (1988) hypothe- 
sized that the Truncatellidae were closely re- 
lated to the Pomatiopsidae (Rosenberg, 
1996a). The Pomatiopsidae share with the 
Truncatellidae and Assimineidae the evolu- 
tion to terresthality from aquatic and amphibi- 
ous habitats in some clades (Rosenberg, 
1996b). However, the anatomical data avail- 
able are insufficient to resolve whether the 
Truncatellidae are closer phylogenetically to 
the Hydrobiidae or to the Pomatiopsidae. 



CYTOCHROME OXIDASE-I-BASED RISSOACEAN PHYLOGENY 



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DAVIS ETAL. 



Kulluirina liinicuta 



Sctia tiiiriciihila 474/476/477 

p Tnincalellu pulchellu 480 
1000 



Tnmcalelhi pulchellu 479 

Hydrohia cf. ponliciixini 346/347 
1000 

' — Hydiobiu cf. poiUit'iixini 351 
Hydrohia iKi;lccla 435/436/439 

— Oncomclaniu bupensis /iiipcnsis 93 
10(10 

'- OncomcUmia ¡nipcnsis Impcnsis 96 
OiKomclunia Inipcnsis rohcrisoni 45 
■— OncomcUmia hupoisis rohcrisoni 48 
Ciunumilriciila cliii!cnsi\ 414'415 
l- (.ianinialriciilu chincn^is 416 



Tríenla sp. 453/454 



FIG. 1 . Unrooted tree based on maximum likelihood with Katharina tunicata as the outgroup. Bootstrap val- 
ues (1 ,000 replicates) are indicated for each node. 



Anatomical data do indicate that the Ris- 
soidae are sister taxa to the Hydrobiidae and 
the Truncatellidae. 

A 28S ribosomal RNA phylogeny placed the 
Hydrobiidae as a sister group to the Truncatel- 
lidae and the Pomatiopsidae, with a terminal 
Гшпса?е//а- Pomatiopsidae clade divergent 
from another Truncatella group (Rosenberg et 
al., 1997). However, as Davis (1994) pointed 
out, one must be circumspect in assessing 
phylogenies based on 28S rRNA. In the re- 
sults presented by both Davis (1994) and 
Rosenberg et al. (1 994, 1 997) involving rRNA, 
there were some considerable surprises not 
supported by comparative anatomy and al- 
lozyme-based phylogenies, due in part to the 
insufficient quantity of informative characters 
(85) to resolve a large assemblage (40) of di- 
vergent taxa. 

In the rRNA data presented by Davis ( 1 994: 
fig. 10) there were many more differences 
among margaritiferine taxa than among all 
other unionid taxa. Cumberlandia was basal 



in the unionid clade, whereas Margaritifera 
margaritifera and M. falcata were highly diver- 
gent from each other in a margaritiferine 
clade. The results were as if rRNA evolution 
went unexplainably berserk (greatly acceler- 
ated) in the Margaritiferidae: results not sup- 
ported by any other data (see also Ledyard et 
al., 1996). In contrast to the rRNA sequence 
data, the results with mitochondrial genes 
have been congruent with results based on 
other data, and the total weight of evidence 
leads us to consider the truncatellids within 
the same clade as, and closely related to the 
Hydrobiidae, but divergent from the Poma- 
tiopsidae. This is our hypothesis to be chal- 
lenged with results based on yet other genes. 
The COI sequence data are congruent with 
cytochrome b gene sequence data involving 
populations of Oncomelania hupensis from 
mainland China; the results showed evidence 
for two distinct subspecies: O. h. hupensis 
and O. h. robertsoni (Spolsky et al., 1996). 
Both data sets are congruent with an al- 



CYTOCHROME OXIDASE-I-BASED RISSOACEAN PHYLOGENY 

Sulla liirriciiiala 474/476/477 



261 



Tnmcalellu pulcliclla 480 



Tnmcutelhi pulcliclla 479 



Hydmbia nc^lccla 435/436/439 

Hydmbia cf. ponticuxini 346/347 



Hydmbia cf. puiiticiixini 351 



Tricula sp. 453/454 



GuiinnalriciiUi clii)K'nsi.s 414/415 
Gamiiialriciila с h incus is 4 1 6 

(hicomehmia liiipciisi.s hiipcn.sis 96 

(hicomelaniu hiipcn.sis liupcnsi.s 93 



()ncoiuclaniii hupcnsis mbcrl.soni 45 



( )nc(imclania hupcnsis robcrtsoni 48 



FIG. 2. Unrooted Nelson consensus tree based on Hennig86 analysis, with Setia turriculata as outgroup. 



lozyme-based phylogeny indicating the occur- 
rence of three subspecies of Oncomelania 
hupensis (the third, tangi. from Fujian Prov- 
ince, was not available for the DNA studies). 
Oncomelania h. robertsoni has a smooth 
shell, no varix, and is relatively shorter in shell 
length than O. h. hupensis. which has strong 
ribs and strong varix when living in the 
Yangtze River flood plains, but lacks ribs (al- 
though retaining a strong varix) when living 
above the effects of the annual flooding. On- 
comelania h. robertsoni lives above the Three 
Gorges of the Yangtze, whereas O. h. hupen- 
sis is found below the gorges along the 
Yangtze River drainages. The distance coeffi- 
cient between the subspecies using cy- 
tochrome b data averaged 0.110 (range of 
0.1021 - 0.1186), based on robertsoni hom 
Yunnan and Sichuan and hupensisirom Jiang 
Xi Province. The equivalent average distance 
in this study is 0.148 ± 0.004 (N = 4) with a 
range of 0.142 - 0.153. In this study, robert- 
soni came from Yunnan, and hupensis from 



Hubei Province, a province upstream from 
Jiang Xi.This suggests that the COI gene has 
diverged more than the cytochrome b gene 
and thus may be more useful to detect popu- 
lation and subspecies divergences and pat- 
terns of evolution. That the COI gene appears 
to have diverged more than the cytochrome b 
is of interest given the conventional under- 
standing that COI tends to be more conserva- 
tive in most taxa. 

The two species of Hydrobia differed from 
each other by a distance coefficient only about 
6% greater than the distance between the sub- 
species of Oncomelania hupensis. a surprise 
given the considerable anatomical differences 
between the hydrobiid species and the great 
geographic distance separating them (thou- 
sands of ocean miles between Bulgaria and 
Denmark). In contrast to the large differences 
between Oncomelania hupensis subspecies, 
two populations of O. h. robertsoni separated 
by over 600 km had a cytochrome Ь difference 
of only 0.038, a relatively small amount of dif- 



262 



DAVIS ETAL. 



■ Slnimonila haemustomu 

( 'critliiiim atratum 

.S'c7/'i/ tiirriciilata 474/476/477 

HyJrohiu cf. poiiiicnxini 346/347 
'— Hydrohiu cf. pcmlieuxini 35 1 

Hydrohiu iieglcclu 435/436/439 

TnmcaiL'Ila piilchella 479 
•• Tnmcalcllu pulchclla 480 

— OncomcUmia hiipcnsis hupensis 93 
*- Oncomdania luipcnsis hiipensi.4 96 
Oncomcliiniii liupciisis roht'rlsimi 48 
Onconiclan'ui hiipcnsis rohcrlsoni 45 
— Triciila sp. 453/454 
( iiimimiiriciila chincusi.s 4 1 4/4 1 5 
GimiWíilriciilíi chhu'iisis 416 

FIG. 3. Unrooted maximum likelihood tree using Stramonita ar\ö Cerithium as outgroups. Character changes 
were optimally weighted at 1 .3:1 for transitions;transversions. 



ference. It appears that the subspecies have 
diverged considerably since Oncomelania dis- 
persed into China about 10 million years ago 
(Davis, 1979, 1980). The considerable genetic 
divergence is also seen in allozyme data 
(Woodruff et al., 1 988: Davis et al., 1 995). The 
Nei minimum D for robertsoni vs. hupensis 
was 0.257 ± 0.077 (N = 21) (Davis et al., 
1995). Population variation within hupensis 
was 0. 1 60 ± 0.085 (N = 21 ). Davis et al. (1 995) 
discuss why we do not consider these taxa as 
full species. Our question here is what has dri- 
ven such large genetic divergence when the 
snails are identical morphologically and 
anatomically (except for size and presence of 
ribs on some populations) and can replace 
each other ecologically? One hypothesis is 
that, as virtually all populations of Oncomela- 
nia hupensis throughout its range have been 
heavily infected with Schistosoma japonicum. 
coevolutionary pressures have been the 
cause. Added to this are the natural geo- 
graphical isolation of Yunnan and Sichuan 



from the central Yangtze River basin and the 
mountain ranges that separate Fujian Prov- 
ince from the other two regions. We now need 
considerable population studies of COI se- 
quences to assess the extent of population di- 
vergence across China. 

Considering the Thculinae issue, it could be 
argued that, on the basis of anatomy, the Th- 
culinae and Pomatiopsinae are not historically 
closely related. The pomatiopsine female re- 
productive system appears considerably dif- 
ferent from that of the Triculinae, and what 
Davis has called the spermathecal duct in 
each taxon may not be homologous. The data 
presented here are congruent with allozyme 
data of Davis et al. (1994) that show general 
agreement of phylogenies based on both 
anatomical and allozyme data; Oncomelania 
hupensis is in a clade apart from the three 
triculine taxa in the allozyme study, Gamma- 
tricula chinensis. Gammatricula songi, and 
Neotricula lilii. However, the two clades are 
very close genetically. The Nei D between On- 



CYTOCHROME OXIDASE-I-BASED RISSOACEAN PHYLOGENY 



263 



Slnmionitu haemusloma 
С 'crilliium atralwn 
Scliu lurriculutu 'М'М'МЫЛИ 
Tnmcalclla pidchella 480 
Tninciitclla ¡nilchcHu 479 
llvilrohiu cf. ponlieiLxini 346/347 
tlydrohia cf. pontieiixini 35 1 
llytlmhiu iK'glectu 435/436/439 
OncoiUi-'lania Inipensis hupensis 93 
Oncomclania hupensis hupensis 96 
Oiicomelania Inipensis mherlsuni 45 
Oncomelaniu hupensis roberlsoni 48 
I'rieula sp. 453/454 
Ciiimiiiíilriciilíi eliinensis 414/415 
(ñmimíilricu/ci ein'ncnsis 416 



FIG. 4. Unrooted PAUP tree: Adams consensus of two shortest trees produced by a branch and bound 
search, with transitions and transversions weighted equally. 



comelania and the three triculines was 1 .293 
± 0.412 (1.000 - 1.764); D among triculines 
was 0.890 ± 0.301 (0.689 - 1.236). Further. 
Oncomelania was less distant from Gamma- 
tricula chinensis (1.1 16) than was Neotricula 
та (1.236). Accordingly, the phenogram 
based on Nei's D does not provide a great 
separation from the triculine taxa because of 
the closer relationship of Oncomelania to N. 
lilii. 

The Tricula of this study is a new species 
that will be described elsewhere; anatomical 
data confirm its placement in Tricula. Hen- 
nig86 produced two trees because O. h. 
robertsoni was closer to Tricula sp. (0.144) 
than it was to O. h. hupensis (0.1 50). The two 
triculine taxa differed by only 0. 1 32. This very 
close relationship between Oncomelania and 
some triculine taxa shows the overall close re- 
lationship between the two pomatiopsid sub- 
families and possibly points the way to unrav- 
eling the pathway of evolution of the triculines 
from early pomatiopsids. For example, the 



Sichuan Tricula is, on the basis of anatomy, 
closely related to Yunnan species of Tricula 
and to the type species, Tricula montana from 
northern India. The average COI distance of 
Tricula sp. from O. h. hupensis is 0.188, 
whereas that of Gammatricula chinensis is 
0.195; the same set of relationships to O. h. 
robertsoni is 0.144 and 0.171. The premise 
that emerges from these data is that O. h. 
robertsoni in Yunnan, with its generalized 
morphological features, is closer genetically 
to the basal Oncomelania stock that gave rise 
to Tricula than is the derived Gammatricula 
and derived O. h. hupensis below the Three 
Gorges. This premise and initial data are con- 
sistent with the hypotheses of Davis (1979, 
1980, 1992) that pomatiopsids were intro- 
duced into Asia from the northeastern Indian 
Plate with the Himalayan orogeny, with sub- 
sequent evolution and dispersal down river 
systems. The closer genetic relationships of 
some triculine taxa to Oncomelania points the 
way to assessing the coevolution of Schisto- 



264 



DAVIS ETAL. 



soma spp. with both Oncomelania ano TúcuW- 
nae. 

All the phylogenetic analyses combined af- 
firm the monophyly of the Pomatiopsidae, al- 
though the placement of Tricula within this 
clade remains unresolved: using Katharina or 
Setia as outgroups in a maximum likelihood 
analysis, Tricula clusters with Gammatricula: 
using the closer Stramonita and Cerithium as 
outgroups, Tricula clusters with Oncomelania 
in a maximum likelihood analysis, but with 
Gammatricula in a parsimony analysis; a Nel- 
son consensus tree of Hennig86 analyses 
leaves relationships within the Pomatiopsi- 
dae as an unresolved trifurcation. In the end, 
the bootstrap value for the Tricula clade tells 
the story; placement of Tncü/a depends on the 
method and choice of outgroups. It is not well 
resolved within the pomatiopsid clade, but all 
evidence places it in this clade. This question 
may best be answered by increasing the num- 
ber of populations and species of Tricula and 
Gammatricula in the analyses, increasing the 
number of nucleotides analyzed, and se- 
quencing an independent nuclear gene. 

All five analyses place Truncatella in a 
clade with Hydrobia. The placement of Setia. 
however, is problematic: in analyses where it 
is not used as an outgroup, it clusters with the 
hydrobiid-truncatellid clade, but its relation- 
ships within this clade are uncertain. The un- 
resolved trifurcations are consistent with 
weak bootstrapping support for those nodes 
in the maximum likelihood analyses. 

Because the distances of KatharinaXo other 
taxa are not much different than distances 
among some ingroup members, we examined 
the number and kind of substitutions occur- 
ring in the COI gene. Substitution rates varied 
tremendously among codon positions, with 
strong constraints on amino acid changes: 
203 of the 21 5 third codon positions were vari- 
able, while 51 of 21 5 first codon positions and 
only ten second codon positions were vari- 
able. Translation of the nucleotide sequences 
clearly pointed out the strong constraints on 
amino acid changes in this gene: the majority 
of changes were synonymous substitutions. 
Among this group of 16 taxa, 40 amino acid 
positions were variable, of which too few (28) 
were phylogenetically informative. PAUP 
analysis of the amino acid sequences pro- 
duces 28 equally parsimonious shortest trees, 
resulting in a consensus tree with no resolu- 
tion. 

In an attempt to avoid saturation effects on 
phylogenetic tree construction, we carried out 



maximum likelihood analyses using only first 
and second codon positions: again, these 
analyses resulted in non-robust and implausi- 
ble trees with poorly supported nodes, al- 
though in this case, the pomatiopsid clade 
does hold together. We plotted pairwise tran- 
sition/transversion (Ts/Tv) ratios vs. pairwise 
distances to look for evidence of substitutional 
saturation. Although saturation must be oc- 
curring only at third codon positions, pairwise 
ratios were based on the whole sequence, as 
that is what the phylogenetic analyses were 
based on. Saturation appears to be occurring 
in pairwise comparisons with the three out- 
group taxa Katharina, Cerithium. and Stra- 
monita. with a mean Ts/Tv ratio of approxi- 
mately 1.1, and pairwise differences greater 
than about 130 nucleotides. For ingroup com- 
parisons, pairwise differences were usually 
less, varying from about 140 to 1 . Ts/Tv ratios 
were roughly correlated with nucleotide differ- 
ences, such that ratios approached saturation 
at distances greater than approximately 120 
nucleotide differences. Thus, there appears to 
be a quantitative difference between ingroup 
and outgroup taxa in the substitution level. 
The existence of a discrete ingroup provides 
further support for the robustness of the phy- 
logeny of this group. Further, although the ef- 
fect of saturation is to shorten branch length, 
in this case it is not likely to have affected the 
topology, that is, branching pattern, of the 
trees because most of the deep branches are 
sufficiently long to retain the correct branching 
pattern. 

This study should conclusively clarify two 
points: (1 ) The Hydrobiidae are not closely re- 
lated historically, biogeographically, or geneti- 
cally to the Pomatiopsidae; they are distinctly 
different families. (2) Schistosomes have 
evolved with the pomatiopsid lineage in Asia; 
hydrobiids do not transmit schistosomes. As 
implied by the term coevolved, there is a his- 
torical genetic linkage between the pomatiop- 
sids and schistosomes extending back to 
Gondwanaland. With the progression of time, 
this linkage has deepened; once lost, it can- 
not be restored (Davis, 1992). Thus, we pre- 
dict that no hydrobiid suddenly de novo, can 
become a host for any schistosome. 



ACKNOWLEDGMENT 

This study was supported by N. I. H. grant I 
P50 A13946, the Tropical Medical Research 
Center, Shanghai, China. We thank the fol- 



CYTOCHROME OXIDASE-I-BASED RISSOACEAN PHYLOGENY 



265 



lowing individuals for reviewing drafts of this 
paper and offering sound advice: Drs. David 
Blair, James Cook University, Townsville, Aus- 
tralia; Donald McManus, Queensland Institute 
of Medical Research, Australia; Charles Led- 
yard, University of Alabama, Tuscaloosa, 
U.S.A.; and Robert Vrijenhoek, Rutgers Uni- 
versity, New Brunswick, New Jersey, U.S.A.. 



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WOODRUFF, D., K. С STAUB, E. S. UPATHAM, V. 
VIVANT & H. С. YUAN, 1 988, Genetic variation in 
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Revised ms. accepted 21 March 1998 



MALACOLOGIA, 1998, 40(1-2): 267-278 

TESTING ALTERNATIVE HYPOTHESES OF NEOTRIGONIA 

(BIVALVIA:TRIGONIOIDA) PHYLOGENETIC RELATIONSHIPS USING 

CYTOCHROME С OXIDASE SUBUNIT I DNA SEQUENCES 

Walter R. Hoeh^ ^ Michael B. Black\ R. Gustafson\ Arthur E. Bogan^, Richard A. Lutz\ & 

Robert 0. Vrijenhoek^ 

ABSTRACT 

Uncertainties regarding the phylogenetic history within the Bivalvia have impeded attempts to 
understand evolution within the group. Estimating the evolutionary relationships surrounding the 
Trigonioida has been especially problematic and has led to disparate hypotheses regarding (1) 
the origin and subsequent diversification of unionoid bivalves and (2) autobranch gill character 
state transitions. In order to test alternative hypotheses of trigonioid phylogeny, 613 base pairs 
of DNA sequence of the cytochrome с oxidase subunit I gene were analyzed from 1 4 species of 
bivalves (ingroup) and three species of non-bivalve mollusks (outgroup). All phylogenetic analy- 
ses, using either nucleotide or inferred amino acid sequences, produced trees that robustly 
placed Neotrigonia (Trigonioida) as the sister taxon to a monophyletic Unionoida. Furthermore, 
the Autobranchia, Veneroida, and Mytiloida were supported as monophyletic groups in these 
analyses, whereas the Bivalvia was not. These phylogenetic relationships suggest that (1 ) there 
was a single invasion of freshwater by a unionoid bivalve ancestor, (2) trigonioid rather than ven- 
eroid bivalves gave rise to the Unionoida, (3) either the eulamellibranchous or filibranchous gill 
condition has evolved multiple times within the Autobranchia, and (4) the molluscan bivalved 
body plan may have evolved more frequently than traditional phylogenetic hypotheses suggest. 

Key words: Bivalvia, Trigonioida, Unionoida, cytochrome с oxidase I, mtDNA, phylogenetics, 
convergence. 



INTRODUCTION 

The higher-level phylogenetic relationships 
within the Bivalvia are poorly understood at 
present (e.g., Allen, 1985). This statement is 
corroborated by the many disparate hypothe- 
ses of evolutionary relationships that have 
been proposed for the higher taxa within the 
Bivalvia (e.g., Purchon, 1990; Waller, 1990; 
Starobogatov, 1992; Cope, 1996; B. Morton, 
1996; Salvini-Plawen & Steiner, 1996). This 
plethora of phylogenetic hypotheses likely 
stems, in part, from arbitrary choices to ex- 
clude certain types of characters and a gen- 
eral lack of explicit and rigorous phylogenetic 
analyses. Although major anatomical charac- 
ter suites distinguish two of the nominal sub- 
classes within the Bivalvia, that is, Proto- 
branchia and Autobranchia, the ordinal-level 
relationships within each subclass are not 
strongly supported by multiple shared-derived 
morphological features (e.g.. Waller, 1990). 

Two contrasting phylogenies of the higher- 
level relationships within the Bivalvia have 



recently been proposed by Salvini-Plawen 
& Steiner (1996; Fig. 1A) and Waller (1990; 
Fig. IB). The former study is an exemplar in 
that explicit data matrices and phylogenetic 
methodologies were presented. A major point 
of disagreement between the two phylogenies 
presented in Figure 1 is the placement of the 
Trigonioida, a relatively ancient bivalve taxon 
that, although currently depauperate, was tax- 
onomically diverse during the Mesozoic (Cox 
et al., 1969; Allen, 1985). The Salvini-Plawen 
& Steiner hypothesis (Fig. 1A) indicates that 
the trigonioids are most closely related to pte- 
riomorph bivalves (represented herein by 
mytiloids), with the Veneroida closely related 
to the Unionoida. Their proposed sister taxon 
relationship for the trigonioid and pteriomorph 
bivalves was supported by the shared pres- 
ence of (1) byssate larvae and adults and (2) 
abdominal sense organs in these taxa 
(Salvini-Plawen & Steiner, 1996). Alterna- 
tively, the hypothesis of Waller (Fig. IB) indi- 
cates that the Trigonioida is the sister taxon to 
the Unionoida. However, no evidential sup- 



'Center for Theoretical and Applied Genetics, Cook College, Rutgers University, New Brunswick, New Jersey 08903, USA: 

hoehw@miavx1 .muohio.edu 

^North Carolina State Museum of Natural Sciences, P.O. Box 29555, Raleigh, North Carolina, 27626, USA. 

^Corresponding author and current address: Department of Biological Sciences, Kent State University, Kent, Ohio 44242, 

USA 



267 



268 



HOEH ETAL. 



Veneroid 1 

Bivalves ^ 



Unionoid 
Bivalves 



3 



Trigonioid Й 

Bivalves Q 

3>2 



Mytiloid 
Bivalves 



В 



Protobranch 
Bivalves 



Non-bivalve 
Mollusks 



FIG. 1 . Bivalve relationships, based on morphological characteristics, according to Salvini-Plawen & Steiner 
(1996; A) and Waller (1990; B). Both hypotheses indicate a single origin for the Bivalvia (1) and filibranchous 
lamellibranch gills (2) but differ in their implications for eulamellibranch gill evolution. Hypothesis A indicates 
a single origin for eulamellibranch gills (3) while В indicates either two origins (solid bars) or a single origin 
followed by a reversal to the filibranch condition in trigonioids (hatched bars). 



port for this relationship was provided by 
Waller (1990). 

The evolutionary affinities of the Trigonioida 
have been a contentious subject for over a 
hundred years (e.g., Steinmann, 1888; Neu- 
mayr, 1889; Cox, 1960; B. Morton, 1987; 
Healy, 1989, 1996) and are central to an un- 
derstanding of bivalve mollusk character evo- 
lution, since representatives of the single ex- 
tant genus (Neotrigonia) have a mixture of 
seemingly primitive (e.g., filibranchous gills 
[possessing ciliary-linked gill filaments], lack 
of posterior mantle fusion, nacreous shells; 
Cox, 1960; Allen, 1985; B. Morton, 1987) and 
derived features (e.g., multi-vesicular sperm 
acrosome; Healy, 1989). This mosaic of 
seemingly primitive and derived character 
states has contributed to the erection of multi- 



ple, disparate hypotheses of trigonioid evolu- 
tionary affinities. According to the hypothesis 
of Salvini-Plawen & Steiner (1996; Fig. 1A), 
the placement of the trigonioids is consistent 
with a single origin of eulamellibranch gills 
(tissue-linked gill filaments) from filibranch 
gills. In contrast, the phylogenetic placement 
of trigonioids in the hypothesis of Waller 
(1990; Fig. IB) suggests that there were ei- 
ther (1) two origins of eulamellibranch gills or 
(2) a single origin of eulamellibranch gills fol- 
lowed by a reversal to filibranch gills in the 
trigonioids. 

The phylogenetic uncertainty within the Bi- 
valvia impedes the rigorous testing of evolu- 
tionary hypotheses. Therefore, the establish- 
ment of a robust phylogenetic hypothesis for 
higher taxa within the Bivalvia will enable criti- 



NEOTRIGONIA PHYLOGENETIC RELATIONSHIPS 



269 



cal evaluations of (1) trigonioid evolutionary 
relationships and (2) hypotheses of auto- 
branch bivalve gill character state transitions. 
Molecular systematic analyses have been 
useful in situations where morphological 
analyses were inconclusive (e.g., Avise, 
1994). Therefore, mitochondrial DNA(mtDNA) 
sequences, obtained from the cytochrome с 
oxidase subunit I (COI) gene, were used to 
construct a phylogenetic hypothesis for the 
major bivalve lineages represented in Figure 
1 . COI was chosen for this analysis because of 
its slow rate of evolution relative to other mito- 
chondrial protein coding genes, relative ease 
of unambiguous sequence alignment (e.g., 
Brown, 1 985: Simon et al., 1 994; Russe et al., 
1996), and demonstrated appropriateness for 
this particular analysis. 



MATERIALSAND METHODS 
Organisms 

The molluscan taxa used in this study, with 
GenBank accession numbers and primary lit- 
erature citation (where applicable), are as fol- 
lows: (1) ingroup. Class Bivalvia, Subclass 
Protobranchia, Order Solemyoida, Solemya 
velum (U56852), Order Nuculoida, Nucula 
tenuis (U56851), Subclass Autobranchia, 
Order Unionoida, Mutela rostrata (U56849), 
Amblema plicata (U56841 ), Anodonta cygnea 
( и 56842), Margaritifera margarltifera 
(U56847), Order Trigonioida, Neotrigonia 
margarltacea (U56850), Order Mytiloida, 
Modiolus modiolus (U56848), Geukensia de- 
missa (U56844), Order Veneroida (the five 
veneroid COI sequences are from Baldwin et 
al. [1996]), Corbicula fluminea (U47647), 
Rangia cuneata (U47652), Mercenaria mer- 
cenaria (U47648), Mytilopsis leucophaeata 
(U47649), Dreissena polymorpha (U47653), 
(2) outgroup. Class Scaphopoda Dentalium 
sp. (U56843), Class Gastropoda Lepetodrilus 
elevatus (U56846), Class Polyplacophora 
Katharina sp. (U56845). 

Methods 

Total DNA was isolated from somatic (man- 
tle) tissues of nine species of bivalves. Male 
gonadal tissues were specifically avoided dur- 
ing dissections to prevent comparisons of 
non-orthologous sequences (due to the actual 
or potential presence of doubly uniparental in- 
heritance of mtDNA in some bivalve taxa: for 



example, Skibinski et al., 1994: Zouros et al., 
1994: Hoeh et al., 1996). DNA was also iso- 
lated from representatives of three additional 
molluscan classes (i.e., Gastropoda, Polypla- 
cophora, and Scaphopoda) for use in gener- 
ating outgroup sequences. Subsequently, a 
710bp fragment of COI was PCR amplified 
and cycle sequenced for each of the 12 taxa 
as deschbed elsewhere (Folmer et al., 1994). 
Both strands of the COI fragment were se- 
quenced from each of two individuals from 
each terminal taxon to guard against PCR- 
based contamination artifacts. The resulting 
12 COI sequences, plus the five veneroid bi- 
valve COI sequences from Baldwin et al. 
(1996), were readily aligned by eye using 
MacClade 3.05 (Maddison & Maddison, 
1992). Sixteen of the 17 OTUs produced se- 
quences 613 bp in length, while that of 
Geukensia was 61 6 bp. The increased length 
of the Geukensia sequence was due to an au- 
tapomorphic, three nucleotide (single codon) 
insertion event. These three contiguous nu- 
cleotides, which are phylogenetically uninfor- 
mative for the taxa considered herein, were 
deleted prior to all phylogenetic analyses. No 
additional hypothesized insertion or deletion 
events were necessary to obtain the align- 
ment utilized in the subsequent analyses. 

The suitability of the COI data set for phylo- 
genetic analyses at the required hierarchical 
level was evaluated by plotting the substitu- 
tion pattern of transitions and transversions 
for each codon position (e.g., Orti & Meyer, 
1996). Furthermore, the degree of phyloge- 
netic signal within the COI data set was eval- 
uated using the g^ statistic of a random tree 
disthbution (from 100,000 random trees: e.g., 
Hillis, 1991; Hillis & Huelsenbeck, 1992) as 
implemented in PAUP (Swofford, 1993). Phy- 
logenetic analyses were carried out on the 
COI nucleotide sequences using the maxi- 
mum likelihood ([ML], DNAML in PHYLIP 
3.5c: Felsenstein, 1993), neighbor-joining 
([NJ], MEGA 1.02; Kumar et al., 1993), and 
maximum parsimony ([MP], PAUP 3.1.1; 
Swofford, 1993) algorithms. Katharina, the 
only non-conchiferan mollusk taxon, was 
used to root the resulting topologies. A transi- 
tion/transversion ratio of 2.0 was utilized in 
the ML analyses and the gamma distance 
(alpha = 0.5, using the Tamura-Nei model of 
nucleotide sequence evolution) was used to 
generate the pair-wise genetic distances for 
the NJ analyses. This particular distance 
takes into consideration among-site substitu- 
tion rate variation (e.g., Yang, 1996). Further- 



270 



HOEH ETAL. 



more, MP and NJ (again using gamma dis- 
tances, alpina = 0.5) analyses were conducted 
on the inferred COI amino acid sequences 
(using the Drosophila mtDNA genetic code). 
Multiple random terminal taxon addition order 
runs, combined with global branch rearrange- 
ment options, were employed to generate 
topologies from ML and MP analyses. These 
options increased the probability of finding the 
actual best topology under each of the two op- 
timality criteria (e.g., Hendy et al., 1 988: Mad- 
dison, 1991). The robustness of the resulting 
topologies was evaluated by bootstrap analy- 
ses (1,000 replicates for MP and NJ, 100 
replicates for ML). 

The best COI-based topology derived from 
the DNAML analysis was compared with the 
phylogenetic hypotheses presented in Figure 
1 using the Kishino-Hasegawa test (paired z 
test; Kishino & Hasegawa, 1989) as imple- 
mented in DNAML. To this end, the topological 
constraints option in PAUP was used to gen- 
erate 82 user trees (all trees < five steps longer 
than the shortest trees found by PAUP) repre- 
senting the two tree topologies (for the partic- 
ular taxa evaluated herein) in Figure 1 . Each of 
these user trees was then compared to the 
best DNAML tree by the Kishino-Hasegawa al- 
gorithm. This test evaluated the significance of 
any potential incongruence between the mor- 
phology- (Figure 1 ) and COI-based topologies 
(Swofford et al., 1996). In addition, character 
optimization, using MacClade (Maddison & 
Maddison, 1992), was carried out on the COI- 
based topologies to investigate their implica- 
tions for morphological character evolution 
within the Bivalvia. 



RESULTS 

Scatter plots of the relationship between 
the number of transitional and transversional 
substitutions at each of the three codon posi- 
tions and the proportion of nucleotide differ- 
ences (all positions) for the COI sequences 
revealed that only transitional substitutions at 
the third codon position had reached satura- 
tion (Fig. 2). Because saturated categories of 
substitution can contribute to erroneous esti- 
mates of evolutionary history (e.g., Swofford 
et al., 1996), all first and second position sub- 
stitutions together with only transversions at 
the third codon position were included in the 
COI nucleotide data matrix used for phyloge- 
netic analyses. Of the 613 nucleotide posi- 
tions in the transformed COI data matrix, 229 



were invariant, while 31 5 (1 02 from 1 st codon 
positions; 59 from 2nd; 154 from 3rd) were 
phylogenetically informative using the parsi- 
mony criterion. Analysis of the tree length dis- 
thbution of 100,000 randomly generated 
trees, using all 17 taxa, suggests that there is 
a significant amount of hierarchical structure 
within the transformed COI data set (g^ = 
-0.794; with 384 variable sites, p « 0.01; 
Hillis & Huelsenbeck, 1992). This analysis 
was repeated using only the Corbicula. Den- 
tallum. Katharina. Lepetodhlus. Modiolus, 
Neothgonia. and Solemya COI sequences 
(seven taxa) in order to minimize the number 
of closely related taxa present in the hierar- 
chical structure analysis. Significant structure 
was still present in this truncated COI data 
matrix (g^ = -0.527; with 295 variable sites, p 
< 0.01), which suggests that the hierarchical 
structure present in the original data matrix 
was not solely due to the presence of closely 
related taxa. The findings from the plots of 
substitution pattern and g, statistics are con- 
sistent with the hypothesis that significant 
phylogenetic signal exists in the transformed 
COI nucleotide data matrix and validate the 
latter's use in this particular phylogenetic con- 
text (e.g., Swofford et al., 1996). Since amino 
acid substitution rates are lower than the un- 
derlying nucleotide substitution rates (e.g., Li 
& Graur, 1 991 ), it follows that the inferred COI 
amino acid sequences are not saturated and, 
therefore, also appropriate for this level of 
phylogenetic analysis. 

The best tree produced by ML analysis of 
the transformed COI nucleotide mathx is pre- 
sented in Figure 3 along with bootstrap per- 
centages for the NJ (above branches, 1,000 
replicates), MP (below branches, 1,000 repli- 
cates), and ML (in parentheses, 100 repli- 
cates) analyses. Only bootstrap percentages 
greater than 50% are shown. This topology is 
largely congruent with the best trees pro- 
duced by MP (three equally parsimonious 
trees) and NJ analyses (trees not shown). 
However, the topological relationships of the 
non-autobranch taxa on the best MP trees 
were identical to those portrayed in the trees 
derived from analyses of the inferred CO! 
amino acid sequences (see below). 

The Kishino-Hasegawa test results (Table 
1) indicate that the morphology-based topol- 
ogy represented in Figure 1 Awas significantly 
worse (p < 0.05) than the best topology from 
ML analyses of the transformed COI data ma- 
trix (Figure 3). However, the morphology- 
based topology represented in Figure 1 В was 



NEOTRIGONIA PHYLOGENETIC RELATIONSHIPS 



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Proportion of Nucleotide Differences (all positions) 

FIG. 2. Substitution pattern for transitions (s) and transversions (v) at each codon position for the CO! frag- 
ment analyzed herein. The number of transitions and transversions is plotted against the proportion of nu- 
cleotide differences over ail positions. 



not significantly worse (p > 0.05) than that de- 
rived from ML analysis. These test results 
confirm significant discordance between the 
morphology-based topology represented in 
Figure 1A and the COI-based topology (e.g., 
Swofford et al., 1996). 

Figure 4 represents the best topology gen- 
erated from NJ analysis of the inferred COI 
amino acid sequences with bootstrap per- 
centages for NJ (above branches) and MP 
(below branches) analyses. Only bootstrap 
percentages greater than 50% are shown. 
The strict consensus tree (not shown) of the 



39 equally parsimonious trees produced by 
MP analysis of the inferred CO! amino acid 
matrix is less resolved but entirely congruent 
with the NJ tree. 

All analyses of the transformed COI nu- 
cleotide and inferred amino acid matrices 
were consistent with the monophyly of the Au- 
tobranchia, Veneroida, Mytiloida, and Union- 
oida (e.g., Figs. 3, 4). The trees in Figures 3 
and 4 are especially noteworthy due to the 
strong inference that the filibranchous 
Neotrigonia (Trigonioida) is more closely re- 
lated to eulamellibranchous freshwater mus- 



272 



HOEH ETAL. 



100 



99 



66 



71 



62 
(55) 



82 
(51) 



100 
(98) 



(57) 



(64) 



100 
1(100) 



_25_ 



75 
(83) 



88 



97 



.m. 



97 
(100) 



83 
(67) 



75 



55 



- Dreissena 

- Mytilopsis 
-Rangia 

- Mercenaria 
-Corbicula 

- Modiolus 
Geukensia 
Amblema 

- Margaritifera 

- Anodonta 
Mutela 



Veneroid 
Bivalves 



~] Mytiloid 
J Bivalves 



Unionoid 
Bivalves 



Neotrigonia 


Trigonioid 
Bivalve 


Solemya 


~ Protobranch 


Nucula 


Bivalves 


Lepetodrilus 


(Snail) 


Dentalium 


(Tusk Shell) 


Katharina 


(Chiton) 



Autobranch 
Bivalves 



Non-bivalve 
Molluscan 
Outgroup Taxa 



FIG. 3. Best tree topology produced by maximum likelihood analysis of the transformed COI nucleotide ma- 
trix. Numerals are bootstrap percentages for NJ (above branches. 1.000 replicates). MP (below branches, 
1.000 replicates), and ML (parentheses. 100 replicates) analyses. Only bootstrap values greater than 50% 
are shown. 



TABLE 1. Kishino-Hasegawa Test evaluation of the two phylogenetic hypotheses presented in Figure 1 
against the best DNAML tree from the CO! nucleotide sequence analysis (Fig. 3). User trees with Z-values 
(= the difference between log likelihood values of best tree and user tree divided by the standard deviation 
of the difference) of absolute magnitude 2.0 or greater are considered significantly worse (p < 0.05) than the 
best DNAML tree. 





Log likelihood value 










(Range of Log 


Range of 






Tree Topology 


likelihood values) 


differences in Ln L 


Range of Ln LS.D. 


Range of Z-values 


best DNAML 










tree 


-6579.54852 


— 


— 


— 


Figure 1A(34 user 


(-6661.59438 10 


-82.04587 to 


26.3566 to 


-3.1129 to 


trees) 


-6634.71091) 


-55.16240 


22.8030 


-2.4191* 


Figure IB (48 user 


(-6625. 17868 to 


-45.63016 to 


27.4627 to 


-1.6615 to 


trees) 


-6601.80601) 


-22.25749 


18.5040 


-1.2028 



'Significantly worse than the best tree topology at the p < 0.05 level. 



NEOTRIGONIA PHYLOGENETIC RELATIONSHIPS 



273 



100 



53 



53 



51 



55 



.5a_ 

98 



SL. 



100 



_ZS_ 



_9fl_ 



_2Z_ 



98 



83 



56 



93 



-84_ 



_Z2_ 



55 



- Dreissena 
-Mytilopsis 

- Mercenaria 
-Rangia 
-Corbicula "" 

Modiolus 
-Geukensia 
■ Margaritifera ~ 

Anodonta 

Amblema 

Mutela 

Neotrigonia 

Nucula 

Dentalium 

Solemya 

Lepetodrilus 

Katharina 



Veneroid 
Bivalves 



~] Mytiloid 
J Bivalves 



Unionoid 
Bivalves 



Trigonioid -I 
Bivalve 

Protobranch 
Bivalve 

(Tusk Shell) 

Protobranch 
Bivalve 

(Snail) 
(Chiton) 



Autobranch 
Bivalves 



FIG. 4. Best tree topology produced by neighbor-joining analysis of the inferred CO! amino acid sequences. 
Numerals are bootstrap percentages for NJ (above branches, 1,000 replicates) and MP (below branches, 
1 .000 replicates) analyses. Only bootstrap values greater than 50% are shown. 



sels (Unionoida) than to the filibranchous 
mytiloids (mean level of bootstrap support = 
98%). This level of bootstrap support sug- 
gests a robust resolution of the evolutionary 
relationships of Neotrigonia among the taxa 
utilized herein (Hillis & Bull, 1993). 

This particular phylogenetic placement of 
Neotrigonia was also manifest in the best 
trees (not shov\/n) constructed from analyses 
of the COI nucleotide sequences when (1 ) the 
native (untransformed) COI sequences were 
utilized (ML, MP and NJ analyses), (2) all 
codon positions were coded for transversions 
only (ML, MP, and NJ analyses), and (3) only 
first and second codon positions were used 
(ML, MP, and NJ analyses). These results 
taken together are consonant with the hy- 
pothesis that there is a strong phylogenetic 
signal in the COI sequences supporting the 



placement of Neotrigonia as sister taxon to 
the Unionoida. 

Another noteworthy aspect of all of the 
above phylogenetic analyses was the ab- 
sence of support for bivalve mollusk mono- 
phyly. In the phylogenetic hypothesis repre- 
sented in Figure 3, the protobranch bivalves, 
Nucula and Solemya. are portrayed as a 
clade, with the gastropod, Lepetodrilus. as the 
sister taxon to that clade. The phylogenetic 
hypothesis represented by Figure 4 portrays 
Nucula as the sister taxon of the Autobranchia 
while Solemya is the sister taxon to Lepeto- 
drilus. While our analyses were somewhat 
limited due to the relatively small number of 
nucleotides and taxa analyzed, the fact that 
none of the best trees or bootstrap trees gen- 
erated from these analyses gave support for a 
monophyletic Bivalvia suggests that the impli- 



274 



HOEH ETAL. 



cations of these results be seriously consid- 
ered. 



DISCUSSION 

Morton (1987) argued, based partially on 
the anatomical discontinuities between trigo- 
nioids and unionoids, that Neotrigonia was 
a transitional taxon, phylogenetically inter- 
mediate between the presumed ancestral 
protobranch bivalves and the more derived 
pteriomorph bivalves. This hypothesis is con- 
sistent with that of Salvini-Plawen & Steiner 
(1996; Fig. 1A). However, the results of the 
COI sequence analyses (Figs. 3, 4) strongly 
suggest that the extant representative of the 
Trigonioida, that is, the genus Neotrigonia, is 
the sister taxon to unionoid bivalves, as sug- 
gested in the hypothesis of Waller (1990; Fig. 
IB). This phylogenetic propinquity is sup- 
ported by similarities in shell structure (Taylor 
et al., 1 969, 1 973; Tevesz & Carter, 1 980), gill 
speculation (Taylor et al., 1969, 1973), sperm 
morphology (Popham, 1979; Healy, 1989), 
and gill cilia patterns (Atkins, 1937; Tevesz, 
1975). Furthermore, the indicated monophyly 
of the Unionoida is consistent with the hy- 
pothesis of a single invasion of freshwater by 
the ancestral unionoid. This finding corrobo- 
rates the hypothesis of a dramatic evolution- 
ary transition in larval morphology, that is, be- 
tween glochidium and haustorium/lasidium 
morphology, during unionoid phylogenesis. 
Evaluating the directionality of this character 
state transition will require further, broad- 
scale phylogenetic analyses. 

Another interesting result is the placement 
of Solemya (in Figs. 3, 4) and Nucula (in Fig. 
3), both protobranch bivalves, among the non- 
bivalve outgroup taxa. This observation is not 
an artifact of the particular rooting scheme em- 
ployed in Figures 3 and 4. It is not possible to 
root either of these topologies such that all of 
the bivalve taxa represented therein form a 
monophyletic group. In all of the phylogenetic 
analyses of the COI sequences, Solemya was 
either (1 ) the sister taxon to Lepetodrilus or (2) 
in a clade with Nucula and Lepetodrilus. 
Therefore, these analyses provide some sup- 
port for the hypothesis that the currently-rec- 
ognized molluscan taxon Bivalvia is a poly- 
phyletic assemblage. The non-monophyletic 
status of the Bivalvia was supported by a re- 
cent phylogenetic analysis of 18S rDNA se- 
quences (Adamkewicz et al., 1 997; fig. 2). Fur- 
thermore, the topology in our Figure 3 



suggests that the protobranch bivalve genera 
Nucula and Solemya are more closely related 
to the snail, Lepetodrilus, than to the other bi- 
valve taxa in the analysis. Thus, the shared 
presence of bipectinate gills and hypobran- 
chial glands (J. E. Morton, 1988), esophageal 
and stomach similarities (Salvini-Plawen, 
1988), ultrafiltration site similarities (Andrews, 
1988), oxygen transport molecule similarities 
(Mangum et al., 1987), and flattened pedal 
areas in both protobranch bivalves and primi- 
tive gastropods may be due to shared com- 
mon ancestry rather than to the retention of 
ancestral character states. 

The phylogenetic relationships of Neotrigo- 
nia. Nucula. and Solemya. as deduced from 
the COI analyses presented herein (e.g.. 
Figs. 3, 4), suggest that a significant amount 
of convergent anatomical and conchological 
evolution has taken place within the Mollusca. 
There is a great deal of precedent for this 
statement (e.g., Allen, 1985; Purchon, 1990; 
Davis, 1994; Salvini-Plawen & Steiner, 1996). 
An important evolutionary implication that 
stems from the phylogenetic placement of 
Neotrigonia as sister taxon to a freshwater 
mussel clade is that it corroborates previous 
hypotheses of convergence (e.g.. Waller, 
1990) in the evolution of autobranch bivalve 
gill structure, i.e., either the filibranchous or 
the eulamellibranchous gill condition evolved 
at least twice in the evolutionary history of 
these bivalve taxa (Fig. 5A). The latter possi- 
bility is favored by Waller (1990). The evolu- 
tion of eulamellibranchous gill organization 
(which facilitated larval brooding) may have 
been a necessary antecedent to the success- 
ful colonization and subsequent marked evo- 
lutionary diversification in freshwater habitats 
by unionoid bivalves. 

The implications of the hypothesized phylo- 
genetic relationships of Nucula and Solemya, 
as inferred from analyses of COI sequences, 
are more profound. It is suggested that the bi- 
valved phenotype has evolved at least three 
times during the evolution of the Mollusca; (1) 
in the ancestor of the Juliidae, a relatively de- 
rived family within the opisthobranch gas- 
tropods (not represented in the analyses 
herein), (2) in the ancestor of the Autobran- 
chia, and (3) in the ancestor of the Proto- 
branchia (assuming a monophyletic Proto- 
branchia, Fig.5B). If the genera Tuarangiaand 
Pseudomyona are found to be bivalved mono- 
placophorans (Runnegar, 1983) rather than 
autobranch bivalves (Mackinnon, 1982; Berg- 
Madsen, 1 987), and if the Solemyoida and Nu- 



NEOTRIGONIA PHYLOGENETIC RELATIONSHIPS 



275 






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absent 
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equivocal 






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FIG. 5. Morphological character optimization using MacClade on the best topology produced from maximum 
likelihood analysis of the transformed CO! nucleotide matrix using Katharina as the outgroup. A. The most 
parsimonious estimate of autobranch bivalve gill character state transitions for the taxa included in these 
analyses is that either the filibranchous or eulamellibranchous character state evolved at least twice. B. The 
most parsimonious estimate of character state transitions for the taxa included in these analyses suggests 
that the bivalved phenotype has evolved at least twice. Justification for the use of Katharina as the outgroup 
for the molluscan taxa included in this analysis is provided by numerous studies (e.g., Salvini-Plawen. 1 980, 
1985, 1988, 1990; Wingstrand, 1985; Eernisse, et al., 1992; Salvini-Plawen & Steiner, 1996). 



276 



HOEH ETAL. 



culoida had independent origins (Purchon, 
1978; Salvini-Plawen & Steiner, 1996), the bi- 
valved condition would have had to evolved at 
least five times within the Mollusca. This strik- 
ing assessment is nonetheless not totally un- 
expected when evaluated in the context of (1 ) 
the great evolutionary mutability of body plan 
exemplified by the phylum Mollusca (e.g., J. E. 
Morton & Yonge, 1964; Allen, 1985; Willmer, 
1990) and (2) the multiple origins of bivalved 
external shells in four phyla (Thomas, 1988). 
Under the hypothesis of a polyphyletic Bi- 
valvia, the degree of morphological conver- 
gence on the bivalved body plan varies con- 
siderably within the extant mollusks. In the 
case of the opisthobranch gastropod genus 
Julia, the shell has converged on the mono- 
myarian (= single adductor muscle) bivalve 
condition while the soft anatomical character- 
istics are clearly those of a gastropod (Kay, 
1968). However, the degree of convergence 
in body plans between autobranch and proto- 
branch bivalves is much greater and involves 
both shell and anatomical character states. 
The phylogenetic hypothesis displayed in Fig- 
ure 3 suggests that in the distinct evolutionary 
histories of the autobranch and protobranch 
mollusks, in addition to the convergent bi- 
valved shell, there were convergent (1 ) losses 
of head and radula, (2)origins of labial palps, 
(3) origins of the dimyarian adductor muscle 
condition, and (4) origins of fibrous ligament. 
Thus, the evolutionary mutability of body 
plans within the Mollusca may be greater than 
that suggested by the traditional classification 
schemes. Phylogenetic evaluations of addi- 
tional molecular and morphological data sets 
are needed to test the hypothesized polyphyly 
of the Bivalvia and further decipher patterns of 
molluscan body plan evolution. 

ACKNOWLEDGMENTS 

We thank B. Baldwin for help with sequenc- 
ing the veneroids used in this analysis. S. L. 
Baldauf, D. J. Berg, S. I. Guttman, S. L. Neale, 
M. O'Connell, P. O'Reilly, D. T Stewart, B. W. 
Sutherland, and T. R. Waller provided helpful 
comments on earlier versions of this manu- 
script. Neothgonia specimens were provided 
by S. Boyd, and Mutela specimens were pro- 
vided by G. Soliman. R. Bieler provided assis- 
tance with literature acquisition. We also wish 
to thank two anonymous reviewers and G. M. 
Davis for comments on earlier versions of the 
manuscript. This study is New Jersey Agricul- 



tural Experiment Station Contribution #D- 
321 04-3-98 and was supported by state funds 
and NSF grants OCE96331 31 , OCE9302205, 
and OCE891 731 1 (to R. С V. and R. A. L.). 



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Revised ms accepted 16 March 1998 



MALACOLOGIA, 1998, 40(1-2): 279-295 

GEOGRAPHIC AND HABITAT-SPECIFIC MORPHOLOGICAL VARIATION OF 
LITTORARIA {LITTORINOPSIS) ANGULIFERA (LAMARCK, 1822) 

Rachel E. Merkt^ and Aaron M. Ellison^ 

Department of Biological Sciences. Mount Holyoke College. Clapp Laboratories. 50 College 
Street, South Hadley, Massachusetts 01075-6418, USA: aellison@mtholyoke.edu 

ABSTRACT 

Recent, detailed examination of the morphology of the Littorinidae inhabiting Indo-West Pa- 
cific mangrove forests led Reid (1986) to identify 20 species of Littoraria. all of which had previ- 
ously been assigned to only three species within the pantropical "Littorina scabra." No similar 
study has been done on the neotropical Littoraria angulifera (Lamarck), which occurs in man- 
grove forests on both sides of the Atlantic Ocean. We quantified variability in shell and genital 
morphology of L. angulifera throughout its range in the tropical Atlantic using material from both 
museum collections and new, field collections. We tested two hypotheses regarding variation in 
shell shape and sculpture, and frequency of color morphs in populations of L. angulifera: (1 ) ob- 
served variation is associated with the five major current regimes that could restrict its dispersal 
throughout the tropical Atlantic; or (2) observed variation is associated with habitat characteris- 
tics that can influence shell thermal properties. Strong geographical variation in shell shape and 
sculptural characteristics suggested initial support for the dispersal hypothesis. Absence of geo- 
graphical variation in genital morphology, however, led to the rejection of the dispersal hypothe- 
sis. Parallel associations of habitat with geography suggests that L. angulifera is a single species 
throughout the tropical Atlantic, and observed variability results primarily from responses to local 
environmental conditions. However, this conclusion can be tested only with additional genetic 
analysis of disparate populations of L. angulifera. 

Key words: Atlantic, currents, Littoraria angulifera. Littorinidae, mangroves, morphology, shell 
sculpture, shell shape. 



INTRODUCTION 

A recent, detailed examination of the mor- 
phology of the Littorinidae inhabiting Indo- 
West Pacific mangrove forests by Reid (1986, 
1989, 1999) resulted in the identification of 
21 species, all of which had previously been 
assigned to only three species within the pan- 
tropical "Littonna scabra' complex by Rose- 
water (1970, 1980). Reid (1986) also re-as- 
signed these mangrove-inhabiting littorinids to 
the genus L/ííorar/a Griffith & Pidgeon. No sim- 
ilar study has been done on the neotropical 
species Littoraria angulifera (Lamarck), which 
occurs in mangrove forests on both sides of 
the Atlantic Ocean, although Reid (1986, 
1989) considered Eastern and Western At- 
lantic populations of L. angulifera to be a sin- 
gle species based on shell morphology and 
genital characteristics. Rosewater (1 980) con- 
sidered the neotropical "Littohna angulifera" to 
be a subspecies of ''Littorina scabra." although 



earlier authorities (e.g., Bequaert, 1943; Mar- 
cus & Marcus, 1964; Bändel, 1974) conferred 
distinct species status on L. angulifera. princi- 
pally because of its geographical isolation 
from the Indo-West Pacific. Like its Indo-West 
Pacific congeners, L. angulifera is variable in 
shell morphology and color, and we studied 
this variability with respect to geography, po- 
tential dispersal routes, and habitat character- 
istics in the tropical Atlantic. In particular, we 
used museum collections and new field-col- 
lected material to test between two hypothesis 
that could account for observed variation in 
shell shape and sculpture, and frequency of 
color morphs in populations of L. angulifera. 
First, such variation could be associated with 
the five major current regimes that could re- 
strict its dispersal throughout the tropical At- 
lantic. Alternatively, observed variation could 
be a consequence of habitat characteristics 
that can influence shell morphology and atten- 
dant thermal properties. We also use these 



'Current address: Department of Marine Science, University of South Florida, St. Petersburg, Flonda 33620. U.S.A. 
^For all correspondence. 



279 



280 



MERKT & ELLISON 



data to discuss the need for further field stud- 
ies and systematic re-evaluation of L. angulif- 
era throughout its range. 

Intraspecific variation in shell morphology of 
littohnids has been attributed both to environ- 
mental influences and genetic variability 
(Berry, 1 961 ; Newkirk & Doyle, 1 975; Jansen, 
1 982a, b; Cook et al., 1 985; Cook, 1 992; Cook 
& Garbett, 1992; Lewis & Williams, 1995; Mill 
& Grahame, 1995). For example, supratidal 
and high intertidal snails subject to dessication 
stress tend to be highly ornamented or 
grooved (Vermeij. 1973). Smaller, more glo- 
bose shells tend to occur in high-intertidal pop- 
ulations subject to frequent, high-intensity 
waves, while high-spired shells tend to be 
found in more protected areas (North, 1954; 
Newkirk & Doyle, 1975; Roberts & Hughes, 
1980; Janson, 1982b; Johannesson, 1986; 
Brown & Quinn, 1 988; Boulding & Van Alstyne, 
1993; Lewis & Williams, 1995; Johannesson 
et al., 1997). Snails in low-density populations 
where food is abundant grow faster and tend 
to have rounder (low-spired) shells (Berry, 
1961; Kemp & Bertness, 1984). By contrast, 
LIttorina subrotundata Carpenter produces 
taller shells when it grows rapidly (Boulding & 
Hay, 1993). High levels of prédation are asso- 
ciated with increased sculpturing (e.g., nod- 
ules and spines) and shell thickening (Reim- 
chen, 1979, 1982; Cook, 1983; Reid, 1992; 
Cook & Kenyon 1993). These patterns have 
been documented primarily in the temperate 
zone, however. In contrast, studies of tropical 
littohnes have been focused primarily on sys- 
tematics (Bequaert, 1943; Rosewater, 1970, 
1972; Reid, 1986, 1989), zonation (Saseku- 
mar, 1974; Reid, 1985), prédation (Reid, 
1992), and intraspecific shell-color polymor- 
phisms (Reimchen, 1 979; Cook, 1 983; Cook & 
Freeman 1986; Reid, 1987; Cook & Kenyon, 
1993) of Indo-Pacific species. Little attention 
has been paid to intraspecific morphological 
variability of littorinids of the tropical Atlantic 
since the studies of Vermeij (1974), Borkow- 
ski (1975), and Rosewater (1981), which pre- 
date Reid's re-evaluation of the genus Lit- 
toraria. 

Here, we document extensive morphologi- 
cal variability in L. angullfera from both sides 
of the Atlantic Ocean. Littoraha angullfera is 
one of only two littorinids known to occur on 
both sides of the Atlantic (Rosewater & Ver- 
meij, 1972) (Fig. 1), and as such is an exem- 
plar with which to address questions of geo- 
graphically based intraspecific morphological 
variability. Because five distinct oceanic cur- 



rents occur within the range of L. angullfera, 
we expected to see regional divergence in 
morphology that could indicate geographi- 
cally defined subpopulations based on re- 
stricted larval dispersal. In addition, the signif- 
icant variation in mangrove forest structure 
and nutrient availability that occurs through- 
out the tropical Atlantic also could contribute 
to variability in morphology. Morphological 
variation caused by local environmental char- 
acteristics could either amplify or mask mor- 
phological variation of some traits due to 
geographic isolation. Thus, we explore how 
several morphological characteristics covary 
with geography and features of local habitats. 



MATERIALS AND METHODS 
Natural History and Morphology 

Littoraha {Littorlnopsis) angullfera (Fig. 2) is 
the only tropical littorinid that is found exclu- 
sively in mangrove swamps of the Atlantic and 
Caribbean (see distribution map in Rosewater 
& Vermeij, 1972). LIttorarIa angullfera is ovo- 
viviparous, with a planktotrophic larval stage 
estimated to be 8-10 weeks long (Gallagher 
& Reid, 1979). Adult snails occur in the supra- 
littoral zone on trunks, roots, stems, and 
leaves of mangroves, primarily Rhizophora 
mangle L., Avicennia spp., and Laguncularia 
racemosa (L.) Gaertn.f., where they feeds on 
epiphytic algae and marine fungi (Kohlmeyer 
& Bebout, 1986). Because of its supralittoral 
habit, local variation in wave strength and ex- 
posure is unlikely to affect L. angullfera. Pré- 
dation on L. angullfera has not been studied, 
although omnivorous grapsid crabs and 
predatory wading birds (egrets, herons) are 
often seen feeding in and around mangrove 
roots at low tide (A. M. Ellison, personal ob- 
servation). 

The normally light-orange protoconch is 
characterized by 3-5 prominent spiral ridges 
running parallel to the 2-4 whorls. Primary 
grooves appear on the 1^'-4"^ whorl of the 
teleoconch, along with the axial striae (growth 
lines), which do not appear to conform to any 
spatial pattern on the shell surface (Fig. 3). 
Beginning between the 3^^ and last whorls of 
the teleoconch, secondary grooves bisect the 
ribs between already existing primary grooves 
(Fig. 3). When present, tertiary grooves, like 
secondary grooves, appear on the ribs be- 
tween already existing grooves (Fig. 3). If they 



MORPHOLOGY OF LITTORARIA ANGULIFERA 



281 




FIG. 1. Map illustrating collection localities of Littoraria angulifera and the prevailing currents in the Atlantic 
Ocean. Solid arrows are warm currents and dotted arrows are cold currents. 



occur, spiral striae typically begin between the 
4'^ and last whorls of the teleoconch (Fig. 3). 

Samples and Measurements 

We followed methods of Reid (1 986) in col- 
lecting morphological data. A total of 1,042 



specimens were examined from 41 sites 
throughout the distribution of L. angulifera 
(Table 1). The sample size from any single lo- 
cation ranged from two specimens to >100. 
The collections of the Academy of Natural Sci- 
ences in Philadelphia, Pennsylvania (ANSP) 
and The Natural History Museum, London 



282 



MERKT & ELLISON 




FIGS. 2-5. Shell shape and sculpture, and genitalia. 2. Illustration of measurements taken on an individual 
shell. CW: Columellar width; AW: Aperture width; AL; Aperture length. 3. Inset showing shell sculpture. 
PGPrimary groove; SO: Secondary groove: TO: Tertiary groove; AS: Axial stria: SS: Sprial striae. 4. Palliai 
oviduct. SP: Spiral loop; ВС: Bursa copulatrix; SR: Seminal receptacle; O; Oviduct. 5. Penis. F; Filament; 
SG: Sperm groove; GD: Glandular disc. 



(BMNH), were examined along with snails 
that we or our colleagues collected in 1996 in 
Florida. Belize, and Jamaica (vouchered at 
BMNH; Registration numbers 1996411 
through 1996416). In most cases, only shells 
were available for study, but when preserved 
material was available (Florida, Belize, Ja- 
maica, Sierra Leone, Ghana), samples were 
dissected and examined for comparison of 
anatomical characteristics as well. Dissected 
specimens were preserved in formalin and 
exhibited a certain degree of shrinkage, con- 
tortion, and discoloration. This made it impos- 
sible to identify finer characteristics, such as 
gamete structure and head-foot coloration. 
Littoraria angulifera secondarily has lost its 
egg capsule glands (Reid, 1 986), so we could 
not use characters associated with them. 
Categories of shell characteristics studied 



included shape, appearance, sculpture, and 
color (when possible) (Figs. 2, 3). The shape 
of L. angulifera shells is typical of ovovivipa- 
rous, mangrove-dwelling littorines, with a high 
spire and an almost circular aperture (Reid, 
1986). Five measurements— height, breadth, 
apertural width and length, and columellar 
width— were taken on each shell (Fig. 2) using 
calipers (± 0.1 mm). Four of these measure- 
ments were collapsed into three standard 
composite variables: proportionality (= height/ 
breadth), circularity (= apertural width/aper- 
tural length), and spire height (= height/aper- 
tural length). 

Sculpture characteristics (Fig. 3, Table 2) 
were identified using a dissecting microscope. 
The central columella of L. angulifera \ends to 
be creamy yellow in color, convex and 
pinched at its base, with excavation of the 



MORPHOLOGY OF LITTORARIA ANGULIFERA 



283 



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MORPHOLOGY OF LITTORARIAANGULIFERA 



285 



TABLE 2. Shell sculpture characteristics identified or measured. 



Character 



Measurement type 



# whorls in the protoconch 

# whorls in the telochonch 

whorl # in which primary grooves first occur 

# primary grooves at first appearance 
whorl in which axial striae occur 

whorl in which secondary grooves first occur 
regularity of secondary grooves 
presence/absence of tertiary grooves 
whorl in which tertiary grooves first occur 
presence/absence of spiral striae 
whorl in which spiral striae first occur 
columella shape 
columella pinching 
columella color 



numeric 

numeric 

numeric 

numeric 

numeric 

numeric 

categorical (0: irregular; 1: regular) 

categorical (0: absent; 1 ; present) 

numeric 

categorical (0; absent; 1 ; present) 

numeric 

categorical (0: concave; 1 ; vertical; 2; convex) 

categorical (0; pinched; 1 ; unpinched) 

categorical (0; creamy yellow; 1 : otherwise) 



base and lip (Fig. 2, Table 2). Shell color is 
variable, and two distinct color morphs, nor- 
mal and orange, have been identified. The 
ground color of the "normal" color morph is 
creamy yellow to reddish-brown, and is over- 
laid with flecks of dark orange and brown. The 
ground color of the "orange" morph is light or- 
ange or yellow, and it is overlaid with faint or- 
ange flecks. Normal morphs were assigned a 
value of zero, and orange morphs, one. 

Genital characteristics were measured for 
dissected specimens only (Figs. 4, 5). Length 
of the penis and palliai oviduct, diameter of 
the spiral portion of the oviduct, and length of 
the bursa copulatrix were measured with an 
ocular micrometer. 



Statistical Analysis 

We used discriminant analysis, cluster 
analysis, and principle components analysis 
(PCA), in SYSTAT version 7.0 (SPSS, 1997) 
and S-Plus for Windows version 4.0 (Math- 
Soft, 1997), to compare morphological varia- 
tion within and among populations. Because 
many of the samples were from sites close to 
each other (e.g., from within the same coun- 
try), we grouped the sites into 19 discrete ge- 
ographic "locations" for most of the analyses. 
Location groupings are indicated in Table 1 . 
Data were transformed when necessary to 
meet assumptions (approximate normality, 
homoscedasticity) of all statistical tests (see 
Kroonenberg et al., 1997, for transformations 
appropriate for categorical data prior to appli- 
cation of these multivariate analyses). Details 
of each technique are given along with their 
associated results in the following section. 



RESULTS 
Geographic Patterns in Shell Shape 

Shell shape showed pronounced changes 
from east to west among samples. Shells from 
the Western Atlantic and Caribbean have com- 
paratively high spires and more circular aper- 
tures (Table 1 , Fig. 6). The thickness of the col- 
umella also increases from east to west. 
Shells from the Eastern Atlantic have more 
whorls per mm of shell height. Primary 
grooves appeared earlier and in larger num- 
bers, whereas secondary grooves occurred 
later on shells from the Eastern Atlantic. Dis- 
criminant analysis using these eight morpho- 
logical variables (proportionality, circularity, 
and spire height, columellar thickness, whorls/ 
mm, number of primary grooves, whorl on 
which primary and secondary grooves first ap- 
pear, all expressed in standard deviation units) 
correctly identified 85% of the shells as com- 
ing from either the Eastern or Western Atlantic 
(F = 106.6, P < 0.0001; Table 3). However, 
shells from four localities generally were mis- 
classified at this coarse level of geographic 
resolution. Shells from Liberia and Senegal 
were routinely assigned to the Western At- 
lantic, shells from Brazil were assigned more 
commonly to the Eastern Atlantic (Table 3), 
and shells from Gabon were assigned equally 
to each side of the Atlantic. Spire height, 
whorls/mm, columellar thickness, and number 
of primary grooves were the principle vari- 
ables that discriminated between shells of the 
Eastern and Western Atlantic. 

To investigate the hypothesis that morpho- 
logical variation was associated with potential 
dispersal routes, we classified sites according 



286 



MERKT & ELLISON 





^ 0.73 
<^ 0.72 




ÏU 1.70 

X 



FIG. 6. Clinal patterns in shell proportionality, circu- 
larity, and spire height. Illustrations are distance- 
weighted, least-squares smoothing through data 
from all 41 sites. 



to the predominant current affecting them 
(Caribbean, Gulf of Mexico, Gulf Stream, 
North Equatohal, South Equatorial; see Fig. 1 ; 
a pr/'or/ current classifications in Table 1). We 
then used discriminant analysis to see if 
shells could be classified correctly with re- 



TABLE 3. Percent of shells correctly identified by 
discriminant analysis as coming from either the 
Eastern or Western Atlantic. Bold type indicates 
overall discrimination. Normal type indicates dis- 
crimination among locations within either the 
Eastern or Western Atlantic. 



Location 



% 



Eastern Atlantic 

Angola 
Congo 
Gabon 
Ghana 
Liberia 
Nigeria 

Principe Islands 
Senegal 
Sierra Leone 
Western Atlantic 
Bahamas 
Belize 
Bermuda 
Brazil 
Cuba 
Florida 
Haiti 
Jamaica 
Nicaragua 
Virgin Islands 



84 

84 
70 
50 
95 
33 
91 
100 
10 
96 
85 
76 
83 
91 
40 
68 
90 
88 
84 
75 
95 



spect to these prevailing currents. Using the 
same eight standardized morphological vari- 
ables, we could classify correctly 61% of the 
shells overall with respect to current of origin 
(F = 51.7, P < 0.0001). The most important 
morphological variables contributing to dis- 
crimination according to prevailing current 
were whorls/mm, spire height, columellar 
width, and shell circularity. In total, we could 
correctly classify 75% of shells from sites as- 
sociated with the North Equatorial current, 
71% from the South Equatorial current, 66% 
from the Gulf Stream, 64% from the Gulf of 
Mexico, and 40% from the Caribbean. 

Within each current grouping, most shells 
from most locations were correctly classified 
into their respective current regimes (Fig. 7). 
Exceptions included Nicaragua (generally as- 
signed to the South Equatorial current instead 
of the Caribbean); Brazil and Liberia (all as- 
signed to the South Equatorial current instead 
of the North Equatorial current); Senegal (as- 
signed to either the Caribbean or South Equa- 
torial current instead of the North Equatohal 
current); and Gabon (30% of which were as- 
signed to the Caribbean current). Shells from 
the Cahbbean islands of Cuba and Jamaica 
frequently were assigned to the Gulf of Mex- 
ico or the Gulf Stream, whereas shells from 



MORPHOLOGY OF LITTORARIA ANGULIFERA 
PREDICTED 
OBSERVED С GM GS NE SE 



287 



Caribbean 












Belize 


Щ 








Cuba 

Jamaica 

Nicaragua 

































Gulf of Mexico 

Florida 


■i 






■ 







Gulf Stream 

Bahamas 
Bermuda 

Haiti 
Virgin is. 




■ 






■ 






■ 








'iV4-" 








■ 





North Equatorial 

Brazil 
Ghana 
Liberia 
Nigeria 

Principe Is. 

Senegal 

Sierra Leone 








■ 










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PERCENT 

100 

90 

80 

70 

60 

50 

40 



30 



20 



10 



South Equatorial 

Angola 
Congo 

Gabon 




































FIG. 7. Classification matrix resulting from discriminant analysis of shells from the five prevailing currents. 
Shading indicates percent classification into each of the five currents, with shading increasing with percent- 
age. For each current, the overall classification is given in the first row (label in bold type), followed by the 
classification for each locality within that current grouping. Predicted current groupings: C— Caribbean; GM— 
Gulf of Mexico; GS— Gulf Stream; NE— North Equatorial; SE— South Equatorial. 



288 



MERKT & ELLISON 



TABLE 4. Loadings of shell morphological variables on the first four principal component axes. Only loadings 
>|0.1| are shown. The first four axes account for 90% of the among-location variance in shell morphology. 
Characters are ordered in descending order of their loadings on the first principal axis. 



Variable 


Axis 1 


Axis 2 


Axis3 


Axis 4 


Thickness of columella 


0.476 


-0.170 


-0.186 


-0.318 


Shell proportionality 


0.471 




0.401 




Whorls/mm of shell height 


-0.464 


0.180 




0.348 


Shell spire height 


0.385 




0.582 


0.249 


Whorl on which secondary groove first appears 


0.276 


0.503 


-0.345 


0.256 


Number of primary grooves 


0.234 


-0.433 


-0.457 




Whorl on which primary groove first appears 


0.197 


0.603 


-0.326 




Shell circularity 


0.137 


-0.353 


-0.159 


0.803 


Cumulative proportion of variance explained 


0.42 


0.66 


0.78 


0.90 



Haiti (collected on the northern [Gulf Stream] 
side of the island) were mis-assigned to either 
the Caribbean or Gulf of Mexico. 

Our eight shell morphology characteristics 
explained 90% of the among-location vari- 
ance identified by principal components anal- 
ysis (Table 4). Columellar width, proportional- 
ity, whorls/mm, and spire height loaded most 
heavily on the first axis, whereas whorl on 
which primary and secondary grooves first 
appeared, number of primary grooves, and 
shell circularity loaded most heavily on the 
second axis (Table 4. Fig. 8). Shells from 
Principe, Ghana, Sierra Leone, Nigeria, and 
Angola were distinguished from the others be- 
cause of their low spire height and shell pro- 
portionality and their relatively large numbers 
of whorls/mm of shell height (Fig. 8). In other 
words, these five locations had the most glo- 
bose shells. Shells from Angola, Congo, and 
Gabon had the most circular apertures (Fig. 
8). Shells from the Virgin Islands, Nicaragua, 
Senegal, and Cuba were relatively high 
spired, and shells from the Virgin Islands and 
Bermuda had the thickest columellae. 

Cluster analysis similarly illustrated the 
groupings of sampling localities according to 
these eight morphological variables (dendro- 
gram not illustrated). We identified five clear 
groupings of locations from the complete-link- 
age dendrogram resulting from our cluster 
analysis: (1) Principe, Ghana, and Sierra 
Leone: (2) Congo, Gabon, Angola, Nigeria, 
and Brazil; (3) Liberia, Senegal, and Nica- 
ragua; (4) Belize, Haiti, Jamaica, the Baha- 
mas, Cuba, and Florida; (5) Bermuda and the 
Virgin Islands. 

Habitat-Specific Patterns in Shell Shape 

Climatic properties, stature of the mangrove 
forests of each location (Table 5), and primary 



nutrient source (oligotrophic vs. estuarine) 
were used to test for relationships between 
habitat characteristics and shell morphology. 
As with the morphology data, we first ordi- 
nated the sites according to the five variables 
using PCA. The loadings of the variables 
for the first two principal axes are shown in 
Table 6. The first axis is a function primarily of 
average canopy height and nutrient source 
(estuarine vs. oligotrophic), whereas the sec- 
ond axis is a function primarily of annual 
temperature and amount and pattern of rain- 
fall. Together, these two composite axes en- 
compassed 70% of the among-habitat vari- 
ance. Standardized morphological and habitat 
scores for each location were computed by 
multiplying each variable by the factor coeffi- 
cient derived from the PCAs morphological 
and habitat data, respectively. These products 
were then summed to yield a single standard- 
ized morphological or habitat score (computa- 
tions done in Systat version 7.0). For clarity, 
we only illustrate the standardized scores 
based on the factor coefficients of the first prin- 
cipal component axis from each analysis. The 
result of this computation is a single compos- 
ite morphological score and a single compos- 
ite habitat score for each of the 19 locations. 
We found a significant association between 
these two scores (r = 0.54, P = 0.018: Fig. 9), 
which indicated a significant correlation of 
overall shell morphology with their local envi- 
ronment. This figure also illustrates clearly the 
similarity in overall shell morphology and habi- 
tat of Brazil, Nicaragua, and all the African 
samples. 

Shell Color 

Most shells had "normal" coloration; of the 
total sample, 68 shells (6.5%) were the "or- 
ange" morph. No differences in relative fre- 



MORPHOLOGY OF LITTORARIA ANGULIFERA 



289 



о 



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ö 



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< 

ü 



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CO 






Ftorida 



Sierra Leone 



WHORLS/mm 

Ghana 
Principe Is. 



START OF 
1° GROOVES 

START OF 
2° GROOVES 
Cuba 



Nicaragua 
Senegal 




SPIRE HEIGHT 

PORTIOr lALITY 

COLUM 
THICI 
Virgin Is. 



CRCULARITY 



# f GROOVES 



Bermuda 



Angola 



Congo 
Gabon 



ELLAR 
THICK viESS 



-0.4 



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FIRST PRINCIPAL COMPONENT 



FIG. 8. Principal components biplot illustrating placement in ordination space of the 19 sampling locations 
with respect to eight morphological variables. All variables were standardized prior to analysis. Loadings for 
these two component axes, as well as axes three and four, are given in Table 4. 



quencies were found between shells from the 
eastern and western Atlantic (x^ = 0.823, P = 
0.360, Fisher's Exact Test). Among current 
regimes, both the Gulf Stream and South 
Equatorial samples had more orange morphs 
than expected by chance alone (13.9% and 
24%, respectively, x^ = 36.096, P < 0.001 , G- 
test). This result was due to unusually high 
frequencies of the orange morph in samples 
from Angola (24%), Bermuda (36.4%), and 
Virgin Islands (20%). Shell color was not 
clearly associated with any habitat-specific 
variable. 

Genitalia 

The palliai oviduct of the ovoviviparous L. 
angulifera has a single spiral loop that passes 



through the albumen and membrane glands 
(Fig. 4), unlike the palliai oviduct of oviparous 
congeners, which have four to six loops that 
contain additional capsule glands through 
which the eggs must pass before being re- 
leased. The penial glandular disc is round, 
flattened, and darker in color than the rest of 
the penis, and the open sperm groove runs 
along the filament (Fig. 5). All specimens from 
which the penis was removed and drawn 
showed a remarkable uniformity in shape and 
size (Table 7). Additional multivariate analysis 
of sites for which we measured genital char- 
acteristics showed that those populations 
were distinguishable based only on charac- 
teristics of the palliai oviduct, which was much 
longer at one Florida site and at Wee Wee 
Cay than at the other sites. However, absolute 



290 



IERKT& ELLISON 



TABLE 5. Habitat characteristics of the 1 9 locations. Data from Walter et al. (1 975); Wilcox et al. (1 975); Ward 
& Bunyard (1992); Surnan (1994); Saenger & Bellan (1995); Spalding et al. (1997). 





Annual 


Number of dry 


Mean monthly 


Mean canopy 


Nutrient 


Location 


rainfall (mm) 


months 


temp. ( = C) 


height (m) 


source 


Eastern Atlantic 












Angola 


363 


9 


26.4 


30 


estuarine 


Congo 


1306 


4 


25.3 


30 


estuarine 


Gabon 


1904 


4 


26.3 


30 


estuarine 


Ghana 


858 


6 


26.5 


15 


estuarine 


Liberia 


3874 


3 


27.0 


30 


estuarine 


Nigeria 


1830 


4 


26.3 


12 


estuarine 


Principe Islands 


721 


4 


26.2 


5 


oligotrophic 


Senegal 


516 


8 


24.0 


4 


estuarine 


Sierra Leone 


4349 


4 


26.6 


35 


estuarine 


Western Atlantic 












Bahamas 


1181 


2 


25.1 


3 


oligotrophic 


Belize 


1500 


2 


29.5 


8 


oligotrophic 


Bermuda 


1483 





21.4 


3 


oligotrophic 


Brazil 


2150 


4 


26.4 


30 


estuarine 


Cuba 


1481 


3 


25.2 


10 


oligotrophic 


Florida 


1004 


1 


25.3 


10 


oligotrophic 


Haiti 


1242 


6 


27.5 


10 


oligotrophic 


Jamaica 


800 


3 


26.4 


12 


oligotrophic 


Nicaragua 


3293 





26.0 


15 


estuarine 


Virgin Islands 


1638 





26.4 


5 


oligotrophic 



TABLE 6. Loadings of habitat variables on the first 
two principal component axes. Only loadings >|0.1 1 
are shown. These two axes account for 70% of the 
among-location variance in habitat. Characters are 
ordered in descending order of their loadings on the 
first principal axis. 



Variable 



Axis 1 



Axis 2 



Canopy height 


0.898 


0.122 


Nutrient source 


0.832 


-0.207 


Annual rainfall 


0.525 


0.788 


Number of dry months 


0.504 


-0.807 


Average annual temperature 


0.412 


0.133 



Cumulative proportion of 
variance explained 



0.44 



0.70 



shell height and palliai oviduct length were 
significantly correlated (r^ - 0.54; P = 0.024), 
so this result simply shows that large snails 
had large palliai oviducts. On the other hand, 
shell height and penis length were not corre- 
lated (r^ = 0.17; P = 0.27) among these sites. 



DISCUSSION 

Our data illustrate substantial variation in 
shell morphology in Littoraha angulifera. and 
this variation is associated both with potential 
dispersal paths and local habitat conditions. 
Despite an 8-10 wk planktonic larval stage, 
long enough to cross the Atlantic on any of the 



trans-Atlantic currents, populations associ- 
ated with different current regimes exhibit 
clear and strong differences in shell morphol- 
ogy (Figs. 6, 7. Table 3). This observation on 
first glance supports the hypothesis that re- 
gional diversification associated with dispersal 
is occurring in this species. The strong associ- 
ation of habitat types with geography (Table 5), 
however, lends some credence to the hypoth- 
esis that morphological variation is deter- 
mined primarily by local environmental condi- 
tions. Furthermore, the principal exceptions to 
the disperal-morphology association (Fig. 8), 
namely shells from Senegal, Liberia, Brazil 
and especially Nicaragua (which is well-iso- 
lated from easy trans-Atlantic dispersal via ei- 
ther equatorial current), and the uniformity in 
genital form and size from snails from both 
sides of the Atlantic (Table 7) suggest that we 
should reject the hypothesis of regional diver- 
sification associated with dispersal as a cause 
for morphological variation in L. angulifera. 

Littorarla angulifera inhabits mangrove 
swamps, and we hypothesize that observed 
variation in its shell morphology is most likely 
caused by habitat-specific differences in nutri- 
ent status associated with local climate, forest 
structure, and prevailing geomorphology. 
Mangrove swamps in Florida, the Bahamas, 
and the Caribbean Islands are primarily found 
on carbonate platforms and are markedly olig- 
otrophic (nutrient-poor) relative to the more 



MORPHOLOGY OF LITTORARIA ANGULIFERA 



291 



Ш 

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г =0.54 
Р=0.02 



Principe 



Ghana 



Nigeria Angola 



Sierra L{ 



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)ne 



''lo^iSlâm 



Congo Liberia 



Cuba Senegal 

Nicaragua 



Virgin Islands 



Bsrmuda 



T — I — I — I — I — I — I — I — I — I — I — I — I — I — I — I — I — I — r 
-2-10 1 2 

FIRST HABITAT FACTOR SCORE 

FIG. 9. Association between standardized habitat and shell morphology scores for the 19 locations. 

TABLE 7. Measurements of genital characteristics (means in mm with standard deviations in 
parentheses). All values are lengths, except for diameter of the spiral portion of the palliai 
oviduct. Sample size for neotropical samples = 20; for African samples = 6. 







Palliai 


Spiral 


Bursa 


Sample site 


Penis 


oviduct 


Portion 


copulatrix 


Florida: Cockroach Bay 


2.5 (2.5) 


1.9(2.2) 


0.7 (0.9) 


1.2(1.5) 


Florida: Little Shark River (mouth) 


2.7(3.0) 


2.6(2.8) 


0.9(1.0) 


1.8(2.1) 


Florida: Little Shark River (middle) 


3.1 (3.9) 


4.1 (4.2) 


1.7(1.9) 


2.8(3.0) 


Florida: Little Shark River (upper) 


2.0 (2.9) 


2.6(2.5) 


0.9(0.9) 


1.9(1.9) 


Florida: Hurricane Island 


2.3(2.8) 


2.1 (2.0) 


0.9 (0.9) 


1.3(1.2) 


Belize: Wee Wee Cay 


2.4 (3.6) 


3.5(2.6) 


1.7(1.2) 


2.1 (1.6) 


Jamaica: St. Anne's Bay 


2.7(2.7) 


1.7(2.1) 


0.7(0.8) 


1.1 (1.4) 


Ghana 


1.9(2.4) 


1.0(1.1) 


0.3 (0.4) 


0.8(0.9) 


Sierra Leone: Freetown (II) 


2.5 (3.4) 


1.7(2.6) 


0.5(0.4) 


1.9(2.1) 



eutropliic (nutrient-rich) estuarine mangroves 
of Africa, Nicaragua and South America (e.g., 
Twilley, 1995). Oligotrophic swamps have 
higher salinity and water clarity (Twilley, 1 995), 
and may be associated with lower fungal bio- 



mass on the leaves where L. angulifera feeds 
(Kohlmeyer & Bebout, 1986) than estuarine 
ones. Lower food availability and higher salin- 
ity may result in slower growth rates of L. 
angulifera. Kemp & Bertness (1984) demon- 



292 



MERKT & ELLISON 



strated experimentally that well-fed, fast- 
growing Littorina littorea produce more 
rounded, globose shells (like L. angulifera 
from most of Africa, Nicaragua, and Brazil), 
while poorly fed, slower-growing Littorina lit- 
torea produced more pointed, high-spired 
shells (like L. angulifera from Florida and the 
Caribbean). Boulding & Hay (1993) found, in 
contrast, that well-fed Littorina subrotundata 
produces high-spired shells. Additional exper- 
imental work is needed to assess the role of 
food availability on shell shape in L. angulifera. 
and in littorines in general. 

The high-spired shells from Senegal occur 
in short-statured mangrove forests that are 
more like those of the Caribbean than the rest 
of the sampled African locations (Table 5, Fig. 
10). Caribbean and Senegalese mangroves 
are short (generally < 10 m) with relatively 
open canopies, and in such forests, insolation 
is likely to be higher and evaporation greater. 
It is likely that snails in these forests experi- 
ence higher mid-day temperatures than snails 
in mangroves with tall, closed canopies. This 
observation, along with the strong association 
of canopy height with the first principal axis of 
the habitat PCA and rainfall and average tem- 
perature on the second principal axis of the 
habitat PCA strongly suggests that shell 
shape in L. angulifera is associated with 
dessication resistance (Fig. 9 links the mor- 
phology and habitat PCAs.) 

Shell sculpturing may also be associated 
with food availability (Berry. 1961: Jansen, 
1982a) and dessication resistance (Vermeij, 
1973). Vermeij (1973) suggested that even 
very small variations in shell sculpture may re- 
duce dessication as grooves may serve to re- 
flect heat and cause cooling through convec- 
tion. Shell sculpture characteristics (number 
and location of primary and secondary 
grooves) loaded heavily on the first two princi- 
pal components axes (Table 4) in the analysis 
of shell morphology. Figure 9 suggests addi- 
tional linkages between shell sculpture and 
habitat characteristics. For example, shells 
from Bermuda, the Virgin Islands, Congo, 
Gabon, and Senegal are distinguished from 
the others by relatively many primary grooves, 
and mangrove forests in these areas are 
sparse and short in stature, or occur in regions 
with pronounced dry seasons (Chapman, 
1976). Note that despite exceptionally low 
rainfall and a 9-month dry season, the canopy 
height in Angolan mangrove forests is very 
high as a consequence of high nutrient input in 
Angolan estuaries. We infer that the lower sur- 



face temperatures, reduced rate of evapora- 
tion, and increased nutrient levels leads to 
snails with globose shells (Table 1 ). Shell color 
polymorphism in Littoraria may also be asso- 
ciated with dessication avoidance (Cook, 
1983; Cook & Freeman, 1986: but see Reid, 
1 987), but we lack detailed microclimatic data 
for any of these sites. In a preliminary study, 
however, we found no association between 
substrate temperature, insolation, and fre- 
quency of orange morphs of L. angulifera at 
Wee Wee Cay, Belize (A. M. Ellison, unpub- 
lished data). We note also that the frequency 
of rare, orange morphs of L. angulifera is likely 
to be artificially high in museum samples be- 
cause of collecting bias. 

Observed variation in columellar thickness 
may be associated with prédation, but we 
know little about predators of L. angulifera 
and other supralittoral littorinids. Reid (1985, 
1986, 1988. 1992) suggests that grapsid 
crabs prey on Littoraria in Pacific mangrove 
forests, and omnivorous grapsids do occur in 
Atlantic mangroves (Sterrer, 1986). However, 
there have been no studies of their diets. 
Shell color polymorphism may also be associ- 
ated with prédation (Reimchen. 1979: Cook, 
1983: Reid, 1988; Cook & Kenyon 1993). Fur- 
ther study of both microclimate and predators 
of L. angulifera is needed, especially in Ber- 
muda, the Virgin Islands, and Angola, where 
we recorded exceptionally high frequencies of 
orange shell morphs. 

We observed site-specific differences in 
palliai oviduct length that were correlated with 
shell size, but penis length was invariant with 
respect to shell size. This result is not unex- 
pected because a larger palliai oviduct would 
be associated with increased clutch size in 
larger snails. Comparable variability in penis 
length, however, could limit male reproductive 
success. 

Genetic variability underlies morphological 
variation in some littorinids (Jansen, 1982b; 
Cook, 1992: Cook & Garbett, 1992; Mill & 
Grahame, 1995). Although the lengthy larval 
stage (Gallagher & Reid, 1979) and likelihood 
of regular gene-flow among populations (at 
least those within current regimes) suggests 
that genetic differentiation among local popu- 
lations of L. angulifera is unlikely, Jansen 
(1985) found unexpectedly high genetic vari- 
ation among Florida populations of L. angulif- 
era. Jansen (1985) attributed this variation ei- 
ther to differential selection due to abiotic 
factors and prédation, or to restricted gene 
flow due to limited larval dispersal affected by 



MORPHOLOGY OF LITTORARIA ANGULIFERA 



293 



current distribution. Larger genetic diver- 
gence was found between Gulf Coast and At- 
lantic Coast populations of L. angulifera than 
was found among populations on either side 
of the peninsula. In another study of genetic 
variability in L. angulifera within the Gulf of 
Mexico however, Gaines et al. (1974) found 
no differences between observed and ex- 
pected numbers of heterozygous individuals 
in 19 of 20 island populations. 

Linking larval dispersal, distribution, and 
variability of genetic and phenotypic origin in 
oviparous and ovoviviparous gastropods is 
complicated by the lack of knowledge con- 
cerning the pelagic portion of the larval stage; 
laboratory breeding experiments and rearing 
of larvae generally have been unsuccessful 
(McOuaid, 1996). Nonetheless, more system- 
atic study of local and regional morphology, 
and further genetic study of these popula- 
tions, combined with the results of this study 
based on opportunistic museum collections 
would provide a more complete explanation of 
observed geographic and habitat-specific 
morphological variation of Littoraha angulif- 
era. 



ACKNOWLEDGMENTS 

We thank David Reid for loaning us the 
BMNH collection of L. angulifera, and Gary 
Rosenberg for allowing us access to the col- 
lection at ANSP. Rick and Donna Nemeth col- 
lected snails in Jamaica. Tom Smith (USGS) 
and the U.S. National Parks Service provided 
access to collecting sites in the Everglades 
National Park (Florida), and Clinton Dawes 
(USE) provided access to collecting sites in 
Cockroach Bay (Florida). Elizabeth Farns- 
worth suggested several of the analytic ap- 
proaches, and critically reviewed early drafts 
of this manuscript. David Reid and Geerat 
Vermeij provided constructive reviews of this 
paper. This research was supported by NSF 
grants to AME (DEB 92-53743 & DEB 97- 
41904) and the Five College Program in 
Coastal & Marine Sciences. 



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Revised ms. accepted 1 June 1998 



MALACOLOGIA, 1998, 40(1-2): 297-304 

IS CYCLININAE A MONOPHYLETIC SUBFAMILY OF VENERIDAE (BIVALVIA)? 

Mary Ellen Harte 
1180 Cragmont Ave.. Berkeley. California 94708-1613. U.S.A.: jharte@violet.berkeley.edu. 

ABSTRACT 

Cyclininae Frizzell, 1936, consists of two extant genera, Cyclina Destiayes, 1850, and Cy- 
clinella Dall, 1902, characterized by subcircular profiles and lack of anterior lateral hinge teeth 
(Keen, 1969). Acladistic analysis utilizing 14 conchological characters was performed on seven 
venerid taxa to determine if the venerid subfamily Cyclininae represents a monophyletic clade. 
Included in the analysis were the following subfamily type species: Cyclina sinensis (Gmelin, 
1791) (Cyclininae), dementia i//frea (Dillwyn, 1817) (Clementiinae), Dosinia concéntrica {Born, 
1 778) (Dosiniinae), Tapes literata Linnaeus, 1 758 (Tapetinae), as well as the type species of Aus- 
trovenus Finlay, 1927 (Chioninae), A. stutchburii(VJood. 1828), the type species of Cyclinella. С 
tenuis (Récluz 1852), and an outgroup species, Lucinisca nuttalli (Conrad 1837) (Lucinidae). 
Methods demonstrate how continuous data can be used to quantitatively define limits of char- 
acter states for cladistic analysis. Results indicate that: (1) Cyclininae is a construct of conver- 
gent traits (subcircular profiles and lack of lateral teeth), (2) Cyclina is a chionine genus, and (3) 
Cyclinella is a clementiinine or tapetine genus. It is proposed that: (1) Cyclininae be discarded 
as a venerid subfamily and possibly Clementiinae as well, (2) Cyclina be reclassified within the 
Chioninae, and (3) Cyclinella be reclassified within the Clementiininae or Tapetinae. 



INTRODUCTION 

Frizzell (1936) broke up Veneridae (Bi- 
valvia), a large global family of marine clams, 
into 1 2 families: within this scheme, Cyclininae 
Frizzell, 1936, is a subfamily assigned to the 
family Clementiidae Frizzell, 1936. This clas- 
sification was later modified by various work- 
ers (Fischer-Piette, 1975: Fischer-Piette & 
Métivier, 1 971 : Fischer-Piette & Vukadinovich, 
1972, 1975, 1977: Keen, 1969, 1971: Habe, 
1977), who continued to view Veneridae as a 
large, heterogeneous family with many sub- 
families, and incorporated Frizzell's families 
as subfamilies. As classified by Keen (1969), 
Cyclininae Frizzell, 1 936, is one of 1 2 subfam- 
ilies within Veneridae, and composed of two 
small extant genera, Cyclina Deshayes, 1850, 
and Cyclinella Dall, 1902, and three extinct 
genera, Сурл/тег/а Conrad, 1864, Frigichione 
Fletcher, 1938, and Luciploma Olsson, 1942. 
Keen (1969) defined Cyclininae as "Like 
Dosiniinae in form but without anterior lateral 
teeth or incised lunule: sculpture concentric 
with few faint radial traces." Dosiniinae is a 
large subfamily of clams that have subcircular, 
often discoid, valves, defined lunules, pre- 
dominantly fine concentric sculpture, and an- 
terior lateral hinge teeth. Olsson (1 964) classi- 
fied Cyclinella in Dosiniinae. Radial sculpture 



is present in Cyclina and absent in Cyclinella 
and the fossil genera. 

Keen (1 969) defined valves of Clementiinae 
as "thin, inequilateral: without escutcheon; 
sculpture subdued or wanting: inner ventral 
margin smooth: hinge without lateral teeth." In 
fact, Clementia possesses an indented es- 
cutcheon, although the structure is not as 
sharply defined as in, for example, the sub- 
family Chioninae. 

Although both extant cyclinine genera are 
present in the fossil record, Cyc//na contains a 
single extant species, the west Pacific type 
species Cyclina sinensis (Gmelin 1791); Cy- 
clinella contains one moderately common ex- 
tant species, the type species Cyclinella tenuis 
(Récluz, 1852), ranging from off Virginia to 
Brazil (Abbott, 1974), and six rarely collected 
species off tropical west Central America 
(Keen, 1971). 

Despite their subcircular profiles, I observed 
several less obvious differences between Cy- 
clina and Cyclinella that made me suspect 
they were not as closely related evolutionarily 
as their classification might indicate. Homo- 
plasic profiles are common in Bivalvia, often 
stemming from functional convergence (Stan- 
ley, 1 970); within Veneridae, numerous exam- 
ples of apparent homoplasy in profile and 
other conchological characters exist (Jukes- 



297 



298 



HARTE 



Browne, 1913; Jones, 1979; Lindberg, 1990; 
Harte, 1992; Roopnarine, 1996). I performed 
the following cladistic analysis, comparing 
conchiological characters of Cyclina and Cy- 
clinella and taxa of other subfamilies to test the 
null hypothesis that these genera were not 
more closely related to other subfamilies than 
to themselves, thus not warranting the 
breakup of this subfamily. 



MATERIALS AND METHODS 

A cladistic analysis was performed on eight 
taxa (Table 1 ), utilizing 1 4 conchological char- 
acters and PAUP 3.1.1 (Swofford, 1993). The 
characters were unweighted, character states 
were unordered, and every possible tree was 
examined. Data for the analysis were col- 
lected from the following subfamily type spe- 
cies: Cyclina sinensis (Gmelin, 1791) (Cy- 
clininae), dementia vitrea (Dillwyn, 1817)^ 
(Clementiinae), Doslnia concéntrica (Born, 
1778) (Dosiniinae), Tapes literata Linnaeus, 
1758 (Tapetinae), as well as the type species 
of Austrovenus Finlay, 1927 (Chioninae), A. 
stutchburll (Wood, 1828), the type species of 
Cycllnella, С tenuis {Réc\uz 1852), Ruditapes 
philippinarum (Adams & Reeve, 1850), and 
an outgroup east Pacific species, Luclnlsca 
nufte/// (Conrad, 1837) (Lucinidae). All speci- 
mens examined came from the U.S. National 
Museum Mollusca collection, the Academy of 
Natural Sciences at Philadelphia Mollusca 
collection, and the Recent Mollusca collection 
at the University of California Museum of Pa- 
leontology at Berkeley. 

Taxa were chosen to represent those sub- 
families with conchological and biogeograph- 
ical affinities to Cyclininae that indicate the 
highest probability of evolutionary affinity. This 
eliminated from the analysis those subfami- 
lies lacking both of the defining conchological 
characteristics of Cyclininae, subcircular pro- 
files and the absence of lateral teeth. Like Cy- 
clininae, all ingroup taxa except Doslnia con- 
céntrica lack anterior lateral teeth, three 
ingroup taxa have subcircular profiles, and 
three have radial sculpture. Like Cyclina. four 



^Madrea vitrea "СЬеглп." of Dillwyn (1817) is a se- 
nior synonym of Venus papyracea Gray, 1825, 
given by Keen (1969) as the type species of 
dementia. Lamy (1913) asserts Madrea vitrea 
Chemnitz, 1795 (pi. 20: figs. 1959-1960), is a 
species of dementia: Smith (1885) notes that it is 
identical to V. papyracea. Both Kevin Lamprell (per- 
sonal communication) and I agree. 



TABLE 1 . P-values for regressions of each of three 
morphometric variables on height for each taxa. 







Palliai 




Genus 


Ligament 


Sinus 


Profile 


dementia 


0.226 


0.533 


0.279 


Cydinella 


0.871 


0.944 


0.874 


Cydina 


0.246 


0.327 


0.342 


Austrovenus 


0.702 


0.510 


0.177 


Dosinia 


0.855 


0.473 


0.679 


Tapes 


0.197 


0.644 


0.350 


Ruditapes 


0.547 


0.530 


0.116 


Ludna 


0.255 


N/A 


0.880 



taxa are west Pacific species. Doslnia con- 
céntrica is a tropical American species, like 
Cycllnella and Clementia solida Dali. 1902, 
one of the few extant species of that genus. 
Rather than choose the type species of the 
subfamily Chioninae to represent that sub- 
family, I chose Austrovenus because its bio- 
gegraphic affinities (west Pacific) to Cyclina 
(west Pacific, both fossil and Recent) in- 
crease the probability that the two taxa are 
more closely related, evolutionarily, than the 
subfamily type species, a tropical Atlantic 
species. Austrovenus is a good conchological 
representative of Chioninae, possessing all 
the subfamily charactehstics; indeed. Keen 
(1969) classified it as subgenus of the type 
genus, Chione. although anatomical differ- 
ences indicate that it is quite different from 
C/?/one (Jones, 1979). 

Conchological characters included: pres- 
ence of posterior purple pigment (1), pres- 
ence of radial sculpture (2), profile (3), bifidity 
of the 1 , 2a, and 2b cardinal hinge teeth (4-6), 
presence of the escutcheon (7), crenulation of 
the ventral margin (8), presence of anterior 
lateral hinge teeth (9), ligament length (10), 
elevation of the ligament (11), palliai sinus de- 
velopment (12), definition of the lunule (13), 
and presence of radial sculpture on the lunule 
(14) (Fig. 1). Parenthetical numbers refer to 
the characters as they appear on the matrix 
(Table 4). Complete definitions of these char- 
acters and their character states are given in 
Appendix I. 

Three of the above conchological charac- 
ters, 3, 10, and 12, were derived from contin- 
uous data. Data were collected from 10 spec- 
imens of each species, utilizing metric 
calipers. For all three characters, measured 
variables were factored for size by dividing 
each by height. Height was chosen as a mea- 



CYCLININAE 



299 




FIG. 1. A composite illustration of a right venerid 
valve and left hinge, ant, anterior lateral teeth; c, 
marginal crenulations; e. escutcheon; L, ligament; 
In, lunule; n, notch at the end of an elevated nymph; 
PS palliai sinus; 1, a bifid right median cardinal 
tooth; 2a, a bifid left anterior cardinal tooth; 2b, a 
bifid left median cardinal tooth. 



sure of size rather than valve length or width 
of conjoined valves, because valve height 
does not vary as much among venerid sub- 
families (e.g., no elongation as is present in 
mussels), as does length (venerids vary from 
circular to elongate) or width (venerids vary 
from compressed to obese). 

I utilized the software package Statistix 4.0 
to analyse the resulting proportions. To deter- 
mine if the proportions were affected by al- 
lometry (i.e., the proportions changed with 
growth, thus exhibiting significant regression), 
each ratio was regressed against the inde- 
pendent size variable, height. Means of the 
proportions were calculated for each variable 
of each species. The quantitative limits of dif- 
ferent character states were based on a me- 
dian value between the limits of nonparamet- 
rically significant clusters of means. Taxa 
assigned different character states but with 
overlapping ranges of data were tested for 
significant nonparametric differences in fre- 
quency distributions with the Signed Wilcoxon 
Rank Test. 



RESULTS 

Table 1 demonstrates that the three ratios 
representing characters derived from continu- 
ous data are proportions that are not affected 
by growth: no significant regressions resulted. 
Table 2 presents the means and ranges of 
characters 3, 1 0, and 1 2; in all cases variation 
within species is much less than among 
species. Table 3 demonstrates significant 
nonparametric differences for those taxa of 
different character states exhibiting overlap in 
raw data. 

Table 4 presents the character state mathx 
for the cladistic analysis. The PAUP analysis 
results in a consensus tree (Fig. 2) derived 
from five most parsimonious trees (total length 
of 31 for each) out of 10,395 examined trees; 
all five trees had a consistency index (exclud- 
ing uninformative characters) of 0.630. In 
these trees, the most homoplasic character, 
judging from averages derived from the ho- 
moplasy index for every variable over all five 
trees, is elevation of the ligament, followed by 
radial valve sculpture, and definition of the es- 
cutcheon and lunule. Cyc//na clades with Aus- 
trovenus. and Cyclinella with dementia and 
the tapetines in the consensus tree. Among 
the five trees, there is only one instance of Cy- 
clinella forming a clade with a single other 
taxon, dementia, dementia clades with the 
tapetines in 80% of the trees. Figure 3 sum- 
marizes character states common to the 
clades throughout the tree. 



DISCUSSION 

The above results indicate that Cyclininae 
is not a monophyletic subfamily, but a group- 
ing of species with a convergent conchologi- 
cal trait, subcircular profile. Stanley (1970) 
noted that shell form is an important adaptive 
feature of a special, ecologically significant 
parameter, rate of burrowing, although shell 
form is only one factor controlling it. His data 
indicate that although both Dosinia and Cy- 
clinella are compressed subcircular species, 
Dosinia is a relatively fast burrower inhabiting 
cleaner, less stable sediments than the slow 
burrower Cyclinella, which lives in muddy 
sediments. Stanley (1970) also linked shell 
form with mode of burrowing. Specifically, he 
observed that subcircular clams (including 
lucinids, Dosinia and Cyclinella), whether 
slender (as in Dosinia and Cyclinella) or in- 
flated (as in Cyclina), typically burrowed verti- 



300 



HARTE 



TABLE 2. Means and ranges of three morphometric variables for all taxa. 







Ligament 


Pallia 


sinus 




Profile 


Genus 


Mean 


Range 


Mean 


Range 


Mean 


Range 


dementia 


0.38 


0.32-.44 


0.48 


0.39-.59 


1.35 


1.27-1.43 


Cyclinella 


0.54 


0.48- 


64 


0.49 


0.41 -.59 


1.28 


1.18-1.38 


Cyclina 


0.55 


0.49- 


61 


0.39 


0.35-.44 


1.12 


1.05-1.18 


Autrovenus 


0.54 


0.45- 


63 


0.20 


0.16-.26 


1.36 


1.23-1.47 


Dosinia 


0.66 


0.62- 


71 


0.44 


0.41 -.48 


1.27 


1.22-1.31 


Tapes 


0.78 


0.66- 


86 


0.54 


0.43-.60 


1.78 


1.64-1.95 


Ruditapes 


0.72 


0.62- 


80 


0.50 


0.48-.55 


1.57 


1.48-1.62 


Lucina 


0.53 


0.49- 


57 


N/A 




1.07 


1.01-1.10 



TABLE 3. Results of Wilcoxon Signed Rank test for taxa of different chiaracter states with overlapping 
data ranges. 



Test clusters of taxa 



Probability 
Variable X + Ranks v _ Ranks (2-tailed) 



Austrovenus& dementia vs. Cyclinella & Dosinia Profile 198 -12 0.0006 

dementia & Cyclinella vs. Cyclina & Dosinia Palliai Sinus 207 -3 0.0002 

TABLE 4. Data matrix used in the cladistic analysis of this study. 
Lucinisca is the outgroup. Characters 1-14 are fully defined in 
Appendix 1. 















Characters 










Taxa 


1 


2 


3 


4 


5 


6 


7 


8 


9 


10 


11 


12 


13 14 


Dosinia 

















1 








1 






1 


1 


Ruditapes 





1 


1 


1 





1 


1 













2 


1 


Tapes 








1 


1 


1 


1 


1 












2 


1 


Austrovenus 


1 


1 


1 


1 


1 


1 


1 


1 













1 1 


Cyclina 


1 


1 








1 








1 









1 


1 


dementia 








1 











1 














2 





Cyclinella 




















1 












2 


1 


Lucinisca 





1 





2 


2 


2 


1 


1 


2 






3 


1 1 



cally downward without any forward compo- 
nent and "with a pronounced rocking motion 
to saw or slice their way into the sediment." 
Stanley (1970) correlated the angle of rocking 
most strongly with elongation of the shell— the 
more elongate species exhibited smaller an- 
gles of rocking. 

The current analysis indicates that elevation 
of the ligament is also a convergent trait. Data 
indicate that subcircular profile (character 3, 
state 0) is strongly correlated with the form of 
the ligament, which is relatively long and 
sunken (characters 1 and 1 1 , states 1 and 1 ) 
in all four subcircular taxa. No other characters 
within the analysis correlate so completely 
with subcircular profile. One might speculate 
that the sunken ligament increases streamlin- 
ing, whereas the relative length confers adap- 
tive strength to compensate for the greater 
shearing stress generated by greater rocking. 



These results have several taxonomic im- 
plications. That Clementiinae does not clade 
separately from the tapetines in the consen- 
sus indicates the subfamily, as based solely 
on dementia, is not monophyletic. Further 
cladistic analysis that includes the other ex- 
tant clementiinine genus, Compsomax Stew- 
art, 1930, and a larger array of characters is 
needed to test the monophyly of that subfam- 
ily. That Cyclinella clades with dementia and 
the tapetines in the consensus tree indicates 
that a more accurate venerid taxonomy would 
be to reject the subfamilies Cyclininae and 
Clementiinae, and classify both Cyclinella anä 
dementia within Tapetinae, a position previ- 
ously proposed by Deshayes (1853). Only 
once in the five most parsimonious trees does 
Cyclinella clade with a single other taxon, 
dementia, a weak implication that these two 
taxa are slightly more related to each other 



CYCLININAE 



301 



60% 



60% 



60% 



Dosinia 



Riiditapes 
Tapes 
dementia 
Cyclinella 



Austrovenus 
Cyclina 



Lucinisca mittalli 



FIG. 2. A 50% majority rule consensus tree derived from five most parsimonious trees resulting from a PAUP 
3.1.1 analysis of 1 4 conchological cfiaracters for seven venerid genera, utilizing a lucinid species, Lucinisca. 
as an outgroup. 60% = branches supported by three of the five trees. 



than to other tapetines. The consensus tree is 
a clear rejection of the venerid taxonomy of 
Dall (1902), who classified dementia and Cy- 
clinella within the subfamily Dosiniinae. That 
the nominate cyclinine genus, Cyclina. ap- 
pears to be more accurately described as a 
modified chionine expands the conchological 
range of that large subfamily. 

There is no formal analytical attempt here 
to reconcile the placement of the extinct 
genera, Cypr/mer/a Conrad, 1864, Frigichlone 
Fletcher, 1938, and Luciploma Olsson. 1942, 
although the conchological characteristics of 
each genus indicate some strong possibilities. 
The most problematic taxon is Cyprimeria 
Conrad, 1864 (Cretaceous), which is in some 
ways similar to the subfamily Sunettinae. Like 



Sunettinae, the shells are moderately thin, 
compressed, ovate, with fine concentric sculp- 
ture that forms a smooth glossy surface, and 
have sharply escavated escutcheons and 
small umbos (personal observation). Unlike 
Sunettinae, the hinge lacks anterior lateral 
teeth, the inner margins are smooth, and the 
geographic distribution (Americas and Eu- 
rope) does not overlap with the Asian-African 
distribution of Sunettinae. Cypr/'mena might be 
more closely linked with C/emeni/a through its 
smooth inner margins, lack of lunule (Palmer, 
1927), lack of lateral teeth, fine concentric 
sculpture, and moderately thin shells and it ge- 
ographically overlaps with Clementiinae. Un- 
der the changes proposed above, this would 
argue for its placement within Tapetinae. 



302 



HARTE 
Ruditnpes Tapes dementia CycUnella 



Dosinia 



no escutcheon; 
• anterior laterals; 
moderate palliai sinus 



Atistrovenus Cydina Lucinisca mittalli 



■ escutcheon; 

■ no anterior laterals; 

■ large palliai sinuses 



smooth margins; 
no radial hmules; 
no purple pigment 



crenulated margins; 
■ radial lunules; 
purple pigment; 
bifid 2a tooth 



- whole 1 tooth; 

- whole 2a tooth; 
"- bifid 2b tooth; 

- moderate palliai 

sinus; 

- no anterior 

laterals 



FIG. 3. Character states common to the clades of the consensus tree. 



Frigichione resembles chionines in that it 
lacks anterior lateral teeth, and has strong 
concentric sculpture. The type species of 
Frigichione. an Antarctic taxon, was originally 
classified as a Cliione (Fletcher, 1 938), and is 
conchologically similar to extant Tawera Mar- 
wick, 1927, a chionine genus which occurs in 
the Antarctic (Dell, 1964). Both genera are 
characterized by somewhat trigonally ovate 
shells with heavy concentric sculpture, and 
with small to no palliai sinus. When specifi- 
cally compared to Antarctic Tawera. both 
Frigiciiione and the Antarctic Tawera 
piiilomela (Smith, 1885) appear to have no 
palliai sinus. Frigiciiione has fine internal ra- 
dial elements, but it is difficult to discern from 
the plates in Fletcher (1938) (the character is 
not mentioned in text) any marginal crenula- 
tions, a condition that is so fine in T piiilomela 
that it is "only just visible to the naked eye" 
(Smith, 1885). Examples of chionines with 
smooth margins, for example, Cryptonomella 
Kuroda & Habe, 1951, exist. Luciploma, a 
Central American taxon, was probably classi- 
fied within the Cyclininae, because Olsson 
(1942) observed that its "hinge structure 
agrees best with Cyclina and Cyclinellä' on 
the basis of the right valve lacking anterior lat- 
eral teeth and having a strong medial cardinal 
tooth. The same, however, can be observed 
in many American chionine species. More im- 
portant is the lack of a lunule, an apparently 



short ligament, the smooth ventral margins, 
and the moderate to weak concentric sculp- 
ture. All these conchological characters indi- 
cate that Luciploma most closely resembles 
dementia. Unlike dementia, Luciploma ap- 
pears to have a thicker shell, with stronger 
hinge teeth (Olsson, 1942: pi. 3, fig. 2). 



CONCLUSIONS 

Cyclininae is a construct of convergently 
subcircular venerids and should be discarded 
as a subfamily of Veneridae. Cyclinella should 
be reclassified within Clementiinae or Tapeti- 
nae, and Cyclina within Chioninae. Concho- 
logical characters indicate that Frigichione 
can be tentatively classified as a subgenus of 
Tawera (Chioninae), and that Cyprimeha and 
Luciploma can be tentatively classified as 
genera of Clementiinae or Tapetinae pending 
further cladistic analysis. 



ACKNOWLEDGMENTS 

I thank Kelly Zamudio for assisting in the 
execution of the cladistic analysis and the 
University of California at Berkeley Museum 
of Paleontology, the Academy of Natural Sci- 
ences at Philadelphia, and the U.S. National 
Museum for the use of their collections. 



CYCLININAE 



303 



LITERATURE CITED 

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Nostrand Reinhold. New York. 410 pp. 

CHEMNITZ, J. H., 1795, Neues systematisches 
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DALL, W. H., 1902, Synopsis of the family Veneri- 
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DELL, R. K., 1964. Antarctic and subantarctic Mol- 
lusca: Amphineura, Scaphopoda and Bivalvia. 
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DILLWYN, L. W.. 1817. Descriptive catalogue of re- 
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FISCHER-PIETTE, E., 1975, Revision de Veneri- 
nae (Mollusques Lamellibranches). Mémoires du 
Muséum National d'Histoire Naturelle. (A-Zoolo- 
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FISCHER-PIETTE, E. & B. MÉTIVIER, 1971, Revi- 
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FISCHER-PIETTE, E. & D. VUKADINOVIC, 1972, 
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FISCHER-PIETTE, E. & D. VUKADINOVIC, 1975, 
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FISCHER-PIETTE, E. & D. VUKADINOVIC, 1977, 
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d'Histoire Naturelle. (A-Zoologie) (n. s.) 106: 186 
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FLETCHER, H. O., 1938, Marine Tertiary fossils, 
and a description of a recent Mytilus from Ker- 
guellen Island. Reports of British Antarctica. New 
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1931, (Series A)2(6): 103-115. 

FRIZZELL, D. L., 1936, Preliminary reclassification 
of veneracean pelecypods. Bulletin du Musée 
Royal d'Histoire Naturelle de Belgique.5 (34): 84 
PP- 

HABE, T., 1977, Systematics of Mollusca in Japan. 
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no-Hokuryukan). 372 pp., 72 pis. 

HARTE, M. е., 1 992, An eastern Pacific Mercenaha 
and notes on other chionine genera (Bivalvia: 
Veneridae). The Veliger 35: 137-140. 

JONES, C, 1979, Anatomy of Chione cancellata. 
and some other chionines (Bivalvia: Veneridae). 
Malacologie. 19: 157-199. 

JUKES-BROWNE, A. J, 1913, On Callista. Ami- 
antis. and Pitarla. Proceedings of the Malacolog- 
ical Society of London. 1 0: 335-347. 

KEEN, A. M., 1969, Veneracea. pp. 670-690, in: 
Treatise on Invertebrate Paleontology Part N, 
Mollusca 6, Bivalvia, Vol. 2, R. с moore, ed. The 



Geological Society of America and the University 
of Kansas. 

KEEN, A. M., 1971, Sea shells of tropical west 
America. Stanford University Press, California. 
1064 pp. 

LAMY, E, 1913, Notes sur les espèces rangées par 
Lamarck dans son genre Lutraha. Bulletin du 
Muséum National d'Histoire Naturelle Paris. 19: 
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LINDBERG, D., 1990. Transennella Dali vs. Nuth- 
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OLSSON, A. A., 1942, Tertiary and Ouaternary fos- 
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OLSSON, A. A., 1964, Neogene mollusks from 
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SMITH, E. A., 1885, Report on the Lamellibranchi- 
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Revised ms. accepted 1 June 1998 



APPENDIX I 

Definition of Characters and Their States 

All characters are defined by either pres- 
ence/absence or quantitative limits. Morpho- 
metric variables (3, 10, 12) were measured 
from the right valve and divided by valve 
height (H) to compensate for specimen size. 
Character state limits are based on signifi- 
cantly different clusters of means of the taxa 
for each variable derived from a minimum 
sample size of 10. H was measured as de- 
scribed below in 3 (Profile). 

1 . Presence/absence of a dark purple pig- 
ment on the inside posterior area of the 
valves. States: presence = 1, absence = 
0. 

2. Presence/absence of radial sculpture 
on the valves (excluding escutcheon 



304 



HARTE 



and lunule). States: presence = 1, ab- 
sence = 0. 

3. Profile is defined as a measure of the 
length/height (L/H) of the right valve. The 
right valve was placed flat on a 0.5 cen- 
timeter grid, oriented so that the dorsal 
tips of the adductor scars were aligned 
horizontally, accomplished by marking 
these positions on the external margins. 
The profile of the valve was traced onto 
the grid. L is the maximum horizontal, 
length; H is the vertical length from the tip 
of the umbo to the ventral margin. States: 
L/H < = 1 .31 subcircular = 0, L/H > 1 .31 = 
other = 1. 

4. Bifidity of the medial cardinal hinge tooth 
in the right valve ("1"): not present (as in 
the outgroup) = 2. bifid = 1 . not bifid = 0. 

5. Bifidity of the anterior cardinal hinge tooth 
in the left valve ("2a"): not present (as in 
the outgroup) = 2. bifid = 1 , not bifid = 0. 

6. Bifidity of the medial cardinal hinge tooth 
in the left valve ("2b"): not present (as in 
the outgroup) = 2, bifid = 1 , not bifid = 0. 

7. Presence/absence of the escutcheon: the 
escutcheon was defined as present if 
there was any easily discernible inden- 
tated area surrounding the ligament. Pre- 
sent = 1, absent = 0. 

8. Crenulated ventral margin of the valves: 
crenulated = 1 , smooth = 0. 

9. Antehor lateral hinge teeth: present = 1 , 
absent = 0, not applicable (the outgroup) 
= 2. 



10. Ligament length = Ц, /H, where L,, = the 
length of the ligameni, and H is the verti- 
cal length from the tip of the umbo to the 
ventral margin, as further defined in 4, 
above. States: [L, /H < 0.45] = 0, [L, /H > 
0.45] = 1. ^ ^ 

11 . Elevation of the ligament: if the ligament 
was not sunken, a notch was present at 
the posterior end of the nymph, indicating 
a partial elevation of the nymph and 
hence, the ligament. Presence of nymphal 
notch = 0. absence of the notch = 1 . 

1 2. Palliai sinus development: = L/H, where 
L I is the straight line distance from the 
ventral base of the palliai sinus at the pal- 
liai line to the most distal point along the 
ventral edge of the palliai sinus, and H is 
the vertical length from the tip of the umbo 
to the ventral margin, as further defined in 
4, above. [LJH < 0.3] - 0. [LJH > 0.3 
and ^0.46] ¿1,[Lp3/H> 0.46] ^¿,[Lp3,/H 

1 3. Presence/absence of lunule: a lunule was 
defined as present if a clearly incised line, 
an impressed area or a distinct change in 
sculpture within the area, or protruding rib 
defined its outline. Present = 1, absent = 
0. 

14. Presence/absence of radial sculpture on 
lunule: Present = 1 , absent = 0. 



MALACOLOGIA, 1998, 40(1-2): 305-320 

MARINE VALVATOIDEA - COMMENTS ON ANATOMY AND SYSTEMATICS 

WITH DESCRIPTION OF A NEW SPECIES FROM FLORIDA 

(HETEROBRANCHIA: CORNIROSTRIDAE) 

Rüdiger Bieler\ Alexander D. Ball^^, and Paula M. Mikkelsen^ 

ABSTRACT 

The "lower heterobranch" gastropod family Cornirostridae Ponder, 1990 (Valvatoidea), has 
been previously known from only six confirmed extant species in three genera (Cornirostra. No- 
errevangla. Tomura). Knowledge of the soft-body morphology is necessary for placement in this 
family. The unique "multi-tentacled, two-tailed" habitus forms a synapomorphy of this group (an 
appearance produced by a combination of characters of the paired anterior oral lobes, cephalic 
tentacles, curved foot processes, and the deeply split hindfoot). As a result of research on "lower 
heterobranchs" of the Florida Keys, a new species of Cornirostra. С floridana Bieler & 
Mikkelsen, n. sp., is described from the Florida Keys, as the seventh known species in the fam- 
ily, the second known species in the genus, and the first member of Cornirostra from the Atlantic 
Ocean. Detailed anatomical descriptions and interpretations of the foregut and nervous system 
are provided from computer-assisted reconstructions of semi-thin histological sections. Shell and 
anatomical characters of the seven confirmed living cornirostrid species are summarized, 
generic and familial diagnoses are discussed, and a redescription of the family Cornirostridae is 
provided, based on shell and anatomical data. Distinguishing characters of other recognized 
families of Valvatoidea (Valvatidae, Orbitestellidae) are surveyed. The problematic assignment 
of fossils to this anatomically defined gastropod family is also addressed. "^ 

Key words: Florida Keys, Gastropoda, lower Heterobranchia, Cornirostra. Atlantic Ocean, sys- 
tematics, nervous system, histology. 



INTRODUCTION 

A focus in recent gastropod research has 
been on the "lower heterobranchs" (also 
termed Allogastropoda, Heterostropha, etc.), 
a grade or clade of several families that 
shows heterobranch anatomical organization 
in many organ systems, distinguishing them 
from the caenogastropods with which many 
were traditionally grouped. In addition to such 
relatively well-known groups as Pyramidel- 
loidea, Architectonicoidea, and Valvatidae, 
this group includes families of lesser-known, 
small-shelled snails, such as Omalogyridae, 
Rissoellidae, Glacidorbidae. and the enig- 
matic and very recently described Tjaer- 
noidae Waren, 1 991 , Hyalogyrinidae Waren & 
Bouchet, 1992. Xylodisculidae Waren, 1992, 
and Cimidae Waren, 1993. The erection of 
new family-group taxa is partly the result of 



newly discovered species, and partly because 
of critical reassessment of anatomical fea- 
tures, warranting the transfer of taxa from tra- 
ditionally recognized "prosobranch" groups 
into the lower heterobranchs (e.g., Hasz- 
prunar, 1988: Rath, 1988; Ponder, 1991: 
Bieler, 1992: Waren et al,, 1993). 

One such example is Tomura bicaudata 
(Pilsbry & McGinty, 1946), described as a vit- 
rinellid caenogastropod from Missouri Key in 
the Lower Florida Keys. Moore (1964) ques- 
tioned its placement in Vitrinellidae, based on 
the uncharacteristic tentacle morphology il- 
lustrated in the original figures. In a reassess- 
ment of available anatomical data on Vitrinel- 
lidae, Bieler & Mikkelsen (1988) removed T. 
bicaudata from the Vitrinellidae on the basis 
of several head-foot characters, but also 
could not suggest a new taxonomic place- 
ment. While the small, thin, transparent shell 



^Department of Zoology. Field Museum of Natural History, Roosevelt Road at Lake Shore Drive. Chicago, Illinois 60605, 
U.S.A.: bieler@fmnh.org 

^Current address: Zoology Department. The Natural History Museum, Cromwell Road, London, SW7 5BD, United Kingdom: 
a.ball@nhm.ac.uk 

^Department of Invertebrates. American Museum of Natural History, Central Park West at 79'" Street. New York. New York 
10024-5192. U.S.A.: mikkel@amnh.org 

"'This paper is dedicated to the memory of our fnend and colleague Dr. Donald R. Moore (1921-1997). who contributed ex- 
tensively to the knowledge of Florida's micromollusk fauna. 



305 



306 



BIELER, BALL & MIKKELSEN 



of T. bicaudata is very similar in overall ap- 
pearance to many vitrinellid species (particu- 
larly that of Vitrinella helicoidea C. B. Adams, 
1850), its body morphology is uniquely pecu- 
liar. The oral lobes, cephalic tentacles, and 
curved anterior foot processes, along with a 
deeply split hindfoot, make the animal appear 
multi-tentacled and two-tailed. 

Other similar "horned-snout, cleft-tail" 
snails have been recently discovered. Ponder 
(1990b) introduced the generic name Comi- 
rostra for Microdiscula pellucida Laseron. 
1954, from Australia, and placed it and To- 
mura in his new family Cornirostridae among 
the lower heterobranchs. Based on extensive 
anatomical comparisons, he recognized the 
position of this family in the Valvatoidea, a 
group previously thought restricted to fresh- 
water. Ponder (1990b) suspected "Cyclo- 
strema" prestoni Me\v\\\, 1906, from Ceylon, 
and the Mediterranean Skenea pellucida 
Monterosato, 1874, also to belong to Cor- 
nirostridae. The latter species, after more de- 
tailed anatomical study, has since been trans- 
ferred to Hyalogyrinidae (Waren et al.. 1993); 
the former remains of uncertain status. Waren 
et al. (1993) also transferred a Mediterranean 
species, Oxysie/ec/epressa Granata, 1877, to 
Tomura. and introduced a third cornirostrid 
genus, Noerrevangia. for N. fragilis Waren & 
Schander (in Waren et al.), 1993, from the 
Faroe Islands. Most recently, Fukuda & Ya- 
mashita (1997) described the first cornirostrid 
species from the Western Pacific, Tomura 
yashima and T. himeshima. Thus to date the 
family is known from six confirmed extant 
species placed in three genera. 

Ongoing research on "lower hetero- 
branchs" of the Florida Keys has brought to 
light an additional extant species of Corniros- 
tra. which is here described. Histological re- 
construction and functional interpretations 
emphasized foregut and nervous system 
anatomy, particularly those structures that dif- 
fered from, or were not addressed, by Pen- 
der's studies (1990b) of cornirostrid species. 
Shell-morphological and anatomical charac- 
ters are discussed for all known extant 
species, and comments are made on the re- 
ported Cretacous-Jurassic-Thassic fossil 
record (Schröder, 1995; Bändel, 1996). 



MATERIALSAND METHODS 

Specimens were collected in the Florida 
Keys by "rock washing" (i.e., scrubbing the 



surfaces of shallow-subtidal rocks that can be 
lifted out of the water, including the underside 
normally resting on the sediment, with brush 
and saltwater) and by shoveling, hand-dredg- 
ing, and sieving of muddy and sandy shallow- 
water substrata. Specimens were sorted from 
the resulting freshly collected material in the 
field laboratory under a dissecting micro- 
scope. 

Cornirostra floridana n. sp. was observed 
alive only once, sketched, and photographed 
with a single-lens reflex camera equipped 
with extension tubes. For this reason, obser- 
vations of gross morphology remained incom- 
plete. Anatomical descriptions are based 
upon histological sections of the single live- 
collected specimen; initially intended for DNA 
studies, the specimen had not been chemi- 
cally fixed before alcohol preservation, so tis- 



Figure and Table Abbreviations 



agp 


accessory glandular pocket 


bm 


buccal mass 


bpl 


black pigmented layer 


bw 


body wall 


с 


cuticle 


eg 


cerebral ganglion 


CO 


cornea 


ct 


connective tissue 


CS 


cuticular sheath 


e 


eye 


g 


gill 


h 


heart 


jt 


jaw tooth 


le 


lens 


lu 


lumen 


m 


muscle 


mm 


mantle margin 


mpp 


metapodial processes 


orí 


oral lobe 


ot 


oral tube 


PC 


protoconch 


pg 


pedal ganglion 


pig 


pigment 


pig 


pleural ganglion 


PMO 


pigmented mantle organ 


pp 


propodial processes 


pt 


palliai tentacle 


sbg 


subesophageal ganglion 


sg 


salivary gland 


sh 


shell 


sn 


snout nerves 


snt 


snout 


spg 


supraesophageal ganglion 


st 


statocyst 


TC 


teleoconch 


te 


cephalic tentacle 


tn 


tentacle nerves 


V 


void 



CORNIROSTRIDAE ANATOMY AND SYSTEMATICS 



307 



sue preparation was not ideal. Following re- 
hydration from 70% ethanol, the shell was dis- 
solved using saturated aqueous ethylene di- 
amene tetraacetic acid (EDTA). After 
dehydration through an ascending graded 
ethanol series, the specimen was infiltrated 
with LR White resin (Polysciences, Inc.) and 
flat-embedded in fresh resin using an inverted 
ВЕЕМ capsule. Polymerization took 8 h at 
70"C. The specimen was mounted in trans- 
verse orientation and serial-sectioned at 1|.im 
thickness. Sections were stained in aqueous 
toluidine blue, and mounted in Polymount 
(Polysciences, Inc.) under coverslips. The 
sections were drawn at 4 цт intervals using a 
camera lucida and the internal anatomy was 
reconstructed using Jandel Scientific's PC-3D 
software. Where greater resolution was re- 
quired, specimens were reconstructed at 1|.im 
intervals. Individual sections were pho- 
tographed using a photomicroscope with au- 
tomatic camera attachment. Scanning elec- 
tron micrographs (SEM) were produced from 
air-dried shells, coated with gold, observed 
and photographed using an AMRAY 1810 
scanning electron microscope at FMNH. 
Spire angle was measured using a protractor 
against photographs or line drawings of shells 
in lateral view. Numbers of protoconch and 
teleoconch whorls were ascertained using the 
method of Taylor as summarized by Jablonski 
& Lutz (1980: 330, fig. 4). This method counts 
the initial embryonic part of the shell as part of 
a whorl; this explains discrepancies between 
our counts and those of other authors who 
expressly or apparently employed different 
methods of whorl counting. 

Comparative material of Tomura (Figs. 
14-17) was collected in the Upper Florida 
Keys (Sta. FK-021, Lake Surprise, northeast- 
ern end of U. S. Route 1 causeway. Mile 
Marker 107.5, Monroe County, Florida, sedi- 
ment/algae at approximately 1.5 m depth, by 
hand dredge, salinity = 22 ppt. 9 July 1995, 
Bieler/Mikkelsen coll.). Voucher specimens 
are deposited in FMNH 278404 (including 
SEM matehal) and AMNH 289603. Speci- 
mens collected for this study were compared 
to the type specimen of Tomura bicaudata 
(ANSP 182042; Missouri Key, Lower Florida 
Keys, Monroe County, Florida, T L. McGinty!, 
March 1945; 1 .18 mm maximum shell diame- 
ter), to Cornirosta pellucida and other mater- 
ial studied by Ponder (AMS). and to other "vit- 
rinelliform" gastropods collected by Pilsbry & 
McGinty in the Florida Keys (ANSP). Several 
major collections, including AMNH, ANSP. 



DMNH, and FMNH, were searched (unsuc- 
cessfully) for additional specimens of the new 

species. 
Museum acronyms used in text are: 

AMNH American Museum of Natural His- 
tory, New York, U.S.A. 

AMS The Australian Museum, Sydney, 
New South Wales, Australia 

ANSP Academy of Natural Sciences of 
Philadelphia, Pennsylvania, U. S. A. 

DMNH Delaware Museum of Natural His- 
tory, Wilmington, U. S. A. 

FMNH Field Museum of Natural History, 
Chicago, Illinois, U. S. A. 

HMNS Houston Museum of Natural Sci- 
ence, Texas, U. S. A. 

USNM National Museum of Natural History, 
Smithsonian Institution, Washington, 
D.C., U. S.A. 



RESULTS 

Valvatoidea Gray, 1840^ 
Cornirostridae Ponder, 1990b 

Cornirostra Ponder. 1990b; type species by 
original designation; Microdiscula pellucida 
Laseron, 1954. 

Cornirostra floridana Bieler & Mikkelsen, 

new species 

Figs. 1-13 

Type Locality 

Indian Key Fill (formerly known as "Central 
Supply"), Mile Marker 79, Middle Florida 
Keys, bay side (Gulf of Mexico), Monroe 
County, Florida; 24"53'25"N, 8040'28"W. 

Type Material 

Holotype (FMNH 278401; shell with dhed 
tissue remains); paratype 1 (AMNH 289256, 
with dried tissue remains), paratype 2 (USNM 
880276, SEM specimen), and paratype 3 
(FMNH 278402, SEM specimen) collected 
with holotype in shallow subtidal habitat by 
hand-dredge, 26 July 1992 (sta. RB-1582). 
Paratype 4 (FMNH 278405), paratype 5 
(AMNH 289806), and paratype 6 (FMNH 
278403, live-observed specimen, serial-sec- 



Availability and authorship established with ICZN 
Direction 27 (1955): in contrast to recent references 
(e.g.. Riedel. 1993). 



308 



BIELER, BALL & MIKKELSEN 



tioned on microslides) from shoveled silty 
mud, among turtle grass (Thalassia testu- 
dinum Banks ex König) and green algae [Peni- 
cillus of. dumetosus (Lamouroux) Blainville, 
and Halimeda spp.], in shallow water (<1 m) at 
low tide, 1 October 1 994 (sta. FK-001 ). All ma- 
terial from type locality, Bieler/Mikkelsen coll. 

Dimensions: 





Diameter 


Height 


Teleoconch 




(mm) 


(mm) 


whorls 


Holotype 


1.70 


1.60 


2 7/8- 


Paratype 1 


1.28 


0.92 


2 1/10 


Paratype 2 


1.66 


1.58 


2 5/8- 


Paratype 3 


2.10 


1.80 


3- 


(damaged 








after SEM) 








Paratype 4 


1.42 


1.04 


2 3/10 


Paratype 5 


1.20 


0.90 


2+ 


(damaged. 








was larger) 









Etymology 

floridanus. -a, -um: named for the State of 
Florida. 

Description 

Teleoconch (Figs. 1-3): Diameter to about 
2 mm at nearly 3 convex whorls; transparent, 
smooth with fine growth lines, high-spired 
(spire angle 105-110). Base simple, smooth, 
umbilicate, without umbilical keel. Aperture 
round; peristome simple, sharp. Fresh speci- 
mens with thin transparent periostracum, im- 
parting very fine spiral sculpture (visible under 
oblique microscope light). 

Protoconch (Fig. 4): 180-185 ,um (para- 
types 3, 2, respectively), about 1.2 whorls, 
coiling near-planispiral but with initial hyper- 
strophy (tip of apex slightly sunken). Proto- 
conch I (embryonic shell) measuring 133-141 
|im (paratypes 3, 2), with reticulated sculp- 
tural pattern as shown for other cornirostrid 
species (Ponder, 1990b: fig. 5F; Waren et al., 
1993: fig. 3); protoconch II (larval shell, com- 
prising about 1/5 of a whorl) smooth, divided 
into two sectors by a growth mark. 

Head-foot {figs. 5-6): Living animal actively 
and rapidly gliding. Head-foot translucent 
white, with palliai organs and coloration clearly 
visible through shell. Black pigment on snout, 
tentacles, and mantle as depicted in Fig. 5; di- 
gestive gland in visceral coil orange-brown, 
gonad milk-white; buccal mass yellow. Snout 



long, split anteriorly into two curved oral lobes. 
Cephalic tentacles long, slightly tapering with 
blunt tips. Large black eyes situated dorsolat- 
erally at base of tentacles. Mantle margin re- 
flected, overlapping shell edge, without obvi- 
ous black pigment. Palliai tentacle about half 
the length of extended cephalic tentacle, 
slightly more slender, heavily ciliated, blunt- 
tipped, unpigmented, extended laterally and 
curved posteriorly in crawling animal. Large 
knob-shaped process ("anterior glandular 
pocket" of Ponder, 1990b) adjacent to base of 
palliai tentacle. Cephalic penis posterior to 
tentacle base. Foot unpigmented. with curved 
anterior lateral extensions (propodial pro- 
cesses); deeply split posteriorly into two 
sharply tapering metapodial processes (of un- 
equal length), grooved at outer lateral edge, 
separated by U-shaped indentation (Fig. 6). 

Anterior pedal mucus gland in anterior part 
of foot, extending posteriorly to pedal ganglia 
where it appears to fold around pedal com- 
missure. Folded dorsal component passing 
anteriorly and then becoming untraceable in 
the material studied. Posterior pedal gland 
absent. 

Operculum present, but not studied in detail. 

Palliai cavity shallow, occupying less than 
half a body whorl. Gill slender-triangular, 
hanging freely in palliai cavity, crossing dorsal 
midline from left posterior to right anterior, 
bordered with black pigment, tip only barely 
emerging from beneath shell edge near right 
tentacle base and cephalic penis. Pulsating 
heart clearly visible in living animal at rear of 
palliai cavity. 

Alimentary System: Mouth ventrally di- 
rected, slit-shaped, at tip of snout. Paired jaws 
(Figs. 7-8) attached to lateral walls of oral 
tube at approximate mid-point of its length; 
composed of overlapping, finely denticulate 
elements (8-10 elements at widest extent; 
each element about 1 цт in length), covered 
by cuticle near posteroventral limit. Each ele- 
ment lying above a single epithelial cell from 
which it was presumably secreted. Epithelium 
of oral tube peripheral to jaws surrounded by 
muscle layer [probably responsible for jaw ar- 
ticulation and movement]. 

Oral tube lined with low, cuticularized, 
columnar epithelium; cavity l-shaped in cross- 
section anterior to jaws, expanding to inverted 
T-shape posterior to jaws (at level of eyes), 
widening further to form buccal cavity. 

Buccal mass lacking true odontophoral car- 
tilages; radula supported by paired connective 
tissue pads, linked by approximator muscles 



CORNIROSTRIDAE ANATOMY AND SYSTEMATICS 



309 




FIGS. 1-4. Cornirostra floridana n. sp., shell (scanning electron micrographs): (1) apical view, paratype 2; 
(2) basal view, paratype 2; (3) apertural view, paratype 3; (4) protoconch, paratype 3; arrows demarcating 
the two sectors of PC-II. Scale bars; Figs. 1-3 = 1 mm, Fig. 4 = 100 |.im. 



along mid-line. Longitudinal protractor mus- 
cles (dorsolateral to pads) originating in ante- 
rior body wall and passing into lateral walls of 
buccal mass to insert into anterior part of 
odontophore [probably responsible for pro- 
traction of odontophore and of buccal mass]. 
Paired lateral muscle bands binding buccal 
mass to lateral walls of haemocoel, also pen- 
etrating buccal wall, and inserting into mid-lat- 
eral part of odontophore. Wall of buccal cavity 
not cuticularized where muscles pass through 
it. (The relationship of these muscles to the 
buccal mass and to the odontophore suggests 
that these serve as lateral odontophoral pro- 
tractor muscles.) Subradular membrane pro- 
tractors and retracto