SYSTEMATIC STUDIES OF CULTIVATED SPECIES OF Codonanthe (MARTIUS) HANSTEIN AND Nematanthus SCHRADER (GESNERIACEAE)

EY

CLAYTON KAZUO KWOCK HUNG YUEN

A DISSERTATION PRESENTED TO THE GRADUATE COUNCIL

OF THE UNIVERSITY OF FLORIDA IN

PARTIAL FULFILLMENT OF THE REQUIREMENTS

FOR THE DEGREE OF DOCTOR OF PHILOSOPHY

UNIVERSITY OF FLORIDA

1982

ACKNOWLEDGEMENTS

I wish to sincerely thank Dr. Thomas J. Sheehan, Professor, Department of Ornamental Horticulture, for his advice and assistance during the course of this research and manuscript preparation.

Very special thanks are offered to Dr. Bijan Dehgan, Assistant Professor, Department of Ornamental Horticulture, for his technical expertise, suggestions and support during all phases of the research project, for his invaluable criticism of the manuscript, and for his friendship.

I am indebted to Dr. Hans Wiehler, Director of the Gesneriad Research Foundation, Sarasota, Florida, for serving as an adjunct professor to the committee, for supplying the plant material, and for providing guidance during the research project and preparation of the manuscript.

Thanks are also extended to the other members of the committee, Dr. William Louis Stern, Professor, Department of Botany and Dr. Paul M. Lyrene, Associate Professor, Department of Fruit Crops, for their suggestions and criticisms of this research and manuscript preparation.

I would like to acknowledge Dr. Laurence E. Skog, Department of Botany, Smithsonian Institution, for his assistance in my herbarium work, Dr. Margaret H. Stone, Department of Botany, University of Florida, for her enthusiasm and support, and Mr. William R. Saylor for supplying additional plant material.

TABLE OF CONTENTS

PAGE

ACKNOWLEDGEMENTS ii

ABSTRACT v

INTRODUCTION 1

CHAPTER

I. TAXONOMIC REVIEW 3

II. MORPHOLOGICAL DESCRIPTION 8

Growth Habit 8

Root 9

Stem 10

Leaf 11

Inflorescence, 14

Flower 14

Fruit 18

Seed and Seedl ing 19

Pollination , 20

Chromosome Number , 24

Distribution 25

III. COMPARATIVE MORPHOLOGY OF THE LEAF EPIDERMIS 68

Introduction , , , 68

Materials and Methods 68

Observations 69

Discussion, 77

IV. COMPARATIVE ANATOMY OF THE STEM AND LEAF 93

Introduction , , 93

Materials and Methods 93

Observations 94

Discussion, ..,...,. 99

V. POLLEN MORPHOLOGY 109

Introduction 109

Materials and Methods.. 110

Observations 110

Discussion 115

VI. CONCLUSION 1 42

APPENDIX: SYNOPSIS OF INFRAGENERIC TAXA 150

Description of the Genera, Subgenera and Sections. 150

Diagnostic Key to the Genera, Subgenera and Sections 156

Checklist of Known Species 157

LITERATURE CITED 1 6l

BIOGRAPHICAL SKETCH 1 6?

Abstract of Dissertation Presented to the Graduate Council

of the University of Florida in Partial Fulfillment of the

Requirements for the Degree of Doctor of Philosophy

SYSTEMATIC STUDIES OF CULTIVATED SPECIES OF Cod on an the (MARTIUS) HANSTEIN AND Nematanthus SCHRADER (GESNERIACEAE)

By

Clayton Kazuo Kwock Hung Yuen

December 1982

Chairman : Thomas J. Sheehan

Major Department: Horticultural Science

Cod on an the (Martius) Hanstein and Nematanthus Schrader

(Gesneriaceae) are morphologically distinct genera of the evergreen and deciduous rain forests of Central and South America. Two subgenera and two sections had been recognized to accommodate the fourteen cultivated species of Cod on an the, whereas no subgeneric ranks were previously reported for the ten cultivated species of Nematanthus. Hybridizations between Codonanthe and Nematanthus have produced progeny that display a high degree of fertility, indicating that the species of Codonanthe and Nematanthus are closely related. The present study examined the species of Codonanthe and Nematanthus and attempted to resolve the relationship of species between genera and within each genus. Conventional taxonomic methods and systematic techniques of light and electron microscopy, microtomy, leaf clearings and karyology were utilized in the study of live plant material.

Flowers of Codonanthe species have obliquely funnel form- ventricose corollas that are primarily white and are presumably pollinated by

Euglossine bees, whereas species of Nematanthus have pouched corollas that are basically orange, red, pink or yellow and are presumably pollinated by hummingbirds. Possession of such differing corolla types and pollinators reproductively isolate these two genera, possibly indicating that Codonanthe and Nematanthus should remain as distinct taxa.

Species of subgenus Codonanthe section Codonanthe have orange berries, a diploid chromosome number of n=8, and a unilacunar nodal anatomy (except C. carnosa and C. gracilis), lack extrafloral nectaries, and are indigenous to southeastern Brazil. Species of subgenus Codonanthe section Spathuliformae and subgenus Codonanthella have red, pink or purple berries or yellow-green fleshy capsules, a tetraploid chromosome number of n=l6, and a trilacunar, split-lateral nodal anatomy, possess extrafloral nestaries, and are geographically widespread from southern Mexico through Central America to northern South America. Nematanthus crass if olius, N. fissus, N. fritschii, N. hirtellus, N. maculatus and N. perianthomegus have a shrubby growth habit, trilacunar, spilt-lateral nodal anatomy, and resupinate flowers, whereas N. gregarius, N. nervosus, N. strigillosus and N. wettsteinii have a viny growth habit, unilacunar nodal anatomy, and nonresupinate flowers.

On the basis of these observations, sections Nematanthus and Far vif olius are established to accommodate the species of Nematanthus , and it is acknowledged that further studies are required before any conclusions are made on the relationships of the infrageneric taxa of Codonanthe. A synopsis of the infrageneric taxa and revised

classification of the genera Codonanthe and Nematanthus is presented.

INTRODUCTION

Gesneriads have been in the horticultural trade for many years and are becoming very popular with the current indoor plant revolution. Potted plants of the Florist Gloxinia (Sinningia speciosa), African Violet (Saintpaulia spp. ) and Gape Primrose (Streptocarpus spp.) are grown in the home, often in light gardens, and in the greenhouse. Nurserymen have recognized that epiphytic and terrestrial gesneriads are ideal candidates for hanging baskets. Species of Aeschynanthus (Lipstick Plant), Codonanthe, Columnea, Episcia (Flame Violet) and Nematanthus (Goldfish Plant) are widely cultivated in hanging baskets for their colorful flowers and foliage (Elbert & Elbert, 1976).

Plantsmen have hybridized many species of Gesneriaceae in an attempt to produce new cultivars. Interspecific crosses have generally yielded fertile progeny, whereas intergeneric combinations have always resulted in offspring of very low fertility to sterility (Wiehler, 1979b). An intergeneric hybrid between Codonanthe and Nematanthus was created in 1977 and designated X Codonatanthus (Saylor, 1978a). This was the first intergeneric combination that displayed a high degree of fertility, indicating that species of Codonanthe and Nematanthus may be more closely related than realized.

A doctoral program was initiated in 1979 to l) examine species of Codonanthe and Nematanthus in cultivation, 2) determine the relationship of species between genera and within each genus, and 3) provide a

synopsis of the infrageneric taxa of Codonanthe and Nematanthus. Conventional taxonomic observations were made of the cultivated species of the two genera to serve as the basis of this thesis.

Systematic methods were employed in an attempt to discover additional characters of taxonomic utility. Light and electron microscopy, microtomy, leaf clearing, chromosome techniques and hybridizations were applied to the study of live plant material. These tools of taxonomy were used to examine the morphology of the leaf epidermis and pollen, and anatomy of the stem and leaf. It is the additive nature of taxonomy that incorporates information from many differing sources to strengthen any final decision of a possible new classification.

CHAPTER I TAXONOMIC REVIEW

Gesneriaceae Dumortier consists of three

subfamilies — Gesnerioideae, Coronantheroideae Wiehler and

Cyrtandroideae Endlicher (Wiehler, 1979b). Gesnerioideae includes 5 tribes, 54 genera and over 1300 species distributed throughout the Neotropics. Coronantheroideae includes 1 tribe, 9 genera and about 20 species in southern Chile, the South Pacific islands and Australia. Cyrtandroideae is composed of 4 tribes, 63 genera and over 1550 species mainly in the Paleotropics. Besides differing distributions, the

subfamilies are distinguished by seedling morphology (e.g., anisocotyledonous seedlings in Cyrtandroideae and isocotyledonous seedlings in Gesnerioideae and Coronantheroideae).

Five tribes that form Gesnerioideae are Gesnerieae, Napeantheae Wiehler, Beslerieae Bartling & Wendland, Gloxinieae Fritsch and Episcieae Endlicher. Gesnerieae and Napeantheae are monogeneric, while Beslerieae is composed of seven genera. Gloxinieae and Episcieae are the larger tribes of this subfamily, and comprised 24 and 21 genera, respectively. Chromosome number serves as a distinguishing character in these tribes — i.e., Episcieae, n = 8, 9; Gloxinieae, n = 10, 11, 12, 13; Gesnerieae, n = 14; Beslerieae, n = 16; Napeantheae, unknown (Wiehler, 1979b).

Episcieae is the largest tribe of Gesnerioideae, with over 630 species in 21 genera. Wiehler ( 1979b) discusses three features of

3

evolutionary significance intrinsic to Episcieae: a) an unusual trilacunar nodal anatomy with split lateral bundles, b) a predominance of epiphytic species, and c) ornithophily and euglossophily as the primary mode of pollination. Also, there are usually two enlarged, connate glands at the base of the ovary serving as a nectary in the hummingbird-pollinated and euglossine bee-pollinated flowers. The fruit is a berry or a fleshy capsule. Although the majority of genera in Episcieae have a chromosome number of n = 9, Godonanthe and Nematanthus are unique in possessing a chromosome number of n = 8.

A chronologically arranged taxonomic history of Codonanthe and Nematanthus is presented in Table 1-1. A current classification system of these two genera according to Wiehler (l979b, 1982, & personal communication) is shown in Table 1-2, with the known cultivated species tabulated.

Table 1-1 . Taxonomic history of the genera Codonanthe and Nema tan thus.

DATE

TAXA

EVENT

1821 Nematanthus Schrader

1829 Hypocyrta Martius & Hypocyrta section Codonanthe Martius

I854 Codonanthe (Martius) Hanstein

1855 Coccanthera C. Koch & Hanstein

193^

Codonanthopsis Mansfeld

The genus Nematanthus is first established in Gottingische gelehrte Anzeigen 1821 (2): 718.

The genus Hypocyrta is first established with the section Codonanthe, in Nova Genera et Species Plantarum 3: 49.

Hypocyrta section Codonanthe is elevated to the genus level with Codonanthe as the conserved name, in Linnaea 26: 209.

A new genus established with its

lectotype relegated to the synonymy of Codonanthe, in Index Seminum in Horto Regio Botanico Berolinensi 1855' Appendix 17.

The genus Codonanthopsis is first

established, in Repertorium Specierum Novarum Regni Vegetabilis 36: 120.

1971 X Hypotanthus Saylor

New intergeneric taxon was created due to the cross of Hypocyrta and Nematanthus , in Gloxinian 21 : 20-21, 31.

1973 Codonanthe section Codonanthopsis (Mansfeld) H. E. Moore

The genus Codonanthopsis is lowered to til e sectional level of the genus Codonanthe, in Baileya 19: 4-23.

1973 Nematanthus Schrader

1978

X Codonatanthus Saylor

Moore combines many species of the genera Nematanthus and Hypocyrta into one genus, in Baileya 19: 35-^1.

New intergeneric taxon was created due to the cross of Codonanthe and Nematanthus, in CrossWords 2: 11-12, Selbyana 5: l-3«

Table 1-1 - continued.

HATE

1979

1979

1982

TAXA

EVENT

Cod on an the (Martius) Wiehler regards Codonanthopsis as a

Hans te in & valid genus, in Wiehler, Ph. D.

Codonanthopsis dissertation.

Mansfeld

Cod on an the subgenus Codonanthella Wiehler

Cod on an the subgenus Cod on an the section Spathuliformae L. B. Smith

New subgenus of Cod on an the established based upon species having fleshy- capsules, in Wiehler, Ph. D. dissertation.

New section of Codonanthe recognized based upon species having purple, red or pink berries, in Selbyana 6(in press) and personal communication with Wiehler.

Table 1-2. Current classification system of the cultivated species in the Nematanthus according to Wiehler (1979b, 1982 and personal communication).

GENUS Codonanthe (Martius) Hanstein SUBGENUS Codonanthe

Accession Number

SECTION Codonanthe

1. C. carnosa (Gardner) Hanstein W-2199

2. C_. devosiana Lemaire W-2215

3. C. digna Wiehler W-1139 k. C. gracilis (Martius) Hanstein W-2203

5. C. paula Wiehler W-2386

SECTION Spathuliformae L. B. Smith

6. C. calcarata (F.A.W. Miquel) Hanstein W-2116

7. C. corniculata Wiehler G-932

8. C. crass if olia (Focke) Morton W-2531

9. C. uleana Fritsch W-1182

SUBGENUS Codonanthella Wiehler

10. C. caribaea Urban G-976

11. C. chiricana Wiehler W-2267

12. C. elegans Wiehler W-2588

13. C. luteola Wiehler W-I63O

14. C. macradenia Donnell-Smith W-2552

GENUS Nematanthus Schrader

1. N. crass if ol ius (Schott) Wiehler G-13^

2. N. fissus (Vellozo) L. Skog G-661

3. N. fritschii Hoehne G-611 k. N. gregarius D. Denham G-597

5. N. hirtellus (Schott) Wiehler G-1092

6. N. maculatus (Fritsch) Wiehler W-2^9^

7. N. nervosus (Fritsch) H. E. Moore G-73^

8. N. perian-ttiomegus (Vellozo) H. E. Moore W-17l8,W-2227

9. N. strigillosus (Martius) H. E. Moore W-388 10. N. wettsteinii (Fritsch) H. E. Moore G-655

CHAPTER II MORPHOLOGICAL DESCRIPTION

Descriptions of the cultivated species of Cod on an the and Nema tan thus species are "based on the literature and personal observations of live plant material cultivated in a growth room at the Department of Ornamental Horticulture, University of Florida. The growth room provided uniform conditions of 22-2 5°C day temperature, 17-20° C night temperature, ifOOO-6000 Lux fluorescent lighting and a fourteen hour daylength. Descriptive terminology is "based on Radford et al. (197*0 « Morphological characters of Codonanthe and Nematanthus are tabulated in Table II-l for ease of comparison, with the species grouped into infrageneric categories based upon Wiehler (l979b, 1982 & personal communication).

Growth Habit Species of Codonanthe and Nematanthus are phanerophytes (Raunkiaer, 193*0. They are perennials that are one-to-many feet tall, have their vegetative buds fully exposed to surrounding air, and are epiphytes. As epiphytes, these species are attached to and depend upon another plant for physical support, Codonanthe and Nematanthus are among thirteen epiphytic genera in the tribe Episcieae (comprise only 21 genera) and 28 epiphytic genera of Gesneriaceae ( Wiehler, 1979b).

Codonanthe (Figures II-l to II-3) and. Nematanthus (Figures II-4 to II-5) species have a vine-like and/or shrub-like growth habit. Vine-like species (e.g. , C, carnosa, _C. gracilis, N. strigillosus, N. wettsteinii) possess stems that initially grow in an upright direction with little branching. With continued growth and elongation, the stem acquires a reclining, clambering or decumbent habit due to the inability of the stem to support itself. Other species have a pendulous mode of growth (e.g., C. elegans, C. luteola, C. macradenia) or grow in an erect, shrub-like fashion (e.g., C. uleana, N. crass if ol ius, N. maculatus , N. perianthomegus). Table II-l presents a list of the cultivated species of Codonanthe and Nematanthus and their growth habit types.

Root Species of Codonanthe and Nematanthus have fine, thread-like fibrous roots that arise adventitiously from the stem. Some species possess pre-formed roots (e.g., C. elegans) or root initials (e.g., N. hirtellus) at the nodes. Adventitious root development corresponds well with the epiphytic habit of the plants. Epiphytes are better sustained on a host if they are anchored to the substrate at numerous locations, that is, attached by many roots. Also, a repent, spreading habit promotes the proliferation of the original plant in such a way that if a stem is severed, one or more individuals are formed. New plants have excellent chances of survival since they already possess well-developed roots.

10

In the ant-gardens of Codonanthe crass if olia, a mutual istic association is maintained with an arboreal, carton-building ant. Kleinfeldt (1978) proposes that the epiphyte's roots add structural support to the ant nests. Seeds of C. crass if olia are often carried by- ants and placed in their nests (mode of seed dispersal). The seeds soon germinate in the nutrient-rich detritus and permeate their roots throughout the carton walls lending support to the framework of the ant-gardens .

Stem

Codonanthe and Nematanthus species have herbaceous stems that are suffrutescent. The stem epidermis is initially green with a smooth texture in many species, with exceptions occurring in N. fissus (tomentose indumentum) and N. strigillosus (strigose vestiture). The transition from the herbaceous condition results in a woody stem with greyish-tan to brown coloration. The texture may be smooth (e.g., G. gracilis) to rough with a fissured appearance (e.g., N. perianthomegus) .

Extrafloral nectaries are present at the nodes of some Codonanthe species (e.g., C. crassifolia) . These species are usually associated with ant-gardens and possess nectaries which attract ants — the agents of seed dispersal (Moore, 1973a; Kleinfeldt, 1978).

Table II-l categorizes species of Codonanthe and Nematanthus into two groups based upon stem size: a) 2-4 mm or b) 5-9 mm stem diameter. This measurement is basically correlated to the growth habit of the taxon. Vine-like plants have stems 2-4 mm in diameter, whereas a 5-9 mm stem denotes a shrubby form. Most Codonanthe species have the small

11

stem size. Nematanthus gregarius, N. nervosus, N, strigillosus and N, wettsteinii form a distinct group of species with 2-4 mm stems and a viny habit, while the other six Nematanthus species exhibit a shrubby form with 5-9 mm stems.

Anatomical aspects of the stem are addressed in CHAPTER IV: COMPARATIVE ANATOMY OF THE STEM AND LEAF.

Leaf Leaf characters are summarized in Table II-l and descriptions follow Hickey's (1973) treatment with respect to architecture. Anatomical features of the leaf are given in CHAPTER IV: COMPARATIVE ANATOMY OF THE STEM AND LEAF.

Arrangement

Most species of Codonanthe and Nematanthus have isophyllous leaves in an opposite arrangement. Leaves are basically decussate but a few of the vine-like species have leaf blades oriented in a distichous -like manner, that is, appearing 2-ranked with the leaves facing one direction. For example, N. fissus, N. maculatus and N. perianthomegus have leaf blades in a 4-ranked arrangement, whereas C. carnosa, C. digna and C. grac il is have leaf blades in a 2-ranked placement.

Petiole

Most species of Codonanthe have rounded, green petioles (except C. corniculata with reddish petioles). Nematanthus species are more variable in possessing petioles that are slightly furrowed on the

12

adaxial surface (e.g., N. crassifolius) and/ or with a red coloration (e.g., N. fissus and N. hirtellus) .

Petiole size may be classified into two length categories: a) 4-10 mm and b) 10-50 mm. Godonanthe species all possess 4-10 mm long petioles (Figures II-6 to II-8). Nema tan thus gregarius, N. nervosus, N. strigillosus and N. wettsteinii also have 4-10 mm petioles (Figure 11-10), but the other six Nematanthus species exhibit petioles 10-50 mm long (Figure II-9).

Blade

Symmetry and Form. Godonanthe and Nematanthus are represented by species that have leaf blades with a symmetrical or asymmetrical lamina and/ or base (Figures II-6 to 11-10 ). Variations in leaf base balance include a) symmetrical lamina and base (e.g., C. caribaea) , b) symmetrical lamina but an asymmetrical base (e.g., N. maculatus ) , c) asymmetrical lamina but a symmetrical base (e.g., N. crassifolius) , and d) asymmetrical lamina and base (e.g., C_. uleana) .

Leaves in Codonanthe and Nematanthus are ovate (e.g., N. nervosus), elliptic (e.g., N. fritschii) and obovate (e.g., N. maculatus ) . Each leaf form is variously modified as narrow, normal or wide (Hickey, 1973) • For example, C. crass if olia, C. car ibaea and G. macradenia have elliptical leaves with a narrow, normal and wide form, respectively. Also, Codonanthe and Nematanthus have leaf length

categories defined as a) 2-4 cm and b) 4-12 cm. Species of Godonanthe subgenus Godonanthe section Godonanthe have ovate to elliptic leaves and leaves 2-4 cm long (except C. gracilis) , whereas species of subgenus Codonanthe section Spathuliformae and subgenus Godonanthella have leaves

13

with an elliptic to obovate form and 4-12 cm long (except C. chiricana). Nema tan thus gregarius, N. nervosus, N. strigillosus and N. wettsteinii have leaves 2-4 cm long, whereas the other six Nema tan thus species have

4-12 cm long leaves.

Apex and Base. Codonanthe and Nema tan thus species have several leaf apex and base shapes. Leaf apex shapes include acute (e.g., N. strigillosus) , acuminate (e.g., C. uleana) , attenuate (e.g., N. nervosus) and obtuse (e.g., C_. digna). Leaf base shapes include acute (e.g., N. gregarius) , obtuse (e.g., N. hirtellus) , rounded (e.g., C. paula) and cordate (e.g., C. gracilis).

Margin. Three types of leaf margins are evident in Codonanthe and Nematanthus. Most species have entire margins such as C. caribaea and N. wettsteinii. There are also species with slightly crenate margins (e.g., C. chiricana and N. perianthomegus) and fully crenate margins (e.g., £. calcarata and N. f issus).

Texture. Codonanthe and Nematanthus species exhibit generally three forms of leaf texture — smooth (e.g., N. gregarius) , puberulous (e.g., N. hirtellus) and pubescent (e.g., N. f issus) . Species of subgenus Codonanthe section Spathuliformae and subgenus Codonanthella display smooth leaf surfaces and species of subgenus Codonanthe section Codonanthe (except C_. gracilis) possess puberulous to pubescent leaves.

Leaf epidermis characters are discussed in CHAPTER III: COMPARATIVE MORPHOLOGY OF THE LEAF EPIDERMIS, and include such morphological

aspects of leaf surface features as glandular and nonglandular trichomes, stomata, extrafloral nectaries and surface ornamentations.

Coloration. Species of Codonanthe and Nematanthus have leaves that are generally green adaxially with a lighter green on the abaxial

14

surface (e.g., C. devosiana and N. gregarius). Various other markings or colorations are present and represented by C. gracilis (red pigmentation at the leaf margins), C. elegans and N. fritschii (red coloration at or around the midvein and/ or secondary veins), N. wettsteinii (red lamina only, with no colored veins), and C. carnosa and C_. paula (red coloration on total abaxial leaf surface).

Stipules

The leaves of Godonanthe and Nema tan thus species are estipulate.

Inflorescence The pair-flowered cyme is the basic inflorescence unit in Gesnerioideae and is typical for the Gesneriaceae (Wiehler, 1979b). Godonanthe and Nema tan thus species possess a reduced cyme of one to several flowers (appearing one at a time) in the upper leaf axils. The inflorescence consists of short pedicels (except very long in N. crass if ol ius and N. fritschii). Bracts are lacking (Moore, 1973a.; Wiehler, 1977, 1979a; Skog, 1978).

Flower Orientation and Pedicel

The orientation of the flower is an important taxonomic trait in delimiting Nema tan thus species (Moore, 1973^). Flowers of N. gregarius, N. nervosus , N. strigillosus (Figures II-11E & II-11F) and N. wettsteinii are consistently nonresupinate so that the pouch of the corolla is in a normal, ventral (abaxial) position. The other six

15

species of Nematanthus (Figures II-11A to II-11D) display their flowers with the corolla pouch in a dorsal (adaxial), resupinate position. This resupinate flower orientation is the result of a 180° twisting of the pedicel from the ventral position.

Of the six Nematanthus species with resupinate flowers, N. crass if ol ius and N. fritschii have pedicels that are 25-200 mm long and flowers that are pendulous. Nematanthus fissus, N. hirtellus, N, maculatus , N. perianthomegus , N. gregarius, N. nervosus, N. strigillosus and N. wettsteinii exhibit flowers that are erect in the leaf axil with pedicels 3-25 i™ long.

Species of Codonanthe (Figures II-12A & II-12B) have pedicels 3-25 mm long and nonresupinate flowers that are erect in the leaf axil.

Calyx

The calyx of Codonanthe and Nematanthus species is deeply 5-parted with basally connate sepals and five unequal lobes. The dorsal lobe is often recurved about the corolla spur with the ventral and lateral lobes frequently connate towards the base presenting a bilabiate shape (Figure II-12C). Codonanthe species have calyx lobes that are linear to lanceolate, whereas species of Nematanthus possess linear to lanceolate and ovate to elliptic calyx lobes. The lobes are variously entire to shallow toothed, veined, glabrous to pubescent, and green to purple, red and orange. Some species of Codonanthe (e.g., C_. macradenia and C_. crass if olia) possess prominent red extrafloral nectaries (Figure II-14C) in the sinuses of the calyx lobe margins (Moore, 1973a, 1973b).

16

Corolla

Codonanthe species (Figures II-12A & II-12B) possess an obliquely funnel form- ven trie os e corolla with a base that is narrow and either rounded (e.g., G. digna) or prominently spurred (e.g., C. chiricana). The corolla tube gradually (e.g., C. crass if olia) or abruptly (e.g., C. paula) broadens towards the throat or is somewhat dorsiventrally compressed, arched and grooved (e.g., C. macradenia, Figures II-12E & II-12F). The three lower lobes are spreading and larger than the upper two lobes providing a bilabiate corolla configuration. The corolla is situated obliquely within the calyx and in a horizontal position. It is basically white or yellow (e.g., C. luteola) , often with spots or lines on the outer areas or on the lower surface of the throat that are yellow, brown, pink, red, lilac or deep purple. The corolla is glabrous to pubescent (Moore, 1973a) •

Nematanthus species (Figures II-11A, II-11C & II-11E) have a mildly to strongly ventricose corolla that is narrow above the base and often with a short spur. The corolla tube gradually expands to a broad, laterally compressed throat (e.g., N. fritschii) , or quickly widens to form a pouch that abruptly narrows to form a constricted throat (e.g., N. nervosus) , with five small rounded lobes. The latter corolla configuration has been named by Wiehler ( 1979b) as a Hypocyrta-type or hypocyrtoid corolla. The corolla tube is erect or slightly oblique within the calyx. The corolla is scarlet, red, pink, orange or yellow with maroon stripes, and glabrous to pubescent in texture (Moore, 1971. 1973a).

17

Androecium

The four stamens in Cod on an the and Nematanthus species (Figures II-12D & II-11E9 are didynamous, epipetalous and coherent, with the anthers in a rectangular configuration. Species of Godonanthe are unique in possessing anther locules separated spatially by a broad connective and dehiscing by a pore near the apex of the thecae. Species of Nematanthus have anthers that are more typical of genera of the Gesnerioideae. They display narrow, elliptical anther connectives and dehisce by a conventional longitudinal slit in the thecae (Wiehler, 1979b).

Gynoecium

Godonanthe and Nematanthus species (Figure II-l^A) have a superior, unilocular ovary that is composed of two united carpels (paracarpum, cf . , Ivanina, 1965). The parietal placenta is usually divided into two and intrudes into the locule from the basal wall of the fruit. In Codonanthe, the placenta forms two tuberculate projections. Ovules are numerous and anatropous. The style (Figure II-14A) is terete and slender, with a bilobed stigma (Figure II-13). The nectary (Figure II-1^A) consists of two large, connate glands positioned adjacent (connivent) and dorsal to the ovary. Nectar collects within the corolla at the base of the superior ovary (Lawrence, 1951 ! Ivanina, 1965; Wiehler, 1979b).

Pollen

The morphology of Codonanthe and Nematanthus pollen is discussed in CHAPTER V: POLLEN MORPHOLOGY.

18

Fruit

Fruit type serves as a valuable taxonomic feature in the infrageneric classification of Codonanthe. Wiehler ( 1979b) delineates two subgenera for Codonanthe based upon the type of fruit: a) subgenus Codonanthe has berries (Figure II-14D) and b) subgenus Codonanthella has fleshy capsules (Figure II-l^-E). The berries are globose to subglobose with pulp consisting of funicular tissue. The fleshy capsules are laterally compressed and pointed to cone-shaped, bivalved and loculicidally dehiscent, and have carpel walls that are concave with reflexed tips. Dehisced capsules split open and display a cone-shaped mass of funicular tissue, seeds and placentae. Subgenus Codonanthe is further subdivided by Wiehler (1982 & personal communication) into sections based upon fruit color: a) section Codonanthe has orange berries and b) section Spathul if ormae has pink, red or purple berries.

Nematanthus species possess fleshy capsules that are similar to the

fruits of species of Codonanthe subgenus Codonanthella. Wiehler ( 1979b)

designates this fruit type a "display fruit" and defines it as

a fleshy bivalved capsule with loculicidal dehiscence whose valves separate at maturity from the placentae which form together with the mass of seeds and the enlarged, glistening funiculi an attractively colored cone-shaped structure or food body positioned upright on the receptacle. The two reflexed or convex carpel valves are usually strikingly colored on the inside (red, pink, yellow, or white) to further offset the food body. This display is surrounded by contrastingly colored calyx lobes which have grown in size since anthesis. This type of display fruit offers an outstanding visual target for the seed dispersal agents which are birds, fruit-eating bats, and possibly monkeys, (p. 69-70)

In summary, the fruit type, color and ability to dehisce appear to

dictate the mode of fruit/seed dispersal. For Codonanthe subgenus

Codonanthe species, orange berries of section Codonanthe and pink, red

19

and purple berries of section Spathul if ormae probably attract and are disseminated by birds. Fleshy capsules of subgenus Godonanthella species have the potential to attract birds and ants as the agent of fruit and seed distribution. The "display fruit" of Nematanthus species, as previously reported, are most likely dispersed by birds or fruit-eating bats.

Seed and Seedling Seeds of Codonanthe and Nematanthus species (Figures 11-15 to 11-17) are comparatively large in Gesneriaceae, with such species as C. calcarata, C. crass if olia, C, macradenia and C. uleana having the largest gesneriad seeds (Wiehler, 1979b). Seeds range from 1-2 mm long, occasionally becoming 3«5-3«9 mm long, and are oblong-elliptic in outline (ivanina, I965). The seeds are brown, red, pink or yellow and longitudinally or obliquely striated (Moore, 1971, 1973a;

Beaufort-Murphy, 1977). Wiehler has estimated that for gesneriaceous fruit, Codonanthe species probably contain the lowest number of seeds with between 15 to 125 seeds per berry (35 as an avesage).

Codonanthe (and probably Nematanthus) seeds are attached to the placenta via a glistening, hyaline funiculus that is 8-11 mm long and fleshy (Wiehler, 1979b). A translucent or opaque aril partially (e.g., N. gregarius) or entirely (e.g., C. crassifolia) surrounds the seeds (Moore, 1973a; Beaufort-Murphy, 1977).

Kleinfeldt (1978) and Madison (1979) have reported on the mutualistic association of a myrmecophyte (C. crassifolia and C_. calcarata) and an ant species (Crematogaster longispina). It appears that ants are the agents of seed dispersal for C. crassifolia, carrying

20

seeds to their carton nests. Wiehler ( 1979b) observed that the seeds are shaped like ant eggs, perhaps an example of mimicry to aid in seed dispersal. Ants eat the seed's fleshy aril, as well as the fruit pulp, and place the seeds in the wall of the nest. The seeds germinate and C. crass if olia plants grow, and their roots provide the nest with structural support.

Pollination

Flowers of Codonanthe and Nema tan thus species are protandrous (Moore, 1973a; personal observations), that is, anthers mature and shed their pollen before stigmas mature and become receptive. This outbreeding device essentially separates gametes of a flower in time and to some degree hinders self-fertilization (Allard, I960). A species population will usually have many individuals flowering with flowers at various stages of an thesis.

Anthesis commences with extention and elongation of the filaments so that the anthers are positioned near the orifice of the corolla tube. In a nonresupinate flower, connate or connivent anthers are dorsally located above the corolla throat with the anther pores or slits shedding pollen downward and inward. Pollen will be deposited on top of the pollinating agents attracted to the flower. On the second or third day, the filaments will coil up and retract the anthers into the flower, removing the source of pollen. The elongating style will bring the stigma into the former position of the anthers (i.e., above the corolla throat). The stigma becomes receptive after retraction of the anthers, removing the opportunity for self-pollination. Pollen

21

deposited on the dorsal surface of a pollinating agent will be picked up by the stigma, thus, completing the pollination cycle ( Jones & Rich, 1972; Wiehler, 1979b).

In a resupinate flower, the sequence of pollination is similar to that of a nonresupinate flower except the flower is inverted by 180°. The anthers and stigma are in a ventral position facing upward, with pollen shedding and reception occurring on the lower surface of the pollinating agent. It appears that the pollination sequence is successful only among nonresupinate and resupinate flowering species, but not between the two flowering types.

In the pollination of a flower, a complex of characteristics is exhibited by the flower as a direct result of being adapted to the form and behavior of the pollinator. Pollination syndromes demonstrate the conformity between the flowers and the animals which pollinate them (van der Pijl & Dodson, 1969).

Wiehler ( 1979b) has estimated that 30% of the Neotropical gesneriads are pollinated by irridescent male and female Euglossine bees (gynandro-euglossophily) , 60% pollinated by hummingbirds

(ornithophily) , and 10% by other biotic agents. Because there is such a high occurrence of bee- and bird-pollinated flowers among gesneriads, the syndromes of gynandro-euglossophily and ornithophily were examined. Flower characters are directly compared with the traits of the pollinator.

Codonanthe species have 5-merous flowers that are zygomorphic and held horizontally in the leaf axil. Ihe three corolla lobes are often enlarged (a possible landing platform), white or yellow in color, sometimes flushed with yellow, and pink, lilac or deep purple on the

22

lower surface of the throat (potential nectar guides). Nectar is contained within a relatively short corolla and/or short spur (nectar accessible to pollinators with short mouthparts) and an thesis is diurnal (feeding activity diurnal). These characters appear to fulfill the syndrome of gynandro-euglossophily flowers.

The white, funnel-form corolla of Codonanthe species is very similar to some corollas of Achimenes, Alsobia, Drymonia, Nautilocalyx and Sinningia species. Wiehler (1979b) states that these genera are pollinated by various kinds of female Euglossine bees. Species of Codonanthe were observed to be visited by Euglossine bees (Williams, personal communication).

Nematanthus species possess flowers that are tubular or pouched and held horizontally in or hanging from the leaf axil (pollinator must be able to hover in front of flower while feeding). Perianth lobes are curved back or absent (do not interfere with flight movements of the pollinator), and are scarlet, red, pink, orange or yellow with maroon stripes (visual sense of the pollinator must be strong). The flower wall is hard, the filaments are stiff and the corolla tube is broad (protection from pollinators' hard mouthparts). Nectar is abundant and stowed away (pollinator must possess long mouthparts to reach the

hidden nectar), and the nectar guides and odor are absent (poor sense

of smell). An thesis is diurnal (feeding activity diurnal). These

characters appear to fulfill the syndrome of ornithophilous flowers.

Of the four different types of hummingbird corollas present with

Neotropical gesneriads, Wiehler (1979b) reports that the majority of

Nematanthus species have a hypocyrtoid corolla (named after the former

23

genus Hypocyrta). This corolla type consists of a tube with a ventrally inflated pouch, tightly constricted throat and narrow limb.

The red, orange and yellow calyx and corolla, coloration is a primary attractant to hummingbirds, but Nematanthus fritschii and N. maculatus additionally display leaves with a red extrafloral attraction pattern. The leaves are red-splotched on the abaxial surface. Jones & Rich (1972) have observed hummingbirds being first attracted to the foliage of Columnea fl or ida , which possess leaves with "two conspicuous red spots located on the upper surface near the apex of the large leaves." Some birds inspected various portions of the plant for several seconds before finding the flowers.

The function of the inflated pouch of Nematanthus corollas is unknown. It does not appear to operate as a receptacle for excess nectar since there are species which have flowers in a nonresupinate orientation (pouch ventrally located) as well as species with resupinate flowers (pouch dorsally located). In fact, N. crass if olius and N. fritschii have pendulous flowers that hang from the leaf axil; here, a pouch could not function as a nectar receptacle since the nectar would run out of the flower.

Wiehler ( 1979b) postulates that the inflated pouch could serve as a target enlargement. With the hummingbird's approach to the front of the flower, the pouch contributes to produce a larger target that would aid in a more effective pollination. The orientation of the flower would not disrupt this hypothesis since the position of the stamens and stigma, as discussed, would remain as a functional unit. Also, the constricted throat of the corolla may serve to exclude larger insects such as Euglossine bees.

2k

Hummingbird-pollinated flowers frequently have some means of protecting the ovules. Grant (1950) surveyed the flowering plant families and examined the relationships between pollinators and any special means of ovule protection of the flowers they visited. He observed that Nematanthus (and Hypocyrta) species provided no special means of ovule protection. In studying Columnea f 1 or ida (a

hummingbird-pollinated species), Jones & Rich (1972) stated that "the 'V-shaped' nature of the connate anthers and the stigmatic surfaces (also present in Nematanthus species) serve to direct the bill away from the superior ovary and into contact with the nectar which collects in a slight depression in the lower portion of the corolla" (p. 115)«

Chromosome Number Cod on an the and Nematanthus are unique in the tribe Episcieae in possessing a basic chromosome number of x = 8, whereas all other genera have a basic chromosome number of x = 9» Table II-l lists the known chromosome numbers of Codonanthe and Nematanthus species (Fussell, 1958; Lee, 1962, 1964, 1966; Ratter, 1963; Lee & Grear, 1963; Morley, 1975; Wiehler, 1971, 1975, 1977; Moore, 1973a; Skog, 1980, 1981; Yuen, personal observation, 1982).

Cultivated species of Nematanthus are diploid (x = 8, n = 8), whereas Codonanthe has diploid and tetraploid (x = 8, n = 16) representatives. Species of subgenus Codonanthe section Codonanthe are diploids, but species of subgenus Codonanthe section Spathuliformae and subgenus Codonanthella are basically tetraploids; exceptions include C. caribaea (diploid) and C. luteola (diploid and tetraploid).

25

Distribution

Species of Codonanthe subgenus Codonanthe section Codonanthe are confined to the coastal areas of southeastern Brazil. In contrast, species of subgenus Codonanthe section Spathuliformae and subgenus Codonanthella inhabit regions from south Mexico, through Central America, to areas of northern South America — with the southernmost representatives in Eolivia, Peru and northwestern Brazil. Thus, the species of this genus have a disjunct distribution.

Nema tan thus species are localized in small areas along the coast of southeastern Brazil as are species of Codonanthe subgenus Codonanthe section Codonanthe. Species of Nema tan thus form a geographically continuous group with no apparent disjuncts.

A discussion of the implications of geographical distribution to the taxonomic status of Codonanthe and Nematanthus is presented in CHAPTER VI: CONCLUSION.

26

Table II-l. Morphological characteristics of the genera Codonanthe and Nematanthus.

TAXA

GROWTH STEM LEAF PETIOLE

HABIT* SIZE** Shape*** Coloration Size****

GENUS Codonanthe

SUBGENUS Codonanthe

SECTION Codonanthe 1

2. C.

3. C.

carnosa

devosiana

digna

gracilis

paula

SECTION Spathuliformae

6. C. calcarata

7. C_. corniculata

8. C. eras si folia

9. C. uleana

SUBGENUS Codonanthe! la

10. C. caribaea

11 . C_. chiricana

12. C. elegans

13. C. luteola

14. C. macradenia

viny	2-4	round	green	4-10
vi ny	2-4	round	green	4-10
viny	2-4	round	green	4-10
viny	2-4	round	green	4-10
viny	2-4	round	green	4-10
vin/shr	2-4	round	green	4-10
viny	2-4	round	red	4-10
viny	2-4	round	green	4-10
vin/shr	2-9	round	green	4-10
vin/shr	2-4	round	green	4-10
vin/shr	2-4	round	green	4-10
viny	2-4	round	green	4-10
viny	2-4	round	green	4-10
viny	2-4	round	green	4-10

GENUS Nematanthus

1. 2. 3.

4. N. hirtellus

5. N. maculatus

N. crass if ol ius NL fissus N. fritschii

N. N.

gregarius nervosus

9. N_. strigillosus 10. N. wettsteinii

shrubby	5-9	rnd/fur	green	10-50
shrubby	5-9	rnd/fur	red	10-50
shrubby	5-9	round	green	10-50
shrubby	5-9	round	red	10-50
shrubby	5-9	round	green	10-50
shrubby	5-9	round	red	10-50
viny	2-4	rnd/fur	green	4-10
viny	2-4	rnd/fur	green	4-10
viny	2-4	rnd/fur	green	4-10
viny	2-4	round	green	4-10

* all species are epiphytes, vin/shr=viny/shrubby. ** diameter, in mm. *** all species possess round petioles, some have a slight furrow on

the adaxial surface of the petiole, rnd/fur=round/furrow. **** length, in mm.

Table II-l - continued,

27

TAXA

LEAF BLADE

Balance*

Form*

Apex'*

Base^

2.	C. C.	devosiana
3.	digna
4. 5.	C.	gracil is paula
6.	c. c. c. c.	calcarata
7.	corn icu lata
8.	crassifol ia
9.	uleana
10.	c.	caribaea
11.	c. c. c.	chiricana
12. 13.	elegans luteola
14.	c.	macradenia

lam sym/base sym wid ellip obtuse obt-rnd

lam sym/base sym wid ellip acute obt-rnd

lam sym/base sym wid ovate obtuse rounded

lam sym/base asym nar ovate acute-acum cordate

lam sym/base sym wid ovate obtuse rounded

lam sym/base asym nar obov acute • cordate

lam sym/base sym wid ellip acute acute

lam sym/base sym nar ellip acute-atten acute

lam & base asym obovate acuminate acute

lam sym/base sym elliptic lam sym/base sym wid obov lam sym/base sym obovate lam sym/base sym wid ellip lam sym/base asym wid ellip

attenuate	acute
acute	acute
acute	acute
acute	acute
acute	acute

1.

crass ifoli us

2.	N.	fissus
3.	N.	fritschii
4.	N.	hirtellus
5.	N.	maculatus
6.	N. N.	perianthomegus
7.	gregarius
8.	N.	nervosus
9.	N. N.	strigillosus
10.	wettsteinii

lam asym/base sym elliptic acum-atten acute

lam sym/base sym elliptic acute acute

lam sym/base sym elliptic acum-atten acute

lam sym/base sym wid ellip acute-obtuse obtuse

lam sym/base asym nar obov acum-atten acute

lam sym/base sym wid ellip acute acute

lam sym/base asym nar ovate attenuate obt-rnd

lam sym/base sym wid ellip acute acute

lam sym/base sym wid ellip acute acute

* lam=lamina, sym=symmetrical , asym=asymmetrical . ** wid=widely, nar=narrowly, ellip=ell iptic, obov=obovate. *** acum=acuminate, atten=attenuate. **** obt=obtuse, rnd=rounded.

Table II-l - continued.

23

TAXA

LEAF BLADE

Margin* Size** Texture Coloration***

1. 2. 3. 4. 5.	C. C. c. c. c.	carnosa devosiana digna gracilis paula	sit cren entire entire sit cren sit cren	2-4 2-4 2-4 4-12 2-4	puberulous pubescent puberulous smooth puberulous
6. 7. 8. 9.	c. c. c. c.	calcarata corniculata crass i folia uleana	crenate sit cren entire sit cren	4-12 4-12 4-12 4-12	smooth smooth smooth smooth
10. 11. 12. 13. 14.	c. c. c. c. c.	caribaea chiricana elegans luteola macradenia	entire sit cren sit cren sit cren sit cren	4-12 2-4 4-12 4-12 4-12	smooth smooth smooth smooth smooth

red abax leaf surf green only red abax leaf surf red leaf margins red abax leaf surf

green only red abax leaf surf red leaf margins green only

red leaf margins green only red 1° & 2° veins green only green only

1. N. crassifolius entire

2. N. fissus crenate

3. N_. fritschii entire

4. N. hirtellus entire

5. N. maculatus entire

6. N. perianthomegus sit cren

7. N. gregarius

8. N. nervosus

entire entire

9. N. strigillosus entire 10. N. wettsteinii entire

4-12 4-12 4-12 4-12 4-12 4-12

2-4 2-4 2-4 2-4

smooth

pubescent

smooth

puberulous

smooth

smooth

green only

green only

red 1° & 2° veins

green only

red 1° & 2° veins

green only

smooth green only

smooth green only

pubescent red 1° & 2° veins

smooth red lam/green veins

* sit cren=slightly crenate.

** length, in cm.

*** all species possess green adaxial leaf surface, coloration pertains to the abaxial leaf surface besides green, abax=abaxial , surf=surface, 1° & 2° veins=midrib & secondary veins, lam=lamina.

29

Table 1 1 — 1 - continued.

TAXA

FLOWER

Orientation* Pedicel** Shape*

FLOWER: Calyx

Color*

Size*

1. 2. 3. 4. 5.	C. C. C. C. c.	carnosa devosiana digna gracilis paula	nonresup/erect nonresup/erect nonresup/erect nonresup/erect nonresup/erect	3- 3- 3- 3- 3-	■25 ■25 ■25 ■25 -25
6. 7. 8. 9.	c. c. c. c.	calcarata corniculata crass if ol ia uleana	nonresup/erect nonresup/erect nonresup/erect nonresup/erect	3- 3- 3- 3-	■25 -25 -25 ■25
10. 11. 12. 13. 14.	c. c. c. c. c.	caribaea chiricana elegans luteola macradenia	nonresup/erect nonresup/erect nonresup/erect nonresup/erect nonresup/erect	3- 3- 3- 3- 3-	-25 -25 -25 -25 -25

linear-lane green 2-10

linear-lane green 2-10

linear-lane green-pur 2-10

linear-lane green-red 2-10

linear-lane green 2-10

linear-lane green 2-10

linear-lane green-red 2-10

linear-lane green 2-10

linear-lane green 2-10

linear-lane green-pur 2-10

linear-lane green-red 2-10

linear-lane green 2-10

linear-lane green-red 2-10

linear-lane green-red 2-10

crassifolius

fissus

fritschii

hirtellus

maculatus

resup/pendulant

resup/erect

resup/pendulant

resup/erect

resup/erect

6. N. perianthomegus resup/erect

7. N_. gregarius

8. N. nervosus

nonresup/erect nonresup/erect

9. N^. strigillosus nonresup/erect 10. N. wettsteinii nonresup/erect

25-200 3-25

25-200 3-25 3-25 3-25

3-25 3-25 3-25 3-25

linear-lane green 10-30 linear-lane green 10-30 linear-lane green-pur 10-30 10-30 10-30 10-30

10-30 10-30 10-30 10-30

ovate-ell ip green ovate-ell ip green ovate-ell ip green

ovate-el lip green ovate-ell ip green ovate-el lip green linear-lane green

* nonresup=nonresupinate, resup=resupinate. ** length, in mm. *** all species possess a 5-parted calyx, shape pertains to calyx lobes,

lanc=lanceolate, ell ip=ell iptic. **** pur=purple.

Table II-l - continued

30

TAXA

Shape'

FLOWER: Corolla

Color

Size'

1.	C.	carnosa	funnel form	white	+	yellow, red, brown	2-4
2.	C.	devosiana	funnel form	white	+	brown	1-2
3.	C.	digna	funnel form	white	+	pink	1-2
4.	c.	gracilis	funnel form	white	+	yellow, red, purple	2-4
5.	I-	paula	funnel form	white	+	pink, red	1-2
6.	c.	calcarata	funnel form	white	+	pink, red, purple	2-4
7.	c.	corniculata	funnel form	white	+	yellow	2-4
8.	c.	crassifolia	funnel form	white	+	yellow, pink	1-4
9.	c.	uleana	funnel form	white	+	yellow, pink, red	2-4
10.	c.	caribaea	funnel form	white	+	yellow, purple	2-4
11.	c.	chiricana	funnel form	white	+	red	2-4
12.	c.	elegans	funnel form	white	+	yellow	2-4
13.	c.	luteola	funnel form	yel 1 ow		2-4
14.	c.	macradenia	funnel form	white	+	pink, red	2-4

1 . N_. crassifolius pouched

2. N. fissus pouched

3. N. fritschii pouched

4. N. hirtellus ' pouched

5. N. maculatus pouched

6. N. perianthomegus pouched

7. N. gregarius

8. N. nervosus

pouched pouched

9. N. strigiTlosus pouched 10. N. wettsteinii pouched

red

red

red

yellow

pink + yellow

yellow + purple

orange + yellow

red

orange

orange + yellow

4-6 2-4 4-6 2-4

2-4 2-4

2-4 2-4 2-4 2-4

* all species possess an obliquely ventricose corolla, pouched=Hypocyrta-

type corolla of Wiehler, 1979b. ** length, in cm.

Table II-l - continued.

31

TAXA

FRUIT POLLINATION CHROMOSOME

TYPE* AGENT** NUMBER*** DISTRIBUTION****

1. 2.	C. C. C. C. c. c. c. c. c. c. c. c. c. c.	carnosa devosiana
3. 4. 5. 6.	digna gracilis paula calcarata
7.	corniculata
8.	crassifolia
9. 10. 11.	uleana caribaea chiricana
12. 13. 14.	elegans luteola macradenia

indeh/orange	bee	2n	se Brazil
indeh/orange	bee	2n	se Brazil
indeh/orange	bee		se Brazil
indeh/orange	bee	2n	se Brazil
indeh/orange	bee		se Brazil
deh/red-pur	bee	4n	s Mex-CA-nw	SA
?deh/red-pur	bee	4n	s Mex-CA-nw	SA
deh/red-pur	bee	4n	s Mex-CA-nw	SA
deh/red-pur	bee	4n	s Mex-CA-nw	SA
deh/red-pur	bee	2n	s Mex-CA-nw	SA
deh/red-pur	bee		s Mex-CA-nw	SA
deh/yel-grn	bee	4n	s Mex-CA-nw	SA
deh/yel-grn	bee	2n,4n	s Mex-CA-nw	SA
deh/red-pur	bee	4n	s Mex-CA-nw	SA

1.	N.	crassifolius	deh/yel-grn	bird
2.	N.	fissus	deh/yel-grn	bird
3.	N.	fritschii	deh/yel-grn	bird
4.	N.	hirtellus	deh/yel-grn	bird
5.	N.	maculatus	deh/yel-grn	bird
6.	N.	perianthomegus	deh/yel-grn	bird
7.	N.	gregarius	deh/yel-grn	bird
8.	N.	nervosus	deh/yel-grn	bird
9.	N.	strigillosus	deh/yel-grn	bird
10.	N.	wettsteinii	deh/yel-grn	bird

2n	se	Brazil
2n	se	Brazil
2n	se	Brazil
2n	se	Brazil
	se	Brazil
2n	se	Brazil
2n	se	Brazil
2n	se	Brazil
2n	se	Brazil
2n	se	Brazil

* indeh=indehiscent berry, deh=dehi scent, tardily dehiscent or occasionally splitting berry or fleshy capsule, red-pur=red, purple or pink, yel-grn=yel low-green.

** bee=euglossine bees, bird=hummingbirds.

r** base chromosome number is x=8, 2n=16 or diploids, 4n=32 or tetraploids.

f** se Brazil=southeastern Brazil, s Mex-CA-nw SA=southern Mexica through Central America to northwestern South America.

Figure II-l . Growth habit of species of Cod on an the subgenus Cod on an the section Cod on an the.

A. C. carnosa.

B. C_. devosiana.

C. C. digna.

D. C. gracilis.

E. C. paula.

33

• * v

Figure II-2. Growth habit of species of Cod on an the subgenus Cod on an the section Spathuliformae.

A. C_. calcarata.

B. C. corniculata.

C. C. crass if olia.

D. C. uleana.

35

Figure II-3. Growth habit of species of Cod on an the subgenus Codonanthella.

A. C. caribaea.

B. C_. elegans. G. C. luteola.

D. C. macradenia.

3?

Figure II-4. Growth habit of species of Nema tan thus. A. N. crass if olius.

B.	N.	fissus.
C.	N.	fritschii.
D.	N.	hirtellus.
E.	N.	maculatus.

F. N. perianthomegus,

39

Figure II-5* Growth habit of species of Nema tan thus.

A. N. gregarius.

B. N. nervosus.

C. N. strigillosus.

D. N. wettsteinii.

M

Figure II-6. Leaf "blade shape of species of Cod on an the subgenus Cod on an the section Codonanthe.

A. C. carnosa, XI.

B. C_. devosiana, XI.

C. C. digna, XI.

D. C. gracilis, XI.

E. C. paula, XI.

i*3

• ft

• •

B

• e

M

#•

Figure II-7. Leaf blade shape of species of Codonanthe subgenus Codonanthe section Spathuliformae.

A. C. calcarata, XI.

B. C. corniculata, XI.

C. C. crass if olia, XI.

D. C. uleana, XI.

45

Figure II-8. Leaf blade shape of species of Codonanthe subgenus Godonanthe.

A. C. caribaea, XI.

B. C_. elegans, XI .

C. C. luteola, XI.

D. C. macradenia, XI.

47

♦ ♦

B

M M

Figure II-9. Leaf "blade shape of species of Nematanthus,

A. N. crass if olius, XI.

B. N. fissus, XI.

C. N. fritschii, XI.

D. N. hirtellus, XI.

E. N. maculatus , XI.

F. N. perianthomegus, XI .

NM

B

i

Figure 11-10. Leaf blade shape of species of Nematanthus.

A. N. gregarius, XI.

B. N. nervosus, XI .

G. N. strigillosus, XI. D. N. wettsteinii, XI.

51

M

B

M

# ♦

Figure 11-11. Floral morphology of species of Nematanthus.

A. N. perianthomegus , side view of resupinate flower with

dorsally-located pouch, XI. 5.

B. N. perianthomegus , face view of resupinate flower. Note

anthers within corolla are facing upwards, X6.

C. N, maculatus , side view of resupinate flower with

dorsally-located pouch, XI. 5*

D. N. maculatus , face view of resupinate flower. Note

anthers within corolla are facing upwards, X6.

E. N. strigillosus, side view of nonresupinate flower with

ventrally-located pouch, X2.5.

F. N. strigillosus, face view of nonresupinate flower. Note

the stigma of the elongating style moves into the former dorsal position of the retracting anthers, XI 1.

53

Figure 11-12. Floral morphology of species of Godonanthe.

A. C. luteola, side view of nonresupinate flower with

obliquely funnelform-ventricose corolla, XI . 5.

B. C. crass if olia, side view of nonresupinate flower with

obliquely funnelform-ventricose corolla, X3.

G. C. luteola, side view of flower displaying

obliquely-situated corolla within calyx and prominent spur, X7.

D. C. digna, face view of nonresupinate flower. Note anthers

are dorsally-located within corolla, X8.5«

E. C. macradenia, ventral view of flower depicting a groove

within the corolla, X5. 5«

F. C. macradenia, face view of flower depicting a groove

within the corolla, X18.

55

Figure 11-13. Stigma and stigmatic surface.

A. C. devosiana, apical portion of stigma, X120.

B. N. f issus , apical portion of stigma, X71 .

C. N. crass if ol ius, papillae of stigmatic surface, X240.

D. N. f issus , papillae of stigmatic surface, X210.

57

Figure 11-14. Floral morphology and fruit of species of Cod on an the.

A. C. luteola, side view of flower with corolla removed to

reveal gynoecium with a nectary connivent and dorsal to the ovary, J.J.

B. C. corniculata, dorsal view of flower with corolla and

dorsal sepal removed to reveal nectary, X30.

G. C. crass if olia, side view of flower with prominent extrafloral nectary in the sinus of the calyx lobe margin, X30.

D. C. crass if olia, side view of subglobose berry, XI . 5.

E. C. luteola, side view of pointed capsule, XI . 5.

Figure 11-15. Seeds of species of Godonanthe subgenus God on an the section Codonanthe.

A. C. devosiana, X75»

B. C. digna, X75.

C. C. paula, X75.

61

Figure 11-16. Seeds of species of Codonanthe subgenus Codonanthe section Spathul if ormae and subgenus Godonanthella.

A. C. calcarata, X30.

B. C. crass if olia, X50. G. C, caribaea, X50.

D. C. macradenia, X50.

63

Figure 11-17. Seeds of species of Nema tan thus.

A. N. gregarius, X75«

B. N. nervosus , X75«

C. N. fissus, X75.

65

Figure 11-18. Seedlings of primary hybrids of Codonanthe and Nema tan thus.

A. Seedlings of C. digna X C. devosiana, X4.

B. Seedlings of N. nervosus X N. strigillosus, X2.

C. Seedlings of N. strigillosus X C. carnosa, X4.

D. Seed germinating container with G. digna X G. paula

seedlings, Xl/3.

67

CHAPTER III COMPARATIVE MORPHOLOGY OF THE LEAF EPIDERMIS

Introduction The taxonomic value of the morphology of leaf epidermal surfaces has been expounded by Stace (1965) and Sinclair & Sharma (l9?l). Conventional light microscopy (LM) methods of examining Gesneriaceae leaf surfaces have been used in the study of the genera Column ea and Alloplectus (Stearn, 1969) 1 Gesneria (Skog, 1976), and in some gesneriads of Africa and Asia (Sahasrabudhe k Stace, 197*0 1 Sri Lanka (Herat & Theobald, 1979) and the Neotropics (Wiehler, 1979b). Taxonomic investigations utilizing scanning electron microscopy (SEM) have been relatively limited. Some recent SEM studies include those of Atwood & Williams (1979) for Cypripedioideae (Orchidaceae) , Thomson & Mohlenbrock (1979) for Quercus (Fagaceae), Hardin (1979, 1981 ) for some North American woody plants, Dehgan (1980) for Jatropha (Euphorbiaceae) and Rudall (1980) for Hyptis (Labiatae). However, the comparative morphology of Gesneriaceae leaf epidermis utilizing SEM has not been reported. This study of leaf surfaces was initiated to discover more characters of taxonomic utility in evaluating the subgeneric categories of Codonanthe and to establish natural groupings in Nematanthus.

Materials and Methods All plant materials examined were from a live collection cultivated in a growth room at the Department of Ornamental

68

69

Horticulture, University of Florida. Uniform conditions were

maintained via a 22-25° C day temperature, 17-20° C night temperture, ^00-6000 Lux fluorescent lighting and a Ik hour daylength. Voucher specimen are deposited at the University of Florida herbarium (FLAS).

In the SEM preparation (cf. , Hayat, 1978), mature leaves were sampled using a no. 2 cork "borer to punch out 5 mm leaf discs which were fixed overnight in 2% glutar aldehyde. Leaf samples were then dehydrated in a 20-100% ethanol series for 2 hours, critical point dried for 30 minutes, mounted on aluminum stubs with TV Tube Koat (GC Electronics), and coated with a gold-palladium mixture. A Hitachi S-450 Scanning Electron Microscope was used to view the specimens and photographs were recorded on Polaroid Type 55 Positive/Negative film.

In the LM preparation, immature and mature leaves were sampled for ontogenetic studies of the stomata and the examination of leaf surfaces, respectively. Free-hand paradermal sections were taken with a razor blade and mounted in water for observation. Guard cell length and width were measured with an eyepiece micrometer and presented as a mean value + the standard error of the mean (x + S.E.x). A guard cell area index was calculated by multiplying the mean length by the mean width of the guard cells. A Wild M-20EB Light Microscope was used to examine the specimens.

Observations Descriptive terminology of epidermal features is based on Dilcher (197^) and summarized in Table III-l. Definitions of terms used in the text are briefly reviewed below.

70

Trichomes. Glandular and nonglandular trichomes can be recognized on the adaxial and abaxial leaf surface. Nonglandular trichomes may be unicellular or multicellular-uniseriate. Glandular trichomes are multicellular and composed of a head and a body. The head consists of 2, k or more cells and the body is either short or long (cf. , Esau, 1965). Short glandular trichomes have a unicellular body while long (stalked) glandular trichomes have a multicellular-uniseriate body. Basal cells of glandular trichomes may be randomly-arranged, radially-arranged or sunken. The sunken basal cell type gives the glandular head a sessile appearance, as though it were attached directly to the epidermis with no basal trichome cell (Sahasrabudhe & Stace, 197^; Wiehler, 1979b).

Stomata. Anisocytic and helicocytic stomata have been observed on the abaxial leaf surface. Anisocytic stomata have guard cells surrounded by three unequal subsidiary cells of which one is distinctly smaller than the other two. Helicocytic stomata have guard cells surrounded by four or more subsidiary cells arranged in a helix (Fryns-Claessens & Van Cotthem, 1973).

Extrafloral Nectaries. These are nectaries (distinct from

glandular trichomes) that appear other than on the flower (Moore, 1973a). In the plants studied here they occur on the abaxial surface of the leaf. These extrafloral nectaries are composed of a central area where the epidermal cells form a pigmented swelling in the leaf surface and a surrounding area which is encircled with short glandular trichomes.

71

Epidermal Cells. Epidermal cell surfaces are rather smooth or contain surface ornamentations in the form of echinate papillae or striations (Dilcher, 197*0.

GENUS Codonanthe (Martius) Hans te in

Several leaf epidermal features were consistent in all species of Codonanthe. Epidermal cells were isodiametric and randomly-arranged. Stomata occurred abaxially and were randomly distributed. Surface ornamentations were not evident on subsidiary or guard cells and all cells were topographically at the same level. SUBGENUS Codonanthe

Nine known species of this subgenus were examined.

SECTION Codonanthe. Five species were studied (Figures III-1A to III-IF): C. carnosa (Gardner) Hanstein, C. devosiana Lem. , C. digna Wiehler, C. gracilis (Martius) Hanstein, and C, paula Wiehler.

Multicellular-uniseriate nonglandular trichomes, occurring on both leaf surfaces (except abaxially only in C. gracilis) t had basal epidermal cells radially-arranged (except randomly-arranged in £. gracilis). Multicellular glandular trichomes, present on both leaf surfaces, had a 4-celled head, a short (unicellular) body and randomly-arranged basal epidermal cells (except basal cell sunken in C_. gracilis). Anisocytic stomata were observed on the abaxial leaf surface. Extrafloral nectaries were absent. No surface ornamentations were evident, except in C. gracilis which had epidermal cells with echinate papillae. Guard cells had a mean length of 23.2um, mean width of 19.7um and area index of k$5 urn .

72

SECTION Spathul if ormae L. B. Smith. Four species were examined (Figures III-2A, III-2C, III-3A to III-3D) i C. calcarata (F. A. W. Miquel) Hanstein, C. corniculata Wiehler, C. crass if olia (Focke) Morton and C. uleana Fritsch.

Unicellular nonglandular trichomes, present on both leaf surfaces, had randomly-arranged basal epidermal cells. Multicellular glandular trichomes, also present on both leaf surfaces, had a 2-celled head, a short (unicellular) body and randomly-arranged basal epidermal cells. Anisocytic stomata and extrafloral nectaries were present on the abaxial leaf surface. No surface ornamentations were evident. Guard cells had a mean length of 30«3um» mean width of 26.2um and area index of 796um2. SUBGENUS Codonanthella Wiehler

Five species in this subgenus were examined (Figures III-2B, III-2D to III-2F) : C. caribaea Urban, C. chiricana Wiehler, C. elegans nomen nudum (to be described by Wiehler, 1982), C. luteola Wiehler and C. macradenia Donnell-Smith.

Unicellular nonglandular trichomes, present on both leaf surfaces (except abaxially-occurring multicellular trichomes of C. caribaea), had randomly-arranged basal epidermal cells. Multicellular glandular trichomes, present on both leaf surfaces, had a 2-celled head (except 4-celled in C. caribaea) and a short (unicellular) body. Basal epidermal cells were randomly-arranged (except basal cell sunken in C. caribaea), Anisocytic stomata and extrafloral nectaries were present on the abaxial leaf surface in C. chiricana, C. elegans, C_. luteola and C_. macradenia but not in G_. caribaea. No surface ornamentations were evident except in C. caribaea which had epidermal cells with echinate

73

papillae. Guard cells had a mean length of 33«lum, mean width of 28.2um and area index of 936um .

GENUS Mema tan thus Schrader

Several leaf epidermal features were consistent in all species of Nema tan thus. Epidermal cells were isodiametric and randomly-arranged. Stomata were abaxially occurring and randomly oriented. No surface ornamentations were evident on subsidiary and guard cells, and all cells were topographically at the same level.

Ten species placed in this genus were examined (Figures III-4A to III-6F) : N. crass if olius (Schott) Wiehler, N. fissus (Vellozo) L. Skog, N. fritschii Hoehne, N. gregarius D. Denham, N. hirtellus (Schott) Wiehler, N. maculatus (Fritsch) Wiehler, N. nervosus (Fritsch) H. E. Moore, N. perianthomegus (Vellozo) H. E. Moore, N, strigillosus (Martius) H. E. Moore and N. wettsteinii (Fritsch) H. E. Moore.

Multicellular-uniseriate nonglandular trichomes with

radially-arranged "basal epidermal cells occurred in all species. Multicellular glandular trichomes with a 4-celled head and only one trichome per basal epidermal cell, a short (unicellular) or long (multicellular) body, and anisocytic stomata were characteristic of N. crass if olius, N. fissus, N. fritschii, N. hirtellus, N. maculatus and N. perianthomegus. Multicellular glandular trichomes with a

4-or -more-celled head and/or more than one trichome per basal epidermal cell, a short (unicellular) body, and helicocytic and anisocytic stomata were characteristic of N. gregarius, N. nervosus, N. strigillosus and N. wettsteinii. The occurrence of nonglandular trichomes varied among Nema tan thus species while glandular trichomes

7^

Table III-l. Leaf epidermal characters of Codonanthe and Nematanthus.

NONGLANDULAR TRICHOMES

TAXON

Occurrence

AB=abaxial AD=adaxial

Number of Cells

l=unicel lular #=multicellular -uni seriate

Basal Epidermal Cell Arrangement

GENUS Codonanthe SUBGENUS Codonanthe SECTION Codonanthe

C. carnosa C. devosiana C. digna C. gracilis C. paula	AB AB AB AB	+ AD + AD + AD AB + AD	# # # #	radial radial radial random radial
SECTION Spathulifornae C. calcarata C. corniculata C. crassi folia C. uleana	AB AB AB AB	+ AD + AD + AD + AD	1 1 1 1	random random random random
BGENUS Codonanthella
C. caribaea C. chiricana C. elegans C. luteola C. macradenia	AB AB AB AB	AB + AD + AD + AD + AD	4 - 1 1 1 1	random random random random random

GENUS Nematanthus N_. crassi foli us N_. fissus N. fritschii

N_. hirtellus

N. maculatus

N_. perianthomegus

N_. gregarius

N. nervosus

NL strigillosus

N. wettsteinii

AB	#	radial
AB + AD	#	radial
AB	#	radial
AB + AD	#	radial
AB	#	radial
AB + AD	#	radial
absent		___
AB + AD	4 rr	radial
AB + AD	#	radial
AB	#	radial

75

Table III-l - continued.

GLANDULAR TRICHOMES

Glandular Head

Basal Epidermal , Body Cell Arrangemenf

TAXON

S=short unicellular L=long multicellular

GENUS Codonanthe
SUBGENUS Codonanthe
SECTION Codonanthe C. carnosa C. devosiana C. digna C. gracilis C. paula	4-celled 4-celled 4-celled 4-celled 4-celled	S s s s s	unmodified unmodified unmodified modified unmodified
SECTION Spathuliformae C. calcarata C. corniculata C. crassi folia C. uleana	2-celled 2-celled 2-celled 2-celled	s s s s	unmodified unmodified unmodified unmodified
SUBGENUS Codonanthella C. caribaea C. chiricana C. elegans C. luteola C. macradenia	4-celled 2-celled 2-celled 2-celled 2-celled	s s s s s	modified unmodified unmodified unmodified unmodified
GENUS Nematanthus N. crassifolius N. fissus N. fritschii N. hirtellus N. maculatus N. perianthomegus	4-celled 4-celled 4-celled 4-celled 4-celled 4-celled	S or L S or L S or L S or L S or L S or L	modified modified modified modified modified modified
N. gregarius N. nervosus N. strigillosus N. wettsteinii	2 >4-celled >4-celled >4-celled >4-celled	S s s s	modified modified modified modified

1 Occurs on both surfaces of the leaves in all species.

2 More than 4 cells per head and/or more than 1 trichome per basal

epidermal cell.

3 Unmodified=randomly-arranged; modified=trichomes with a unicellular

body have a sunken epidermal cell while trichomes with a multicellular stalked body have radially-arranged epidermal cells.

76

Table 1 1 1 — 1 - continued.

	STOMATA	EXTRAFLORAL	EPIDERMAL CELL
		TYPE	NECTARY	ORNAMENTATION
	AN=anisocytic
	HEL=helicocytic
TAXON
GENUS Codonanthe
SUBGENUS Codonanthe
SECTION Codonanthe
C. carnosa		AN	absent	none
C. devosiana		AN	absent	none
C. diqna		AN	absent	none
C. gracilis		AN	absent	echinate papillae
C. paula		AN	absent	none
SECTION JBpathuliformae
C. calcarata		AN	abaxial	none
C. corniculata		AN	abaxial	none
C. crassifolia		AN	abaxial	none
C. uleana		AN	abaxial	none
SUBGENUS Codonanthe! la
C. caribaea		AN	absent	echinate papillae
C. chiricana		AN	abaxial	none
C. elegans		AN	abaxial	none
C. luteola		AN	abaxial	none
C. macradenia		AN	abaxial	none
GENUS Nematanthus
N. crassifolius		AN	absent	none
N. fissus		AN	absent	striations
N. fritschii		AN	absent	none
N. hirtellus		AN	absent	none
N. maculatus		AN	absent	none
N. perianthomegus		AN	absent	none
N. gregarius	AN	+ HEL	absent	none
N. nervosus	AN	+ HEL	absent	none
N. strigj'llosus	AN	+ HEL	absent	none
N. wettsteinii	AN	+ HEL	absent	striations

77

were situated abaxially only. Glandular trichomes had modified "basal epidermal cells, i.e., trichomes with a unicellular body had a sunken basal epidermal cell while trichomes with a multicellular body had radially-arranged basal epidermal cells. Extrafloral nectaries and surface ornamentations were absent, except for striations on epidermal cells in N. fissus and N. wettsteinii. Guard cells had a mean length of 29«5uin» mean width of 22.5um and area index of 666um .

Discussion

Although features of the adaxial and abaxial surfaces of the leaves are consistent within sections of genus Codonanthe, differences are noted among sections in subgenus Codonanthe. Species of subgenus Cod on an the section Spathul if ormae share more epidermal characters with species in subgenus Codonanthella than with those species in subgenus Godonanthe section Codonanthe. Multicellular -uniseriate nonglandular trichomes (Figures III-1A & Ill-IB) with radially-arranged basal epidermal cells (Figure III-IC), glandular trichomes with 4-celled heads (Figure Ill-ID), and the absence of extrafloral necteries are consistent characters in species of section Codonanthe. Species in section Spathul if ormae and subgenus Codonanthella share certain epidermal characters which include unicellular glandular trichomes (Figures III-2A & III-2B) with randomly-arranged basal epidermal cells, multicellular glandular trichomes with 2-celled heads (Figures III-2C & III-2D), and the presence of extrafloral nectaries (except in C. caribaea; Figures III-3A & III-3D).

Codonanthe gracilis and C. caribaea (Figure III-2F) have been placed in different subgenera (Wiehler, 1982), but are identical in all

78

leaf epidermal characters. For example, both species possess

multicellular-uniseriate n on glandular trichomes, multicellular glandular trichomes with a 2-celled head and a short (unicellular) body, anisocytic stomata and epidermal cells with echinate papillae. Codonanthe caribaea also shares some epidermal characters with the section Codonanthe.

Kleinfeldt (1978) and Madison (1979) described the mutualistic association between Codonanthe crass if olia, C. calcarata and C. uleana and tropical arboreal ants. Ants are the agents of seed dispersal, carrying Codonanthe seeds to their carton nests. The seeds germinate and penetrate the carton with fibrous roots. The roots function as a framework, providing the ant nests with structural support. Codonanthe plants furnish food to the ants in the form of floral and extrafloral nectar, fruit pulp and seed arils. Kleinfeldt (1978) observed that the major food source for the ants is the nectar of Codonanthe. Extrafloral nectaries are located on the abaxial leaf surface and occur in species of subgenus Codonanthe section Spathul if ormae and subgenus Codonanthella, but are absent in species of subgenus Codonanthe section Codonanthe. The presence of foliar extrafloral nectaries in Codonanthe species appears to be associated with the occurrence of an ant-plant mutual ism .

Species of Nematanthus exhibit similar leaf epidermal features, but differ with respect to the type of glandular trichomes and stomata. In N. gregarius, N. nervosus , N. strigillosus and N. wettsteinii, glandular trichomes have a head of more than 4 cells (Figures III-6D to III-6F) and/ or more than one trichome per basal epidermal cell (Figure III-4D). The capacity for secretion appears to be greater in these four

79

species, when compared to the six species of Nema tan thus , perhaps due to the greater number of cells in the head of the glandular trichomes. Although N. gregarius has only a 4-celled glandular head, two or more glandular trichomes occur in a single locale and this arrangement may increase the potential of secretion by compensating for the 4-celled condition with more secreting heads.

The anisocytic type of stomata (Figure III-jjC) is present in all species of Nema tan thus, whereas the anisocytic and helicocytic stomatal types (Figure III-5D) occur in N. gregarius, N. nervosus , N. strigillosus and N. wettsteinii. The occurrence of two stomatal types in one species is unusual, however, the anisocytic and helicocytic stomatal types are derived from the same developmental sequence ( Payne, 1970 and personal observation), so their occurrence together might not be unexpected. The stomatal initial forms only three subsidiary cells in the anisocytic stomatal type but continues to divide forming four or more subsidiary cells in a helix in the helicocytic type of stomata. Since guard cells and subsidiary cells originate from the same stomatal initial, the developmental sequence is referred to as mesogenous (Fryns-Claessens & Van Cotthem, 1973) or eumesogenous (Stevens & Martin, 1978). Stomatal types in Nematanthus , therefore, are

classified ontogenetically as aniso-mesogenous or aniso-eumesogenous, and helico-mesogenous or helico-eumesogenous.

Guard cell area indices are calculated to provide a value representative of guard cell size, allowing a comparison among taxa. Subgenus Codonanthe section Spathuliformae (area index 796um ) have guard cells that are more similar in size with subgenus Godonanthella (area index 936um ) than with subgenus Codonanthe section Codonanthe

80

(area index 458um ) . Wiehler (1975) reported that species of subgenus Codonanthe section God on an the are diploids (n=8) while species of subgenus Codonanthe section Spathul if ormae and subgenus Codonanthella are tetraploids (n=l6), except C, caribaea (diploid) and C. luteola (diploid and tetraploid). The larger size of the guard cells of the tetraploid species is apparently related to the gigas effect of polyploidy (Stebbins, 1971).

Species of Nematanthus are diploids (n=8; Skog, 1981 ) and have a guard cell area index of 666um . This area index is intermediate between area indices of diploid and tetraploid species of Codonanthe. Nema tan thus species appear to be distinct from species of Codonanthe with respect to guard cell dimensions and ploidy level.

Nematanthus species share many epidermal characters with species in subgenus Codonanthe section Codonanthe (including

multicellular -uniseriate nonglandular trichomes) and only a few characters with species of subgenus Codonanthe section S pathul if ormae and subgenus Codonanthella. Morphological similarities in the epidermal surfaces of the leaves in subgenus Codonanthe section Codonanthe and Nematanthus are either an ancestral feature shared by the two genera, or are the result of parallel evolution related to a similarity of ecogeographical conditions.

Figure III-l. Leaf epidermal features of species of God on an the subgenus God on an the section Cod on an the.

A. C. paula, multicellular nonglandular and glandular

trichomes, XI 00.

B. C. digna, multicellular nonglandular and glandular

trichomes, X250.

G. C. carnosa, radially-arranged basal epidermal cells of nonglandular trichomes, XI 000.

D. C. gracilis, 4-celled head of glandular trichome, XI65O.

E. C, gracilis, echinate papillae and stoma, XI 000.

F. C. devosiana, anisocytic stoma, X1500.

82

if? •

Figure III-2. Leaf epidermal features of species of Codonanthe subgenus Codonanthe section Spathuliformae and subgenus Codonanthella.

A. C. crass if olia, unicellular nonglandular trichome, XI 000,

B. C. elegans, unicellular nonglandular trichome, X1200.

C. C. calcarata, 2-celled head of glandular trichome, X2000,

D. C. luteola, 2-celled head of glandular trichome, X1120.

E. C. macradenia, anisocytic stoma, X1260.

F. G. caribaea, multicellular nonglandular trichome and

sunken epidermal cell of glandular trichome, X350.

84

^

seat

g

E

Figure III-3. Leaf epidermal features of species of Godonanthe subgenus Godonanthe section Spathuliformae.

A. C. crass if olia, extrafloral nectary, X100.

B. C. uleana, extrafloral nectary, XI 50.

C. C. uleana, glandular trichomes that encircle extrafloral

nectary, X1000.

D. C. corniculata, extrafloral nectary, XI 10.

86

Figure III-4, Leaf epidermal features of species of Nematanthus.

A. N. fissus, multicellular nonglandular trichome, X110.

B. N. strigillosus, multicellular nonglandular trichome, X500.

C. N. perianthomegus, glandular trichome with short

(unicellular) and long (multicellular) "body cells, X500.

D. N. strigillosus, 2 short glandular trichomes per single

basal epidermal cell, X400.

Figure III-5. Leaf epidermal features of species of Nematanthus.

A. N. hirtellus, glandular trichome with bicellular body,

XI 500.

B. N. wettsteinii, glandular trichome, stomata and striated

epidermis, X$00.

C. N, crass if olius, anisocytic stoma, X1330.

D. N. gregarius, helicocytic stoma, X1230.

90

.v$?YV

,

s

Figure III-6. Leaf epidermal features of species of Nematanthus.

A. N. fissus, 4-celled head of glandular trichome, X500.

B. N. nervosus , 6-celled head of glandular trichome, X2000.

C. N. hirtellus, ^-celled head of glandular trichome, X500.

D. N. wettsteinii, 8-celled head of glandular trichome, XI 400.

E. N. maculatus , unicellular basal epidermal cell of

glandular trichome, XI k^O.

F. N. wettsteinii, unicellular basal epidermal cell of

glandular trichome, XI 300.

92

V
m \ ml** y

\

vv%*

X

}

v- "•I

-**&%

^

T\ » >

CHAPTER IV COMPARATIVE ANATOMY OF THE STEM AND LEAF

Introduction Anatomical studies of Codonanthe and Nematanthus are restricted to plants considered in Wiehler's (1970, 1979"b, 1982) taxonomic treatment of the Neotropical Gesneriaceae, where node, petiole and leaf structure were described for some species. Related anatomical studies are presented "by Skog (1976) for the genus Gesneria, Jong & Burtt (1975) for the genus Streptocarpus, Herat & Theobald (1979) for various gesneriad species of Sri Lanka, Rosser & Burtt (1969) for the tribe Trichosporeae, and Solereder (1908) and Metcalfe & Chalk (1950) for various species of Gesneriaceae. Nodal and wood anatomy were discussed by Howard (1970 ) for the genus Alloplectus, and Bierhorst (1964), Chalk (1937), Sinnott (191 k) and Sinnott & Bailey (191*0 for Gesneriaceae. Bokhari & Burtt (1970) and Burtt & Bokhari (1973) described foliar sclereids in gesneriads of the Old World. This preliminary study of stem and leaf anatomy of Codonanthe and Nematanthus species was initiated to disclose more taxonomically useful characters.

Materials and Methods

Live specimens of all known cultivated species of Codonanthe and

Nematanthus were examined. Plant materials were cultivated in a growth

room at the Department of Ornamental Horticulture, University of

Florida. The growth room provided uniform conditions of 22-25°C day

93

9^

temperature, 17-20° C night temperature, 4000-6000 Lux fluorescent lighting and a fourteen hour daylength. Voucher specimens were deposited at the University of Florida herbarium (PLAS).

Mature portions of nodes and internodes, petioles and blades were collected. Freehand serial sections of fresh material were stained with and mounted in toluidine blue 0 (Sakai, 1973; Dehgan, 1982). Microtome serial sections of paraffin-embedded material were stained with toluidine blue 0 and safranin-fast green (Berlyn & Miksche, 1976) and mounted in Permount (Fisher Scientific Company). Specimens were examined with a Wild M-20EB Light Microscope.

The leaf clearing method of Shobe & Lersten (1967) was utilized for the study of leaf architecture. All steps were followed except chloral hydrate was omitted and only safranin 0 stain was used. Terminology employed for describing the leaf venation patterns is based upon Hickey's (1973) classification of the architecture of dicotyledonous leaves. Specimens were examined with a Wild M8 Zoom Stereomicroscope.

Observations Stem Anatomy

The epidermis consisted of a single layer of tabular cells (rarely 2-3 cells thick). The cuticle was thin, and glandular and nonglandular trichomes were randomly situated around the stem. The cortex and pith were composed of chlorenchyma of basically isodiametric cells among which were many intercellular spaces or cells were irregularly-shaped with few intercellular spaces (i.e., cells tightly appressed to each other). Druses were often present in cortex cells, whereas prismatic

95

cells were frequently observed in pith cells. Sclereids with thick secondary walls and numerous pits were seen in the cortex as single cells or small groups of cells (Figures IV-1A, IV-4A & IV-4B). Vessel elements of the xylem had a helical structure. A thin suberized layer or periderm completely encircled the stem and was located between the epidermis and cortex. Node and Petiole Vasculature

Nodes were unilacunar or trilacunar in Codonanthe and Nematanthus. The unilacunar condition (Figures IV-1A & IV-1B) was marked by one leaf trace diverging from a single leaf gap (l:l) in the stele. Since Codonanthe and Nematanthus species possess opposite leaves, each node maintained two opposing leaf gaps with one leaf trace per leaf gap. The leaf trace continued to separate from the stem proper and entered the petiole as an arc-shaped, collateral vascular bundle (Figure IV-3A). The curvature of this vascular bundle was aligned with the abaxial surface of the petiole. At the abscission zone, two (e.g., N. wettsteinii) to five (e.g., C. digna) small vascular bundles branched adaxially from the large arc-shaped vascular bundle. •

The trilacunar condition (Figures IV- 1C to IV- IF & Figure IV-2) was marked by three leaf traces originating from three leaf gaps (3:3) in the stele. With the opposite leaf condition in species of Codonanthe and Nematanthus, each node displayed two median and two lateral leaf gaps with one leaf trace per gap. The median leaf trace diverged from the stem proper and entered the petiole as an arc-shaped, collateral vascular bundle. The curvature of this large vascular bundle was aligned with the abaxial surface of the petiole. The lateral leaf traces divided upon entering the stem cortex and each 'split-lateral'

96

trace (cf . , Howard, 1970 ) "branched- off towards a leaf. Two pairs of split-lateral traces (i.e., each trace of a pair derived from a different lateral leaf gap) traveled laterally through the stem cortex and converged upon the median leaf trace. At the abscission zone region, 2-3 small vascular "bundles often separated from the arc-shaped median leaf trace. Small vascular "bundles originating from the split-lateral and median leaf traces were situated within the petiole cortex tissue adaxial to the large arc-shaped vascular bundle.

Species of subgenus Codonanthe section Codonanthe (except C. gracilis and C. carnosa) , as well as Nema tan thus gregarius, N. nervosus, N. strigillosus and N. wettsteinii, displayed the unilacunar nodal anatomy. Species of subgenus Codonanthe section Spathul if ormae and subgenus Codonanthella, as well as Nematanthus crass if olius, N. fissus, N. fritschii, N. hirtellus, N. maculatus and N. perianthomegus, possessed the trilacunar, split-lateral nodal configuration.

The presence of prismatic crystals in the pith (Figure IV-4A) and sclereids in the cortex (Figure IV-4E) coincided with the formation of leaf gaps. Crystals and sclereids frequently occurred in areas adjacent to lacunae and leaf traces, respectively (Figure IV-1B). Leaf Mesophyll

Species of Codonanthe and Nematanthus possessed simple, dorsiventral leaves (Figure IV-3B). Adaxial and abaxial epidermis consisted of a single layer of tabular -shaped cells with a thin cuticle. Stomata, glandular and nonglandular trichomes occurred on the epidermis and were discussed in CHAPTER III.

A hypodermis (cf . , Esau, 1965) of enlarged parenchyma cells was located adjacent to the adaxial epidermis. The cells were iscdiametric

97

and tightly-appressed such that few intercellular spaces were present. Hypodermal cells were filled with water and chloroplasts were not evident. Depending upon the location on the blade and species of Codonanthe and Nema tan thus, the hypodermis was 2-12 cells thick. For example, C. elegans and N. hirtellus had a 2-3 cell thick hypodermis, C. luteola and N. fissus had a 5-& cell thick hypodermis, and C. carnosa and C. paula had a 10-12 cell thick hypodermis in the midvein area.

A uniseriate palisade mesophyll was adaxial to the hypodermis and consisted of elongated parenchyma cells oriented perpendicular to the blade surface. Numerous chloroplasts occurred along the anticlinal and abaxial periclinal walls. Spongy mesophyll was located abaxial to the palisade mesophyll and consisted of isodiametric to irregularly-shaped parenchyma cells. The cells contained few chloroplasts that were smaller than palisade mesophyll chloroplasts. Many large intercellular spaces were present. Depending upon the location on the blade and the species of Codonanthe and Nematanthus , the spongy mesophyll was 2-10 cells thick. For example, N. strigillosus had a 2-5 cell spongy mesophyll while C. digna had a 7-10 cell spongy mesophyll.

The midrib and secondary veins often protruded from the lamina and consisted of collateral vascular bundles encircled by small, tightly-appressed parenchyma cells. Collenchyma often occurred abaxial to the vascular bundles, adjacent to the lower epidermis (e.g., C. gracilis). The vascular bundles were rounded (e.g., C. digna) to arc-shaped (e.g., N. crass if olius). Codonanthe caribaea displayed a large arc-shaped bundle and a small dorsally-located bundle in the midrib (Figure IV-3C).

Leaf Vascular Skeleton

Species of Codonanthe and Nema tan thus possessed leaves with pinnate venation (Figure IV-3D). The course of the single primary vein (i.e., midvein) was straight and its size diminished towards the leaf apex as secondary veins branched-off . Secondary veins diverged from the midvein in an opposite, subopposite and/ or alternate arrangement and at moderate angles of ^5° to 65°. The course of the secondary veins was a series of prominent arches extended towards the leaf margins, upturned and gradually diminished apically inside the margin to tertiary veins.

This eucamptodromous venation type (cf . , Hickey, 1973) had the secondary veins join superadjacent secondary veins via tertiary veins at acute angles.

Tertiary veins had a random reticulate pattern with variable angles of anastomoses. Tertiary veins often diverged from the petiolar vascular bundle while still within the petiole (Figure IV-3D) and traveled along the leaf margin upon entering the leaf blade (e.g., C. luteola). It was not possible to resolve higher order venation. Areoles were often imperfectly-developed, randomly-arranged and irregularly-shaped. Terminal veinlets were either absent or, if

present, were simple and linear (cf . , Hickey, 1973). One median, tertiary vein and 1-2 lateral, smaller veins fused together before supplying marginal teeth (Figure IV-3F).

Sclereids often occurred along the petiolar vascular bundle (Figure TV-kF) and midvein (e.g., N. fritschii and N. gregarius), sometimes also traveling along secondary veins (e.g., N. perianthomegus, Figure IV-to). Styloids were grouped into small clusters parallel to the

99

higher order veins of all Nematanthus species observed, as well as in Codonanthe caribaea (Figure IV-4C) , C. grac il is and C. paula.

Discussion

Anatomical features of the stem, petiole, leaf mesophyll and leaf vascular skeleton were uniform among species of Codonanthe and Nematanthus. Only nodal anatomy proved to be taxonomically useful in distinguishing subgenera and sections of Codonanthe and Nematanthus.

In the genus Codonanthe, species of subgenus Codonanthe section Codonanthe (except C. carnosa and C. gracilis) possessed the unilacunar nodal configuration (Figures IV- 1 A & IV-1B), whereas species in subgenus Codonanthe section Spathuliformae and subgenus Codonanthella displayed the trilacunar, split-lateral nodal anatomy (Figures IV-1C to IV-1F & Figure IV-2). Although all species of Codonanthe have 2-4 mm thick stems (cf. , Table II-l), C. devosiana, C. digna and C. paula of subgenus Codonanthe section Codonanthe maintained the smallest stem size of ca. 2 mm thick and shorter leaf blade lengths of 20-40 mm.

In the genus Nematanthus , N. gregarius, N. nervosus , N. strigillosus and N. wettsteinii had the unilacunar nodal anatomy, whereas N. crass if olius, N. fissus, N. fritschii, N. hirtellus, N. maculatus and N. perianthomegus possessed the trilacunar, split-lateral nodal configuration. The former four Nematanthus species consistently displayed 2-4 mm thick stems, 4-10 mm long petioles and 20-40 mm long leaf blades while the latter six species had 5-9 mm thick stems, 10-50 mm long petioles and 40-120 mm long leaf blades (cf. , Table II-l).

The occurrence of the unilacunar nodal anatomy is apparently correlated with the smaller stem and leaf size in Codonanthe and

100

Nema tan thus species. In reference to epiphytes that are very thin-stemmed, Wiehler ( 1979b: p. 115) states that "there is just not enough space left in the small node for either lateral lacunae in the stele or lateral traces in the cortex." The single leaf trace appears to be sufficient in fulfilling the vascular requirements of the small leaves. Thus, the structure and size of the stem may provide an explanation of the occurrence of the unilacunar nodal anatomy.

Howard (1970) reported nodal vascular pattern changes when wild plants of Alloplectus ambiguus were grown under cultivation. Originally-collected, split-lateral trace plants were observed to possess two separate trilacunar nodes when cultivated in a greenhouse. Species of Godonanthe and Nematanthus sampled in this study were only cultivated in a growth room and it is not known how these plants would react if they were placed under greenhouse or natural conditions.

The presence of water-filled hypodermal cells (Figure IV-3B) within the leaf blade of Codonanthe and Nematanthus species relates well with their epiphytic habit. Occurring adaxially to the palisade mesophyll, the hypodermis is derived from the protoderm (Esau, 1965)1 i.e., the primary meristem which develops into the epidermis, and evidently functions in the storage of water. Epiphytes usually do not have access to the readily-available water source of the forest floor and must possess some means of water storage and conservation. Yellowing, old leaves were observed as enlarged and swollen with water in such taxa as C. devosiana ( Wiehler, 1979b) and C. luteola (Yuen, personal observation). In a sense, whole leaves were serving as water-storage organs.

Figure IV-1 . Nodal anatomy of species of Codonanthe.

A. C. digna, transverse section of stem at intern ode, X350.

B. C. digna, transverse section of unilacunar node with leaf

trace extending into cortex. Note prismatic crystals associated with pith in lacunae and cortex adjacent to leaf trace, X350.

C. C. corniculata, transverse section of trilacunar node with

lateral leaf trace occurring in cortex, X350*

D. C. corniculata, transverse section of trilacunar node with

lateral leaf trace dividing in half, X350«

E. C. corniculata, transverse section of trilacunar node with

split-lateral leaf trace diverging towards leaf, X350.

F. C, carnosa, tangential section of node with lateral leaf

trace splitting towards leaf base, X350«

L02

t*r ~K- C, v. " ■

IP

r^::^JS^<iz-

th

r-

- ■• -> -"v-Ao* i v4L>*<v'itV ^?:^^v- ;■•" '-* V** -■«'*'•' ■*<■;:■

Figure IV-2. Transverse sections of the node of Cod on an the corniculata, X80.

A. Internode prior to divergence of leaf traces.

B. Median and lateral leaf traces diverging from the vascular

cylinder.

G. Lateral leaf trace "beginning to split in half and median leaf trace continuing to separate from vascular cylinder.

D. Split-lateral leaf traces traveling through cortex towards

the median leaf traces.

E. Split-lateral leaf traces converging upon median leaf

trace.

F. Median leaf trace enters petiole with two split-lateral

leaf traces approaching the leaf abscission zone.

104

'"6-' •"*>:-**.•■•*

B

..«*.*

-■ -/*?"*>

•W*

&tfftl

3"

* •

t '«*

. -

E '

Figure IV-3. Leaf anatomy of species of Codonanthe and Nematanthus.

A. N. wettsteinii, transverse section of petiole with

arc-shaped vascular "bundle, X350.

B. C. digna, transverse section of leaf at the margin. Note "multiple layer of hypodermal cells, X350.

C. C. caribaea, transverse section of leaf midrib with an "unusual double arc-shaped vascular bundle, X350.

D. C. carnosa, clearing of leaf with xylary elements of

secondary veins diverging from midvein, XI 80.

E. N. strigillosus, clearing of leaf displaying leaf apex

innervated by midvein and smaller lateral veins, XI 80.

F. C. carnosa, clearing of leaf with two lateral higher order

veins joining a median tertiary vein at the leaf margin, XI 80.

106

-x

B

b%

Vfl

VtSfrSXt' f \- ,

^«- -- ■ ; -■ ...

\ i

«k> WW

<#t-

Figure IV-4. Crystals and sclereids in species of Codonanthe and Nematanthus.

A. N. wettsteinii, transverse section of stem with prismatic

crystals in pith cells, XI 400.

B. C. corniculata, transverse section of stem with druses in

cortex cells, XI 400.

C. C. carihaea, transverse section of leaf with styloid

crystals associated with vascular bundles, XI 400.

D. N. perianthomegus , clearing of leaf with styloid crystals

associated with leaf venation, XI 80.

E. C. digna, transverse section of stem with sclereids

clustered in cortex, XI 400.

F. C. elegans, clearing of leaf with sclereids associated

with petiole vasculature, XI 80.

108

^

•

CHAPTER V POLLEN MORPHOLOGY

Introduction

The significance of pollen morphology as a taxonomic tool has "been recognized since the comprehensive palynological work of Wodehouse (l935» 1936). Light microscopy (LM) methods were used by Erdtman (1952) and Woods (1964) to examine and characterize the pollen of Gesneriaceae, and to distinguish between the pollen of Cyrtandroideae and Gesnerioideae, respectively. Melhem & Mouro (1973) also used LM to describe the pollen morphology of Brazilian species of Gesneria, Hypocyrta and Nematanthus.

Scanning electron microscopy (SEM) methods were utilized by Skog (1976) to observe the pollen of 27 species from the tribe Gesnerieae. Williams (1978) studied the pollen structure of the Neotropical Gesneriaceae in an attempt to support or refute the new classification system of Wiehler (1979b). Preliminary results of pollen surface features of 30 Neotropical gesneriads of Gesnerioideae were reported.

This preliminary study of the pollen morphology of God on an the and Nematanthus species was undertaken to uncover more characters of taxonomic utility. Only pollen surface features are presented as determined through LM and SEM. Pollen structure as determined through LM and transmission electron microscopy (TEM) will be addressed at a later time.

109

110

Materials and Methods

Pollen of God on an the and Nematanthus species was collected from live specimens cultivated in a growth room at the Department of Ornamental Horticulture, University of Florida. The growth room provided uniform conditions of 22-25 °C day temperature, 17-20 °C night temperature, ^4-000-6000 Lux fluorescent lighting and a fourteen hour daylength. Voucher specimens were deposited at the University of Florida herbarium (FLAS).

In the SEM preparation (after Hayat, 1978), nondehisced and dehiscing anthers were sampled, fixed overnight in 2% glutaraldehyde , dehydrated in a 20-100% ethanol series for 2 hours and critical point dried for 30 minutes. The dried anthers were pierced with a needle and pollen was sprinkled onto double-sticky tape that was mounted on an aluminum stub. The pollen was coated with a gold-palladium mixture, viewed with a Hitachi S-450 Scanning Electron Microscope and photographed with Polaroid Type 55 Positive/Negative film.

In the LM preparation, dehiscing anthers were sampled and pollen was mounted directly in a drop of Alexander's stain <•( 1969) • This differential stain preparation permitted the observation of pollen stainability (i.e., viability) and pollen structure. A Wild M-20EB Light Microscope equiped with an eyepiece micrometer was used to examine and measure the pollen specimens. Pollen size is presented as a mean value + the standard error of the mean (x + S.E.x).

Observations The basic descriptive terminology of pollen characters is according to Walker & Doyle (1975) and Moore & Webb (1978). SEM

Ill

photomicrographs of Nowicke & Skvarla (1977 » 1980) were consulted as a reference in the designation of pollen exine sculpturing types. Definitions of terms used in the text are "briefly reviewed "below.

Pollen aperture. Any thin or missing part of the exine which is independent of the exine pattern is called an aperture. Elongate, furrow-like apertures are known as colpi. Pollen with colpi located equidistantly on the equator and aligned with the polar axis are referred to as zonocolpate pollen. The area bordered by two colpi is the mesocolpium while the polar area of the pollen is the apocolpium.

Pollen shape. Pollen shape is globose (globe-shaped), isopolar (with two poles) and radios ymmetric (Figure V-1C). The outline of the pollen grain as seen in polar view is referred to as the amb. A polygonal pollen (angular in appearance) with the apertures situated in the angles of the amb is known as angulaperturate (Figure V-1D),

Pollen size. Small-sized pollen are 10-24 urn and medium-sized pollen are 25-^-9 urn for the longest pollen axis length.

Pollen wall stratification. The pollen wall is composed of an inner intine strata and an outer exine strata which is further subdivided into endexine and ektexine layers. Extexine consists of a foot-layer, rod-like columellae arranged perpendicular to the pollen surface, and a roof-like tectum (Figure V-1A).

Exine structure. Three basic exine structure types are tectate, semitectate and intectate (Figure V-1B). Tectate pollen may be further subdivided into tectate- imperforate pollen (without any holes in the tectum) and tectate-perforate pollen (with holes in the tectum). Semitectate pollen possess larger spaces or lumina in the tectum

112

providing a reticulated surface appearance. Intectate pollen have no tectum but display rod-like columellae.

Exine sculpturing. Exposed surface features of the pollen wall are referred to as exine sculpturing. Some exine sculpturing types are psilate (smooth), foveolate (pitted), fossulate (grooved), verrucate (warty), rugulate (elongate sculpturing elements irregularly

distributed tangentially over the pollen surface) , reticulate (sculpturing elements forming an open nerwork or reticulum over the pollen surface) and spinulose (spiny).

GENUS Codonanthe (Martius) Hans te in

Pollen grains were solitary as monads, globose, isopolar and radiosymmetric with three zonate colpi (i.e., 3-zonocolpate except C. chiricana with some 4- and 5-zonocolpate pollen; Figures V-6C & V-12A). Apertures were simple without a margo (Figure V-12E). Polar views displayed a circular to slightly triangular, angulaperturate amb with convex mesocolpia and retiulate apocolpia. Equatorial views yielded circular to slightly elliptic profiles. SUBGENUS Codonanthe

Nine known species of this subgenus were examined.

SECTION Codonanthe. Five species were studied (Figures V-2 & V-3) : C. carnosa (Gardner) Hanstein, C. devosiana Lemaire, C. digna Wiehler, C. gracilis (Martius) Hanstein and C. paula Wiehler.

Pollen size was small with an 18.1 + .75 um polar axis (P) and an 18.5 + .35 urn equatorial diameter (e). The P/E index of 0.98 designates an oblate spheroidal pollen shape (Figure V-1C). Exine structure was tectate-perf orate. Exine sculpturing was fossulate for

U3

C. carnosa, foveolate for C. devosiana and C. paula, and finely reticulate for C. digna and C. gracilis.

SECTION Spathuliformae L. B. Smith. Four species were studied (Figures V-4 & V-5) ' C. calcarata (F. A. W.- Miquel) Hanstein, C. corniculata Wiehler, C. crass if olia (Focke) Morton and C. uleana Fritsch.

Pollen size was medium with a 26.7 + .93 um polar axis (p) and a 29.6 + .94 urn equatorial diameter (e). The P/E index of 0.90 designates an oblate spheroidal pollen shape (Figure V-1C). Exine structure was tec tate-perf orate. Exine sculpturing was

spinulose-verrucate for C. calcarata, spinulose-reticulate for C. corniculata, spinulose-irregularly microreticulate for G. crass if olia and rugulate for C. uleana. SUBGENUS Codonanthella Wiehler

Five known species of this subgenus were examined (Figures V-6 & V-?) : C. caribaea Urban, C. chiricana Wiehler, C. elegans nomen nudum (to be described by Wiehler, 1982), C. luteola Wiehler and C. macradenia Donnell-Smith.

Pollen size was medium with a 29.7 ± .60 um polar axis (p) and a 32.6 + .94 um equatorial diameter (e). The P/E index of 0.91 designates an oblate spheroidal pollen shape (Figure V-1C). Exine structure was tectate-perf orate (Figure V-12C). Exine sculpturing was reticulate-secondarily foveolate for C_. caribaea, slightly

spinulose-microreticulate for C. chiricana and C. luteola,

spinulose-irregularly microreticulate for C. elegans and

spinulose-microreticulate for C. macradenia.

114

GENUS Nematanthus Schrader

Pollen grains were solitary as monads, globose, isopolar and radiosymmetric with three zonate colpi (i.e., 3-zonocolpatei except N. hirtellus with some 4-zonocolpate pollen; Figure V-12B). Apertures were simple with a margo (Figure V-12F). Polar views displayed a triangular, angulaperturate amb with straight to convex mesocolpia and nonreticulate to reticulate apocolpia. Equatorial views yielded circular to strongly elliptic profiles.

Ten species placed in this genus were examined (Figures V-8 to V-ll): N. crass if ol ius (Schott) Wiehler, N. fissus (Vellozo) L. Skog, N. fritschii Hoehne, N. gregarius D. Denham, N. hirtellus (Schott) Wiehler, N. maculatus (Fritsch) Wiehler, N. nervosus (Fritsch) H. E. Moore, N. perianthomegus (Vellozo) H. E. Moore, N. strigillosus (Martius) H. E. Moore and N, wettsteinii (Fritsch) H. E. Moore.

Pollen size was medium with a 25.3 + «80 urn polar axis (p) and a 25.5 + .48 urn equatorial diameter (E). The P/E index of 0.99 designates an oblate spheroidal pollen shape. Exine structure was tectate-perf orate to semitectate (Figure V-12D). Exine sculpturing was reticulate with foveolate reticula in the mesocolpia of all Nematanthus species. Nematanthus crass if ol ius, N. fritschii and N. perianthomegus possessed narrow reticula and the other seven Nematanthus species exhibited relatively wider reticula. Nematanthus gregarius, N. nervosus, N. strigillosus, N. wettsteinii and N. hirtellus possessed reticulate apocolpia, N. fritschii had sparcely foveolate apocolpia and N. crass if ol ius, N. fissus, N. maculatus and N. perianthomegus exhibited psilate apocolpia.

115

Discussion

Species of Godonanthe and Nema tan thus possess pollen that are solitary as monads, isopolar, radiosymmetric, globose-oblate spheroidal and 3-zonocolpate (except C, chiricana and N. hirtellus with some k- and 5-zonocolpate pollen; Figure V-6G, V-12A and V-12B) with an angulaperturate amb, but differ in some key aspects. Godonanthe pollen have apertures without a margo (Figure V-12E), a basically circular polar configuration, a tectate-perforate exine structure (Figure V-12C) and various degrees of finely reticulate exine sculpturing, whereas Nema tan thus pollen have apertures with a margo (Figure V-12F), a basically triangular polar configuration, a tectate-perforate and semitectate (Figure V-12D) exine structure and coarsely reticulate exine sculpturing.

Walker (1975) postulates that primitive angiosperm pollen was psilate with a tec tate- imperforate exine structure. The evolutionary trend was the succesive dissolution of tectum areas in the tectate-imperf orate exine to form tectate-perforate, semitectate and intectate exine configurations (Figure V-1B; Walker, 197*0 •

In the genus Godonanthe, exine sculpturing differences are noted among sections of subgenus Codonanthe. Species of subgenus Godonanthe section Godonanthe have foveolate, fossulate and finely reticulate exines, whereas species of subgenus Godonanthe section S pathul if ormae and subgenus Codonanthella possess verrucate, rugulate to reticulate and microreticulate pollen surfaces.

The foveolate and fossulate exine patterns of C. carnosa, C. devosiana and C, paula are possible the preliminary stages of tectum dissolution of an ancestral psilate exine type, with the pollen surface

116

simply appearing pitted and grooved. The finely reticulate exine sculpturing of C. digna and C, gracilis may be a more advanced stage of tectum dissolution, but the pattern is still a simple network of reticula. Further tectum dissolution appears to occur with the

rugulate and reticulate-secondarily foveolate exine patterns of C. uleana and C. caribaea that lack spines, the slightly

spinulose-microreticulate exine types of C. chiricana and C. luteola that have few small spines, and the various spinulose-verrucate and spinulose-microreticulate exine configurations of C. calcarata, C. corniculata, C. crass if olia, C. elegans and C. macradenia that possess distinct spines.

Species of subgenus Godonanthe section Codonanthe have small-sized pollen and are diploids (n = 8; Wiehler, 1975) « while species of subgenus Codonanthe section Spathul if ormae and subgenus Codonanthella

possess medium-sized pollen and are tetraploids (n = 16; Wiehler, 1975), except C. caribaea (n = 8) and C. luteola (n = 8, 16). This difference in pollen size is possibly correlated to the ploidy level of the species and the related to the gigas effect of polyploidy (Stebbins, 1971).

In the genus Nema tan thus , species possess reticulate exine sculpturing with foveolate reticula in the mesocolpia. The narrow reticula of N. crass if olius, N. fritschii and N. per ianthomegus are apparently correlated to the semitectate exine structure, whereas the

wider reticula of the other seven Nematanthus species correspond to the tectate-perforate structure type. Since tectate-perforate and

semitectate pollen are contiguous stages in the trend of pollen

117

evolution (Walker, 197*0 » it is conceivable that two exine structural

types occur in one genus.

Reticulate apocolpia are present in N. gregarius, N. nervosus , N.

strigillosus, N. wettsteinii and N. hixtellus, whereas very sparcely foveolate to psilate apocolpia occur in N. crass if olius, N. fissus, N. fritschii, N. maculatus and N. perianthomegus .

Although species of Nematanthus have medium-sized pollen, they are

diploids (n = 8; Skog, 1981 ) and apparently do not follow the gigas

effect of polyploidy of Codonanthe species, that is, medium-sized

pollen denoting tetraploidy. Nematanthus species are distinct from

species of Codonanthe with respect to pollen size and ploidy level.

Figure V-l . Diagrams depicting the pollen terminology used in the text (according to Walker & Doyle, 1975) •

A. Cross-section of pollen wall illustrating the strata of a tec tate- imperforate pollen.

E. Evolutionary trends in exine structure types.

Cross-sectional views of pollen wall to the left and surface views to the right. Arrows 1-3 indicate direction and sequence of exine structure evolution and arrows 4-5 depict possible reversibility of the evolutionary trend.

C. Isopolar-radiosymmetric, globose-spheroidal and

globose-oblate pollen grains, respectively, that are zonocolpate.

D. Pollen grains with polygonal, angulaperturate ambs.

119

tectum —| 1 1 1 1 1 1 i 1 columellae J 1 1 1 II 1 foot- layer	a:	MJUUl intectate 4 EUUli semitectate 4i4	u o c O o o O o o ■
[ J ektexine [ ~~] endexine | intme	A
		ffiE	"■ n ■" u °oO°o ° o °
		tectate -perforate jl5	^ a n
	D	]DD_nac tpr tntp-imnerf orate

<2_£

Figure V-2. Pollen morphology of species of Codonanthe subgenus God on an the section Codonanthe.

A. C. carnosa, pollen grain, X3000.

B. C. carnosa, fossulate exine sculpturing, X10.000.

C. C. devosiana, pollen grain, X3000.

D. C. devosiana, foveolate exine sculpturing, X10,000.

E. C. digna, pollen grain, X3000.

F. C. digna, finely reticulate exine sculpturing, X10.000.

121

Figure V-3. Pollen morphology of species of Codonanthe subgenus Cod on an the section Codonanthe.

A. C. gracilis, pollen grain, X3000.

B. C. gracilis, finely reticulate exine sculpturing, X10.000.

C. C. paula, pollen grain, X3000.

D. C. paula, foveolate exine sculpturing, XIO.OOO.

123

tJ,.f>4B.

Figure V-4. Pollen morphology of species of Codonanthe subgenus Cod on an the section Spathuliformae.

A. C. calcarata, pollen grain, X2000.

B. C. calcarata, spinulose-verrucate exine sculpturing,

X10.000.

C. C. corniculata, pollen grain, X2000.

D. C. corniculata, spinulose-reticulate exine sculpturing,

X10.000.

125

Figure V-5. Pollen morphology of species of Godonanthe subgenus Godonanthe section Spathul if ormae .

A. C. crass if olia, pollen grain, X2000.

B. C. crass if olia, spinulose-irregularly microreticulate exine

sculpturing, XlO-,000.

G. C. uleana, pollen grain, X2000,

D. C. uleana, rugulate exine sculpturing, X10.000.

12?

Figure V-6. Pollen morphology of species of Codonanthe subgenus Codonanthella.

A. C. caribaea, pollen grain, X2000.

B. C. caribaea, reticulate-secondarily foveolate exine

sculpturing, X10.000.

C. C. chiricana, pollen grain, X1500.

D. C. chiricana, slightly spinulose-microreticulate exine

sculpturing, X10.000.

E. C. elegans, pollen grain, XI 500.

F. C. elegans, spinulose-irregularly microreticulate exine

sculpturing, X10.000.

129

Figure V-7. Pollen morphology of species of Godonanthe subgenus Codonanthella.

A. C. luteola, pollen grain, XI 500.

B. C. luteola, slightly spinulose-microreticulate, X10.000.

C. C. macradenia, pollen grain, X2000.

D. G. macradenia, spinulose-microreticulate, X10,000.

131

Figure V-8. Pollen morphology of species of Nema tan thus (section Nema tan thus , cf. CONCLUSION and APPENDIX) . ~~~

A. N. crass if ol ius, pollen grain, X2000.

B. N. crassifolius, reticulate exine sculpturing with narrow,

foveolate reticula in the mesocolpia, X10.000.

C. N. fissus, pollen grain, X2500.

D. N. fissus, reticulate exine sculpturing with wide,

foveolate reticula in the mesocolpia, X10.000.

E. N. frits chii, pollen grain, X2500.

F. N. fritschii, reticulate exine sculpturing with narrow,

foveolate reticula in the mesocolpia, X10,000.

133

Figure V-9. Pollen morphology of species of Nema tan thus (section Nema tan thus , cf. CONCLUSION and APPENDIX"^ ™

A. N. hirtellus, pollen grain, X2500.

B. N. maculatus , pollen grain, X2500.

C. N. perianthomegus, pollen grain, X2000.

D. N. perianthomegus, reticulate exine sculpturing with

narrow, foveolate reticula in the mesocolpia, XI 0,000.

135

Figure V-10. Pollen morphology of species of Nematanthus (section D Parvifolius, cf. CONCLUSION and APPENDIX).

A. N. gregarius, pollen grain, X2500.

B. N. ^regarius, reticulate exine sculpturing with wide,

foveolate reticula in the mesocolpia, XIO.OOO.

C. N. nervosus, pollen grain, X2500.

D. N. nervosus , reticulate exine sculpturing with wide,

foveolate reticula in the mesocolpia, X10,000.

137

Figure V-ll. Pollen morphology of species of Nematanthus (section ° Parvifolius, cf. CONCLUSION and APPENDIX).

A. N. strigillosus, pollen grain, X2500.

B. N. strigillosus, reticulate exine sculpturing with wide,

foveolate reticula in the mesocolpia, X10,000.

C. N. wettsteinii, pollen grain, X3000.

D. N. wettsteinii, reticulate exine sculpturing with wide,

foveolate reticula in the mesocolpia, X10.000.

139

Figure V-12. Varying features of pollen morphology and exine structure.

A. C, chiricana, 5-apertured pollen, XI 500.

B. N. hirtellus, 4-apertured pollen, X2500.

C. C. crass if olia, profile of tectate-perforate pollen,

X10.000.

D. N. perianthomegus, profile of semitectate pollen, X10.000,

E. C. macradenia, aperture without margo, X3400.

F. N. hirtellus, aperture with margo, X3500.

141

CHAPTER VI CONCLUSION

Lawrence (1951 ) states that a genus is a taxonomic and "biological category and should consist of morphologically similar species as well as be indicative of genetic relationships. Codonanthe and Nematanthus share many characters of taxonomic significance, including an identical basic chromosome number, similar fleshy fruit types and geographical distribution, an exclusively epiphytic growth habit, and numerous morphological and anatomical traits of the stem and leaf (Table VI-l), Since the first intergeneric cross was made in 1977 (Saylor, 1978a), several fertile X Cod onatan thus hybrids have been produced (Saylor,

1978b, 1979. 1981; Yuen, personal hybridizations, 1982), demonstrating a kinship between Codonanthe and Nematanthus species. Should the genera Codonanthe and Nematanthus be united based upon these results?

Flower type and pollination ecology of Codonanthe and Nematanthus species are very distinct. Species of Codonanthe have an obliquely funnelform-ventricose corolla that is primarily white and is pollinated by Euglossine bees, whereas species of Nematanthus have a pouched corolla that is basically orange, red, pink or yellow and is presumably pollinated by hummingbirds. Possession of such differing corolla types and pollinators reproductively isolates these two genera though species of Codonanthe subgenus Codonanthe section Codonanthe occur sympatrically with Nematanthus species. Natural hybrids between

142

143

species of Codonanthe and Nematanthus have not been reported. Also, God on an the pollen have apertures without a margo, a basically circular polar configuration, small- and .medium-sized pollen (10-24 & 25-49 urn, respectively), a tectate-perf orate exine structure and various degrees of finely reticulate exine sculpturing, whereas Nematanthus pollen have apertures with a margo, a basically triangular polar shape, medium-sized pollen, a tectate-perf orate and semitectate exine structure and coarsely reticulate exine sculpturing. It appears that though Codonanthe and Nematanthus are closely related genera, they should remain as distinct entities since they differ in these significant traits.

For Codonanthe, species of subgenus Codonanthella share many significant taxonomic traits with species of subgenus Codonanthe section Spathuliformae and relatively few features with species of subgenus Codonanthe section Codonanthe (Table VI-2). Species of subgenus Codonanthe section Codonanthe have orange berries, a diploid chromosome number of n=8 and small pollen grains (10-24 urn), a unilacunar nodal anatomy (except C. carnosa and C. grac il is ) , multicellular nonglandular trichomes with radially-arranged basal epidermal cells, glandular trichomes with a 4-celled head, and a guard cell area index of 458 urn 2, lack extrafloral nectaries, and are indigenous to southeastern Brazil. Species of subgenus Codonanthe section Spathuliformae and subgenus Codonanthella have red, pink, purple or yellow-green berries or fleshy capsules, a tetraploid chromosome number of n=l6 (except C. caribaea is a diploid and C. luteola has diploid and tetraploid representatives) and medium pollen grains (25-49 urn), a trilacunar, split-lateral nodal anatomy, unicellular nonglandular trichomes with randomly-arranged basal epidermal cells (except C. caribaea), glandular trichomes with a

144

2-celled head (except C, caribaea) , and a guard cell index of 796 urn ^ and 936 urn , possess extrafloral nectaries, and are geographically widespread from southern Mexico through Central America to northern South America. Based upon these observations, it is acknowledged that further studies are required before any final conclusions are made on the relationships of the infrageneric taxa of Codonanthe.

There are two morphologically distinct groups of Nematanthus species (Table VI-3). Nematanthus crass if ol jus, N. fissus, N.

fritschii, N. hirtellus, N. maculatus and N. perianthomegus have a shrubby growth habit with thick stems (5-9 mm diameter), long petioles (10-50 mm length), large blades (4-12 cm length), a trilacunar, split-lateral nodal anatomy, glandular trichomes with a 4-celled head and unicellular or multicellular body, anisocytic stomata, pollen with psilate apocolpia (except N. hirtellus) , and resupinate flowers that are erect or hanging from the leaf axil. N. gregarius, N. nervosus , N. strigillosus and N. wettsteinii have a viny growth habit with thin stems (2-4 mm), short petioles (4-10 mm length), small blades (2-4 cm length), a unilacunar nodal anatomy, glandular trichomes with a more-than-4-celled head and unicellular body, anisocytic and helicocytic stomata, pollen with reticulate apocolpia, and

nonresupinate flowers that are erect in the leaf axil. Based upon these observations, two new sections are established for Nematanthus — section Nematanthus for the former group and section Parvif ol ius for the latter group.

Codonanthe and Nematanthus possess several contrasting features that are important in determining possible modes of speciation. Species of subgenus Codonanthe section Codonanthe are exclusively

145

located in southeastern Erazil and separated from species of subgenus Codonanthe section Spathuliformae and subgenus Codonanthella by a savanna and scrub expanse (cf . , Strahler, 1967; Walter, 1973). Codonanthe species, being epiphytes, are restricted to areas where their host trees occur, that is, regions of tropical evergreen and deciduous rain forests. The sizeable savanna and scrub expanse serves as a possible spatial or geographical isolating mechanism of these two disjunct groups (cf. , Grant, 1971, 1977).

In addition, species of subgenus Codonanthe section Codonanthe are diploid (n=8), whereas species of subgenus Codonanthe section Spathul if ormae and subgenus Codonanthella are tetraploids (n=l6; except C. caribaea is diploid and C. luteola is diploid or tetraploid). This difference in ploidy, theoretically, would not obstruct the interbreeding of species in the two groups nor the subsequent production of interspecific hybrids. It is the isolating mechanism of hybrid sterility (cf., Grant, 1977) that would hinder the establishment of future generations of interspecific hybrids in that these hybrids would be triploid and sterile. Stebbins (l97l) reports that polyploidy is indeed important in the diversification of tropical woody genera. Hence, varying ploidy levels and disjunct geographical distribution effectively isolate the species of these two groups and may lead to allopatric speciation.

Species of section Nematanthus may be reproductively isolated from species of section Parvifolius because the orientation of the flower effectively excludes pollen exchange between species of these two sections. Species of section Nematanthus possess flowers that are resupinate with anthers and stigma in the ventral position facing

146

upward, and pollen shedding and reception occurring on the lower surface of the pollinating agent. In contrast, species of section Parvifolius possess flowers that are nonresupinate with the anthers and stigma in the dorsal position facing downward, and pollen shedding and reception occurring on the upper surface of the pollinating agent. Hummingbirds are presumably the pollinating agents and deposition of Nema tan thus pollen is on the lower or upper surface of their beaks. If a hummingbird was to first visit a flower of a species in section Nematanthus , pollen would be deposited on the lower surface of its beak. Visiting another flower of a species in section Nematanthus would effect pollination because pollen reception is also from the lower surface of the hummingbird's beak, but visiting a flower of a species in section Parvifolius would not effect pollination because pollen reception is from the upper surface of the hummingbird's beak. Gross pollination between species of these two sections is unlikely due to the differing pollination mechanism, thus, possibly isolating these two taxa reproductively (cf . , Grant, 1971 , 1977).

14?

Table VI-1 . Key morphological and anatomical Cod on an the and Nematanthus.

CHARACTER

Codonanthe

characters of the genera

Nematanthus

1) FLOWER

a) Corolla Shape

b) Corolla Color

c) Anther

Connective

d) Anther

Dehiscence

2) POLLINATION AGENT

(presumed)

3) FRUIT

4) CHROMOSOME NUMBER

5) GEOGRAPHICAL

DISTRIBUTION

6) LEAF EPIDERMIS

MORPHOLOGY

a) Nonglandular

Trichomes

b) Glandular

Trichomes

c) Stoma ta Type

d) Extrafloral

Nectaries

7) POLLEN MORPHOLOGY

a) Margo around

Aperture

b) Polar View

c) Equatorial View

d) Pollen Size

e) Exine Structure

f) Exine

Sculpturing

funnel form white, yellow

broad

pores euglossine bees

berry, fleshy capsule

diploid (n=8), tetraploid (n=l6)

southern Mexico through Central America to northern South America; southeastern Brazil

unicellular,

multicellular 2- & 4-celled head;

unicellular body

anisocytic present & absent

absent

circular

(slightly triangular) circular to slightly

elliptic small (10-24 urn) &

medium (25-49 urn) tectate-perforate

psilate to finely reticulate

pouched

red, yellow, pink, orange

longitudinal slits hummingbirds

fleshy capsule diploid (n=8)

southeastern Brazil

multicellular

4- & >4-celled head;

unicellular & multicellular

body anisocytic, helicocytic absent

present

triangular

circular to strongly

elliptic medium (25-49 urn)

tectate-perforate &

semitectate coarsely reticulate

148

Table VI-2. Key morphological and anatomical characters of Cod on an the at the subgenus and section level.

SUBGENUS Codonanthe

CHARACTER

SECTION SECTION SUBGENUS

Codonanthe Spathuliformae Codonanthella

1) FRUIT

a) Type

b) Color

2) CHROMOSOME

NUMBER

berry orange

diploid (n=8)

3) GEOGRAPHICAL southeastern DISTRIBUTION Brazil

4) LEAF EPIDERMIS

MORPHOLOGY

a) Nonglandular

Trichome multicellular Cells

b) Nonglandular

Trichome radial (except Basal Cell C. grac il is ) Arrangement

c) Glandular 4-celled

Trichome Head

d) Extrafloral absent

Nectaries „

e) Guard Cell 458 urn

Area Index

5) NODAL unilacunar

ANATOMY (except

C. carnosa & C. gracilis)

small (10-24 urn)

berry red, pink, purple

tetraploid (n=l6)

Central America to South America (excluding southeastern Brazil)

fleshy capsule red, pink, purple; yellow-green

tetraploid (n=l6); (except C. caribaea, n=8; C. luteola, n=8, 16)

southern Mexico through Central America to northern South America

unicellular

random

2-celled

present 796 urn2

trilacunar , split-lateral

unicellular (except C. caribaea)

random

2-celled (except C. caribaea)

present (except

C, caribaea) 936 urn2

trilacunar, split-lateral

6) POLLEN SIZE

medium (25-4-9 um) medium (25-49 urn)

149

Ta"ble VI-3. Key morphological and anatomical characters of Nema tan thus at the section level.

CHARACTER

SECTION Nematanthus

SECTION Parvifolius

1) GROWTH HAEIT

2) STEM SIZE

(diameter)

3) LEAF SIZE (length)

a) Petiole

b) Blade

4) FLOWER

ORIENTATION

5) LEAF EPIDERMIS

MORPHOLOGY

a) Glandular

Trichome Head

b) Glandular

Trichome Eody

c) Stomata Type

6) NODAL ANATOMY

7) POLLEN APOCOLPIA

shrubby 5-9 mm

10-50 mm 4-12 cm

resupinate

4-celled

unicellular,

multicellular anisocytic

trilacunar, split-lateral

psilate (except N. hirtellus)

vmy 2-4 mm

4-10 mm 2-4 cm

nonresupinate

>4-celled

unicellular

anisocytic, helicocytic

unilacunar

reticulate

APPENDIX SYNOPSIS OF INFRAGENERIC TAXA OF CODONANTHE AND NEMATANTHUS

Description of the Genera, Subgenera and Sections

GENUS Cod on an the (Martius) Hanstein, Linnaea 26: 209. April 1854

('1853' )i nom. cons. Hypocyrta section Codonanthe Martius, Nova Genera et Species

Plantarum 3: 49. 1829.

Type: Hypocyrta gracilis Martius. (=Codonanthe gracilis

( Mar t ius) Hanstein). Coccanthera C. Koch & Hanstein, Index Seminum in Horto Regio

Botanico Berolinensi 1855: Appendix 17. I855.

Type: C. Hookerana G. Koch & Hanstein. (^Codonanthe gracilis

(Martius) Hanstein). Codonanthopsis Mansfeld, Repertorium Specierum Novarum Regni

Vegetabilis 36: 120. 1934.

Type: C. Ulei Mansfeld. (=Codonanthe Ulei (Mansfeld)

H. E. Moore).

Type species: Codonanthe gracilis (Martius) Hanstein.

Vine-like or shrub-like epiphytes sparsely branched. Roots adventitious and fibrous; often mutual is tically associated with ants with the roots providing structural support to the ant nests. Stems woody, erect, repent or pendulous, 2-9 mm in diameter, with extrafloral nectaries frequently produced near compressed nodes. Leaves opposite, decussate or 2-ranked, equal or subequal in a pair; petioles 4-19 mm in length; blades entire, sinuate or serrulate towards the apex, ovate, oval, obovate or elliptic in shape, with some species 2-4 cm and some 4-12 cm in length, reddish, mammillate extrafloral nectaries on the abaxial surface present or absent, mostly pubescent, usually fleshy and thick with a prominent dorsal hypodermis; estipulate. Inflorescences are cymes reduced to one or a few flowers borne in upper leaf axils; peduncles very short if present; bracts absent; pedicels 3-25 mm in length. Flowers having a calyx deeply 5-parted with subequal to very unequal lobes, linear to lanceolate, or bilabiate, 2-10 mm in length, with the dorsal calyx lobe recurved about the spur, red extrafloral

150

151

nectaries often in sinuses of the calyx lobe margins; corolla white and yellow, sometimes flushed with yellow, brown, pink, red, lilac or deep purple spots or lines on the lower surface of the throat or outer areas, obliquely funnelform-ventricose, 1-4 cm in length, base rounded to prominently spurred, then gradually or abruptly broader towards the throat, or somewhat dor si-ventr ally compressed and arched/ grooved, limb of 5 rounded, spreading lobes, bilabiate with the upper lobes shorter than the three lower lobes; stamens k, filaments epipetalous and didynamous, distinct or connate at the base, recoiled or lowered towards the ventral surface of the corolla after pollen is shed, anthers connivent in pairs by tips or margins in a square at anthesis, sometimes separating after anthesis, laterally oblong with connectives narrow or often broad, anther sacs more or less separated, dehiscing by round or ellipsoid pores; ovary superior, unilocular, with 2 parietal placentas ©villiferous on the inner side, ovules numerous and anatropous, style terete and slender, elongating after pollen is shed, stigma stomatom orphic to bilobed; nectary or disc of 2 large, connate glands positioned adjacent and dorsal to the ovary. Fruit a fleshy capsule, dehiscent or tardily dehiscent by 2 valves, or a berry with distinct sutures, globose, ovoid or compressed, red pink, orange, purple or yellow-green, placentas fleshy; seeds often with thickened fleshy funicles that are entirely or partially surrounded by a translucent or opaque aril, fusiform or ellipsoid, longitudinally or obliquely striated, red, pink or yellow. Chromosome number as x = 8 with n = 8 & 16. Distribution from southern Mexico through Central America to northern South America, and southeastern Brazil (Moore, 1973a; Skog, 1978; Wiehler, 1979b).

152

SUBGENUS Godonanthe

Fruit a globose berry.

SECTION Codonanthe

SECTION Codonanthe. H. E. Moore, Baileya 19: 9. 1973.

Fruit an orange berry.

Type species: Codonanthe gracilis (Martius) Hanstein.

Additional species: C. carnosa (Gardner) Hanstein, C. devosiana

Lemaire, C. digna Wiehler, C. paula Wiehler.

SECTION Spathuliformae L. B. Smith, Bulletin of the Torrey Botanical Club 60: 657. 1933 .

Fruit a red, pink or purple berry.

Type species: Codonanthe calcarata (F. A. W. Miquel) Hanstein.

Additional species: C. corniculata Wiehler, C. crass if olia (Focke)

Morton, C. uleana Fritsch.

SUBGENUS Codonanthella Wiehler, Selbyana 6 (in press). 1982.

Fruit a yellow-green, pointed, fleshy capsule.

Type species: Codonanthe luteola Wiehler.

Additional species: C. caribaea Urba/i, C. chiricana Wiehler, C. macradenia Donn ell-Smith.

153

GENUS Nematanthus Schrader, Gottingische gelehrte Anzeigen 1821(2): 718. 1821. Hypocyrta Martius, Nova Genera et Species Plantarum 3: 48. 1829.

Type species: Nematanthus crass if olius (Schott) Wiehler.

Shrub-like or vine-like epiphytes sparsely branched. Roots fibrous, often adventitious at compressed nodes. Stems woody, erect or repent, with some species 2-4 mm or 5_9 mm in diameter. Leaves opposite, decussate or 2-ranked, equal or subequal in a pair; petioles either 4-10 mm or 10-50 mm in length, slightly furrowed adaxially, green to red and maroon; blades entire, serrulate or slightly crenate towards the apex, ovate, oval, obovate or elliptic in shape, with some species 2-4 cm and some 4-12 cm in length, sometimes red or maroon-splotched on the abaxial surface, mostly pubescent, usually fleshy and often coriaceous with a notable dorsal hypodermis; estipulate. Inflorescences are reduced cymes of one or a few flowers in upper leaf axils; peduncles very short if present; bracts absent; pedicels either 3-25 mm or 25-200 mm in length, usually exceeding subtending leaves; orientation of flowers nonresupinate, resupinate or pendulous. Flowers having a calyx deeply 5- parted with subequal to very unequal lobes, ovate to elliptic, sometimes toothed, 10-30 mm in length, with dorsal calyx lobe recurved about the spur; corolla scarlet, red, pink, orange or yellow with maroon stripes, erect or oblique in the calyx, mildly to strongly ventricose, 2-6 cm in length, often with a short spur, narrow above the base, gradually expanding to a broad, laterally compressed throat or quickly widening to form a pouch and abruptly narrowing to form a constricted throat (hypocyrtoid) , limb of 5 rounded, small lobes; stamens 4, filaments epipetalous and didynamous, distinct or connate at the base, recoiled towards the

1&

corolla base after pollen is shed, anthers coherent in a rectangle, laterally oblong in shape, with elliptical connectives, dehiscing by slits; ovary superior, unilocular, with 2 parietal placentas ovuliferous on the inner side, ovules numerous and anatropous, style terete and slender, elongating after pollen is shed, stigma stomatomorphic; nectary or disc of 2 large, connate glands positioned adjacent and dorsal to ovary. Fruit a fleshy capsule, dehiscent or tardily dehiscent by 2 valves, sometimes laterally compressed and ovoid, placentas fleshy; seeds often with thickened fleshy funicles that are entirely or partially surrounded by a translucent or opaque aril, fusiform or ellipsoid, longitudinally or obliquely striated, often shiny brown. Chromosome number as x = 8 with n = 8. Distribution localized in south eastern Brazil (after Moore, 1971, 1973b). SECTION Nematanthus

Shrub-like epiphytes. Stems erect, 5-9 mm in diameter, with nodes trilacunar. Leaves with petioles green to red and maroon, 10-50 mm in length; blades entire, serrulate or slightly crenate towards the apex, 4-12 cm in length, sometimes red or maroon-splotched on the abaxial surface, glandular trichomes with a 4-celled head and unicellular or multicellular-uniseriate body cells, stomata anisocytic. Flowers resupinate or pendulous with pedicels either 3-25 or 25-200 mm in length; corolla scarlet, red, pink, orange or yellow with maroon stripes, mildly to strongly ventricose or pouched.

Type species: Nematanthus crass if olius (Schott) Wiehler. Additional species: N. fissus (Vellozo) L. Skog, N. fritschii Hoehne, N. hirtellus (Schott) Wiehler, N. maculatus (Fritsch) ¥iehler, N. perianthomegus (Vellozo) H. E. Moore.

155

SECTION Parvifolius Yuen, sect. nov.

Vine-lUce epiphytes. Stems repent, 2-k mm in diameter, with nodes unilacunar. Leaves with petioles green, 4-10 mm in length; blades entire, narrowly ovate to widely elliptic, 2-k cm in length, sometimes red on the abaxial surface, glandular trichomes with more-than-4-celled heads and only unicellular body cells, stomata anisocytic and helicocytic. Flowers nonresupinate with pedicels 3-25 mm in length; corolla red, orange or yellow, pouched.

Type species: Nematanthus wettsteinii (Fritsch) H. E. Moore.

Additional species: N. gregarius D. Denham, N. nervosus (Fritsch) H. E. Moore, N. strigillosus (Martius) H. E. Moore.

156

Diagnostic Key to the Genera, Subgenera and Sections

A. Corolla obliquely funnelform or mildly ventricose, white, pink, lilac or deep purple; flowers nonresupinate; fruit a berry or fleshy capsule; extrafloral nectaries pr.esent or absent; hairs unicellular or multicellular-uniseriate on leaves; chromosome number n = 8 & 16; distribution from southern Mexico through Central America to northwestern South America, and southeastern Brazil GENUS Codonanthe

B. Fruit a globose berry SUBGENUS Codonanthe

C. Fruit an orange berry SECTION Codonanthe

C. Fruit a red, pink or purple berry

SECTION Spathuliformae

B. Fruit a yellow- green, pointed, fleshy capsule

SUBGENUS Codonanthella

A. Corolla mildly to strongly ventricose or pouched (hypocyrtoid) , scarlet, red, pink, orange or yellow with maroon stripes; flowers nonresupinate, resupinate or pendulous; fruit a fleshy capsule; extrafloral nectaries absent; hairs multicellular-uniseriate on leaves; chromosome number n = 8; distribution in southeastern Brazil only GENUS Nematanthus

D. Growth form shrub-like epiphyte; nodal anatomy trilacunar; flowers resupinate or pendulous; leaves having glandular trichomes with 4-celled heads and unicellular and multicellular-uniseriate body cells, stomata anisocytic. . . . . SECTION Nematanthus

D. Growth form vine-like epiphyte; nodal anatomy unilacunar; flowers nonresupinate; leaves having glandular trichomes with more-than-4-celled heads and unicellular body cells;

stomata anisocytic and helicocytic.

SECTION Parvifolius

157

Checklist of Known Species in Cultivation

GENUS Codonanthe (Martius) Hans te in

C. calcarata (F. A. W. Miquel) Hanstein, Linnaea 34: 41 6. I865.

Nematanthus calcaratus F. A. W. Miquel, Linnaea 22: 472. 1849.

Type: Surinam, Berlyn, Focke 941 (u). Codonanthe bipartita L. B. Smith, Bulletin of the Torrey Botanical

Club 60 : 65?. 1933.

Type: Guyana, Kartabo Region. I. W. Bailey 181

(GH; fragment NY).

C. caribaea Urban, Symbolae Antillanae 2: 365. 1901.

Type: Guadeloupe, Riviere Noire, Puss 3776 (isotype, NY, US). C. Eggersii Urban, Symbolae Antillanae 2: 366. 1901.

Type: Tobago, Morne d'Cr, Eggers 5848 (B?, destroyed?). C. triplinervia Britton, Bulletin of the Torrey Botanical Club 48:

399: 1922.

Type: Trinidad, Crtoire River, Britton, Freeman & Nowell 2543

(isotypes, GH, US). C. triplinervia var. latifolia Morton in R. 0. Williams et al. ,

Flora of Trinidad and Tobago 2(5): 308. 1954.

Type: Trinidad, Mt. Tocuche, Simmonds 241 (Herb. Trinidad

14061; fragment US). C, triplinervia var. purpurea Morton in R. 0. Williams et al. ,

Flora of Trinidad and Tobago 2(5): 308. 1954.

Type: Trinidad, Arima-Blanchisseuse Rd. , Simmonds 147 (Herb.

Trinidad 13796; fragment US).

C. earn os a (Gardner) Hanstein in Martius, Flora Brasiliensis 8(l):

418. 1864. Hypocyrta carnosa Gardner in W. J. Hooker, London Journal of

Botany 1 : 178. 1842.

Type: Brazil, Corcovado, Gardner 73_ (k). Or oban che carnosa Vellozo, Florae Fluminensis 1 : 225. 1829;

Atlas 6: plate 61 . 1831.

Type: Brazil, Florae Fluminensis description and plate. Codonanthe carnosa (Vellozo) Hoehne, Sellowia 9: 52. 1958;

nom. ill eg. Codonanthe Hookeri Lemaire, L' Illustration Horticole 2: sub plate

Hr~l855.

Type: Hort. Backhouse (K) (Curtis' s Botanical Magazine 76:

plate 4531. 1850.) Coccanthera Hooker ana C. Koch & Hanstein, Index Seminum in Horto

Regio Botanico Berolinensi 1855: Appendix 17. 1855,

nom. illeg. Codonanthe florida Pampanini, Nuovo Giornale Botanico Italiano

series 2, 14: 597. 1907.

Type: Brazil, Bahia, cultivated in Florence Botanical Garden.

C. chiricana Wiehler, Selbyana 2(l): 95. 1977.

Type: Panama, Chiriqui, Dressier s.n. (Holotype, SEL; Isotype, K, MO, PMA, US).

158

C. corniculata Wiehler, Selbyana 2(l): 95. 1977.

Type: Panama, Loreto, Dressier s.n. (Holotype, SEL; Isotype, F, K, MO, NY, US).

C. crass if olia (Focke) Morton, Field Museum of Natural History,

Botanical Series 18: 1159. 1938. Hypocyrta crass if olia Focke, Tijdschrift voor de wissen

natuurkundige Wetenschappen 5* 199. 1852.

Type: Surinam, Focke, colored pencil drawing (L;

photograph US). Codonanthe confusa Sandwith, Kew Bulletin 1931: 492. 1931.

Type: French Guiana, Sagot 426 (Kj Isotype W). Episcia Hookeri Hanstein, Linnaea 34: 350. I865.

Type: Trinidad, Purdie, Hooker's Icones Plantarum 9: 873.

1852.

C_. devosiana Lemaire, L" Illustration Horticole 2: sub plate 56. 1855.

Type: Brazil. C. picta Lemaire, L' Illustration Horticole 4: sub plate 144. 1857.

C. digna Wiehler, Selbyana 5(2): 214. 1979.

Type: Cultivated plants of unknown origin, Wiehler 7330 (Holotype, SEL; Isotype, F, HB, K, MO, NY, R, RB, SP, US).

C. elegans Wiehler, Selbyana 6(in press). 1982.

C. gracilis (Martius) Hanstein, Linnaea 26: 209. I854.

Hypocyrta gracilis Martius, Nova Genera et Species Plantarum 50.

Jan.-Jun. 1829.

Lectotype: Brazil, Rio de Janeiro, Martius (M, photograph US). Orobanche crenata Vellozo, Florae Fluminensis 1: 254. Sept. -Nov.

1829; Atlas 6: plate 60. 1831.

Type: Florae Fluminensis, Atlas 6: plate 60. 0. ven trie os a Vellozo, Florae Fluminensis 1: 259. Sept. -Nov.

1829; Atlas 6: plate 74. 1831.

Type: Florae Fluminensis, Atlas 6: plate 74. Codonanthe ventricosa ( Vellozo) Hoehne, Sellowia 9: 53. 1958.

C. luteola Wiehler, Selbyana l(2): 159. 1975.

Type: Panama, Cerro Jefe, Wiehler & Dressier 71184 (Holotype, US; Isptype, PAN, SEL, M0, NY, GH, F, UC, K, P, B) .

C. macradenia Donnell-Smith, Botanical Gazette 25: 154. 1898. Lectotype: Costa Rica, Boruca, Tonduz 6769 (US).

C. paula Wiehler, Selbyana 5(2): 215. 1979.

Type: Brazil, Sao Paulo, Wiehler 79360 (Holotype, SEL; Isotype, F, HB, K, MO, NY, R, RB, SP, US).

159

C. uleana Fritsch, Botanische Jahrbucher fur Systematik 37: 492. 1906. Type: Brazil, Rio Jurua, Ule g6l 7 (B, destroyed). Columnea calcarata Donnell-Smith. Botanical Gazette 33: 254. 1902. Type: Guatemala, Cubilquitz, Tuerckheim 7645 (US; Isotype GH). Godonanthe decurrens I. M. Johnston, Sargentia 8: 275. 1949.

GENUS Nematanthus Schrader

N. crass if olius (Schott) Wiehler, Selbyana 5(3-4): 382. 1981. Besleria crass if olia Schott, Oesterreichische medicinische

Jahrbucher 6(2) : 93. 1820; reprinted in K. von Schreibers,

Nachrichten von den kaiserlichen oesterreichischen

Na turf orsch era in Brasilien, Anhang 7, p. 93. 1820. Nematanthus corticola Schrader, Gottingische gelehrte Anzeigen 1:

718. 1821. N. chloronema Martius, Nova Genera et Species Plantarum 3: 47.

tab. 220. 1829. N. jonema Martius, Nova Genera et Species Plantarum 3: 48. 1829. Orobanche brasiliensis Vellozo, Florae Fluminensis 1: 240. 1829. 0. fluminensis Vellozo, Florae Fluminensis 1: 240. 1829, pro

parte (sp, mixta). Nematanthus fluminensis ( Vellozo) Fritsch, Botanische Jahrbucher

fur Systematik 37: 488. 1906. N. longipes DC, Prodromus 7: 544. I839.

N. guillemii Brongn., L'Horticulteur Universal 3: 327. 1842. Columnea splendens Paxton, Paxton's Mag. Bot. 10: 5. 1843. Nematanthus calycinus Presl, Botanische Bemerkungen 145. 1844. N. heterophyllus Presl, Botanische Bemerkungen, nan Poeppig. 1840, N. per eskiaef olius Presl, Botanische Bemerkungen 143. 1844. N. radicans Presl, Botanische Bemerkungen 143. 1844. N. serrulatus Presl, Botanische Bemerkungen 144. 1844.

N. fissus (Vellozo) L. Skog, Baileya 19(4): 150. 1975.

Orobanche fissa Vellozo, Florae Fluminensis 257. Sept. -Nov.

1829; Atlas 6: plate 69. 1831. Hypocyrta Selloana Klotzsch & Hanstein in Hanstein in Martius,

Flora Brasiliensis 8: 409. 1864. H. fissa (Vellozo) Handro & L. B. Smith, Phytologia 20: 390. 1970. Nematanthus Selloana (Klotzsch & Hanstein) H. E. Moore, Baileya

19: 38. 1973.

N. fritsch ii Hoehne, Sellowia 9: 76. 1958; 0. Handro, Arquivos de

Botanica de Estado de Sao Paulo, series 2, 3(5): 228,

plate 57B. 1962. Hypocyrta Kuhlmannii 0. Handro, Arquivos Botanica de Estado de

Sao Paulo, series 2, 3(6): 339, plate 79B. 1964. Hypocyrta Mattosiana 0. Handro, Arquivos Botanica de Estado de

Sao Paulo, series 2, 3(6): 338, plate 79A. 1964. Nematanthus Mattosiana (0. Handro) H. E. Moore, Baileya 18:

143. 1972. N. fluminensis Hort. not N. fluminensis (Vellozo) Fritsch.

160

N. gregarius D. Denham, Baileya 19: 126. 1974.

Hypocyrta radicans Klotzsch & Hanstein in Hanstein in Martius, Florae Brasiliensis 8(l): 409. t. 67, f. 2. 1 Dec. 1864.

Golumnea radicans (Klotzsch & Hanstein) 0. Kuntze, Revisio Generum Plantarum 2: 472. 5 Nov. 1891.

Nematanthus radicans (Klotzsch & Hanstein) H. E. Moore, Baileya

19(1): 38. 20 Nov. 1973, illegitimate name, not Nema tan thus radicans K. Presl, Abhandlung der Bohmischen Gesellschaft der Wissenschaften V, 3: 573. 1845 and in Botanische Bemerkungen 143 (typographic error *145') "1844" (1846?).

N. hirtellus (Schott) Wiehler, Baileya 18(4): 134. 1971.

Besleria hirtella Schott, Medicinische Jahrbucher 6(2): 94.

(=p. 66). T820. Alloplectus spars if lorus Martius, Nova Genera et Species Plantarum

3: 55, t. 55,, fig. 1. 1829. A. parviflorus (in error for spars iflorus) Hanstein, Linnaea 34:

377. 1865. Grantzia parviflora Fritsch in Engler & Prantl, Naturlichen

Pflanzenfamilien 4(3b): 168. 1894. Hypocyrta discolor Lindley, Botanical Register 31, Misc. 19. 1845. Alloplectus dichrous Hooker, Botanical Magazine 72: t. 4216.

1846, not A. dichrous De Candolle, Prodromus 7: 5467 1839. Crantzia hirtella (Schott) Frtisch, Beiblatt zu den Botanischen

Jahrbucher 65-. 8. 1900. Alloplectus hirtellus (Schott) Preston ex Hoehne, Sellowia 9: 45.

1958; cf. Preston in Chittendon, RHS Dictionary of

Gardening 1: 79. 1951.

N. maculatus (Fritsch) Wiehler, Selbyana 5(1): 63. 1978.

Hypocyrta maculata Fritsch, Beiblatt zu den Botanischen Jahrbucher Systematik 65: 10. 1900.

N. nervosus (Fritsch) H. E. Moore, Baileya 19(l): 38. 1973.

Hypocyrta nervosa Fritsch, Denkschriften der Kaiserlichen Akademie der Wissenschaften mathematisch-naturwissenschaftliche Klasse, Wien 79: 288. 1908.

N. perianthomegus (Vellozo) H. E. Moore, Baileya 19(l): 38. 1973.

Or oban che perianth omega Vellozo, Florae Fluminensis 257. 1829.

N. strigillosus (Martius) H. E. Moore, Baileya 19(l): 38. 1973.

Hypocyrta strigillosa Martius, Nova Genera et Species Plantarum 3: 52. 1829.

N. wettsteinii (Fritsch) H. E. Moore, Baileya 19(l): 38. 1973.

Hypocyrta Wettsteinii Fritsch, Denkschriften der Kaiserlichen Akademie der Wissenschaften mathematisch- naturwissenschaftliche Klasse, Wien 79: 287. 1908.

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BIOGRAPHICAL SKETCH

Clayton Kazuo Kwock Hung Yuen was born in Honolulu, Hawaii, on August 30, 1953. He graduated from Saint Louis High School, Honolulu, Hawaii, in May 1971.

In September 1971 1 he entered the University of Hawaii at Manoa and received the Bachelor of Arts and Bachelor of Science degrees, majoring in Zoology and Horticulture, respectively, in August 1977.

In September 1977i he began work towards a Master of Science degree majoring in Horticulture. He worked as a graduate assistant and research technician during this time and graduated in August 1979.

In September 1979 1 be entered the graduate program at the University of Florida, majoring in Horticultural Science and minoring in Botany, and pursued the degree of Doctor of Philosophy. He worked as a greenhouse manager (Department of Botany) and graduate assistant (Department of Ornamental Horticulture) during this time.

167

I certify that I have read this study and that in my opinion it conforms to acceptable standards of scholarly presentation and is fully adequate, in scope and quality, as a dissertation for the degree of Doctor of Philosophy.

va 4<^

Thomas J. Sheehan, Chairman Professor of Horticultural Science

I certify that I have read this study and that in my opinion it conforms to acceptable standards of scholarly presentation and is fully adequate, in scope and quality, as a dissertation for the degree of Doctor of Philosophy.

fau ■' ±jy= il£k£k^

Bijan Piehgan <T

Assistant Professor of Horticultural Science

I certify that I have read this study and that in my opinion it conforms to acceptable standards of scholarly presentation and is fully adequate, in scope and quality, as a dissertation for the degree of Doctor of Philosophy.

i

LU

Hans Wiehler

Director of the Gesneriad Research

Foundation

I certify that I have read this study and that in my opinion it conforms to acceptable standards of scholarly presentation and is fully adequate, in scope and quality, as a dissertation for the degree of Doctor of Philosophy.

uZxk

William L. Stern

Professor of Botany

I certify that I have read this study and that in my opinion it conforms to acceptable standards of scholarly presentation and is fully adequate, in scope and quality, as a dissertation for the degree of Doctor of Philosophy.

UM

Paul M. Lyrene Associate Professor of Horticultural Science

This dissertation was submitted to the Graduate Faculty of the College of Agriculture and to the Graduate Council, and was accepted as partial fulfillment of the requirements for the degree of Doctor of Philosophy.

December 1982 I / - -f '1

Dean, College of Agriculture U cr

Dean for Graduate Studies and Research