The Biology of the Cycads 9781501737329

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THE BIOLOGY OF THE CYCADS

Plant of Cycas revoluta, the sago palm of horticulture, on the grounds of Kagoshima High School, Kyushu, Japan. This photo, taken in 1914 by E. H. Wilson, is of the plant from which S. Ikeno had obtained the flagellated spermatozoids he described in 1896, to a stunned readership. (See “Sex in Cycads,” Chapter 3.) (Missouri Botanical Garden Archives)

THE

BIOLOGY OF THE

CYCADS KnutJ. Norstog Fairchild Tropical Garden Miami, Florida

TrevorJ. Nicholls University of Bristol Bristol, England

COMSTOCK PUBLISHING ASSOCIATES a division of CORNELL UNIVERSITY PRESS | Ithaca and London

Copyright © 1997 by Cornell University All rights reserved. Except for brief quotations in a review, this book or parts thereof, must not be reproduced in any form without permission in writing from the publisher. For information, address Cornell University Press, Sage House, 512 East State Street, Ithaca, New York 14850. First published in 1997 by Cornell University Press.

Printed in the United States of America. Color plates printed in Hong Kong. Cornell University Press strives to utilize environmentally responsible suppliers and materials to the fullest extent possible in the publishing of its books. Such materials include vegetable-based, low-VOC inks and acid-free papers that are also either recycled, totally chlorine-free, or partly composed of nonwood fibers Library of Congress Cataloging-in-Publication Data Norstog, Knut, 1921— The biology of the cycads / Knut J. Norstog and Trevor J. Nicholls. p.

cm.

Includes index. ISBN 0-8014-3033-X (cloth : alk. paper) 1. Cycads.

I. Nicholls, Trevor J.

II. Title.

QK494.N67 1997 585\9 —DC21

Cloth printing

10

987654321

96-48889

Contents

Preface

vii

1.

General Features, Genera, and Relationships I Structural and Functional Features 2 The Genera of Living Cycads 7 Systematic Relationship of the Cycadales 20 Problems of Taxonomy, Classification, and Description 28 A Key for the Identification of Extant Genera 31

2.

Anatomy of the Stems, Leaves, and Roots 33 General Form of the Stem 33 Root and Stem Contraction 36 Structure of the Stem 37 Leaves and Leaf Homologues 49 System 58 Cycad Structures and Long-Term Survival 62

Internal The Root

3.

Reproduction and Embryo Development 63 Sex in Cycads 63 Pollen Cones and Seed Cones 66 Male Reproductive Structures 71 Female Reproductive Structures 74 The Female Gametophyte 78 The Male Gametophyte and Sexual Union 82 Evolution of Cycad Spermatozoids 91 Fertilization 92 The Embryo, the Seed, and the Seedling 95 Cycad Hybrids 98 Asexual Reproduction 99

4.

Physiology and Growth 101 Nitrogen Fixation 102 Salt Tolerance 108 Growth Rates and Growth-Limiting Factors 109 Longevity in Cycads 113 Seasonal Events 115 The Production of Toxins 121

5.

Population Biology and Pollination Dynamics 131 Biogeography 131 Habitat Requirements 132 Demography 136 Age, Size, and Sex Classes and Reproduction Rate 137 Population Genetics 143 The Advantages of Dioecy 146 Pollination Biology 147 Coevolution of Cycads and Insects 158 Seed Dispersal and Animals 159 Mast Seeding 160 The Status and Prospects of Cycad Populations

6.

The Fossil Cycadophytes 169 The Extinct and Living Gymnosperm Groups Habit 171 Early Cycadophytes 172 The Bennnettitales (Cycadeoidales)

161

169 Evolution of the Seed-Bearing The Cycadales: Fossil Cycads 178

194 v

vi

7.

Contents

Old World Genera and Species

202

The Indo-Australian Cycads: Cycas and Its Species Cycad Genera

8.

222

The African Cycads

New World Genera and Species

9.

Glossary

Conclusions

267

Zamia

314

317

References

329

Figure Credits Index

238

311

Afterword

The Endemic Australian

267

Ceratozamia, Chigua, Dioon, and Microcycas Conclusions

202

351

353

Thirty-two pages of color illustrations follow page 130.

285

266

Preface

Living cycads are the lingering remnants of a cycadophyte flora that “invented” and then ex¬ ploited the seed-bearing habit and, as a conse¬ quence, achieved worldwide dominance for a very long period, from about 300 to 70 million years ago, when the familiar flowering plants of today gained ascendancy. Interest in the surviv¬ ing cycads seems to have been increasing in the past few years, for several reasons. One is that as the toxic and carcinogenic substances pro¬ duced by cycads are identified and studied, there is a clearer appreciation of the possible dangers the plants pose to grazing and browsing live¬ stock and to people who eat foods prepared from the seeds or stems. Conversely, science has come to realize that some of the compounds may prove valuable in biomedical research, and such considerations have led to the organization of several international conferences specifically devoted to the subject of cycad toxicity. Another major reason for the resurgence of interest in the cycads is the growing public real¬ ization, at least in more enlightened quarters, of the urgent need for strict conservation of en¬ dangered organisms. Almost too late it is ac¬ knowledged that many species of cycads, some of which have survived since perhaps the Meso¬ zoic era, are on the brink of extinction, often as a direct result of human activities in just the last few decades. If these plants now become extinct we shall lose forever both a rich source of in¬ formation about the early evolution of the seed plants and an evocative exemplar of the flora of a remote past. Yet, despite the considerable botanical signifi¬ cance of the living cycads —there are some 190 species of them, several across a vast range —

the amount of scientific literature relating spe¬ cifically to them is relatively sparse. We esti¬ mate that not more than 3,500 scientific articles on cycads have been published in the last 150 years, and many of these are concerned with complex taxonomic problems. Likewise, few major monographs and books have been de¬ voted to the group, but some of these have been invaluable to ongoing cycad science and in the preparation of the present volume, and are cer¬ tainly worthy of mention here. In the early 1900s, Charles Joseph Chamberlain traveled extensively in the major cycad lo¬ calities of the Americas, Australia, and Africa, collecting information on living and preserved material in order to work on the general biol¬ ogy of the plants at the University of Chicago. His interests in cycads were wide-ranging; he and his students worked out many details of the cycad pollination and fertilization processes, in¬ cluding descriptions of the spectacular flagel¬ lated sperms of Dioon, Ceratozamia, and Stangeria. They described the anatomical details of these and other genera, explored various aspects of cycad ecology and biogeography, and even began some pioneering hybridization studies. In addition to preparing a series of scientific papers, Chamberlain coauthored Morphology of Gymnosperms with John Merle Coulter in 1917. This book contains an excellent section on cy¬ cads and probably laid the pattern for Cham¬ berlain’s semipopular The Living Cycads, pub¬ lished in 1919, which recounts his experiences during his journeys, discusses the ecology of many species in natural conditions, and presents a rather brief account of their reproductive biol¬ ogy and morphology. Because of its refreshing §•

VII

viii

Preface

style, mild taxonomic skepticism, and accuracy it remains the best and most readable introduc¬ tion to the subject, even though it contains some inconsistencies and is, alas, out of print. A third book by Chamberlain, Gymnosperms: Structure and Evolution, published in 1935 and reprinted in 1965, complements the information on cycads presented in the two earlier books. Such plaudits, regrettably, cannot be accorded the next monographer of cycads, J. Schuster, who in 1932 contributed a section on the Cycadaceae to a worldwide survey of plants, Das Pflanzenreich. Intended primarily as a nomenclatural work, it is by present standards inaccu¬ rate and confusing, though it can be of use to those who are aware of its limitations. A major problem with Schuster’s approach is that many of his descriptions relied on specimens in the Berlin Herbarium that were destroyed in World War II, and his decisions and conclusions are thus no longer verifiable. Moreover, the work fails to employ modem mles of nomenclatural priorities as well as the type concept (the desig¬ nation of a specific preserved specimen as the “type” that represents the essence of a given species). These shortcomings may be attributed, Dennis W. Stevenson and Sergio Sabato (1986) point out, to the fact that the official publication of the International Code of Botanical Nomen¬ clature did not appear until after Schuster’s book was published. Though there currently exists no comprehen¬ sive taxonomic monograph of the world’s cy¬ cads, several authors have addressed themselves to resolving the status of species within spe¬ cific genera. Among these is L. A. S. Johnson’s 1959 monograph on the taxonomy of Australian Zamiaceae (Bowenia, Lepidozamia, Macrozamia). Although Johnson chose to ignore the Aus¬ tralian species of Cycas, the work is a model of clarity and problem solving. Likewise, the no¬ menclature of South African species of cycads by R. A. Dyer (1965) is excellent but leaves one unsatisfied because it ignores the many interest¬ ing cycads of Central Africa. Fortunately, the latter are covered in a slightly earlier study by R. Melville (1957), which was augmented by a later study of Dyer and I. Verdoom (1969). It is also important to note that Stevenson and Sa¬ bato (1986) have taken the initial steps toward

straightening out the thoroughly confusing no¬ menclature of the genus Zamia, with their typification of the presently known species in that large group. And in recent years, the taxonomic jungle surrounding the widely scattered species of Cycas — which occur across a vast region stretching from Fiji to Madagascar — has be¬ gun to be cleared away, principally through the studies of Ken Hill of the National Herbarium in Sydney, Australia. As Johnson had done for Macrozamia, Hill has revised the systematics of the Australian species of Cycas and is now in¬ vestigating the broader reaches of its distribution in the Southern Hemisphere (Hill, 1992, 1993a, b, 1994a-c, 1995a). Of considerable interest to both the specialist and the general reader is the second edition of Cycas and the Cycadales, by D. D. Pant (1973), which despite the restrictive implications of its title is really a fine guide to the general biology of cycads. Similarly, Cycads of South Africa, by Cynthia Giddy (1984), although not intended to be scientifically detailed, contains such a com¬ prehensive collection of color photographs of the plants that extensive written descriptions are hardly necessary. More recently, Cycads of Africa, by Douglas Goode (1989), with its beau¬ tiful watercolor illustrations of the habit and fo¬ liar and reproductive structures of African spe¬ cies, fills a void in the cycad literature in such a satisfying way that one only wishes similar lit¬ erature were available for the other regions of great cycad diversity. One of the more important recent works deal¬ ing with all the world’s cycads is, aptly, Cy¬ cads of the World, written by David L. Jones (1993). This book is lavishly illustrated with color photos of nearly all extant cycad species, and is a reliable guide to the currently accepted species. The book also presents information on horticultural practices pertaining to the propa¬ gation and care of cycads in cultivation. Many modem botanical textbooks, of course, include sections dealing with the cycads. One is the chapter on the Cycadaceae by E. M. Gifford and A. S. Foster in the book Comparative Mor¬ phology of Vascular Plants (1989), which con¬ tains many excellent photographs and drawings. A second is the fine chapter in Morphology of Vascular Plants, by David W. Bierhorst (1971).

Preface

This book is also particularly good in its cover¬ age of reproductive structures. A third general plant morphology book, which we can recom¬ mend to those wishing an introduction to the structural characteristics and evolutionary rela¬ tionships of cycads, is Morphology of Plants and Fungi, by Harold C. Bold, Constantine J. Alexopoulos, and Theodore Delevoryas (1980). The last-named author has an enviable record of paleobotanical research into cycadophytes, hav¬ ing authored a number of landmark studies of seed ferns, cycadeoids (near cycad allies), and cycads. The very readable Paleobotany and the Evolution of Plants by Wilson Stewart (1983) and a later edition by Stewart and Gar W. Rothwell (1993) are helpful in understanding the ori¬ gins of the cycadophytes, and the fine paleo¬ botany text by Thomas and Elizabeth Taylor (1993), The Biology and Evolution of Fossil Plants, is most instructive. A fairly comprehensive bibliography of the literature of the cycads, listing some 1,800 arti¬ cles, has been prepared by R. W. Read and M. L. Solt (1986); their publication will prove useful to anyone wishing to gain access to the literature covering particular aspects of the biology of the group. At the time of his death in 1942, Chamberlain was working on a manuscript tentatively titled “A Taxonomic Monograph of the Cycads.” Ar¬ thur Haupt of the University of California, Los Angeles, then took on the task of editing and completing the manuscript. But when the work was submitted for review, one reviewer gave it such a devastating critique, purely on nomenclatural grounds, that it was withdrawn and laid aside. Subsequently, Paul Voth of the University of Chicago fell heir to the manuscript and some years later gave a copy to the first author of the present book. Because so much new informa¬ tion on the cycads has accumulated since Cham¬ berlain made his last entries in his manuscript, it was decided rather than to edit or revise it, simply to place copies of the manuscript in the library of Fairchild Tropical Garden, where it is available to all who wish to read it. We have frequently cited this work in the following pages as Chamberlain, ND (no date). Three societies, two of which are devoted solely to cycads, the third to palms and cycads,

ix

provide access to cycad lore and in some cases quite detailed information on recent advances in cycad research, horticultural practices, and, probably most important, cycad conservation. The International Cycad Society, headquartered in the United States (Carrie Landry, Department of Biology, University of Southwest Louisiana, Lafayette, La. 70504) publishes The Cycad Newsletter, which carries short articles on re¬ cent developments in cycad research, and con¬ ducts programs of pollen and seed exchange. Encephalartos, the publication of the Cycad So¬ ciety of Southern Africa (Giel Fourie, 9 Hobson St., 2550 Stilfontein, South Africa) is a valuable source of up-to-date information on all aspects of cycad biology, but naturally focuses most of its attention on the African genera. Palms & Cycads, the publication of the Palm & Cycad Societies of Australia Ltd. (Box 1134, Milton, Queensland) nearly always includes interesting articles on the Australian cycads. Membership in these societies is open to individuals of all nations and the dues are quite modest. Finally, an appreciably wider interest in cy¬ cads seems to have developed recently on the strength of their increased popularity as decora¬ tive plants in ornamental horticulture. To the en¬ thusiast, the archaic beauty of a clump of large Encephalartos or Cycas, the graceful tropical appearance of a Lepidozamia or Microcycas, or even perhaps the private pleasure of owning a small but rare Zamia can prove irresistible. As Cynthia Giddy (1984) remarked, referring par¬ ticularly to South Africa, it has become a status symbol to have a cycad growing on the lawn, regardless of cost. In the past, and in certain re¬ gions in the present, collection of mature wild plants for use as ornamental specimens has con¬ tributed significantly to their decline in nature, and this practice is to be deplored. An alter¬ native, in the years to come, may be the use of cultivated cycads as insurance against the total extinction of the most endangered species, par¬ ticularly if fairly large numbers of individuals are kept together with their pollinators to form viable breeding populations. Certainly, the horti¬ cultural use of these plants is to be encouraged so long as the demand for stock can be met using seedlings produced by already “captive plants. Although the more recent books on cycads

x

Preface

are superb in their photography and their species descriptions, they do not provide comprehen¬ sive surveys of the scientific literature. Nor are they directed toward the elucidation of recent findings in phytochemistry, physiology, cytol¬ ogy and cytogenetics, and population ecology. Accordingly, it seems to us timely that another book on the general biology of cycads be writ¬ ten. In preparing this volume we have tried at all times to be concise and accurate, while avoiding so far as possible some of the worst pedantries of scientific prose and the more obscure botani¬ cal terms. Where the latter are unavoidable, we have defined them upon first appearance and have provided a short glossary for follow-up reference. We hope that the book will be useful as a review of current knowledge of cycads for research workers and students of biology, and yet also appeal to those whose main interests are in the fields of conservation and horticulture rather than academic biology. We are grateful to the Directors, Officers, and Trustees of Fairchild Tropical Garden for sup¬ porting our efforts to produce a useful and inter¬ esting book and wish to single out specifically Nixon Smiley, John Popenoe, William McK. Klein, and Brinsley Burbidge, past, recent, and present Directors of the Garden, and Arthur Montgomery, Trustee, for their long-term sup¬ port of field and laboratory studies of cycads. We would also like to thank Stanley Keim, formerly Superintendent of the Garden, for his comrade¬ ship and graceful demeanor in all our contacts with him, both in the Garden and in the field. In addition, we wish to express our appreciation for courtesies extended by the Natural History Mu¬ seum (London); The Missouri Botanical Gar¬ den, St. Louis; The Royal Botanical Gardens, Kew; Orto Botanica, Naples; and the New York Botanical Garden, in our perusals of cycad spec¬ imens and libraries at these outstanding insti¬ tutions. We are also grateful to the University of Bristol and the Library of the Botany and Zool¬ ogy departments for their support of this project. The staff of the Morrison-Talbot Library of Wa¬ terloo, Illinois, were very helpful in providing copying and lending services to one of us (KJN). We would especially like to acknowledge the

contributions of all cycadologists and other bio¬ logical specialists, past and present and too nu¬ merous to name, whose publications, words, and deeds helped us write this book. In particular we thank Priscilla Fawcett for her beautiful and highly accurate drawings and paintings, which, we think, add much to both the scientific and aesthetic value of this book. Many individuals contributed valuable infor¬ mation without always knowing how it would be used. Others contributed photographs, answered specific questions, gave advice and help, and read parts or all of the manuscript. We therefore thank Charmian Ahem, Heidi and John Ander¬ son, Sidney Ash, Jean-Claude Audran, Jill Bar¬ ker, Arthur Bell, Brien Bosworth, Tom Broome, Victor Chavez, C. J. Chen, Paul Conant, Wil¬ liam Crepet, Frank Dakin, Bijan Dehgan, D. J. De Laubenfels, Paolo De Luca, John Donald¬ son, Jeff Duckett, Mark Duncan, Geir Edland, Joseph Ewan, Jack Fisher, William Fritz, GaoZhifeng, Cynthia Giddy, Rita Graham, Maria Grilli Caiola, Nat Grobbelaar, John Hendrix, Gail Hewson, Edward Hick, Chris Hill, Charles Hubbuch, Leonard Kurland, C. F. Liang, Rich¬ ard Litz, John MacDougal, Sergius Mamay, D. V. Molsen, Michel Monnier, Aldo Moretti, Robert Nash, K. Niklas, R. Osborne, Rose Overstreet, D. D. Pant, John Pate, Mick Richard¬ son, Helga Schuchmann, Bart Schutzman, JeanPierre Sclavo, B. D. Sharma, Rita Singh, A. D. Spreeth, Wilson Stewart, Ian Staff, William Tang, Donald Tankel, George Taylor, Tom and Edith Taylor, Mario Vazquez-Torres, Andrew Vovides, Terence Walters, James Watson, Loren White lock, H. Wohlberg, S. L. Yang, and, espe¬ cially, Ted Delevoryas, Robert Omduff, Roy Os¬ borne, Dennis Stevenson, Ken Hill, and Piet and Elsa Vorster, who patiently answered our many questions, read much of the manuscript, and contributed photographs and diagrams as well as many valuable suggestions. Dian Molsen cheer¬ fully and without reservation helped us many times with photographs and electron micro¬ graphs, and we are truly grateful to her. The late Sergio Sabato, to whose memory we dedicate this book, was a source of inspiration for us. Last but not least we are grateful to Robb Reavill, who presided over this project during the long

Preface

xi

years since its inception, and to other editors and

can be found in the Figure Credits, at the back of

facilitators at Cornell University Press, espe¬ cially Helene Maddux and Laura Healey. We particularly appreciate the expert editorial help we received from Bill Carver, whose painstak¬

the book. We gratefully acknowledge the gener¬ ous cooperation of publishers, authors, and art¬

ing editing of our manuscript was superb.

ists in allowing us to reproduce their work. Knut J. Norstog

Waterloo, Illinois All previously published figures, as well as those lent to us, are reproduced here by per¬ mission. Sources of individual illustrations are given in the captions; more complete credit lines

Trevor J. Nicholls

Bristol, England

THE BIOLOGY OF THE CYCADS

I

General Features, Genera, and Relationships

Cycads are among the most ancient and primi¬ tive of living seed-bearing plants. Their near¬ est relatives are thought to have been the longextinct seed ferns of the Late Paleozoic and Mesozoic eras, millions of years ago. The ar¬ chaic nature of the cycads is one of their many attractions; in a real sense cycads are the “dino¬ saurs” of the plant world, and because, unlike dinosaurs, a few cycad genera and species sur¬ vive today, they can excite the same feeling of wonder as do those amazing extinct animals. In this era of great public interest in the Meso¬ zoic plants and animals, particularly the latter, cycads are sometimes represented simply as the food of the dinosaurs. Though this may well have been the case to some degree, the major scientific interest that cycads should justly hold is in exemplifying some of the early stages in the evolution of reproductive mechanisms of even more advanced forms of plant life. Cycads were among the earliest seed plants, and there is reason to believe that insect-pollination systems and relationships may also have originated with cycads, considerably earlier than such relation¬ ships ensued with the later-evolving flowering plants. Moreover, all cycads employ bacteria in the fixing of atmospheric nitrogen within their specialized roots and in this fashion produce much the same sorts of useful nitrogenous mol¬ ecules as are found in the later-evolved clovers, alfalfas, and other legumes. On many grounds, then, one can make a strong scientific case for the study and preservation of these ancient plants. What are often more appealing to the general public, however, in addition to their great an¬ tiquity, are the beauty many species display in the wild, in gardens, and in conservatories and,

of course, their great value to collectors. This small group of superficially palmlike plants, confined in nature to limited areas in tropical and subtropical regions but now introduced as ornamental specimens into private and public gardens and conservatories the world over, is noted for its beautiful foliage and brightly col¬ ored cones and seeds (Color Figs. 1, 2, 4, 13, 14, 16). Cycads were first given taxonomic status by Linnaeus, who in 1737 named one of the genera Cycas, derived from koikas, a name used by the ancient Greek botanist Theophrastus for the doum palm of Egypt (Hyphaene thebaica). Un¬ fortunately, Linnaeus listed Cycas erroneously under the Palmae in Hortus Cliffortianus (1737), and the fact that cycads are gymnosperms and thus quite distinct from palms was not recog¬ nized until almost a century later, by Robert Brown in 1827. Subsequently, the family Cycadaceae was established —by Lindley in 1831 and Endlicher in 1836-1840-but there con¬ tinued to be confusion concerning just where among major plant groups the cycads should be placed. Various authors included them among the dicotyledons (Brongniart, 1843), or between monocotyledons and dicotyledons (Bentham and Hooker, 1862-1880), until they were finally reinstalled among the gymnosperms by van Tieghem in 1898. Technically, gymnosperm is a term of conve¬ nience and as such does not necessarily indicate a particularly close genetic relationship between the several groups of plants that happen to share only a common reproductive character —gym¬ nosperms being simply those plants in which seeds develop from ovules that are directly ex¬ posed to pollen grains. In contrast, angiosperms

2

The Biology of the Cycads

the top of the stem, and in part from the stems themselves, which in many species form sturdy, straight, unbranched trunks covered with an ar¬ mor of persistent leaf bases and reduced, scale¬ like leaves called cataphylls (Figs. 1.3, 1.5; Color Figs. 3, 18). Some kinds of cycads, how¬ ever, have relatively small and naked under¬ ground stems, perhaps an adaptation to help them survive periodic brushfires, and in some species (e.g., Stangeria eriopus and Zamia vazquezii) the foliage is rather more femlike than palmlike (Color Figs. 15, 124). One species, Z pseudoparasitica, lives a peculiar existence as an epiphyte perched high in the trees in the Pana¬ manian rainforest (Figs. 8.57, 8.58). Other cy¬ cads are xerophytes, flourishing in the semidesert environments of South Africa, Australia, and Mexico. In such habitats, their stiff, thorny foliage and stout trunks resemble those of other species of characteristic, thorn-scrub, desert vegetation (Color Figs. 106-108).

PF

Figure 1.1. Gymnosperms and angiosperms contrasted. Diagrams: A, Ginkgo, ovuliferous branch; B, Zamia (a cycad), female cone; C, cycad ovule; D, angiosperm flower; E, angiosperm ovule. Structures: E = egg, I = in¬ tegument, II = inner and outer integuments, M = megagametophyte, O = ovule, PG = pollen grains, PT = pollen tube. (Priscilla Fawcett)

(flowering plants) have ovules that are enclosed within an ovary and are never directly exposed to pollen grains (Fig. 1.1). Many aspects of the biology of cycads and their relatives are discussed in detail in the later chapters. Here we will offer brief descriptions of the major structural features of the group as a whole and the distinguishing characteristics of the several cycad families and genera, as in¬ ferred from morphological, cytological, chemi¬ cal, and molecular data. The world distribution of the living cycads is shown in Fig. 1.2.

Leaves All cycads bear pinnately compound leaves composed of a leaf stalk, or petiole, and an ex¬ tension, the rachis, that bears opposite or sub¬ opposite pairs of leaflets (pinnae). The length of these fronds varies considerably, from about 20 cm. in the smallest cycad, Zamia pygmaea, to more than 3 meters in such species as Cycas circinalis, Dioon spinulosum, and Macrozamia moorei, and nearly 7 meters in Encephalartos laurentianus (Color Figs. 2, 6). In all but the Australian genus, Bowenia, the leaves are oncecompound; in the two Bowenia species, the leaves are doubly compound, with secondary branches from the rachis bearing the leaflets

The palmlike general appearance of cycads alluded to arises in part from their large, pin-

(Color Figs. 101, 102). In all genera and species of cycad but Stan¬ geria:, which tends to form new leaves one at a time, the new leaves are produced all at once, usually on an annual or biennial basis. The pro¬ duction of such a flush of new leaves is often preceded by the shedding of the entire collec¬ tion of old leaves, usually by their detachment by abscission just above the leaf bases, which then persist as an armor over the trunk’s surface (Figs. 1.3, 2.4).

nately compound leaves, carried as a “crown” at

In general, cycad leaves, when young, are

Structural and Functional Features

Features, Genera, and Relationships

3

Figure 1.2. Worldwide distribution of cycads. Note that cycads are found mainly in regions between the Tropic of Cancer and the Tropic of Capricorn. The numbered regions are home to the following genera: 1. Ceratozamia, Chigua, Dioon, Microcycas, and Zamia. 2. Encephalartos and Stangeria. 3. Cycas, including northwestern Australia. 4. Bowenia, Lepidozamia, and Macrozamia.

covered with epidermal hairs, or trichomes, which in some species approach the texture of a dense wool or down. As the leaves mature, the trichomes often are lost and the leaves become smooth and glossy. In most cases mature cycad leaves have a rather harsh and leathery texture and are usually of a glossy dark-green hue, but there are exceptions. The leaves of some xerophytic forms may have a distinct blue-green cast, and in several species of the African En¬ cephalartos the leaflets are quite thick, have hard woody internal elements, and bear very

Figure 1.3. The lower part of the trunk of an old, trans¬ planted specimen of Encephalartos gratus at Fairchild Tropical Garden, Miami, showing its armor of cataphylls (arrow) and leaf bases (arrowhead). Some of the leaf bases still show traces of the veins that formerly passed through the petioles into the trunk; each trace, often de¬ scribed as an inverted omega, lies within the more or less diamond-shaped scar left by the abscised leaf). Each cataphyll end, more or less triangular in outline, is marked by an upthrust tip. Near the lower left of the trunk is an adventitious shoot, or “pup,” in the terms of the nursery trade. The girdling region at the top of the photo, proba¬ bly related to a period of dormancy or transplantation stress, or both, consists of several rows of cataphylls. Bar = 5 cm.

4

The Biology of the Cycads

sharp spines (Color Fig. 1). A cycad of this kind can be quite formidable when approached too closely by either man or beast. Still other spe¬ cies, as mentioned earlier, have rather soft, fernlike leaves. Another feature of cycad leaves also deserves mention here: cross sections of the leaf petioles typically exhibit vascular bundles arranged in the form of an omega (fl) or horseshoe pattern (Color Fig. 30).

Leaf Homologies Mature cycads tend to produce three classes of foliar organs in a series of cycles, often on an annual or biennial basis (Fig. 2.3). The growing season begins with the production of a new flush of cataphylls. If the plant is reproductive, a cone (or, only in Cycas, a flush of megasporophylls) is the next to be produced. What follows is a flush of cataphylls, then a flush of foliage leaves, and, finally, another flush of cataphylls surmounting the now quiescent stem apex. In all cycads except the female of Cycas, the sporophylls are arranged in cones. In Cycas, the megasporophylls are free, and arranged in a spi¬ ral phyllotaxy in much the same arrangement as are the foliage leaves (Color Fig. 89).

Stems The stems of cycads are manoxylic: they have comparatively little vascular tissue and wide zones of pith and cortex composed of starchfilled storage tissue (parenchyma) (Fig. 2.2; Color Figs. 7, 22, 24). This characteristic has given rise to the common name of one species, “sago palm,” which is owing to its occasional use as a source of starch for human food. But note that commercial sago is extracted not from cycads but from a true palm, Metroxylon. In the early 1900s, settlers in South Florida adopted the Indian custom of extracting starch from the native cycad, Zamia integrifolia, and for a time produced enough for export to the northeastern cities. This has never been a commercially via¬ ble trade, however, because cycads are quite slow-growing, and though sometimes locally numerous in the wild, are rapidly depleted. Per¬ haps more important, most parts of all cycads

contain several extremely poisonous neurotoxic and carcinogenic substances, which must first be removed by leaching, a process that offers its own dangers of accidental poisoning. Because cycads exhibit very little secondary growth, the stems are usually about as wide at the apex as at the base, thus engendering a fur¬ ther superficial resemblance to palms. In both palms and cycads, stem girth is the result of the activity of a thickening meristem at the periph¬ ery of the stem apex (Stevenson, 1980b) (Figs. 2.6, 2.8, 2.9). Internally, palm stems bear little resemblance to cycad stems, because they lack a well-defined pith and cortex and in transverse view display more or less evenly spaced vascu¬ lar strands throughout the section (Niklas, 1996). The result is that palm trunks are more durable and often grow to much greater heights than the relatively soft trunks of cycads can. Although the tallest cycad known, Lepidozamia hopei, may attain a height of nearly 18 meters (Color Fig. 13), none of the others exceeds much more than 10 meters in height, whereas some palms grow to 30 meters or more. An even greater height disparity exists between cycads and some conifers (e.g.. Sequoia), as shown in a diagram by Chamberlain (1935) (Fig. 1.4). An unusual and conspicuous feature of the internal structure of the cycad stem is the pres¬ ence of girdling leaf-vascular traces, which de¬ scribe a rather circuitous path on the way to the leaf from the vascular cylinder of the stem. This character has proved to be useful in addressing whether fossilized stems are those of true cycads or of the enigmatic, extinct cycadeoids (Color Fig. 7; Fig. 2.2). Although stem fossils of either group, sufficiently well-preserved to show inter¬ nal structure, are uncommon, the presence or absence of girdling leaf traces can be helpful in diagnosing their affinities. The absence of such traces is not a certain clue, however, because those parts of cycad stems bearing cataphylls (Fig. 1.5) or sporophylls or both, but not leaves, may lack girdling leaf traces.

Roots Most cycads that have grown naturally as seedlings have a long, thick taproot from which secondary roots arise, and these may be very

Features, Genera, and Relationships

5

Figure 1.6. Male plant of Zamia furfuracea. C = coral loid roots, F = fibrous secondary roots, M = male cone, S = stem, T = primary taproot. Figure 1.4. Diagram showing the disparity in height be¬ tween a cycad and a conifer. Bar = 2 m. (Redrawn from Chamberlain, 1935)

Figure 1.5. The apex of a stem of Cycas revoluta, show¬ ing cataphylls surrounding and overtopping the broad apical meristem. S = spiny cataphylls, W = woolly cata¬ phylls.

extensive, especially if the plants are growing in arid conditions or, as sometimes happens, on virtually bare rock (Fig. 2.27). In some genera,

such as Macrozamia, Zamia, and Stangeria, the primary roots may contain contractile elements that tend to draw the stem deeper into the soil (Fig. 2.5) (Stevenson, 1980a). The evidence of past contractions is persistent in those species with a subterranean stem habit; but in species having arborescent trunks, which generally re¬ place their taproots with an adventitious, sec¬ ondary root system, the stems are not drawn farther into the earth. From the normal cycad root system there usually arise many specialized branches that grow laterally or upward (apogeotropically), or both, and end in a nodular mass just below or just above the soil surface (Color Fig. 11; Fig. 1.6). These coralloid roots, whose dichotomous, club-shaped endings are quite dis¬ cernible at the stem-root junctures of the plant, contain host-specific cyanobacteria (also called blue-green algae) that actively fix atmospheric nitrogen. Coralloids are unique to the cycads, and the availability of an essential nutrient from this source is undoubtedly one of the reasons

6

The Biology of the Cycads

cycads are able to colonize barren sand dunes and scrublands. It may also account in part for their survival through several geological ages.

Reproduction Perhaps the most spectacular and most inter¬ esting feature of the cycads is their mode of reproduction. All cycads are dioecious: each in¬ dividual plant is strictly male or strictly female for the whole of its life. The pollen, on the male plant, and also the ovules, which are the struc¬ tures on the female plant each of which even¬ tually becomes a seed, are produced on sporophylls. Sporophylls are considered to be muchreduced fertile leaves which, in all but Cycas females, are aggregated as cones. But these are not the fairly small cones produced by pines, spruces, and other kinds of gymnosperms. Cycad cones often are enormous — some female cones are nearly a meter long and may weigh 40 kg (84 lbs.) (Color Fig. 44, 46). In certain spe¬ cies, the cones are brightly colored, and it seems likely that in at least some cases their visibility relates to attracting animal agents of pollina¬ tion and, later, of seed dispersal (Color Figs. 108, 123). The male cones of some cycads produce pro¬ digious amounts of pollen (Color Figs. 9, 10), and even cones of lesser dimensions are pollenprolific. The lower surfaces of the mature microsporophylls (male sporophylls) of pollen cones are covered with pollen sacs (microsporangia; Figs. 3.9,3.10). When these mature, three-celled pollen grains are produced and released into the air or in many cases picked up and transported to the female plant by insects. Concurrently with pollen-cone development and pollen maturation, megasporophylls (fe¬ male sporophylls) develop on the female plants and produce ovules. The megasporophylls of most cycads each bear two ovules, rarely three, but those of Cycas bear one to six pairs of ovules. At the time of pollination, the ovules are consid¬ erably smaller than they will be at maturity and consist of an integument equipped with a termi¬ nal open canal, the micropyle, that encloses a fleshy megasporangium, also called the nucellus. The megasporangium early on produces a single megaspore from which a large female ga-

Figure 1.7. Chamberlain’s elegant drawing of fertiliza¬ tion in Dioon edule: a section of a cycad ovule at the time of pollination. The pollen tube on the left shows the body cell still undivided; the one in the middle shows two sperms and the remains of the prothallial and stalk cells; the one on the right shows the two sperm mother-cells and the spiral ciliated band beginning to develop. Two pollen tubes have discharged their sperms (at lower right). (From Chamberlain, 1906)

metophyte, or megagametophyte, will develop (see Figs. 1.1, 1.7). In whatever way the pollen is transported, whether by wind, insect, or humans, when the grains arrive at the micropyle they are trapped in a drop of fluid exuded from micropylar cells and subsequently drawn in through the canal. There, they come to lie in the pollen chamber, a cavity in the tip of the nucellus. Here the pollen grains germinate and for some months grow slowly. Eventually, mature male gametophytes (microgametophytes), containing large, flagellated male gametes (spermatozoids), are formed. Inside the ovule, meanwhile, two to several large, functional archegonia are produced by the megagametophyte, each archegonium contain¬ ing one proportionately large female gamete (egg), about 3 mm long. The archegonia are sur¬ mounted by neck cells that project into the archegonial chamber, a space that functions as a fertilization chamber at the time spermatozoids are released from the microgametophytes in the pollen chamber (Fig. 1.7). Under normal condi-

Features, Genera, and Relationships

tions, the spermatozoids, which are upwards of a third of a millimeter in diameter, swim about in the archegonial chamber briefly and then squeeze past the archegonial neck cells into the egg cytoplasm. Fertilization then occurs when male and female nuclei fuse to form a zygote (the process is discussed more extensively in Chapter 3). Among living seed plants, only the cycads and the maidenhair tree of China, Gink¬ go biloba, have independently motile male ga¬ metes, and this characteristic almost certainly is one that they have retained virtually unmodified from their distant seed fern relatives of many millions of years ago (Garbary et al., 1993). So far as we can tell from the fossil record, the seeds of cycads are also similar to those of at least some of the seed ferns. (This subject is discussed more extensively in Chapter 6.) Cycad seeds usually are comparatively large, often sev¬ eral centimeters long, and contain a considerable store of starch. This body of starch, sometimes incorrectly referred to as “endosperm,” consti¬ tutes the ripe megagametophyte in its entirety. It normally contains a single, usually functionally dicotyledonous embryo and is surrounded by the three-layered integument: an inner membrane layer, a middle stony layer, and an outer fleshy layer. In most cases the outer layer is brightly colored, often in shades of red, orange, or yellow (Color Fig. 108). As one might suspect from the highly colored seeds of cycads, seed dispersal most often depends on the activities of animals that eat the fleshy seed layer and then drop the stony layer and its contents — the embryo and its food supply — some distance away from the mother plant. Even so, few cycads are noted for pos¬ sessing particularly efficient means of seed dis¬ persal. The greenish-brown seeds of Cycas rumphii, which contain a special flotation tissue, are an exception: the floating seeds of this cycad and a couple of closely related species are prob¬ ably responsible for its spread throughout the islands of the South Pacific (Dehgan and Yuen, 1983).

The Genera of Living Cycads The living representatives of the cycads, as we are increasingly coming to realize, show re¬

7

markable diversity in their anatomical and phys¬ iological adaptations; and, perhaps more than is generally thought and despite an apparently long history of genetic stability, they may still retain a potential for further significant evolutionary change. Although in some cases differing mark¬ edly among themselves, the cycads are nonethe¬ less quite distinct, as a group, from other living plant groups. Collectively, they form a natural and coherent group constituting a single order, the Cycadales. Although they are at the gymnospermous level of reproduction, the cycads are clearly not closely related to other living gymnosperms, such as the conifers. The extinct cycads, together with their apparent near relatives, are presented in Chapter 6. Three families and 11 genera of living cycads are currently recognized, one of these genera the recently described Chigua, and each genus has a unique and distinctive combination of vegeta¬ tive and reproductive characters. As we learn more about the physiological, genetic, and eco¬ logical characteristics of the cycads, areas of study that to date have been poorly explored, further clear differences between the genera may well come to be exposed. In this chapter we describe the main diagnostic features of the 11 genera and their natural distribution ranges, so far as these are known at present. Cycas

Cycas is generally recognized as the most dis¬ tinct of all living genera of cycads (Johnson, 1959), and its reproductive organs are consid¬ ered by some authorities to be the most primi¬ tive in this very ancient group of plants (Color Figs. 79, 83, 87). In fact, the characteristics of its megasporophylls are seen by many botanists as reflecting the morphology of scarcely differ¬ ing seed leaves seen in certain long-extinct seed ferns (Mamay, 1976). The genus is in need of a thorough taxonomic overhauling, for at present no one can be very sure how many of the roughly 45 described species are distinct entities and “good” species in their own right. D. D. Pant, an acknowledged authority on the genus, cites opinions on the actual number of species ranging from 8 (Schuster, 1932), 15 (Pilger, 1926) to 20 (Willis, 1973) and points out that “the total num-

8

The Biology of the Cycads

ber of specific names in the literature is much larger and the specific classification of the genus is, at present, in a confused state” (Pant, 1973, p. 29). He further states that “until each of the species of Cycas is revised on the basis of de¬ tailed studies in their morphological, genetic and other characteristics and the range of variation, it would perhaps be better to recognize all the gen¬ erally accepted species as distinct.” Cycas is the most widely ranging cycad ge¬ nus (Fig. 1.2), and its species occur naturally from the southern tip of Japan through the Malay Archipelago and the mainland of South¬ east Asia, west through parts of southern India and Sri Lanka, and as far as Madagascar and possibly the eastern African coast. The range also extends south through the Philippines and Indonesia and eastward to New Guinea and the northern half of Australia (Fig. 7.2). In addition, three of its species, C. revoluta, C. rumphii, and C. circinalis, are easily the most popular cycads cultivated for decorative purposes and are to be seen in parks and gardens in most warm coun¬ tries (Color Fig. 4; Fig. 7.13). All members of the genus have an above¬ ground stem, usually but not always forming a trunk which in older specimens of some species (e.g., C. angulata) may reach a height of 8-10 meters (Color Fig. 92) and in older specimens of other species (e.g., C. circinalis, C. revoluta) is often branched. The outward appearance of the trunk is very similar to that of many other ar¬ borescent cycads, being clothed in an armor of persistent leaf-bases and cataphylls, which in old specimens may be partially or wholly re¬ placed by cork. Internally, the stems exhibit a thick pith, separated from an equally substan¬ tial cortex by one or more cylinders of woody tissue. The leaves of larger species of Cycas may reach a length of 3 meters. They are typically cycadalean (i.e., once-pinnately compound), but are unique in both venation and vernation. Each leaflet has a prominent midrib containing a sin¬ gle vascular strand, and no other veins (Figs. 2.23, 2.24), a feature sufficient to distinguish plants of this genus from all others. Also, as new leaves emerge at the top of the stem, each rachis is straight for most of its length but every leaflet is tightly coiled (circinate) (Color Fig. 14).

In many ways, Cycas is the most structurally and genetically distinct genus in the Cycadales. The leaves and stems have certain peculiarities as outlined above, but the most characteristic and unique feature is the apparently primitive nature of the reproductive organs. Unlike their counterparts in other genera, the megasporophylls of Cycas do not form a determinate fe¬ male cone, although they are somewhat tightly clustered together when first emerging (Color Fig. 12), and as such this cluster has been termed a pseudocone (Niklas and Norstog, 1984). After pollination, the megasporophylls of certain spe¬ cies relax and spread out like leaves, then hang down, and eventually, after the seeds ripen and are shed, fall off the plant individually. Each sporophyll has a petiole, expanded at the outer end into a terminal blade, which in some species is merely serrated, but in others is deeply di¬ vided, though whether these divisions are equiv¬ alent to the leaflets of foliage leaves, as has sometimes been suggested, is perhaps dubious. The ovules, up to 12 in number, are attached to both sides of the petiole (Fig. 7.12; Color Figs. 84, 85, 89). Whereas the female “cones” of Cycas are in¬ determinate, if indeed one calls them cones at all, the male cones are determinate, like those of other cycads. The male sporophylls of Cycas are much less leaflike than those of the female, be¬ ing short and thickened and arranged spirally in a compact cone (Color Fig. 87). Even so, they bear a resemblance to the female sporophylls in having a middle fertile part and a terminal “blade” region (Fig. 3.9), a point emphasized by Schuster (1932). Most students of the cycads accept the theory that in its female reproductive structures, Cycas has essentially retained the seed fern condition wherein the ovules are borne upon the foliage. If this interpretation is correct, the genus is a valu¬ able “missing link,” showing an intermediate stage in the evolution of female cones. It has also been argued, however, that the indetermi¬ nate arrangement of leaflike female sporophylls of Cycas is an advanced feature, and therefore not revealing of some ancestral condition (e.g., Arnold, 1953; Meeuse, 1964). Some recent dis¬ coveries of cycad megasporophylls resembling those of Cycas revoluta and C. pectinata, to-

Features, Genera, and Relationships

9

If the male cones of Cycas were indetermi¬

Figure 1.8. The germinating seeds of two cycads. Above, platyspermic seed of Cycas revoluta. Below, radiospermic seed of Dioon spinulosum. (From Stevenson, 1990a)

gether with evidence that organs of this kind may have been borne upon a strobilar axis, sug¬ gest that we keep an open mind with respect to evolutionary pathways within the genus and among its fossil ancestors (Gao and Thomas, 1991). The ovules of Cycas are bilateral in symme¬ try, although their flattened nature is more ob¬ vious in C. revoluta than in other species, such as C. circinalis. This is all the more apparent when the seeds germinate, for the emerging em¬ bryonic root causes the hard seed coat to open like a clamshell (Fig. 1.8). Conversely, seeds of other cycads are radially symmetrical and have thin, circular areas at their distal ends through which their roots emerge. The genus Cycas, ir¬ respective of whether it is considered primitive or advanced, seems to be widely separated from the other genera by the unique structure and ar¬ rangement of its female sporophylls and the bi¬ lateral rather than radial symmetry of its ovules. Moreover, the genus differs from other genera in its leaf characters. It is the only genus in which the leaflet has just a single vein, and it is also a genus in which only the leaflets are circinate when young.

nate, as are the female “cones,” our view of the integrity of the cycads as a natural group would be rather different, and Cycas might well be classified as a sole surviving seed fern. Either the genus has been separate from the other gen¬ era for an extraordinarily long period and has retained some very primitive features, or it has diverged from the other cycads in relatively re¬ cent times and evolved, for unknown reasons, toward a pseudoprimitive state in its female re¬ productive organs. Nevertheless, the prevailing view held by students of the group (e.g., Hutch¬ inson, 1924; Pilger, 1926, Johnson, 1959) is that Cycas is such a distinctive and unusual genus that it mandates placement in a separate family of cycads, the Cycadaceae. Compared with Cy¬ cas, the remaining genera are all basically simi¬ lar to one another in their reproductive struc¬ tures and possess compact cones in both sexes, although the degree of specialization of the sporophylls varies considerably. Encephalartos Three genera, Encephalartos, Lepidozamia, and Macrozamia, share so many characteristics that despite the present geographical separation of Encephalartos from the other two, the pre¬ vailing view today is that they constitute a natu¬ ral subgroup of cycads. All three bear compara¬ tively massive cones (Color Figs. 46, 103); all three share similar sporophyll morphology, dif¬ fering substantially only in the distal ornamen¬ tation of the sporophylls (Stevenson, 1990a). The ends of the sporophylls, which we will refer to as the shields in descriptions of cone mor¬ phology, are more or less diamond-shaped, so that in overall aspect the sporophylls present an obvious spiral relationship to each other (Color Fig. 114). In contrast, the sporophyll shields of Zamia, Ceratozamia, and Microcycas are hex¬ agonal and seemingly arranged in vertical rows, even though, basically, they too are spirally dis¬ posed on the cone axis (Color Fig. 126; Fig. 8.27). In another aspect, too, there is similarity: Encephalartos, Macrozamia, and perhaps Lepi¬ dozamia, produce ovules with fully developed female gametophytes even in the absence of pollination and fertilization (in effect, embryo¬ less seeds); in other genera, ovule abortion oc-

10

The Biology of the Cycads

curs in the absence of pollination and fertiliza¬ tion. We therefore tend to agree with Johnson’s (1959) and Stevenson’s (1990a) placement of the three in the tribe Encephalarteae of the fam¬ ily Zamiaceae, but would prefer to see them placed in a separate family. Encephalartos gets its name, translated as “bread-head,” from the use of its cones and seeds as food by African aboriginals. Its spe¬ cies are found throughout Africa south of the Sahara, ranging from north of the Equator on both coasts, through the central tropical regions bordering the Congo River, and southeastward to the extreme southern coast of Cape Province (Figs. 1.2, 7.36). Currently about 55 species are recognized, but new species are still being de¬ scribed and the total may eventually reach 65 or so. Certain species of Encephalartos have rather small, subterranean stems (e.g., E. cycadifolius), but others have massive aerial trunks, several to nearly 10 meters tall when mature (for example, E. transvenosus), always protected by a sturdy covering of old leaf bases and cataphylls. Al¬ most all of the species have a tendency to pro¬ duce basal suckers when old, so that in nature the plants sometimes occur in clumps. The leaves of Encephalartos frequently are leathery and very stiff, characters associated with arid conditions. They are always pinnately once-compound, and in many of the species the leaflets (pinnae) have lobes that may be twisted and tipped with spines (Color Figs. 107, 108). The cones of both sexes are frequently long and heavy, sometimes solitary but more often several in number (Figs. 7.51, 7.52; Color Figs. 1, 111). The cones appear to be lateral in posi¬ tion with respect to the stem apex, but according to Bierhorst (197i) they are initiated apically. The sporophylls are overlapping and spirally arranged, with thickened, prismoid ends having several flat facets, a general characteristic of this genus. This character is especially notice¬ able in female cones (Color Figs. 1, 114). The sporophylls are sometimes woolly but never spiny, and in many species the mature cones are brightly colored in red, orange, yellow, or green. Seeds of Encephalartos are eaten by monkeys (baboons) and birds (Giddy, 1984; Grobbelaar et al., 1989), all of which have color vision. An

intriguing question therefore is that if the cones and seeds of ancient cycads were also brightly colored, might they have been fed upon by an¬ cient reptiles and birdlike dinosaurs that may well have had color vision, as do present-day lizards and birds (Bauman and Yokoyama, 1976)7 But because cycads are armed with an array of toxins, it is equally possible that the bright colors may serve (and might have served) as warnings to at least some predators. Stangeria Named for Dr. Max Stanger, Surveyor Gen¬ eral of Natal, South Africa, this genus is quite distinct from the other cycads; its only species is S. eriopus. Richardson (1990) remarks that bio¬ chemical systematics is not very definitive when applied to cycad genera, but the absence of biflavonoids in Stangeria reinforces the concept that it differs from the other genera. (But for a different view, see Meurer-Grimes and Steven¬ son, 1994, in which Stangeria was found to con¬ tain complex biflavones.) In this context, Rich¬ ardson also points out that Cycas and Dioon con¬ tain unique biflavonoids. These observations tend to support suggestions that these two genera and Stangeria are rather distant from the remain¬ ing eight genera, as has also been suggested by Johnson (1959) and Stevenson (1990a). Stan¬ geria now has a very restricted distribution along the southeastern coastal region of the Re¬ public of South Africa (Figs. 1.2, 7.36). The stems of Stangeria are completely sub¬ terranean and, because the leaf bases are decid¬ uous, naked. The stems may attain a length of about 30 cm and a diameter of 15-20 cm, and quite frequently are branched. Stangeria leaves are once-pinnately compound, as are those of nearly all other cycads (two species of Bowenia being the sole exceptions), but are unique in their femlike aspect, by contrast with the quite palmlike appearance of the foliage of other gen¬ era (Fig. 1.9). The hooklike vernation of the emerging leaves, with their folded and twisted pinnae, reminds one of the young fronds of the primitive fern Botrichium (Fig. 2.21; Color Fig. 27). Stangeria is one of only three genera of cycads to have leaflets with midribs (Cycas and Chigua are the others). The venation of the leaf¬ lets, consisting as it does of a prominent midrib

Features, Genera, and Relationships

I I

Figure 1.9. Leaf of Stangeria eriopus. Note the midrib in each leaflet.

and numerous, parallel branch veins, is also reminiscent of some fern genera, such as Blechnum and Acrostichum (Brashier, 1968; Dehgan et al., 1993) (Color Fig. 15). As is now well known, when the plant was first described by Kuntze in 1836 from a sterile specimen col¬ lected by Drege, it was assigned to the fern genus Lomaria. It was recognized as a cycad only in 1853, when a plant collected by Stanger and sent to the botanical garden in Chelsea, En¬ gland, produced cones (Vorster and Vorster, 1985). Alone among cycads, Stangeria does not pro¬ duce its new leaves in an annual flush of several to many, but singly throughout the year. Only a few leaves, usually not more than four, are pres¬ ent at any one time, and these vary considerably in size and general appearance according to en¬ vironmental conditions, occasionally approach¬ ing 2 meters in length. Longer leaves occur in populations growing in the shade of wood¬ lands, shorter ones occur in savanna popula¬ tions. There is always a long petiole and few, relatively large leaflets (Fig. 1.9; Color Fig. 15). The developing leaf displays circinate verna¬ tion, with a hooklike, inwardly curved rachis (“inflexed” according to Stevenson, 1981); the leaflets are folded “book-fashion” (i.e., conduplicate) and are somewhat twisted about each other (Fig. 2.21). The cones of Stangeria are borne singly on comparatively long stalks (peduncles) holding the reproductive structures well clear of the stem apex, which is usually below the soil level. The cones are silver-gray and covered with a short velvety wool; the cylindrical male cones are up

Figure 1.10. Cones of Stangeria eriopus: female cone at left, detached male cone at right.

to about 25 cm long and the ovoid female cones are about 20 cm long and 10 cm in diameter (Fig. 1.10). Before they are completely mature, the rather flat sporophyll ends of both male and fe¬ male cones overlap very tightly, like fish scales, only separating slightly at pollination time. This cone morphology, neither unique nor especially primitive, seems somewhat intermediate be¬ tween that of Zamia and that of Dioon. Largely on the basis of foliage characteristics, Johnson (1959) places Stangeria in a separate family, Stangeriaceae (see Table 1.2). Macrozamia Macrozamia (large “Zamia") is a fairly large genus in terms of numbers of species, 27 at pres¬ ent count, but is confined to Australia, where it occurs mainly in the subtropical regions and in areas with a Mediterranean climate (Fig. 7.21). In many ways its members, like those of Encephalartos and Lepidozamia, are rather “gen¬ eralized” cycads with few dramatically distinc¬ tive diagnostic features, though the genus is readily recognizable by several foliage, stem, and cone characteristics. A few species, such as Macrozamia moorei (Color Fig. 19), have large, unbranched, aerial trunks as much as 5 meters tall, and from a dis¬ tance can appear very palmlike, but in others the stem is mainly or wholly subterranean, though in all cases covered with persistent leaf bases and relatively few cataphylls. In large species.

12

The Biology of the Cycads

the general appearance of old plants, even with¬ in a comparatively local area, can be quite vari¬ able, because in deep, soft soil the plant’s con¬ tractile roots can slowly drag the stem into the ground, whereas on shallow soils, where this is not possible, an arborescent, though sometimes

The shield of each sporophyll carries a single, sharp, upward-pointed spine, which is longest in

procumbent, trunk tends to develop. The leaves of large macrozamias are often

Lepidozamia

long and gently recurved, whereas in small spe¬ cies the fronds frequently are spirally twisted (Color Figs. 93, 98). Those of some species are gray-green; others are grass-green. They are al¬ ways once-pinnately compound (though in three species the leaflets are deeply forked), and the base of the petiole is usually covered with long, silky hairs. The leaflets, in contrast to those of Lepidozamia, are inserted laterally on the rachis,

The genus Lepidozamia was first described in 1857 by Regel, but was merged with Macro¬ zamia by Miquel in 1868. In that era, its two taxa were also described as species of Zamia, of Encephalartos, of the now unrecognized Catakidozamia, and even of Cycas (Schuster, 1932). Such uncertainties are rather typical of early de¬ cisions on plant nomenclature, made before key generic and specific criteria were worked out and agreed upon. L. A. S. Johnson (1959), after a detailed study of Macrozamia as then con¬ stituted, pointed out that two species, them¬ selves very similar to each other, differed so significantly from the others that they should be returned to Regel’s genus, Lepidozamia. The species, L. hopei and L. per off sky ana as

and those of mature plants usually have smooth margins and always have parallel venation, without a midrib. Often, they point somewhat upward from their insertion on the rachis, and there is a more or less pronounced colored re¬ gion, or callus, at the base of each (Color Fig. 57). The vernation of the leaves is straight; that is, neither the rachis nor the leaflets are coiled or twisted when they are young and emergent. The cones of Macrozamia are stalked. Those of male plants are sometimes very numerous (up to 100 according to Coulter and Chamberlain [1917]) but commonly fewer than 10 in our experience). In most cases the cones are pro¬ duced at the top of the stem, as in other cy¬ cads, but those of several species are thought to be initiated subterminally (i.e., laterally). This rather complicated subject will be explored in more detail in Chapter 3. The sporophylls of both sexes are markedly thickened toward their ends and overlap tightly until the cone is ma¬ ture; sporophylls of male cones separate mark¬ edly when the pollen is mature and being shed, but female cones at maturity are variable in this character. In some species the female cone re¬ mains closed until the seeds are shed; in others the seeds, which commonly are pink to orangered, grow to such a size that the sporophyll shields are spread apart. In any event, the sporo¬ phylls of both sexes are clearly spiral in aspect and do not appear as if arranged in vertical rows.

the sporophylls near the top of the cone (Color Fig. 97; Fig. 7.25). This characteristic is unique to Macrozamia.

now circumscribed, are restricted to the eastern coastal regions of Australia (Fig. 7.21). Chamberlain (ND, no date; unpublished manuscript) states that one of the two species, L. hopei, is the tallest of all cycads, with erect trunks up to 18 meters high and up to 40 cm in diameter (Color Fig. 13). The trunks are heavily clothed in leaf bases and cataphylls, the latter structures being produced in much greater pro¬ fusion than in Macrozamia. This characteris¬ tic gives the trunk a strongly armored appear¬ ance, which no doubt suggests the generic name, “scale-zamia.” The leaves of Lepidozamia are 40 or more in a crown, each about 2 meters long and bearing about 80 recurved (falcate) leaflets inserted on the sides of a dorsal ridge on the rachis. Each leaflet base has a flange extending basally to¬ ward the next lower leaflet (Figs. 7.31, 7.33), a character referred to as decurrent. The leaflets, glossy dark-green, have parallel veins, lack a midrib, are straplike with a smooth edge, and are slightly drooping. Two further differences from Macrozamia are the absence of a basal

Features, Genera, and Relationships

callus on the leaflets and the lack of reduced, spinelike leaflets in the lower part of the rachis, such as are found in the larger species of that genus. The female cones of Lepidozamia are very large (up to 60 cm long, 20 cm wide) and may weigh as much as 40 kg (Color Fig. 103). They are sessile and at least superficially in a lateral position. Unlike those of Macrozamia, the ends of the sporophylls, though pointed, do not bear a spine and are covered with very short hairs. Ac¬ cording to Johnson (1959), a peculiar feature of Lepidozamia is its tendency to produce, fairly often, three ovules per sporophyll, rather than two, as in most other cycads (many species of Cycas, of course, always produce more than two ovules per sporophyll), and in Lepidozamia the three ovules may all mature into seeds. This may be a primitive characteristic if one accepts Cycas with its several ovules as exemplifying a primi¬ tive state (Johnson, 1959). The male cones of Lepidozamia are usually more than one, about 20 cm long, and stalked. Bowenia Bowenia, like Stangeria, has distinctive foli¬

age: its twice-pinnately compound leaves (Color Figs. 101,102; Fig. 7.34) and peculiar branching of the upper stem led Stevenson (1981) to sug¬ gest that it also is sufficiently different from other cycads to warrant classification in its own family. He has subsequently (1990b) modified this view and now places the genus and its two species in a second subfamily of the Stangeriaceae (Table 1.2). The two species of Bowenia, named for George Bowen, the first Governor of Queensland, are currently restricted to three small areas of tropical northeastern Queensland: B. spectabilis in the northeast, in the vicinity of Cairns, and B. serrulata farther south, in the vicinity of Rockhampton (Fig. 7.21). The two species are the only cycads to have invari¬ ably twice-pinnately compound leaves. (Cycas micholitzii has superficially similar leaves but a form, simplicipinna, has once-pinnately com¬ pound leaves, as do the other members of the genus.) The leaflets of Bowenia are parallel-

13

veined without a midrib, and the vernation of the emerging leaf, but not the leaflets, is circinate. The leaves are few in number, a flush typically numbering only two to five. The stem of Bowenia is always subterranean and rather cylindrical, though variable in shape and size. Its main characteristic, not normally found in other genera, is that it is divided at the apex into several or many short branches, each of which may bear a terminal cone or leaves (or both) and a few cataphylls. The cones of Bowenia resemble those of Zamia. Male cones are cylindroid and up to 7 cm long and 5 cm wide (Color Fig. 104); female cones are ovoid and up to 15 cm long and 10 cm wide (Color Fig. 37). The latter are dark-green and borne on short, fleshy peduncles; they have peltate, hexagonal sporophyll shields that fit rather closely together when young, but when mature separate widely to expose the large, pur¬ ple seeds (2.5 by 3.5 cm). Dioon

Our knowledge of the Mexican and Hondu¬ ran cycad Dioon (“two ova”) stems principally from the studies and explorations of Charles J. Chamberlain, whose first visit to Mexico was in 1904, when he visited Xalapa (= Jalapa) in the state of Veracruz, which lies to the east of Mex¬ ico City and borders on the Gulf of Mexico. Describing this occasion, Chamberlain (1919, pp 13-14) wrote that he “found Dioon edule in great abundance at Chavarillo, a small station on the International Railway about an hour’s ride east of Jalapa” (Fig. 8.13), and, further, “the plant grows in the blazing tropical sun and is a prominent feature of the landscape, although its stocky trunk seldom reaches a height of more than 4 or 5 feet” (Color Fig. 117; Fig. 8.20). At the time Chamberlain wrote, only two species of Dioon were known: D. edule and D. spinulosum (Color Fig. 2). The latter was “practically unknown” at the time, and its description was “based on a few small leaves of young plants,” a situation Chamberlain rectified on a later trip to Mexico in 1908. Chamberlain located a population of D. spin-

14

The Biology of the Cycads

ulosum in the mountains near Tuxtepec, about 160 km south of Veracruz. After an hour’s ride on horseback he found large specimens of this beautiful cycad and, later, in a forest of ma¬ hogany, kapok, ferns, orchids, and other pri¬ mary wet-forest vegetation, found other stately specimens, one of which measured 11 meters in height, and two of his colleages found speci¬ mens “50 feet tall!” Chamberlain said that, in this locale, D. spinulosum was so abundant that “it would be no exaggeration to speak of a Di¬ oon forest” (Chamberlain, 1917, pp. 19-20). This, it should be noted, is a far cry from the circumstances today, in which populations of Dioon and other cycads consist of a few scat¬ tered individuals in habitats too poor to be used for lumbering or agriculture (Fig. 8.14). According to Sabato and De Luca (1985),

per frond (Color Figs. 2, 116-118). Those of D. spinulosum are equipped with marginal spines, as the species name implies, though this character is somewhat variable; the leaflets of D. rzedowskii and D. mejiae are entire (i.e., smooth-margined). Other species of Dioon are generally of a lower stature, with stiff fronds and sharp-pointed leaflets, which, depending on the

who have studied populations of Dioon in Mex¬ ico for more than 15 years, individuals of the several species are generally very scattered now, forming small communities but never playing an important (i.e., dominant or subdominant) role in the vegetation. In this respect, however, members of this genus are no different from those in other cycad genera; nowhere do cycads now constitute dominant or even subdominant components in any vegetation types. The dis¬ tribution of Dioon is shown on Figs. 1.2 and 8.1. While individuals of D. spinulosum may at¬ tain a height of 16 meters (Sabato and De Luca, 1985), more typical individuals run 3-6 meters tall and other Dioon species are lower. Dioon edule, for example, seldom reaches a height of 3 meters, and it is usually in the 1-1.5-meter

masses of nitrogen-fixing nodules. Females of D. spinulosum (and probably

range. Most cycad stems show little wood in cross sections, but older stems of Dioon display a zone of xylem 8-10 cm thick (Greguss, 1968); nevertheless, the bulk of the stem is composed of thick zones of starch-laden pith and cortex. Typical of all species of Dioon are nonarticulated leaflets, broadly inserted along the leaf rachises (Fig. 8.16), and Dioon is thus the only New World cycad having nonarticulated pinnae. The leaves of the closely related D. spinulosum, D. rzedowskii, and D. mejiae are on the order of 2-3 meters in length, somewhat, lax and a glossy dark-green, with up to 120 leaflet pairs

species, may or may not have marginal teeth. The roots of Dioon can be quite long. Cham¬ berlain (1935) found a root of D. spinulosum that was exposed where it hung over a rock a distance of 12 meters from the stem, and was still 3 cm thick at the point where it entered a crevice and could not be traced farther (Fig. 2.27). As in other cycads, some branch roots are apogeotropic, i.e., growing laterally and even upward rather than down, and forming coralloid

D. mejiae, whose female cones have not been described) produce very large, pendant cones, among the largest in the Cycadales (Color Figs. 38, 45). The megasporophylls are somewhat like those of Lepidozamia but most nearly re¬ semble those of Stangeria (Fig. 3.17). Mature female cones of these species measure up to 60 cm in length and 27 cm in diameter; those of other Dioon species are smaller and semi-erect. Fertilization and embryo development in D. edule were studied in some detail by Cham¬ berlain (1909a, 1910). In female cones collected in the field on April 10, 1905, he found active spermatozoids in pollen tubes and continued to find them in cones picked as late as May 10. (In Microcycas and Zamia pumila, the period when motile sperms may be found lasts no more than a week.) Each Dioon pollen tube forms a pair of multiflagellated spermatozoids, each about 300 |xm in diameter. Meanwhile, the large, starchy female gametophyte is fully formed in the ovule, and its several eggs, each about 5.5 mm long, are fertilized. After fertilization, the large, dicoty¬ ledonous embryo, remarkable in being densely hairy, develops in about five months. The seeds of this species, ivory to light yellow, are com¬ paratively large (about 2 by 3 cm). They are shed chiefly in November or December (in Miami) and germinate readily without any dormant pe-

Features, Genera, and Relationships

15

nod. (The name, Dioon, [“two ova”], by the way, is a rather bad misnomer: if it refers to the actual eggs in the female gametophyte, it is in¬ correct, for these number 2-10 and usually 3 [Chamberlain, 1935]; and if it refers to the seeds, it is far too inclusive, because that count can apply to all the genera except Cycas.)

Microcycas Microcycas, a genus of one species (M. calo¬ coma), has an extremely limited distribution in western Cuba (Fig. 8.24), and although one of the most attractive cycads, it is still rare in culti¬ vation. Its name, literally “tiny Cycas,” is ow¬ ing to the mistaken impression of A. De Can¬ dolle (1864-1868), who based his description on dried and pressed specimens having imma¬ ture male cones. Quite to the contrary, it is a robust tree, one of the tallest cycads; moreover, its mature cones are among the largest of any of the cycads. Microcycas has erect, occasionally branched trunks sometimes reaching 10 meters in height (Color Fig. 60). When young, the stem is cov¬ ered with old leaf bases and bands of persistent cataphylls, but eventually these are lost, and the trunks of older individuals are covered with a corky bark (Color Fig. 25). The vernation of the developing leaves is straight; the leaves are numerous and in mature specimens are quite distinctive, accounting for the specific name calocoma, literally “beautiful hair.” The long, narrow, smooth-edged leaflets droop markedly from the rachis, and the termi¬ nal leaflets are virtually as long as the others, thus giving the impression that the end of each leaf has been chopped off (Figs. 1.11, 8.25). Furthermore, there is no series of reduced leaf¬ lets in the lower part of each leaf, so that the fronds, which are about a meter and a half long, have a rather sweeping appearance. The leaflets, articulated with the rachis, lack a midrib and the veins are parallel. The articulation of the leaves, which enables senescent leaflets to be shed indi¬ vidually, is unique to Microcycas, Ceratozamia, Zamia, and Chigua. It is a key character de¬ limiting these four genera from other cycads, all of which have nonarticulated pinnae, a feature

Figure 1.11. Leaf crown of Microcycas calocoma, show¬ ing the distinctive, “chopped off” appearance of the leaves. Note also the senescent leaf stalks (rachises) from which the leaflets have abscised (arrow).

that is discussed in some detail by Stevenson (1990a). Again, the cones of Microcycas are rather large. Both male and female sporophylls (microand megasporophylls) are covered with a short wool, and both have projecting truncatedconical shields that are notched at the apex (Fig. 1.12). The latter feature may indicate a relation¬ ship with Ceratozamia, in which the shield is surmounted by a pair of prominent spines (Color Fig. 112; Fig. 1.3). The overall appearance of the male and female cones is one of great geometric regularity, for the sporophylls fit very closely together and appear to be arranged in vertical rows even though their phyllotaxy is basically spiral. In mature males of Microcycas, a new cone (sometimes two or three) appears in early June, matures during July and August, and releases pollen in early September. The spent cone may persist several months; meanwhile, a new an¬ nual crown of 15-20 fronds is formed, the crown having a distinctive spherical form, as in Fig. 1.11. Female individuals also initiate a sin¬ gle cone in early June, but only in alternate years. The cone is pollinated in September and persists until the following June. Because a flush of new leaves is not produced during this period, the fronds of a cone-producing female

16

The Biology of the Cycads

Figure 1.13. Female cone of Ceratozamia mexicana, showing the pairs of horns on the sporophyll ends.

Figure 1.12. Female sporophyll shields of Microcycas calocoma, showing the vertical cleft in the sporophyll ends, especially evident near the insertion of the pencil,

persist for two years before they are replaced by a new flush. By that time they have become rather worn and tattered-looking. A final unique, and perhaps primitive, char¬ acteristic of Microcycas is the production of supernumerary gametes. The female gametophyte contains a large number of archegonia (nearly 100, most of them incomplete and lack¬ ing eggs), and as many as 16 male gametes are produced in each pollen tube (Figs. 3.30, 3.37). In all other cycads, six or fewer archegonia are present in a female gametophyte, and with the occasional modest exception of Ceratozamia only two male gametes are produced per pol¬ len tube.

Ceratozamia Ceratozamia, literally the “homed Zamia,” is a genus restricted in nature to Mexico, Gua¬ temala, and Belize, mainly in dense, moist woodland (Figs. 1.2, 8.1, 8.2), but also widely cultivated. Much of our understanding of the

occurrence of Ceratozamia in its native Mexi¬ can habitats has come from the exploratory work of Chamberlain (1919) and his colleagues and students. (The field aspects of this work were carried on simultaneously with those of Dioon, described above.) In recent years, this base of information has been greatly augmented by a group of botanists from Mexico and Italy (see Moretti and Sabato, 1988). In its vegetative state, Ceratozamia is much like certain robust species of Zamia (e.g., Z. poeppigiana), but differs markedly in its cone characteristics. The shield-shaped ends of both male and female sporophylls, each equipped with pairs of sharp, outwardly curving spines or “horns,” are responsible for the vernacular name “homcone” (Fig. 1.13). If one should shave off these stout spines, the cone would be much like those of some of the larger species of Zamia, (e.g., Z. poeppigiana, Z. roezlii). Over¬ all, Ceratozamia gives evidence of a close rela¬ tionship with Zamia but even closer affinities with Microcycas, and the latter relationship has been underscored by phylogenetic analyses using chloroplast DNA restriction fragment length polymorphisms (Fig. 1.14). (Caputo et al., 1991). The chromosome number in all species of Ce-

Features, Genera, and Relationships

ratozamia, 2n =16, is the same as that for many species of Zamia, and Chamberlain (1926b) ob¬ tained hybrid offspring of crosses of C. mexi¬ cana and Z. monticola. He reported that the foli¬ age of the hybrid resembled that of C. mexicana, but the embryos were similar to those of Zamia (Zamia is dicotyledonous, whereas Ceratozamia was then thought to be monocotyledonous, a condition, however, that has recently been dis¬ puted; see Caputo et al. 1985-1968). All species of Ceratozamia are basically ar¬ borescent, though the stems are rarely more than about 1 meter tall. The unbranched trunks, often leaning or curved, are covered with stout, per¬ sistent leaf bases and cataphylls. A seedling rapidly develops a large taproot that persists and enlarges further as the plant matures. Many fi¬ brous branch roots are present, as well as coralloid roots, the latter containing cyanobacteria and therefore of a bluish green cast (Color Figs. 11,52). The leaves in this genus are often long and curving, approaching 3 meters in C. mexicana, and always once-pinnately compound. Except in C. kuesteriana, both rachis and petiole are armed with sharp prickles. As in Microcycas and Zamia, the leaflets are articulated with the rachis and shed separately; the vernation is straight. Ceratozamia leaflets are in most cases comparatively long (to about 50 cm) with re¬ spect to their width, which is variable as to spe¬ cies, from only about a centimeter in C. kues¬ teriana to as much as 10 cm in C. latifolia. The leaflets are smooth-edged, and except for basal dichotomies the veins are parallel. One species, C. hildae, has clustered pinnae, which give the frond the appearance of having whorls of leaf¬ lets (Figs. 8.6, 8.7). Ceratozamia cones are, of course, the most distinctive feature of the genus. They are rather variable in size: those of C. mexicana are large, the female cones being about 45 cm long by 10 cm in diameter; the male cones of C. mexicana are slender and become very elongate and re¬ curved at the time of pollen shedding, when they may attain a length of about 60 cm (Color Fig. 33). Pollen maturation occurs in October in cultivated C. mexicana, and fertilization — by means of large, typically multiflagellated spermatozoids-occurs in late January and early

17

February. The female cones become mature in June and July, some six to seven months later, when greenish yellow seeds are shed. A peculiarity of Ceratozamia shared only with Microcycas is the production of super¬ numerary spermatozoids rather than the pairs found in other cycads; in Ceratozamia, how¬ ever, it is a rare occurrence and only an occa¬ sional pollen tube is found to contain four sper¬ matozoids (Chamberlain, 1912a), whereas in Microcycas it occurs regularly and upwards of 16 are present (Caldwell, 1907). Another pecu¬ liarity of Ceratozamia is that its pollen tubes are somewhat elevated from the nucellus by stiltlike processes.

Zamia Among all of the cycad genera, Zamia is prob¬ ably the most difficult to characterize. The name is derived from the younger Pliny’s name for the cone of Abies (fir), and the genus includes the most ecologically and structurally diverse assemblage of species among all the cycads. Several years ago, Stevenson and Sabato (1986) listed all the legitimately described species, which at that time came to 47. Others have been added or revised since, as we will describe here¬ in. Complicating this and other enumerations of Zamia species is the frequency with which new species are being discovered and described, so that it is difficult to achieve a fixed grasp of the taxonomy of the group. Chromosome numbers and chromosome morphology (karyotype) also suggest that the genus is genetically more plastic than are the other genera of cycads (Moretti, 1990a, b; Moretti et al., 1991). After Cycas, Zamia is the most wide-ranging cycad genus; although restricted to the Amer¬ icas, it occurs from Florida and the Caribbean Islands, through Mexico and Central America, to South America, as far as Brazil, Chile, and Bolivia (Fig. 8.24). Many botanists think of the genus as a group of rather small plants with underground stems, and several authors have considered Zamia to be basically geophilous (e.g., Chamberlain, 1935; Gaussen, 1950-1952; Greguss, 1968). Greguss, for example, in his otherwise excellent survey of the vascular anatomy of cycads, included only

18

The Biology of the Cycads

one arborescent species of the genus (Z skinneri). Seven of the other eight species of Zamia he studied have subterranean stems, and six of these were later reduced to synonymy with Z pumila (Eckenwalder, 1980a). Gaussen (1950-1952) presented a phylogeny of cycads in his survey of fossil and extant gymnosperms, and, on the basis of Z pumila and its under¬ ground stem, placed the genus at the base of his cycad series as the most primitive. His rationale is that species with reduced stems must be prim¬ itive, more advanced taxa being characterized by arborescence. In actuality, the stems of many species of Zamia are quite variable. Al¬ though the stems of the majority are mainly or wholly subterranean (Fig. 1.6), naked and often branched, and in some cases only a few centi¬ meters long (Z. pygmaea), the trunks of others can be above ground and fairly high (Figs. 8.60, 8.70,8.72). A few forms, particularly those from dense tropical forests in the southwestern part of the range, such as Z poeppigiana, Z obliqua, and Z. roezlii, have trunks several meters tall. Unlike the trunks of most other arborescent gen¬ era, however, these are clothed in leaf bases and cataphylls only at the apex. Arnold (1953) refers to forms of cycads with subterranean stems as “persistent juveniles,” and a more recent interpretaton (Norstog, 1980) is that they are in fact rather specialized, the more primitive forms being represented by equatorial and subequatorial species with rela¬ tively large trunks. The subterranean stems of many, perhaps all, cycads are specializations for survival during and after the periodic brushfires that sweep through their grassland or scrub¬ land habitats, as for example the pine-palmetto woodland in which the Florida cycad, Zamia integrifolia, often occurs (Color Fig. 70). Ecologically, Zamia demonstrates a consider¬ able capacity for niche exploitation. Schutzman et al. (1988) describes a species of cliff¬ dwelling Zamia, which they named Z. cremnophila. Zamia cremnophila grows on vertical limestone cliffsides; its underground stems, or tubers, develop in crevices and cracks in the rock, and its fronds are lax and pendant. Al¬ though thus far its seed-dispersal relationships are unknown, the most obvious agents would appear to be rodents and perhaps birds.

Zamia pseudoparasitica, a true epiphyte, has almost the same growth form but lives high up in tree branches in the Panamanian rainforest (Figs. 8.57, 8.58). It is nourished to a consider¬ able degree by the products of its massive, ball¬ shaped aggregations of coralloid roots. It has been suggested (R. Dressier, pers. comm.) that squirrels are the agents of dispersal. The fronds of this cycad are markedly pendant, and it ap¬ parently does not survive on the ground, where erect fronds are the rule. When fully ripened, the seeds of many species of Zamia become rather sticky as their outer seed coats, or sarcotestas, break down and become mucilaginous. They then can be quite adhesive, as anyone who has cleaned Zamia seeds at this stage can testify, and it is possible that this feature is an aid in seed dispersal, especially in the case of Z psuedoparasitica. As is the case in mistletoes, whose sticky seeds adhere to bird’s beaks and tree limbs, the seeds of Z. pseudoparasitica may be similarly adapted to dispersal in an aerial existence. Among other diversely adaptive species, the small Caribbean species Z. integrifolia displays a tenacity and adaptivity that is truly remarkable. In Florida, and elsewhere in the Caribbean Ba¬ sin, Z. integrifolia is most often found growing on a substratum of limestone in pine-palmetto habitats of low relief (Color Fig. 121). At Fairchild Tropical Garden in Miami, remnants of the original habitat still support small but flourish¬ ing populations of Zamia. One such area was graded in about 1967 to make room for a house for the Garden’s director. A small lawn was planted and maintained by regular mowing, but despite the removal of all original surface vege¬ tation and subsequent efforts to maintain a smooth lawn, fronds of this little cycad con¬ tinued to push up through the grass for the next dozen years. Another nearby area of scrubland, of about 0.6 hectare, was destroyed by fire in 1980. It was subsequently leveled by bulldozer and all emerging vegetation was scraped away. The area was then sprayed with a weed killer before planting to rows of Ceiba. Even after this harsh treatment, a number of zamias survived, sending up new flushes of leaves. This tenacity of ground-loving cycads is due mostly to the resiliency of the subterranean

Features, Genera, and Relationships

stems, with their considerable store of starch, and to the ability of fragments of such stems to regenerate new roots and shoots. It was, in fact, the starchy stems that in some cases led to de¬ pletion of wild zamias in some regions of Flor¬ ida. Aboriginal peoples, particularly the Calusa tribe, collected and may even have planted Za¬ mia tubers for their starch, and the methods were perpetuated by the Seminole Indians of the Florida Everglades and, at the turn of the twen¬ tieth century, by early white settlers. These pio¬ neers relied on natural foods to a considerable degree, and a number of Zamia starch mills were in operation until local supplies of tubers were exhausted or were supplanted by a some¬ what more sophisticated agriculture (Fig. 4.7). In general, the stems and roots of Zamia are much like those of other cycads, with extensive pith and cortex and sparse vascular tissue (Color Fig. 7; Fig. 2.2). Taproots, found in those species of Zamia having subterranean stems, may per¬ sist for many years, but arborescent zamias often have extensive adventitious root systems, espe¬ cially in such forms as Z. roezlii, in which the larger stems fall to earth, take root, and once again turn upward. The roots of all species form coralloid rootlets that contain cyanobacteria. Zamia leaves, at least in general appearance, are likewise extremely variable, though always once-pinnately compound. On the whole, the species with the larger stems also have larger leaves, but a wide range of leaflet shapes and sizes occurs. In some cases the leaflets are nu¬ merous and spaced regularly along the rachis in common cycadalean fashion (more than 70 pairs per leaf in Z. chigua), but in others the pinnae are rather few in number and very broad. A Colombian species, Z. wallisii, for example, has fronds about 2 meters long, each usually bearing two to six large, paddle-shaped leaflets (Color Fig. 131), the widest found in any cycad (to 30 cm). The stem of this species is nonethe¬ less subterranean and of only modest dimen¬ sions (20-30 cm long). Generally, the widest leaflets are associated with growth in dense shade under rainforest canopies. Remarkably, some of these zamias have among the smallest male cones known (Color Fig. 130). In all cases within this genus the leaflets have parallel veins with basal dichotomies and are articulated with

19

the rachis, usually falling individually from the plant when they reach senescence. In the de¬ veloping leaf the vernation is slightly curved to straight, and that of the leaflets is slightly twisted to straight. In contrast to the variability of the vegetative structures, the cones are very uniform through¬ out the genus, except in size. Both male and female cones are compact structures with hex¬ agonal sporophyll ends (shields) that fit tightly together and appear to be arranged in vertical rows, although as in other cycads they are basi¬ cally arranged in a spiral (Color Fig. 1; Fig. 8.64). Female plants usually bear just one or two cones, and in nature these are not produced every year but on the average about every three years. Male plants produce cones pretty much on an annual basis and, unlike those cycads that bear one or two large male cones, many species of Zamia bear several to a dozen or more small cones (Fig. 5.7). These mature at different times, spreading out their pollen production over a number of weeks. The production of numerous, small cones appears to be an adaptation for in¬ sect pollination (Norstog and Fawcett, 1989). The genus Zamia, as presently constituted, is so large and varied that, alone among the Cycadales, it may eventually be subdivided into new genera, as our knowledge of the taxa increases.

Chigua The most recent addition to the genera of cy¬ cads is Chigua, a relatively small plant found in lowland wet-forest habitat in northwest Colom¬ bia, South America (Fig. 8.24). The name is an adaptation of that applied by Colombian Indians to several species of Zamia and to Acrostichum, a fern with similar foliage (Stevenson, 1990b). Only a few specimens have thus far been col¬ lected, and comparatively little is known of its structural and functional characteristics. Its stems are subterranean, and the fronds are erect, with prickly petioles and somewhat femlike pin¬ nae (Figs. 8.9, 8.11). The most unique feature of Chigua is its leaf venation; its leaflets are subopposite and have definite midribs, with branch veins departing at a low angle of about 40° (Fig. 8.9; Color Fig. 28). The only other cycad with similar pinnae

20

The Biology of the Cycads

Dioon Ceratozamia Microcycas Chigua Z. fischeri

N.

Nw

^X

X.

^*6%/ \99%S

X.

Z skinneri

5

\98%/^ 11

\

\

X

\90%/

\

14

V 13

\99%/

Xz i6 /25

Figure 1.14. A cladogram based on chloroplast DNA (cpDNA), showing possible evolutionary relationships among six genera of cycads. The species from which cpDNA was extracted are Cycas revoluta, Dioon edule, Ceratozamia mexicana, Microcycas calocoma, Chigua restrepoi, Zamia fischeri, and Z skinneri. The lastnamed species represents the Aulacophyllum complex within the genus, species of which have in the past been accorded separate generic status. The number below each branch interval indicates the number of synapomorphies (shared derived characters) supporting the clade above. The percentages indicate the number of times that that clade was monophyletic. (After Caputo et al., 1991)

venation is Stangeria (Color Fig. 28). Were it not for this feature, Chigua would undoubtedly be lumped with Zamia, as some botanists have suggested despite the unique leaf morphology. Recent studies of chloroplast DNA (Fig. 1.14) indicate a close relationship with Zamia, and the genetic distances do not appear to be greater between Chigua and Zamia than between Chi¬ gua, Ceratozamia, and Microcycas (Caputo et al., 1991; De Luca et al., 1995). The morphol¬ ogies of the male and female cones of Chigua differ somewhat from those of Zamia. They are slender and lack the abrupt expansion of the fer¬ tile region one sees in Zamia, but the peduncle in both male and female cones expands rather gradually until it merges with the fertile regions (Fig. 8.10). Eventually, the peduncle of the fe¬ male cone attains a length exceeding that of nearly all other cycads (an exception is the very long peduncle of the large, dangling female cone of Dioon spinulosum). The shields of the Chigua megasporophylls have depressed cen¬ ters with borders of six evenly spaced bumps. The seeds are red and resemble those of Zamia in both shape and color.

Systematic Relationships of the Cycadales In view of our fairly meager understanding of the evolution of the cycads, decisions about phylogenetic relationships above the family level are based pretty much on superficial char¬ acters and inferences. If these inferences even¬ tually prove to relate to what might actually have happened in the course of evolution in the group, that will have been due largely to intu¬ ition and luck. The reason for that contention is that connections between seed-plant lineages and their origins are buried so deeply in the (largely undiscovered) fossil record that one can often only guess at phylogenetic interrelation¬ ships. Even so, the extraction of possibly funda¬ mental characters at the morphological and mo¬ lecular levels, together with the multifactorial approaches now possible with computer analy¬ ses, gives hope that in coming decades some of these questions may be resolved.

Placement of the Cycadales within Seed-Plant Phylogenies Broad relationships between suprafamilial groups of seed plants have been analyzed by Crane (1985, 1988), Doyle and Donoghue (1986), Donoghue and Doyle (1989), and Loconte and Stevenson (1990). All but the lastnamed emphasize the relationships of primitive seed plants to angiosperms; Loconte and Steven¬ son confine themselves to phylogenies pertain¬ ing to cycads. In such models of evolutionary trees, cycads and medullosan pteridosperms (seed ferns) appear to represent one lineage, per¬ haps allied with several other kinds of seed ferns. Primitive and modem conifers and Ginkgo may constitute another branch system, with the Gnetales and the flowering plants (an¬ giosperms), and just possibly the Bennettitales (Cycadeoidales), making up a clade of reproductively advanced forms. To students of the cy¬ cads, such cladograms are interesting not only because they show a close relationship between the Cycadales and the extinct medullosan pteridosperms, but also because they remove them farther from the Ginkgoales, an order with

Character

OSP

{CHI}

LEP

+ + + + + + + + I + + I

MAC

+ + + + + + + + I + + I

ENC

+ + + + + + + + I + + I

DIO

+ + + + + + + + I + + I

MIC

+ + + + + + + + I + + + I

ZAM

+ + + + + + + + I + + + I

CER + + + + + + + + I + + + I

STA + + + + + + + +I+ + + + +I

BOW

+ + + + + + + + I + + + + + + I I l + l + l

CYC

Table 1.1. Characters and character states that serve to define the Cycadales in relation to each other and to other extant seed plants (these data were used in the preparation of Fig. 1.16)

O- »• + + o- + + + I o- o- 4- C-. c- C-.

+++++

I I

CN I I I

in I I l + l I I I I I I I++I

I I I I I I I I

CO

I

CT\

I I + + I + I + + I

I

I + + I + I + + I 1 + 1+ + I I I

I I++I + I + I I I + I+ +I

I I I l + l

l + l

I+ + +I I I I++I I I l + l

I+ + +I I I I++I + I I l + l

I+ + + I I I I + I

l + l I

I

I

I

l + l

I

I + I+ +I

I I

I

I

I + I

I

I I I

1 + 1 +

I

I I

I I

I I l + l

I I I I + + +

I + I +

I I I I

I I I I

X

W U (Nri'tin'Ohooa'O-N^i-iri'Ohcooo

Source: From Stevenson, 1990a: table 1, by permission of the New York Botanical Garden. Notes: + = apomorphic characters; - = plesiomorphic characters; ? = unknown. BOW = Bowenia, CER = Ceratozamia, CHI = Chigua (presented here for comparative purposes but omitted from the cladograms because the genus is insufficiently known), CYC = Cycas, DIO = Dioon, ENC = Encephalartos, LEP = Lepidozamia, MAC = Macrozamia, MIC = Microcycas, OSP = other seed plants, STA = Stangeria, and ZAM = Zamia.

+ • + I c-. e- c- I 4- I C-- C-- c-- I

22

The Biology of the Cycads

-- Spermatophyta — Cycadales --Cladospermae

Figure 1.15. A cladogram showing the postulated phylogenetic relationships of the seed plants. Sper¬ matophyta = all seed plants, including Cycadales; Cla¬ dospermae = Ginkgoales plus mesospermae; mesospermae = Coniferales plus anaspermae; anaspermae = Gnetales plus angiosperms. (From Loconte and Steven¬ son, 1990)

which they sometimes are associated because the two share, if only coincidentally, a charac¬ teristic found among no other known living seed plants, the possession of multiflagellated, motile male gametes. With variations, most cladograms of contem¬ porary seed plants suggest similar relationships. For example, Stevenson (1990a) presents a phy¬ logenetic tree based on an analysis of 39 seedplant character states (Table 1.1). These trees generally support the conclusions of Crane (1988), but differ as said in considering only living forms. Diagrams from Loconte and Ste¬ venson (1990) and Stevenson (1990a) depict re¬ lationships among seed plants (Fig. 1.15) and among the living cycads (Fig. 1.16). Interrelationships among the Families and Genera of Cycadales The genera of living cycads share so many basic characteristics that they all appear to have descended from a common ancestry rather than arriving at their current, shared-character states by convergent evolution (i.e., they are monophyletic). Moreover, all available paleobotanical evidence suggests that the present families must have originated in the very remote past, possibly in the late Paleozoic era, and certainly by the early Mesozoic. They are, therefore, not recent evolutionary innovations. More than

Figure 1.16. A cladogram showing the possible evolu¬ tion of 10 genera of Cycadales, based on 30 characters (see Table 1.1); Chigua is not included. The solid circles represent characters undergoing reversals; i.e., a rever¬ sion to an earlier state. The open ovals represent charac¬ ters exhibiting parallelism; i.e., the independent evo¬ lution of an identical character. The figures are those shown in Table 1.1, and the characters employed in con¬ structing Fig. 1.16 are named in Table 1.1. (From Steven¬ son, 1990a)

likely the living genera are the surviving rem¬ nants of at least four or five lineages that have been following separate evolutionary paths for a long time. Stevenson (1992) has placed these lineages into families and subfamilies, as shown in Table 1.2. These families and subfamilies have probably maintained their mutual distinctions at least since mid-Mesozoic times, although some mem¬ bers within each group (possibly genera and cer¬ tainly species) have changed markedly in some features, while retaining other characteristics in a comparatively unmodified state. In such a situ¬ ation, and with little help available from the fos¬ sil record, it is difficult to assess what the early interrelationships of at least some of the modem genera really were. This is especially true of Bowenia and Stangeria, which display unique

Features, Genera, and Relationships

Table 1.2. A provisional classification of the extant Cycadales Order Cycadales Suborder Cycadineae Family Cycadaceae Cycas Suborder Zamiineae Family Stangeriaceae Subfamily Stangerioideae Stangeria Subfamily Bowenioideae Bowenia Family Zamiaceae Subfamily Encephalartoideae Tribe Diooeae Dioon Tribe Encephalarteae Subtribe Encephalartinae Encephalartos Subtribe Macrozamiinae Macrozamia Lepidozamia Subfamily Zamiodeae Tribe Ceratozamieae Ceratozamia Subtribe Microcycadinae Microcycas Subtribe Zamiinae Zamia Chigua Source: From Stevenson, 1990a, 1992, by permission of the New York Botanical Garden.

foliar features (circularly arranged petiolar traces and twice-compound leaves in Bowenia, and femlike foliage with midribbed leaflets in Stangeria). Dioon seems to be an ancient genus showing a common Pangaean origin with the ancestors of Encephalartos, Macrozamia, and Lepidozamia (Sabato and De Luca, 1985; Moretti et ah, 1993).

Cycad Interrelationships Inferrable on Other Grounds Mindful of the need to assess the interre¬ lationships of living cycads on grounds other than morphological, anatomical, and reproduc¬ tive, botanists in recent years have increasingly turned to the cytological, chemical, and molecu¬ lar characteristics of the genera and species, with mixed results. The findings of some ol the more informative recent studies along these lines follow.

23

Chromosomes Sufficient information about cycad chromo¬ somes has accumulated during the past several decades to provide some generalizations about interrelationships, but not enough has been learned to provide much insight into the direc¬ tions in which evolution has worked among families, genera, and, especially, species. It is noteworthy that studies of chromosomal characteristics as a means of identifying possi¬ ble evolutionary pathways in at least the higher taxonomic rankings agree well with evidence provided by morphological studies. Thus living cycads differ in chromosome number (funda¬ mentally n- 9) from living conifers (fundamen¬ tally n - 12) (Khoshoo, 1961). This finding sug¬ gests that the two groups have been mutually distinct for a very long period, perhaps even since the middle of the Paleozoic. Nevertheless, both of these groups of gymnosperms have fewer and larger chromosomes, with a higher DNA content, than do the angiosperms. The majority of cycads of known karyotype (number plus morphology) are either 2n = 18 (Bowenia, Chigua, Dioon, Encephalartos, Lepi¬ dozamia, Macrozamia, Zamia [in part] or 2n 16 (Ceratozamia, Stangeria, Zamia [in part]). Cycas is 2n = 22, while the sole species of Microcycas is In = 26. A few species of cycads show chromosome numbers other than those common to the particular genus, but many spe¬ cies of Zamia have divergent chromosome num¬ bers (e.g., 2n =16, 2n = 18), and still other species have novel karyotypes (e.g., 2n = 22,23, 24, 25, 26, 27, and 28; Norstog, 1980, 1981; Moretti, 1990b; Moretti et al., 1991; Vovides and Olivares, 1996), which suggests that Zamia may be evolving more rapidly than genera such as Dioon and Ceratozamia, which show little karyotypic variation (Fig. 1.18). Zamia aside, the cycad karyotypes exhibit sta¬ ble patterns among species within such genera as Dioon, Encephalartos, and Macrozamia (all species in the three genera are 2n = 18, but see Abraham and Mathew, 1966, for a sole excep¬ tion: a specimen of E. hildebrandtii), and also reveal intergeneric similarities, as between En¬ cephalartos, Macrozamia, Lepidozamia, Bo-

24

The Biology of the Cycads

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