Cycad Classification:

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CYCAD CLASSIFICATION CONCEPTS AND RECOMMENDATIONS

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Cycad Classification Concepts and Recommendations Edited by

Terrence Walters and

Roy Osborne

CABI Publishing

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CABI Publishing is a division of CAB International CABI Publishing CAB International Wallingford Oxfordshire OX10 8DE UK

CABI Publishing 875 Massachusetts Avenue 7th Floor Cambridge, MA 02139 USA

Tel: +44 (0)1491 832111 Fax: +44 (0)1491 833508 E-mail: [email protected] Web site: www.cabi-publishing.org

Tel: +1 617 395 4056 Fax: +1 617 354 6875 E-mail: [email protected]

©CAB International 2004. All rights reserved. No part of this publication may be reproduced in any form or by any means, electronically, mechanically, by photocopying, recording or otherwise, without the prior permission of the copyright owners. A catalogue record for this book is available from the British Library, London, UK. Library of Congress Cataloging-in-Publication Data Cycad classification : concepts and recommendations / edited by Terrence Walters and Roy Osborne. p. cm Includes bibliographical references (p. ). ISBN 0-85199-741-4 (alk. paper) 1. Cycads--Classification. I. Walters, Terrence, 1955. II. Osborne, Roy. III. title QK494.C93 2004 585´.9´012--dc21 2003010044 ISBN 0 85199 741 4 Typeset by MRM Graphics Ltd, Winslow, Bucks Printed and bound in the UK by Cromwell Press, Trowbridge

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Contents

Contributors About the Editors Preface Acknowledgements 1. ‘We Hold these Truths …’ Terrence Walters, Roy Osborne and Don Decker

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2. Saving Ghosts? The Implications of Taxonomic Uncertainty and Shifting Infrageneric Concepts in the Cycadales for Red Listing and Conservation Planning 13 John Donaldson 3. Character Evolution, Species Recognition and Classification Concepts in the Cycadaceae 23 Ken D. Hill 4. Morphological Characters Useful in Determining Species Boundaries in Cycas (Cycadaceae) Anders Lindström

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5. Comments on Cycas, Dyerocycas and Epicycas (Cycadaceae) 57 Chia-Jui Chen, Ken D. Hill and Dennis Wm. Stevenson 6. Classification Concepts in Encephalartos (Zamiaceae) Piet Vorster

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7. Classification Concepts in Macrozamia (Zamiaceae) from Eastern Australia Paul I. Forster 8. Classification Concepts in Ceratozamia (Zamiaceae) Loran M. Whitelock

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9. Relationships and Phytogeography in Ceratozamia (Zamiaceae) 109 Andrew P. Vovides, Miguel A. Pérez-Farrera, Dolores González and Sergio Avendaño 10. A Morphometric Analysis of the Ceratozamia norstogii Complex (Zamiaceae) 127 Miguel A. Pérez-Farrera, Andrew P. Vovides, Luis Hernández-Sandoval, Dolores González and Mahinda Martínez 11. Hypotheses on the Relationship between Biogeography and Speciation in Dioon (Zamiaceae) 137 Timothy J. Gregory and Jeffrey Chemnick 12. Molecular Phylogeny of Zamia (Zamiaceae) Paolo Caputo, Salvatore Cozzolino, Paolo De Luca, Aldo Moretti and Dennis Wm. Stevenson

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13. Systematics of Meso-American Zamia (Zamiaceae) Bart Schutzman

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14. Zamiaceae of Bolivia, Ecuador and Peru Dennis Wm. Stevenson

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15. In Search of the True Tree: Guidelines for Classification Roy Osborne and Terrence Walters

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Appendix 1: The World List of Cycads Ken D. Hill, Dennis Wm. Stevenson and Roy Osborne Appendix 2: Glossary of Terms Encountered in Cycad Systematics Roy Osborne and Terrence Walters Index

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Contributors

Avendaño, S., Instituto de Ecologia A.C., Apartado Postal 63, Xalapa, Veracruz 91000, Mexico. Caputo, P., Dipartimento di Biologia Vegetale, Università degli Studi di Napoli Federico II, Via Foria 223, 80139 Napoli, Italy. Chemnick, J., Ganna Walska Lotusland, 695 Ashley Road, Santa Barbara, California 93108, USA. Chen, C.-J., Institute of Botany, Chinese Academy of Sciences, 20 Nanxincum, Xiangshan, Beijing 100093, China. Cozzolino, S., Dipartimento di Biologia Vegetale, Università degli Studi di Napoli Federico II, Via Foria 223, 80139 Napoli, Italy. Decker, D., Decker & Associates, Inc., PO Box 222153, Carmel, California 93923, USA. Donaldson, J., Kirstenbosch Research Center, National Botanical Institute, Private Bag X7, Claremont 7735, South Africa. Forster, P.I., Queensland Herbarium, Environmental Protection Agency, Brisbane Botanic Gardens, Mt Coot-tha Road, Toowong, Queensland 4066, Australia. González, D., Instituto de Ecologia A.C., Apartado Postal 63, Xalapa, Veracruz 91000, Mexico. Gregory, T.J., Montgomery Botanical Center, 11901 Old Cutler Road, Miami, Florida 33156-4242, USA. Hernández-Sandoval, L., Facultad de Biologia, Universidad Autónoma de Querétaro, Centro Universitario, Cerro Las Campanas S/N, Querétaro 76010, Mexico. Hill, K.D., Royal Botanic Gardens, Mrs Macquaries Road, Sydney 2000, Australia. Lindström, A., Nong Nooch Tropical Botanical Garden, 34/1 Sukhumvit Highway, Najomtien, Sattahip, Chonburi 20250, Thailand. De Luca, P., Dipartimento di Biologia Vegetale, Università degli Studi di Napoli Federico II, Via Foria 223, 80139 Napoli, Italy. vii

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Martínez, M., Facultad de Biología, Universidad Autónoma de Querétaro, Centro Universitario, Cerro Las Campanas S/N, Querétaro 76010, Mexico. Moretti, A., Dipartimento di Biologia Vegetale, Università degli Studi di Napoli Federico II, Via Foria 223, 80139 Napoli, Italy. Osborne, R., PO Box 244, Burpengary, Queensland 4505, Australia. Pérez-Farrera, M.A., Escuela de Biología, Universidad de Ciencias y Artes de Chiapas (UNICACH), Calzada Samuel León Brindis 151, Tuxtla Gutiérrez, Chiapas 29000, Mexico. Schutzman, B., Environmental Horticulture Department, University of Florida, 1525 Fifield Hall, Gainesville, Florida 32611-0670, USA. Stevenson, D.W., Institute of Systematic Botany, New York Botanical Garden, Bronx, New York 10458, USA. Vorster, P., Botany Department, University of Stellenbosch, Private Bag X1, Matieland 7602, South Africa. Vovides, A.P., Instituto de Ecología A.C., Apartado Postal 63, Xalapa, Veracruz 91000, Mexico. Walters, T., Montgomery Botanical Center, 11901 Old Cutler Road, Miami, Florida 33156-4242, USA. Whitelock, L.M., 4524 Toland Way, Los Angeles, California 90041, USA.

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About the Editors

Terrence Walters is the executive director of Montgomery Botanical Center, a botanical garden in Miami, Florida, that concentrates on scientifically documented population-based collections of cycads and palms. Since 1990, he has conducted numerous field expeditions to parts of Asia, Africa and the Americas to investigate and document the cycad flora of the world. He is on the board of directors of the Cycad Society, a member of IUCN’s Cycad Specialist Group and on the research faculty of Florida International University. (Photography by Mary Andrews.)

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About the Editors

Roy Osborne has been studying and growing cycads in Africa and Australia for more than 20 years. He is a member of the IUCN’s Cycad Specialist Group, and founder and first President of the Cycad Society of South Africa. Now living in Brisbane, Australia, he has published more than 100 scientific papers, books and book chapters and has participated in major international conferences on cycad biology. (Photography by Mary Andrews.)

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Preface

On 7 April 2002, the Cycad Classification Concepts (CCC) Workshop was convened at Montgomery Botanical Center in Miami, Florida, USA. Seventeen of the world’s leading authorities on cycad systematics were invited to participate in the workshop and to submit manuscripts for this volume. Fifteen of these systematists submitted manuscripts and 14 were able to attend the 3-day CCC Workshop. The purpose of the CCC Workshop was to develop a suite of classification guidelines in support of the advancement of an internationally accepted and stable evolutionary classification system for taxa in the Cycadales. Increased research activity in the field of cycad systematics has led in some cases to increased confusion. As researchers across the globe pursue the many new lines of inquiry provided by technological advances of the past two decades (e.g. DNA sequencing, random amplified polymorphic DNA analysis, etc.), focus on consensus for how the approximately 300 species of cycads should be classified has become clouded. There is an urgent need for guidelines that all cycad systematists can follow in the designation of species, species boundaries and species groupings. The CCC Workshop provided the venue for the development of these guidelines. Although workshops with a similar purpose have been held to examine critically the systematics of other plant groups, the CCC Workshop was uniquely designed using progressive business methodologies. Five arenas were identified as necessary for the planning and management of this event. The Personnel Arena dealt with the subject of who would be involved as CCC Participants, who would be on the CCC Support Team and who would be in leadership roles during the Workshop process. The Site Arena dealt with everything concerning the facilities required for the Workshop – such as rooms for the various events and work sessions, transportation, housing, furniture, catering and audio-visual equipment. The Operations Arena dealt with identifying and taking those actions required to xi

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produce the major product of the Workshop – this volume. The Planning Arena dealt with determining all of the tasks required, their flow, their content and their sequence – from the overall purpose and concept of the Workshop to the minute details associated with the organization and objectives of the Workshop sessions themselves. Finally, the Management Arena dealt with how all of the above would be led and managed. The first step was to bring in a management consultant, Don Decker, to support the Management Arena objectives and to oversee development of the other four arenas. The next steps were to articulate the purpose, or reason, for having the CCC Workshop, and to determine the products, or results, required to meet the purpose successfully. The overall process of actions that would be required to obtain the products was outlined and then the functioning capabilities, or resources, required for the process were identified. These processes and the development of the above five arenas provided the overall planning and execution structure for the CCC Workshop. Bringing together a group of world-renowned cycad systematists representing several countries, cultures and languages for consensus building can be difficult. That this event was successful is a tribute to the considerable work that took place prior to, during and after the Workshop by the CCC Support Team and the CCC Participants. The CCC Participants were 14 of the world’s leading and most respected cycad systematists. Paolo Caputo from the Università degli Studi di Napoli Federico II in Italy represented one of the largest concentrations of cycad systematists at any one institution in the world. The Naples cycad group has worked extensively on New World taxa. Participants representing Asia included Chia-Jui Chen from the Institute of Botany in Beijing, China, an expert on the cycads of China, and Anders Lindström, the cycad curator at Nong Nooch Tropical Gardens in Thailand. Lindström is one of the leading experts on the cycads of Thailand. Cycas lindstromii was named in his honour. John Donaldson, from the National Botanical Institute, and Piet Vorster, from the University of Stellenbosch, were the workshop’s representatives from South Africa. Donaldson is Chairman of the IUCN (World Conservation Union) Cycad Specialist Group. Vorster is currently the President of the Cycad Society of South Africa and is an authority on the African genus, Encephalartos. Due to the large number of active cycad systematists in Australia, this country was well represented at the workshop. Attendees included Paul Forster of the Queensland Herbarium, Australia’s expert on Macrozamia. Ken Hill, from the Royal Botanic Gardens in Sydney, is the world’s expert on the taxonomically difficult genus Cycas. Roy Osborne, who currently resides in Queensland and formerly lived in South Africa, began the development many years ago of the world list of cycads. Hill and Osborne recently published the authoritative work Cycads of Australia. Andrew Vovides directs the National Cycad Collection of Mexico, and has developed the concept of local conservation of native cycads by initiating projects in which local villagers create nurseries to grow native cycads from sustain-

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able seed harvests. Americans Tim Gregory and Jeff Chemnick continue to undertake extensive systematic fieldwork in Mexico. Their commitment to walking up every canyon in search of each and every population of a species is to be admired. Other participants from the United States included Bart Schutzman of the University of Florida, the editor of The Cycad Society Newsletter and expert on Meso-American Zamia. Dennis Stevenson of the New York Botanical Garden is the leading authority on Central and South American taxa and has published extensively on evolutionary concepts in the Cycadales. Loran Whitelock from California, after a decade of fieldwork, research and writing, has recently completed what will become the major reference work on the cycad flora of the world – The Cycads. Ceratozamia whitelockiana and Encephalartos whitelockii are named in recognition of Whitelock’s extensive research on the world’s cycad flora. The first session of the CCC Workshop, held on 7 April, created the opportunity for each CCC Participant to give a 20-minute oral presentation of their professional views on cycad classification concepts, systematics and taxonomy. This 1-day work session was organized as a symposium (CCC Symposium) that included invited guests. The second work session, conducted on day 2, focused on elucidating the beliefs and philosophies that the participants held to be true concerning cycad systematics. Also on day 2, during work session three, Katherine Kron of Wake Forest University presented a discussion on a relatively new and somewhat controversial approach to plant nomenclature called ‘phylocode’. On the third day of the Workshop, the fourth and fifth work sessions required that the CCC Participants come to alignment on a suite of classification concepts or guidelines that they, as a group, would support and encourage the use of presently and in the future. In this volume, Chapter 1 presents why the CCC Workshop was convened and the beliefs, or working hypotheses and assumptions, that the CCC Participants hold to be true for cycad classification. This chapter resulted from work sessions two and three. The final chapter, Chapter 15, based on the products obtained from work sessions four and five, summarizes the classification guidelines that the CCC Participants have agreed to follow, support and encourage the use of to produce a universally accepted stable classification system for the Cycadales. Prior to the Workshop, each CCC Participant submitted a manuscript to the editors. These manuscripts were detailed discussions of the oral presentations presented by the participants during the CCC Symposium (work session one). These manuscripts constitute Chapters 2–14 of this volume. In Chapter 2, John Donaldson discusses the practical need for a durable classification system in the Cycadales when dealing with cycad conservation issues and planning. In Chapters 3 and 4, Ken Hill and Anders Lindström critically examine the usefulness of various characters for defining species and species concepts within Cycas. Three of the CCC Participants, Chia-Jui Chen, Ken Hill and Dennis Stevenson, report on a study of a recently described genus in the Cycadaceae in Chapter 5. They present a methodology for how cycad systematists should critically evaluate proposed new taxa. Cycad experts Piet Vorster,

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Paul Forster and Loran Whitelock present their individual thoughts on infrageneric classification concepts for African Encephalartos taxa, Australian Macrozamia taxa and New World Ceratozamia taxa in Chapters 6, 7 and 8, respectively. Chapters 9 and 10 were submitted by the participants from Mexico, Andrew Vovides and Miguel A. Pérez-Farrera. Unfortunately, Miguel was not able to attend the Workshop. These two researchers evaluate the usefulness of characters for defining species and species complexes within Ceratozamia. Tim Gregory and Jeff Chemnick develop in Chapter 11 an exciting hypothesis that extant species of Dioon are the result of rapid evolution in a dynamic group of plants. Two of the participants, Paolo Caputo and Dennis Stevenson, along with their colleagues, report on a molecular study in Chapter 12 that examines the usefulness of molecular and morphological data sets when trying to develop a phylogenetic tree for species of Zamia. Results from Bart Schutzman’s extensive and detailed morphological studies on Meso-American species of Zamia are given in Chapter 13. Dennis Stevenson, in Chapter 14, presents a monograph on the Zamiaceae from Bolivia, Ecuador and Peru. His chapter illustrates many of the guidelines the participants discussed during the last day of the workshop concerning content, style and format for the type of publication resulting from floristic cycad research. Two appendices are included in this volume. Firstly, the ongoing discovery of new species and the continuous refinements to the taxonomy of the alreadyknown taxa mean that the list of ‘officially recognized’ taxa needs to be timeously revised. Appendix 1 gives details of the ‘World List of Cycads’ at the time the manuscript for this volume was submitted to the publisher and is based on ‘The Cycad Pages’ website (http://plantnet.rbgsyd.nsw.gov.au/PlantNet/cycad). Secondly, the interdisciplinary nature of work on cycad systematics has led to a large and complex vocabulary of terms, the precise meanings of which are sometimes obscure and occasionally misused. Appendix 2 provides a glossary of these terms, drawn up after extensive consultations with specialists, and amplified where possible with cycad-specific examples. For consistency with author citations for taxa, we have followed the International Plant Names Index (IPNI Website: http://www.ipni.org/ index.html) for the chapters and appendices. In Chapters 1–15, authors’ names are unabbreviated. They are cited when the taxon first appears within a chapter and are also cited when appropriate in figure captions and tables. For Appendix 1, authors’ names are abbreviated. Taxa known to be distinct by the authors of each chapter, but as yet not ‘officially’ published, are indicated by double quotes in Chapters 1–15. The work presented in this volume is not only a report on the current state of affairs in cycad classification, but also highlights areas of difficulty and leads to guidelines for meaningful future advances. We hope it will become a widely used reference for the benefit of all cycad researchers, enthusiasts, conservationrelated public and private agencies and students of plant systematics. Terrence Walters and Roy Osborne

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Acknowledgements

The directors, members, staff and volunteers of Montgomery Botanical Center (MBC) deserve thanks and gratitude for their commitment to planning, hosting and sponsoring the Cycad Classification Concepts (CCC) Workshop. The Workshop was the first of its kind held at MBC, and therefore demanded an extremely fast learning curve by the MBC Team. We hope they will consider organizing and hosting CCC Workshop II in the future. The Workshop was 11 months in the planning stage. Numerous meetings were held during this period to define clearly the purpose, expected products and agenda for the Workshop. Tim Gregory and William Tang provided much needed guidance during the early planning stages. Don and Sonja Decker are thanked for hosting a pre-Workshop planning session at their home in December 2001. At this 1-day session, Don Decker, Tim Gregory, Deena Walters and Terrence Walters clearly identified the purpose and the products expected from the Workshop, as well as plotting the 3-day agenda. Jeff Chemnick, Tim Gregory and Loran Whitelock provided encouragement and support throughout the entire planning period for the Workshop. Their input was much appreciated. The CCC Participants’ commitment to the success of the Workshop was greatly valued, given their own responsibilities and time constraints. They were truly an amazing group of individuals with whom to collaborate. The CCC Support Team oversaw the planning and logistics of the Workshop beginning in April, 2001. Jean Stark of Stark Connections took care of all the details associated with the participants’ travel and housing needs before, during and after the Workshop. Don Decker of Decker & Associates was the management consultant and leader for the Workshop. Katherine Kron of Wake Forest University was kind enough to lecture and field numerous questions on ‘phylocode’ during one of the work sessions. Evelyn Young planned and coordixv

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nated all of the on-site meals and events at MBC during the 3 days. Larry Noblick coordinated the audio-visual equipment and supplies required for the Workshop. Lee Anderson oversaw facility preparations for all of the events each day during the Workshop. Deena Walters and Mary Andrews documented the Workshop photographically. Mayna Hutchinson created magnificent cycad arrangements for all of the facilities used at MBC during the Workshop. Barbara Judd, Sue Katz and Eric Shroyer were scribes for the break-out groups. All of the above individuals, as well as their own support teams, ensured that every aspect of the Workshop ran smoothly and according to the agenda. The CCC Workshop was supported through grants from the Bressler Foundation, Ajax Foundation and General Mills Foundation. Libby and By Besse, Judith and Richard Bressler, Tim Gregory, Eileen and Loyd Kelly and Linda and Mark Smith were significant contributors to the Workshop. The commitment of these foundations and individuals to the Workshop was very much appreciated. The officers, directors and members of the Central Florida Palm & Cycad Society are acknowledged for providing support towards the publication of this volume. A number of individuals were involved in the preparation and publication of this volume. The Montgomery Botanical Center directors, members and staff gave the editors the time and resources to prepare the manuscript. The first editor gratefully acknowledges Deena Walters for graphic design and illustration production assistance and, most of all, for her support during the preparation of the manuscript. The second editor similarly acknowledges the support of the Osborne family and friends. Finally, we wish to express our thanks to Tim Hardwick and the many individuals at CAB International who have so professionally managed the publication aspects of this volume.

Cycad Classification Concepts Workshop support team seated from left to right: Terrence Walters; Jean Stark; Don Decker and Katherine Kron. (Reprinted by permission of Montgomery Botanical Center, Miami, Florida, USA.)

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Cycad Classification Concepts Workshop participants seated from left to right: Andrew P. Vovides; Ken D. Hill; Chia-Jui Chen; Roy Osborne; Paolo Caputo; John Donaldson; Loran Whitelock; Paul I. Forster; Dennis Wm. Stevenson; Jeffrey Chemnick and Piet Vorster. On the floor in front: Anders Lindström; Bart Schutzman and Timothy J. Gregory. (Reprinted by permission of Montgomery Botanical Center, Miami, Florida, USA.)

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Terrence Walters,1 Roy Osborne2 and Don Decker3 1Montgomery

Botanical Center, Miami, Florida, USA; 2PO Box 244, Burpengary, Queensland, Australia; 3Decker & Associates, Inc., Carmel, California, USA

Abstract In order to develop classification guidelines for the Cycadales, a workshop was held in April 2002, at Montgomery Botanical Center in Miami, Florida, USA. Fourteen internationally-renowned cycad systematists spent 3 days identifying and developing guidelines that would provide a stable, practical and informative classification scheme for cycads. The participants agreed that convening such a workshop was vital, timely and necessary to produce a universally accepted evolutionary classification for the Cycadales in the near future. Before developing the guidelines, the participants first needed to identify the assumptions, or beliefs, that they hold to be true about cycad classification. These beliefs are presented under three categories: (i) beliefs about biological relationships; (ii) beliefs about what systematists can and should do in order to understand biological relationships; and (iii) beliefs about what cycad systematists can and should do in order to understand relationships in the Cycadales.

Cycad Classification Concepts Workshop The field of cycad systematics, which focuses on all members of the plant order Cycadales, has seen a flurry of activity during the past 20 years. New species are being discovered and described on an annual basis. Existing species circumscriptions are being critically tested for their scientific soundness. Familial and generic circumscriptions and relationships are being re-evaluated by a number of laboratories worldwide. Certain key developments in recent years (e.g. advances in systematic technologies and tools; ease of international travel, including access to countries previously unavailable to systematists; horticultural demand for rare ©CAB International 2004. Cycad Classification: Concepts and Recommendations (eds T. Walters and R. Osborne)

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cycads; recognition of the rare and endangered status of cycads; and an urgency for cycad conservation in many countries) have collectively stimulated cycad systematists to try to better understand and manage the taxonomy of the world’s cycad flora. Today, field and laboratory equipment can quickly generate massive amounts of systematic data, which often far surpass the immediate needs of systematists. This is particularly true for molecular data, which are being analysed in a multitude of ways with a plethora of user-friendly software programs. Consequently, systematists sometimes find it difficult to decide which analyses are appropriate for their work and how to interpret the hundreds of statistical summaries produced from these computer programs. Also, with these wonderful new opportunities and ever-increasing knowledge of cycads, it is easy to lose sight of the ultimate mission, which is to provide a universally accepted, consistent and informative evolutionary classification scheme. Although scientists do not believe that any truth can be exactly known, it is the purpose of science to approach truths as closely as possible. Scientists are forced to perform this work in an unsteady grounding of assumptions. These assumptions are not self-evident, but arise from the observations and experimentations of previous researchers. So, for any particular scientific field, there is a collection of assumptions, or beliefs, based on previous work that forms the framework for further discovery. As the scientific method proceeds, these assumptions are subject to change, usually in the form of minor modifications but sometimes in the form of radical reassessment. But, whatever insights future inquiry may bring, current hypotheses and guidelines for future research must be rooted in presently held assumptions. The major objectives of this volume are to enumerate the currently held assumptions, or beliefs, in the field of cycad systematics, and to present guidelines for future systematic work within the Cycadales. These concepts were fleshed out during a Cycad Classification Concepts (CCC) Workshop held in April 2002, at Montgomery Botanical Center in Miami, Florida. The CCC Workshop provided a forum for cycad systematists to ‘regroup’ and clarify as a team what they believe to be true (the best working assumptions) and important in the realm of cycad systematics. The participants then went a step further, agreeing on a suite of guidelines that they would follow in support of actualizing the team’s beliefs when engaging in future research (see Osborne and Walters, Chapter 15 this volume). The participants agreed not only to follow these guidelines in their own systematic studies, but also to encourage the global use of these guidelines by all cycad systematists and students. This chapter attempts to record the beliefs raised by the participants during the CCC Workshop, whereas the final chapter enumerates the proposed guidelines for developing a useful, evolutionary-based classification system for cycads. Before presenting the beliefs, it is necessary to provide some background on cycads and systematics and to explain some terms that the reader will encounter either in the list of beliefs or in other chapters of this volume.

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What is a Cycad? Cycads are an ancient group of seed plants that evolved in the Carboniferous or early Permian, some 280 million years ago (Norstog and Nicholls, 1997). They reached their zenith of abundance and diversity in the Mesozoic era. Cycads are one of four groups (cycads, ginkgos, conifers and gnetophytes) that are collectively and commonly referred to as gymnosperms. The Cycadales (the order containing all cycad families) is considered to be monophyletic. A monophyletic group is composed of an ancestor and all of its descendants based on a suite of shared derived characters, called synapomorphies. Some synapomorphies within the Cycadales include girdling leaf traces, a specialized pattern of vascular bundles in the petiole, distinctive meristems, buffer cells surrounding the archegonium, and the presence of mucilage canals, methylazoxymethanol glycosides and the non-protein amino acid BMAA (β-n-methylamino-L-alanine). Coralloid roots (specialized roots that host cyanobacteria) are found in all cycad taxa. Cycads also bear cataphylls, which are scale-like leaves that serve to protect the apical meristem. Cycad reproductive structures typically occur in cones, with each strobilus consisting of an axis and a series of spirally arranged megasporophylls (‘leaves’ bearing ovules) or microsporophylls (‘leaves’ bearing pollen sacs). All cycads are dioecious, with male and female reproductive structures on separate plants. Insects appear to be the primary vectors for pollination, although wind may be a factor for some genera (see discussion by Grobbelaar, 2002). Although not fully substantiated yet, evidence is accumulating to suggest coevolutionary processes between cycads and their pollinators. Once these processes are uncovered, resulting data will probably have a significant impact on how cycad taxa are classified. All genera except Cycas Linnaeus form a determinate female cone. In Cycas, the female ‘cones’ are indeterminate. Ovules are borne on loosely arranged whorls of megasporophylls (for an interpretive discussion on female ‘cones’ in Cycas, see Norstog and Nicholls, 1997). Cycad seeds usually have a brightly coloured, fleshy outer layer called the sarcotesta that encourages dispersal by animals. Birds, rodents and probably many other animals disperse cycad seeds by digesting the sarcotesta and dropping the stony layer and its contents away from the mother plant (Hill and Osborne, 2001). Seeds of some species of Cycas have a thick layer of spongy tissue, instead of the usual fleshy layer. This spongy layer allows these seeds to remain buoyant and viable for long periods of time in salt water. This may explain the wide distribution of this genus compared with the narrower ranges of other cycad genera. With the exception of Cycas, all cycad genera are restricted to single landmasses (Jones, 2002). Encephalartos Lehmann and Stangeria T. Moore occur only on the continent of Africa. Bowenia Hooker ex Hooker filius, Lepidozamia Regel and Macrozamia Miquel are endemic to Australia. Microcycas (Miquel) A. de Candolle is restricted to the island of Cuba. Ceratozamia Brongniart, Chigua D.W. Stevenson, Dioon Lindley and Zamia Linnaeus are endemic New World genera. Cycas is found

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in subtropical and tropical countries of the Old World that have Pacific or Indian Ocean coastlines and in neighbouring countries. Although cycad taxa are widely distributed in subtropical and tropical regions worldwide, extant populations are often widely disjunct. A cycad population is frequently found as an isolated pocket of individuals quite far removed from other such pockets. A major dilemma that faces today’s cycad systematists is understanding the evolutionary histories and futures of these populations. Part of the problem is determining whether these populations have been artificially separated because of human fracturing of the habitat, or are naturally occurring entities that are either gradually going extinct, are restricted to a very specialized niche, or are continuing to evolve as separate entities.

Cycad Taxonomy and Systematics Taxonomy is the process of circumscribing and assigning scientific names to the diversity of taxa, and then ordering this diversity into an appropriate classification system. In the realm of biology, a ‘taxon’ (plural ‘taxa’) is a group of individuals given a proper name or a group that could be given a proper name. For example, the taxon Dioon includes all named and as yet unnamed groups of individuals within this genus. An important aim of the cycad systematist is to describe and name only ‘natural taxa’ and to place these in a classification system that represents the order of nature. A natural taxon is a taxon that exists in nature independent of human ability to perceive it. It can be discovered, but not invented (Wiley, 1981). The same assumption can be applied to the order of nature, i.e. that it can be discovered for what and how it is. The basic assumption for biological order is that it is based on reproductive ties (genealogy) as they are affected by the process(es) of evolution. Classification is the process of organizing knowledge so that it facilitates communication and comprehension. The objectives of classification are: (i) to define and distinguish among ‘kinds’; and (ii) to position these kinds in a system that reflects their natural relationships and imparts information about these kinds. A classification system is a human construct that attempts to make natural order comprehensible to the human mind. The classification of biological organisms has its own language and rules of language use. For assigning a taxonomic name and having the name recognized by the botanical community, cycad systematists must follow recommendations outlined in the most recent edition of the International Code of Botanical Nomenclature (ICBN; Greuter et al., 2000). These recommendations are built on a hierarchical system of classification wherein each level of the hierarchy is referred to as a distinct rank. Typical ranks of use in the field of cycad systematics start with the all-inclusive ‘order’ (Cycadales) and move down to increasingly less inclusive ranks such as family (e.g. Zamiaceae), genus (e.g. Macrozamia), section (e.g. Parazamia) and species (e.g. Macrozamia lucida). The basic rank of species holds a special place in terms of the usefulness and importance of bio-

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logical entities to humanity; therefore, most cycad systematists undertake studies at the species level. Cycad systematics is the study of the cycad diversity that exists on earth today and the evolutionary history of this diversity. One of the main objectives is to convey knowledge about the genealogical relationships among cycad taxa in a hierarchical system of classification. The field of cycad systematics often requires that systematists have knowledge from many other scientific disciplines, such as taxonomy, morphology, ecology, molecular biology, pollination biology, anatomy, embryology, genetics, physiology, phytochemistry and palaeontology, so we are better able to uncover the true genealogical relationships among taxa. The number of described cycad species has almost doubled since 1985. Today, over 300 species are known (see Hill et al., Appendix 1 this volume) and many researchers believe the number may reach as many as 400 species when all potential cycad habitats have been investigated and taxonomic studies have been completed. Exactly what constitutes a cycad species remains unclear. Defining what makes a species is not a problem limited to cycad taxonomists, but is a basic source of consternation throughout the biological world. Generally, delimitation of a population or suite of populations as a new species is based on the training, background, knowledge and the basic scientific philosophy of the describer. No unified concept is in place to guide cycad systematists in defining and circumscribing new species. A variety of species concepts are used throughout the biological world. One of these, the biological species concept, does not work particularly well with cycads. The major premise of the biological species concept is that individuals within a species, when tested, are interfertile, while interspecific individuals are not. However, clearly defined and widely accepted species within a number of cycad genera can produce viable offspring with one or more other species in the same genus (Norstog and Nicholls, 1997). Consequently, cycad systematists generally agree that interspecific fertility, when tested, is just another character for systematic studies, and that the character of interspecific sterility should not be unduly weighted in the determination of cycad species. Moreover, the determination of the production of fertile offspring from putative hybrids is not practical for those species, like cycads, with long life cycles. Another out-of-favour species concept for cycad taxonomists is the phenetic species concept. This concept defines a species based on the overall similarity of its individuals combined with a significant gap in variation when these individuals are compared with individuals of another species. In practice, this qualitative approach does not always define natural taxa (Judd et al., 1999). The CCC Workshop participants agreed that the most common (unstated, but de facto) species concept in use by cycad systematists is what they termed a ‘morphogeographic’ species concept. This concept recognizes the importance of both morphological characters and geographical isolation in circumscribing a species. The large geographical disjunctions among cycad populations have greatly influenced the cycad systematist’s species concept. These disjunct populations are viewed as maintaining separate identities and having their own evolu-

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tionary tendencies and fates. In this respect, the cycad systematist’s view is a form of the evolutionary species concept. By the end of the CCC Workshop, participants were still not able to agree on exactly what constitutes a cycad species. This was not surprising, since cycad lineages have a variety of unique and long histories. Species differ to varying degrees and, therefore, a single species concept does not work for all cycads. Today, data from a wide variety of sources, including molecular analyses, ecology, geography, pollination biology and life history strategies, are providing independent measures of the evolutionary reality of existing and proposed species in the Cycadales. In contrast with species, circumscriptions of cycad genera are clearly defined and stable, with the possible exception of Chigua, which may be congeneric within Zamia (Whitelock, 2002; and see Caputo et al., Chapter 12 this volume). Cycad genera can usually be identified using gross vegetative features and can always be identified with gross features of the female reproductive structures. Family circumscriptions within the Cycadales are still somewhat unclear, being confounded by the age of the group and the inability of cycad systematists to decide on the amount of character differentiation required for family recognition within the order. Three to four families are typically recognized, with the only uncertainties revolving around the placement of two genera, Stangeria and Bowenia. Given recent advances in molecular systematics and the number of laboratories actively studying generic and familial relationships, it is predicted that a stable familial classification will be available in the very near future. Historically, the characters chosen, the importance of specific characters for differentiating genera and species, and the analyses used for describing new cycad species have been left to the discretion of each investigator. Vegetative characters, especially those associated with the leaf, along with characters related to various aspects of the female reproductive structure, are commonly used for distinguishing taxa. Male cone characters are usually not used for differentiating taxa. Cycad systematists are well aware of the plasticity of various morphological features among plants within a taxon, especially when plants are brought under cultivation. However, the degree of plasticity and the taxonomic importance of this plasticity continue to remain unclear. Another ongoing problem for cycad systematists is the lack of a consistent terminology for describing morphological features that are unique within the Cycadales. This lack of standardized morphological terminology creates problems when trying to compare characters in one taxonomic description with those in another description, or when trying to identify an individual plant based on specific characters. For this reason, a glossary of terms commonly encountered in cycad systematics is included in this volume (see Osborne and Walters, Appendix 2 this volume).

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Cycad Phylogenetics – Uncovering Genealogical Relationships Although never really attainable, systematists work toward producing a natural classification system that arranges taxa in a way that reflects the natural evolutionary order of the taxa. Since the first basic assumption is that the natural order is created by the process(es) of evolution, systematists typically strive to produce an evolutionary classification scheme. More specifically, phylogeneticists aim to recover the broad genealogical lineages within a group of taxa and to produce a classification system that reflects these genealogical or phylogenetic relationships. The starting point in phylogenetic analysis is usually the divergence of a previously occurring lineage into two or more progeny lineages. The next step is to reconstruct the separation of these lineages by identifying changes, or modifications, in characters. A character is a feature having one or more states that can be described, figured, measured, weighed, counted, scored or otherwise communicated from one systematist to another. Certain characters are biologically connected to the concept of genealogy and these characters can provide cycad systematists with justification for group membership in a phylogenetic tree. These types of characters are called apomorphies. An apomorphic character (sometimes referred to as a specialized character or a derived character) has evolved directly from its pre-existing homologue (Wiley, 1981). The task of phylogeneticists is to attempt to discover those characters that reflect the phylogeny of natural taxa. Because species are considered to be naturally occurring entities, by inference, phylogenetic characters are inherent to species. A phylogenetic character is one in which its occurrence in two or more taxa is believed to be the product of descent from a shared ancestor. A phylogenetic character shared by two organisms implies a phylogenetic relationship. Of particular importance is the synapomorphy, which is a genealogically shared, derived character state that arose in an ancestor of a lineage and is present in all of that lineage’s descendants (Hennig, 1966). Synapomorphies are the strongest evidence for shared ancestry. They are distinguished from symplesiomorphies, which are earlier character states that are shared by members of a lineage and by a more ancient ancestor to the lineage. In practice, symplesiomorphic versus synapomorphic character states for a lineage are determined by comparison with an outgroup (i.e. a related taxon that is not part of the monophyletic lineage being examined). The outgroup of choice is the ‘sister group’ to the lineage, which is genealogically the closest non-ancestral relative of the lineage. In other words, two or more taxa are sister groups if they share an ancestor not shared by any other taxon. Phylogenetic studies depict results by a graphical representation of the genealogy of one or more descendants from a common ancestor. Phylogenetic trees are branching diagrams that portray the hypothesized genealogical relationships and sequence of historical events linking taxa. A clade within a phylogenetic tree incorporates the common ancestor of a group and all of its descendants.

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Cycad systematists use phylogenetic trees to try to produce a phylogenetic classification that reflects the best estimate of the evolutionary history of cycads. Construction of a classification based on a phylogenetic tree essentially involves two steps: (i) the delimitation and naming of groups that are monophyletic in the tree; and (ii) the ranking of these monophyletic groups and placement of them into a hierarchical classification system (Wiley, 1981). Phylogenetic studies do not always lead to a new classification. These studies can provide support to an existing classification. Also, naming every monophyletic group would become cumbersome and in some cases not provide any additional information to the end-user. Cycad systematists continue to put forth hypotheses about the genealogical relationships among taxa in the Cycadales. These hypotheses are tested with evidence derived from a wide variety of sources. Hypotheses and test results are published, usually peer-reviewed, and evaluated, and some phylogenetic trees are provisionally chosen over others. In other words, the evolutionary tree for the Cycadales continues to be tested as additional and new types of data become available. An important conclusion made by the CCC Workshop participants was that the knowledge of genealogical relationships among taxa should be placed in an unambiguous and stable natural classification system that is useful for a multitude of end-users and purposes. It is believed that such a system can orient human understanding of life and the world around us.

CCC Workshop Beliefs The CCC Workshop participants enumerated their beliefs concerning cycad classification during the second day of the Workshop. Clarity and consensus with regard to these beliefs were needed so that the participants could go on to produce a final set of guidelines for future research aimed at establishing a suitable classification scheme for cycads (see Osborne and Walters, Chapter 15 this volume). For purposes associated with the production of this chapter, the suite of beliefs generated during the work sessions at the CCC Workshop has been reworded and organized to provide consistency in wording, style and format. The authors have organized the beliefs under the following three categories: (i) beliefs about biological relationships; (ii) beliefs about what systematists can and should do in order to understand biological relationships; and (iii) beliefs about what cycad systematists can and should do in order to understand relationships in the Cycadales.

Beliefs about biological relationships ● ●

We believe there is value in the biological world. We believe there is a natural order to the biological world.

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We believe that the natural order is based on genealogical relationships. We believe that the pattern of genealogical relationships naturally produces a hierarchical structure of lineages. We believe that each species (as a natural group) is a monophyletic lineage that evolves independently of other such lineages.

Beliefs about what plant systematists can and should do in order to understand biological relationships ●

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We believe we can construct hypotheses that are testable, and that the process of testing and refining hypotheses leads to a better understanding of the natural world. We believe that genealogical relationships can be recovered through hypothesis testing. We believe that as technology, resources and data increase and change, we will be better able to construct a classification scheme that approximates true genealogical relationships. We believe that we should construct hierarchical classification schemes that best reflect actual genealogical relationships. Such schemes have greater predictive power, have greater heuristic value, and improve our ability to understand and communicate about the biological world as it existed, as it exists, and as it may exist in the future. We believe that the process of refining classification schemes brings us closer to approximating true genealogical relationships and therefore converges towards stability of the classification. We believe that the most important evolutionary entity to define and circumscribe is the species. We believe that species are not evolutionarily static (i.e. they change through time). We believe that species can be difficult to recognize, and, therefore, the definitions and circumscriptions that we apply to particular species are hypotheses to be tested. We believe that the exploration of species and species concepts will provide the common language for understanding speciation, species interactions and plant systematics. We recognize the existence of the International Code of Botanical Nomenclature (ICBN) and support the beliefs, philosophies, and principles of the Code to provide one correct name for each taxonomic group within a stable classification system. We believe that systematists should share information through the publication of data and analyses.

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Beliefs about what cycad systematists can and should do in order to understand relationships in the Cycadales ●

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We believe that the Cycadales forms a distinct monophyletic lineage, and genealogical relationships within this lineage can be inferred through the collection and analysis of data. We believe that higher ranks in the Cycadales (e.g. genera and above) are easily recognizable and definable. We believe that the greatest challenge in cycad systematics is recognizing appropriate units to call species. We believe that there are differing opinions concerning cycad species definitions and circumscriptions. Given the uncertainty of species definitions and the lack of infraspecific data on cycads, we believe that it is not yet appropriate to try to define and identify relationships of taxa below the species level. We believe that to better understand cycad species, we must concentrate our resources on variation and relationships at the population level. We believe that there is a wealth of available data on cycads that still must be captured and analysed. We believe that a classification system should be valuable for a variety of known and unknown end-users and purposes. We believe that the extinction of cycad species is accelerating and that access to native populations is decreasing rapidly. Actions must be undertaken immediately to describe, classify, conserve and preserve species for continuing scientific studies. We believe that the process of understanding cycad systematics should be a collaborative endeavour.

Acknowledgements The Cycad Classification Concepts Participants spent many hours developing and discussing the suite of beliefs presented in this chapter. Their commitment to and support of undertaking this long and arduous task is greatly appreciated. The authors are deeply indebted to Deena Walters for her critical comments on early drafts of this manuscript.

References Greuter, W., McNeill, J., Barrie, F.R., Burdet, H.M., Demoulin, V., Filgueiras, T.S., Nicolson, D.H., Silva, P.C., Skog, J.E., Trehane, P., Turland, N.J. and Hawksworth, D.L. (2000) International Code of Botanical Nomenclature (Saint Louis Code). Koeltz Scientific Books, Köningstein, Germany, 474 pp.

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Grobbelaar, N. (2002) Cycads – with Special Reference to the Southern African Species. Published by the author, Pretoria, South Africa, 331 pp. Hennig, W. (1966) Phylogenetic Systematics. University of Illinois Press, Champaign-Urbana, Illinois, 263 pp. Hill, K. and Osborne, R. (2001) Cycads of Australia. Kangaroo Press, New South Wales, Australia, 116 pp. Jones, D.L. (2002) Cycads of the World – Ancient Plants in Today’s Landscape, 2nd edn. Reed New Holland, Sydney, Australia, 456 pp. Judd, W.S., Campbell, C.S., Kellogg, E.A. and Stevens, P.F. (1999) Plant Systematics: a Phylogenetic Approach. Sinauer Associates, Inc., Sunderland, Massachusetts, 464 pp. Norstog, K.J. and Nicholls, T.J. (1997) The Biology of the Cycads. Cornell University Press, Ithaca, New York, 363 pp. Whitelock, L.M. (2002) The Cycads. Timber Press, Portland, Oregon, 374 pp. Wiley, E.O. (1981) Phylogenetics: the Theory and Practice of Phylogenetic Systematics. John Wiley & Sons, New York, 439 pp.

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Saving Ghosts? The Implications of Taxonomic Uncertainty and Shifting Infrageneric Concepts in the Cycadales for Red Listing and Conservation Planning

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John Donaldson Kirstenbosch Research Centre, National Botanical Institute, Claremont, South Africa

Abstract A comparison of the cycad Red Lists from 1978 to 2002 shows that taxonomy has had a profound influence on the outcomes of the Red List process. The descriptions of new species, as well as taxonomic revisions, have increased the number of recognized cycad taxa from 136 in 1978, to over 300 at the time of publication. During this time, the proportion of threatened taxa has fluctuated from a low of 46% of all cycad taxa in 1978, to a high of 82% in 1997, and is currently estimated to be 52%. At least one-third of the changes in the Red List are due to taxonomic changes, which reflects an increase in taxonomic activity between 1978 and 2002. In addition to new species, there were 48 changes in the Red List between 1978 and 2002 as a result of uncertainty about the infrageneric status of cycad taxa. Frequent changes in threatened status are not helpful for conservation planning and could even undermine the Red List process. The IUCN has introduced robust criteria for Red Listing to deal with inadequate population data and ecological uncertainty. The results of this analysis show that cycad taxonomists need to develop consistent and widely accepted concepts for infrageneric taxa to reduce the influence of taxonomic uncertainty on the Red Listing process.

Introduction Ongoing assessment of the threatened status of the world’s cycad flora (Red Listing) is an essential process for conservation planning and actions (Osborne, ©CAB International 2004. Cycad Classification: Concepts and Recommendations (eds T. Walters and R. Osborne)

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1995; Donaldson, 2003). Having a clear picture of which cycads are most threatened with extinction, and where they are located, enables conservation agencies and funding bodies to allocate resources to the most threatened taxa or to the most effective conservation actions. Red Listing and conservation planning are dynamic processes. Typically, Red Listing assessments are based initially on inadequate information and they are modified as more information becomes available. As a result, changes in threatened status are unavoidable, and they can come about for several reasons: ●

●

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Actual changes in plant distribution or abundance due to ongoing threats or to the success of conservation actions. The discovery of new populations or additional demographic data that provide more accurate estimates of population numbers and trends. Changes in the criteria used for assigning threatened status. The discovery of previously unknown species. Taxonomic revisions that result in the splitting of existing species into several taxa or the lumping of several described species into one species.

Frequent changes in Red List status are not helpful for conservation planning and they may even undermine the credibility of Red Listing as a conservation tool. The aim of Red Listing should be to create a reasonably stable and scientifically based system that can portray real changes in the distribution and abundance of threatened species as well as the relative status of different species. To achieve such a system, the IUCN introduced revised categories of threat and more rigorous criteria for assessing threatened status (IUCN, 1994; IUCN/SSC Criteria Review Working Group, 1999; Mace, 2000). The revised system provides a framework for dealing with the uncertainty that arises from using inadequate ecological data to assess threatened status. However, the IUCN system does not deal specifically with an important area of uncertainty in threat assessments, i.e. the taxonomic status of threatened species. Clearly, a credible Red List relies on a consistent and widely accepted system of classification. Within the Cycadales, there is still considerable uncertainty about what a taxon is, especially at the infrageneric level, and this problem has important implications for cycad Red Listing. This chapter examines changes in the threatened status of cycad taxa from 1978 to 2002 to show how taxonomy influences the outcome of Red Listing assessments and conservation planning. During this time there have been five Red Listing accounts of the world cycad flora, starting with the list drawn up by the IUCN Threatened Plant Unit and based on the criteria outlined in The IUCN Plant Red Data Book (Lucas and Synge, 1978). The initial list was followed by Gilbert (1984), Osborne (1995), the 1997 IUCN Red List of Threatened Plants (Walter and Gillett, 1998) and the Cycad Action Plan (Donaldson, 2003). These accounts provide a basis for evaluating changes in threatened status over a 24year period and for determining the relative contributions of taxonomic uncertainty and ecological uncertainty to these changes.

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Taxonomy and the Threatened Status of Cycads In the first cycad Red List, based on The IUCN Plant Red Data Book (Lucas and Synge, 1978), there were 136 recognized cycad taxa (species and subspecies), comprising one Extinct species (Encephalartos woodii Sander), 63 Threatened taxa (46%), 45 taxa of Unknown threatened status (33%) and only 15 taxa (11%) that were Not Threatened (Fig. 2.1). In 1984, the number of cycad taxa had risen to 168, comprising one Extinct species, 65 Threatened taxa (38.6%), 86 taxa of Unknown status (51%) and 16 taxa (9.5%) that were classified as Not Threatened (Gilbert, 1984). Eleven years later, using the same criteria, Osborne (1995) recognized 197 taxa, comprising one Extinct species, 124 Threatened taxa (63%), 42 taxa that could not be assessed (21%) and 30 taxa that were Not Threatened (15%) (Fig. 2.1). In the last assessment using these criteria, Walter and Gillett (1997) recognized only 180 taxa, comprising three Extinct species, 147 Threatened taxa (82%), three taxa of Unknown status (1.6%) and 27 taxa that were Not Threatened (15%) (Fig. 2.1). Finally, the Cycad Action Plan

Not Threatened

Fig. 2.1. The number of cycad taxa (species, subspecies and undescribed species) classified as Extinct, Threatened, Not Threatened or Unknown, according to the IUCN Threatened Plant Unit database (1978), Gilbert (1984), Osborne (1995), the 1997 IUCN Red List of Threatened Plants (Walter and Gillett, 1998) and the 2002 assessments for the Cycad Action Plan (Donaldson, 2003). The total height of each bar represents the total number of recognized taxa. Taxa of unknown conservation status include those classified as ‘Indeterminate’, ‘Unknown’ and ‘Data Deficient’.

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(Donaldson, 2003), based on the latest revised IUCN criteria (Mace, 2000), included 297 taxa, comprising two species that are ‘Extinct in the Wild’ (no ‘Extinct’ species), 154 Threatened taxa (52%), 18 taxa that are ‘Data Deficient’ (6%) and a further 123 taxa (41%) that are not classified as threatened (Fig. 2.1). Clearly there are substantial differences between these assessments and it is necessary to examine these differences in greater detail to determine how taxonomic uncertainty has influenced the outcome of the Red Listing process. The substantial increase in the number of recognized cycad taxa (at the species and subspecies level) between 1977 and 2002 (Fig. 2.1) has obviously influenced the overall threatened status of the world’s cycads. Even at this level, there is a degree of confusion about what constitutes a valid taxon for Red List evaluation. Osborne (1995) recognized 197 taxa whereas Walter and Gillett (1998) recognized only 180 taxa. The taxa omitted by Walter and Gillett (1998) comprised six species of Cycas Linnaeus, both species of Bowenia Hooker ex Hooker filius, and nine taxa in the Zamiaceae, including one undescribed species of Encephalartos Lehmann. Walter and Gillett (1998) also included Cycas celebica Miquel, which is now considered synonymous with C. rumphii Miquel (Hill et al., 2003). Species classified as Extinct (pre-1994 categories) or Extinct in the Wild (IUCN, 1994) provide a useful starting point for exploring the influence of taxonomic uncertainty on Red Listing. Until 1995, only Encephalartos woodii was classified as an Extinct species and this status has been consistent in later assessments. Walter and Gillett (1998) also included Cycas szechuanensis C.Y. Cheng, W.C. Cheng & L.K. Fu and Zamia monticola Chamberlain as Extinct taxa. Cycas szechuanensis was first classified as Extinct because it was known only in cultivation. It was later thought to be conspecific with the more widespread C. guizhouensis K.M. Lan & R.F. Zou (Hill et al., 2003), which would warrant a downlisting to ‘Near Threatened’. However, it is now regarded as a valid species (Chen, 2000), but it no longer warrants a status of Extinct in the Wild because two wild populations have been discovered. In this case, changes in both taxonomic interpretation and new discoveries of wild populations have influenced the Red List status. In contrast, the taxonomic status of Zamia monticola has not been in doubt and the species was downgraded to ‘Critically Endangered’ (Stevenson et al., 2003) after the discovery of new populations. The Cycad Action Plan (Donaldson, 2003) also lists Encephalartos relictus P.J.H. Hurter as Extinct in the Wild. This species was described from a cultivated specimen. Two undescribed taxa that were classified as Extinct (herbarium specimen) and Extinct in the Wild (cultivated specimen) in an assessment of African cycads by J. Golding and P.J.H. Hurter (unpublished results) were not included in the Cycad Action Plan, due to their uncertain taxonomic status. A clear and consistent approach to infrageneric delimitations would help to resolve the Red List status of these taxa. Some of the same problems recur with other categories of threat (Fig. 2.2). The overall change in the number of threatened taxa shows a gradual increase in threatened taxa from 1978 to 1997 using the pre-1994 criteria. Based on the

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Pre-1994 Rare

Post-1994 Vulnerable

Pre-1994 Vulnerable

Post-1994 Endangered

Pre-1994 Endangered

Post-1994 Critical

180 160 140 120 Number of taxa

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1984

1995 1997 Year of assessment

1995

2002

Fig. 2.2. The number of cycad taxa (species, subspecies and undescribed species) assigned to IUCN threatened categories according to the IUCN Threatened Plant Unit database (1978), Gilbert (1984), Osborne (1995), the 1997 IUCN Red List of Threatened Plants (Walter and Gillett, 1998) and the 2002 assessments for the Cycad Action Plan (Donaldson, 2003). Assessments for 1978 and 1997 used the ‘old’ IUCN (pre-1994) criteria whereas the 2002 assessment used the criteria introduced after 1994. Osborne (1995) used both sets of criteria to evaluate cycad species.

post-1994 criteria, there is also an increase in the number of threatened taxa from Osborne (1995) to the Cycad Action Plan in 2002 (Donaldson, 2003) (Fig. 2.2). The low number of taxa of unknown status in the later assessments (Fig. 2.1) indicates that there is increasing ecological information on threatened taxa so that changes in the number of taxa assigned to different threatened categories may be due to better ecological information. However, an analysis of changes due to better ecological information (distribution and abundance data) compared with those due to taxonomic changes (new species, change in infrageneric status) (Fig. 2.3) shows that taxonomy accounts for a large number of changes in the number of threatened cycads. Clearly, many changes in the number of threatened species could arise from

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Cy ca s Sta ng eri a Bo we nia Ch igu Ce a rat oz am ia

Dio En on ce ph ala r to s Le pid oz am ia Ma cro za mi a Mi cro cyc as Za mi a

ca s Sta ng eri Bo we nia Ch igu Ce a rat oz am ia

Dio En on ce ph ala r to Le s pid oz am ia Ma cro za mi a Mi cro cyc a Za mi a

J. Donaldson

Cy

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Fig. 2.3. The number of cycad taxa where a change in threatened status was recorded between assessments. (A) Changes between the TPU Red List based on Lucas and Synge (1978) and Osborne (1995) using the pre-1994 IUCN criteria. (B) Changes between the 1997 IUCN Red List of Threatened Plants (Walter and Gillett, 1998) and the 2002 assessments for the Cycad Action Plan (Donaldson, 2003). Changes that resulted from taxonomic revisions (new species, split taxa and combined taxa) are represented by black bars, and those that resulted from more complete ecological data are represented by white bars.

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the description of new species as a result of increased field work in areas such as Australia, Central Africa, Mexico and South-East Asia between 1978 and 2002. It is therefore important to distinguish between the influence of new taxa on Red List assessments, compared with the influence of other changes that reflect uncertainty about the infrageneric status of cycad taxa. The number of taxa included in one Red List assessment that were no longer considered to be valid taxa in the following assessment (Fig. 2.4A) can be compared with the number of new taxa that were included in each Red List assessment (Fig. 2.4B). The results show that a considerable number of changes could be attributed to the description of new species (Fig. 2.4B), especially in Cycas, but also in Encephalartos, Macrozamia Miquel and Zamia Linnaeus. However, a large number of changes also occurred because of changes in the infrageneric status of described species, especially in Zamia, Cycas and Macrozamia. The data indicate that there were fewer changes due to uncertain taxonomic status between 1997 and 2002 than between earlier assessments (Fig. 2.4A), suggesting that the species limits of cycad taxa are better understood now than they were in 1978. The data summarized in Figs 2.1–2.4 do not reveal the many subtle influences that taxonomic changes have on cycad Red Listing. The description of new species and changes in species concepts can have different outcomes on Red Listing depending on the genus under review. For example, the delimitation of new species and subspecies of Cycas resulted in an increase in recognized taxa from eight in 1978 to 98 in 2002, while the number of threatened taxa increased from four in 1978 (50%) to 38 in 2002 (39%). As a result, there has been a substantial decrease in the proportion of Cycas species that are listed as threatened with extinction. In Africa, the delimitation of new species and subspecies of Encephalartos over the same period resulted in an increase from 48 taxa in 1978 to 67 taxa in 2002, with an increase in threatened taxa from 32 (66%) in 1978 to 46 (68%) in 2002. In the case of Cycas, many new species were discovered and described in areas where cycads are still abundant. In contrast, several new species of Encephalartos were described as a result of the revision of already threatened taxa, such as the split of E. eugene-maraisii I. Verdoorn into several taxa, all classified as threatened.

The influence of higher-level classification on conservation planning The focus of this chapter is primarily on what happens at the infrageneric level, but it is worth noting that taxonomic changes at higher levels also affect conservation planning. Vane-Wright et al. (1991) argued that systematics should be used as a criterion for prioritizing conservation actions. Their reasoning was that, given the high number of species that are threatened with extinction, priority should be given to those species that represent more threatened lineages (represented by higher taxonomic groups). For cycads, the genus Chigua D.W. Stevenson comprises two Critically Endangered species (Stevenson et al., 2003) and represents the second most threatened genus within the Cycadales [after Microcycas

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Fig. 2.4. Changes in recognized cycad taxa between different Red List assessments, from Gilbert (1984) to Osborne (1995), from 1995 to the 1997 IUCN Red List of Threatened Plants (Walter and Gillett, 1998), and from 1997 to 2002 (Donaldson, 2003). (A) The number of taxa listed on the first date but not recognized as valid taxa when the next list was published. (B) The number of taxa listed in the later assessment that were not recognized as distinct taxa in the earlier assessment. Only the major genera are included, as there were no differences in the genera Bowenia, Lepidozamia, Microcycas and Stangeria.

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(Miquel) A. de Candolle]. Based on Vane-Wright et al. (1991), the two species of Chigua should receive higher conservation priority than equally threatened species in larger genera (Walters, 2003). However, if Chigua is viewed as part of the genus Zamia (sensu Schutzman and Dehgan, 1993), then the two species currently included in Chigua become part of a much larger genus and therefore have lower conservation priority.

Conclusions A comparison of the cycad Red Lists from 1978 to 2002 shows that taxonomy has had a profound influence on the outcomes of the Red List process. By far the greatest contribution has been from the description of new taxa, due to a resurgence of interest in cycad taxonomy within the past 25 years. Greater taxonomic activity has also resulted in revised species concepts and the sorting out of nomenclatural problems so that many early names are no longer recognized as valid species. In both cases, the changes reflect developments within the science of cycad taxonomy that are a positive contribution to our knowledge of the Cycadales. These changes do, however, influence the process of Red Listing and it is essential to ensure that taxonomic changes are both necessary and consistent. To achieve this, taxonomists need to agree on concepts used to delimit infrageneric taxa and then apply these concepts consistently.

References Chen, C.J. (2000) Cycadaceae. In: Fu, L.K. et al. (eds) Higher Plants of China, Vol. 3. Qingdao Press, Qingdao, China, pp. 1–11. Donaldson, J.S. (ed.) (2003) Cycads. Status Survey and Conservation Action Plan. IUCN/SSC Cycad Specialist Group, IUCN, Gland, Switzerland and Cambridge, UK, ix + 86 pp. Gilbert, S.G. (1984) Cycads: Status, Trade, Exploitation and Protection 1977–1982. TRAFFIC, Washington, DC, 74 pp. Hill, K.D., Chen, C.J. and Loc, P.K. (2003) Regional overview: Asia. In: Donaldson, J.S. (ed.) Cycads. Status Survey and Conservation Action Plan. SSC Cycad Specialist Group, IUCN, Gland, Switzerland and Cambridge, UK, 25–30 pp. IUCN (1994) IUCN Red List Categories. Prepared by the IUCN Species Survival Commission, IUCN, Gland, Switzerland, 22 pp. IUCN/SSC Criteria Review Working Group (1999) IUCN Red List Criteria review provisional report: draft of the proposed changes and recommendations. Species 31–32, 43–57. Lucas, G. and Synge, H. (1978) The IUCN Plant Red Data Book. IUCN Threatened Plants Committee, Kew, UK, 540 pp. Mace, G. (2000) Summary of the results of the review of IUCN Red List categories and criteria 1996–2000. In: Hilton-Taylor, C. (compiler) 2000 Red List of Threatened Species. IUCN, Gland, Switzerland and Cambridge, UK, pp. 57–61.

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Osborne, R. (1995) The world cycad census and a proposed revision of the threatened species status for cycad taxa. Biological Conservation 71, 1–12. Schutzman, B. and Dehgan, B. (1993) Computer assisted systematics in the Cycadales. In: Stevenson, D.W. and Norstog, K.J. (eds) The Biology, Structure, and Systematics of the Cycadales. Proceedings of the Second International Conference on Cycad Biology. Palm & Cycad Societies of Australia Ltd, Milton, Queensland, Australia, pp. 281–289. Stevenson, D.W., Vovides, A. and Chemnick, J. (2003) Regional overview: New World. In: Donaldson, J.S. (ed.) Cycads. Status Survey and Conservation Action Plan. SSC Cycad Specialist Group, IUCN, Gland, Switzerland and Cambridge, UK, 31–38 pp. Vane-Wright, R.I., Humphries, C.J. and Williams, P.H. (1991) What to protect? Systematics and the agony of choice. Biological Conservation 55, 235–254. Walter, K.S. and Gillett, H.J. (eds) (1998) 1997 IUCN Red List of Threatened Plants. Compiled by the World Conservation Monitoring Centre, IUCN, Gland, Switzerland and Cambridge, UK, 862 pp. Walters, T. (2003) Off-site collections. In: Donaldson, J.S. (ed.) Cycads. Status Survey and Conservation Action Plan. SSC Cycad Specialist Group, IUCN, Gland, Switzerland and Cambridge, UK, 48–53 pp.

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Character Evolution, Species Recognition and Classification Concepts in the Cycadaceae

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Ken D. Hill Royal Botanic Gardens, Sydney, Australia

Abstract A number of systems of infrageneric classification of the family Cycadaceae have been presented by different authors. No two systems have been the same in structure or species recognition, and some have been strikingly discordant. Phylogenetic analysis of combined morphological and molecular datasets has yielded a cladogram with good resolution and support on many deeper branches. Plotting characters used by different authors in developing infrageneric systems of classification allows an independent assessment of the value of these characters and of the systems of classification derived from them. No classification system presented to date is wholly concordant with the results of the phylogenetic studies, and a number of characters previously heavily relied upon in defining groups are shown to be highly plastic. In particular, the recently described segregate genus Epicycas is shown to be polyphyletic, as are the four subgenera of Cycas erected by the same authors. The analysis supports the recognition of a single genus with five sections, although a number of taxa are insufficiently known to be clearly placed. Species recognition and species concepts are discussed.

Introduction The genus Cycas Linnaeus has long been accepted as the single constituent genus of the family Cycadaceae, itself the basal divergence within the extant Cycadales or Cycadophyta (Johnson, 1959; Stevenson, 1992). The genus (and family) has a present-day distribution concentrated in a zone between northern Australia and southern China, and extending westwards to Madagascar, the Comoros and the adjacent African mainland, and eastwards to Tonga. Many regional taxonomic ©CAB International 2004. Cycad Classification: Concepts and Recommendations (eds T. Walters and R. Osborne)

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treatments have been published over the years, but all suffer to some extent from the lack of an up-to-date comprehensive monographic treatment (e.g. Backer and Bakhuizen van den Brink, 1963; Smitinand, 1971; Fu et al., 1978; Hiêp and Vidal, 1996; Chen and Stevenson, 1999). The comprehensive treatment by Schuster (1932) is generally acknowledged to have created more problems than it solved (Johnson, 1959), and the most recent overall treatment by de Laubenfels and Adema (1998), wherein a second genus is erected, has proved controversial and has not been widely accepted (see Chen et al., Chapter 5 this volume). The different regional and comprehensive treatments also differ markedly in species recognition and circumscription. Analysis of combined morphological and molecular data yields a resolved cladogram with good support on many deeper branches (Fig. 3.1). Plotting characters used by different authors in developing infrageneric systems of classification allows an independent assessment of the value of these characters and of the systems of classification derived from them.

Historical background A number of authors have attempted to divide the genus Cycas internally and present systems of infrageneric classification. These are most notable in their discordancy. This is partly an indication that the known species are closely related and form a coherent group, but also a reflection of the poor understanding of specific limits and relationships within the group. The first attempt to subdivide the genus was that of Miquel, who firstly separated C. revoluta Thunberg from all other species on the basis of the revolute leaflet margins (Miquel, 1843), and later recognized two informal groups separated by tomentose vs. glabrous ovules (Miquel, 1861). He was followed by de Candolle (1868). Other early authors recognized two informal groups on the basis of the degree of division of the lamina of the megasporophyll (Carruthers, 1893). Warburg (1900) divided the genus, again informally, on the basis of the number of ovules per megasporophyll. Warburg was followed by Pilger (1926). Schuster (1932) attempted the first formal infrageneric classification of Cycas (discussed below), recognizing three major groups as sections. A second formal system was presented by Smitinand (1971), with a very different major division into two sections. Dehgan and Dehgan (1988) published an informal infrageneric classification based on seed structure and pollen morphology that was completely different from either of the above, recognizing two subgenera. Hill (1994, 1996) recognized four sections, each with two or three subsections, in part merging the systems of Schuster and Smitinand. Wang (1996) erected two subgenera and within these a number of sections, subsections and series, many corresponding in circumscription, but not rank or placement, to taxa recognized by Hill. De Laubenfels and Adema (1998) presented an entirely different system, separating the new genus Epicycas de Laubenfels and dividing the remainder of Cycas

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C. wadei C. curranii C. revoluta C. panzihuaensis C. changjiangensis C. guizhouensis C. sexseminifera C. bifida C. diannanensis C. pectinata C. clivicola C. lindstromii C. pranburiensis C. condaoensis C. siamensis C. inermis C. scratchleyana C. beddomei C. circinalis C. spherica C. riuminiana C. thouarsii C. rumphii C. micronesica C. bougainvilleana C. seemannii C. apoa C. tuckeri C. yorkiana C. cairnsiana C. ophiolitica C. maconochiei C. calcicola C. furfuracea C. silvestris C. media C. papuana C. armstrongii

Fig. 3.1. Combined molecular and morphological analysis for species of Cycas (strict consensus tree). Bootstrap support values shown above branches. From Hill (1999 and in preparation).

into four subgenera. The classification systems of Schuster and subsequent authors are examined in the light of recent cladistic studies below. Species concepts Species definition in Cycadaceae is complicated by the variability of some of the characters that have been traditionally used to separate taxa and by the inade-

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quacy of specimens and recorded observations in representing the differences and similarities occurring within and between populations and taxa. For example, development of spines on petioles is often variable within populations, and changes with age in most taxa. Microsporophylls vary considerably in size and shape from base to apex of the cone; in particular, the apical spine is reduced or absent on the lowermost sporophylls, gradually increasing in size towards the apex or towards the centre of the cone (Amoroso, 1986). Megasporophylls also vary, often widely, in size, shape of lamina and number of ovules. This can depend on their position within a growth flush, the first and last produced often being markedly smaller and less elaborate than those in the centre. Because herbarium collections are frequently fragmentary, incomplete and often sterile, many characters are not represented or recorded. Comprehensive field study is thus essential to understanding the ranges of variation of characters that may distinguish taxa. An example is in the recent segregation of seven taxa in Cape York Peninsula, Australia, from what had long been accepted as a single species (Hill, 1995). Many of the characters that discriminate these taxa were unrepresented in specimens or notes, and it was only by comprehensive and systematic field observation that the totality of morphological variation could be observed. This is achieved in a rigorous and reproducible manner by following a standard pro forma (Fig. 3.2) and making a standard set and number of observations on each population. Data recorded can then be statistically analysed if required, and groups can be defined. This synthesis can then lead to satisfactory species recognition, following which identification keys and classifications can be developed (Table 3.1). In the Cape York example, the cataphyll characters critical in discriminating taxa had not been previously recorded. It is also of note that these taxa occur in discrete, geographically separated populations. The genus Cycas in general shows a similar geographical replacement pattern throughout its range, often with many closely related entities. Although these taxa are often similar in many respects, the homoplasy evident in the defining characters does not always allow unequivocal aggregation into groups that could be treated as species with subordinate infraspecific taxa. In order to satisfactorily separate and recognize groups of populations that show real, albeit sometimes small differences, it is strongly recommended that these groups be treated as distinct species. This rather narrow view of species is considered preferable to the arbitrary submerging of these recognizably distinct and truebreeding groups of populations into broader and less meaningful ‘species’ and the consequent loss of information on the real diversity of these plants.

Phylogenetic studies Phylogenetic analyses of the family Cycadaceae sensu stricto have been conducted using sets of data obtained from DNA molecular sequences and from morphological and anatomical characters. Sequence data of the internal transcribed spacer region from the nuclear genome for 40 terminal taxa were analysed (Hill,

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–

– – –

Fig. 3.2. Pro forma used for rigorous systematic observations in populations of Cycas.

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Table 3.1. Key to the species of Cycas in Cape York Peninsula, Australia. Characters observed in field studies are shown in bold. 1 Cataphylls hard, strongly spinescent 2 1 Cataphylls soft, not spinescent 4 2 Hypodermis absent; leaf margins flat; leaflet midrib equally raised above and below C. xipholepis K.D. Hill 2 Hypodermis present; leaf margins recurved; leaflet midrib almost flat above, strongly raised below 3 3 Pinnae > 9 mm wide; cataphylls deciduous C. silvestris K.D. Hill 3 Pinnae < 9 mm wide; cataphylls persistent C. media R. Brown 4 Crown and cataphylls densely orange-woolly or floccose 5 4 Crown and cataphylls very shortly grey to white-sericeus 6 5 Megasporophyll apex 60–100 mm long, with 24–32 lateral spines 3–6 mm long, apical spine 2–16 mm long C. yorkiana K.D. Hill 5 Megasporophyll apex 40–55 mm long, with 16–24 lateral spines 1–4 mm long, apical spine 21–25 mm long C. badensis K.D. Hill 6 Megasporophylls short (10–13 cm); apex dilated (35–50 mm wide, 50 –65 mm long) C. tuckeri K.D. Hill 6 Megasporophylls longer (15–22 cm); apex not dilated (18–35 mm wide, 60–75 mm long) C. semota K.D. Hill

in preparation), and morphological and anatomical data were taken for the same 40 taxa from a data set used in morphological studies (Hill, 1999 and in preparation). The combined data yielded a result that was not completely consistent with any published morphological studies or recent taxonomic classifications (Fig. 3.1). The resultant cladogram from these studies will be taken as a basis for character analysis below.

Character Analysis Previously published classifications have been examined and characters used to define groups recorded (Table 3.2). These were then plotted on to the cladogram previously obtained from analysis of combined morphological and molecular data (Fig. 3.1). Consistency indices (CI) are assigned to each character as a measure of the degree of homoplasy shown by that character, and also as a measure of the reliability and efficacy of that character in defining and recognizing natural groups. Most of the characters that have been widely used in infrageneric classification in the past are shown to be useful, although character polarities were not always as previously assumed. Each character state is discussed individually below.

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Table 3.2. Characters used by different workers in defining groups in Cycas.

Character

States

Outgroup conditions

Ovules

Glabrous/tomentose

Glabrous

Sclerotesta

Smooth/striate/ribbed/ Smooth/striate verrucose/crested Spongy Absent/present Absent megagametophytic tissue Fibrous sarcotesta Absent/present Absent Ovule number Seed cone Megasporophyll apex Megasporophyll length Pollen cones

1–14 Closed/open Pectinate/dentate/ entire Long/short

Pollen cones

Cylindrical/ovoid

Microsporophyll apex Base of plant

Attenuate/truncate

Soft/rigid

Swollen/not swollen

Habit

Caulescent/ acaulescent

Petiole

Long/short

Leaflet Leaflet margins

Entire/divided Flat/revolute

Leaflet apex Leaflet midrib

Soft/spinescent Raised/flat

Reference Miquel, 1861; Schuster, 1932 Hill, 1996; Wang, 1996 Deghan and Yuen, 1983; Hill, 1994

Hill, 1994; Wang, 1996 2 Warburg, 1900 Not comparable Wang, 1996 Entire Schuster, 1932 Not comparable Schuster, 1932 Soft/rigid

Smitinand, 1971; Hill, 1996, 1999 Cylindrical/ovoid de Laubenfels and Adema, 1998 Not comparable de Laubenfels and Adema, 1998 Swollen/not de Laubenfels and swollen Adema, 1998 Caulescent/ Smitinand, 1971; acaulescent de Laubenfels and Adema, 1998 Long/short de Laubenfels and Adema, 1998 Entire/divided Wang, 1996 Flat de Laubenfels and Adema, 1998 Soft/spinescent Schuster, 1932 Raised/flat de Laubenfels and Adema, 1998

Ovule tomentum Two species, Cycas revoluta and C. taitungensis C.F. Shen, K.D. Hill, C.H. Tsou & C.J. Chen, possess tomentose ovules. This is a synapomorphy uniting these taxa (CI 100%, Fig. 3.3A) but of no value in further grouping or taxonomically classifying this small group. Miquel (1861), Schuster (1932) and Hill (1996, 1999) had used this character state as a key defining character for section Asiorientales. This section proves to be a natural group, supported by several other synapomorphies,

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and the character of tomentose ovules is clearly a useful character in identification of this group.

Ribbed sclerotesta Two species, Cycas wadei Merrill and C. curranii (J. Schuster) K.D. Hill, possess a strongly ribbed sclerotesta. This is a synapomorphy uniting these taxa (CI 100%, Fig. 3.3A) but of no value in further grouping or taxonomically classifying this small group. This section proves to be a natural group, supported by several other synapomorphies, and the character of ribbed sclerotesta is clearly a useful character in identification of this group. This clade was recognized as subsection Wadeanae by Hill (1996) and Wang (1996) on the basis of this character.

Verrucose sclerotesta A verrucose sclerotesta is shown to be a well-corroborated synapomorphy (CI 100%, Fig. 3.3A) supporting quite a large natural group of mainland Asian species occurring in southern China and northern Indochina. This group was formally named by Smitinand (1971) as section Stangerioides, although at that time with a single constituent species and not on the basis of sclerotesta characters. Section Stangerioides was adopted by Hill (1996) and Wang (1996), although with wider circumscriptions that differed from each other and that in both cases rendered the natural group non-monophyletic. The verrucose sclerotesta was recognized as a defining character for smaller groups within the broader groups by these authors.

Crested sclerotesta A small group of taxa from the Western Pacific and eastern Malesian regions possesses a crested sclerotesta. This is a synapomorphy uniting these taxa (CI 100% in the best-case scenario, Fig. 3.3B) but of no value in further grouping or taxonomically classifying this small group. While the crested sclerotesta is a useful character in recognition of the group, the relationships of this group with other more distantly allied species are unclear, and no formal nomenclatural recognition of this group has yet been attempted.

Spongy megagametophytic tissue The presence of spongy megagametophytic tissue is shown to be a synapomorphy (CI 50% in the strict consensus tree, 100% in the best-case scenario, Fig. 3.3A) supporting a small and widely distributed group of species that occurs in near-coastal situations from Tonga westwards to East Africa. When present, the

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Fig. 3.3. Character state distribution on the consensus cladogram. Species of Cycas indicated by their specific epithet. (A) Seed characters. (B) Seed characters. (C) Megasporophyll characters. (D) Female cone characters.

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‘truncate’ microsporophyll

Fig. 3.3. (continued) Character state distribution on the consensus cladogram. Species of Cycas indicated by their specific epithet. (E) Megasporophyll length (cm). (F) Pollen cone. (G) Microsporophyll characters. (H) Stem characters.

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Fig. 3.3. (continued) Character state distribution on the consensus cladogram. Species of Cycas indicated by their specific epithet. (I) Petiole length (cm). (J) Leaflet characters.

spongy tissue may cause the seeds to float and facilitate aquatic dispersal on oceanic currents (Dehgan and Yuen, 1983), although not all seeds with spongy tissue float. Although the taxonomic implications of this character were recognized by these authors, misidentifications of study materials and a general lack of understanding of specific limits hindered application of these observations. The group of species, defined by presence of spongy megagametophytic tissue, was recognized as subsection Rumphiae by Hill (1994). The 50% CI arises from the uncertain placement of Cycas riuminiana Porte ex Regel, an inland forest species from the Philippines that is not aquatically dispersed and lacks other features of subsection Rumphiae. Placement of this species requires further study.

Fibrous sarcotesta A fibrous or corky layer within the sarcotesta that apparently grows outwards from the outer surface of the sclerotesta is present in a range of taxa, and has been recognized as a grouping character by Hill (1996) and Wang (1996). This character state appears to have been gained near the base of the tree, below Cycas pectinata Buchanan-Hamilton (Fig. 3.3B), and lost below C. riuminiana, although deltran optimization suggests two independent acquisitions on the clades below

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C. pectinata and below C. inermis Loureiro. The moderate level of homoplasy shown (CI 33%) highlights the uncertain placement and need for further study of C. apoa K.D. Hill, an inland forest species from New Guinea. Nevertheless, this is shown to be a useful character for defining and recognizing several groups.

Ovule number The number of ovules per megasporophyll has been used both in defining species (Mueller, 1874; Wei, 1994; Chang et al., 1998) and in subdividing the genus (Warburg, 1900; Pilger, 1926). This character is highly variable in most if not all species, with only a slight tendency for mainland Asian species to carry fewer ovules (CI 9%, Fig. 3.3C). The degree of overlap, however, renders this character ineffective both in recognizing species and in defining groups.

Megasporophyll pectinate The pectinate state is shown to be ambiguous (Fig. 3.3D). In one scenario, the transition to the dentate or entire condition is a synapomorphy defining a large clade including Cycas inermis and all species above (corresponding to section Cycas), with the exception of two apparent reversals in C. scratchleyana F. Mueller and C. riuminiana (CI 33%). This section was first recognized informally by Carruthers (1893) and formally by Schuster (1932). This group has been recognized by most workers at some level, ranging from subsection (Smitinand, 1971) through section (above and Hill, 1996) to subgenus (Wang, 1996). In fact, only the systems presented by Deghan and Deghan (1988) and de Laubenfels and Adema (1998) have failed to discriminate this group.

Seed cone closed or open The closed seed cone is shown to be plesiomorphic (Fig. 3.3D). The transition to the open condition is a synapomorphy (CI 50%) defining a large clade including Cycas inermis and all species above (section Cycas) as well as a clade of two species – C. lindstromii S.L. Yang, K.D. Hill & Hiêp and C. pranburiensis S.L. Yang, K.D. Hill, W. Tang & Vatcharakorn. This character is correlated with the pectinate megasporophyll, but with less ambiguity.

Megasporophyll long or short A long megasporophyll was regarded by Schuster (1932) as a diagnostic character for subsection Pandemicae. The analysis indicates that this condition has arisen independently in at least four lineages (CI 17%, Fig. 3.3E). This character is con-

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sequently of no value in recognizing major groupings, although it is useful in discriminating related species and is a potential synapomorphy for Cycas thouarsii R. Brown ex Gaudichaud and C. micronesica K.D. Hill.

Pollen cone cylindrical or ovoid A cylindrical pollen cone was regarded by de Laubenfels and Adema (1998) as a diagnostic character for the new genus Epicycas, although the cylindrical state was acknowledged also to occur in Cycas. The analysis indicates that this condition is present in three separate lineages (CI 14% for cone shape, including the states ovoid and narrow-ovoid, Fig. 3.3F) and that the cylindrical condition may in fact be plesiomorphic for Cycas. Cone shape is also shown to be homoplastic within clades, and is consequently of little value in recognizing natural groups.

Microsporophyll soft, waxy or hard Microsporophyll texture shows no clear evolutionary progression, with the presence of all three states near the base of the tree and an ambiguous ancestral condition (Fig. 3.3G). The different states are, however, highly consistent (CI 100%). The soft condition defines the group discussed above as section Stangerioides; the waxy condition characterizes two small clades (the Cycas revoluta clade and the C. wadei clade) and C. panzhihuaensis L. Zhou & S.Y. Yang; and the hard condition prescribes a large clade that includes C. pectinata and all species above. The soft pollen cone character was used by Smitinand (1971) in defining section Stangerioides.

Microsporophyll ‘truncate’ Microsporophylls with a shortened apex (‘truncate’) were regarded by de Laubenfels and Adema (1998) as the diagnostic character for subgenus Truncata. The analysis indicates that such shortening has arisen independently in three separate clades (CI 22%, Fig. 3.3H) and is consequently of little value in recognizing major groupings, although it does suggest the possibility that Cycas rumphii Miquel, C. micronesica and C. seemannii A. Braun might form a clade.

Caudex with a bulbous base A caudex with a bulbous base was regarded by de Laubenfels and Adema (1998) as the key diagnostic character for the new genus Epicycas. The analysis indicates that this condition has arisen independently in at least two and possibly six separate lineages (CI 11%, Fig. 3.3H) and is consequently of little value in recognizing major groupings.

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Caudex wholly subterranean Wholly hypogeous growth habits are shown by a few species. This character and the bulbous base (above) were concatenated by de Laubenfels and Adema (1998) in defining the genus Epicycas. The truly hypogeous habit is much less frequent than the bulbous base, and is shown to have arisen in two groups independently (CI 25%, Fig. 3.3H). This character was used by Smitinand (1971) in defining section Stangerioides.

Petiole long or short A short petiole (less than 30 cm long) was regarded by de Laubenfels and Adema (1998) as a key diagnostic character for Cycas subgenus Revoluta, and a long petiole for subgenus Pectinata. The analysis indicates that the long condition has arisen independently in at least seven different lineages (CI 20%, Fig. 3.3I), possibly with subsequent reversals, and is consequently of little value in recognizing major groups.

Leaflet dichotomously divided Dichotomously divided leaflets are a striking character present in four species occurring in southern China and Vietnam. This section was recognized as a series Multipinnata by Wang (1996), who regarded the divided state as primitive. This analysis shows the divided state to be advanced (Fig. 3.3J), but is not sufficiently detailed to examine the value of this character as a grouping character. Other morphological characters do not separate these four taxa and the divided leaflets are a useful grouping character on this basis.

Leaflet margins revolute Revolute leaflet margins were first used to subdivide the genus by Miquel (1843). In contrast, flat, often undulate leaflet margins were considered characteristic of the genus Epicycas by de Laubenfels and Adema (1998). Flat leaflets are here shown to be ancestral. The change to revolute margins is shown by the analysis to occur in several lineages (CI 22%, Fig. 3.3K), and is consequently ineffective in defining groups, although it is at times a useful character in discriminating species within groups.

Leaflet apex spinescent A spinescent leaflet apex was regarded by Schuster (1932) as a diagnostic character for subsection Endemicae. The analysis indicates that this condition has arisen independently in all major lineages (CI 10%, Fig. 3.3K), possibly more

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than once in some of these clades, and is consequently of little value in recognizing major groups.

Leaflet midrib raised or flat A flat midrib was regarded by de Laubenfels and Adema (1998) as a diagnostic character for Cycas subgenus Revoluta. The analysis indicates that this condition has arisen independently in three separate lineages (CI 12%, Fig. 3.3K), possibly more than once in some clades, and is consequently of little value in recognizing major groups. Alternatively, flat midribs can be almost as parsimoniously explained by only two origins and multiple subsequent losses.

Assessment of Previous Classifications Schuster (1932) attempted the first formal subgeneric classification of Cycas (Fig. 3.4A). He recognized three major groups (sections), corresponding basically to the pectinate megasporophyll (section Indosinenses) and non-pectinate megasporophyll (section Lemuricae) groups, with the further separation of C. revoluta (in which he included C. taiwaniana Carruthers) as a monotypic group defined by narrow revolute leaflets and tomentose ovules (section Asiorientales). He further subdivided section Lemuricae into two subsections, Pandemicae and Endemicae, on differences in tips of pinnae and length of megasporophylls. Although the major groups erected by Schuster take nomenclatural priority, two of his three sections are paraphyletic as he circumscribed them. He also allocated species and infraspecific taxa within these groups erratically and often apparently on the basis of guesswork, placing many previously recognized species as infraspecific taxa within complex hierarchies under C. circinalis Linnaeus and C. rumphii. Many of these are clearly distinct and distantly related species, rendering his concepts of C. circinalis and C. rumphii polyphyletic. In addition, Schuster’s work does not comply with the requirement for subgroups including the type of a genus to carry automatically the generic name (the autonym rule – International Code of Botanical Nomenclature (ICBN), Greuter et al., 2000). Hence section Lemuricae should correctly be section Cycas and subsection Pandemicae should be subsection Cycas. In summary, Schuster recognized five infrageneric taxa, three of which are shown to be polyphyletic (Fig. 3.4A). Only four infrageneric groups are marked on Fig. 3.4A. One of the marked groups (Endemicae) is monophyletic, while the other is monotypic (and thus monophyletic by definition). If the unmarked lineages collectively form another of his taxa (section Lemuricae?) then it might be said that it is poly- and not paraphyletic. Similarly, Pandemicae would be most appropriately described as polyphyletic. Smitinand (1971) proposed a very different major division into two groups (Fig. 3.4B), separating Cycas micholitzii Dyer in the monotypic section Stangerioides on the basis of the soft, shortly apiculate microsporophylls in very small, slender

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Fig. 3.4. Previous systems of classification. Incorrect names under the ICBN are indicated by*. Monophyletic clades supported in this analysis shown in bold. Species of Cycas indicated by their specific epithet. Classifications by: (A) Schuster (1932); (B) Smitinand (1971); (C) Dehgan (1987); (D) Hill (1996, 1999).

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Fig. 3.4. (continued) Previous systems of classification. Incorrect names under the ICBN are indicated by*. Monophyletic clades supported in this analysis shown in bold. Species of Cycas indicated by their specific epithet. Classifications by: (E) Wang (1996); (F) de Laubenfels (1998).

cones, and the dwarf, mainly subterranean habit with very few leaves (‘Stangerioid’ habit). The remainder of the genus he placed in section Cycas, which he divided into two subsections on the basis of pectinate megasporophylls (subsection Pectinatae, also given as Pinnatidae in the key) and non-pectinate megasporophylls (subsection Circinnalidae). The former subsection included C. revoluta. Again, the requirement for autonyms was not strictly followed, and subsection Circinnalidae is correctly (and automatically) subsection Cycas. Subsection Pectinatae (or Pinnatidae) is also illegitimately described, no type species being designated. Of the four infrageneric taxa recognized by Smitinand, three are shown to be polyphyletic (Fig. 3.4B). Dehgan and Dehgan (1988) alluded to an infrageneric classification and published a series of names with a major division based on presence or absence of spongy tissue in seeds and incorporating differences in pollen structure (Fig. 3.4C). This classification was not formally published, and neither the requirement for autonyms nor the rule of priority was followed. Although the character basis for this subdivision was sound, incorrect identifications and a lack of understanding of specific limits made the arrangement untenable. The proposed classification recognized two subgenera with three sections and three subsections. No assignment of species to the lower groups was made, however, apart from the

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listing of a single ‘typical’ species. On the basis of these inclusions, the two subgenera are shown to be polyphyletic, as is the one section that has more than one included species (Fig. 3.4C). Hill (1996, 1999) presented an arrangement incorporating four sections corresponding in name to the three erected by Schuster plus section Stangerioides as described above (Fig. 3.4D), in all cases with different circumscriptions, on the basis of morphological cladistic analyses. Nine subordinate groups corresponding to subsections were also proposed, most of them informal. Of the four sections, two are shown to be polyphyletic, and one of the nine subsections is shown to be polyphyletic, with two others possibly paraphyletic (Fig. 3.4D). Wang (1996) presented another formal infrageneric classification, recognizing two subgenera on the basis of pectinate vs. non-pectinate megasporophylls. Within these a number of sections, subsections and series were erected (Fig. 3.4E). These are not altogether internally consistent and several of the names are in contravention of the ICBN (Greuter et al., 2000). Of the two subgenera, one (subgenus Panzhihuaensis) is shown to be polyphyletic, and one of the sections is paraphyletic (Fig. 3.4E). Full enumeration of species included in a number group is not attempted, making assessment uncertain. De Laubenfels and Adema (1998) presented an entirely different system, recognizing a new genus Epicycas for taxa with a largely subterranean habit and a bulbous underground base. They divided the remainder of Cycas into four subgenera based on a combination of leaf, microsporophyll and megasporophyll morphology. Every generic and infrageneric group as circumscribed by these authors is shown to be polyphyletic (Fig. 3.4F).

Conclusions No previously published system of classification is wholly in accord with the results of molecular and morphological phylogenetic analyses. Many of the key characters on which previously published classifications were based are shown to be plesiomorphic, homoplastic or autapomorphic and of little value in defining infrageneric relationships and developing classifications based on these. In particular, separation of the genus Epicycas is clearly unwarranted (see Chen et al., Chapter 5 this volume). However, certain of the characters discussed above are shown to be synapomorphic characters that are useful in defining natural groups. Seed characters in particular are shown to be highly consistent, as are some aspects of sporophyll morphology. These characters are useful in developing a workable key to groups (Table 3.3) and to species within the genus Cycas. Data are still lacking on many recognizable species in the genus, and consequently placement of a number of species on the basis of the characters discussed above is uncertain. It is at present premature to develop a comprehensive system of infrageneric classification on this basis, but an interim arrangement recognizing demonstrably monophyletic groups and the nearest possible placements of species or groups incertae sedis can

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Classification Concepts in the Cycadaceae

Section Asiorientales Section Wadeanae

Section Stangerioides

Section Indosinenses

Species incertae sedis

Subsection Cycas

Section Cycas

Subsection Rumphiae

Subsection Endemicae

Fig. 3.5. Comprehensive enumeration of species in Cycas. Consensus morphological and molecular tree shown in bold, other species interpolated from morphological cladistic analysis using available data.

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Table 3.3. Key to major recognizable subdivisions of the genus Cycas. 1 1 2 2 3

Ovules tomentose Ovules glabrous Megasporophyll lamina pectinate Megasporophyll lamina not pectinate Male cones soft, microsporophyll apices not deflexed 3 Male cones rigid, waxy, microsporophyll apices deflexed 4 Sclerotesta not ribbed

Section Asiorientales 2 3 Section Cycas 4 5 Cycas panzhihuaensis L. Zhou & S.Y. Yang Section Wadeanae

4 Sclerotesta ribbed 5 Microsporophylls flexible, rounded; sarcotesta not fibrous; sclerotesta verrucose Section Stangerioides 5 Microsporophylls rigid, acuminate; sarcotesta fibrous; sclerotesta smooth Section Indosinenses

be informally presented here (Table 3.4). The primary division is made into sections rather than subgenera for the reason that basal branches are short and additional data may well collapse these or elucidate different relationships. The sections recognized are distinct and well-supported clades. A comprehensive enumeration of taxa in the genus Cycas that are recognizable as species or comparable terminal taxa is presented in Fig. 3.5. The tree is based on the strict consensus of a combined morphological and molecular analysis (shown in bold). Species for which molecular data are unavailable are interpolated on the basis of morphological cladistic analysis using available data (Hill, 1999 and in preparation). Not all species are adequately known, and data are incomplete for a number of taxa. This again represents an informal interim arrangement that shows known groups and relationships and highlights areas requiring further study.

Acknowledgements The Hermon Slade Foundation is warmly thanked for the financial support that allowed this and related studies to proceed. The Vietnamese Institute of Ecology and Biological Resources and the Chinese Academy of Science are thanked for assistance with laboratory and field studies in Vietnam and China. Kampon Tansacha and the Nong Nooch Tropical Garden are gratefully acknowledged for hospitality and logistical assistance. Anders Lindström assisted in the field and in valuable discussions of the taxonomic and distributional limits of the cycads of Asia. The keepers of the herbaria at A, B, BKF, BM, G, K, L, NY and P are acknowledged for access to their collections. Peter Weston is thanked for constructive comment on earlier drafts of the manuscript.

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Table 3.4. A provisional classification of Cycas. Section Asiorientales Synapomorphies: encrypted stomata 3 species. No subgroups Section Wadeanae Synapomorphies: ribbed seeds 2 species. No subgroups Section Stangerioides Synapomorphies: verrucose seeds, soft pollen cones About 25 species. No clear subgroups. Section Indosinenses Synapomorphies: fibrous sclerotesta, hard pollen cones About 15 species. No clear subgroups. Section Cycas Synapomorphies: open seed cones, non-pectinate megasporophylls About 53 species. Three distinct monophyletic subgroups and a number of unplaced species Subsection Cycas: about 4 species Synapomorphies: fibrous sclerotesta Subsection Rumphiae: about 10 species Synapomorphies: spongy megagametophyte Subsection Endemicae: about 32 species Synapomorphies: palisade tissue in lower mesophyll species incertae sedis; about 8 species

References Amoroso, V.B. (1986) Morphological study of the sporophylls of Philippine Cycas. Philippine Journal of Science 115(3), 177–198. Backer, C.A. and Bakhuizen van den Brink, R.C. (1963) Cycadaceae. In: Flora of Java, Vol. 1. Noordhoff, Groningen, The Netherlands, p. 87. Carruthers, W. (1893) On Cycas taiwaniana sp. nov. and C. seemannii A.Br. Journal of Botany 31, 1–3; t. 330–331. Chang, H.T., Huang, Y.Y. and Zheng, H.X. (1998) Acta Sci. Nat. Univ. Sunyatseni 37, 8. [Cycas septemsperma.] Chen, C.J. and Stevenson, D.W. (1999) Cycadaceae. In: Wu, Z.Y. and Raven, P.H. (eds) Flora of China, Vol. 4, Cycadaceae through Fagaceae. Science Press, Beijing and Missouri Botanical Garden Press, St Louis, Missouri, pp. 1–7. De Candolle, A.P. (1868) Cycadeae. In: Prodromus Systema Natura and Regnum Vegetabile 16(2). Victor Massen, Paris, pp. 361–521. De Laubenfels, D.J. and Adema, F. (1998) A taxonomic revision of the genera Cycas and Epicycas gen. nov. (Cycadaceae). Blumea 43, 351–400. Dehgan, B. and Dehgan, N.B. (1988) Comparative pollen morphology and taxonomic affinities in Cycadales. American Journal of Botany 75, 1501–1516.

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Dehgan, B. and Yuen, C.K.K.H. (1983) Seed morphology in relation to dispersal, evolution and propagation of Cycas L. Botanical Gazette 144, 412–418. Fu, S.H., Cheng, W.C., Fu, L.K. and Chen, C.J. (1978) Cycadaceae. In: Cheng, W.C. and Fu, L.K. (eds) Flora Reipublicae Popularis Sinicae 7. Science Press, Beijing, China, pp. 4–17. Greuter, W., McNeill, J., Barrie, F.R., Burdet, H.M., Demoulin, V., Filgueiras, T.S., Nicolson, D.H., Silva, P.C., Skog, J.E., Trehane, P., Turland, N.J. and Hawksworth, D.L. (2000) International Code of Botanical Nomenclature (Saint Louis Code). Koeltz Scientific Books, Köningstein, Germany, 474 pp. Hiêp, N.T. and Vidal, J.E. (1996) Cycadaceae. In: Morat, Ph. (ed.) Flore du Cambodge, du Laos et du Viêtnam, Vol. 28, Gymnospermae. pp. 6–23. Hill, K.D. (1994) The Cycas rumphii complex (Cycadaceae) in New Guinea and the Western Pacific. Australian Systematic Botany 7, 543–567. Hill, K.D. (1995) Infrageneric relationships, phylogeny and biogeography of the genus Cycas (Cycadaceae). In: Vorster, P. (ed.) Proceedings of the Third International Conference on Cycad Biology. Cycad Society of South Africa, Stellenbosch, South Africa, pp. 139–162. Hill, K.D. (1996) A taxonomic revision of the genus Cycas (Cycadaceae) in Australia. Telopea 7, 1–64. Hill, K.D. (1999) Cycas – an evolutionary perspective. In: Chen, C.J. (ed.) Biology and Conservation of Cycads, Proceedings of the Fourth International Conference on Cycad Biology. International Academic Publishers, Beijing, China, pp. 98–115. Johnson, L.A.S. (1959) The families of cycads and the Zamiaceae of Australia. Proceedings of the Linnaean Society of New South Wales 84, 64–117. Miquel, F.A.W. (1843) Genera et species Cycadearum viventium. Linnaea 17, 675–744. Miquel, F.A.W. (1861) Prodromus Systematis Cycadearum. Van der Post, Utrecht, Holland, 35 pp. Mueller, F.A.W. (1874) Fragmenta Phytographie Australiae, Vol. 8. Government Printer, Melbourne, Australia, 304 pp. Pilger, R. (1926) Cycadaceae. In: Engler, A. (ed.) Die Naturlichen Pflanzenfamilien, 2nd edn 2, 13, pp. 44–82. Schuster, J. (1932) Cycadaceae. In: Engler, A. (ed.) Das Pflanzenreich, Fascicle 99, Vol. 4, Part 1, pp. 1–168. Smitinand, T. (1971) The genus Cycas Linn. (Cycadaceae) in Thailand. Natural History Bulletin of the Siam Society 24, 163–175. Stevenson, D.W. (1992) A formal classification of the extant cycads. Brittonia 44, 220–223. Wang, D.Y. (1996) Systematic classification and brief introduction to Cycadales (Chapter 2) and Taxonomy of Cycas in China (Chapter 3). In: Wang, F.X. and Liang, H.B. (eds) Cycads in China. Guangdong Science and Technology Press, Guangdong, China, pp. 9–142. Warburg, O. (1900) Cycadaceae. In: Warburg, O. (ed.) Monsunia. Engelmann, Leipzig, Germany, pp. 178–181. Wei, F.N. (1994) A new cycad from Guangxi. Guihaia 14, 300. [Cycas ferruginea.]

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Morphological Characters Useful in Determining Species Boundaries in Cycas (Cycadaceae)

4

Anders Lindström Nong Nooch Tropical Botanical Garden, Najomtien, Sattahip, Chonburi, Thailand

Abstract Morphological characters within the genus Cycas, based on previously published descriptions and on recent field research, are evaluated for their usefulness in distinguishing among distinct, yet morphologically similar, pairs of taxa within the genus. A standardized suite of taxonomically useful morphological characters in support of future designation of species within Cycas is recommended.

Introduction Taxonomy has traditionally used certain morphological characters or suites of morphological characters to define taxa. These characters are often chosen in a way that permits convenient measurement from herbarium specimens. For cycads, this usually restricts the choice to those characters derived from limited aspects of leaf and sometimes cone morphology, since these are usually the only parts represented in herbarium accessions. Annotations of herbarium vouchers often lack data significant to taxonomic studies or even identification. Leaf length, petiole length, stem height, stem profile and branching pattern are examples of these characters that cycad researchers require in their evaluation of taxa. Cycads, especially representatives of the genus Cycas Linnaeus, typically have long leaves that are difficult to process as herbarium specimens. Therefore, the ©CAB International 2004. Cycad Classification: Concepts and Recommendations (eds T. Walters and R. Osborne)

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majority of Cycas vouchers in herbaria are represented only by portions of leaves – usually a group of about four to six pinnae. Specimens often lack the petiole, a feature of the plant that can be of particular taxonomic significance. Labels accompanying Cycas specimens most often lack the necessary data to describe the whole leaf and seldom indicate from which portion of the leaf the pinnae were obtained. Within a leaf, terminal, central and basal pinnae each have distinctive features. Herbarium accessions only infrequently include reproductive material from Cycas plants and representation of both male and female carpological material for any given taxon is rare. A major problem associated with past herbarium-based Cycas studies has been that different suites of characters had to be used in the analysis of different specimens. The taxonomist is often faced with having to study specimens that have different portions of a leaf represented, or a portion of a leaf on one specimen and a complete leaf on another, different reproductive material present or reproductive material absent, and few descriptive or quantitative data in the annotations. A further limitation arises in that herbarium specimens often do not necessarily represent the ‘average’ plant for any given population. It is known that plants within a population of cycads express a wide variation for numerous morphological characters. Identifying a plant that represents a population can be time consuming, difficult and is often not a priority when herbarium specimens are collected. Very few specimen labels include details of the morphological variation within the population. The assignment of sectional and subsectional ranks in Cycas has been based primarily on the sharing of characters associated with the seed, and secondarily with other reproductive and pinna features (see Hill, Chapter 3 this volume). For any given section or subsection, seed structure is in several aspects linked to animate and inanimate dispersal processes and thus implicit in part for infrageneric genetic exchange. However, these seed characters are usually not available from herbarium specimens or accompanying data, making it difficult to assign the sectional or subsectional ranks. A suite of useful characters, that can be conveniently documented in the field and later included in the specimen annotation, is needed to assist future taxonomic studies at the section and subsection ranks. To facilitate future taxonomic studies at the sectional, subsectional and specific ranks within Cycas, it is critical to identify a suite of morphological characters that can be accessed, whether through herbarium specimens with their associated annotations and/or through publications. Hill (see Chapter 3 this volume) proposes a suite of such characters. Understanding the significance of a specific suite of characters is essential in the classification of new taxa into the appropriate section or subsection within the genus. The aim of this chapter is to test a suite of characters that may reflect measurable and taxonomically useful features in a consistently reliable classification within Cycas.

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Materials and Methods The author has visited wild populations of almost every non-Australian species in the genus Cycas and herbarium specimens have been made from each population. Prior to collecting specimens, measurements were taken from a number of mature plants within each population using a pre-defined suite of characters. The characters chosen for this study were based on their use in past taxonomic studies within the genus, as well as those that showed potential for supporting future taxonomic studies. The 30 quantitative and qualitative characters (Table 4.1) are associated with seven aspects of a plant: plant habit, leaf, pinna, cataphyll, megastrobilus, microstrobilus and seed. Most of these characters and their measurement aspects are presented in Fig. 4.1. To understand the potential value of the chosen morphological characters for future studies within Cycas, three pairs of distinct yet morphologically similar species were identified, and measurements were obtained from selected wild populations. One population was sampled for four of the six species (C. edentata de Laubenfels, C. elephantipes A. Lindström & K.D. Hill, C. micronesica K.D. Hill and C. siamensis Miquel) and two populations were sampled for the remaining species (C. seemannii A. Braun and C. rumphii Miquel). The first pair of taxa studied was Cycas siamensis and C. elephantipes. Both species are arborescent and native to Thailand. The second pair, C. edentata and C. rumphii, are tall, erect, arborescent cycads from islands in the Pacific Ocean. Cycas edentata and C. rumphii are believed to hybridize naturally where their distributions overlap. The third pair examined was C. seemannii and C. micronesica. Cycas seemannii is a tall, erect, arborescent and usually unbranched species found in Fiji, Vanuatu, the Tonga Islands and New Caledonia. Cycas micronesica (often misidentified in collections as either C. circinalis Linnaeus or C. rumphii) is an erect, arborescent species up to 8 m tall from the Mariana Islands. Populations of these two species are widely separated geographically and no spontaneous hybridization is likely to occur. Nevertheless, molecular evidence indicates that, in addition to being morphologically similar, they are evolutionarily closely related (Ken Hill, Australia, 2002, personal communication). Measurements were recorded for multiple plants within each population for the six species. In some cases, not all characters were measured – male cones and seeds were often not available for all species during the time of the fieldwork. For each population sampled, the number of plants measured, the mean for each character and the standard deviation for each character are listed in Tables 4.2–4.4. Data derived from each species pair were compared using a t-test with an alpha level of 0.05. The t-test assesses whether the means of two groups are statistically different from each other and yields the same results as a one-way analysis of variance (ANOVA). Results from the t-tests are included in Tables 4.2–4.4.

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Table 4.1. Vegetative and reproductive characters for taxonomic studies in Cycas. Characters of questionable use for taxonomic studies are indicated by *. Characters determined to be unstable and variable among species at the onset of the investigation are indicated by **. Unstable and variable characters were removed from the analyses. Plant part

Character/character state

Plant habit

Stem height (cm) Stem minimum diameter (cm) Leaf number Length (cm)* Petiole length (cm) Petiole thickness (mm) Number of spines on petiole** Petiole length percentage spines Terminus (spine, single leaflet, leaflet pair)** Number Length (cm) Width (mm) Basal width (mm) Arrangement of pinnae (opposing, alternate)** Spacing between pinnae (mm) Pinna length (cm) Length (cm) Megasporophyll length (cm) Megasporophyll lamina length (mm) Megasporophyll lamina width (mm)* Megasporophyll apical spine length (mm)* Megasporophyll lateral spine number Megasporophyll number of ovules Microstrobilus length, excluding peduncle (cm) Microstrobilus diameter (cm) Microsporophyll length (mm) Microsporophyll width (mm) Microsporophyll apical spine length (mm) Length (mm) Width (mm)

Leaf

Pinna

Cataphyll Megastrobilus

Microstrobilus

Seed

Results Characters of questionable use Three characters preliminarily included in the study as potentially useful taxonomic characters were proven to be unstable and variable within and among

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Fig. 4.1. Vegetative and reproductive characters measured from Cycas specimens: (1) leaf length; (2) petiole length; (3) pinna number; (4, 8) pinna length; (5) pinna width; (6) pinna basal width; (7) spacing between pinnae; (9) megasporophyll length; (10) megasporophyll lamina length; (11) megasporophyll lamina width; (12) megasporophyll apical spine length; (13) megasporophyll lateral spine number; (14) megasporophyll number of ovules; (15) microstrobilus length (excluding peduncle); (16) microstrobilus diameter; (17) microsporophyll length; (18) microsporophyll width; (19) microsporophyll apical spine length. Characters not shown (see Table 4.1), but included in the study, are those associated with the stem, cataphyll, seed, petiole thickness and petiole length percentage spines.

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SD

n

ELEb Mean

P

SD

8.43 11.43 18.86

4.72 1.72 3.24

10 10 10

87.6 22.7 37.4

48.20 3.23 13.60

< 0.001* < 0.001* < 0.001*

12 12 12 12

75.58 13.79 7.4 69.75

10.35 3.22 1.3 26.37

10 10 10 10

167.3 25.7 15.0 54.0

12.08 6.52 2.7 19.6

< < < =

0.001* 0.001* 0.001* 0.124

12 12 12 12 12 12

73.54 10.04 5.83 3.25 4.33 2.82

8.67 1.6 0.58 0.45 0.78 1.05

10 10 10 10 10 9

117.3 18.76 9.1 3.9 8.2 39.3

20.0 2.8 0.9 0.7 1.3 23.4

< < < = < <

0.001* 0.001* 0.001* 0.028* 0.001* 0.001*

6

2.68

0.84

9

8.14

2.0

2 2 2 2 2

9.25 24 20 25.5 11

1.06 8.48 8.48 14.85 4.24

5 5 5 5 5

siamensis plants from Tak Province, Thailand. elephantipes plants from Chaiyaphum Province, Thailand.

1.9 3.8 9.9 10.0 0

< 0.001* = = = = =

0.006* 0.187 0.051 0.297 0.144

Page 50

7 7 7

15.5 41.6 48.8 44.0 25.2

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aCycas bCycas

SIAa Mean

A. Lindström

Plant habit Stem height (cm) Stem minimum diameter (cm) Number of leaves Leaf Length (cm) Petiole length (cm) Petiole thickness (mm) Petiole length percentage spines Pinna Number Length (cm) Width (mm) Basal width (mm) Spacing between pinnae (mm) Pinna length (cm) Cataphyll Length (cm) Megastrobilus Megasporophyll length (cm) Megasporophyll lamina length (mm) Megasporophyll lamina width (mm) Megasporophyll apical spine length (mm) Megasporophyll lateral spine number

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Character

50

Table 4.2. Sample sizes (n), means, standard deviations (SD) and results from t-tests (P = probability; * = P < 0.05) for morphological characters of Cycas siamensis Miquel (SIA) and C. elephantipes A. Lindström & K.D. Hill (ELE). Material was not available to allow analyses of microstrobilus and seed characters for these taxa.

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Table 4.3. Sample sizes (n), means, standard deviations (SD) and results from t-tests (P = probability; * = P < 0.05; calculated for species comparisons only) for morphological characters of Cycas seemannii A. Braun (SEE) and C. micronesica K.D. Hill (MIC). Material was not available to allow analyses of cataphyll and microstrobilus characters for these taxa.

n

SEEb Mean

SD

n

MICc Mean

SD

8 8

6.5 20.13

2.39 6.49

14 14

2.68 20.29

2.00 11.29

11 11

3.64 15.19

1.23 3.22

= 0.544 = 0.034*

8 8 8 8

230.5 41.63 2.63 34.5

27.21 10.86 0.23 38.92

14 14 14 14

186.1 31.57 2.32 20.71

26.70 6.27 0.42 22.86

15 15

185.8 60.47

72.62 27.98

= 0.423 = 0.003*

15

1.4

2.53

< 0.001*

8 8 8 8 8 7

101.7 28.25 14.75 7.25 8.5 16.43

18.13 1.83 4.00 1.49 2.78 4.16

14 14 14 14 14 12

96.43 24.43 10.86 5.43 8.5 13.34

7.08 3.37 1.10 0.65 2.35 3.73

15 15 15 15 15 15

71.93 16.44 8.2 2.47 8.4 10.23

16.17 13.47 6.69 1.73 6.96 8.58

< = = < = =

0.001* 0.018* 0.041* 0.001* 0.958 0.936

6 6 6 6 6

32.5 50.83 41.83 22.5 11.5

4.68 2.04 5.95 6.90 2.26

12 12 12 12 2

32.42 53.33 36.17 13.42 11.5

5.42 4.44 4.90 4.66 0.71

3 5 5 5 5

36 35.6 31.4 25.6 6

7.81 2.61 6.70 18.67 1.22

= < = = <

0.516 0.001* 0.091 0.338 0.001*

1 1

55 42

2 2

57.5 49

3.54 1.41

5 5

52 49

seemannii plants from Tanna Island, Vanuatu. seemannii plants from Bourail, New Caledonia. micronesica plants from islands of Micronesia (Rota, Guam, Yap and Palau Island).

2.74 6.52

P

= 0.085 = 0.560

Page 51

SD

51

aCycas bCycas cCycas

SEEa Mean

Determining Species Boundaries in Cycas

Plant habit Stem height (cm) Stem minimum diameter (cm) Leaf Length (cm) Petiole length (cm) Petiole thickness (mm) Petiole length percentage spines Pinna Number Length (cm) Width (mm) Basal width (mm) Spacing between pinnae (mm) Pinna length (cm) Megastrobilus Megasporophyll length (cm) Megasporophyll lamina length (mm) Megasporophyll lamina width (mm) Megasporophyll apical spine length (mm) Megasporophyll lateral spine number Seed Length (mm) Width (mm)

n

3:44 pm

Character

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52

A. Lindström

populations of non-Australian Cycas species (Table 4.1). Therefore, the following three characters were excluded early in the study: 1. Terminus of the leaf. Three separate character states have been found: 1. (a) terminating in a spine; 1. (b) terminating in a single leaflet; 1. (c) terminating in leaflet pair. Although sometimes quite uniform in several of the taxa studied, the level of variation seen in the majority of Cycas species indicates that this is not a consistent reliable character for taxonomic studies. This character was removed from the analyses. 2. Number of spines on the petiole. The number of spines is variable and depends on a plant’s age, size and condition. Number of spines on the petiole was therefore removed from the analyses. A more consistent and useful character associated with petiole spines is the percentage of the petiole length that bears spines. 3. The arrangement of the pinnae. The arrangement of pinnae, opposite or alternate to each other on either side of the leaf rachis, was highly variable from individual to individual within a population and was removed from the analyses. During the course of the study, leaf length was often found to be a variable character within a population and within a species. Leaf length can be dependent on light conditions and overall condition of the plant. However, this character was retained in the analyses because it was found to be useful in distinguishing Cycas siamensis and C. elephantipes (Table 4.2). For all three pair comparisons (Tables 4.2 and 4.3), megasporophyll lamina width and megasporophyll apical spine length were the only characters not significant for distinguishing between any of the three pairs of species. These two characters were retained in the analyses because they show promise for delimiting other species in the genus.

Species-specific characters A number of characters examined were found to be taxonomically useful when comparing morphologically similar but distinct species pairs. Table 4.2 presents the results of t-tests for 19 characters for Cycas siamensis and C. elephantipes. Based on the results of the t-tests, 14 of the 19 characters associated with the stem, leaf, pinna, cataphyll and megastrobilus were valuable for distinguishing these two taxa. Although not presented here, similar types of analysis indicated that C. siamensis is morphologically more similar to C. nongnoochiae K.D. Hill and C. elephantipes is morphologically more similar to C. pachypoda K.D. Hill. Fewer than 14 characters differentiated C. siamensis from C. nongnoochiae and C. elephantipes from C. pachypoda. Table 4.3 presents the results for the analyses of data obtained from

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Table 4.4. Sample sizes (n), means, standard deviations (SD) and results from t-tests (P = probability; * = P < 0.05; calculated for species comparisons only) for morphological characters of Cycas edentata de Laubenfels (EDE) and C. rumphii Miquel (RUM). Material was not available to allow analysis of stem and microstrobilus characters for these taxa.

7 7 7

163.7 44.71 88.57

7 7 7 7 7 6

140.3 30.29 13.71 6.14 19.71 22.83

2

7

4 4 4 4 3 4

30.23 63.75 35.5 27.5 8.67 6

edentata plants from Culion Island, Philippines. rumphii plants from Halmahera Island, Indonesia. rumphii plants from Sulawesi, Indonesia.

SD

34.77 11.98 17.73

4 4 4

213.7 59.25 82.5

20.70 3.99 1.704 0.90 4.46 5.85

4 4 4 4 4 4

0 6.263 13.77 5.45 8.67 4.167 0

n

SD

43.04 15.22 5

2 2 2

211 50.5 40

45.25 12.02 14.14

= 0.100 = 0.159 = 0.422

80.5 26 16.25 5.25 13.75 1.25

20.07 6.48 2.5 0.5 3.5 0.5

2 2 2 2 2 1

96.5 25 12.5 4.5 11 18

26.16 5.66 2.12 0.71 1.41 0

= = = = = <

2

1.9

0.85

3 3 3 3 3

29.67 34.33 27.67 26 2.337

4.51 10.07 6.81 10.39 0.58

3

4

0

P

0.002* 0.292 0.135 0.063 0.040* 0.001*

= 0.074 1 1 1 1 1

26 45 25 33 2

1

8

= = = = =

0.896 0.022* 0.180 0.849 0.116

> 0.860

Page 53

SD

53

aCycas bCycas cCycas

n

RUMc Mean

Determining Species Boundaries in Cycas

Leaf Length (cm) Petiole length (cm) Petiole length percentage spines Pinna Number Length (cm) Width (mm) Basal width (mm) Spacing between pinnae (mm) Pinna length (cm) Cataphyll Length (cm) Megastrobilus Megasporophyll length (cm) Megasporophyll lamina length (mm) Megasporophyll lamina width (mm) Megasporophyll apical spine length (mm) Megasporophyll lateral spine number Seed Length (mm)

n

RUMb Mean

3:44 pm

Character

EDEa Mean

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A. Lindström

measuring plants of the morphologically similar Cycas seemannii and C. micronesica. Nine of the 20 characters examined were found to be valuable for discriminating between the two species. At least one of the characters associated with the stem, leaf, pinna and megastrobilus was significant in distinguishing between the species. Table 4.4 presents the summary for the analyses of Cycas edentata and C. rumphii. These two species can be distinguished based on four of the 16 characters examined: pinna number, spacing between pinnae, proximal pinna length and megasporophyll lamina length. Although not presented here, the presence of stout spines terminating the microsporophylls can also be used to distinguish these two species. Most importantly, it was the number of pinnae that was the only character in all three analyses that was consistently significant in distinguishing between morphologically similar species (Tables 4.2 to 4.4).

Discussion A suite of morphological characters has been selected that can be used successfully to distinguish and compare different species in Cycas, even for species that are morphologically similar to one another. The analysis of characters tested in this project indicates that if measurements were obtained using the prescribed suite of characters (Table 4.1), taxonomists would be able to document more rigorously the degree of similarities and differences among taxa. This type of data would strongly augment herbarium specimen studies, as well as provide for a more reliable classification system within Cycas. In support of future taxonomic studies that are dependent on herbarium specimens, specimens from plants within a population should, whenever possible, represent both male and female material. Specimen collectors should obtain specimens that best represent the ‘norm’ within the range of morphological variation in any population. When possible, a whole leaf for each specimen should be preserved. If this is not feasible, the fieldworker should thoroughly document all of the relevant leaf characters (see Table 4.1) for inclusion in the specimen annotation. Herbarium specimens that contain cataphylls, seeds, megasporophylls and male cones should, if possible, represent each population sample. Dried specimens can have loosely distinguishing features such as shape, size and colour. Therefore, these features must be noted in the field and then transcribed to the specimen label. A photographic image of the plant should accompany the herbarium specimen. It is recommended that a form similar to Hill (see Fig. 3.2, Chapter 3 this volume) is used when sampling a population prior to collecting herbarium specimens for any Cycas population. Data derived from the completion of such a form will: (i) document the variation within the population; (ii) ensure that appropriate and taxonomically useful characters are assessed in the field; and (iii) provide the necessary information for incorporation in the herbar-

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Determining Species Boundaries in Cycas

55

ium specimen annotations, thus serving the needs of future generations of Cycas scientists.

Acknowledgements I thank Ken Hill of the Royal Botanic Gardens (Sydney, Australia) who initiated the use of a character sheet for the genus Cycas (see Hill, Chapter 3 this volume). Kampon Tansacha, Director of Nong Nooch Tropical Botanical Garden (Thailand) is most gratefully acknowledged for his committed support, both financially and inspirationally. Kyle Williams helped in preparing this text.

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Comments on Cycas, Dyerocycas and Epicycas (Cycadaceae)

5

Chia-Jui Chen,1 Ken D. Hill2 and Dennis Wm. Stevenson3 1Institute

of Botany, Chinese Academy of Sciences, Xiangshan, Beijing, China; 2Royal Botanic Gardens, Sydney, Australia; 3Institute of Systematic Botany, New York Botanical Garden, Bronx, New York, USA

Abstract The recently described genus Epicycas and the obscure genus Dyerocycas (both separated from Cycas) are evaluated, and generic concepts in Cycadaceae are discussed. Epicycas is a superfluous and illegitimate name, based on the same type as Dyerocycas (i.e. Cycas micholitzii). Dyerocycas is a valid name for a group distinguished by differences in leaflet morphology, but the differences with Cycas are slight, and inconstant in other correlative characters. A taxonomic treatment for the genus Cycas is presented, subsuming Dyerocycas as a generic synonym. Relative diagnostic characters are tabulated and different stem types are illustrated.

Introduction Recently D.J. de Laubenfels described a new genus, Epicycas de Laubenfels, based on a subterranean bulbous stem base (de Laubenfels and Adema, 1998), with eight species from south-eastern Asia. He combined Schuster’s (1932) section Indosinensis and Smitinand’s (1971) section Stangerioides in the new genus with the type Epicycas micholitzii (Dyer) de Laubenfels. The core character for the genus is plants with a mostly underground bulbous base, one or more leafy apices on the surface of the bulb, each eventually developing a short, usually slender trunk or ©CAB International 2004. Cycad Classification: Concepts and Recommendations (eds T. Walters and R. Osborne)

57

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underground bulb branched and generally reaching the fertile stage before any trunk forms.

This is unlike the case in cycad genera in other families, where above-ground trunks are an unmodified continuation of the underground part, or where the bulbous bases are not underground at all (Bowenia Hooker ex Hooker filius is an exception, with a bulbous underground base and multiple slender underground stems). Other characters of Epicycas are: (i) pinnae with flat, often undulate margins; (ii) pinnae in some species dichotomously forked; (iii) pollen cones taperingly cylindrical, while those of Cycas are mostly ovoid; and (iv) terminal lobes in the sterile blade of megasporophylls often dichotomous, even in species with simply pinnate leaves. Fifty-five years before Epicycas was published, Dyerocycas was described by Nakai (1943), named for botanist W.T. Thistleton-Dyer and based principally on the presence of dichotomous pinnae. Other distinguishing characters cited were a subterranean trunk, cylindrical or narrowly oblong pollen cones, and microsporophylls with evenly scattered sporangia beneath – unlike those in Cycas sensu stricto with clusters of sporangia (‘sori’) beneath. Dyerocycas micholitzii (Dyer) Nakai (basionym Cycas micholitzii Dyer) was designated as the type of the genus. Epicycas thus becomes a superfluous and illegitimate name based on the same type as Dyerocycas (St Louis Code Articles 7.4, 11.5, and 52.1; see Greuter et al., 2000). Dyerocycas has a simple description but is a valid name. Although Epicycas is an illegitimate name, it is described in detail and includes almost half the species of Cycas in south-eastern Asia, especially in China. As the authors (de Laubenfels and Adema, 1998) of Epicycas said: Our knowledge of the species of the here newly described genus Epicycas is quite incomplete, much of what we know has only recently been uncovered and several specialists, particularly from China, are actively studying this material. Therefore the treatment of Epicycas will have to be necessarily less complete than that of Cycas.

In our recent fieldwork and laboratory studies of Chinese cycads, in conjunction with herbarium studies both in China and abroad, we have attempted to examine the new described genus in detail and establish its justification. The more deeply our studies proceed, the more firmly we hold to Cycas as the only genus in Cycadaceae. Chen and Stevenson (1999) placed Epicycas as a synonym of Cycas. Hill et al. (K.D. Hill, N.T. Hiêp and P.K. Loc, 2003, unpublished results) followed this treatment, and made a short comment on it. To date, no other authors have recognized either Dyerocycas or Epicycas, and no detailed assessment of these names has been published. We comment below on the newly described genera and discuss the genus concept in Cycadaceae sensu stricto.

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Comments on Cycas, Dyerocycas and Epicycas

59

Characters Among Different Genera In order to make comments on the genera Dyerocycas and Epicycas, and to compare them with Cycas, it is necessary to summarize their diagnostic characters and biogeography (Table 5.1). The species selected in the table include all members of the segregated genera and selected species of Cycas, especially from south-eastern Asia, that show some morphological similarities. Species names are as published in the segregate genera, without implying any acceptance of the segregates. The observations and measurements in Table 5.1 originate from recent literature (Fu et al., 1978; Jones, 1993; Chen and Yang, 1994a,b, 1996; Hill and Chen, 1994; Walters and Yang, 1994; Wei, 1994; Chen et al., 1995; Wang, 1995; Wang and Deng, 1995; Guan and Zhou, 1996; Hill, 1996; Wang et al., 1996; Chen and Zhong, 1997; Yang et al., 1997; Chen and Saren, 1998; de Laubenfels and Adema, 1998; Liu, 1998; Chen, 1999; Chen and Stevenson, 1999; Hill and Yang, 1999; Hill and Osborne, 2001; Hill et al. (K.D. Hill, N.T. Hiêp and P.K. Loc, 2003, unpublished results)); additional data were obtained from PE herbarium and from our own fieldwork. The stem forms in Cycas are illustrated diagrammatically in Fig. 5.1A–F.

Discussion Although the name is superfluous and illegitimate, the generic circumscription of Epicycas becomes that of Dyerocycas under the rules of priority. Since formal transfers of all species included in Epicycas have not been made to Dyerocycas, the group will be discussed below under the name Epicycas. The circumscription of Epicycas, including Smitinand’s (1971) section Stangerioides and Schuster’s (1932) section Indosinenses, delimits a far wider range than the original Dyerocycas. In de Laubenfels’ genus concept, Epicycas far exceeds the eight species listed by him in 1998 – probably to at least 17 species in south-eastern Asia, about half the species of Cycadaceae in this region.

Diagnostic characters inconsistent As shown in Table 5.1, the diagnostic characters of Epicycas are almost all unstable and inconsistent. A mainly underground base as in E. micholitzii and E. multipinnata (C. J. Chen & S.Y. Yang) de Laubenfels (Fig. 5.1A) is a principal defining character for the new genus, but this character is neither wholly consistent within the genus nor restricted to the species placed in the genus (Hill et al., 2002). For example, the trunk of E. elongata (D. Yue Wang ex Leandri as “Cycas elonga”) de Laubenfels sometimes gradually thickens toward the base without any subterranean bulbous structure, and this species has an arborescent, often forked, stem to 8 m in height (Fig. 5.1F). In E. siamensis (Miquel) de Laubenfels, the stem is acaulescent or arborescent and to 2 m tall, but always abruptly swollen at the

ch05.qxd

Stems Distribution

Height (m)

Pinnae Width (mm)

Pollen cones Flat margin

Shape

Size (cm)

MLB

Unbranched

0.6 × 0.3

2

15–28

+

f–c

35–55 × 6–8

+

+

Unbranched

0.6 × 0.25

3

10–24

+

f–c

15–30 × 4–6

+

+

Unbranched

0.8 ×.3

1

15–20

+

c

15–25 × 4–7

+

+ +

Dichotomous Dichotomous

0.5–4 × 0.1–0.3 1 × 0.2

1 1

10–13 6–11

± ±

o–f

Unknown 20–30 × 6–8

+ +

–

Dichotomous

4–8 × 0.5–0.8

1

5–11

+

o

20–25 × 8–9

+

+

Unbranched

2 × 0.3

1

5–8

+

o

22 × 8

–

+

Dichotomous

0.1 × 0.1

1

7–11

+

f

12–20 × 4–5

+

+ + +

Unbranched Congested Congested

12 × 0.4 0.4 × 0.35 0.5 × 0.15

1 1 1

4–5 2–3.5 4–9

– – ±

o o c

15–25 × 12–15 15–20 × 5–7.5 15–25 × 4–6

– – +

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C.-J. Chen et al.

Dyerocycas micholitzii SE Asia (Dyer) Nakai [Epicycas micholitzii (Dyer) de Laubenfels] Epicycas multipinnata China–Vietnam (C.J. Chen & S.Y. Yang) de Laubenfels E. tonkinensis (Linden & SE Asia Rodigas) de Laubenfels E. sp. novum #1 Vietnam E. miquelii (Warburg) China–Vietnam de Laubenfels E. elongata (D. Yue Wang SE Asia ex Leandri as “C. elonga”) de Laubenfels E. siamensis (Miquel) SE Asia de Laubenfels E. lindstromii (S.L. Yang, Vietnam K.D. Hill & Hiêp) de Laubenfels Cycas angulata R. Brown Australia C. beddomei Dyer India C. changjiangensis N. Liu China

Branching

Pinna dissection

3:45 pm

Taxon

Bulbous base

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60

Table 5.1. Character states among Dyerocycas, Epicycas and Cycas.

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5 × 0.45 0.7 × 0.4

1 3

9–12 8–15

+ +

o–c f–c

30–80 × 10–11 13–25 × 4–9

– +

China–Vietnam China

+ –

Dichotomous Unbranched

0.8 × 0.18 1–3 × 0.25–0.3

1 1

6–9 6–7

– ±

f c

20–35 × 6–10 25–45 × 6–8

+ +

Asia

–

Dichotomous

1–17 × 0.15–0.9

1

6–8

±

o

30–55 × 15–22

–

Australia Asia, Pacific China

+ – +

Unbranched Adventitious Unbranched

0.8–4 × 0.2–0.4 1.5–12 × 0.2–0.5 0.15–0.8 × 0.1–0.4

1 1 1

4–6 12–18 12–18

– – +

o o–c c

15–20 × 8–11 35–45 × 12–20 30–60 × 5–12

– + +

China

+

Dichotomous

0.6 –3 × 0.3–0.5

1

10–15

+

c

35–60 × 5.5–10

–

China China–Vietnam Philippines

– + +

Dichotomous Unbranched Unbranched

2–8 × 0.2–0.8 1 0.8–2 × 0.15–0.35 1 5 × 0.4 1

8–16 15–22 5–8

+ + ±

c c c

35–60 × 7–11 30–40 × 5–8 40–70 × 9–10

+ + +

+, present; ±, variable; –, absent. MLB, megasporophyll lamina lobes branched. Pinna dissection: 1, none; 2, twice; 3, thrice. Pollen cone shape: c, cylindrical; f, fusiform; o, ovoid.

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Congested Unbranched

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– +

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S Asia China

Comments on Cycas, Dyerocycas and Epicycas

C. circinalis Linnaeus C. debaoensis Y.C. Zhong & C.J. Chen C. ferruginea F.N. Wei C panzhihuaensis L. Zhou & S.Y. Yang C. pectinata Buchanan–Hamilton C. platyphylla K.D. Hill C. rumphii Miquel C. segmentifida D.Yue Wang & C.Y. Deng C. szechuanensis C.Y. Cheng, W.C. Cheng & L.K. Fu C. taiwaniana Carruthers C. tanqingii D.Yue Wang C. wadei Merrill

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Fig. 5.1. Stem forms of Cycas and Epicycas. (A) Stem subterranean, mostly underground [e.g. C. debaoensis Y.C. Zhong & C.L Cheng, E. micholitzii (Dyer) de Laubenfels, E. multipinnata (C.J. Chen & S.Y Yang) de Laubenfels and E. tonkinensis (Linden & Rodigas) de Laubenfels (= C. balansae Warburg)]. (B) Bulbous underground base producing a slender aerial stem or branched short stem [e.g. C. ferruginea F.N. Wei and E. miquelii (Warburg) de Laubenfels (= C. sexseminifera F.N. Wei)]. (C) Stem almost all subterranean and frequently branched [e.g. C. chevalieri Leandri and E. lindstromii (S.L. Yang, K.D. Hill & Hiêp) de Laubenfels]. (D) Trunk abruptly swollen at base [e.g. C. changjiangensis N. Liu and E. siamensis (Miquel) de Laubenfels]. (E) Trunk simple and erect as in most species [e.g. C. media R. Brown and C. panzhihuaensis L. Zhou & S.Y Yang]. (F) Trunk often dichotomously branched [e.g. C. pectinata Buchanan-Hamilton and E. elongata (D. Yue Wang ex Leandri as "C. elonga") de Laubenfels].

base (Fig. 5.1D). These stems are unlike the subterranean bulbous stem considered typical of Epicycas (Fig. 5.1A–C). In Cycas, however, there are some species possessing a more or less thickened or swollen stem at the base like those in

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Comments on Cycas, Dyerocycas and Epicycas

63

Epicycas, e.g. Cycas changjiangensis N. Liu in Hainan, China (Fig. 5.1D), which has a stem similar to Epicycas siamensis. Similar stems are seen sometimes in Cycas beddomei Dyer in south-east India, C. wadei Merrill in the Philippines, and even in C. circinalis Linnaeus (the type of Cycas) in southern India. Pinnae with flat and often undulate margins were also regarded as distinctive of Epicycas. However, this character is not always consistent in Epicycas (Table 5.1), especially in E. miquelii (Warburg) de Laubenfels and E. sp. novum #1, and it is also common in Cycas in both Asia and Australasia. Even in C. circinalis, the type of the genus, the pinnae show a flat margin and are often undulate. Dichotomous pinnae appear in only a few species, e.g. Epicycas micholitzii, E. multipinnata and Cycas debaoensis Y.C. Zhong & C.J. Chen. Dichotomous lobing of the sterile lamina of the megasporophyll is common in many species of Cycas, especially in Asia, but typical only in C. segmentifida D. Yue Wang & C.Y. Deng. Pollen cones in Epicycas are not always tapering and cylindrical in shape; for example, E. elongata and E. siamensis have ovoid pollen cones. Most species of Cycas in Asia also have cylindrical pollen cones.

Subterranean and thickened stems shown to be specialized forms Cycas, in general, like Dioon Lindley, Lepidozamia Regel and Encephalartos Lehmann, is characteristically arborescent, except for a few species. The trunks retain a close covering of narrow cataphylls and large overlapping leaf bases, and sometimes show a prominent megasporophyll base ring for many years. These persistent processes have a supportive and protective function (Norstog and Nicholls, 1997). In Cycas there are two main stem types and six subtypes (Fig. 5.1): I.

Subterranean 1. Stem subterranean, at least half of stem underground, but with nearly equal thickness in both ends (Fig. 5.1A), e.g. Cycas debaoensis, Epicycas micholitzii, E. multipinnata and E. tonkinensis (Linden & Rodigas) de Laubenfels (= C. balansae Warburg). 2. Bulbous underground base producing a slender aerial stem or many branched small and short stems (Fig. 5.1B), e.g. Cycas ferruginea F.N. Wei and Epicycas miquelii (= Cycas sexseminifera F.N. Wei). 3. Branched subterranean stem almost without aerial stems (Fig. 5.1C), e.g. Cycas chevalieri Leandri and Epicycas lindstromii (S.L. Yang, K.D. Hill & Hiêp) de Laubenfels.

II. Arborescent 4. Trunk swollen at base (Fig. 5.1D), e.g. Cycas changjiangensis and Epicycas siamensis. 5. Trunk simple and erect (Fig. 5.1E), e.g. Cycas media R. Brown and Cycas panzhihuaensis L. Zhou & S.Y. Yang. 6. Trunk erect and dichotomously branched (Fig. 5.1F), e.g. Cycas pectinata Buchanan-Hamilton and Epicycas elongata.

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Epicycas, as circumscribed by de Laubenfels, includes five of the above stem types (Fig. 5.1A–D, F), i.e. E. micholitzii, E. multipinnata and E. tonkinensis with stem type I-1, E. miquelii and E. sp. novum #1 with type I-2, E. lindstromii and partly E. miquelii with type I-3, E. siamensis with type II-4 and E. elongata with type II-6. All stem types also exist in Cycas (sensu stricto in de Laubenfels’ definition). This stem character is therefore not diagnostic for either genus. The growth habitats of many of these species are often dry or seasonally dry and sunny. The swollen or thickened stem in Epicycas and in some Cycas species might therefore be a result of convergence in relatively similar environments. The subterranean and thickened stems could be considered as specialized forms adopted to survive particular harsh environmental conditions, such as drought and repeated burning, minimizing the possibility of damage (Norstog and Nicholls, 1997). These species, however, have been placed in different taxonomic groups (Hill, 1995, 1999; Wang et al., 1996) and both morphology and micromorphology suggests that relationships of some of these species are not close (Xi and Wang, 1989; Wang et al., 1996). Epicycas miquelii (= Cycas sexseminifera) and C. ferruginea growing in crevices in bare outcrops in rugged karst limestone hills in west Guangxi, China, and in north Vietnam, are dwarf in habit with short, above-ground bulbous stems, often with multiple branches when older. However, they are not closely related to C. micholitzii (Wang et al., 1996). In contrast to the short stems adapted to dry environments on limestone cliffs, Epicycas micholitzii (= Cycas micholitzii), E. multipinnata and E. tonkinensis (= Cycas balansae) have mostly subterranean stems, and are adapted to dense tropical forests. In these conditions, the plants may receive limited light. Reduction of the emerging aerial stem, leaf number and size of the megasporophyll cluster may decrease energy consumption, while lengthening leaves and enlarging and even dividing the leaflets as in E. multipinnata would allow more light assimilation in dense forests.

Sole character inadvisable Epicycas is defined almost solely on having an underground bulbous base on which one or more leafy apices grow, each eventually developing a short, usually slender trunk, or branched bulb (de Laubenfels and Adema, 1998). In actual fact, in most species of Epicycas, such as E. micholitzii, E. multipinnata, E. tonkinensis, E. siamensis and at least partly in E. miquelii, the emergent trunks are an unmodified continuation of the underground part, like those of Cycas (Fig. 5.1A). Only in E. lindstromii and E. miquelii (Fig. 5.1C) are subterranean stems often branched to produce modified, shortly slender aerial stems. The subterranean habit is maintained by the activity of contractile elements in roots and stems themselves, a phenomenon known in several groups of plants and investigated in cycads most recently by Stevenson (1980) and Norstog and Nicholls (1997). Stevenson found that, in arborescent cycads, the contractile property is confined to the roots, but all subterranean forms also have contractile

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stems. In these, the stem itself is often observed to have external wrinkles. Stem contraction, almost certainly a further adaptation to keep the stem underground, correlates well with the development of a subterranean habit rather than with evolutionary affinities (Norstog and Nicholls, 1997). Although the subterranean stem appears to be a specialized, advanced character, no other consistent characters are correlated with this habit in defining an Epicycas group. Dichotomous pinnae appear only in two or three species. Pinnae with flat and sometimes undulate margins can be found in many species in both genera. Most species in both genera, especially in Asia, commonly possess more or less dichotomous lobes in the sterile blade of megasporophylls. The cylindrical pollen cones are common in the two genera, especially in Asia. Therefore, Epicycas is defined based solely on the bulbous underground base.

Sister species referred to the different genera Some pairs of clearly sister species are placed in the different genera in de Laubenfels and Adema (1998). A good example is that Cycas elongata (Leandri) D. Yue Wang as C. “elonga” (Fig. 5.1F) and C. siamensis (Fig. 5.1D) are placed in Epicycas, while Cycas pectinata (Fig. 5.1F) is referred to Cycas. All occur in southeastern Asia, and are closely allied to one another in their narrow pinnae with a midrib flat above and raised below, ovoid pollen cone with a long apical spine on each microsporophyll, and seed structure with a fibrous layer over a smooth sclerotesta.

Dyerocycas a natural genus? Nakai (1943) separated Dyerocycas from Cycas and designated Dyerocycas micholitzii as the type of the genus. This genus was defined principally by the subterranean stems and dichotomous pinnae, correlated with cylindrical or narrowly oblong pollen cones, microsporophylls with separate sporangia beneath, and megasporophylls with a flabellate-pectinate sterile blade. Dyerocycas when erected included only D. micholitzii, but would now include two or three recently described species in Cycas. This small group is readily distinguishable from Cycas (sensu stricto) by the dichotomous pinnae. In this circumscription, Dyerocycas is more likely a natural group, more restricted in membership than Epicycas and with diagnostic characters discontinuous with those of Cycas and correlated with other characters. However, the members of Cycas sensu lato present a uniform appearance, the same chromosome number (2n = 22), and common morphology such as megasporophylls foliiform, ovules more than two, seeds zygomorphic (platyspermic), young pinnae coiled (circinate ptyxis), and pinnae with a midrib and no lateral veins. The degree of difference between Nakai’s genus and Cycas sensu stricto is small, and inconstant in other correlative characters such as these and the sub-

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terranean trunk and pollen cone shape. Therefore, the present authors consider Cycas a natural genus, and Cycadaceae a monotypic family. The many current infrageneric categories need further study to determine relationships between species, but this does not hinder us in continuing to use the old binomial. The changes of genera should not be undertaken unless there are strong taxonomic reasons for the change (Davis and Heywood, 1963) and these have not yet been demonstrated. Nakai (1943) also described ‘microsporophylla……subtus tota facie sporangiata’ in his Dyerocycas, but as ‘subtus sorifera’ in Cycas. In our examination of materials in the different groups, no apparent pattern in microsporangium arrangement has been revealed and in fact, at least in our examined species, microsporangia are arranged radially in clusters of three to five microsporangia (‘sori’) on the abaxial surface of microsporophylls. Possibly, the radial symmetry of cycad ‘sori’ suggests a relationship to those of pteridosperms, e.g. Potoniea (Norstog and Nicholls, 1997) or eusporangiate ferns such as the Marattiaceae (Stevenson, 1990).

Conclusions 1. Dyerocycas Nakai is an effectively and validly published name. Epicycas de Laubenfels is a later name based on the same type as Dyerocycas Nakai (i.e. Cycas micholitzii); therefore Epicycas must be a superfluous and illegitimate name. 2. Epicycas is defined principally based on a single character (the subterranean stem), not on the sum total of characters manifested in Cycas. Even this character is inconsistent within the genus Epicycas. There are also examples of sister species placed in different genera. The Epicycas concept is not a natural group and can not be accepted. Similarly, the name Dyerocycas based on the Epicycas circumscription cannot be accepted. 3. Dyerocycas in the original circumscription of Nakai may be a natural group, but the relationship with the remaining species of Cycas is unclear and does not appear to be a simple sister relationship. Therefore, Dyerocycas should be placed in synonymy with Cycas. The nomenclatural treatment for the genus Cycas thus becomes: Cycas Linneaus (1753) Species Plantarum, 1188. LECTOTYPE: C. circinalis Linnaeus, designated by Stevenson in Jarvis et al. (1993). Synonym: Dyerocycas Nakai, 1943. Ordines, familiae, tribi, genera, sectiones, species, varietates, formae et combinationes novae, a Prof. Nakai-Takenosin adhuc ut novis edita, Appendix quaestiones characterium naturalim plantarum. Universitatis Imperialis Tokyoensis. p. 208. TYPE: Dyerocycas micholitzii (Dyer) Nakai (= Cycas micholitzii Dyer). Synonym: Epicycas de Laubenfels in de Laubenfels and Adema (1998), Blumea 43, 388. TYPE: Epicycas micholitzii (Dyer) de Laubenfels (= Cycas micholitzii Dyer).

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References Chen, C.J. (1999) Taxonomical and biogeographical studies on Cycas L. (Cycadaceae) in China. In: Chen, C.J. (ed.) Biology and Conservation of Cycads. Proceedings of the Fourth International Conference on Cycad Biology. International Academic Publishers, Beijing, China, pp. 116–128. Chen, C.J. and Saren, J. (1998) Cycads in Asia, with notes on the conservation of cycads in China. In: Chiu, S.T. and Peng, C.I. (eds) Proceedings of the Cross-strait Symposium on Floristic Diversity and Conservation. National Museum of Natural Science, Taichung, Taiwan, pp. 47–64. Chen, C.J. and Stevenson, D.W. (1999) Cycadaceae. In: Wu, Z.Y. and Raven, P.H. (eds) Flora of China, Vol. 4, Cycadaceae through Fagaceae. Science Press, Beijing, China, and Missouri Botanical Garden Press, St Louis, Missouri, pp. 1–7. Chen, C.J. and Yang, S.Y. (1994a) Cycas multipinnata C.J. Chen & S.Y. Yang – a remarkable new cycad from China. Acta Phytotaxonomica Sinica 32, 239. Chen, C.J. and Yang, S.Y. (1994b) Supplementary description of Cycas multipinnata C.J. Chen & S.Y. Yang. Acta Phytotaxonomica Sinica 32, 480–481. Chen, C.J. and Yang, S.Y. (1996) Notes on Cycas multipinnata C.J. Chen & S.Y. Yang. Acta Phytotaxonomica Sinica 34, 563–564. Chen, C.J. and Zhong, Y.C. (1997) Cycas debaoensis Y.C. Zhong & C.J. Chen – a new cycad from China. Acta Phytotaxonomica Sinica 35, 571. Chen, C.J., Zhou, L., Yang, S.Y. and Han, Z.S. (1995) Cycas in China, with notes on its conservation status. In: Vorster, P. (ed.) Proceedings of the Third International Conference on Cycad Biology. Cycad Society of South Africa, Stellenbosch, South Africa, pp. 177–191. Davis, P.H. and Heywood, V.H. (1963) Principles of Angiosperm Taxonomy. Oliver and Boyd, Edinburgh, 556 pp. De Laubenfels, D.J. and Adema, F. (1998) A taxonomic revision of the genera Cycas and Epicycas gen. nov. (Cycadaceae). Blumea 43, 351–400. Fu, S.H., Cheng, W.C., Fu, L.K. and Chen, C.J. (1978) Cycadaceae. In: Cheng, W.C. and Fu, L.K. (eds) Flora Reipublicae Popularis Sinicae 7. Science Press, Beijing, China, pp. 4–17. Greuter, W., McNeill, J., Barrie, F.R., Burdet, H.M., Demoulin, V., Filgueiras, T.S., Nicolson, D.H., Silva, P.C., Skog, J.E., Trehane, P., Turland, N.J. and Hawksworth, D.L. (2000) International Code of Botanical Nomenclature (Saint Louis Code). Koeltz Scientific Books, Köningstein, Germany, 474 pp. Guan, Z.T. and Zhou, L. (1996) Cycads of China. Sichuan Science and Technology Press, Chengdu, China, 242 pp. Hill, K.D. (1995) Infrageneric relationships, phylogeny and biogeography of the genus Cycas (Cycadaceae). In: Vorster, P. (ed.) Proceedings of the Third International Conference on Cycad Biology. Cycad Society of South Africa, Stellenbosch, South Africa, pp. 139–162. Hill, K.D. (1996) A taxonomic revision of the genus Cycas (Cycadaceae) in Australia. Telopea 7, 1–64. Hill, K.D. (1999) Cycas – an evolutionary perspective. In: Chen, C.J. (ed.) Biology and Conservation of Cycads. Proceedings of the Fourth International Conference on Cycad Biology. International Academic Publishers, Beijing, China, pp. 98–115. Hill, K.D. and Chen, C.J. (1994) On Cycas taiwaniana Carruthers (Cycadaceae) and the cycads of south-eastern China. Acta Phytotaxonomica Sinica 32, 538–548.

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Hill, K.D. and Osborne, R. (2001) Cycads of Australia. Kangaroo Press, Sydney, Australia, 116 pp. Hill, K.D. and Yang, S.L. (1999) The genus Cycas (Cycadaceae) in Thailand. Brittonia 51, 48–73. Jarvis, C.E., Barrie, F.R., Allan, D.M. and Reveal, J.L. (1993) A list of Linnaean generic names and their types. Regnum Vegetabile 127, 1–100. Jones, D.L. (1993) Cycads of the World – Ancient Plants in Today’s Landscape. Reed, Chatswood, Australia, 312 pp. Liu, N. (1998) A new species of the genus Cycas from Hainan Island, China. Acta Phytotaxonomica Sinica 36, 552–554. [Cycas changjiangensis.] Nakai, T. (1943) Ordines, familiae, tribi, genera, sectiones, species, varietates, formae et combinationes novae, a Prof. Nakai-Takenosin adhuc ut novis edita, Appendix Quaestiones characterium naturalim plantarum. Universitatis Imperialis Tokyoensis, Tokyo, Japan, 208 pp. Norstog, K.J. and Nicholls, T.J. (1997) The Biology of the Cycads. Cornell University Press, Ithaca, New York, 363 pp. Schuster, J. (1932) Cycadaceae. In: Engler, A. (ed.) Das Pflanzenreich, Fascicle 99, Vol. 4, Part 1, pp. 1–168. Smitinand, T. (1971) The genus Cycas Linn. (Cycadaceae) in Thailand. Natural History Bulletin of the Siam Society 14 (1–2), 163–175. Stevenson, D.W. (1980) Observations on root and stem contraction in cycads (Cycadales) with special reference to Zamia pumila L. Botanical Journal of the Linnaean Society 81, 275–281. Stevenson, D.W. (1990) Morphology and systematics of the Cycadales. In: Stevenson, D.W. (ed.) The Biology, Structure, and Systematics of the Cycadales. Proceedings of the Symposium CYCAD 87. Memoirs of the New York Botanical Garden 57, pp. 8–55. Walters, T.W. and Yang, S.L. (1994) The cycads of China: findings from the Montgomery Foundation/Fairchild Tropical Garden 1992 expedition. Journal of the Cycad Society 1, 6–11. Wang, D.Y. (1995) A preliminary study of the Cycas micholitzii complex. Encephalartos 44, 31–38. Wang, D.Y. and Deng, C.Y. (1995) A new species of Cycas (Cycadaceae) from China. Encephalartos 43, 11–14. [Cycas segmentifida.] Wang, F.X., Liang, H.B., Chen, T.Q. and Wang, D.Y. (1996) Cycads in China. Guangdong Science and Technology Press,. Guangzhou, China, 295 pp. Wei, F.N. (1994) A new cycad from Guangxi. Guihaia 14, 300. [Cycas ferruginea.] Xi, Y.Z. and Wang, F.H. (1989) Pollen exine ultrastructure of extant Chinese gymnosperms. Cathaya 1, 119–142. Yang, S.L., Hill, K.D. and Hiêp, N.T. (1997) Cycas lindstromii. Novon 7, 213–215.

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Piet Vorster Botany Department, University of Stellenbosch, Stellenbosch, South Africa

Abstract Much progress has been made towards recognizing and circumscribing species of Encephalartos, and currently 65 species plus two subspecies are recognized. Some of the characteristics used for circumscription of species could be used to construct a phylogenetic tree, but others have merely diagnostic value. When constructing a phylogenetic tree, it is essential to keep in mind basic biological principles concerning reproductive behaviour, isolation and geographical distribution, because the first two especially are key factors in evolution. The following evidence is available for phylogenetic reconstruction: vegetative morphology, morphology of reproductive structures, pollen morphology, leaflet anatomy, chromosome number and morphology, chemical characteristics, isoenzyme profiles, DNA analyses and geographical information.

Introduction Taxonomy consists of several phases. The first phase is to recognize and circumscribe taxonomic units, be it families, genera, species or subspecies. In practice this is done on morphological evidence, but it is meaningless unless reproductive behaviour as a driving force of evolution is recognized. The second phase is naming of the circumscribed taxonomic units, an activity often denigrated by taxonomists who do not understand the significance of a correct and practical nomenclature. The third phase comprises the determination of evolutionary relationships between the previously circumscribed taxonomic units. This is the ©CAB International 2004. Cycad Classification: Concepts and Recommendations (eds T. Walters and R. Osborne)

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most difficult phase; it involves assessing all the available evidence and deducing the relationships that we find most satisfactory. What makes this phase even more difficult is that practically all the available evidence represents a status at the present time, whereas evolution is a process that in the case of cycads spans a period of tens of millions of years. Much progress has been made towards recognizing and circumscribing species of Encephalartos Lehmann and currently 65 species plus two subspecies are recognized (Hill et al., Appendix 1 this volume). Much of the known distribution range outside South Africa is still imperfectly explored, even in respect of such relatively large and conspicuous plants as is the case for most species of Encephalartos, and it seems likely that more species will be discovered. The leading South African cycad botanist, Dr R.A. Dyer (personal communication), was against recognizing infraspecific categories in Encephalartos and the present author has followed that principle. Recognition of infraspecific categories implies a closer evolutionary relationship between the infraspecific taxa than between species, and such views cannot be substantiated with currently available evidence. In this regard, caution should also be exercised when using genetic distance when analysing molecular data. As long ago as 1930 Du Rietz argued convincingly that the taxonomic discontinuity between infraspecific taxa belonging to the same species may be greater than between different species, because reproductive behaviour is the prime isolating factor in speciation. It follows that an apparently minor genetic change may cause total reproductive isolation between two otherwise genetically identical taxa which would then behave like separate species; and conversely that two taxa at opposite ends of a somewhat discontinuous range of variation may differ genetically to a considerable extent, but still be reproductively compatible and exhibit many common features. Some of the characteristics used for circumscription of species could be used to construct a phylogenetic tree, but others have merely diagnostic value. At this stage of knowledge of Encephalartos, the evolutionary significance of morphological characteristics simply is not known and caution about convergence must remain. When constructing a phylogenetic tree, it is essential to keep in mind basic biological principles concerning reproductive behaviour, isolation and geographical distribution, because the first two especially are key factors in evolution.

Available Evidence Vegetative morphology The vegetative morphology of Encephalartos has never been studied as such, but is well known although poorly understood in respect of its evolutionary significance. In comparison with other living genera of the Cycadales, Encephalartos is well endowed with taxonomically useful vegetative characteristics (Vorster, 1993). From observations on cultivated plants it is evident that some of these characteristics are plastic.

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Firstly, some characteristics change unrecognizably with the age of the plant. For example, in immature plants, leaves of basal offshoots and the first leaves produced after defoliation tend to have heavily dentate leaflets, while a few leaf flushes later the leaflets on the same plant may be completely entire. Thus in Encephalartos woodii Sander the very characteristic pattern of dentation in such early leaves vanishes completely in later-produced leaves. Similarly, many species produce copious amounts of trichomes at the apices of the stems prior to the emergence of cones or new foliage, and in some cases the emerging leaves themselves are hairy; but in some species the trichomes on the stem apices are not persistent, and in most species the hairs on the foliage are caducous. Useful information may yet be discovered in a study of trichome types at species level (Stevenson, 1981). For this same reason seedling plants often bear no similarity to mature plants and are consequently difficult to identify. Apart from illustrations of seedling leaflets of a few species (Giddy, 1974; Jones and Wynants, 1997), it is not known what seedlings look like. Secondly, some characteristics are influenced by environmental factors. For example, in Encephalartos equatorialis P.J.H. Hurter, leaflets characteristically overlap (Vorster and Heibloem, 1995), but if a leaf develops under less bright conditions, leaflets are more widely spaced and do not overlap. Similarly, the angle between opposing leaflets is used in descriptive taxonomy, but this angle can also be much larger than normal under more moist or shady conditions.

Morphology of reproductive structures The morphology of reproductive structures in Encephalartos is also reasonably well known, but again poorly understood. Until fairly recently, species of Encephalartos were defined in terms of vegetative characteristics, but Dyer (1956, 1965) distinguished E. princeps R.A. Dyer from E. lehmannii Lehmann, E. arenarius R.A. Dyer from E. latifrons Lehmann, and E. trispinosus (Hooker) R.A. Dyer from E. horridus (Jacquin) Lehmann on their cone morphologies. Vorster (1993) listed cone characteristics used in taxonomy and described a number of new species in terms of their cones (Robbertse et al., 1988a,b; Vorster, 1990, 1995, 1996a,b,c). The underlying philosophy is that the reproductive processes are of prime importance in affecting and maintaining reproductive isolation as a factor in speciation. Although it is possible to divide many species into groups on the basis of cone morphology, the evolutionary significance of these characteristics is unclear.

Pollen morphology The pollen morphology has been studied in a number of South African cycad species (Dehgan and Dehgan, 1988; Marshall et al., 1989a). Unlike in some other plant groups, the pollen grains within Encephalartos seem to be very similar between species in respect of shape and surface sculpturing, and unlikely to con-

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tribute towards the taxonomy and understanding of the phylogeny of the genus. Nevertheless, the pollen grains of unstudied species should be studied to complete the database.

Leaflet anatomy Leaflet anatomy has been studied in some South African cycads (Koeleman et al., 1981; Spreeth and Vorster, 1995), but should be investigated for all species. It is also necessary to study several samples of every species, taken throughout their distribution range, in order to assess variation within species. This neglected type of evidence is very likely to yield phylogenetically useful information, though convergence and divergence are ever-present pitfalls. Useful information may be discovered in a study of the morphology of wax platelets deposited on the leaf surfaces (Osborne and Stevens, 1996; Hill and Stanberg, 1999).

Chromosome number and chromosome morphology The chromosome number has been determined for only a few Encephalartos species (Marchant, 1968; Mogford, 1981; Moretti, 1990), and in all these is 2n = 18. Breeding experiments with cultivated plants suggest reproductive barriers between some species within the same genus. For instance, the group of species (Group 1, see later) comprising E. brevifoliolatus Vorster, E. cycadifolius (Jacquin) Lehmann, E. friderici-guilielmi Lehmann, E. ghellinckii Lemaire, E. humilis I. Verdoorn, E. laevifolius Stapf & Burtt Davy and E. lanatus Stapf & Burtt Davy seems to have a cytological reproductive barrier against hybridization outside this group. Similarly, E. inopinus R.A. Dyer seems to be reproductively incompatible with any other species, and attempts to hybridize E. ferox Bertolini filius with other species have met with a very low success rate. Chromosome number for all species should be determined as a matter of priority, while individual karyotypes, which may explain reproductive incompatibility between species, should be documented.

Associated organisms Associated organisms have not been studied in proportion to their possible importance to the taxonomy, and indeed survival, of Encephalartos. Apart from the leaf-eating larvae of Zerenopsis leopardina Felder (Lepidoptera: family Geometridae), a considerable number of snout beetle species (Coleoptera: family Curculionidae) appear to be associated exclusively in nature with different species or species groups of Encephalartos (Oberprieler, 1995) and have been used in the taxonomy of Encephalartos (Vorster and Oberprieler, 1999). Some of these have been demonstrated to be pollinators (Donaldson et al., 1995); others, like species

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of Antliarrhinus Schoenherr, are seed predators; but the majority seem to live and breed on the plants without playing any part in the plants’ reproductive processes. Oberprieler’s ongoing studies on the taxonomy and phylogeny of these beetles may well be significant in reconstructing the phylogeny of Encephalartos. Norstog (1987) and Norstog and Nicholls (1997) speculated that the beetle–cycad relationship is very old, at least in respect of pollinating beetles, and the phylogeny of the beetles may be surmised to mirror that of Encephalartos, adding another type of phylogenetic evidence. The same argument applies to the symbiotic Cyanophyta which inhabit and probably cause development of coralloid roots. Numerous studies have been published on the physiology of these (e.g. Pate et al., 1988), but of more importance to taxonomy is the work on the identity and specificity of the Cyanophyta by Grilli Caiola (1975), Grobbelaar et al. (1987), Marshall et al. (1989b) and Grobbelaar and Marshall (1993). Grobbelaar et al. (1987) isolated seven species of Cyanophyta, in two genera, from 31 species of Encephalartos. It is possible that these Cyanophyta have a wide tolerance of host species (Grobbelaar et al., 1987) and thus may not contribute much to phylogenetic reconstruction in Encephalartos. Lastly, Vovides (1991) demonstrated the association of mycorrhiza with Mexican cycads. Should it be proved that mycorrhiza are associated with all the Cycadales, it may be profitable to study the taxonomy and partner-specificity of the fungus involved. Regrettably it seems unlikely that the associated Cyanophyta and mycorrhiza will be studied in sufficient detail in the foreseeable future.

Chemical characteristics The chemical characteristics of Encephalartos are poorly known. All species investigated have methylazoxymethanol (MAM) glycosides (De Luca et al., 1980; Moretti et al., 1983), but finer distinctions that may illuminate evolutionary history have not been recorded, and it seems as if the MAM glycosides do not show the kind of variability found, for example, in alkaloids in other plant groups. Most, if not all, species have deposits of alkane waxes on leaf surfaces (Osborne and Stevens, 1996), the thickness and crystallization pattern of the deposits being responsible for the range of leaf colours from bright green to silvery grey. At least the thickness of the deposits seems to have taxonomic implications, and it is conceivable that thick deposits evolved independently in different parts of the geographical range. The chemistry of these waxes was studied by Osborne et al. (1989) and a study of their chemical evolution may shed light on the phylogeny of the species. Stephens and Stephen (1988) found that sugars resulting from acid hydrolysis of gummy exudates varied considerably between three species examined. Flavonoids should be investigated, because the analysis is relatively inexpensive and has proved useful in other plant groups. Perhaps the phylogenetically most important chemical compounds associated with Encephalartos are the volatile substances released by cones, especially male cones, some details of which have been reported by Pellmyr et al. (1991) and Tang

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(1993). These have far-reaching taxonomic implications, because they serve to attract very particular species of pollinating vectors. This is especially important in areas where several species of Encephalartos occur together and cone simultaneously, yet where hybridization seldom occurs. Apart from characterizing the constituent compounds responsible for a specific odour, the study should take account of the synthesis of the compounds and mechanisms by which the different compounds can evolve. The relationship between volatile substances of different Encephalartos species is likely to mirror that of the plants themselves.

Isoenzymes Isoenzymes have yielded promising results in other cycad genera (Walters and Decker-Walters, 1991) and have been compared for a few South African species (Van der Bank et al., 1998, 2001). This method is less expensive than DNA comparisons, and in a pilot study (Van der Bank et al., 2001) yielded results that are more compatible with morphological evidence than DNA. While this type of evidence has relatively high resolution and is a useful tool in circumscribing and even identifying species, its value in reconstructing phylogenetic relationships is less tested. The method is also difficult to use, because freshly collected material has to be fixed in liquid nitrogen, which presents logistic difficulties in the field. The technical constraints of the method largely preclude its application to wild plants, but it is ideally suited to cultivated material, which fortunately abounds.

DNA analysis DNA analysis is the current fashionable evidence of phylogenetic history. At face value, it certainly seems to be an appropriate approach, because it is the genes that change in evolutionary processes. However, it should be kept in mind that only a very small part of the genome can at present be analysed and compared between species. It is not known whether this portion of the genome plays any part in the evolution of any species, because many completely different factors may result in reproductive isolation and consequent evolution. Van der Bank et al. (2001) used rbcL and internal transcribed spacer 1 and 2 sequences in an exploratory study of some Eastern Cape cycads, which were assessed together with isoenzyme and morphological evidence. On the whole the results were acceptable against the background of morphological and geographical evidence, but should be accepted with reservations because the work implies that the rare phenomenon of strong and characteristic lobing of the leaflets arose independently in different Eastern Cape species but nowhere else in the genus. In view of the perceived antiquity of cycads and their slow reproduction rate, a surprising deduction was that all the species examined were derived from a common ancestor less than a million years ago. Overall there was little genetic variation in

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the material examined, similar to results obtained through isoenzyme analysis for Macrozamia Miquel by Sharma et al. (1998, 1999). As part of an MSc project, M.E. Coetzer (2000, University of the Orange Free State, Bloemfontein, South Africa, unpublished) intended to carry out a molecular study of the whole genus by means of DNA amplification fingerprinting and random amplified polymorphic DNA techniques. She had at her disposal material of most species in the genus, but was not successful in extracting DNA from all the species. Neither did she have sufficient replicates of all the species. The results of her analysis are disappointing in that her phylogenetic tree shows little agreement with morphological and geographical evidence. Nevertheless, this type of evidence holds promise, and both ribosomal and chloroplast DNA data should be gathered for all species, with sufficient replicates from different parts of the distribution range, and using the widest possible range of genes. However, this method should be applied only in collaboration with botanists who understand the plant group’s biology.

Geographical evidence The non-taxonomist is often perplexed by the value accorded by taxonomists to geographical evidence. Yet this type of evidence is an obvious reflection of the evolutionary process, often indicative of groups of related species that are geographically grouped together. Species that became reproductively isolated from each other relatively recently tend to occur in closer geographical proximity to each other than species that separated reproductively in the more distant past, reflecting the amount of time available to these species to disperse. The fact that at present there is little evidence of any species occupying a very wide geographical range (the exceptions being Encephalartos altensteinii Lehmann/E. natalensis R.A. Dyer & I. Verdoorn, E. villosus and E. barteri Carruthers ex Miquel), as well as the absence of any marked geographical disjunctions (the exception being E. laevifolius), seems to be indicative of relatively recent speciation of the living species, which is supported by the small amount of genetic variation. Viewed on a geographical basis, certain parts of the distribution range of the genus contain groups of species with common morphological characteristics, such as strongly lobed leaflets in the Eastern Cape Province of South Africa, white wool on the emerging foliage in Zimbabwe and Mozambique, green and cylindrical stalked female cones in central Africa, successive emergence of male cones in tropical Africa, and a dwarf habit plus soapy green leaves in the tropical savanna. It is not unreasonable to consider these individual groups as closely related species. In view of the large number of species involved, the difficult accessibility in nature of many of the species, the time and expense required to collect all the data for the phylogenetic assessment, and the unfortunate fact that research funding is closely linked to frequent publications, it seems prudent to divide the genus into manageable geographically/morphologically similar portions which can be studied in succession. Any anomalies can be ironed out at the

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final assessment of the whole genus. It would, however, not be wise to accept blindly these geographical/morphological groups as phylogenetic groups and use only one or a few representatives of each group to determine relationships between them. The following groups are tentatively circumscribed and their distributions are illustrated in Fig. 6.1: ●

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Group 1: Encephalartos brevifoliolatus Vorster, E. cycadifolius (Jacquin) Lehmann, E. friderici-guilielmi Lehmann, E. ghellinckii Lemaire, E. humilis I. Verdoorn, E. laevifolius Stapf & Burtt Davy and E. lanatus Stapf & Burtt Davy. Together these species occur over a wide area in the eastern part of South Africa, in most cases favouring relatively cool and high elevations that receive frost and even snow in winter. They are readily distinguished by their narrow (almost linear) leaflets and hairy cones. They produce cones 6 months out of phase with the other species (in spring rather than in autumn), and the female cones disintegrate after 3 months instead of staying on the plants for 6–12 months or longer. In cultivation they could not be hybridized with any species outside this group. Group 2: Encephalartos arenarius R.A. Dyer, E. horridus (Jacquin) Lehmann, E. latifrons Lehmann, E. lehmannii Lehmann, E. longifolius (Jacquin) Lehmann and E. trispinosus (Hooker) R.A. Dyer. These species occur in a relatively small area in the Eastern Cape Province of South Africa, usually in dry conditions. They carry solitary cones, and several of them have markedly glaucous leaves and/or very prominently spiny-lobed leaflets. None of them has prickles on the petiole. Group 3: Encephalartos princeps R.A. Dyer. This species has a very strong vegetative likeness to E. lehmannii, but bears multiple cones and is probably not very closely related. This is borne out by Van der Bank et al.’s (2001) molecular results. Group 4: Encephalartos aplanatus Vorster, E. caffer (Thunberg) Lehmann, E. cerinus Lavranos & D.L. Goode, E. ngoyanus I. Verdoorn, E. umbeluziensis R.A. Dyer and E. villosus Lemaire. These species, loosely referred to as the ‘E. villosus group’, occur over a long distance along the eastern part of South Africa, often close to the coast. They share a non-emergent caudex, relatively few and initially erect leaves, externally rather poor sexual dimorphism of the cones and sporophyll apices drawn out into drooping and often fringed lips. Group 5: Encephalartos altensteinii Lehmann/E. natalensis R.A. Dyer & I. Verdoorn and E. transvenosus Stapf & Burtt Davy. These occur along the eastern coast, and the eastern and northern escarpment of South Africa. They share a large stature and bright green leaves, and their cones are almost indistinguishable so that they are defined in terms of their individual diagnostic foliage morphologies. Group 6: Encephalartos woodii Sander. This species, known from a single gathering in northern KwaZulu-Natal in South Africa, closely resembles

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Encephalartos delucanus E. marunguensis E. poggei E. schaijesii E. schmitzii

Encephalartos mackenziei E. macrostrobilus E. septentrionalis

Encephalartos bubalinus E. equatorialis E. hildebrandtii E. ituriensis E. kisambo E. sclavoi E. tegulaneus E. whitelockii

Encephalartos barteri Encephalartos laurentianus Encephalartos inopinus Encephalartos cupidus E. dolomiticus E. dyerianus E. eugene-maraisii E. hirsutus E. middelburgensis E. nubimontanus

Encephalartos gratus Encephalartos chimanimaniensis E. concinnus E. manikensis E. munchii E. pterogonus E. turneri

Encephalartos brevifoliolatus E. cycadifolius E. friderici-guilielmii E. ghellinckii E. humilis E. laevifolius E. lanatus

Encephalartos heenanii E. paucidentatus E. relictus Encephalartos ferox

Encephalartos altensteinii/natalensis E. transvenosus Encephalartos arenarius E. horridus E. latifrons E. lehmannii E. longifolius E. trispinosus

Encephalartos aemulans E. lebomboensis E. msinganus E. senticosus Encephalartos princeps

Encephalartos woodii Encephalartos aplanatus E. caffer E. cerinus E. ngoyanus E. umbeluziensis E. villosus

Fig. 6.1. Known geographical distribution of the genus Encephalartos in Africa, showing geographical groups of species with common characteristics.

some forms of E. natalensis. It is cryptically distinguished by its softer-textured and bright glossy green foliage, and its juvenile-type leaflets have a characteristic ovate profile and three to four conspicuous teeth near the base of the upper margin, a characteristic that is not found in any other South African species but is seen as a regular feature in a number of equatorial species such

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as E. hildebrandtii A. Braun & Bouché, E. ituriensis Bamps & Lisowski and E. kisambo Faden & Beentje. Group 7: Encephalartos aemulans Vorster, E. lebomboensis I. Verdoorn, E. msinganus Vorster and E. senticosus Vorster. These cycads, of northern KwaZulu-Natal of South Africa, vegetatively resemble the previous group and may be phylogenetically close to it, but are distinguished by their individual female cone morphologies. Encephalartos aemulans and especially E. msinganus are probably the closest to the previous group on account of their warty female cones, while E. lebomboensis and E. senticosus are more distant but closer to each other on account of their apricot-yellow female cones with short downy indumentum. Group 8: Encephalartos heenanii R.A. Dyer, E. paucidentatus Stapf & Burtt Davy and E. relictus P.J.H. Hurter. These occur on mountains surrounding Swaziland. They share corrugately raised veins on the abaxial leaflet surfaces, otherwise known only in E. latifrons. They have widely differing cones. While E. heenanii and E. relictus are vegetatively similar, E. paucidentatus has a quite different aspect. Group 9: Encephalartos cupidus R.A. Dyer, E. dolomiticus Lavranos & D.L. Goode, E. dyerianus Lavranos & D.L. Goode, E. eugene-maraisii I. Verdoorn, E. middelburgensis Vorster, E. nubimontanus P.J.H. Hurter and possibly the recentlydescribed but almost unknown E. hirsutus P.J.H. Hurter. These species occur on the northern escarpment of South Africa, mostly at relatively cool and high elevations. They share conspicuously glaucous foliage, but there are differences in leaf morphology. The female cones of E. eugene-maraisii and E. middelburgensis are very similar, as are those of E. nubimontanus, E. cupidus and E. dyerianus, while those of E. dolomiticus are quite different. Encephalartos hirsutus was very poorly described and is still virtually unknown. Group 10: Encephalartos inopinus R.A. Dyer. This occurs in the same geographical area as the previous group. It is an enigma in the genus. It has an arresting vegetative appearance quite unlike any other, with glaucous and entire falcate drooping leaflets. Being glabrous, glaucous and having smooth scale surfaces, the female cones are almost indistinguishable from those of E. dyerianus. It has not been found possible to hybridize E. inopinus with any other species. Group 11: Encephalartos chimanimaniensis R.A. Dyer & I. Verdoorn, E. concinnus R.A. Dyer & I. Verdoorn, E. manikensis (Gilliland) Gilliland, E. munchii R.A. Dyer & I. Verdoorn, E. pterogonus R.A. Dyer & I. Verdoorn and perhaps E. turneri Lavranos & D.L. Goode. These occur along the Zimbabwe–Mozambique border. They all have relatively soft foliage, leaflets reduced to spines towards the base of the leaf, distinct short whitish wool on the emerging fronds, and green and glabrous cones of which the females are ovoid. Their stems tend to have a soft texture such as is usually associated with species like those of the E. villosus group or E. ferox.

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Group 12: Encephalartos gratus Prain. This occurs in southern Malawi and adjacent Mozambique. It has soft-textured foliage like the previous group, but differs by the cones being dark salmon pink instead of green. This pigmentation is shared by only E. ferox, which is probably not closely related. On the other hand, the cylindrical female cones and successively emerging male cones of E. gratus may point to an affinity with the next group. Group 13: Encephalartos bubalinus Melville, E. equatorialis P.J.H. Hurter, E. hildebrandtii A. Braun & Bouché, E. ituriensis Bamps & Lisowski, E. kisambo Faden & Beentje, E. sclavoi De Luca, D.W. Stevenson & A. Moretti, E. tegulaneus Melville (including subsp. powysii Miringu & Beentje) and E. whitelockii P.J.H. Hurter. These cycads are distributed on both sides of the equator. They all have hard-textured leaves, and the leaflets progressively reduce to a series of prickles so that there is no clear petiole. Several of the species have three to four teeth grouped together near the base of the upper leaflet margin. The cones are green to yellow, glabrous; the female cones are cylindrical in several species but ovoid in others, with the facets smooth and the terminal facet only moderately raised. The male cones tend to emerge in succession. Encephalartos sclavoi is included here for geographical reasons; but its smaller stature, and its few cones (one to two) plus the ovoid shape of the female cone, may signify a more distant relationship to the rest of the group. Group 14: Encephalartos macrostrobilus S. Jones & Wynants, E. mackenziei L.E. Newton and E. septentrionalis Schweinfurth. It seems doubtful if any botanist has seen E. septentrionalis since Schweinfurth discovered it in the southern Sudan in 1869; consequently the identity of this species is uncertain. Plants from Moyo in Uganda are ascribed to E. septentrionalis. Encephalartos macrostrobilus was described from north-eastern Uganda, but so poorly that it is impossible to visualize the species. Plants from near Didinga in south-eastern Sudan have recently been described under the name E. mackenziei (Newton, 2002). All species in this group have leaflets reduced to prickles towards the base of the leaf, all have three to four teeth near the base of the upper leaflet margin, all have green and cylindrical female cones with a sparse and ephemeral russet-brown indumentum and all have numerous male cones emerging in succession. Except for their soft-textured leaflets, these plants are very similar to the previous group and may well belong there. Group 15: Encephalartos laurentianus De Wildeman. This is known only from a small area on the Angola–Congo border. It resembles the previous two groups by the leaflets being reduced to a series of prickles towards the base of the leaf and the male cones emerging in succession. It differs most conspicuously by its gigantic stature, its soft-textured foliage with the leaflets lacking the concentration of three to four teeth near the base of the upper margin, and the short russet-brown indumentum on the cones (a similar but sparser indumentum occurs on the group 14 species). The morphological and geographical discontinuities probably indicate a considerable evolutionary divergence from all the other species.

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Group 16: Encephalartos barteri Carruthers ex Miquel (including subsp. allochrous L.E. Newton). This is geographically well isolated, though it occurs over a wide area of Ghana, Benin and Nigeria. The plants are somewhat nondescript. The leaves are erect and straight, with leaflets soft-textured, rather narrow, and reduced to prickles towards the base of the leaf. The cones are ovoid, glabrous, and green to olive green, the female cones being sessile. This is a poorly known group. Group 17: Encephalartos delucanus Malaisse, Sclavo & Crosiers, E. poggei Ascherson, E. marunguensis Devred, E. schaijesii Malaisse, Sclavo & Crosiers and E. schmitzii Malaisse. These cycads occur in the savanna of Zambia, Tanzania, Congo and Angola on fire-prone sandy flats where there seems to be no obvious barrier against migration. They are small, almost dwarf plants. The stems are underground or shortly emergent. The leaves are deciduous during the hottest and driest part of the year, soapy glaucous green; the leaflets are entire or less commonly with a few small teeth and gradually reduced to spines towards the base of the leaf. The cones emerge glaucous green and may turn yellowish at maturity. They are rather nondescript, but the female cones are ovoid and sessile with the males shortly stalked. Morphologically and geographically they are distinct from other groups, but may be variants of one species. Group 18: Encephalartos ferox Bertolini filius. This occurs on the coast of Mozambique and the KwaZulu-Natal province of South Africa, on white beach sand immediately next to the ocean. It is morphologically very distinct, with a shortly emergent and soft textured stem, hard-textured dull green leaves and broad leaflets with teeth all around. The cones are conspicuously salmon-red. This species appears to stand apart from all others and has proved difficult to hybridize with any other species in cultivation.

Postcript The greatest danger when compiling a phylogenetic tree is to rely, for example, on cytological, chemical or molecular evidence and build a phylogeny on any single type of evidence. Such a tree cannot truly be called a phylogenetic tree but is really a cytological tree, a chemical tree or a molecular tree. Finally, it should always be remembered that a phylogenetic tree is an approximation only, based on the seemingly most logical interpretation of the available evidence, with many missing components because we have only the presently available evidence of a process that spans tens of millions of years. As such it can never be final.

References De Luca, P., Moretti, A., Sabato, S. and Siniscalco Gigliano, G. (1980) The ubiquity of cycasin in cycads. Phytochemistry 19, 2230–2231.

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Dehgan, B. and Dehgan, N.B. (1988) Comparative pollen morphology and taxonomic affinities in Cycadales. American Journal of Botany 75, 1501–1516. Donaldson, J.S., Nänni, I. and de Wet Bösenberg, J. (1995) The rôle of insects in the pollination of Encephalartos cycadifolius. In: Vorster, P. (ed.) Proceedings of the Third International Conference on Cycad Biology. Cycad Society of South Africa, Stellenbosch, South Africa, pp. 423–434. Du Rietz, G.E. (1930) The fundamental units of biological taxonomy. Svensk Botanisk Tidskrift 24, 333–427. Dyer, R.A. (1956) A new cycad from the Cape Province. Journal of South African Botany 22, 1–4. [Encephalartos arenarius.] Dyer, R.A. (1965) New species and notes on type specimens of South African Encephalartos. Journal of South African Botany 31, 111–121. [Encephalartos princeps.] Giddy, C. (1974) Cycads of South Africa. Purnell, Cape Town, South Africa, 122 pp. Goode, D. (2001) Cycads of Africa, Vol. 1. Cycads of Africa Publishers, Gallomanor, South Africa, 351 pp. Grilli Caiola, M. (1975) A light and electron microscopic study of blue-green algae growing in the coralloid roots of Encephalartos altensteinii and in culture. Phycologia 14, 25–33. Grobbelaar, N. and Marshall, J. (1993) Specificity of the cycad–cyanobiont symbiosis. In: Stevenson, D.W. and Norstog, K.J. (eds) The Biology, Structure and Systematics of the Cycadales. Proceedings of the Second International Conference on Cycad Biology. Palm & Cycad Societies of Australia Limited, Milton, Queensland, Australia, pp. 162–164. Grobbelaar, N., Scott, W.E., Hattingh, W. and Marshall, J. (1987) The identification of the coralloid root endophytes of the southern African cycads and the ability of the isolates to fix dinitrogen. South African Journal of Botany 53, 111–118. Hill, K.D. and Stanberg, L.C. (1999) Epicuticular waxes in the Cycadales, and their systematic implications. In: Chen, C.J. (ed.) Biology and Conservation of Cycads. Proceedings of the Fourth International Conference on Cycad Biology. International Academic Publishers, Beijing, China, pp. 159–174. Jones, S. and Wynants, J. (1997) Encephalartos macrostrobilus (Zamiaceae), a new cycad species from northern Uganda. Encephalartos 50, 13–16. Koeleman, A., Robbertse, P.J. and Eicker, A. (1981) Die anatomie van die pinnas van die Suid-Afrikaanse spesies van Encephalartos Lehm. Journal of South African Botany 47, 247–271. Marchant, C.J. (1968) Chromosome patterns and nuclear phenomena in the cycad families Stangeriaceae and Zamiaceae. Chromosoma 24, 100–134. Marshall, J., Grobbelaar, N., Coetzee, J. and Osborne, R. (1989a) Pollen morphology of the Cycadales with special reference to the Encephalartos species. Pollen et Spores 31, 229–249. Marshall, J., Huang, T.C. and Grobbelaar, N. (1989b) Comparative morphological and physiological studies on cyanobionts of Encephalartos transvenosus. South African Journal of Botany 55, 574–580. Mogford, D.J. (1981) Chromosome studies in the southern African flora: 1–3. Journal of South African Botany 47, 2–6. Moretti, A. (1990) Cytotaxonomy of cycads. In: Stevenson, D.W. (ed.) The Biology, Structure, and Systematics of the Cycadales. Proceedings of the Symposium CYCAD 87. Memoirs of the New York Botanical Garden 57, pp. 114–122. Moretti, A., Sabato, S. and Siniscalco Gigliano, G. (1983) Taxonomic significance of methylazoxymethanol glycosides in the cycads. Phytochemistry 22, 115–118.

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Newton, L.E. (2002) A new species of Encephalartos (Zamiaceae) in Sudan. Botanical Journal of the Linnean Society 140, 187–192. [Encephalartos mackenziei.] Norstog, K. (1987) Cycads and the origin of insect pollination. American Scientist 75, 270–279. Norstog, K.J. and Nicholls, T.J. (1997) The Biology of the Cycads. Cornell University Press, Ithaca, New York, 363 pp. Oberprieler, R.G. (1995) The weevils (Coleoptera: Curculionoidea) associated with cycads. 2. Host specificity and implications for cycad taxonomy. In: Vorster, P. (ed.) Proceedings of the Third International Conference on Cycad Biology. Cycad Society of South Africa, Stellenbosch, South Africa, pp. 335–365. Osborne, R. and Stevens, J.F. (1996) Epicuticular waxes and glaucousness of Encephalartos leaves. Phytochemistry 42, 1335–1339. Osborne, R., Salatino, M.L.F. and Salatino, A. (1989) Alkanes of foliar epicuticular waxes of the genus Encephalartos. Phytochemistry 28, 3027–3030. Pate, J.S., Lindblad, P. and Atkins, C.A. (1988) Pathways of assimilation and transfer of fixed nitrogen in coralloid roots of cycad–Nostoc symbiosis. Planta 176, 461–471. Pellmyr, O., Tang W., Groth, I., Bergström, G. and Thien, L.B. (1991) Cycad cone and Angiosperm floral volatiles: inferences for the evolution of insect pollination. Biochemical Systematics and Ecology 19, 623–627. Robbertse, P.J., Vorster, P. and Van der Westhuizen, S. (1988a) Encephalartos graniticolus (Zamiaceae): a new species from the north-eastern Transvaal. South African Journal of Botany 54, 363–366. Robbertse, P.J., Vorster, P. and Van der Westhuizen, S. (1988b) Encephalartos verrucosus (Zamiaceae): a new species from the north-eastern Transvaal. South African Journal of Botany 54, 487–490. Sharma, I.K., Jones, D.L., Forster, P.I. and Young, A.G. (1998) The extent and structure of genetic variation in the Macrozamia pauli–guilielmi complex (Zamiaceae). Biochemical Systematics and Ecology 26, 45–54. Sharma, I.K., Jones, D.L., Forster, P.I. and Young, A.G. (1999) Low isozymic differentiation among five species of the Macrozamia heteromera group (Zamiaceae). Biochemical Systematics and Ecology 27, 67–77. Spreeth, A.D. and Vorster, P. (1995) Anatomical studies on the leaflets of glaucous-leaved Encephalartos species in South Africa [abstract]. In: Vorster, P. (ed.) Proceedings of the Third International Conference on Cycad Biology. Cycad Society of South Africa, Stellenbosch, South Africa, p. 263. Stephens, D.C. and Stephen, A.M. (1988) Exudates from Encephalartos cones as chemical taxonomic markers. South African Journal of Science 84, 263–266. Stevenson, D.W. (1981) Observations on ptyxis, phenology, and trichomes in the cycadales and their systematic implications. American Journal of Botany 68, 1104–1114. Tang, W. (1993) Heat and odour production in cycad cones and their role in insect pollination. In: Stevenson, D.W. and Norstog, K.J. (eds) The Biology, Structure, and Systematics of the Cycadales. Proceedings of the Second International Conference on Cycad Biology. Palm & Cycad Societies of Australia Limited, Milton, Queensland, Australia, pp. 140–147. Van der Bank, F.H., Vorster, P. and Van der Bank, M. (1998) Phylogenetic relationships, based on allozyme data, between six cycad taxa indigenous to South Africa. South African Journal of Botany 64, 182–188. Van der Bank, H., Wink, M., Vorster, P., Treutlein, J., Brand, L., Van der Bank, M. and Hurter, J. (2001) Allozyme and DNA sequence comparisons of nine species of Encephalartos (Zamiaceae). Biochemical Systematics and Ecology 29, 241–266.

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Vorster, P. (1990) Encephalartos aemulans (Zamiaceae), a new species from northern Natal. South African Journal of Botany 56, 239–243. Vorster, P. (1993) Taxonomy of Encephalartos: taxonomically useful external characteristics. In: Stevenson, D.W. and Norstog, K.J. (eds) The Biology, Structure, and Systematics of the Cycadales. Proceedings of the Second International Conference on Cycad Biology. Palm & Cycad Societies of Australia Limited, Milton, Queensland, Australia, pp. 294–299. Vorster, P. (1995) The identity of Encephalartos lebomboensis. In: Vorster, P. (ed.) Proceedings of the Third International Conference on Cycad Biology. Cycad Society of South Africa, Stellenbosch, South Africa, pp. 245–254. Vorster, P. (1996a) Encephalartos msinganus (Zamiaceae): a new species from KwaZulu-Natal. South African Journal of Botany 62, 67–70. Vorster, P. (1996b) Encephalartos venetus (Zamiaceae): a new species from the Northern Province. South African Journal of Botany 62, 71–75. Vorster, P. (1996c) Encephalartos senticosus (Zamiaceae): a new species from northern KwaZulu-Natal and Swaziland. South African Journal of Botany 62, 76–79. Vorster, P. and Heibloem, P. (1995) Encephalartos imbricans (Zamiaceae): a new species from Uganda. Novon 5, 388–394. Vorster, P. and Oberprieler, R. (1999) Entomological evidence for and against taxonomical decisions in Encephalartos. In: Chen, C.J. (ed.) Biology and Conservation of Cycads. Proceedings of the Fourth International Conference on Cycad Biology. International Academic Publishers, Beijing, China, pp. 198–207. Vovides, A.P. (1991) Vesicular–arbuscular mycorrhiza in Dioon edule Lindl. (Zamiaceae) in its natural habitat in central Veracruz, Mexico. [Abstract of paper presented at 1991 Annual meeting of the Botanical Society of America.] American Journal of Botany 78 (6), supplement, Ecological Section, p. 76. Walters, T.W. and Decker-Walters, D.S. (1991) Patterns of allozyme diversity in the West Indies cycad Zamia pumila (Zamiaceae). American Journal of Botany 78, 436–445.

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Classification Concepts in Macrozamia (Zamiaceae) from Eastern Australia

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Paul I. Forster Queensland Herbarium, Environmental Protection Agency, Brisbane Botanic Gardens, Toowong, Queensland, Australia

Abstract The genus Macrozamia currently comprises at least 40 species and is endemic to Australia. Thirty-seven of these species occur in eastern Australia – in Queensland and New South Wales. Species concepts in the genus are discussed and useful character states outlined. Descriptive examples are included and suggestions for identification tools made. Future directions for research are outlined.

Introduction The genus Macrozamia Miquel is one of seven extant genera in the cycad family Zamiaceae. Species of Macrozamia are endemic to Australia with 40 (Hill et al., Appendix 1 this volume) or 41 recognized species (Table 7.1). The main concentration of species is in eastern Australia, with at least 37 species (Hill and Osborne, 2001; Jones et al., 2001; Forster, 2002). A single species, M. macdonnellii (F. Mueller ex Miquel) A. de Candolle, is present in central Australia near Alice Springs and three species are currently recognized from south-west Western Australia. The first modern account of Macrozamia was by Johnson (1959) but the extremely broad concept of taxa employed therein has now been discarded. Johnson also regarded many geographically disjunct and incomplete specimens as representing hybrids, although no scientific evidence was ever presented to support this pronouncement. Juvenile foliage of many species of Macrozamia can be quite different to that found on mature individuals and misidentification of ©CAB International 2004. Cycad Classification: Concepts and Recommendations (eds T. Walters and R. Osborne)

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Table 7.1. Species recognized in Macrozamia and their general distribution.

Species epithet and author

Australian state of distribution

Macrozamia section Macrozamia M. cardiacensis P.I. Forster & D.L. Jones M. communis L.A.S. Johnson M. diplomera (F. Mueller) L.A.S. Johnson M. douglasii W. Hill ex F.M. Bailey M. dyeri (F. Mueller) C.A. Gardner M. fraseri Miquel M. johnsonii D.L. Jones & K.D. Hill M. longispina P.I. Forster & D.L. Jones M. macdonnellii (F. Mueller ex Miquel) A. de Candolle M. macleayi Miquel M. miquelii (F. Mueller) A. de Candolle M. montana K.D. Hill M. moorei F. Mueller M. mountperriensis F.M. Bailey M. riedlei (Gaudichaud) C.A. Gardner M. reducta K.D. Hill & D.L. Jones M. serpentina D.L. Jones & P.I. Forster

Queensland New South Wales New South Wales Queensland Western Australia Western Australia New South Wales Queensland Northern Territory Queensland Queensland New South Wales Queensland Queensland Western Australia New South Wales Queensland

Macrozamia section Parazamia M. concinna D.L. Jones M. conferta D.L. Jones & P.I. Forster M. cranei D.L. Jones & P.I. Forster M. crassifolia P.I. Forster & D.L. Jones M. elegans K.D. Hill & D.L. Jones M. fawcettii C. Moore M. fearnsidei D.L. Jones M. flexuosa C. Moore M. glaucophylla D.L. Jones M. heteromera C. Moore M. humilis D.L. Jones M. lomandroides D.L. Jones M. lucida L.A.S. Johnson M. M. M. M. M. M. M. M. M. M. M.

machinii P.I. Forster & D.L. Jones occidua D.L. Jones & P.I. Forster parcifolia P.I. Forster & D.L. Jones pauli-guilielmi W. Hill & F. Mueller platyrhachis F.M. Bailey plurinervia (L.A.S. Johnson) D.L. Jones polymorpha D.L. Jones secunda C. Moore spiralis (Salisbury) Miquel stenomera L.A.S. Johnson viridis D.L. Jones & P.I. Forster

New South Wales Queensland Queensland Queensland New South Wales New South Wales Queensland New South Wales New South Wales New South Wales New South Wales Queensland Queensland, New South Wales Queensland Queensland Queensland Queensland Queensland New South Wales New South Wales New South Wales New South Wales New South Wales Queensland, New South Wales

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juveniles of some species (e.g. M. johnsonii D.L. Jones & K.D. Hill – then known as the New South Wales form of M. moorei F. Mueller – as M. lucida L.A.S. Johnson) also aided and abetted confusion when using his account. Revision of the genus Macrozamia was commenced in the early 1990s by D.L. Jones and the current author, using a variety of methods, but primarily those of macromorphology. Accounts of new taxa, species complexes or nomenclature of specific epithets have been published sequentially (Jones, 1991; Forster and Jones, 1992; Jones and Hill, 1992; Jones and Forster, 1994; Forster and Jones, 1998; Forster, 1999a,b; Jones et al., 2001), but no detailed monograph has yet been published. A Flora of Australia compilation of the majority of species was published by Hill (1998) and a populist account derived directly from this source by Hill and Osborne (2001). It is likely that a small number of additional species (to those in Table 7.1) will be recognized once the ongoing revision is finalized. These will be primarily from northern New South Wales and south-western Western Australia.

Species Concepts At present the genus is divided into two sections: Macrozamia section Macrozamia and M. section Parazamia (Miquel) Miquel. These two sections are primarily distinguished by the presence or absence of mucilage canals in the leaflets, although the presence of this character has not been determined for most species now recognized and the proposed sectional classification of at least one species (M. lucida) remains suspect. Species in Macrozamia have been defined in terms of morphological discontinuity in character states and are similar to those recognized in most vascular plant groups. All of the recognized species of Macrozamia differ from one another in at least two character states. Some of the species are highly distinctive and unlikely to be confused with any others [e.g. M. macdonnellii (F. Mueller ex Miquel) A. de Candolle, M. platyrhachis F.M. Bailey]. Others form part of complexes of taxa of similar appearance and therein potential problems lie with how many species are to be recognized. Once the individual taxa have been defined, it is necessary to allocate them a taxonomic rank, with decisions having to be made as to whether the use of infraspecific taxa is justified. The only workers to have applied infraspecific ranks in the genus Macrozamia have been Schuster (1932) and Johnson (1959), both utilizing subspecies. While the work of Schuster has been largely discounted, the system proposed by Johnson was recognized for many years, even though he did not define what was meant by a species or a subspecies. All of the subspecific taxa covered by Johnson are now recognized at the species level. This approach of using infraspecific ranks is fraught with supposition and is also unpopular with the end-user. If there is morphological discontinuity in a couple of characters then little is gained in having the classification reflect a hypothetical phylogeny by using infraspecific

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ranks. Inferred relationships between the taxa can be discussed when dealing with individual species complexes. Some species complexes in Macrozamia section Parazamia comprise very closely related taxa [e.g. M. conferta D.L. Jones & P.I. Forster, M. cranei D.L. Jones & P.I. Forster, M. machinii P.I. Forster & D.L. Jones, M. plurinervia (L.A.S. Johnson) D.L. Jones (the latter two species are considered synonymous by Hill et al., Appendix 1 this volume, but this view is not supported by the author), M. occidua D.L. Jones & P.I. Forster, M. viridis D.L. Jones & P.I. Forster], disjunct into adjacent geographical areas and on dissimilar geologies. There is relatively low genetic dissimilarity among these taxa based on isozyme techniques (e.g. Sharma et al., 1999b). Because of the inherent beetle-pollination system in some species of Macrozamia and the apparent poor dispersal of the beetles between populations, disjunct populations are unlikely to have any recent genetic integration. Their low genetic diversity and lack of difference (at least in the limited isozyme systems studied) within or between populations tends to indicate that speciation is relatively recent and that inbreeding within populations has occurred for some time (Sharma et al., 1998, 1999b). A similar situation seems to be present in some complexes of Encephalartos Lehmann in southern Africa (Van der Bank et al., 1998, 2001), and no proposal to recognize those particular taxa as subspecies of a single species has appeared, nor is it likely to be a popular option. In comparison, some taxa of Macrozamia section Macrozamia are readily separated by isozymes (Sharma et al., 1999a; Jones et al., 2001). Ongoing investigations into insect pollination systems in Macrozamia by Irene Terry of the University of Utah may well shed further light on the sectional relationships of species (Mound and Terry, 2001; Terry, 2001). Species in M. section Parazamia appear to be purely beetle-pollinated by species of Tranes, whereas those in M. section Macrozamia are pollinated either by thrips (Cycadothrips spp.), beetles (Tranes spp.) or a combination of the two. These differing pollination systems are associated with marked differences in cone volatile fragrances and it is likely that these will prove to be of taxonomic significance. An attempt to further subdivide the taxa within Macrozamia section Parazamia into informal groups has been undertaken by Hill (1998) and Hill and Osborne (2001), but these hypotheses require validation using a range of anatomical and molecular techniques as some of the groups appear artificial. By contrast, the species in M. section Macrozamia can be easily allocated to four groups: ●

●

●

Group 1: Macrozamia dyeri (F. Mueller) C.A. Gardner, M. fraseri Miquel, M. riedlei (Gaudichaud) C.A. Gardner. Restricted to Western Australia. Large trunked cycads, leaflets amphistomatic, rachis with clear base. Group 2: Macrozamia johnsonii D.L. Jones & K.D. Hill, M. macdonnellii (F. Mueller ex Miquel) A. de Candolle, M. moorei F. Mueller. Central and Eastern Australia. Large trunked cycads, leaflets amphistomatic, rachis with pinnacanths to base. Group 3: Macrozamia communis L.A.S. Johnson, M. elegans K.D. Hill & D.L. Jones, M. montana K.D. Hill, M. reducta K.D. Hill &

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D.L. Jones. Eastern Australia, in New South Wales. Medium sized cycads with short or minimal trunk development, leaflets hypostomatic, broad-based spines on the female sporophylls (5–12 mm wide). Group 4: Macrozamia cardiacensis P.I. Forster & D.L. Jones, M. douglasii W. Hill ex F.M. Bailey, M. longispina P.I. Forster & D.L. Jones, M. macleayi Miquel, M. miquelii (F. Mueller) A. de Candolle, M. mountperriensis F.M. Bailey, M. serpentina D.L. Jones & P.I. Forster. Eastern Australia, in Queensland. Medium to large sized cycads with short or minimal trunk development, leaflets hypostomatic, narrow-based spines on the female sporophylls (2–5 mm wide).

As a result of the recent detailed account of the Macrozamia miquelii complex (Jones et al., 2001) and an earlier account of M. section Parazamia in Queensland (Jones and Forster, 1994), further discussion of approaches to cycad classification and character state definition will be undertaken mainly using examples from these groups with which the author is most familiar.

Approaches to Classification Any proposed classification has to be user-friendly. It is of little value if the diagnostic characters used are so esoteric or difficult to observe that only a specialist can utilize them. This is perhaps even more relevant with plants such as cycads. These plants are of interest to people for a number of reasons, mainly economic (e.g. livestock poisoning), horticultural, or legalistic (conservation legislation). It is therefore essential that a range of end-users can identify plant material, given that basic specimen requirements are applied. At the Queensland Herbarium (BRI) there is a constant array of queries concerning the identity of native cycads. These enquiries cover the gamut from poisons queries to harvesting or land-clearing permits, horticultural identifications and nature conservation act enforcement. In this respect the Herbarium is an integral part of the Queensland Environmental Protection Agency and its efforts to document the floral biodiversity of the state and to ensure its long-term protection in a sustainable manner. Staff at the Herbarium decide which species are to be recognized for the state, and may also propose conservation ratings for species using the IUCN categories. After external ratification (by a non-government committee), these conservation ratings are then included in the schedules attached to the Queensland Nature Conservation Act and applied federally by Environment Australia for the national Rare and Threatened list. With so much interest in the native cycads, the requirement for modern accounts of all the species has been critical, with concurrent adaptation and updating of protective legislation. It has been particularly important to resolve some of the more difficult species complexes, as conservation decisions based on ‘omnibus’ species will not reflect the genetic diversity present. The approach to revision of the genus Macrozamia has been both field- and laboratory-based. Considerable effort was undertaken in fieldwork to determine

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the geographical range of taxa, to assess the full range of morphological variation present, and to create durable and informative herbarium collections. It has often been difficult to obtain complete material of these dioecious plants that reproduce irregularly and repeated visits to some, often remote, localities has been necessary. It was realized early in the study that this field-based approach to elucidation of the various taxonomic complexes was essential. Plants of Macrozamia (or any cycad for that matter) have an abundance of measurable characters; however, these are not accurately determined merely from the material that ends up preserved in herbaria. An extensive checklist of character states in M. section Parazamia was developed by Jones for use in the field. Up to 20 mature plants were used to capture the data used in the descriptions published by Jones and Forster (1994). An abridged version of this checklist follows: 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23. 24. 25.

Locality Date Collection number Stem branching Trunk emergence Colour and density of trunk wool Petiole wool Petiole cross-section Leaf number and orientation Rachis twisting Leaflet colour and glaucousness Leaflet twist and base Leaflet orientation Leaflet crowding Leaflet spacing along rachis Stomate distribution Callus colour Lower leaflets form Juvenile leaf colour Juvenile leaf shape Venation prominence on upper leaflet surface Venation prominence on lower leaflet surface Number of male cones/plant Number of female cones/plant Cone colour at maturity.

Shrinkage occurs of both reproductive material (cones or seeds) and foliage (leaflet dimensions) during the drying process used in producing herbarium vouchers, hence dimensions were checked on the subsequent dried material and descriptions adjusted accordingly to reflect this. Many end-users are interested in the ‘diagnostic’ characters in identification keys. The following are the key diagnostic characters used in the identification key for Macrozamia section Parazamia from Queensland (Jones and Forster, 1994):

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Leaf orientation/disposition Leaf rachis curvature Leaflet texture Leaflet shape in cross-section Leaflet orientation to rachis Leaflet colour (wax cover often important) Leaflet size Cone colour (glaucous or green) Microsporangiate cone spination.

In this particular identification key, nearly all use of fertile characters was avoided, with a range of leaf characters being more useful. With respect to the revision of the Macrozamia miquelii complex, we tried to use characters that were readily observable, although it eventuated that a combination of vegetative (from mature plant foliage) and reproductive characters was necessary to separate species successfully. The diagnostic characters used in the key to species (Jones et al., 2001) were as follows: 1. 2. 3. 4. 5. 6. 7. 8. 9.

Leaflet texture and appearance (e.g. thin/glossy) Leaflet number Leaflet width Leaflets reduced/not reduced to pinnacanths at base of leaf Female cone shape (ovoid or cylindrical to barrel-shaped) Female cone size Megasporophyll spination Male cone size Microsporophyll size.

For the key to work, one would need ideally to have both male and female cones and foliage of the plant. Given that a detailed revision now exists, material that lacks some of this information can probably still be identified by locality inference. This key requirement for fertile material is not at all unusual in the process of plant identification and should not be considered an impediment. A cursory examination of identification keys for species in other genera of cycads (e.g. Ceratozamia Brongniart, Cycas Linnaeus, Dioon Lindley, Encephalartos) revealed that the following characters were commonly used: 1. Stem development (Giddy, 1984; Hill, 1996; Wang, 1996) 2. Stem apex wooliness (Giddy, 1984; Wang, 1996) 3. Cataphyll form (Hill, 1996; Wang, 1996) 4. Cataphyll indumentum form and colour (Hill, 1996) 5. Hypodermis development (Hill, 1996) 6. Leaf orientation (De Luca and Sabato, 1979; Giddy, 1984; Hill, 1996) 7. Leaflet size (De Luca and Sabato, 1979; Giddy, 1984; Vovides et al., 1993; Hill, 1996; Wang, 1996) 8. Leaflet orientation (Giddy, 1984; Hill, 1996; Wang, 1996) 9. Leaflet texture (Giddy, 1984; Wang, 1996)

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10. Leaflet colour (Giddy, 1984; Vovides et al., 1993; Hill, 1996) 11. Leaflet indumentum (Hill, 1996) 12. Leaflet lobing or division (De Luca and Sabato, 1979; Giddy, 1984; Wang, 1996) 13. Leaflets reduced to pinnacanths or not (Giddy, 1984; Hill, 1996) 14. Leaflet disposition (i.e. overlapping or not) (Giddy, 1984; Hill, 1996) 15. Leaflet number (Hill, 1996; Wang, 1996) 16. Disposition of stomata in leaflets (Hill, 1996) 17. Leaflet margin flat, recurved or revolute (Hill, 1996; Wang, 1996) 18. Cone colour (Giddy, 1984; Vovides et al., 1993) 19. Megasporophyll spination (Hill, 1996; Wang, 1996) 20. Megasporangiate cone size (Vovides et al., 1993) 21. Microsporangiate cone shape (Hill, 1996) 22. Microsporangiate cone size (Hill,1996; Wang, 1996) 23. Seed size (Wang, 1996) 24. Seed colour (Giddy, 1984; Wang, 1996) 25. Ovule/seed indumentum (Wang, 1996). It is obvious from the above that most workers use similar morphological characters to distinguish cycad species. Irrespective of the most important diagnostic characters, it is still essential to provide a detailed morphological description. The following example (from Jones et al., 2001) is considered most appropriate for species of Macrozamia. Any revision of a group of cycads (or any plant for that matter) should provide similar detailed descriptions and identification aids such as keys or discussion of important features, preferably concentrating on vegetative characters.

Macrozamia macleayi Miquel Caudex usually subterranean, occasionally emergent, erect, columnar or barrel-shaped, to 35 cm tall and 30 cm diameter, unbranched. Young leaves light green. Mature leaves elliptic-lanceolate in outline, 0.5–2 m long, obliquely erect to spreading, dark green, glossy, flat in cross-section, arching in profile, 6–50 in a moderately dense crown; expanded leaf base 8–12 cm × 2.5–3.5 cm, covered with grey-brown, soft wool; petiole (including the woolly expanded base) 10–30 cm long, 0.8–1.2 cm wide at the first leaflet, greenish, flat adaxially, convex and angular abaxially; rachis straight, or slightly twisted, pale green, the cross-section similar to that of the petiole; leaflets 80–160, inserted at about 40° to the rachis, widely spreading, moderately crowded, distal leaflets densely packed, proximal leaflets becoming more widely spaced, narrowly linear-lanceolate, 15–50 cm × 6–9 mm, flat, thin-textured, hypostomatic, dark green and glossy adaxially, slightly paler beneath, contracted proximally to a whitish callous base, margins entire, tapered to a pungent apex; lower leaflets gradually reduced to 8–28 pairs of

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rigid pinnacanths. Male cones 1–5, cylindrical, 15–20 cm × 3.8–6.5 cm, straight or curved with age, green; peduncle 15–29 cm × 1.5–2 cm, elliptical to round in cross-section; microsporophylls broadly cuneate, 1.5–2.5 cm × 1–1.5 cm, with an erect, apical spine 0.5–1.5 cm long. Female cones 1 or 2, cylindrical to barrel-shaped, 19–30 cm × 7–10 cm, green; peduncle 15–41 cm × 2–3 cm, elliptical in cross-section, furrowed; megasporophylls broadly wedge-shaped, 1.5–2.5 cm × 3–3.5 cm, with an erect apical spine 0.5–4.5 cm long, the distal sporophylls with spines 2.5–4.5 cm long. Seeds oblong to obovoid, 2.5–3.5 cm × 1.5–2.5 cm, the sarcotesta orange to red.

Future Directions While unambiguous diagnostic morphological characters are the backbone of any classification, other methods such as isozymes, chromosomes (cf. Osborne, 2001), anatomy and, most importantly, DNA data have yet to be extensively investigated in Macrozamia. Incidental observations also support further study of seeds and seedling form, cone structure, and megasporophyll and microsporophyll form. The descriptive phase of Macrozamia systematics is now nearly complete. The next steps should be in determining the phylogeny of related species and overhauling the infrageneric classification of the genus based on a range of characters.

Acknowledgements I thank Peter Bostock and Irene Terry for commenting on the manuscript.

References De Luca, P. and Sabato, S. (1979) Dioon califanoi (Zamiaceae), a new species from Mexico. Brittonia 31, 170–173. Forster, P.I. (1999a) Proposal to conserve the name Encephalartos miquelii (Zamiaceae) with a conserved type. Taxon 48, 569–570. Forster, P.I. (1999b) Typification and application of the name Macrozamia macleayi Miq. (Zamiaceae). Austrobaileya 5, 577. Forster, P.I. (2002) Plantae – Conifers and allies. In: Henderson, R.J.F. (ed.) Names and Distribution of Queensland Plants, Algae and Lichens. Environmental Protection Agency, Brisbane, Australia, pp. 201–202. Forster, P.I. and Jones, D.L. (1992) Neotypification of Macrozamia mountperriensis (Zamiaceae) with notes on its distribution. Telopea 5, 289–290. Forster, P.I. and Jones, D.L. (1998) Macrozamia cardiacensis sp. nov., M. longispina sp. nov. In: McCarthy, P. (ed.) Flora of Australia, Vol. 48. CSIRO Publishing, Melbourne, Australia, p. 717. Giddy, C. (1984) Cycads of South Africa, 2nd edn. C. Struik Publishers, Cape Town, South Africa, 112 pp.

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Hill, K.D. (1996) A taxonomic revision of the genus Cycas (Cycadaceae) in Australia. Telopea 7, 1–64. Hill, K.D. (1998) Cycadophyta. In: McCarthy, P. (ed.) Flora of Australia, Vol. 48. CSIRO Publishing, Melbourne, Australia, pp. 597–661. Hill, K.D. and Osborne, R. (2001) Cycads of Australia. Kangaroo Press, Sydney, Australia, 116 pp. Johnson, L.A.S. (1959) The families of cycads and the Zamiaceae of Australia. Proceedings of the Linnean Society of New South Wales 84, 64–117. Jones, D.L. (1991) Notes on Macrozamia (Zamiaceae) in Queensland with the description of two new species in section Parazamia (Miq.) Miq. Austrobaileya 3, 481–487. [Macrozamia fearnsidei, M. lomandroides.] Jones, D.L. and Forster, P.I. (1994) Seven new species of Macrozamia section Parazamia (Miq.) Miq. (Zamiaceae section Parazamia) from Queensland. Austrobaileya 4, 269–288. [Macrozamia conferta, M. cranei, M. crassifolia, M. machinii, M. occidua, M. parcifolia, M. viridis.] Jones, D.L. and Hill, K.D. (1992) Macrozamia johnsonii, a new species of Macrozamia section Macrozamia (Zamiaceae) from northern New South Wales. Telopea 5, 31–34. Jones, D.L., Forster, P.I. and Sharma, I.K. (2001) Revision of the Macrozamia miquelii (F. Muell.) A. DC. (Zamiaceae section Macrozamia) group. Austrobaileya 6, 67–94. Mound, L.A. and Terry, I. (2001) Thrips pollination of the central Australian cycad, Macrozamia macdonnellii (Cycadales). International Journal of Plant Sciences 162, 147–154. Osborne, R. (2001) New research initiative in Macrozamia. Palms & Cycads No. 72, 14–15. Schuster, J. (1932) Cycadaceae. In: Engler, A. (ed.) Das Pflanzenreich, Fascicle 99, Vol. 4, Part 1, pp. 1–168. Sharma, I.K., Jones, D.L., Forster, P.I. and Young, A.G. (1998) The extent and structure of genetic variation in the Macrozamia pauli–guilielmi complex (Zamiaceae). Biochemical Systematics and Ecology 26, 45–54. Sharma, I.K., Jones, D.L. and Forster, P.I. (1999a) Contribution of isozymic analysis in differentiating Macrozamia moorei D.L. Jones and K.D. Hill from M. johnsonii F. Muell. (Zamiaceae). Austrobaileya 5, 363–365. Sharma, I.K., Jones, D.L., Forster, P.I. and Young, A.G. (1999b) Low isozymic differentiation among five species of the Macrozamia heteromera group (Zamiaceae). Biochemical Systematics and Ecology 27, 67–77. Terry, I. (2001) Thrips and weevils as dual, specialist pollinators of the Australian cycad Macrozamia communis (Zamiaceae). International Journal of Plant Sciences 162, 1293–1305. Van Der Bank, F.H., Vorster, P. and Van Der Bank, M. (1998) Phylogenetic relationships, based on allozyme data, between six cycad taxa indigenous to South Africa. South African Journal of Botany 64, 182–188. Van Der Bank, F.H., Wink, M., Vorster, P., Treutlein, J., Brand, L., Van Der Bank, M. and Hurter, J. (2001) Allozyme and DNA sequence comparisons of nine species of Encephalartos (Zamiaceae). Biochemical Systematics and Ecology 29, 241–266. Vovides, A.P., Vázquez Torres, M., Schutzman, B. and Iglesias, C.G. (1993) A new species of Ceratozamia (Zamiaceae) from Querétaro and Hidalgo, Mexico. Novon 3, 502–506. [Ceratozamia sabatoi.] Wang, D.Y. (1996) Taxonomy of Cycas in China. In: Wang, F. and Liang, H. (eds) Cycads in China. Guangdong Science and Technology Press, Guangzhou, China, pp. 33–142.

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Loran M. Whitelock 4524 Toland Way, Los Angeles, California, USA

Abstract General cycad taxonomy is reviewed, along with the problems associated with separating species using morphology, genetics and laboratory procedures. The past and present taxonomy of Ceratozamia is reviewed and discussed. Morphological similarities and, more importantly, differences between Ceratozamia species and forms are listed and discussed with a view to using them as criteria in the separation of new taxa. Suggestions are made for criteria to be used in the investigation and documentation of putative new species.

Cycad Taxonomy At the present time there seems to be little disagreement about the separation of the 11 cycad genera, with the possible exception of the small genus, Chigua D.W. Stevenson. The genera are separated on the basis of clear diagnostic features, which leaves little room for argument as to their status. The same cannot be said for the separation and description of taxa at the infrageneric level. At this level there has historically been a great deal of disagreement, caused by the often minor differences between taxa. Taxonomists hold differing concepts as to how the delimitation of new species should be approached. At present there are no guidelines as to how substantial the separation between species should be, and this has caused inconsistencies from one species description to another. It is generally accepted that taxonomic classification should reflect the results of evolution. However, the meagre fossil evidence relating to the cycads generally ©CAB International 2004. Cycad Classification: Concepts and Recommendations (eds T. Walters and R. Osborne)

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produces more questions than answers. If this evolutionary train of thought is followed, the conclusion is that the basic difference between species should be one of genetics, but proving genetic differences is not an easy task. Generally, the taxonomy of cycad species has been based on morphology. Johnson (1959) considered a species to be a population or group of plants that was effectively isolated in nature ‘by any means’ so that they were not able to interbreed with other related but genotypically and phenotypically different populations. These vicariants (generally believed to be separated by past geological or climatic events) gradually evolved into new species because of isolation, and often the subsequent change in habitat. This theory works well with cycads because of their rather inefficient means of dispersal and the fact that most cycad species are found as small relic populations. The inability of Ceratozamia Brongniart species to be widely dispersed results in the genus being restricted to small populations that are not able to interbreed with other neighbouring populations. This genetic isolation occurring over a period of thousands, or millions, of years can result in the establishment of genetically distinct populations, or species. The logical way to validate a possible new species is proving how genetically similar it is to another related species. Hybridizing the possible new species with its closest relative and then crossing the resulting offspring to observe the amount of variation in genetically controlled characters appearing in the second generation could do this. With annuals this would not be a difficult task. However, cycads take a number of years to reach sexual maturity. The taxonomist might die of old age before being able to assess a new species in this manner! In recent times considerable laboratory work has been done on the cytological, chemical and molecular characteristics of both the genera and species of cycads. Investigations into cycad chromosomes have produced results that provide useful information about cycad interrelationships but this work has not revealed much about evolutionary trends in cycad taxonomy, especially at a species level. Chromosome numbers in most cycad genera agree in all of their species with the exception of Zamia Linnaeus, which has some divergent karyotypes that have led investigators to believe that Zamia is evolving more rapidly than the other genera (Norstog, 1980, 1981; Moretti et al., 1991; Vovides and Olivares, 1996). Recent studies in chloroplast DNA (Caputo et al., 1991; De Luca et al., 1995) have enabled researchers to estimate evolutionary distances between various plant taxa but it has not been particularly helpful in the separation of species. Other researchers have studied cycasin and macrozamin (Moretti et al., 1981, 1983), which tend to reflect certain evolutionary relationships, but once again the results are not applicable for separating species. Cuticular waxes of cycads have been studied (Osborne et al., 1989) and the findings suggest that these waxes may provide sufficient resolution for the separation of genera and species. Although these tests provide useful information to the taxonomists in making their determinations, at this time they merely indicate, but do not prove, the separation of species. An important consideration is that all of these tests require laboratory facilities and trained personnel that are not always available to the

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taxonomist.

Taxonomic History of Ceratozamia The taxonomic history of Ceratozamia and its 21 species has taken 156 years to reach its present status. Adolphe Theodore Brongniart (1846) described Ceratozamia and its type species C. mexicana Brongniart from cultivated material in Paris, France. The following 10 years produced four more species that are still valid: C. robusta Miquel (1848), C. latifolia Miquel (1848), C. miqueliana H. Wendland (1854) and C. kuesteriana Regel (1857). Ceratozamia fusco-viridis D. Moore was described in 1878. The next taxonomic change to Ceratozamia did not take place for another 61 years, when C. matudae Lundell (1939) was described. Another 24 years were to pass before the description of C. zaragozae MedellinLeal (1963). Renewed interest in the genus Ceratozamia began in 1979 with the description of C. hildae G.P. Landry & M.C. Wilson (1979). The period from 1979 to the present has produced 12 additional species, more than doubling the number of species that were described in the previous 133 years. These new species included C. norstogii D.W. Stevenson (1982), C. microstrobila Vovides & J.D. Rees (1983), C. euryphyllidia Vázquez Torres, Sabato & D.W. Stevenson (Stevenson et al., 1986), C. sabatoi Vovides, Vázquez Torres, Schutzman & Iglesias (1993), C. whitelockiana Chemnick & T.J. Gregory (1995), C. mixeorum Chemnick, T.J. Gregory & Salas-Morales (1997), C. morettii Vázquez Torres & Vovides (1998), C. alvarezii Pérez-Farrera, Vovides & Iglesias (1999), C. mirandae Vovides, PérezFarrera & Iglesias (2001), C. zoquorum Pérez-Farrera, Vovides & Iglesias (2001), C. huastecorum S. Avendaño, Vovides and Castillo-Campos (2003) and C. sp. “becerrae” (A.P. Vovides, 2003 in review). There is little doubt that Ceratozamia will have additional taxa described over the next few years. This will be the result of renewed interest in the genus as well as increased field studies by a number of botanists and botanical organizations. Foremost among the botanists investigating Ceratozamia are Jeffrey Chemnick, Timothy Gregory, Miguel A. Pérez-Farrera, Silvia SalasMorales, Mario Vázquez Torres and Andrew Vovides. Due to the efforts of these botanists we can expect to see Ceratozamia begin to receive the critical study it deserves. Because all the species are closely related and have a somewhat similar appearance, the taxonomy of Ceratozamia has been debated for many years. As taxonomy is based on interpreting data, and taxonomists are notoriously divergent in their interpretations, there have been disagreements on the justification for some proposed new species. Taxonomists are often categorized as either ‘lumpers’ or ‘splitters’ – some want to see only the similarities, while others prefer to see the differences. Whether Ceratozamia consists of ten species or 40 is basically a matter of personal opinion. The detailed relationships between all the species have not yet been determined through DNA analysis, but even if that was done, there would probably still not be unanimous agreement as to which species

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to recognize. If any consensus concerning the species concept develops naturally, it will no doubt come slowly. It is therefore imperative that a set of criteria, that are agreeable to all cycad taxonomists, be developed for circumscribing new species.

Distribution of Ceratozamia Currently, there are 21 validly described species of Ceratozamia. Their distribution starts in a restricted narrow band that follows the mountains along the Gulf of Mexico from Tamaulipas and continues through San Luis Potosi, Querétaro, Hidalgo and Puebla. The direction changes slightly just west of the Isthmus of Tehuantepec in the states of Veracruz, Tabasco and Oaxaca, where it moves south and east through Tabasco and Chiapas, then continues from Mexico into Guatemala, Belize and central Honduras. At the present time Ceratozamia is not known to occur west or south of Honduras.

Speciation within Ceratozamia For the past 40 years the author has been investigating Ceratozamia in habitat, and studying the various populations to see how they differ. One of the most interesting observations over this period of time was that most populations of Ceratozamia are restricted in size and generally found only in a limited area (such as a mountain top, portion of a canyon, etc.). Although forms of Ceratozamia are not generally sympatric, it has been reported that C. microstrobila and C. latifolia grow together (Stevenson et al., 1986; Moretti and Sabato, 1988), but the author has never seen this personally. This separation of populations leads to speculation that Ceratozamia was once a widespread genus that was vicariously separated into numerous populations that have evolved over the past millions of years into individual identifiable colonies. These small colonies are not the result of land clearance or collectors, as many of them were known long before conservation issues arose. The author has studied the morphology of many of these populations and found them to be sufficiently distinct to be identified when growing in a collection of cultivated plants, far from their native territory. The changes in these populations were no doubt the result of their adapting to differing climates, plant associations, soils, light conditions, etc. As previously noted, laboratory tests are useful primarily in identifying species relationships; however, they have not been perfected to the point where they can reliably distinguish between species. This makes it necessary to continue to rely mainly on morphological differences in the identification and description of new species. All of the variable morphological characters within Ceratozamia must be identified and as many of these as possible should be addressed when a new species is described. The following similarities and differences have been observed within Ceratozamia and each of these points should be

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considered individually in the circumscription of a suspected new species.

Similarities within Ceratozamia All species and forms of Ceratozamia are similar in that they have: (i) pinnate leaves; (ii) persistent leaf bases; (iii) entire leaflet margins; (iv) articulated leaflets; (v) stipulate leaves and cataphylls; (vi) cone sporophylls arranged in a spiral, but appearing to be in vertical rows; (vii) two spines or horns on the face of each sporophyll; and (viii) a chromosome number of 2n = 16 (where determined).

Differences within Ceratozamia Species and forms of Ceratozamia differ in the following respects: ●

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Leaves are either upright or arching, short or long, green or brown emergent and heavily tomentose to almost glabrous. Mature plants produce varying numbers of new leaves, from a single leaf to over 20, depending on the species. Petioles may be unarmed (e.g. C. microstrobila, C. zaragozae), lightly armed (e.g. C. mexicana, C. hildae) or heavily armed (e.g. C. robusta, C. miqueliana) with stiff spines. The spines may be restricted to the petiole or may sometimes extend up the rachis almost to its apex. Female cones may be erect (e.g. C. microstrobila, C. whitelockiana), decumbent (e.g. C. mexicana, C. robusta) or pendulous (e.g. C. mixeorum, C. zaragozae). The position of the cone is dependent on the length and diameter of the peduncle. Erect cones have short thick peduncles, decumbent cones have somewhat longer thinner peduncles, and pendulous cones have long, thin peduncles (Figs 8.1–8.3). Male cones vary from short cylindrical to short or long conical and have sporophylls that vary in size. The size, length and orientation of the ‘horns’ also varies considerably between species. Leaflets vary from narrow (3–7 mm) to wide (16 cm), and short (15–18 cm) to long (25–40 cm). Long narrow leaflets generally indicate a bright dry habitat, whereas very broad leaflets indicate moist, shady conditions (Fig. 8.4). Leaflet veins are either prominent or obscure in transmitted light. Leaflet veins in Ceratozamia can be separated into two types: those with transparent veins (e.g. C. zoquorum), and those with obscure veins (e.g. C. miqueliana). These two types are easily distinguished by viewing the leaflets when held up to the light (Fig. 8.5). Leaflet shape is generally lanceolate, oblong or linear, straight or falcate, with the adaxial surface flat or channelled. The leaflet apex may be acute (e.g. C. matudae), obovate (e.g. C. miqueliana) or oblanceolate (e.g. C. euryphyllidia) and may be either equally or unequally attenuate. Leaflet texture (or thickness) may be either coriaceous or leathery (e.g. C.

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Fig. 8.1. Ceratozamia hildae G.P. Landry & M.C. Wilson displaying upright female cone.

Fig. 8.2. Ceratozamia mexicana Brongniart displaying decumbent female cone.

Fig. 8.3. Ceratozamia zaragozae Medellin-Leal displaying pendulous female cone.

latifolia, C. zoquorum), papyraceous (e.g. C. miqueliana) or membranaceous (e.g. C. euryphyllidia). Leaflet texture is generally controlled by habitat in that species with coriaceous leaflets are generally found in seasonally dry habitats that are often subjected to wind, those with papyraceous leaflets are found in dark continually moist habitats, and those species with membranaceous leaflets are

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Fig. 8.4. Leaflet forms of Ceratozamia, left to right: C. norstogii D.W. Stevenson; C. matudae Lundell; C. sabatoi Vovides, Váquez Torres, Schutzman & Iglesias; C. mexicana Brongniart; C. microstrobila Vovides & J.D. Rees; C. latifolia Miquel; C. miqueliana H. Wendland; C. sp. ‘‘becerrae’’ and C. euryphyllidia Vázquez Torres, Sabato & D.W. Stevenson.

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restricted to shady and continually wet habitats. Leaflet margins are either strongly or lightly revolute, or flat. Emergent leaves vary in conformation, colour and texture of rachis and leaflets, and amount and colour of tomentum (Figs 8.6–8.8). The adaxial surface of emergent leaflets is glossy (e.g. C. mexicana, C. robusta), or pruinose, as those of the C. miqueliana complex (e.g. C. whitelockiana, C. zoquo-

Fig. 8.5. Transparent as opposed to obscure leaflet veins as seen by transmitted light: left, Ceratozamia sp. ‘‘becerrae’’; right, C. miqueliana H. Wendland.

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Fig. 8.6. Emergent leaf of Ceratozamia norstogii D.W. Stevenson.

Fig. 8.7. Emergent leaf of Ceratozamia zoquorum Pérez-Farrera, Vovides & Iglesias.

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Fig. 8.8. Emergent leaves showing differences in tomentum of Ceratozamia latifolia Miquel.

rum). They may have leaflets with the veins on the abaxial surface prominently raised or flat. Eophylls (first seedling leaves) display differences in the leaflet shape, length

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and width, number of leaflets (Figs 8.9–8.11), and their colour and texture. For example, C. zoquorum has one pair of leaflets that are coriaceous and pruinose, C. miqueliana has two pairs of leaflets that are papyraceous and pruinose, while C. norstogii has three pairs of leaflets that are papyraceous. Stems are either subterranean, shortly emergent or arborescent. Ceratozamia stems that are either subterranean or shortly emergent are generally < 20 cm

Fig. 8.9. Eophylls (first seedling leaves): left, Ceratozamia zoquorum Pérez-Farrera, Vovides & Iglesias; right, C. miqueliana H. Wendland.

Fig. 8.10. Eophylls (first seedling leaves) of Ceratozamia mexicana Brongniart.

Fig. 8.11. Eophylls (first seedling leaves) of Ceratozamia norstogii D.W. Stevenson.

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in height (e.g. C. microstrobila, C. whitelockiana) or arborescent with stems > 1 m in height (e.g. C. mexicana, C. robusta). Stems also exhibit either smooth (e.g. C. microstrobila) or rough (e.g. C. norstogii) exteriors. The difference in stem surface is caused by the conformation of the cataphylls. The ‘rough’ surface is produced by cataphylls that are deeply wrinkled and have a recurved apex, whereas a ‘smooth’ surface is produced by cataphylls with a more-or-less flat exterior and an apex that is held flush with the stem (Figs 8.12–8.13).

Fig. 8.12. Ceratozamia sp. ‘‘El Mirador’’ displaying a more-or-less smooth surface of short, tightly appressed cataphylls.

Fig. 8.13. Ceratozamia norstogii D.W. Stevenson displaying long, wrinkled and divergent cataphylls.

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Leaf variation in Ceratozamia Leaves of Ceratozamia are very plastic in response to the amount of light or shade they receive. Plants growing in shade will have longer and broader leaves and leaflets; conversely, plants growing in more sunlight will have shorter and narrower leaves and leaflets. Seedling and immature plants of a species will also display leaflets that are generally much broader than those on a mature plant. These differences can be so great that if one was shown an immature specimen and a mature specimen of the same species, they might easily be identified as two different species (Fig. 8.14).

Fig. 8.14. Ceratozamia matudae Lundell showing the remarkable difference between a juvenile leaf (upper left) and mature leaves.

The leaflets of Ceratozamia display a number of character differences not related entirely to environmental conditions; these differences persist with plants in cultivation and can be used as diagnostic characters in identifying or describing species (Table 8.1).

Suggested Criteria for New Species Descriptions If the following criteria dealing with distribution, location, habitat, morphology and reproduction are incorporated into future descriptions for new taxa of Ceratozamia, there should be little doubt as to their validity (see Osborne and Walters, Chapter 15 this volume, for a complete list of guidelines for describing new cycad taxa). ●

The taxonomist must study the plant in its natural habitat and not rely entirely on herbarium vouchers and the notes of others.

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New leaflets pruinose

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Leaflets membranaceous

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Leaflets papyraceous

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C. alvarezii Pérez-Farrera, Vovides & Iglesias C. euryphyllidia Vázquez Torres, Sabato & D.W. Stevenson C. hildae G.P. Landry & M.C. Wilson C. kuesteriana Regel C. latifolia Miquel [Xilitla, San Louis Potosi] C. matudae Lundell C. mexicana Brongniart [Jalapa, Veracruz] C. microstrobila Vovides & J.D. Rees C. miqueliana H. Wendland [Tabasco] C. miqueliana H. Wendland [Chiapas] C. mirandae Vovides, Pérez-Farrera & Iglesias C. mixeorum Chemnick, T.J. Gregory & Salas-Morales C. morettii Vázquez Torres & Vovides C. norstogii D.W. Stevenson C. robusta Miquel [El Sumedero, Chiapas] C. sabatoi Vovides, Vázquez Torres, Schutzman & Iglesias C. whitelockiana Chemnick & T.J. Gregory C. zaragozae Medellin-Leal C. zoquorum Pérez-Farrera, Vovides & Iglesias C. sp. “Palma Sola” [Veracruz] C. sp. “Santiago Tuxtla” [Veracruz] C. sp. “San Gabriel Mixtepec” [Oaxaca] C. sp. “El Mirador” [Veracruz] C. sp. “Naranjal” [Veracruz] C. sp. “Belize” C. sp. “becerrae” [Tabasco] C. sp. “Lake Catemaco” [Veracruz] C. sp. “Honduras” C. sp. [Chiapas] C. sp. “Redback” [Puebla]

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Table 8.1. Ceratozamia leaflet characteristics.

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Herbarium vouchers should be made from several plants that exhibit the full range of variation within the population. The exact location should be carefully noted, using a GPS if possible. If a GPS is not available, exact distance and direction from permanent landmarks (e.g. a bridge, a railroad crossing, geological formation) should be given. Notes on the habitat should be as complete as possible, and include such details as altitude, aspect, geology, soil type, climatic data and plant associations. The presence or absence of cones and/or seed or seedlings and the extent of regeneration should be noted. If cones are in the process of shedding pollen they should be investigated for pollinators. When pollinators are found, specimens should be collected and preserved so that they can later be identified. Conservation considerations such as land clearance, damage by livestock, road and dam building, introduced pests and predators, etc. should be noted. Photographic documentation should be made of the habitat, the plants and their reproductive structures when present. Results from laboratory tests such as DNA sequence profiling, chromosome counts, electrophoretic assays, etc., when available, should be included and discussed.

References Avendaño, S., Vovides, A.P. and Castillo-Campos, G. (2003) A new species of Ceratozamia (Zamiaceae, Cycadales) from Veracruz, Mexico. Botanical Journal of the Linnaean Society 141, 395–398. [Ceratozamia huastecorum.] Brongniart, A.T. (1846) Note sur un nouveau genre de Cycadées du Mexique. Annales des Science Naturelles, series 3, 5, 5–10. [Ceratozamia; C. boliviana, C. mexicana.] Caputo, P., Stevenson, D.W. and Wurtzel, E.T. (1991) A phylogenetic analysis of American Zamiaceae (Cycadales), using chloroplast DNA restriction fragment length polymorphisms. Brittonia 43, 135–145. Chemnick, J. and Gregory, T.J. (1995) A new species of Ceratozamia (Zamiaceae) from Oaxaca, Mexico, with comments on distribution, habitat, and relationships. Phytologia 79, 51–57. [Ceratozamia whitelockiana.] Chemnick, J., Gregory, T.J. and Salas-Morales, S. (1997) Ceratozamia mixeorum (Zamiaceae), a new species of Ceratozamia from Oaxaca, Mexico, with comments on distribution, habitat, and species relationships. Phytologia 83, 47–52. De Luca, P., Moretti, A., Siniscalco Gigliano, G., Caputo, P., Cozzolino, S., Gaudio, L., Stevenson, D.W., Wurtzel, E.T. and Osborne, R. (1995) Molecular systematics of cycads. In: Vorster, P. (ed.) Proceedings of the Third International Conference on Cycad Biology. Cycad Society of South Africa, Stellenbosch, South Africa, pp. 131–137. Johnson, L.A.S. (1959) The families of cycads and the Zamiaceae of Australia. Proceedings of the Linnaean Society of New South Wales 84, 64–117. Landry, G.P. and Wilson, M.C. (1979) A new species of Ceratozamia (Cycadaceae) from San Luis Potosí. Brittonia 31, 422–424. [Ceratozamia hildae.] Lundell, C.L. (1939) Studies of Mexican and Central American plants, VII. Lloydia 2, 73–76. [Ceratozamia matudae.]

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Medellin-Leal, F. (1963) A new species of Ceratozamia from San Luis Potosí. Brittonia 15, 175–176. [Ceratozamia zaragozae.] Miquel, F.A.W. (1848) Over eenige nieuwe of zeldzame Cycadeën in den Hortus Botanicus te Amsterdam. Tijdschrift voor de Wis- en Natuurkundige Wetenschappen 1, 33–34, 197–209. [Ceratozamia robusta, C. latifolia.] Moretti, A. and Sabato, S. (1988) Systematics and evolution of Dioon and Ceratozamia. Fairchild Tropical Garden Bulletin 43(1), 22–28. Moretti, A., Sabato, S. and Siniscalco Gigliano, G. (1981) Monosaccharide composition of the mucilages in Encephalartos Lehm. (Zamiaceae). Giornale Botanico Italiano 115, 291–297. Moretti, A., Sabato, S. and Siniscalco Gigliano, G. (1983) Taxonomic significance of methylazoxymethanol glycosides in the cycads. Phytochemistry 22, 115–118. Moretti, A., Caputo, P., Gaudio, L. and Stevenson, D.W. (1991) Intraspecific chromosome variation in Zamia (Zamiaceae, Cycadales). Caryologia 44, 1–10. Norstog, K.J. (1980) Chromosome numbers in Zamia (Cycadales). Caryologia 33, 419–428. Norstog, K.J. (1981) Karyotypes of Zamia chigua (Cycadales). Caryologia 34, 255–260. Osborne, R., Salatino, M.L.F. and Salatino, A. (1989) Alkanes of foliar epicuticular waxes of the genus Encephalartos. Phytochemistry 28, 3027–3030. Pérez-Farrera, M.A., Vovides, A.P. and Iglesias, C.G. (1999) A new species of Ceratozamia (Zamiaceae, Cycadales) from Chiapas, Mexico. Novon 9, 410–413. [Ceratozamia alvarezii.] Pérez-Farrera, M.A., Vovides, A.P. and Iglesias, C.G. (2001) New species of Ceratozamia (Zamiaceae) from Chiapas, Mexico. Botanical Journal of the Linnean Society 137, 81–85. [Ceratozamia mirandae, C. zoquorum.] Regel, E. (1857) Zwei neue Cycadeen, die im Botanischen Garten zu Petersburg kultivirt werden, nebst Beiträge zu Kenntniss dieser Familie. Bulletin de la Société Impériale des Naturalistes de Moscou 30, 161–191. [Ceratozamia kuesteriana.] Stevenson, D.W. (1982) A new species of Ceratozamia (Zamiaceae) from Chiapas, Mexico. Brittonia 34, 181–184. [Ceratozamia norstogii.] Stevenson, D.W., Sabato, S. and Vázquez Torres, M. (1986) A new species of Ceratozamia (Zamiaceae) from Veracruz, Mexico with comments on species relationships, habitats, and vegetative morphology in Ceratozamia. Brittonia 38, 17–26. [Ceratozamia euryphyllidia.] Vázquez Torres, M. and Vovides, A.P. (1998) A new species of Ceratozamia (Zamiaceae) from Veracruz, Mexico. Novon 8, 87–90. [Ceratozamia morettii.] Vovides, A.P. and Olivares, M. (1996) Karyotype polymorphism in the cycad Zamia loddigesii (Zamiaceae) of the Yucatan peninsula, Mexico. Botanical Journal of the Linnean Society, 120, 77–83. Vovides, A.P. and Rees, J.D. (1983) Ceratozamia microstrobila (Zamiaceae), a new species from San Luis Potosí, Mexico. Madroño 30, 39–42. Vovides, A.P., Vázquez Torres, M., Schutzman, B. and Iglesias, C.G. (1993) A new species of Ceratozamia (Zamiaceae) from Querétaro and Hidalgo, Mexico. Novon 3, 502–506. [Ceratozamia sabatoi.] Wendland, H. (1854) Index Palmarum, Cyclanthearum, Pandanearum, Cycadearum, quae in Hortis Europaeis Coluntur. Hahn, Hannover, Germany, pp. 49–54, 68. [Ceratozamia miqueliana.]

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Relationships and Phytogeography in Ceratozamia (Zamiaceae)

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Andrew P. Vovides,1 Miguel A. Pérez-Farrera,2 Dolores González1 and Sergio Avendaño1 1Instituto de Ecología 2Escuela de Biología,

A.C., Xalapa, Veracruz, Mexico; Universidad de Ciencias y Artes de Chiapas (UNICACH), Tuxtla Gutiérrez, Chiapas, Mexico

Abstract Species relationships and phytogeography of Ceratozamia, an endangered neotropical cycad genus, based on morphology, leaflet histology, DNA sequencing and ecological data, are analysed and discussed. Seven species complexes are assigned within the genus. A centre of origin in south-eastern Mexico, with recent speciation and immigration patterns, is proposed.

Introduction Ceratozamia Brongniart presents morphological variation both within and between species. Miquel (1870) noted differences in leaflet shape and size as well as varying sizes of cones with age of any given species of Ceratozamia but he saw stability in the morphology of micro- and megasporophylls. Thiselton-Dyer (1882–1886) commented: ‘This variableness [sic] with age makes the separation of nearly allied forms an all but hopeless task’. Chromosome number and karyotype within the genus is extremely stable (Vovides, 1983, 1985; Moretti, 1990), which contrasts with chromosome variation found in Zamia Linnaeus (Moretti and Sabato, 1984, Vovides and Olivares, 1996). Vovides (1983, 1985) noted differences in secondary constriction or satellite number and position within Ceratozamia. Few anatomical and morphological characters appear to separate related Ceratozamia species. To date, species descriptions within the genus have ©CAB International 2004. Cycad Classification: Concepts and Recommendations (eds T. Walters and R. Osborne)

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been based largely on gross morphological characters, strobilus indumentum, colouring, and geographical distribution.

Phytogeography The genus Ceratozamia presently comprises 21 species (Hill et al., Appendix 1 this volume) and this figure will probably increase to about 26 in the near future. It is largely distributed in the warm temperate and tropical regions of eastern and southern Mexico, from the state of Tamaulipas at its extreme northern limit in Mexico, to Belize and Guatemala in central America (Balduzzi et al., 1982). Recently a taxon related to the C. miqueliana complex has been found in northern Honduras, hence the range of the genus has been extended. The Ceratozamia complexes in southern and south-eastern Mexico appear to coincide with floristic refuges, according to Toledo (1982) and Wendt (1987). In support of the Pleistocene refuge theory, there appears to be fossil evidence of Ceratozamia of Miocene age from a Cenozoic floristic refuge in Oaxaca (Rzedowski and Palacios, 1977).

Morphology and distribution In terms of gross morphology, plants from north-eastern Mexico are generally characterized as having small and often branching trunks with few leaves per crown. Leaflets are usually narrow (i.e. < 2 cm wide), with the exception of those of Ceratozamia microstrobila Vovides & J.D. Rees and another two isolated species in northern Veracruz (under investigation). In addition, the plants from the northeastern areas bear relatively smaller cones than those in southern and southeastern Mexico. Plants from southern and south-eastern Mexico are generally large, single trunked plants, although branching has been observed in some taxa, e.g. Ceratozamia alvarezii Pérez-Farrera, Vovides & Iglesias from Chiapas. These southern and south-eastern taxa have leaflets usually > 2 cm wide, the widest being found in C. euryphyllidia Vázquez Torres, Sabato & D.W. Stevenson. Exceptions to the generally wide leaflet morphology are seen in C. norstogii D.W. Stevenson, C. mirandae Vovides, Pérez-Farrera & Iglesias and C. alvarezii, all three of which have leaflets < 1.5 cm wide. Moretti et al. (1980) were the first to recognize species complexes within the genus highlighting separate Ceratozamia mexicana and C. matudae complexes (Fig. 9.1). Stevenson et al. (1986) proposed two main groups in Ceratozamia, based on leaflet morphology: (i) a C. mexicana group with long narrow leaflets; and (ii) a C. euryphyllidia/miqueliana group with shorter and wider leaflets. However, throughout the distribution of Ceratozamia, various other related groups or complexes can also be found. We have confirmed the complexes identified by the earlier workers, as well as other new complexes – principally in southern and south-eastern

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Fig. 9.1. Distribution in Mexico and Guatemala of four Ceratozamia species complexes: A = C. kuesteriana species complex; B = C. latifolia species complex; C = C. mexicana species complex; D = C. matudae species complex.

Mexico. Our main two additional groups are a C. norstogii complex (Fig. 9.2) (Pérez-Farrera et al., 1999; Vovides et al., 2001) and a C. miqueliana complex (Fig. 9.3) (Pérez-Farrera et al., 2001). The distribution of these complexes is apparently related to their habitats. For instance, C. miqueliana H. Wendland and related species occur in evergreen tropical rainforest and are not generally found at elevations > 1000 m; these plants are characterized by having both decumbent and erect female cones, and leaves up to 2.5 m long with oblanceolate leaflets. By contrast, species of the C. norstogii group are largely found in oak and pine/oak forests at elevations between 800 and 1400 m; characteristic features of these species are branching or cylindrical and non-branching trunks, erect male and female cones, and linear, flat or channelled leaflets with a straight or spirally twisted rachis. The C. robusta species complex (sensu Stevenson et al., 1986) (Fig. 9.4) appears to have a wide range of habitat type ranging over evergreen and deciduous tropical forests, oak forests and cloud forests; plants within this group are large and robust with leaves up to 3 m long and bear large erect or decumbent male and female cones. On the basis of gross morphology we now believe that there are at least seven species complexes in the genus: 1. The Ceratozamia mexicana complex is mainly distributed on the transMexican Neovolcanic mountain range, covering central Veracruz, parts of Puebla and Hidalgo states and possibly north-eastern Oaxaca (Fig. 9.1). Included

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Fig. 9.2. Distribution in Mexico (encircled area) of the Ceratozamia norstogii species complex.

here is C. mexicana Brongniart var. robusta Dyer (sensu Thiselton-Dyer, 1882–1886; Vovides et al., 1983) and C. mexicana var. mexicana. 2. The Ceratozamia latifolia complex, a species group to the north and north-east of the trans-Mexican Neovolcanic mountain range, is a somewhat

Fig. 9.3. Distribution in Mexico (encircled area) of the Ceratozamia miqueliana species complex.

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Fig. 9.4. Distribution in Mexico, Guatemala and Belize (encircled area) of the Ceratozamia robusta species complex.

loose assemblage and may subsequently prove to comprise more than one complex. As presently circumscribed, the group consists of C. latifolia Miquel, C. hildae G.P. Landry & M.C. Wilson, C. microstrobila Vovides & J.D. Rees, C. huastecorum S. Avendaño, Vovides & Castillo-Campos, C. brevifrons Miquel (= C. mexicana Brongniart; see Hill et al., Appendix 1 this volume) and C. morettii Vázquez Torres and Vovides (the latter two species are on the Neovolcanic transverse mountain range). 3. The Ceratozamia kuesteriana complex occurs in north-eastern Mexico and includes C. kuesteriana Regel, C. sabatoi Vovides, Vázquez Torres, Schutzman & Iglesias, and C. zaragozae Medellin-Leal. These are three taxa with narrow lanceolate to linear leaflets. Other taxa in this region are at present under investigation. 4. The wide leaflet Ceratozamia miqueliana complex which occurs to the south and south-east of the trans-Mexican Neovolcanic belt, comprises about five taxa. These are C. miqueliana, C. euryphyllidia, C. zoquorum Pérez-Farrera, Vovides & Iglesias, a new taxon that will be described in the near future (Ceratozamia sp. “becerrae”) and another possibly new species from Chiapas. 5. The Ceratozamia norstogii complex is largely distributed to the south in Chiapas and eastern Oaxaca, with three apparently well-defined species: C. norstogii, C. alvarezii and C. mirandae Vovides, Pérez-Farrera & Iglesias (see Pérez-Farrera et al., Chapter 10, this volume). We are also tentatively placing a new taxon, yet to be described, in this complex (Ceratozamia sp. “chimalpensis”).

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6. The Ceratozamia robusta (sensu Stevenson) group is found in Chiapas, Oaxaca, southern Veracruz, Guatemala and Belize. This is another loose assemblage in which we place C. robusta Miquel, C. whitelockiana Chemnick & T.J. Gregory, C. mixeorum Chemnick, T.J. Gregory & Salas-Morales, and a further new species of Ceratozamia, yet to be described, from Oaxaca. 7. The Ceratozamia matudae complex, which is distributed from the extreme south of Chiapas into Guatemala consists of C. matudae Lundell and a newly discovered species yet to be described (Ceratozamia sp.). The taxonomy of Ceratozamia is far from resolved and there is still much confusion at the species level within these complexes. It is hoped that the molecular, anatomical and phytogeographical studies at present under way on the genus will eventually contribute to the clarification of the status of species within Ceratozamia.

Habitats Most species of Ceratozamia can be found within 15–17.5° north and 92.5–98.5° west. Typical habitats for Ceratozamia in north-eastern Mexico are broadleaf deciduous cloud forest and pine/oak forest at elevations between 500 and 2000 m. In southern and south-eastern Mexico, Ceratozamia can be found in lowland evergreen tropical rainforest at elevations < 100 m, to cloud forests and pine/oak forests from about 600 to 1400 m. Populations can be locally abundant, and in some cases dominant in the herbaceous undergrowth of cloud forests, such as in the cases of C. mexicana in Veracruz and C. mirandae in Chiapas. Using multivariate analysis on taxa and their habitat types (McCune and Mefford, 1997) species with wide oblanceolate to oblong leaflets (C. euryphyllidia, C. mexicana var. robusta, C. miqueliana, C. zoquorum and C. sp. “becerrae”) are confined to evergreen tropical rainforest, whilst a number of species with narrow, linear or falcate leaflets are frequently associated with cloud forests, oak and pine/oak forests (Fig. 9.5).

Molecular Studies Molecular phylogenetic analyses on New World cycads are scarce, and those so far published have examined restriction fragment length polymorphism variation data at generic level (Caputo et al., 1991, 1993; Moretti et al., 1993; De Luca et al., 1995). In order to gain insight into phylogenetic relationships within the genus Ceratozamia, we undertook a study of variation in sequences of non-coding regions from the chloroplast and nuclear genomes. We selected two regions that have been used in phylogenetic studies at infrageneric level for a variety of plants (Schilling et al., 1998; Potter et al., 2000). One is the nuclear internal transcribed spacer (ITS) region, which has proved to be an excellent source of information

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Number of species

Types of vegetation

Principal component 2

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Principal component 1 Fig. 9.5. Relationships between taxa of Ceratozamia and habitat (BTSC, tropical sub-deciduous rainforest; BTP, evergreen tropical rainforest; BMM, cloud forest; BQ, oak forest; BC, coniferous forest; BTC, tropical deciduous forest). (A) Number of taxa of Ceratozamia present in six vegetation types. (B) Summary of a principal components analysis of habitat and leaflet width for taxa of Ceratozamia.

from the nuclear genome (Baldwin et al., 1995). However, only 29 characters out of 1083 of the ITS region were informative among 24 exemplars. The second region we examined is the chloroplast genome trnL-F non-coding region and trnL-trnF spacer. Here, the alignment for a subsample of 16 Ceratozamia sequences from the trnL-F non-coding region generated 998 characters, from which only two were informative. The selection of Zamia as an outgroup was based on the

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results obtained with the analyses of the trnL-F non-coding region, where Zamia appeared as the sister group to Ceratozamia. The sequence data generated in this study were used to evaluate: (i) the hypothesis that Ceratozamia is monophyletic; and (ii) the species relationships within the genus. The results of these analyses yielded 112 trees of 51 steps; the strict consensus of these trees is shown in Fig. 9.6A (with bootstrap values and decay index) and one randomly chosen minimal length tree is presented in Fig. 9.6B to show average branch and distribution of the taxa. The low level of variation detected among species limits the conclusions that could be drawn from the study; however, the cladograms did enable us to infer a tentative but interesting scenario for the genus (González and Vovides, 2002). Other molecular techniques, such as random amplified polymorphic DNA (now in progress), might help to identify the more variable regions of the genome in order to enable us to design primers to sequence those regions in the near future. Microsatellite techniques also appear to be promising.

Leaflet Anatomy Leaflets from five adult plants from each of five taxa were taken from the midportion of a mature leaf. Leaflets were fixed in formalin acetic alcohol then hand microtome sections were made. These were stained in phloroglucinol HCl to show lignified tissues and in alcoholic Sudan III and IV mixture for cutin and other fatty acid tissues. Nineteen measurements were obtained from each individual plant using a calibrated eyepiece scale (Table 9.1). Analysis was done using analysis of variance (ANOVA) and multiple range tests from Statistica (StatSoft, Inc. Tulsa, Oklahoma, USA). Results so far from leaflet anatomy appear to be promising in our attempts to isolate useful characters for delimiting species. Nevertheless, a homogeneity of states has been observed in about 50% of the characters studied, reflecting a similar situation to that found in DNA sequencing of the ITS region mentioned previously. From a suite of 19 characters analysed using morphometric and phenetic techniques, nine were found to be taxonomically useful and enabled us to separate a mean of nine groups from a total of 18 operational taxonomic units.

Discussion Ceratozamia is largely found along the Sierra Madre Oriental, in southern and south-eastern Mexico and through Guatemala and Belize to Honduras. The genus presents disjunct populations in Mexico (Sabato and De Luca, 1985; Moretti et al., 1993) with the exception of C. robusta (sensu Stevenson) where the majority of populations are found in south-east Veracruz, north-west Chiapas and the southern sierra of Oaxaca, Belize and Guatemala. Future work will help

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Fig. 9.6. Phylogenetic relationships within Ceratozamia based on ITS sequences (length 51, consistency index = 0.8235, retention index = 0.9151, rescaled consistency index = 0.7536) (from González and Vovides, 2002). (A) Strict consensus tree. (B) Minimal length tree chosen at random.

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Table 9.1. Leaflet anatomical characters used to distinguish Ceratozamia taxa. Five plants from each of five taxa were sampled for the total 19 characters. Characters

Dimensions

Abaxial epiderm cells Cuticles abaxial and adaxial Epiderm cells abaxial and adaxial Palisade parenchyma cells Sclereids associated with vascular bundles Sclereids not associated with vascular bundles Bulliform-like cells Stomatal pores

Length and width Thickness Length and width Length and width Number, length and width

2 2 4 2 3

Number, length and width

3

Length and width Depth

2 1

Total number of characters examined

Number

19

to resolve whether these represent a single disjunct species or a complex of related taxa. Stevenson et al. (1986) proposed that leaflet morphology and habitat are correlated, with those species of Ceratozamia having wide and thin leaflets being confined to the more humid environments and taxa with narrow and more coriaceous leaflets to the more xeric habitats. We have confirmed this with our observations. So far, leaflet anatomy appears to group the species into nine groups. Figures 9.7 and 9.8 show examples of two useful anatomical characters: (i) there appear to be lower leaflet cuticle thickness differences between C. miqueliana and C. zaragozae but no differences in stomatal pore depth; and (ii) there are differences in the number of associated and non-associated fibres with the vascular bundles of the leaflets of C. mexicana var. robusta and C. kuesteriana (S. Avendaño, Veracruz, 2002, personal communication). Although there appears to be a certain correlation of the anatomical features with distribution, it is too early to draw conclusions. Stevenson et al. (1986) mentioned vicariance as a possible explanation for the present distribution of Ceratozamia and that the genus is monophyletic. PérezFarrera (1999) suggested that at least some species could be dispersed by mammals such as the peccari (Tayassu tajacu). Some of the present unusual distribution patterns could be the result of now-extinct dispersal agents, as suggested by Jansen and Martin (1982) for tropical trees bearing large fruits. It appears that Ceratozamia (Cycadopodites) was present in Miocene floras in Pichucalco, Chiapas, southern Mexico (Palacios and Rzedowski, 1993) and in Cenozoic Engelhardtia forests in Oaxaca, where the fossil pollen spectrum is remarkably similar to that of the modern; it is noted that Engelhardtia used to be widely distributed over the northern hemisphere in the Tertiary (Rzedowski and Palacios, 1977). However, owing to climatic changes during the Pleistocene

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11 10 Cuticle thickness (micron)

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± Std. Dev. ± Std. Error Mean

7 6 5 4 3 2 C. miqueliana #1 C. zaragozae #1 C. miqueliana #2 C. zaragozae #2

Fig. 9.7. Significant differences in cuticle thickness of lower leaflet epidermis between two samples of Ceratozamia miqueliana H. Wendland and two samples of C. zaragozae Medellin-Leal.

(Burnham and Graham, 1999) some members of Ceratozamia survived in the south of Mexico, where the greatest diversity appears to be concentrated, and very probably an ancestral form became isolated in Honduras, a territory with a history of geographical isolation (Coney, 1982). Isolation and subsequent speciation in the genus appear to be relatively recent, since DNA sequencing data show a low level of variation amongst species (Gonzáles and Vovides, 2002). However, some interesting insights into the phytogeography of this genus can be seen where a correlation with geographical distribution patterns appears to be evident. The three main clades in Fig. 9.9A are consistent with distributional ranges of the species. The two basal clades contain the species that are distributed in southern and south-eastern Mexico, both at and south of the Neovolcanic mountain range of Pliocene–Quaternary (Pleistocene) age (Fig. 9.9B). Here the Ceratozamia norstogii clade integrates well with what we consider the C. norstogii complex. Though we consider C. zoquorum to be part of the C. miqueliana complex, it appears to be paraphyletic to the C. miqueliana clade, but, owing to the low number of molecular characters that generated this tree, this is a tentative hypothesis and further research is still in progress. By and large, there is consistency with the findings of Marshall and Liebherr (2000), who identified two biogeographic assemblages, one north of the Neovolcanic range and another to the south. The large unresolved clade contains a group of morphologically distinct species to the north and north-east of the Neovolcanic range which appears to be of more recent speciation (Fig. 9.9). The vegetational history of southern Mexico and the Maya Mountains

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af

af

Fig. 9.8. Differences in number of associated (af) and non-associated (nf) fibres with the vascular bundles of leaflets (ue, upper epidermis; pa, palisade mesophyll; sm, spongy mesophyll; s, bundle sclerenchyma; x, xylem; ph, phloem; le, lower epidermis). (A) Ceratozamia mexicana Brongniart var robusta Dyer. (B) Ceratozamia kuesteriana Regel.

(Belize) has been studied by Lundell (1939, 1945) and Miranda (1957, 1959), who agreed that the region contains relict floral elements of great age. During the past 40,000 years, tropical forests in Mexico have been disrupted and displaced to lower latitudes due to the onset of Pleistocene climatic changes with cycles of cold-dry, cold-wet and warm-dry climates, thus leaving relict pockets or refuges that protected the biota from lowering of temperature, rainfall and precipitation (Toledo, 1982). Graham (1976), using palynological analysis, maintained that modern tropical rainforest in Mexico is recent. However, there is a general consensus on the existence of floristic and faunistic refuges of great age in southern Mexico (Brown, 1976; Toledo, 1982, 1988), but these are apparently absent in the areas north of the Neovolcanic mountain range. From the data presented in this study we put forward the hypothesis that Ceratozamia has its origin in southern/south-eastern Mexico. The unresolved clade of Ceratozamia species at and north of the Neovolcanic range is very likely the result of adaptive radiation or

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C. matudae

Fig. 9.9. Relationships among species of Ceratozamia (from González and Vovides, 2002). (A) Phylogenetic relationships using ITS sequences. (B) Geographical distribution in Mexico of the three major clades shown in Fig. 9.9A.

recent speciation processes. Those populations north of the range are morphologically distinct, with gross morphological characters that do not change when cultivated under similar conditions over several years; these are, however, homogeneous in DNA sequencing. It may be argued that there are very few mutations in those species that are resolved, but the relatively long generation times for Ceratozamia must be considered: species have a generation time (germination to maturity to seed set) of at least 15 years under optimal cultivation conditions and this period can safely be doubled for conditions in the wild. Therefore, only about 300 generations of a putative Ceratozamia

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would have occurred since the end of the Pleistocene (10,000 years ago); thus any speciation within the genus would be understandably slow. It is hoped that anatomical, morphometric and other molecular studies will throw more light on this matter. Examining the cladogram (Fig. 9.9A), better-resolved clades (all south of the Neovolcanic belt) can easily be placed into the known refuges (Fig. 9.9B). The Ceratozamia matudae clade is found in the Soconusco refuge of Chiapas on the Sierra Madre del Sur while C. mixeorum is from the adjacent northern mountains of Oaxaca near the Sierra de Juarez refuge. The C. miqueliana, C. euryphyllidia, C. sp. “becerrae”, C. whitelockiana and C. zoquorum clades are situated on and adjacent to the Los Tuxtla refuge of Toledo and the ‘arc refuge area’ of Wendt (1987), covering southern Veracruz, northern Chiapas, northern Oaxaca and south-western Tabasco. These species comprise what might be called the C. miqueliana complex. On the Neovolcanic range we find the C. mexicana complex with a separate species on the Cordoba refuge of Toledo (1982, 1988). The rest of the unresolved cladogram consists of Ceratozamia species that are north of the Neovolcanic belt. These species appear to be much younger, suggestive of adaptive radiation with a northwards migratory pattern following a general warming of climate. The C. mexicana clade (on the Neovolcanic range) appears to be the most recently derived.

Conclusions We put forward the hypothesis that Ceratozamia, a relict palaeoendemic, is currently in the process of active speciation. This process was probably initiated during the early Cenozoic and was stimulated by climate changes of the late Tertiary and Quaternary periods giving rise to the present taxa, which are apparently well adapted to modern ecosystems. From a conservation point of view, we reiterate that cycads, which are phylogenetically basal to the living seed plants, should be given top priority in the agendas of countries that are rich in their cycad diversity. With 303 species (see Hill et al., Appendix 1 this volume), cycads are relatively few worldwide; efforts for their conservation should not be too expensive and the returns very great, considering the vast information contained in their genomes. As Norstog and Nicholls (1997) commented, ‘they are the Rosetta Stone of spermatophyte evolution’.

References Balduzzi, A., De Luca, P. and Sabato, S. (1982) A phytogeographical approach to the New World Cycads. Delpinoa 23–24, 185–202. Baldwin, B.G., Sanderson, M.J., Porter, J.M., Wojciechowski, M.F., Campbell, C.S. and Donoghue, M.J. (1995) The ITS region of nuclear ribosomal DNA: a valuable source

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of evidence of angiosperm phylogeny. Annals of the Missouri Botanical Garden 82, 247–277. Brown, K.S. Jr (1976) Centros de evolução, refugios Quaternários, e conservação de patrimônios genéticos na região neotropical: Padrões de diferenciação em Ithomiinae (Lepidoptera: Nymphlidae). Acta Amazonica 7, 75–137. Burnham, R.J. and Graham, A. (1999) The history of neotropical vegetation: new developments and status. Annals of the Missouri Botanical Garden 86, 546–589. Caputo, P., Stevenson, D.W. and Wurtzel, E.T. (1991) A phylogenetic analysis of American Zamiaceae (Cycadales) using chloroplast DNA restriction fragment length polymorphisms. Brittonia 43, 135–145. Caputo, P., Marquis, C., Wurtzel, T., Stevenson, D.W. and Wurtzel, E.T. (1993) Molecular biology in cycad systematics. In: Stevenson, D.W. and Norstog, K.J. (eds) The Biology, Structure, and Systematics of the Cycadales. Proceedings of the Second International Conference on Cycad Biology. Palm & Cycad Societies of Australia Limited, Milton, Queensland, Australia, pp. 213–219. Coney, P.J. (1982) Plate tectonic constraints on the biogeography of middle America and the Caribbean region. Annals of the Missouri Botanical Garden 69, 432–443. De Luca, P., Moretti, A., Siniscalco Gigliano, G., Caputo, P., Cozzolino, S., Gaudio, L., Stevenson, D.W., Wurtzel, E.T. and Osborne, R. (1995) Molecular systematics of cycads. In: Vorster, P. (ed.) Proceedings of the Third International Conference on Cycad Biology. Cycad Society of South Africa, Stellenbosch, South Africa, pp. 131–137. González, D. and Vovides, A.P. (2002) Low intralineage divergence in the genus Ceratozamia Brongn. (Zamiaceae) detected with nuclear ribosomal DNA ITS and chloroplast DNA trnL-F non-coding region. Systematic Botany 27, 654–661. Graham, A. (1976) Late Cenozoic evolution of tropical lowland vegetation in Veracruz, Mexico. Evolution 29, 723–735. Jansen, D.H. and Martin, P.S. (1982) Neotropical anachronisms: the fruits the Gomphotheres ate. Science 215, 19–27. Lundell, C.L. (1939) Studies of Mexican and Central American Plants,VII. Lloydia 2, 73–76. [Ceratozamia matudae.] Lundell, C. (1945) Vegetation and natural resources of British Honduras. In: Lundell, C.L. (ed.) Plant and Plant Science in Latin America. Chronica Botanica, Waltham, Massachusetts, pp. 270–273. Marshall, C.J. and Liebherr, J.K. (2000) Cladistic biogeography of the Mexican transition zone. Journal of Biogeography 27, 203–216. McCune, B. and Mefford, J. (1997) Multivariate Analysis of Ecology Data. Version 3.17. MJM Software, Gleneden Beach, Oregon, 126 pp. Miquel, F.A.W. (1870) À la connaissance des cycadées. Adansonia 9, 154–180. Miranda, F. (1957) Vegetación de la vertiente del Pacífico de la Sierra Madre de Chiapas (México) y sus relaciones florísticas. Proceedings of the Eighth Pacific Congress 4, 438–452. Miranda, F. (1959) Estudios acerca de la vegetación. In: Beltran, E. (ed.) Los recursos naturales del sureste y su aprovechamiento. D.F. Instituto Mexicano de Recursos Naturales Renovables, Mexico, pp. 215–217. Moretti, A. (1990) Karyotypic data on North and Central American Zamiaceae (Cycadales) and their phylogenetic implications. American Journal of Botany 77, 1016–1029. Moretti, A. and Sabato, S. (1984) Karyotype evolution by centromeric fission in Zamia (Cycadales). Plant Systematics and Evolution 146, 215–223.

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Moretti, A., Sabato, S. and Vázquez Torres, M. (1980) The distribution of Ceratozamia Brongn (Zamiaceae). Delpinoa 20, 13–21. Moretti, A., Caputo, P., Cozzolino, S., De Luca, P., Gaudio, L., Siniscalco Gigliano, G. and Stevenson, D.W. (1993) A phylogenetic analysis of Dioon (Zamiaceae). American Journal of Botany 80, 204–214. Norstog, K.J. and Nicholls, T.J. (1997) The Biology of the Cycads. Cornell University Press, Ithaca, New York, 363 pp. Palacios, C.R. and Rzedowski, J. (1993) Estudio palinológico de las floras fósiles del Mioceno inferior y principios del Mioceno Medio de la región de Pichucalco, Chiapas, México. Acta Botánica de México 24, 1–96. Pérez-Farrera, M.A. (1999) Dinámica poblacional de Ceratozamia matudae en la Reserva de la Biosfera el Triunfo, Chiapas, México. Tesis de Maestria, El Colegio de la Frontera Sur. San Cristóbal de Las Casas, Chiapas, Mexico. Pérez-Farrera, M.A., Vovides, A.P. and Iglesias, C.G. (1999) A new species of Ceratozamia (Zamiaceae, Cycadales) from Chiapas, Mexico. Novon 9, 410–413. [Ceratozamia alvarezii.] Pérez-Farrera, M.A., Vovides, A.P. and Iglesias, C.G. (2001) A new species of Ceratozamia (Zamiaceae) from Chiapas, Mexico. Botanical Journal of the Linnean Society 137, 77–80. [Ceratozamia zoquorum.] Potter, D., Luby, J.J. and Harrison, R.E. (2000) Phylogenetic relationships among species of Fragaria (Rosaceae) inferred from non-coding nuclear and chloroplast DNA sequences. Systematic Botany 25, 337–348. Rzedowski, J. and Palacios, C. (1977) El bosque de Engelhardtia (Oreomunnea) mexicana en la región de la Chinantla (Oaxaca, México). Una reliquia del Cenozoico. Boletín de la Sociedad Botánica de México 36, 93–123. Sabato, S. and De Luca, P. (1985) Evolutionary trends in Dion [sic] (Zamiaceae). American Journal of Botany 72, 1353–1363. Schilling, E.E., Linder, C.R., Noyes, R.D. and Rieseberg, L.H. (1998) Phylogenetic relationships in Helianthus (Asteraceae) based on nuclear ribosomal DNA transcribed spacer region sequence data. Systematic Botany 23, 177–187. Stevenson, D.W., Sabato, S. and Vázquez Torres, M. (1986) A new species of Ceratozamia (Zamiaceae) from Veracruz, Mexico with comments on species relationships, habitats, and vegetative morphology in Ceratozamia. Brittonia 38, 17–26. [Ceratozamia euryphyllidia.] Thiselton-Dyer, W.T. (1882–1886) Cycadaceae. Biologia Centrali-Americana 3, 190–195. Toledo, V.M. (1982) Pleistocene changes of vegetation in tropical Mexico. In: Prance, G.T. (ed.) Biological Diversification in the Tropics. Proceedings of the Fifth International Symposium of the Association for Tropical Biology. Columbia University Press, New York, pp. 93–111. Toledo, V.M. (1988) La diversidad biológica de México. Ciencia y Desarrollo 14, 17–30. Vovides, A.P. (1983) Systematic studies on the Mexican Zamiaceae. I. Chromosome numbers and karyotypes. American Journal of Botany 70, 1002–1006. Vovides, A.P. (1985) Systematic studies on the Mexican Zamiaceae II. Additional notes on Ceratozamia kuesteriana from Tamaulipas, Mexico. Brittonia 37, 226–231. Vovides, A.P. and Olivares, M. (1996) Karyotype polymorphism in the cycad Zamia loddigesii (Zamiaceae) of the Yucatan Peninsula, Mexico. Botanical Journal of the Linnean Society 120, 77–83. Vovides, A.P., Rees, J.D. and Vázquez Torres, M. (1983) Familia Zamiaceae. In: Sosa, V. and Gomez-Pompa, A. (eds) Flora de Veracruz. INIREB, Xalapa, Veracruz, Mexico, Fascículo 26.

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Vovides, A.P., Pérez-Farrera, M.A. and Iglesias, C.G. (2001) Another new species of Ceratozamia (Zamiaceae) from Chiapas, Mexico. Botanical Journal of the Linnean Society 137, 81–85. [Ceratozamia mirandae.] Wendt, T. (1987) Las selvas de Uxpanapa, Veracruz-Oaxaca, México: evidencia de refugios florísticos Cenozoicos. Anales del Instituto de Biología UNAM – Serie botánica 58, 29–54.

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A Morphometric Analysis of the Ceratozamia norstogii Complex (Zamiaceae)

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Miguel A. Pérez-Farrera,1 Andrew P. Vovides,2 Luis Hernández-Sandoval,3 Dolores González2 and Mahinda Martínez3 1Escuela

de Biología, Universidad de Ciencias y Artes de Chiapas (UNICACH), Tuxtla Gutiérrez, Chiapas, Mexico; 2Instituto de Ecología A.C., Xalapa, Veracruz, Mexico; 3Facultad de Biología, Universidad Autónoma de Querétaro, Centro Universitario, Querétaro, Mexico

Abstract The three species forming the Ceratozamia norstogii complex (C. alvarezii, C. mirandae and C. norstogii) are found in adjacent areas of the Sierra Madre de Chiapas in Mexico. Taxonomic limits within this complex have not yet been fully defined, but are investigated in this project. Twenty morphological variables from 90 individuals from three populations have been analysed using ANOVA and discriminant analysis. The results reveal a clear number of differences for these variables among the three species.

Introduction The taxonomy and distribution of the genus Ceratozamia Brongniart (Zamiaceae) is little known due to various problems: (i) there is no clear delimitation of some of the species, principally in the C. mexicana Brongniart, C. latifolia Miquel and C. miqueliana H. Wendland complexes or species groups; (ii) many of the type specimens on which the original descriptions were based have been lost or destroyed and the descriptions themselves are often based on sterile or juvenile material and ©CAB International 2004. Cycad Classification: Concepts and Recommendations (eds T. Walters and R. Osborne)

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on plants cultivated in botanic gardens (Vovides et al., 1983); (iii) species complexes are found throughout the distribution of the genus (Moretti et al., 1980); and (iv) some neotypifications appear to be doubtful (e.g. C. robusta Miquel) (Stevenson and Sabato, 1986). Ceratozamia norstogii D.W. Stevenson was described in 1982 as having the distinctive characteristics of channelled leaflets and a straight rachis, but the type specimen assigned (C.A. Purpus 6) has a twisted rachis (Stevenson, 1982). On the basis of herbarium vouchers, Stevenson et al. (1986) assigned some populations and forms with channelled leaflets and a straight rachis to C. norstogii under the assumption that this species was polymorphic. However, it now appears that C. norstogii is not polymorphic and we believe that this species belongs in a group with two recently described related species (Pérez-Farrera et al., 1999, 2001; Vovides et al., 2001). Unfortunately the range of morphological variation within this complex and others of the genus is not yet fully understood. This lack of information, coupled with the difficulty in obtaining morphological characters from fertile specimens, has contributed to taxonomic confusion in the genus. In this study we examined the morphological variation within the Ceratozamia norstogii complex using multivariate statistical techniques to test the morphological differentiation between C. alvarezii Pérez-Farrera, Vovides & Iglesias, C. mirandae Vovides, Pérez-Farrera & Iglesias and C. norstogii.

Study Area The study was done in the La Sepultura Biosphere Reserve on the western side of the Sierra Madre de Chiapas in Mexico. This physiographical region runs parallel to the Pacific coastal plain, from the extreme south of the Isthmus of Tehuantepec, across Chiapas and reaches as far as Guatemala. It ranges in altitude from 1000 m in the north to 4000 m (Mount Tacaná) on the Guatemalan border with Chiapas (Müllerried, 1957). The predominant vegetational types are deciduous tropical forest, oak forest, conifer forest, cloud forest and evergreen tropical rainforest (Rzedowski, 1978). According to De La Rosa et al. (1989) the major part of the area is formed by Palaeozoic igneous rocks (granites and granidiorites) and Precambrian rocks (pink granitic gneiss and granidiorite gneiss). Specific metamorphic substrate is present only on slopes in some areas (Hernández-Yañez, 1995). Most populations within the Ceratozamia norstogii complex are found in oak and cloud forests or intermediate zones of these two ecosystems. The cycads grow in poor clay soils on steep slopes within an altitude range of 800–1200 m. The majority of populations are subjected to periodic fires at least once a year. All species within this complex are characterized by erect male and female cones, and plain or channelled leaflets.

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Materials and Methods Three natural populations were analysed (Fig. 10.1) using 30 individuals each of Ceratozamia norstogii, C. alvarezii and C. mirandae (Figs 10.2–10.4) and recording data from 14 vegetative and six reproductive morphological variables (Table 10.1). Measurements were done using a flexible tape measure (3 m) and a precision digital vernier (0.01 mm resolution). Data were captured and electronically stored. Analysis of variance (ANOVA) tests were done using JMP version 3.2 statistical software (SAS Institute, Cary, North Carolina, USA) and discriminant analyses (McCune and Mefford, 1997) with Statgraphics version 2.0 software (Manugistics, Rockville, Maryland, USA).

Results Univariate analysis Tables 10.2 and 10.3 summarize the ANOVA results. Species characters do not overlap, with the exception of intervein distance, leaf length, microsporophyll

Fig. 10.1. Location in Mexico of populations of the Ceratozamia norstogii complex sampled in this study.

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Fig. 10.2. Species in the Ceratozamia norstogii complex: C. alvarezii Pérez-Farrera, Vovides & Iglesias.

Fig. 10.3. Species in the Ceratozamia norstogii complex: C. norstogii D.W. Stevenson.

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Fig. 10.4. Species in the Ceratozamia norstogii complex: C. mirandae Vovides, Pérez-Farrera & Iglesias. Table 10.1. List of morphometric variables used in the analysis of populations in the Ceratozamia norstogii complex. No.

Abbreviation

Character and measurement units (parentheses)

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20

LARGTR PERMTR NHOJA LARHOJ ANCHHOJ LARESPPEC LARGOPEC PERIMPEC LARGORAQ NFOLIOL LARGOFOL ANCHOFOL NVENAS DISTVEN LARGOMICRO ANCHOMICRO ANCHOMEGAS LARGOMEGAS DIAMSEMI LARGSEMI

Trunk length (cm) Trunk perimeter (cm) Number of leaves per trunk Leaf length (cm) Leaf width (cm) Petiole prickle length (mm) Petiole length (cm) Petiole perimeter (cm) Rachis length (cm) Number of leaflets per leaf Leaflet length (cm) Leaflet width (cm) Number of veins per leaflet Intervein distance (mm) Microsporophyll length (mm) Microsporophyll width (mm) Megasporophyll distal face width (mm) Megasporophyll distal face length (mm) Seed diameter (mm) Seed length (mm)

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Table 10.2. Mean values and standard deviations (SD) for the ratios used in the analysis of populations in the Ceratozamia norstogii complex (C. alvarezii PérezFarrera, Vovides & Iglesias, C. mirandae Vovides, Pérez-Farrera & Iglesias and C. norstogii D.W. Stevenson). Species/character LARGTR PERMTR NHOJA LARHOJ ANCHHOJ LARESPPEC LARGOPEC PERIMPEC LARGORAQ NFOLIOL LARGOFOL ANCHOFOL NVENAS DISTVEN LARGOMICRO ANCHOMICRO ANCHOMEGAS LARGOMEGAS DIAMSEMI LARGSEMI

C. alvarezii

SD

C. mirandae

SD

C. norstogii

SD

20.55 42.68 8.91 79.64 45.36 0.34 20.59 2.45 47.00 45.00 22.98 0.65 7.55 0.08 14.90 6.99 35.54 15.54 16.0 22.36

± 7.67 ± 6.64 ± 3.99 ± 15.5 ± 6.61 ± 0.09 ± 8.52 ± 0.57 ± 10.2 ± 9.97 ± 3.28 ± 0.11 ± 0.93 ± 0.03 ± 0.83 ± 0.76 ± 5.32 ± 2.26 ± 1.34 ± 2.73

58.23 71.30 13.33 151.87 69.15 0.46 39.92 3.42 104.55 65.67 36.07 0.98 8.67 0.10 14.55 7.17 52.41 12.14 16.58 27.45

± 18.5 ± 7.28 ± 4.74 ± 17.9 ± 8.69 ± 0.07 ± 9.97 ± 0.63 ± 61.7 ± 9.05 ± 4.80 ± 0.12 ± 1.56 ± 0.02 ± 0.99 ± 0.70 ± 3.82 ± 1.97 ± 0.97 ± 1.12

32.07 58.31 4.83 98.60 94.24 0.40 18.18 2.61 62.11 51.17 35.55 0.41 5.31 0.09 14.32 7.74 46.82 9.88 17.55 27.13

± 21.76 ± 6.79 ± 0.97 ± 17.35 ± 135.3 ± 0.51 ± 6.93 ± 0.56 ± 9.90 ± 9.32 ± 7.65 ± 0.07 ± 0.71 ± 0.01 ± 0.99 ± 0.80 ± 1.64 ± 1.61 ± 1.37 ± 1.30

length, petiole length and petiole prickle length. The rest of the variables analysed were all highly significant (P < 0.0001).

Discriminant analyses Figure 10.5 shows the scatter diagram of data derived from discriminant function analysis. The three species separate ordinately in bidimensional space and do not present any overlapping between groups. Of the 20 variables included in the standardized discrete canonical function, the six variables with the highest values in factor 1 were trunk perimeter, petiole length, leaflet width, vein number, microsporophyll length and megasporophyll width. In factor 2, the highest variables were trunk perimeter, leaf length, petiole length, leaflet length and width. The first canonic variable showed that 70% of the variation is largely due to vegetative morphology. The positive correlations (Table 10.4) of all the variables show differences between species. The Wilks lambda test was highly significant (P < 0.0001) for the two factors (Table 10.5) thus showing that all the species were classified correctly.

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Table 10.3. Summary of analysis of variance of the 20 morphometric characters used in the analysis of populations in the Ceratozamia norstogii complex (R2 = correlation coefficient, F = F value, P = probability). Character

R2

F

LARGTR PERMTR NHOJA LARHOJ ANCHHOJ LARESPPEC LARGOPEC PERIMPEC LARGORAQ NFOLIOL LARGOFOL ANCHOFOL NVENAS DISTVEN LARGOMICRO ANCHOMICRO ANCHOMEGAS LARGOMEGAS DIAMSEMI LARGSEMI

0.47 0.71 0.52 0.76 0.06 0.02 0.06 0.37 0.30 0.45 0.49 0.87 0.56 0.01 0.61 0.09 0.76 0.62 0.25 0.61

40.04 108.18 43.41 138.79 2.81 1.02 3.02 25.63 19.04 36.61 42.92 241.20 55.90 0.77 1.36 4.83 145.52 71.80 15.27 68.8

■

C. alvarezii × C. mirandae

●

P < < < <

< < < < < <

< < < <

0.0001 0.0001 0.0001 0.0001 0.06 0.34 0.05 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.46 0.25 0.01 0.0001 0.0001 0.0001 0.0001

C. norstogii + centroids

5 3 Discriminant Function 2

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–3

0 3 Discriminant Function 1

6

9

Fig. 10.5. Scatter plot of scores derived from the functions produced by stepwise discriminant analysis of 20 morphometric ratios from populations in the Ceratozamia norstogii complex.

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Table 10.4. Standardized discriminate function values for each of two factors used in the analysis of populations in the Ceratozamia norstogii complex. Character LARGTR PERMTR NHOJA LARHOJ ANCHHOJ LARESPPEC LARGOPEC PERIMPEC LARGORAQ NFOLIOL LARGOFOL ANCHOFOL NVENAS DISTVEN LARGOMICRO ANCHOMICRO ANCHOMEGAS LARGOMEGAS DIAMSEMI LARGSEMI EIGENVALUE CANONICAL CORRELATION AMONG-GROUP VARIANCE

Factor 1

Factor 2

0.1027 0.3713 0.3498 – 0.0975 0.0106 – 0.0079 0.3594 – 0.1413 – 0.0492 0.0191 – 0.0914 0.9860 – 0.3850 – 0.0180 0.2383 – 0.0865 0.5815 – 0.2986 – 0.1918 0.1804 15.6008 0.9694 70.78%

– 0.1943 0.3334 – 0.1579 0.3914 0.0358 – 0.0098 – 0.3624 0.1011 – 0.0142 – 0.0452 0.5259 – 0.3467 – 0.1930 0.0047 – 0.2232 – 0.0007 0.2458 – 0.2986 0.0766 0.2074 6.4400 0.9304 29.22%

Table 10.5. Summary of the discriminant analysis results from the analysis of populations in the Ceratozamia norstogii complex (χ2 = chi-squared factor, DF = degrees of freedom, P = probability). Functions derived Factor 1 Factor 2

Wilks lambda

χ2

DF

P

0.00809 0.1344

276.94 115.39

40 19

0.0000 0.0000

Discussion and Conclusions Amongst the three species in the complex, Ceratozamia alvarezii has the longest and narrowest microsporophylls, and the shortest and narrowest leaves. By contrast, C. mirandae has the longest trunks with the highest circumference and leaves having the longest petiole with the largest circumference. The discrete analysis

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clearly showed the morphological differences between the species in the C. norstogii complex. However, some results from the univariate analysis showed some overlapping between species. The analysis provides evidence that delimits the three species analysed. In the present study, the measurements of leaflets, leaves and sporophylls were particularly well represented and it is not surprising that the differences between these characters emerge as important discriminators between the species. A long interpopulational distance could probably be indicative of a long isolation period if a constant rate of evolution and allopatric speciation is assumed (Grant, 1985). This hypothesis is based on Wright’s (1943) theory of ‘isolation by distance’. According to this hypothesis, populations within a taxon with a continuous distribution pattern will show genetic differentiation proportional to the distance between populations. It is interesting to observe that, particularly in this complex, all the species share the same habitat (oak forest) and that distances between species and populations are relatively close, but morphologically the plants are distinct. Isolation barriers other than distance have had a part to play here, namely high mountain ranges and deep canyons where vegetation types change drastically over short distances. However, preliminary DNA sequencing data show a homogeneity of characters in the nuclear ribosomal ITS and chloroplast trnL-F non-coding region (González and Vovides, 2002), which presumes geologically recent isolation events, perhaps the Cenozoic climatic changes prior to and during the Pleistocene that gave rise to the floristic refuges in southern Mexico (Toledo, 1982; Burnham and Graham, 1999).

Taxonomic Key The following vegetative key may be used to separate the species in the Ceratozamia norstogii complex: 1. Spirally twisted rachis ………………………….…………....... C. norstogii 1. Straight rachis 2. Leaflets channelled or partly channelled, 8–12 mm wide ... C. mirandae 2. Leaflets not channelled, 4–9 mm wide ………………….... C. alvarezii

Acknowledgements The authors thank Montgomery Botanical Center (Miami, Florida, USA) for a student grant ‘Taxonomic revision of the genus Ceratozamia Brongn. (Zamiaceae) in the neotropics’ awarded to the first author to complete PhD studies, and CONACYT (Grant Number 29379N) for the project ‘Systematics, distribution and conservation of Mexican cycads’. The principal author thanks Rigoberto Hernández Jonapa, Jesus De La Cruz Rodriguez, Emerit López Melendez, Nayeli Martínez Melendez and Ruben Martínez Camilo for their help in the field work.

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References Burnham, R.J. and Graham, A. (1999) The history of neotropical vegetation: new developments and status. Annals of the Missouri Botanical Garden 86, 546–589. De La Rosa, J.L.A., Eboli, M. and Dávila, S.M. (1989) Geología del estado de Chiapas. Subdirección Construcción, Unidad de Estudios de Ingeniería Civil, Subjefatura de Estudios Geológicos, Departamento de Ecología, CFE, Mexico, 192 pp. González, D. and Vovides, A.P. (2002) Low intralineage divergence in the genus Ceratozamia Brongn. (Zamiaceae) detected with nuclear ribosomal DNA ITS and chloroplast DNA trnL-F non-coding region. Systematic Botany 27, 654–661. Grant, V. (1985) The Evolution Process. A Critical Review of Evolutionary Theory. Columbia University Press, New York, 587 pp. Hernández-Yañez, A. (1995) Propuesta para establecer el área natural protegida (Reserva de la Biosfera) La Sepultura, en la porción oeste de la Sierra Madre de Chiapas, México. MSc thesis, Facultad de Biología, Universidad Veracruzana, Xalapa, Veracruz, Mexico. McCune, B. and Mefford, J. (1997) Multivariate Analysis of Ecology Data.Version 3.17. MJM Software, Gleneden Beach, Oregon, USA, 126 pp. Moretti, A., Sabato, S. and Vázquez Torres, M. (1980) The distribution of Ceratozamia Brongn. (Zamiaceae). Delpinoa 21, 13–21. Müllerried, F.K.G. (1957) Geología de Chiapas. Gobierno Constitucional del Estado de Chiapas, Tuxtla Gutiérrez, Chiapas, Mexico, 180 pp. Pérez-Farrera, M.A., Vovides, A.P. and Iglesias, C.G. (1999) A new species of Ceratozamia (Zamiaceae, Cycadales) from Chiapas, Mexico. Novon 9, 410–413. Pérez-Farrera, M.A., Vovides, A.P. and Iglesias, C.G. (2001) The cycad Ceratozamia norstogii Stevenson (Zamiaceae) from southern Mexico: new information on distribution, habitat and vegetative morphology. Botanical Journal of the Linnean Society 137, 71–76. Rzedowski, J. (1978) La Vegetación de México. Edit. LIMUSA, D.F., Mexico, 432 pp. Stevenson, D.W. (1982) A new species of Ceratozamia (Zamiaceae) from Chiapas, Mexico. Brittonia 34, 181–184. [Ceratozamia norstogii.] Stevenson, D.W. and Sabato, S. (1986) Typification of names in Ceratozamia Brongn., Dioon Lindl., and Microcycas A.D.C. (Zamiaceae). Taxon 35, 578–584. Stevenson, D.W., Sabato, S. and Vázquez Torres, M. (1986) A new species of Ceratozamia (Zamiaceae) from Veracruz, Mexico with comments on species relationships, habitats, and vegetative morphology in Ceratozamia. Brittonia 38, 17–26. [Ceratozamia euryphyllidia.] Toledo, V.M. (1982) Pleistocene changes of vegetation in tropical Mexico. In: Prance, G.T. (ed.) Biological Diversification in the Tropics. Proceedings of the Fifth International Symposium of the Association for Tropical Biology. Columbia University Press, New York, pp. 93–111. Vovides, A.P., Rees, J.D. and Vázquez Torres, M. (1983) Zamiaceae. In: Sosa, V. and Gomez-Pompa, A. (eds) Flora de Veracruz. INIREB, Xalapa, Veracruz, Mexico, Fascículo 26. Vovides, A.P., Pérez-Farrera, M.A. and Iglesias, C.G. (2001) Another new species of Ceratozamia (Zamiaceae) from Chiapas, Mexico. Botanical Journal of the Linnean Society 137, 81–85. [Ceratozamia mirandae.] Wright, S. (1943) Isolation by distance. Genetics 28, 114–138.

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Hypotheses on the Relationship between Biogeography and Speciation in Dioon (Zamiaceae)

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Timothy J. Gregory1 and Jeffrey Chemnick2 1Montgomery

Botanical Center, Miami, Florida, USA; 2Ganna Walska Lotusland, Santa Barbara, California, USA

Abstract Hypotheses are presented on the relationships between palaeoclimatic conditions during the late Pleistocene and Holocene, and the current biogeography of cycads in the genus Dioon. A proposal is made that Dioon populations have migrated up and down in elevation, and north and south, with the warming and cooling climatic cycles corresponding to glaciations. This suggests that since the end of the Wisconsin glaciation Dioon populations have moved upward in elevation in southern Mexico with shifts in their preferred transition zone habitat. This migration has sometimes resulted in disjunction and rapid speciation within river canyon systems. Mechanisms for these activities are discussed. The chapter culminates with the proposal that the extant Dioon species are the result of rapid evolution in a dynamic and viable group of plants instead of the classical concept that they are slowly evolving relicts.

Introduction The pioneering collaborative work between staff of the Orto Botanico in Naples and the Instituto de Ecología in Veracruz greatly expanded the understanding of the cycad genus Dioon Lindley. Six new species were described (Dioon califanoi De Luca & Sabato, D. caputoi De Luca, Sabato & Vázquez Torres, D. rzedowskii De Luca, A. Moretti, Sabato & Vázquez Torres, D. holmgrenii De Luca, Sabato & Vázquez Torres, D. merolae De Luca, Sabato & Vázquez Torres and D. tomasellii De Luca, Sabato & Vázquez Torres) and two of the original three species (D. edule Lindley and D. purpusii Rose) were redefined in a modern context (De Luca et al., ©CAB International 2004. Cycad Classification: Concepts and Recommendations (eds T. Walters and R. Osborne)

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1978, 1980a,b, 1981a,b, 1982, 1984; De Luca and Sabato, 1979). The collaboration culminated in a summary of the characteristics of the genus and a wellfounded hypothesis on evolutionary trends in Dioon (Sabato and De Luca, 1985) that has served as the foundation for our recent work. Since 1995 we have been engaged in a study of the cycad populations in southern Mexico. Our objectives have been to document populations of the known species and find new populations; to study their biology, phenology and morphology; and to attempt to understand the biogeographic distribution and history of speciation of each population. The results of our work to date are: (i) the descriptions of three new species (Chemnick and Gregory, 1995; Chemnick et al., 1997b; Gregory et al., 2003); (ii) a proposal to raise a previously described subspecies of D. tomasellii, to specific rank; and (iii) a dramatic range extension for D. merolae (Chemnick et al., 1997a). We have also acquired considerable information on the biogeography of each of the Dioon species and their populations. These populations are confined to very restricted habitats, generally in the transition zones between major forest types. Each species is composed of two or more well-defined populations that share specific morphological characteristics. Several key characteristics of Dioon, such as distribution within steep rocky habitats, separate sexes, large brightly coloured seeds, and beetle pollination, raise interesting questions about how these populations are established and distributed. Our attempts to answer these questions led us to the literature concerning the movement of plant species during periods of climatic change, especially those changes since the last glaciation. The climate changes associated with the retreat of the continental glaciers have caused major movements of individual plant species to new habitats (Sauer, 1988). The purpose of this chapter is to summarize our field observations, correlate them with what is known about the climatic changes that have occurred in the last 35,000 years and propose a hypothesis for the mechanism by which speciation occurs within the genus Dioon.

Field Observations Our observations in the field have confirmed and expanded those of Sabato and De Luca (1985). Dioon populations are geographically discrete and frequently confined to steep rocky slopes or cliffs in the transition zone between major forest types. Dioon spinulosum Dyer occurs on kaarst hummocks in lowland tropical forest at 70–120 m. Dioon rzedowskii is found in the transition zone between lowland tropical rainforest and premontane rainforest at 100–500 m. Dioon holmgrenii and the populations of an undetermined taxon that occur between D. holmgrenii and D. tomasellii on the Pacific coast are found at higher elevations, 900–1100 m, in the tropical dry forest, below the oak/pine forest. The remaining Dioon species are found primarily in the transition zone between thorn forest and oak/pine forest at 1400–2000 m. The restriction to rocky transition zones suggests that Dioon species are adapted to exist in habitats where other species are less able to compete. These elevation/habitat associations are sufficiently consistent that we

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have used them to predict the existence of populations from topographic maps and later confirm their existence in the field. We have also observed that only a small proportion of the potentially available habitat is utilized. The patchy distributions may be related to biological and ecological constraints on the establishment of new Dioon populations, as discussed below. Most species comprise two to eight homomorphic populations and the individual species or groups of species tend to be restricted to particular river drainages. Those species with numerous populations (e.g. D. edule and D. tomasellii) are currently treated as complexes of populations with inadequately analysed variation. Relatively subtle leaf morphology is the defining characteristic of Dioon species. Unfortunately, the intraspecific variation in leaf and seedling morphology and reproductive characters of Dioon are not adequately treated in most species descriptions. Within each population approximately 10% of the adult plants exhibit a leaf morphology at variance with the description. Such variation is even observed between flushes of leaves on the same plant and these atypical individuals or cohorts of leaves are often more characteristic of other species, especially those most closely distributed geographically. The suite of characters exhibited by the vast majority of plants is, however, consistent within the population and the species, although D. holmgrenii is a notable exception. The variation in leaf morphology present within populations of D. holmgrenii is extreme and leaves that could be mistaken for those of D. merolae and D. tomasellii occur on approximately 40% of the plants. The subtle, yet discrete, variation defining each Dioon species, the restricted habitat occupied and the association of species with particular river valleys and canyons have led us to consider possible mechanisms of speciation within the genus. Dioon species possess large seeds that make their long-range dispersal problematic. It is difficult to hypothesize potential medium- or long-range dispersal agents among the extant animals occurring in Mexico. In Dioon populations we frequently observe that the seed sarcotesta are eaten by rodents, as evidenced by the diagnostic teeth marks left in the dried sarcotesta and on the surface of the sclerotesta. Occasionally the megagametophyte is eaten but the sarcotesta appears to be the primary food element. Sometimes caches of cleaned seeds are found near or at the base of the mother plant and individual seeds are found up to 20 m away. However, we also frequently observe that the majority of seeds from a cone are cleaned by rodents and yet remain in the crown of the parent plant. The relationship between dispersal and recruitment into the population is not known for Dioon but we observe that the vast majority of seed that germinates near the parent plant gives seedlings that die within the first year or two. The attrition of germinated seed and young seedlings is apparently due to desiccation. We have observed that many of the seedlings that survive the first 2 years after germination are those buried deeply in the ground. This suggests that successful recruitment could be dependent on the rodents’ deep internment caching of seed that then germinates before consumption. The question remains as to whether Dioon seed is ever dispersed over distances that would allow establishment of new populations. Dioon sarcotesta are coloured yellow to orange which suggests that they might be attractive to a diurnal animal that can recognize colour. In many

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species the megastrobilus dehisces when the cone is held above the crown of leaves. In these cases the female cone dehisces with the yellow sarcotesta exposed skywards and visible for hundreds of metres. This raises the possibility that large diurnal birds might be attracted and thus serve as longer-range dispersal agents, though no such association has been reported for Dioon to date. Currently the most likely local extant Mexican birds potentially capable of carrying such large seeds to new suitable habitats are the common raven (Corvus corvax) and the military macaw (Ara militaris). We have observed both species of bird perched in Dioon plants in Oaxaca but have not observed any direct interaction with cones or seed. Two possible mechanisms of population establishment present themselves from our observations. The first is the possibility that large diurnal birds, or other dispersal agents, transport seeds to new cliff habitats, followed by a colonization by the pollinator, thus to establish new viable populations. The need for concomitant dispersal of individual plants of both sexes and the pollinating insect, and the paucity of different populations within each species relative to the vast amount of suitable cliff habitat, make this mechanism unlikely, but not impossible. Furthermore, such a colonization mechanism would generate a very significant genetic bottleneck, because the founding genes would come from as few as two individuals. The genetic repertoire of the new population would be limited to that of the two founding parents. If the founding plants possessed characteristics that are outside the norm in the parental population then the new population would be correspondingly different. The possibility of genetic exchange back with the parent population is extremely limited by the same impediments to the founding of a new population. The genetic bottleneck could lead to rapid speciation by the founder effect analogous to speciation that sometimes occurs on islands. The second potential mechanism for generating new Dioon populations is through slow local dispersal by rodents resulting in the eventual schism of an existing population over time into new sister populations. This mechanism avoids the problem of concomitant colonization by plants of both sexes and the pollinator but requires a changing environment to create new contiguous habitats into which the population can colonize by fission. Such a mechanism also lacks the genetic bottleneck that could drive rapid speciation. We hypothesize that both processes are important. The fission process could be an important mechanism for generating new populations within a species and the colonization mechanism could be important for generating new species through a founder effect. Very little is known about the pollination mechanism for Dioon species. Insects may be obligate pollinators, as demonstrated in other members of the Zamiaceae. We have collected weevils (Curculionidae), having an orange pronotum and black elytra, from fresh and old male cones of several Dioon species throughout Oaxaca. Typically, these weevils are found covered with pollen and we have recovered the remains of similar weevils from fertilized female cones. Larvae have been recovered from dried male cones that are up to 1 year old but not from older cones. These observations are consistent with the proposed life history of weevils as a cycad pollinator (Norstog et al., 1986). Superficially, there appears to be a single species that pollinates D. califanoi, D. purpusii, D. merolae and

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D. argenteum T.J. Gregory, Chemnick, Salas-Morales & Vovides, but the taxonomic status of the beetles is currently under investigation. Since it appears that there is no obvious gene flow between Dioon species, and possibly not even between populations of the same species, it is reasonable to conclude that the pollinators are unable to range beyond a particular population. Some fortuitous information arose from an inadvertent experiment carried out by the people in a village near the D. argenteum habitat. Several decades ago three male and one female D. argenteum plants were transplanted to the churchyard in the village. The wild population from which the plants originated is less than 5 km from the village. On two occasions we observed that the old male cones showed no signs of insect occupation (e.g. exit holes or excavation of the microsporophylls) and there were no signs of fertile seed around the female plant. The villagers also confirmed that they had never observed viable seed or seedlings produced by the female plant. The anecdotal evidence suggests that the pollinator was not able to colonize this artificial pioneer population over at least two decades and that the range of the pollinator is quite restricted. This confirms that any new Dioon population must have a concomitant colonization by the pollinator to be viable and that the range of the pollinator is so restricted that this colonization is a rare event. We have directly observed more than 35 Dioon populations in southern Mexico. Several of those populations that have not been directly impacted by human activity are relatively large, consist of hundreds to thousands of individuals in all life stages, and exhibit excellent recruitment. However, many of the populations are small (20–100 individuals). Some of these small populations are apparently viable with some recruitment, but others appear to be senescent. We define senescence as a population containing mostly older mature adults that, despite regular coning and seed production, exhibits very little or no recruitment of seedlings. Such senescent populations are usually located on cliff faces or talus slopes in the tropical deciduous forest at sites where there is no oak/pine forest above them. These plants appear stressed by drought and generally inhospitable conditions. We propose that these Dioon populations are dying out naturally because the habitat at their current location has changed and moved to higher elevations with the drying and warming of the climate during the Holocene. No higher topography exists adjacent to them to permit their upward migration with their preferred transition zone habitat. An alternative hypothesis is that these populations are new colonies in various phases of relative success or failure. However, we have yet to discover similar populations at higher elevations in the oak/pine forest, above the preferred Dioon habitat. Rather, the most robust populations occur at sites where there is cliff habitat and oak/pine forest above. Thus we believe that we are observing Dioon populations in various phases of maturity to senescence possibly caused by movement of the preferred habitat to higher elevations over time. Alternatively, the extant populations of Dioon in Mexico might merely be scattered remnants that have persisted for millennia at the same sites through several glacial climate cycles, somehow withstanding generally inhospitable conditions under which they do not reproduce even in horticulture.

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Palaeoclimatic Implications Fossils attributable to Dioon have been found in Alaska and California (Wolfe, 1972; Axelrod, 1975). These fossils are of Eocene and Miocene age, respectively, and suggest that the ancestors of the current Dioon species were present in Mexico at least 10–15 million years ago. The fossils demonstrate that the genus was able to expand into northern North America during a very warm period. The extant Dioon species are confined to Mexico and Honduras and have been assigned to three subgeneric groupings (Sabato and De Luca, 1985). Reproductive characters are important for distinguishing between these groups, but within each group the species are differentiated primarily by leaf morphology. The species within the groupings appear to be closely related and to have only recently evolved into new taxa. We regard a Dioon species as a group of populations with consistent morphological characters sufficient to distinguish it as an entity from its closest congeners. Implicit in this species concept is the assumption that the closest congeners of a particular species are also some of its closest geographical neighbours. In the field we find that groups of related species are often confined to river valleys or drainage systems. The mountains or deserts surrounding the river systems lack suitable Dioon habitats and provide significant barriers to the migration of Dioon populations. Their patchy distribution suggests that populations of Dioon are expanding their ranges upward and becoming increasingly isolated in the river valleys that they occupy today. The current distribution of the various taxa conforms to this model and thus we are seeking possible mechanisms that could drive this migration and speciation. Sauer (1988) summarized data on plant migrations in the Holocene that may be useful in explaining the current distributions of Dioon species. Palynological data, as well as data from wood rat (Neotoma) middens from East Africa, Japan, Colombia, northern Europe and south-eastern and south-western USA, indicate that, following the collapse of the Wisconsin ice sheet 12,000 years ago, there were dramatic movements of entire forests northward and to higher elevations. The data indicate that individual tree species moved independently of each other and not as a forest biome per se. It also appears from the pollen data that some species advanced their ranges at mean rates of 250 m/year. Some species in the northern hemisphere exhibited a general northward migration and colonization of newly available habitat while species in tropical latitudes (e.g. the Colombian Andes and the high mountains of East Africa) clearly moved upward in elevation by 1200–1500 m. Neither palynological nor Neotoma midden data from Mexico are currently available but McDonald (1993) has assembled biogeographical data on alpine plants and Toledo (1982) has assembled a variety of biogeographical and oceanographical data that support a similar post-glacial plant migration. The data from alpine plants in central Mexico indicate an upward movement of the treeline in excess of 1000 m during the past 10,000 years. During the peak glaciation, approximately 40,000 years ago, the treeline in central Mexico descended to 2500 m, in contrast to the current elevation of 3500 m. This created a sub-alpine corridor extending from the southern Rocky Mountains to

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the transverse Neovolcanic belt in central Mexico. This cycle appears to repeat with every glaciation cycle. Toledo (1982) has been cited by several authors for his delineation of Pleistocene refugia in southern Mexico, though this aspect is only a minor component of his work. The majority of his data are from palaeoclimatic analysis of sediment cores from the Gulf of Mexico and geomorphological studies of mountain glaciers in central Mexico. From these data, the pattern of warm/wet and cool/dry climate cycles over the past 40,000 years has been discerned at the latitude of the central Caribbean. This pattern shows, not unexpectedly, that the mean temperature at sea level during the last ice age was 6–7°C lower than it is now and has steadily increased to the present. Toledo (1982) then combined the temperature data with biogeographical data from the lowland forests on the gulf coast of Mexico to recreate the history of the gulf coastal vegetation during and since the glacial period. He suggested that there was no rainforest on the gulf plain of Veracruz during the glaciation. Instead there was oak/pine forest at sea level. The current rainforest elements have been migrating northward from refugia in Chiapas and Guatamala for 12,000 years. This provides an explanation for the relatively low species diversity and the presence of oak and pine forest remnants in the gulf coastal rainforest. During the same time, the alpine, cloud, oak/pine and tropical deciduous forests may have migrated to higher elevations at the same latitude and to higher latitudes in the north. As these forest biomes moved northward and upward, the transition zone habitats of the Dioon taxa moved in concert (i.e. to 1500 m at present in southern Mexico). As the habitats moved, the attendant populations presumably migrated with them up the river valleys, at an average rate of approximately 12 cm in elevation per year. Previous authors (Sabato and De Luca, 1985; Moretti et al., 1993) have attributed the current biogeography of Dioon to events that occurred throughout the Cenozoic. We agree that the history of the genus has certainly been shaped by the events of the last 60 million years but also believe that the available data suggest that the events of the most recent few hundred thousand years have much more relevance to the current distribution of Dioon in Mexico. Since the early Pleistocene there have been as many as 20 ice age cycles (Gould, 2001). Each of these cycles has caused the same dramatic climatic changes in North America and Mexico that Toledo and Sauer have described. As we suggest above, these climatic changes have probably had profound effects on the habitats of Dioon populations over thousands of years, not millions. The available molecular-biological (Moretti et al., 1993) and biochemical data (Siniscalco Gigliano, 1990) imply that many of the current Dioon species are very closely related. In the restriction fragment length polymorphism analysis of Moretti et al. (1993), the species of their D. edule clade are so closely related that many of the sub-clades are not statistically valid. Similarly, analyses of several biochemical characters failed to show any distinctions between Dioon species. The close genetic and biochemical relationship within the Dioon species could be interpreted either as an unusually slow rate of evolution in a relict group over a long period of time, or as rapid evolution and speciation in a short time frame. Moretti et al. (1993) and

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Sabato and De Luca (1985) considered both options but seemed to prefer the former. We favour the latter as we seem to be observing the relatively rapid evolution of populations into species over a period of thousands of years, not hundreds of thousands or millions. We also seem to be observing a dynamic response of a viable and successful group of plants to correspondingly rapid climatic and environmental changes.

Examples of Interpretations of Dioon Biogeography Using the Dynamic Habitat Hypothesis The positions and status of several Dioon populations today may be explained by a ‘dynamic habitat’ hypothesis. Three closely related species, D. califanoi, D. purpusii and D. argenteum, are found in nearly identical habitat but at different localities in the Rio Grande/Cuicatlan/Rio Salado canyon system in the upper reaches of the Rio Santo Domingo drainage of Oaxaca. These taxa support our species concept as each comprises two to five independent homomorphic populations but possesses a unique and diagnostic morphology. Some populations within a species can be differentiated from each other by very subtle characters such as size of leaves, carriage of leaves in the crown, number of prickles on the leaflets, or amount of wax on the leaflets. All populations are found on steep rocky slopes at altitudes of 1500–2000 m. Some populations are near the tops of ridges, some are midway down canyon walls, and still others are found along water courses. The common factor among them is their occurrence in the transition zone between tropical deciduous forest and oak/pine forest. The palaeoclimatic data from Toledo (1982) suggest that the floor of the canyon, at approximately 1100 m, was occupied by high-altitude pine or cloud forest 10,000–12,000 years ago. If this were the case, then these three distinct species, if they existed at that time, would likely have been forced to retreat and converge their ranges either in the lower part of the Rio Santo Domingo canyon or out on the coastal plane in a refugium. It seems unlikely that they could have maintained their genetic uniqueness under such conditions. Rather it seems more likely that these taxa have evolved recently from a common ancestor that colonized the canyon system in the Holocene following warming after the collapse of the Wisconsin ice sheet. We propose that the individual populations within each of these species have evolved by vicariance. We also propose that the species themselves could have evolved more rapidly from each other by the type of moderaterange dispersal discussed above in which a founder effect could have facilitated the establishment of a new cohort with slightly different morphology (i.e. more or less keeled leaves). If the putative common ancestor found refuge in the lower Rio Santo Domingo canyon during the ice age then the most distant populations of D. purpusii, D. califanoi and D. argenteum have moved into the smaller river valleys at an average rate of approximately 9 m per year over the past 12,000 years. This rate is feasible by either rodent or bird dispersal. Dioon caputoi illustrates a dilemma that can potentially be resolved by the

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‘dynamic habitat’ hypothesis. It is currently found only in remnant oak forest on the peaks of mountains on the south-eastern side of the Tehuacan valley. Its populations are located on mountain ‘islands’ surrounded by a ‘sea’ of high desert and in a very unusual geographical location relative to other Dioon species. Archaeological evidence suggests that there has been a dramatic drying of the Tehuacan valley over at least the last 7000 years (MacNeish, 1961) which could have pushed D. caputoi into its current geographical position. Dioon caputoi does not appear to be closely related to its nearest neighbours, D. califanoi, D. purpusii and D. argenteum, by either morphological or molecular characters (Stevenson, 1992; Moretti et al., 1993). Instead it appears to be most closely related to an undescribed taxon found to the south-east in the Mixteca region of Oaxaca. This cycad, in turn, appears to be most closely related to D. holmgrenii and D. tomasellii, both of which are found on the Pacific coast. The Mixteca area is part of the upper drainage of the Rio Balsas that drains to the Pacific Ocean. Thus D. caputoi populations may have shared a common ancestral lineage with the species on the Pacific coast. Quite possibly, that common ancestor migrated with climatic changes up the Rio Balsas valley to the low mountains on the south-eastern wall of the Tehuacan valley. Subsequently, the Tehuacan population may have become isolated on mountain islands of habitat in the high desert of southeastern Puebla following the end of the last ice age. The locations and characteristics of several populations of the Dioon edule complex present biogeographical dilemmas that can potentially be resolved by the above hypothesis. Most of the disjunct forms of D. edule are found in similar habitats within drainages in central Veracruz, San Luis Potosi, Querétaro and Hidalgo, such as the Rio Pescado and Rio Monctezuma valleys. One unusual disjunct population occurs near sea level on the top of a high sand dune on the central coast of Veracruz. This population is restricted to a remnant patch of tropical deciduous forest but consists of hundreds of individuals within its small range. Perhaps this population is a remnant of the original populations that were at sea level during the ice age. A population with similar morphology occurs at 1100 m on the ancient volcanic mountain directly above the dune population on the coast. Perhaps this illustrates an upward migration by one population in response to climatic warming while the dune population remained behind. This would occur as the range of suitable habitat expanded with the warming conditions. Another observation, recorded by Sabato and De Luca (1985), is that the northern populations of D. angustifolium Miquel possess smaller leaves, narrower leaflets and smaller seeds. These populations are among the largest known for Dioon and become a major component of the vegetation in the states of San Luis Potosi, Tamaulipas and Nuevo Leon. They give the impression of being more vigorous and ecologically aggressive than their more restricted southern relatives. The smaller leaves and leaflets of these northern populations have been proposed (Sabato and De Luca, 1985) as an adaptation to the lower temperatures and drier conditions experienced by these plants. We propose that the significantly smaller seeds, possibly more easily dispersed, together with adaptations for cooler and drier conditions, have allowed these northern populations rapidly and successfully

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to colonize new habitat in a northward extension from their ice age refugium. The D. edule complex could be interpreted as a group of recently evolved species or subspecies that have differentiated by migration and isolation within river valleys and by colonizing newly available habitat to the north as conditions became sufficiently favourable since the last glaciation. Dioon rzedowskii is another illustrative example. This species consists of two populations within a narrow range on the limestone cliffs of the lower canyon of the Rio Santo Domingo. It is closely related to D. spinulosum, which occurs over a wider range in a different habitat along the limestone hills at the base of the mountains where the Rio Santo Domingo flows out on to the coastal plain. According to the ‘dynamic habitat’ hypothesis, D. rzedowskii could be colonizing new habitat made available by post-glacial warming, and in so doing migrating up the river canyon. This migration and disjunction is allowing D. rzedowskii to evolve independently of D. spinulosum. The examples presented above seem to demonstrate the utility of the ‘dynamic habitat’ model as a means of framing interpretations of Dioon biogeography. If Dioon species are rapidly and dynamically evolving in response to climatic changes caused by glacial cycles, instead of the traditional view that they are slowly evolving and relictual, then the preservation and study of individual populations should be of paramount importance. Supra- and subspecific naming conventions should be considered to reflect the interplay between these processes and speciation in the genus.

Conclusions Dioon species currently occur chiefly in restricted habitats primarily in transition zones between major forest biomes where they presumably can best compete. The establishment of new populations probably occurs primarily by expansion and fission of existing populations, or vicariance. The establishment of new populations may also occur through medium-range dispersal requiring concomitant colonization by at least two individuals (i.e. one of each sex) and their pollinator. This mechanism would generate a genetic bottleneck that could drive rapid speciation. The morphological data and the available molecular data both support a proposal that many Dioon species are closely related and have recently evolved. Several lines of palynological and palaeoclimatic evidence suggest that there have been dramatic climate changes since the collapse of the last ice age and, by inference, during each of the many ice age cycles of the past 2 million years. These climatic changes suggest that the restricted Dioon habitats have moved upward in elevation by 1500 m and northward by hundreds of kilometres in just the past 12,000 years. Similarly this suggests that Dioon species have moved with their respective habitats and that this movement has resulted in colonization of river valleys as the species move to higher elevations. The secondary isolation of populations within and between these river drainages has resulted in the rapid evolution of the majority of the extant species. During the cooling phases of the

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glacial cycles, the Dioon habitats and their attendant species move down in elevation and southward. This phenomenon could result in a contraction of ranges and a genetic remixing as well as possible extinctions. We offer the speculations presented above as a working hypothesis that raises many testable questions concerning the mechanism(s) of dispersal in Dioon, the mechanisms and possible directionality of recruitment in Dioon, the degree to which the species are related at the molecular level, and ultimately the rate at which they are evolving.

Acknowledgements The authors would like to thank Satie Aramé for very helpful input on the manuscript. We would also like to thank Silvia Salas-Morales, Leo Schibli and the staff of SERBO in Oaxaca for collaboration and friendship in the field.

References Axelrod, D.I. (1975) Evolution and biogeography of Madrean-Tethys sclerophyll vegetation. Annals of the Missouri Botanical Garden 62, 280–334. Chemnick, J. and Gregory, T.J. (1995) A new species of Ceratozamia (Zamiaceae) from Oaxaca, Mexico with comments on distribution, habitat, and relationships. Phytologia 79, 51–57. [Ceratozamia whitelockiana.] Chemnick, J., Gregory, T.J. and Salas-Morales, S. (1997a) A revision of Dioon tomasellii (Zamiaceae) from western Mexico, a range extension of D. merolae, and clarification of D. purpusii. Phytologia 83, 1–6. Chemnick, J., Gregory, T.J. and Salas-Morales, S. (1997b) Ceratozamia mixeorum (Zamiaceae), a new species of Ceratozamia from Oaxaca, Mexico with comments on distribution, habitat, and species relationships. Phytologia 83, 47–52. De Luca, P. and Sabato, S. (1979) Dioon califanoi (Zamiaceae), a new species from Mexico. Brittonia 31, 170–173. De Luca, P., Sabato, S. and Vázquez Torres, M. (1978) Dioon purpusii Rose (Zamiaceae), a misknown species. Delpinoa 20, 31–35. De Luca, P., Sabato, S. and Vázquez Torres, M. (1980a) Dioon caputoi (Zamiaceae), a new species from Mexico. Brittonia 32, 43–46. De Luca, P., Moretti, A., Sabato, S. and Vázquez Torres, M. (1980b) Dioon rzedowskii (Zamiaceae), a new species from Mexico. Brittonia 33, 225–229. De Luca P., Sabato, S. and Vázquez Torres, M. (1981a) Dioon merolae (Zamiaceae), a new species from Mexico. Brittonia 33, 179–185. De Luca, P., Sabato, S. and Vázquez Torres, M. (1981b) Dioon holmgrenii (Zamiaceae), a new species from Mexico. Brittonia 33, 552–555. De Luca, P., Sabato, S. and Vázquez Torres, M. (1982) Distribution and variation of Dioon edule (Zamiaceae). Brittonia 34, 355–362. De Luca, P., Sabato, S. and Vázquez Torres, M. (1984) Dioon tomasellii (Zamiaceae), a new species with two varieties from western Mexico. Brittonia 36, 223–227. Gould, S.J. (2001) The Book of Life. W.W. Norton & Co. New York, 256 pp. Gregory, T.J., Chemnick, J., Salas-Morales, S. and Vovides, A.P. (2003) A new species in

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the genus Dioon (Zamiaceae) from north-central Oaxaca, Mexico. Botanical Journal of the Linnean Society 141, 471–476. [Dioon argenteum.] MacNeish, R.S. (1961) First Annual Report of the Tehuacan Archaeological-Botanical Project. R.S. Peabody Foundation for Archaeology, Andover, Massachusetts, 115 pp. McDonald, J.A. (1993) Phytogeography and history of the alpine-subalpine flora of northeastern Mexico. In: Ramamoorthy, T.P., Bye, R., Lot, A. and Fa, J. (eds) Biological Diversity of Mexico, Origins and Distribution. Oxford University Press, New York, pp. 681–703. Moretti, A., Caputo, P., Cozzolino, S., De Luca, P., Gaudio, L., Siniscalco Gigliano, G. and Stevenson, D.W. (1993) A phylogenetic analysis of Dioon (Zamiaceae). American Journal of Botany 80, 204–214. Norstog, K.J., Stevenson, D.W. and Niklas, K.J. (1986) The role of beetles in the pollination of Zamia furfuracea. Biotropica 18, 300–306. Sabato, S. and De Luca, P. (1985) Evolutionary trends in Dion [sic] (Zamiaceae). American Journal of Botany 72, 1353–1363. Sauer, J.D. (1988) Plant Migration, the Dynamics of Geographic Patterning in Seed Plant Species. University of California Press, London, 282 pp. Siniscalco Gigliano, G. (1990) Chemotaxonomic significance of MAM glycosides and mucilages in cycads. In: Stevenson, D.W. (ed.) The Biology, Structure, and Systematics of the Cycadales. Proceedings of the Symposium CYCAD 87. Memoirs of the New York Botanical Garden 57, pp. 123–131. Stevenson, D.W. (1992) A formal classification of the extant cycads. Brittonia 44, 220–223. Toledo, V.M. (1982) Pleistocene changes in vegetation in tropical Mexico. In: Prance, G.T. (ed.) Biological Diversification in the Tropics. Proceedings of the Fifth International Symposium of the Association for Tropical Biology. Columbia University Press, New York, pp. 93–111. Wolfe, J.A. (1972) An interpretation of Alaska tertiary floras. In: Graham, A. (ed.) Floristics and Paleofloristics of Asia and Eastern North America. Elsevier Publishing Co., Amsterdam, The Netherlands, pp. 210–233.

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Molecular Phylogeny of Zamia (Zamiaceae)

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Paolo Caputo,1 Salvatore Cozzolino,1 Paolo De Luca,1 Aldo Moretti1 and Dennis Wm. Stevenson2 1Dipartimento

di Biologia Vegetale, Università degli Studi di Napoli Federico II, Napoli, Italy; 2Institute of Systematic Botany, New York Botanical Garden, Bronx, New York, USA

Abstract The preliminary results of a phylogenetic analysis of genus Zamia, based on the sequences of the internal transcribed spacer 2 of the nuclear ribosomal DNA combined with a morphological data set, are reported. The consensus tree among the six equally parsimonious cladograms obtained shows Zamia divided in various, often poorly resolved, clades. The most inclusive dichotomy defines two groups: one composed of mainly Central American species, i.e. Z. acuminata, Z. neurophyllidia, Z. obliqua, Z. pseudoparasitica and Z. skinneri; and the other including the rest of the investigated species. The latter clade basally shows Z. inermis and, more internally, a small unit composed of one Mexican and two West Indian taxa (Z. fischeri, Z. portoricensis and Z. pumila). This group is in a sister group relationship with a large, poorly resolved clade which has Z. standleyi at the base. The internal clade includes Z. soconuscensis and two groups, one made of North American species and the other of mainly South American species. The first group includes Z. furfuracea, Z. loddigesii, Z. paucijuga, Z. polymorpha and Z. verschaffeltii. The other group includes mainly South American taxa (i.e. Chiqua restrepoi, Zamia muricata, Z. boliviana, Z. leicontei, Z. manicata, Z. roezlii and Z. wallisii). The results indicate that morphological resemblance in the genus does not correspond to the pattern of phylogenetic relationships, whereas the latter pattern is broadly congruent with geographical distribution.

Introduction Within the Zamiaceae, Zamia Linnaeus, with nearly 60 species (Hill et al., Appendix 1 this volume) from south-eastern USA, through Central America and ©CAB International 2004. Cycad Classification: Concepts and Recommendations (eds T. Walters and R. Osborne)

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the Caribbean to Brazil, and belonging to subfamily Zamioideae (Stevenson, 1992), is probably the most studied genus. This is largely on account of its infrageneric (Marchant, 1968; Norstog, 1980; Moretti, 1990a,b; Moretti et al., 1993b; Caputo et al., 1996) and infraspecific (Norstog, 1980, 1981; Moretti and Sabato, 1984; Moretti et al., 1991) karyotype variation, both characteristics being unique among cycads. The botanical relevance of cycads has caused their inclusion in virtually all the studies dealing with large-scale phylogenetic relationships in higher plants; moreover, the endangered status, the commercial value and the beauty of many species have fostered a large number of investigations on cycad biology. In spite of this, few of the modern studies focus on the phylogeny of cycads at lower taxonomic circumscription. Among them, Stevenson (1990a) dealt with the phylogeny of the whole order using morphological traits; Caputo et al. (1991) focused on the phylogeny of neotropical Zamiaceae using chloroplast DNA characters; Moretti et al. (1993a) investigated the phylogeny of Dioon Lindley using chloroplast DNA; while Caputo et al. (1996), in a study on the karyology of Meso-American Zamia species, published a preliminary cladogram on the relationships of the species of Zamia based mainly on morphological and karyological characters. The authors of the latter study showed that Zamia is divided in two major clades, one of which includes mainly North American and Caribbean species and the other containing mainly Central and South American species. In the same cladogram, Zamia appeared as a strictly monophyletic unit, and the small genus Chigua D.W. Stevenson from Colombia (Stevenson, 1990b) was its sister group. In this contribution, we discuss ongoing studies on the phylogeny of genus Zamia, based on the sequence of the internal transcribed spacer 2 (ITS2) of the nuclear ribosomal DNA in combination with a morphological data set that represents an expansion of that used in Caputo et al. (1996). The ITS sequences are regarded as suitable for inferring phylogeny at the level of genus or below (Baldwin et al., 1995; Andreasen et al., 1999).

Materials and Methods Taxa A wide selection of the species present in cultivation at the ‘Orto Botanico’ (Naples Botanical Garden), as well as at the New York Botanical Garden, was employed. In particular, for this chapter the following species of Zamia were investigated (Table 12.1): Z. acuminata Oersted ex Dyer, Z. boliviana (Brongniart) A. de Candolle, Z. fischeri Miquel, Z. furfuracea Linnaeus filius, Z. inermis Vovides, J.D. Rees & Vázquez Torres, Z. lecointei Ducke, Z. loddigesii Miquel, Z. manicata Linden ex Regel, Z. muricata Willdenow, Z. neurophyllidia D.W. Stevenson, Z. obliqua A. Braun, Z. paucijuga Wieland, Z. polymorpha D.W. Stevenson, A. Moretti &

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Table 12.1. Species, genebank accession numbers and origin of material (NY, New York Botanical Garden; FTG, Fairchild Tropical Garden; NAP, Orto Botanico di Napoli) used in the study. The length of sequences (bp, base pairs) and percentage of bases that are guanine (G) and cytosine (C) are indicated for each species.

Z. verschaffeltii verschaffeltii Miquel Miquel Z. Z. wallisii A. Braun Z. wallisii A. Braun

AJ287350 AJ287350 AJ287361 AJ287361

NY 64 NY specimen260 specimen FTG FTG 89-159 89-159 NAP, s.n. s.n. NAP, NAP537/1-1 NAP537/1-1 NAP501/8-1 NAP501/8-1 NAP540/1-1 NAP540/1-1 NAP943/22-1 NAP943/22-1 NAP539/0-1 NAP539/0-1 NAP ZZ M204 M204 1984 1984 NAP NAP533/10-1 NAP533/10-1 FTG 93-816 93-816 FTG FTG 89-163 89-163 FTG NAP928/74-1 NAP928/74-1 NAP2285/0-1 NAP2285/0-1 NAP528/0-1 NAP528/0-1 Stevenson 1149 1149 Stevenson NAP531/3-1 NAP531/3-1 FTG 71-535 71-535 FTG FTG 76-609 76-609 FTG NAP939/1-1 NAP939/1-1 From the the collection collection From of J. P. Sclavo, France of J. P. Sclavo, France NAP535/6-1 NAP535/6-1 FTG Stevenson Stevenson et et al. al. 582 582 FTG

GC%

260 260 260 261 261 260 260 261 261 260 260 261 261 260 260 260 260 260/261 260/261 260 260 260 260 260 260 260 260 260 260 261 261 260 260 260 260 260 260 260 260

64 64 64 62 62 67 67 64 64 66 66 65 65 65 65 66 66 65/64 65/64 63 63 65 65 65 65 65 65 66 66 66 66 66 66 65 65 65 65 67 67

260 260 260 260 260 260

66 66 65 65 65 65

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ITS2 length (bp)

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Chigua Chigua restrepoi restrepoi D.W. D.W. Stevenson Stevenson Zamia Zamia acuminata acuminata Oersted Oersted ex ex Dyer Dyer Z. boliviana boliviana (Brongniart) (Brongniart) A. A. de de Candolle Candolle Z. Z. fischeri fischeri Miquel Miquel Z. Z. furfuracea furfuracea Linnaeus Linnaeus filius filius Z. Z. inermis inermis Vovides, Vovides, J.D. J.D. Rees Rees & & Vázquez Vázquez Torres Torres Z. Z. lecointei lecointei Ducke Ducke Z. Z. loddigesii loddigesii Miquel Miquel Z. Z. manicata manicata Linden Linden ex ex Regel Regel Z. Z. muricata muricata Willdenow Willdenow Z. Z. neurophyllidia neurophyllidia D.W. D.W. Stevenson Stevenson Z. Z. obliqua obliqua A. A. Braun Braun Z. Z. paucijuga paucijuga Wieland Wieland Z. Z. polymorpha polymorpha D.W. D.W. Stevenson, Stevenson, A. A. Moretti Moretti & & Vázquez Vázquez Torres Torres Z. Z. portoricensis portoricensis Urban Urban Z. Z. pseudoparasitica pseudoparasitica Yates Yates in in Seemann Seemann Z. Z. pumila pumila Linnaeus Linnaeus Z. Z. roezlii roezlii Linden Linden Z. Z. skinneri skinneri Warszewicz Warszewicz ex ex A. A. Dietrich Dietrich Z. Z. soconuscensis Schutzman, Vovides & & Dehgan Dehgan Z. soconuscensis Schutzman, Vovides Z. standleyi standleyi Schutzman Schutzman Z.

Origin of specimen

151

Genebank accession number

Molecular Phylogeny of Zamia

Species

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Vázquez Torres, Z. portoricensis Urban, Z. pseudoparasitica Yates in Seemann, Z. pumila Linnaeus, Z. roezlii Linden, Z. skinneri Warszewicz ex A. Dietrich, Z. soconuscensis Schutzman, Vovides & Dehgan, Z. standleyi Schutzman, Z. verschaffeltii Miquel, Z. wallisii A. Braun, Chigua restrepoi D.W. Stevenson, Microcycas calocoma (Miquel) A. de Candolle, as well as representatives of other zamiaceous genera as outgroups. Voucher specimens of the plants examined are deposited at Orto Botanico di Napoli (NAP) or at New York Botanical Garden (NY).

Morphological and micromolecular data The majority of the morphological and micromolecular characters employed have already been published (Stevenson, 1980, 1981, 1987, 1988, 1990a,b, 1993; Dehgan and Dehgan, 1988; Stevenson and Siniscalco Gigliano, 1989; Richardson, 1990; Norstog, 1993; Meurer-Grimes and Stevenson, 1994; Caputo et al., 1996; Stevenson et al., 1996). These comprise stem characters (e.g. epigeous vs. hypogeous), leaf and petiole characters (e.g. presence/absence of prickles, stipules, terminal pinnae, leaflet plication, stomata guard cell shape), sporophyll characters (e.g. cone shape, pubescence, sporophyll vasculature, sporophyll shape, colour, microsporangia position), pollen and sperm characters and secondary compound characters (e.g. mucilage monosaccharide patterns).

Molecular data Extraction of total DNA was carried out following the method described in Caputo et al. (1991) and ITS2 was amplified according to Aceto et al. (1999) and double-strand sequenced in both directions using a modification of the Sanger dideoxy method (Sanger et al., 1977) in a double-strand DNA cycle sequencing system with fluorescent dyes. Sequence reactions were then loaded into a 373A Applied Biosystems Automated DNA sequencer (Applied Biosystems, Foster City, California, USA). Some sequencing experiments had to be repeated to solve all uncertainties. In several cases this approach was unsuccessful and the purified PCR product was ligated into a pUC18 vector (Farmacia Biotech, Uppsala, Sweden) and then automatically sequenced in the same manner as above by using universal M13 primers.

Data analysis The optimal alignment was searched by using CLUSTAL W version 1.74 (Thompson et al., 1994) and employing the same approach described in Aceto et al. (1999), i.e. all the gap opening and extension parameters of the CLUSTAL W software were varied across every alignment with unit increments from 4 to 15

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and from 4 to 10, respectively. This imposed the constraint that gap opening parameters should always be greater than, or at least equal to, gap extension parameters within any single alignment, while all the other parameters were set at the default values. After cladistic analysis of all the alignments obtained, the optimal alignment was chosen as that with the highest values of consistency index (CI) × retention index (RI) values, i.e. that giving the highest rescaled consistency index (RC) (Farris, 1989). This alignment was combined with the morphological data set, and the resulting matrix was investigated by using the cladistic software environment WINCLADA (Nixon, 1999), running Nona (Goloboff, 1993–1999) as a daughter process, with the following parameters: hold 100,000; hold/100; mult*100; max. The resulting cladograms were investigated with WINCLADA, which was also used to calculate branch support (up to trees five steps longer).

Results The selected alignment, when analysed in combination with the morphological data set, gave six equally parsimonious cladograms (length = 345 steps, CI = 0.80 and RI = 0.89), the consensus tree of which is shown in Fig. 12.1. Zamia appears divided in several incompletely resolved clades. The most inclusive dichotomy defines two clades, one composed of mainly central American species (the only partial exception being Z. obliqua, distributed from southern Panama to the southern Chocó in Colombia), i.e. Z. acuminata, Z. neurophyllidia, Z. obliqua, Z. pseudoparasitica and Z. skinneri, referred to as the ‘pseudoparasitica clade’, and the other including the rest of the investigated species. The latter clade basally shows Z. inermis, a species endemic to Veracruz, Mexico. More internally, a small unit composed of one Mexican species (Z. fischeri, endemic to San Luis Potosi and neighbouring Querétaro, Mexico) and two West Indian taxa (Z. portoricensis, distributed in central Cuba and the Dominican Republic, and Z. pumila, from western Puerto Rico) is in a sister group relationship with a large, poorly resolved clade that has Z. standleyi (endemic to Honduras) at the base. The internal clade includes Z. soconuscensis (endemic to Sierra Madre de Soconusco, Chiapas, Mexico) and two groups, one made of North American species and the other of mainly South American species. The first group includes Z. furfuracea, Z. loddigesii, Z. paucijuga, Z. polymorpha and Z. verschaffeltii (this group we loosely refer to as the ‘loddigesii clade’). The other group, here indicated as the ‘Chigua clade’ has two unresolved South American taxa (C. restrepoi and Z. muricata) at the base and then a clade including Z. boliviana and Z. lecointei, which is in turn unresolved compared with another clade including Z. manicata, Z. roezlii and Z. wallisii. Branch support for the great majority of the clades is low. Among the main clades, only the ‘pseudoparasitica clade’, the ‘loddigesii clade’ and the ‘Chigua clade’ show a support greater than one.

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Fig. 12.1. Consensus tree out of six maximum parsimony cladograms obtained for the combined data set (matrix consensus length 378 characters, 272 of which represent ITS2; length = 345 steps, CI = 0.80 and RI = 0.89). Numbers above branches represent synapomorphies; numbers below indicate branch support (up to five steps longer trees). Taxa of Zamia are indicated with acronyms derived from the first letter of the genus and the first three letters of the specific epithet. Chigua restrepoi D.W Stevenson and Microcycas calocoma (Miquel) A. de Candolle are indicated with acronyms derived from the first four letters of the genus.

Discussion The results of this investigation offer new insights on the phylogeny of Zamia, as they do not match in entirety with any previous hypothesis on the relationships within the genus. However, the consensus tree in Fig. 12.1 seems to show good correlations with geographical distribution. Among the major clades that can be observed, the ‘pseudoparasitica clade’ is composed of mainly Central American species; a second (the ‘loddigesii clade’) comprises mainly North American species, and a third (the ‘Chigua clade’) includes Central and South American species. This latter group basally shows a poorly resolved assemblage of taxa (C. restrepoi,

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Z. boliviana, Z. lecointei, Z. muricata), the members of which (excluding Chigua D.W. Stevenson) have been informally included by Norstog and Nicholls (1997) in the ‘eastern South American Zamias’. A fully resolved Central–South American clade is the fourth major group in the analysis. Caribbean Zamia species (represented here by Z. portoricensis and Z. pumila) form a clade, which, together with Z. fischeri, is in a sister group relationship with a group basally showing Z. standleyi, and including both the ‘loddigesii clade’ and the ‘Chigua clade’. Chigua is strongly nested in Zamia, in spite of the presence of a midrib, as well as the male cone peduncle which is scarcely narrower than the fertile portion (characters that have been used to segregate it from Zamia); these are simple albeit evident species-level autapomorphies. Previous work based on chloroplast DNA (Caputo et al., 1991) and karyology, supplemented by morphological characters (Caputo et al., 1996), tentatively indicated that Chigua was the sister group of Zamia. However, in the first case (Caputo et al., 1991), the study, aiming at a genus-level phylogeny of American Zamiaceae, used only Z. fischeri and Z. skinneri as representative of genus Zamia. Also in the latter paper (Caputo et al., 1996) the Central and South American species, which belong to the ‘Chigua clade’ (Fig. 12.1), were under-represented, as Z. boliviana, Z. lecointei and Z. muricata were missing from that analysis. Interestingly enough, various of the morphological characters that have been thought to define synapomorphic units in the genus (e.g. strong leaflet plication, possession of a trunk, presence of adaxial microsporangia) seem to represent the consequence of pervasive parallel evolution which besets this taxon. Indeed, Zamia itself is hardly definable in terms of morphological synapomorphies, as the only morphological character which acts as a synapomorphy at genus level (distinct male cone facets) reverts more than once within the genus. No trait, among the morphological character used, seems to have evolved only once in the genus. As a consequence, various species that show great morphological resemblance have to be interpreted as the product of similar selective pressures on quite different lineages. For example, the Aulacophyllum Regel body plan (here represented by Z. neurophyllidia, Z. roezlii, Z. skinneri and Z. wallisii) seems to have evolved at least twice in the genus. Chromosome characters were not included in our analysis, because they, as well as karyotypes, show infraspecific variation in several taxa (Norstog, 1980, 1981; Moretti and Sabato, 1984; Moretti et al., 1991). Plotting the chromosome number on to the phylogenetic tree of Fig. 12.1 under unambiguous optimization reconstructs the plesiomorphic chromosome number for the genus as 2n = 16, and reconstructs the plesiomorphic number for the ‘loddigesii clade’ as 2n = 18. This would imply that centric fission occurred more than once in the genus, i.e. in the ‘pseudoparasitica clade’, the ‘loddigesii clade’ and the ‘Chigua clade’. The fact that morphological resemblance does not always correspond to patterns of descent, and that also chromosomal rearrangement seems to have developed more than once, is not surprising given the comparative antiquity of a genus whose stem lineage dates back at least to the early Cenozoic. Long times

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under similar selective pressures have probably caused morphological convergence in lineages that are quite separate from a phylogenetic point of view. Further study, including a totality of species in the genus, will probably show that the above-mentioned cases of parallelism are even more pervasive than shown in this contribution.

References Aceto, S., Caputo, P., Cozzolino, S., Gaudio, L. and Moretti, A. (1999) Phylogeny and evolution of Orchis and allied genera based on ITS DNA variation: morphological gaps and molecular continuity. Molecular Phylogenetics and Evolution 13, 67–76. Andreasen, K., Baldwin, B.G. and Bremer, B. (1999) Phylogenetic utility of the nuclear ITS region in subfamily Ixoroideae (Rubiaceae): comparison with cpDNA rbcL sequence data. Plant Systematics and Evolution 217, 119–135. Baldwin, B.G., Sanderson, M.J., Porter, M.J., Wojciechowski, M.F., Campbell, C.S. and Donoghue, M.J. (1995) The ITS region of nuclear ribosomal DNA: a valuable source of evidence in angiosperm phylogeny. Annals of the Missouri Botanical Garden 82, 247–277. Caputo, P., Stevenson, D.W. and Wurtzel, E.T. (1991) A phylogenetic analysis of American Zamiaceae (Cycadales) using chloroplast DNA restriction fragment polymorphisms. Brittonia 43, 135–145. Caputo, P., Cozzolino, S., Gaudio, L., Moretti, A. and Stevenson, D.W. (1996) Karyology and phylogeny of some Meso-American species of Zamia (Zamiaceae). American Journal of Botany 83, 1513–1520. Dehgan, B. and Dehgan, N.B. (1988) Comparative pollen morphology and taxonomic affinities in Cycadales. American Journal of Botany 75, 1501–1516. Farris, J.S. (1989) The retention index and the rescaled consistency index. Cladistics 5, 417–419. Goloboff, P.A. (1993–1999) Nona. Instruction manual. Distributed by the author. Marchant, C.J. (1968) Chromosome patterns and nuclear phenomena in the cycad families Stangeriaceae and Zamiaceae. Chromosoma 24, 100–134. Meurer-Grimes, B. and Stevenson, D.W. (1994) The biflavones of the Cycadales revisited: biflavones in Stangeria eriopus, Chigua restrepoi and 32 other species of Cycadales. Biochemical Systematics and Ecology 22, 595–603. Moretti, A. (1990a) Cytotaxonomy of cycads. In: Stevenson, D.W. (ed.) The Biology, Structure, and Systematics of the Cycadales. Proceedings of the Symposium CYCAD 87. Memoirs of the New York Botanical Garden 57, pp. 114–122. Moretti, A. (1990b) Karyotypic data on North and Central American Zamiaceae (Cycadales) and their phylogenetic implications. American Journal of Botany 77, 1016–1029. Moretti, A. and Sabato, S. (1984) Karyotype evolution by centromeric fission in Zamia (Cycadales). Plant Systematics and Evolution 146, 215–223. Moretti, A., Caputo, P., Gaudio, L. and Stevenson, D.W. (1991) Intraspecific chromosome variation in Zamia (Zamiaceae, Cycadales). Caryologia 44, 1–10. Moretti, A., Caputo, P., Cozzolino, S., De Luca, P., Gaudio, L., Siniscalco Gigliano, G. and Stevenson, D.W. (1993a) A phylogenetic analysis of Dioon (Zamiaceae). American Journal of Botany 80, 204–214.

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Moretti, A., Caputo, P., Cozzolino, S. and Gaudio, L. (1993b) Karyotypes of New World Cycads. In: Stevenson, D.W. and Norstog, K.J. (eds) The Biology, Structure, and Systematics of the Cycadales. Proceedings of the Second International Conference on Cycad Biology. Palm & Cycad Societies of Australia Limited, Milton, Queensland, Australia, pp. 263–269. Nixon, K.C. (1999) WinClada (BETA), Version 0.9.9. Published by the author, Ithaca, New York. Norstog, K.J. (1980) Chromosome numbers in Zamia (Cycadales). Caryologia 33, 419–428. Norstog, K.J. (1981) Karyotypes of Zamia chigua (Cycadales). Caryologia 34, 255–260. Norstog, K.J. (1993) Spermatogenesis in Microcycas: evolutionary significance of male gametes of seed plants. In: Stevenson, D.W. and Norstog, K.J. (eds) The Biology, Structure, and Systematics of the Cycadales. Proceedings of the Second International Conference on Cycad Biology. Palm & Cycad Societies of Australia Limited, Milton, Queensland, Australia, pp. 270–278. Norstog, K.J. and Nicholls, T.J. (1997) The Biology of the Cycads. Cornell University Press, Ithaca, New York, 363 pp. Richardson, P.M. (1990) Flavonoid chemistry and the taxonomy of the cycads. In: Stevenson, D.W. (ed.) The Biology, Structure, and Systematics of the Cycadales. Proceedings of the Symposium CYCAD 87. Memoirs of the New York Botanical Garden 57, pp. 132–141. Sanger, F., Niklen, S. and Coulson, A.R. (1977) DNA sequencing with chain terminating inhibitors. Proceedings of the National Academy of Sciences, USA 74, 5463–5467. Stevenson, D.W. (1980) Radial growth in the Cycadales. American Journal of Botany 67, 465–475. Stevenson, D.W. (1981) Observations on ptyxis, phenology, and trichomes in the Cycadales and their systematic implications. American Journal of Botany 68, 1104–1114. Stevenson, D.W. (1987) Comments on character distribution, taxonomy, and nomenclature of the genus Zamia L. in the West Indies and Mexico. Encephalartos 9, 3–7. Stevenson, D.W. (1988) Strobilar ontogeny in the Cycadales. In: Leins, P., Tucker, P.C. and Endress, P.K. (eds) Aspects of Floral Development. G. Fischer, Stuttgart, Germany, pp. 205–224. Stevenson, D.W. (1990a) Morphology and systematics of the Cycadales. In: Stevenson, D.W. (ed.) The Biology, Structure, and Systematics of the Cycadales. Proceedings of the Symposium CYCAD 87. Memoirs of the New York Botanical Garden 57, pp. 8–55. Stevenson, D.W. (1990b) Chigua, a new genus in the Zamiaceae with comments on its biogeographical significance. In: Stevenson, D.W. (ed.) The Biology, Structure, and Systematics of the Cycadales. Proceedings of the Symposium CYCAD 87. Memoirs of the New York Botanical Garden 57, pp. 169–172. Stevenson, D.W. (1992) A formal classification of the extant cycads. Brittonia 44, 220–223. Stevenson, D.W. (1993) The Zamiaceae in Panama with comments on phytogeography and species relationships. Brittonia 45, 1–16. Stevenson, D.W. and Siniscalco Gigliano, G. (1989) The systematic value of the monosaccharide composition and distribution pattern of cycad mucilages. Biochemical Systematics and Ecology 17, 185–190. Stevenson, D.W., Norstog, K.J. and Molsen, D. (1996) Midribs of cycad pinnae. Brittonia 48, 67–74. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.

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Bart Schutzman Environmental Horticulture Department, University of Florida, Gainesville, Florida, USA

Abstract The author’s work includes morphological, geographical and phenetic analyses of Meso-American Zamia representatives and is a continuation of earlier Master’s and Doctoral studies. This research has led to the publication of six new species descriptions; in addition, several others are in progress, several preliminary species groups have been recognized and recommendations made for future work. However, an infrageneric classification has not yet been included. Such a classification will depend on the culmination of alpha-taxonomic work in the genus, thorough morphological and geographical characterization of all known species, and finally, cladistic analyses, including those arising from molecular systematic investigation. Examination of possible introgression and hybrid species complexes is also necessary for a thorough understanding and development of an infrageneric classification in Zamia.

Introduction In the past, taxonomy of the genus Zamia Linnaeus has been based primarily on leaflet number, size and shape. Newell (1985) first pointed out the predominance of leaflet morphology in taxonomic treatments and demonstrated that it could be environmentally influenced. Leaf and leaflet features, unfortunately, are highly plastic, being affected by environment and juvenility, and data commonly overlap between species. This is best illustrated in Eckenwalder’s (1980) work with the Caribbean zamias. He did not consider other sources of data such as reproductive features before ‘lumping’ all the Caribbean species into Z. pumila Linnaeus ©CAB International 2004. Cycad Classification: Concepts and Recommendations (eds T. Walters and R. Osborne)

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subspecies pumila and subspecies pygmaea (Sims) Eckenwalder (= Z. pygmaea Sims; see Hill et al., Appendix 1 this volume). Stevenson (1987) looked at strobilar features and revised the Caribbean species to six, but this number of taxa still does not separate the Florida species (one, two, or three, depending on the systematist) from other Caribbean taxa. The author’s approach in the study of Meso-American species (Schutzman, 1982, 1998) was Adansonian and called for the examination of as many characters as possible. This approach will be necessary to resolve other groups of cycad taxa, e.g. the Caribbean Zamia species.

Materials and Methods Plant material was collected by the author and others during field expeditions to Mexico, Honduras, Panama and Costa Rica. Additional material was obtained from private collectors and botanical gardens, including the Montgomery Botanical Center, Fairchild Tropical Garden, Marie Selby Botanical Gardens and the Huntington Botanical Gardens. Herbarium specimen loans were obtained from 32 institutions in the USA and elsewhere. Gross morphology of eophylls (first seedling leaves) and the progression of juvenile to adult leaflets were compared. Scanning electron micrographs were made of vegetative and reproductive features, including leaflets, microsporophylls and microsporangia. Light microscopy was used to examine leaf epidermal clearings after treatment with Jeffrey’s (1917) solution. Fourier morphometrics and phenetic analyses of leaflet shape were conducted on several groups of specimens. These included comparisons of leaflets from the same plant, from different plants in the same population, from different populations, and from different species.

Results and Discussion Results by character Eophyll (first leaf) morphology Eophyll morphology was useful in identifying individual species in most cases, and species groups in others, but was not useful at all in some cases. Variation depended on species; most significant was the number of leaflets per eophyll. Morphological features that were observed to vary in a meaningful way included leaflet number and shape. Examples shown in Fig. 13.1 include Zamia cremnophila Vovides, Schutzman & Dehgan, Z. vazquezii D.W. Stevenson, Sabato, A. Moretti & De Luca, Z. sp. “maritima” and Z. spartea A. de Candolle. Gross morphology of microsporophylls Examples of microsporophylls are shown in Fig. 13.2, and include Zamia fairchildiana L.D. Gómez, Z. pseudoparasitica Yates in Seemann, Z. spartea and Z. vazquezii. Apomorphic species were easily identified. The characteristics most

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Fig. 13.1. Example of eophyll shape. (A) Zamia cremnophila Vovides, Schutzman & Dehgan. (B) Zamia vazquezii D.W. Stevenson, Sabato, A. Moretti & De Luca. (C) Zamia sp. ‘‘maritima’’. (D) Zamia spartea A. de Candolle.

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Fig. 13.2. Example of microsporophyll shape (a, abaxial; b, adaxial). (A) Zamia fairchildiana L.D. Gómez. (B) Zamia pseudoparasitica Yates in Seemann. (C) Zamia spartea A. de Candolle. (D) Zamia vazquezii D.W. Stevenson, Sabato, A. Moretti & De Luca.

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Fig. 13.3. Diagram illustrating from where standardized scanning micrographs of microsporophyll surfaces were taken (a, area where pubescence generally ends; b, ‘wing’ area on adaxial surfae).

useful in identifying species were: (i) shape of microsporophyll, including presence or absence of narrowing to a pedicel; (ii) presence or absence of microsporangia in the ‘interstitial region’; (iii) shape and size of the apex; and (iv) surface features of the distal microsporophyll surface. Scanning electron microscopic examination of microsporophylls Microsporophylls were examined under SEM and two primary useful regions were identified, as illustrated in Fig. 13.3 (see regions ‘a’ and ‘b’). Examples of one region (‘a’ in Fig. 13.3) are shown in Fig. 13.4 for Zamia cremnophila, Z. loddigesii Miquel, Z. pseudoparasitica and Z. soconuscensis Schutzman, Vovides & Dehgan. Useful characteristics included shape, size and frequency of trichomes, frequency of stomata, and visibility of cellular outlines. Scanning electron microscopic examination of microsporangia Microsporangial features were visible under low SEM magnification and were rich in morphological variation. Examples are shown in Fig. 13.5 and include Zamia neurophyllidia D.W. Stevenson, Z. standleyi Schutzman, Z. vazquezii and Z. tuerckheimii Donnell Smith. Useful characteristics observed were ornamentation of the suture (line of dehiscence), stomatal frequency and position, and visibility of cellular outlines. The usefulness of these features was also mentioned by Schutzman and Dehgan (1988) and Dehgan et al. (1993).

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Fig. 13.4. Example of microsporophyll variation; scanning micrograph of area ‘a’ in Fig. 13.3. (A) Zamia cremnophila Vovides, Schutzman & Dehgan. (B) Zamia loddigesii Miquel. (C) Zamia pseudoparasitica Yates in Seemann. (D) Zamia soconuscensis Schutzman, Vovides & Dehgan.

Leaflet shape While leaflet shape and size did not always resolve taxa, the fine resolution of Fourier analysis was a better quantifier of shape than length:width ratios or absolute measurements, as also discussed by Schutzman and Dehgan (1993). If enough Fourier coefficients are used, shape may be satisfactorily reconstructed. It

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Fig. 13.5. Example of microsporangial variation. (A) Zamia neurophyllidia D.W Stevenson. (B) Zamia standleyi Schutzman. (C) Zamia vazquezii D.W. Stevenson, Sabato, A. Moretti & De Luca. (D) Zamia tuerckheimii Donnell Smith.

was found that 32 coefficients gave sufficient details in the shape reconstruction, and could be ‘plugged into’ phenetic analyses to allow resolution of taxa in many cases. Figures 13.6 and 13.7 exemplify the results of a Fourier analysis of leaflet shapes. In the example, Zamia spartea, Z. furfuracea Linneaus filius and their artificial hybrid were analysed and principal component analysis was used to display the results graphically. The hybrid fell between the parents, but was closer to the Z. spartea parent, consistent with the resemblance between the hybrid and that parent.

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●

Fig. 13.6. Example of phenetic analysis of leaflet shape Fourier transforms from Zamia furfuracea Linnaeus filius (filled circle), Z. spartea A. de Candolle (filled square) and their hybrid [‘Norstog hybrid’] (open circle), respectively. The coding symbols shown correspond to the principal component analysis of these leaflet shapes shown in Fig. 13.7.

Results by taxa Species concept The widely used ‘morphogeographical’ species concept has been employed in the author’s studies of Zamia. Species are recognized by distinct morphological gaps between groups correlated with geographical distribution patterns. Species described Descriptions of six new species have been published: Zamia splendens Schutzman (1984) (not synonymous with Z. verschaffeltii Miquel; Hill et al., Appendix 1 this

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10 ■ Z. spartea ● Z. furfuracea

8 Principal component 2 (21.0%)

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●

Z. (Norstog hybrid)

4 2 0 –2 –4 –6 –6

–4

–2

0

2

4

6

8

10

Principal component 1 (51.8%)

Fig. 13.7. Principal component analysis of leaflet shapes from Zamia furfuracea Linnaeus filius, Z. spartea A. de Candolle and their hybrid [‘Norstog hybrid’] described in Fig. 13.6.

volume), Z. standleyi Schutzman (1989), Z. soconuscensis Schutzman, Vovides & Dehgan (1988), Z. cremnophila Vovides, Schutzman & Dehgan (Schutzman et al., 1988), Z. lacandona Schutzman & Vovides (1998) and Z. elegantissima Schutzman, Vovides & R.S. Adams (1998). Species descriptions in progress include Zamia species nova #1 (from Guatemala), Z. species nova #2 (from Guatemala) and Z. species nova (from Honduras).

Remaining Taxonomic Problems in Meso-American Zamias Studies of living plants and herbarium material have identified several taxonomic problems that exist amongst the Meso-American species, including the following examples.

Misapplied species names

Zamia acuminata Oersted ex Dyer The species was described from the San Juan River in Nicaragua, but cultivated plants from El Valle, Panama, are mislabelled as this species and in reality are undescribed. We are acquiring materials of the Nicaraguan species to make detailed comparisons with the Panamanian plants.

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Zamia fischeri Miquel / Z. vazquezii At first the author believed two varieties to be present, but is now leaning toward the existence of two species. The commonly cultivated plants range from Veracruz to San Luis Potosi and Hidalgo, Mexico, and belong to Z. vazquezii, while Z. fischeri is narrowly endemic to a small area in western San Luis Potosi. Some believe that the large San Luis Potosi plant belongs to Z. fischeri while only the large plant from Veracruz belongs to Z. vazquezii. Zamia fairchildiana / Z. pseudomonticola L.D. Gómez / Z. elegantissima The first of these was described using Costa Rican material from the Osa Peninsula, and includes plants considered Z. pseudomonticola. The morphogeographically well-separated central Panamanian plants, once whimsically referred to as Z. ‘pseudo-pseudoparasitica’, then later known as Z. fairchildiana, are correctly described as Z. elegantissima, but are still frequently referred to as Z. fairchildiana.

Possible hybrid species complexes Zamia loddigesii /Z. sp. “maritima” / Z. furfuracea / Z. paucijuga Wieland There are multiple forms of Z. loddigesii that appear distinct, exhibiting variation in strobilar features, but certain populations seem to be introgressing into the coastal species referred to as Z. sp. “maritima” (Schutzman, 1998). The coastal species was never named but the putative introgressive hybrid was used by Stevenson and Sabato (1986) to lectotypify Z. furfuracea (Schutzman, 1998). Zamia polymorpha D.W. Stevenson, A. Moretti & Vázquez Torres / Z. variegata Warszewicz The variegated species from the east coast of Guatemala appear to intergrade with the interior species found there and in Belize. Plants range from enormous specimens, with prominent variegation and 4-metre long leaves, to diminutive plants less than a metre tall with only a few dull yellowish spots on their leaflets. The name Z. polymorpha has been applied to populations from Yucatan, Mexico, Belize and the Guatemalan interior (Maya Mountains) but some of these Guatemalan plants exhibit the leaf spotting, indicating possible contact with Z. variegata. Zamia neurophyllidia / Z. skinneri Warszewicz ex A. Dietrich The former is described from the vicinity of Panama’s border with Costa Rica, and interior Costa Rican plants quite unlike the type are mislabelled Z. neurophyllidia. Several distinct and non-overlapping morphological groups of populations are all lumped under the name Z. skinneri, and these should be resolved into different taxa.

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Discussion Species delimitation Reasons for difficulties in Zamia species delimitation are several and are enumerated here: Scant herbarium materials Herbarium specimens often consist only of vegetative parts, because reproductive material in Zamia is very rarely found in the field. Rarity of fertile specimens in the field has therefore commonly limited the use of reproductive characters in species descriptions. Cycads as ‘survivors’ Under unfavourable conditions (situations in which other plants would simply not be found alive), many cycads are often be found in a highly reduced form, often reverting to a juvenile condition. This frequently happens in regrowth circumstances, after fires or other catastrophic events, under low soil fertility, or when plant cover has been stripped away from shade-loving species. A corollary to this is that plants of a given species may easily outgrow their descriptions under cultivation. Entire populations of plants under unfavourable conditions often survive and can even reproduce, but vegetative and reproductive structures may not reach the sizes that would be found under optimal growing conditions. This, combined with cycads’ juvenile-to-adult transition in vegetative features, the unique ability of small plants of many apparently immature zamias to produce equally small mega- and microstrobili, and the fact that plants may never outgrow ‘juvenile’ vegetative characters, could easily have resulted in overlapping species descriptions. Typological thinking This is a belief that a member of a species should conform to a predefined model or ‘type’. Typological thinking was employed early in the evolution of systematic thought, prior to the idea that species could be polythetic (members of a group sharing multiple, but not necessarily all, features). Typology attempted to ‘straight-jacket’ a species to agree with its type specimen or description; anything that did not fit the type must ‘certainly’ be another species. A corollary of typological thinking is that a published species name must be associated with a taxon; this results in an approach to taxonomic revision in which a group’s nomenclature is dealt with prior to the determination of taxa; this modus operandi brings to mind the expression ‘putting the cart before the horse’. Use of unicates to describe new species Because it is now realized that taxa can be and most often are polythetic, the collection of a single specimen and the description of a taxon from that specimen is the least accurate way to delimit taxa. Unfortunately, this is the situation

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inherited from 18th and 19th century taxonomists; the rule of nomenclatural priority forces us to deal with these poor collections and ambiguous names rather than by extirpating dubious ones. Many treatments simply list a name as nomen dubium but this decreases nomenclatural stability because the question may later be resolved and newer names reduced to synonymy in favour of the older ones. Conservation of species names, now an acceptable practice, is a stabilizing influence in nomenclature that eliminates the need to use the term nomen dubium. Misunderstanding of plasticity of leaves and leaflets Since leaves were the primary characteristic used in descriptions, their extreme variability was the predominant factor in the misunderstanding of Zamia species. Production of small mega- and microstrobili by small sexually mature plants, and successively larger strobili by older, larger plants The diameter of successive strobili and length of sporophylls of individual plants appear to reach a stable size earlier than the lengths of those strobili, until they, too, reach some maximum size range for that individual, population or species. ‘Nearsighted’ local floras with taxa overlapping other areas Regional geographical areas of taxonomic study can often produce misleading results for two major reasons: taxa are not always confined to the areas of study; and related taxa that could shed light on many systematic questions are often not considered. This has been an especially prevalent problem in Zamia taxonomy, because of nearsighted local floras that duplicated naming of species spanning several political divisions. This has most notably occurred in the Caribbean area, where the cycad taxonomy still remains to be elucidated to the satisfaction of most cycadologists. Selection of Meso-America as the geographical range of the author’s project was in full cognizance of these facts; as he worked with the plants, he attempted to keep the Caribbean and South American taxa in perspective. Bijan Dehgan (Florida, 2002, personal communication) believes that cycad taxonomists have become carried away with new species descriptions and are using minute differences to differentiate new taxa.

Infrageneric classification Successful completion of an infrageneric classification in Zamia will depend on several factors: ●

●

To increase the potential accuracy of a phylogenetic analysis, the alpha-taxonomic stage of classification must include as many species as possible in the analysis. Nomenclatural difficulties must be resolved. These include the resolution of species complexes and the role of hybridization, old descriptions that lack geographical information, and/or type specimens that are difficult to identify.

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Thus far, cladistic characters, other than DNA sequence data, are few in number, and further study must be completed to amass sufficient data to enumerate cladistic characters fully.

Future use of molecular systematics Molecular biological applications to systematics, specifically the use of DNA sequences to uncover phylogeny, are currently very popular. The successful use of molecular phylogenetics in cycads will unfortunately be delayed by alpha-taxonomy, because species of Zamia, Ceratozamia Brongniart and Dioon Lindley are still being described. This is especially true for the genus Zamia, which is estimated to include a dozen or more undescribed species in Meso-America alone. The situation in South America is most probably similar. Successful species delimitation relies on the totality of characters, most importantly the successful interpretation of morphogeographical variation. Ultimately, the use of cladistic methods to produce an evolutionary hypothesis will be likely to be more accurate the closer species delimitation is to completion. Species sampling problems are mentioned by Wendel and Doyle (1998) as one of five organism-level processes that can cause conflicting phylogenetic hypotheses in molecular systematics. Incomplete alpha-taxonomy would almost certainly result in this type of problem. Also listed among these causes are rapid morphological evolution or convergence, hybridization and/or introgression and rapid diversification.

Conclusions While DNA sequence data have proved invaluable as a tool in the reconstruction of infrageneric relationships, the value of an Adansonian approach to taxonomy that utilizes all available data cannot be overstressed. The relative value of the wide variety of data, both vegetative and reproductive, uncovered in the author’s work in Meso-American Zamia remains to be determined in the context of an infrageneric classification of the genus. It is the challenge of continuing and future systematic studies to establish a balance between molecular and morphological data that will result in the most accurate classification. Additionally, the value of phenetic studies must not be dismissed merely because of the possibility of parallel or convergent features; these data can be compared and will provide additional insight into relationships within the genus.

References Dehgan, B., Schutzman, B. and Almira, F. (1993) Utilization of scanning electron microscopy in the study of surface features in Cycadales. In: Stevenson, D.W. and

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Norstog, K.J. (eds) The Biology, Structure, and Systematics of the Cycadales. Proceedings of the Second International Conference on Cycad Biology. Palm & Cycad Societies of Australia Limited, Milton, Queensland, Australia, pp. 228–235. Eckenwalder, J.E. (1980) Taxonomy of the West Indian cycads. Journal of the Arnold Arboretum 61, 701–722. Jeffrey, E.C. (1917) The Anatomy of Woody Plants. University of Chicago Press, Chicago, Illinois, 478 pp. Newell, S. (1985) Intrapopulational variation in leaflet morphology of Zamia pumila L. in relation to microenvironment and sex. American Journal of Botany 72, 217–221. Schutzman, B. (1982) Preliminary systematic and taximetric studies of Meso-American Zamia L. (Zamiaceae). MSc thesis, University of Florida, Gainesville, Florida. Schutzman, B. (1984) A new species of Zamia (Zamiaceae, Cycadales) from Chiapas, Mexico. Phytologia 55, 299–304. [Zamia splendens.] Schutzman, B. (1989) A new species of Zamia (Zamiaceae, Cycadales) from Honduras. Systematic Botany 14, 214–219. [Zamia standleyi.] Schutzman, B. (1998) Revisionary studies of Meso-American Zamia L. (Zamiaceae, Cycadales). PhD Dissertation. University of Florida, Gainesville, Florida. Schutzman, B. and Dehgan, B. (1988) Microsporophylls and microsporangia of Cycadales: comparative morphology and systematic implications. American Journal of Botany 75, 204–205. Schutzman, B. and Dehgan, B. (1993) Computer assisted systematics in the Cycadales. In: Stevenson, D.W. and Norstog, K.J. (eds) The Biology, Structure, and Systematics of the Cycadales. Proceedings of the Second International Conference on Cycad Biology. Palm & Cycad Societies of Australia Limited, Milton, Queensland, Australia, pp. 281–289. Schutzman, B. and Vovides, A.P. (1985) Phenetic and other systematic studies of the Zamia loddigesii / Z. furfuracea complex. Abstract of paper presented at 36th annual AIBS meetings, University of Florida, Gainesville, Florida 11–15 August 1985. Schutzman, B. and Vovides, A.P. (1998) A new Zamia (Zamiaceae, Cycadales) from eastern Chiapas, Mexico. Novon 8, 441–446. [Zamia lacandona.] Schutzman, B., Vovides, A.P. and Dehgan, B. (1988) Two new species of Zamia (Zamiaceae, Cycadales) from Southern Mexico. Botanical Gazette 149, 347–360. [Zamia cremnophila, Z. soconuscensis.] Schutzman, B., Vovides, A.P. and Adams, R.S. (1998) A new Zamia (Zamiaceae, Cycadales) from Central Panama. Phytologia 85, 137–145. [Zamia elegantissima.] Stevenson, D.W. (1987) Again the West Indian Zamias. Fairchild Tropical Garden Bulletin 42, 23–27. Stevenson, D.W. and Sabato, S. (1986) Typification of names in Zamia L. and Aulacophyllum Regel (Zamiaceae). Taxon 35, 134–144. Wendel, J.F. and Doyle, J.J. (1998) Phylogenetic incongruence: window into genome history and molecular evolution. In: Soltis, D.E., Soltis, P.S. and Doyle, J.J. (eds) Molecular Systematics of Plants II: DNA Sequencing. Kluwer Academic Publishers, Boston, Massachusetts, pp. 265–296.

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Dennis Wm. Stevenson Institute of Systematic Botany, New York Botanical Garden, Bronx, New York, USA

Abstract Ten previously known species of Zamia from Bolivia, Ecuador and Peru are discussed and a new species from Peru, Zamia macrochiera, is described. Keys to all 11 species are given as well as complete descriptions, synonymy, types, exsiccata, distributional data and conservation status as used in the 1997 IUCN Red List of Threatened Plants. Zamia boliviana is found only in Bolivia and one collection from contiguous Brazil; Z. gentryi is endemic to Ecuador, while Z. macrochiera and Z. urep are endemic to Peru. The other seven species are more widespread, with Z. poeppigiana and Z. ulei found in both Ecuador and Peru; Z. disodon known from only one locality in Peru, in an area disjunct from northern Colombia; Z. hymenophyllidia found only in north-eastern Peru and contiguous south-eastern Colombia; and Z. roezlii found only in north-western Ecuador and contiguous south-western Colombia. Although widespread in the Amazon basin of Colombia, Venezuela and Brazil, Z. lecointei and Z. amazonum are each known from only one or two collections, respectively, in north-eastern Peru.

Introduction The last treatment of the neotropical species of Zamia Linnaeus was that of Schuster (1932). As discussed in Sabato (1990), Stevenson (1990, 1991, 2001) and Norstog and Nicholls (1997), the nomenclature and species descriptions in Schuster’s work are inadequate, mainly because of a paucity of collections and a lack of field experience. This treatment of the cycad genus Zamia is intended to complement previous treatments of the neotropical cycads that have appeared in the past 10 years ©CAB International 2004. Cycad Classification: Concepts and Recommendations (eds T. Walters and R. Osborne)

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for the Floras of the Guianas (Stevenson, 1991), Panama (Stevenson, 1993), Colombia (Stevenson, 2001) and the checklists for Peru (Brako, 1993) and Ecuador (Stevenson, 1999). Information from recent collections and fieldwork is collated here to augment data presented on the conservation status of those species of Zamia listed by Walter and Gillett (1998) in the 1997 IUCN Red List of Threatened Plants.

Key to the species of Zamia in Bolivia, Ecuador and Peru 1. Leaflets with a distinct petiolule and a gland-like collar at the base of the lamina …………............................... 7. Z. macrochiera 1. Leaflets sessile and without a gland-like collar 2. Leaflets deeply grooved above between veins, appearing plicate ..........................................................… 9. Z. roezlii 2. Leaflets smooth to striate, not appearing plicate 3. Leaflets membranous, almost translucent 4. Leaflet margins coarsely toothed, at least some teeth biserrate …...…........................… 3. Z. disodon 4. Leaflet margins entire or with only a few uniserrate teeth apically ………… 5. Z. hymenophyllidia 3. Leaflet papyraceous to coriaceous 5. Leaflets entire or rarely with a few minute teeth apically 6. Petiole smooth, leaflet margins strongly revolute …...................... 2. Z. boliviana 6. Petiole with at least a few prickles, leaflet margins flat 7. Petiole and rachis densely prickled throughout, prickles often branched ..…...... 1. Z. amazonum 7. Petiole sparsely to densely prickled in lower half, prickles unbranched, rachis smooth 8. Leaflet surfaces striolate, veins obvious …….................... 4. Z. gentryi 8. Leaflet surfaces smooth, veins obscure ….................…. 6. Z. lecointei 5. Leaflets obviously and variously toothed 9. Leaflets long linear-lanceolate, marginal teeth aculeate and nearly at right angles, strongly falcate basally ..................................... 8. Z. poeppigiana 9. Leaflets elliptic to oblong-elliptic, marginal teeth at an acute angle, leaflets straight or only slightly subfalcate basally 10. Petiole with prickles, leaflet surface smooth veins obscure ……….........…... 10. Z. ulei 10. Petiole smooth, leaflet surface striolate, veins obvious …......................…… 11. Z. urep

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Fig. 14.1. Distribution map of Zamia amazonum D.W. Stevenson, Z. bolivana (Brongniart) A. de Candolle, Z. disodon D.W. Stevenson & Sabato, Z. gentryi Dodson, Z. hymenophyllidia D.W. Stevenson and Z. lecointei Ducke in Bolivia, Ecuador and Peru.

Fig. 14.2. Distribution map of Zamia macrochiera D.W. Stevenson, Z. poeppigiana Martius & Eichler, Z. roezlii Linden, Z. ulei Dammer and Z. urep Wallnöfer in Bolivia, Ecuador and Peru.

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1. ZAMIA AMAZONUM D.W. Stevenson (Fig. 14.3), (2001) Flora de Colombia 21, 33 and Fig. 3 TYPE: BRAZIL. Amazonas, Confluence of Rio Tauri and Rio Icana, D. Stevenson 886 (HOLOTYPE: INPA; ISOTYPES: COL, MO, NY, U) Stem subterranean, 3–8 cm in diameter. Cataphylls triangular basally, linearlanceolate apically, 3–8 cm long, 1–2 cm wide. Leaves 2–6, 0.5–2.5 m long, oval to elliptic; petiole 0.5–1 m long, often ferrugineous, armed with small to stout branched prickles; rachis 0.5–1 m long, with 10-30 subopposite pairs of leaflets, armed with prickles in the lower third. Leaflets chartaceous to papyraceous, oblong-lanceolate to lanceolate, acuminate at apex, denticulate in upper half, 15–20 cm long, 2–4 cm wide. Pollen strobili 2–6, cylindrical, brown, 6–10 cm long, 1–2 cm in diameter; peduncle 8–15 cm long. Ovulate strobili usually solitary, dark

Fig. 14.3. Zamia amazonum D.W. Stevenson. (A) Habit. (B) Habit. (C) Detail of a leaflet and rachis. (D) Ovulate strobilus.

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red-brown, 10–15 cm long, 3–5 cm in diameter; peduncle 5–8 cm long. Seeds with a red outer fleshy layer, ovoid, 1 cm long, 0.5 cm in diameter. A widespread species found in Amazonian areas of Brazil, Colombia, Ecuador, Peru (Fig. 14.1), Venezuela and disjunct in the Chocó of Colombia. ECUADOR. NAPO: Limoncocha, Maddison et al. 5419 (AAU, F, FTG, K, QCA, SEL, US); Jatun Sacha, D. Neill 9461 (MO). PERU. LORETO: Fundo Ciudadela, Rio Itaya, J. Schunke 14240 (F, NY): Iquitos, R. Tryon & A. Tryon 5185 (F).

DISTRIBUTION

ETYMOLOGY The specific epithet refers to the wide distribution of this species throughout the upper Amazon basin.

Zamia amazonum is a variable species that most closely resembles Z. lecointei Ducke and Z. muricata Willdenow. However, it can be distinguished from these two species on the basis of the rachis being densely tomentose when young and being densely prickled with the prickles often branched. The seed cone is smaller, being < 15 cm, including the peduncle, than the seed cones of Z. lecointei and Z. muricata, which are longer than 15 cm. DISTINGUISHING FEATURES

Fairly common locally throughout its range. However, Z. amazonum is known from only two collections in Peru and two collections in Ecuador and is not known from Bolivia, but is to be expected in the Amazonian region of the latter. Not yet listed in the 1997 IUCN Red List of Threatened Plants but the status throughout its range would be R,II,R.

CONSERVATION STATUS

2. ZAMIA 540

BOLIVIANA

(Brongniart) A. de Candolle (1868) Prodromus 16(2),

TYPE: BOLIVIA. Coteaux de Sn. Xavier, A. d’Orbigney 663 (LECTOTYPE: P; ISOLECTOTYPES: P, W; fide Stevenson and Sabato, 1986). Ceratozamia? boliviana Brongniart (1846) Annales des Sciences Naturelles, Series 3, Volume 5, 9. Z. brongniartii Weddell (1849) Annales des Sciences Naturelles, Series 3, Volume 13, 249 and Planche III, nomen illegitimum, superfluous name for Ceratozamia boliviana Brongniart. Stem subterranean and tuberous, 3–10 cm in diameter. Cataphylls from 1–2 cm long, sheathing at first, with a pair of inconspicuous stipules. Leaves 2–5, 0.3–0.7 m long; petiole smooth; rachis bearing 5–20 pairs of opposite to subopposite leaflets. Leaflets linear-lanceolate to lanceolate, 12–25 cm long and 0.5–1.5 cm wide, margins entire and strongly revolute, rarely with 2–10

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indistinct teeth in the upper third, somewhat pungent apically. Pollen strobili usually solitary, cylindrical, slender, pedunculate, tan to brown, 0.5–1.5 cm long and 0.6–0.8 cm in diameter, peduncle 2–4 cm long. Ovulate strobili oblong, acuminate apically, pedunculate, brown, 12–15 cm long and 3–5 cm in diameter, peduncle 8–10 cm long. Seeds with a red to orange-red sarcotesta, ovoid, 1–2 cm long. Known only from Beni, Cochabamba and Santa Cruz in Bolivia (Fig. 14.1) and a single collection from adjacent Mato Grosso of Brazil, where it grows in sandy well-drained soils. It grows essentially under conditions similar to those for Caribbean species of Zamia. BOLIVIA. BENI: U. Patino s.n. (GH); El Porvenir, C. Paz & E. Polanco 205 (MO); J.C. Solomon 6244 (MO); Trinidad, E. Werdermann 2486 (MO); Lake Rogoaguado, C.E. White 1543 (GH, K, NY, P, PH). COCHABAMBA: Campero, C. Antezana 1029e (BOLV). SANTA CRUZ: Lomerio, J.R. Abbott 16303 (USZ); Cerro Puquio Norte, J.R. Abbott & A. Jardim 16630 (USZ); Huanchaca II, A. Carriónet et al. 406 (USZ, MO); M. de Castelnau s.n. (P); San Matias, R. Guillén et al. 2249 (USZ); Porongo, A. Henderson & M. Morales 767 (NY); Nuflo de Chavez, M. Hopkins 117 (NY), 175 (NY), 204 (NY); Velasco, M. Nee 41141 (MO, NY), 41468 (NY); Nuflo de Chavez, T. Killeen 1164 (F, MO, NY), 2223 (F, MO, NY); Nuflo de Chavez, A. Krapovickas & A. Schinini 32209 (F, G, MO); S. Moore 389 (BM); Aserradero Cerro Pelao, M. Saldías et al. 2965 (USZ); San Ignacio, E. Schmidt 183 (M); J. C. Solomon & S. Urcullo 14152 (MO); Lomerio, Marisol, Toledo et al. 526 (USZ); Mato Grosso, Weddell 3331 (P). BRAZIL. MATO GROSSO: Bantel et al. 1342 (MG). DISTRIBUTION

ETYMOLOGY

Based upon its presumed endemism in Bolivia at the time of its

description. DISTINGUISHING FEATURES This species is very similar in appearance to Caribbean species of Zamia, particularly Z. integrifolia Linnaeus filius in Aiton and Z. portoricensis Urban. It may be distinguished from these two species by its more or less sharp leaflet tips, strongly revolute leaflet margins and brown cones. SYSTEMATIC AND NOMENCLATURAL HISTORY Zamia boliviana was originally described as Ceratozamia boliviana by Brongniart, most probably because he had no cones of the species at the time of his description. In fact, he questioned the assignment of this species to his newly described genus, Ceratozamia. Consequently, when cones became available, Weddell redescribed the species as Zamia brongniartii, while at the same time citing Ceratozamia boliviana Brongniart as a synonym as well as citing its type. Because the specific epithet was available at that time for transfer to Zamia, Weddell created a superfluous name. This was later corrected by A. de Candolle. Also, some material cited by Weddell as Z. brongniartii was thought by him to be from the Mato Grosso of Brazil but is in fact from Bolivia (Sabato, 1990). However, a single collection, Bantel et al. 1342, of this species from the

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Mato Grosso of Brazil is in the collectionsof the Museo Goeldi (MG). This species is commonly collected but there is no in-formation on the size or extent of the populations and thus it is hard to assess its status. It may well be collected simply because it is a novelty. This leads one to think that it is very rare. 1997 IUCN Red List of Threatened Plants Category R,II,R.

CONSERVATION STATUS

3. ZAMIA DISODON D.W. Stevenson & Sabato (Fig. 14.4), (2001) Flora de Colombia 21, 38–39 and Fig. 4 TYPE: COLOMBIA. Antioquia, D. Restrepo et al. s.n. (HOLOTYPE: COL; ISOTYPE: NY).

Fig. 14.4. Zamia disodon D.W. Stevenson & Sabato. (A) Habit. (B) Leaflets and rachis.

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Stem to 50 cm, 5–8 cm in diameter. Cataphylls triangular basally, linear-lanceolate apically, 3–6 cm long, 1–2 cm wide. Leaves 2–4, erect or slightly recurved, oblong, 50 cm long; petiole terete, to 25 cm long, sparsely armed with small prickles; rachis terete, usually unarmed, to 25 cm long, 3–5 pairs of leaflets. Leaflets membranous, elliptic, subfalcate, acute at apex, margins serrate and always with some doubly serrate teeth near the apex, the median ones 12–20 cm long, 6–10 cm wide. Strobili unknown. Known only from the type locality and another nearby population in Antioquia, Colombia, and disjunct to a single locality in Peru (Fig. 14.1). PERU. HUÁNUCO: Pachitea, Llullapichis, R. Dressler 4938, 4939 (NY); Puerto Inica, R. Foster 8688 (MO).

DISTRIBUTION

ETYMOLOGY

The specific epithet is derived from the doubly serrate leaflets.

DISTINGUISHING FEATURES Zamia disodon is the only cycad with doubly toothed leaflet margins. In addition, it is the only Zamia besides Z. hymenophyllidia D.W. Stevenson with transparent leaflets. However, Z. hymenophyllidia has entire to minutely toothed margins. In many respects, Z. disodon resembles an acaulescent to short trunked Z. obliqua A. Braun with transparent biserrate leaflets.

Because Zamia disodon has been so infrequently collected it is assumed that the species is very rare. However, it is apparently available in local markets in Colombia (Ian Turner, Zimbabwe, 1996, personal communication). Because cones have not been seen, reproduction is assumed to be limited. Rodrigo Bernal (Colombia, 2002, personal communication) believes that the habitat in Colombia is severely threatened. In Peru, very little is known about this species other than the fact that two sterile collections have been made. More fieldwork is needed to assess the situation. Not yet listed in the 1997 IUCN Red List of Threatened Plants but the status throughout its range would be I,II,I.

CONSERVATION STATUS

4. ZAMIA

GENTRYI

Dodson (1998) Novon 8, 12–14 and Fig. 1a–f

TYPE: ECUADOR. Esmeraldas, C.H. Dodson & A.H. Gentry 17520A (HOLOTYPE: QCNE; ISOTYPES: AAU, MO, NY, RPSC, SEL, U). Stems up to 1.5 m long, generally prostrate when terrestrial or U-shaped when growing on fallen logs, 5–15 cm in diameter, smooth. Cataphylls up to 12 cm long and of two forms, either elongate triangular or with a long acuminate apex. Leaves 5–9, 0.5–2.5 m long; petiole 45–90 cm long, very densely prickled; rachis with 15–25 (less in juvenile plants) pairs leaflets, densely prickled in lower half. Leaflets long-lanceolate and subfalcate, chartaceous to membranous, margins entire, attenuate basally, acute apically, the larger median ones 10–40 cm long, 3.5–6 cm wide. Pollen strobili 1–7, wine-red, cylindrical, 30–40 cm long, 3–4 cm in

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diameter; peduncle 20–25 cm long, decumbent. Ovulate strobili singular, redbrown, narrowly ovoid to cylindrical, 20–30 cm long, 8–12 cm in diameter, peduncle short. Seeds obovoid, 3.5 cm long, 1.7 cm in diameter, pink to red. Endemic to Ecuador (Fig. 14.1), where it grows at altitudes from 300 to 800 m in extremely wet premontane (cloud) forest on compact clay soils. Although having a trunk, Zamia gentryi is generally prostrate along the soil surface. Contrary to some reports, this species is not epiphytic. ECUADOR. CARCHI: Canton Tulcan, G. Tipaz et al. 1878 (QCNE). ESMERALDAS: Lita to San Lorenzo, B. Øllgaard et al. 98726 (AUU, QCNE); C. Dodson et al. 17107 (MO, QCNE), 19098 (QCNE); H. Luther et al. 1235 (SEL). DISTRIBUTION

ETYMOLOGY Named in honour of Alwyn H. Gentry, intrepid botanist and botanical explorer of the neotropics who had an early death as the result of an aeroplane crash in Amazonian Peru. DISTINGUISHING FEATURES The smooth prostrate trunks, combined with several leaves up to 2.5 m long bearing several narrow entire leaflets, serve to distinguish Zamia gentryi from other species of Zamia. This species appears most similar in many aspects to Z. chigua Seemann from the Chocó of Colombia and northwestern Panama. Most plants of the latter in fact have semi-prostrate trunks with numerous adventitious roots on the bottom surface and are without any subterranean stem. Both species have very thin leaflets with entire margins and appear slightly grooved, but not to the extent of Z. skinneri Warszewicz ex A. Dietrich and its allies. The two species differ in that Z. gentryi has neither as many leaflets nor imbricate leaflets as in Z. chigua. Also, the pollen cones of the former are larger than those of the latter and the leaflets are much broader. Juvenile plants of both species are quite difficult to distinguish from one another. CONSERVATION STATUS This species is known only from an area that is very poorly known botanically and is presumed to have a wider distribution. For the present time it is considered very rare pending further data. Not listed in the 1997 IUCN Red List of Threatened Plants.

5. ZAMIA HYMENOPHYLLIDIA D.W. Stevenson (Fig. 14.5), (2001) Flora de Colombia 21, 43–44 and Fig. 6 TYPE: COLOMBIA. Amazonas, D. Cardenas et al. 10089 (HOLOTYPE: COAH; ISOTYPE: NY). Stem subterranean and tuberous, 2–4 cm in diameter. Cataphylls triangular basally, linear-lanceolate apically, membranous, 2–3 cm long, 0.5–1 cm wide. Leaves 2–5, erect, oblong, 30–70 cm long; petiole terete, to 35 cm long, armed with very small prickles; rachis terete, usually unarmed, to 20–35 cm long, 4–10 pairs of

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Fig. 14.5. Zamia hymenophyllidia D.W Stevenson. (A) Habit. (B) Leaflet. (C) Pollen strobilus. (D) Microsporophyll, abaxial view. (E) Microsporophyll, adaxial view. (F) Ovulate strobilus.

leaflets. Leaflets membranous, elliptic to elliptic-lanceolate, long acuminate apically, cuneate to oblique basally, margins entire or rarely with a few diminutive apical teeth, 12–15 cm long, 1–2 cm wide. Pollen strobili brown, ovoid, 1–3 cm long, 0.1–0.3 cm in diameter; peduncle 10–15 cm long; microsporophylls with both abaxial and a few (1–3) adaxial sporangia. Ovulate strobili dark red-brown, cylindrical to ovoidcylindrical, to 5 cm long, 3–4 cm in diameter; peduncle to 15 cm long, 0.5 cm in diameter. Seeds red to orange-red, 1–1.2 cm long, 0.5–0.8 cm in diameter. Only four small populations are known, three in south-eastern Amazonian Colombia and one in adjacent north-eastern Peru (Fig. 14.1). PERU. LORETO: Maynas, Pebas, Brillo Nuevo, M. Balick et al. 1035 (NY); Plowman et al. 6773, 7065, 7255, 7256 (F, GH).

DISTRIBUTION

ETYMOLOGY

The specific epithet refers to the extremely thin and almost trans-

parent leaflets. DISTINGUISHING FEATURES Zamia hymenophyllidia is most similar to the Colombian species Z. melanorrhachis D.W. Stevenson. Both species are unique among the cycads in having extremely long thin peduncles (up to 30 cm long and 1–3 mm in diameter) terminated by very small pollen cones (1–3 cm long and 1–3 mm in

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diameter). Zamia hymenophyllidia has membranous, elliptic, long acuminate leaflets in contrast to the papyraceous, lanceolate, generally acute leaflets of Z. melanorrhachis. The leaflet margins of Z. hymenophyllidia are generally entire and, if toothed, the teeth are inconspicuous and apical. In contrast, Z. melanorrhachis has well-developed marginal teeth. Living plants of Z. melanorrhachis have a dark purple to black rachis, a feature not found in Z. hymenophyllidia. CONSERVATION STATUS Zamia hymenophyllidia was discovered only in the past 3 years in three small populations. The plants are reproductive and produce seeds and seedlings. Little is known about its biology and distribution but the paucity of collections indicates that it is rare. Not yet listed in the 1997 IUCN Red List of Threatened Plants but the status throughout its range would be R,II,R.

6. ZAMIA LECOINTEI DUCKE (Fig. 14.6), (1915) Archivos do Jardim Botânico do Rio de Janeiro 1, 9–10 and Tabula 1 TYPE: BRAZIL. Pará, Rio Erepecurú, 2 October 1913, Ducke MG 15027 (HOLOTYPE: MG). Z. obidensis Ducke, (1922) Archivos do Jardim Botânico do Rio de Janeiro 3, 20. TYPE: BRAZIL. Pará, Rio Branco de Obidos, March 1918, Ducke s.n. (Museu Goeldi 17015) (HOLOTYPE: MG; ISOTYPE: F). Z. ulei subsp. lecointei (Ducke) Ducke, (1935), Archivos do Instituto Biologia Vegetale do Rio de Janeiro 2, 27–28. Z. jirijirimensis R.E. Schultes, (1953) Mutisia 15, 2–5 and Fig. p. 5 s.n. TYPE: COLOMBIA. Amazonas: Rio Apaporis, Raudal de Jirijirimo, March 1951, R.E. Schultes 12101 (HOLOTYPE: GH–2 sheets) Stem subterranean and tuberous, 5–8 cm in diameter. Cataphylls triangular basally, linear-lanceolate apically, 3–6 cm long, 1–2 cm wide. Leaves 2–4, erect or slightly curved, oblong, 1–2 m long; petiole terete, to 75 cm long, sparsely armed with stout prickles; rachis terete, usually unarmed, to 1 m long, 30–40 pairs of leaflets. Leaflets subcoriaceous to coriaceous, linear-lanceolate, subfalcate, long acuminate at apex, margins entire or rarely with 2–3 indistinct teeth near the apex of lower margin, the median ones 30–37 cm long, 1–2 cm wide. Pollen strobili 2–6, cylindrical, cream to light brown, 6–10 cm long, 1–2 cm in diameter; peduncle 10–20 cm long. Ovulate strobili usually solitary, brown, 10–15 cm long, 3–5 cm in diameter; peduncle 5–8 cm long. Seeds with a red outer fleshy layer, ovoid, 3 cm long, 2 cm in diameter. 2n = 16 (Caputo et al., 1996). In Amazonas and Bolivar, Venezuela, and Pará, Brazil, north of the Amazon River to central Colombia and Brazil. For Bolivia, Ecuador and Peru, known from only a single collection in Peru (Fig. 14.1). PERU. LORETO: Ucayali, J. Schunke 14269 (F, NY).

DISTRIBUTION

ETYMOLOGY The specific epithet honours Paul LeCointe who lived in Obidos, Brazil and who accompanied Adolf Ducke when the species was discovered.

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Fig. 14.6. Zamia lecointei Ducke. (A) Habit. (B) Leaflet. (C) Ovulate strobilus.

DISTINGUISHING FEATURES Zamia lecointei is most similar to Z. muricata. The two taxa share a common distribution pattern but are not sympatric and prefer different habitats. Zamia lecointei grows in open dry areas of sandy to pure sand soils whereas Z. muricata grows as an understorey plant in mesic conditions in wet clay soils. Consequently, Z. lecointei has subcoriaceous to coriaceous, linear-lanceolate, subfalcate leaflets that are entire or with only 1–3 indistinct apical teeth. By contrast, Z. muricata has chartaceous to papyraceous, oblong-lanceolate to lanceolate,

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inequilateral leaflets that are clearly denticulate in the upper half of both margins. In the open in direct sun, or as an understorey in secondary vegetation, the leaflets often become narrower and quite coriaceous with entire margins, but in more shaded conditions the leaflets are wider, thinner and show well-developed serrations in the upper third. Plants growing in extremely dry, sandy soil were described as Z. jirijirimensis. Ducke (1915) described Zamia lecointei and mentioned another probable new Zamia, which he described as Z. cupatiensis in 1922. The type, illustration (Ducke, 1915, tabula 1) and description of Z. lecointei all show linear-lanceolate leaflets. Ducke’s (1915) concept of Z. ulei is presented in tabula 2 of the same paper; this bears little resemblance to the type or description (Dammer, 1907) of Z. ulei Dammer, which has ovate-lanceolate to elliptic leaflets. As a result of his misconception, Ducke (1922) described Z. cupatiensis Ducke. The description and photograph of Z. cupatiensis (Ducke 1922, tabula 2) match the photograph and isotypes of Z. ulei. In the same paper, Ducke (1922) also described Z. obidensis Ducke which was intermediate between his Z. lecointei and his Z. cupatiensis. Because Ducke mistakenly thought that Z. ulei had linear-lanceolate leaflets, he (Ducke, 1935) considered Z. lecointei to be a subspecies, Z. ulei subsp. lecointei. This problem was compounded by Schuster (1932). As a result, Schultes (1953) redescribed Z. lecointei as Z. jirijirimensis. However, the type specimens for these two names are identical. Thus, Z. cupatiensis is a synonym of Z. ulei, and Z. jirijirimensis is a synonym of Z lecointei. Moreover, Z. obidensis is a shade and/or juvenile form of Z. lecointei.

SYSTEMATIC AND NOMENCLATURAL HISTORY

Zamia lecointei is most common in Bolivar, Venezuela, in both pristine and disturbed habitats. Seed set appears high and the populations are not at present threatened by development or destruction. Collections in Colombia indicate that it is locally common with good seed set. It does well in minor disturbed situations. However, because Z. lecointei is known from only a single collection from Peru, it is assumed that the species is very rare in Peru and does not occur in either Ecuador or Bolivia even though suitable habitat does occur in the latter two countries. Not listed in the 1997 IUCN Red List of Threatened Plants but the status throughout its range would be R,II,R.

CONSERVATION STATUS

7. ZAMIA

MACROCHIERA

D.W. Stevenson, species nova (Fig. 14.7)

TYPE: PERU. LORETO: Maynas, Pebas, Rio Amiyacu, D. Stevenson 1160 (HOLOTYPE: NY; ISOTYPES: AMAZ, FTG, NY, U) Zamia manicata Regel praesertim collo glanduliformi ad foliolorum basi sito oblongoelliptico e basi cuneato spiraliter adscendenti ultra medium serrato, distaliter concavo inter alia diversa. Stem subterranean, subcylindric to cylindric, 10–20 cm in diameter. Cataphylls triangular basally, long acuminate apically, 3–8 cm long, 1–2 cm wide. Leaves 1–3,

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Fig. 14.7. Zamia macrochiera D.W. Stevenson. (A) Habit. (B) Leaflets. Gland-like structure at the juncture of petiole and lamina: (C) adaxial view, (D) abaxial view, (E) apical view and (F) basal view. (G) Ovulate strobilus.

0.5–3.5 m long; petiole 0.2–2 m long, slightly to densely prickled; rachis often with prickles in lower third, with 10–30 pairs of leaflets. Leaflets with distinct petiolule and abaxial gland-like collar or flap that curves upward to touch the lamina forming a tunnel at the juncture, oblong to long-elliptic, margins serrate in upper third, cuneate basally, acute to acuminate apically, the larger median leaflets 20–45 cm long, 5–15 cm wide. Pollen strobili cream to tan, cylindrical, 4–6 cm long, 1–1.5 cm in diameter; peduncle 15–30 cm long. Ovulate strobili wine-red to dark red-brown, cylindrical to ovoid-cylindrical, 10–15 cm long, 4–7 cm in diameter. Seeds red, 1–1.5 cm long, 0.5–0.8 cm in diameter. 2n = 18 (Aldo Moretti, Italy, 1993, personal communication). DISTRIBUTION Zamia macrochiera occurs in rainforest and secondary forest from 100 m to 300 m in a limited area of Peru (Fig. 14.2). PARATYPES: PERU. LORETO: Maynas, Rio Napo, M. Mathias s.n. (MO, NY); Pebas, T. Plowman et al. 6937 (F, GH), 7254 (F, GH, K, NY, U), 7275 (F, GH, K).

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The specific epithet refers to the large gland-like collar at the

leaflet base. The petiolule and gland-like collar occur among cycads only in Zamia manicata Linden ex Regel (Stevenson, 1990, 2001) and Z. macrochiera. However, these structures are not present in seedling leaves, are only diminutively present in juvenile leaves but become distinct in adult leaves of both species. Also, in transplanted adult plants, the structures may not be produced in the first set of leaves after transplanting. The most obvious difference between the two species is in the morphology of the gland-like collar. The collar in Z. manicata is a rim-like structure, in contrast to that of Z. macrochiera where it is a welldeveloped flap of tissue that curves up to meet the lamina forming a tunnel (Fig. 14.7). In addition, both the leaves and ovulate strobili of Z. macrochiera are much larger than those of Z. manicata. This is the undescribed species discussed by Wrinkle (1993). DISTINGUISHING FEATURES

CONSERVATION STATUS Zamia macrochiera has been collected only four times in the past 25 years and all collections have been near the type locality. Although some seedlings were seen at the type locality, only one seed cone has been observed. However, the species appears to be threatened by continual habitat disturbance. The type locality was being converted from secondary forest into a communal garden. Not yet listed in the 1997 IUCN Red List of Threatened Plants.

8. ZAMIA POEPPIGIANA Martius & Eichler, (1863) Flora Brasiliensis 4(1), 414–416 and Tabula 109 TYPE: PERU. Maynas Alto, Toache River, 1830, Poeppig s.n. (LECTOTYPE: F ex Herbario Musei Palatino Vindobensis; ISOLECTOTYPE: GH ex Herbario Musei Palatino Vindobensis; fide Stevenson and Sabato, 1986). Z. lindenii Regel ex André, (1875) L’Illustration Horticole 22, 23 and Planche 195. LECTOTYPE: Planche 195 in L’Illustration Horticole 23, (1875) (fide Stevenson and Sabato, 1986). Aulacophyllum lindenii (Regel ex André) Regel, (1876) Gartenflora 25, 141. Z. baraquiniana Regel, (1876) Acti Horti Petropolitani 4(4), 308–309. TYPE: ex Horto Petropolitano, Regel s.n. (HOLOTYPE: LE). Z. wielandii Schuster, (1932) Das Pflanzenreich IV.1, Heft 99, 149, nomen illegitimum, superfluous name for Z. baraquiniana Regel. Stem arborescent, to 3 m tall and 25 cm in diameter. Cataphylls cuneate basally and acuminate apically, to 2 cm wide and 4 cm long. Leaves 10–15, 1–3 m long; petiole with numerous small prickles, 30–70 cm long; rachis with prickles in lower third, 20–40 pairs of leaflets. Leaflets long-lanceolate, falcate basally, acuminate to acute apically, margins strongly spinulose in upper third with serrations at nearly 90° and 0.5–1 cm apart; median leaflets 15–40 cm long, 2–4 cm wide.

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Pollen strobili cream to tan, long cylindrical, 20–30 cm long, 3–5 cm in diameter; peduncle 5–8 cm long; microsporophylls with sterile tip composed of six steeply inclined facets surrounding a centrally depressed terminal facet. Ovulate strobili tan to brown, cylindrical to ovoid-cylindrical, 25–40 cm long, 10–15 cm in diameter. Seeds red, oblong, distinctly flattened, 1–1.5 cm long, 0.5–0.8 cm in diameter. 2n = 18 (Norstog, 1980). Known from the coastal plains and foothills of the Cordillera Occidental in Ecuador and rich humus soils of Acre, Brazil and south-western Colombia and eastern Peru (Fig. 14.2). ECUADOR. E. André 3687 (F, GH, K, NY, P, US); F. Barclay 709 (US); H. Eggers 14034 (GH); C. Horn s.n. (US); F. Lehmann 658 (G); A. Rimbach 85, (F), 252 (US). AZUAY: Huigra, J.N. Rose & G. Rose 22613 (US); Saraguro, J. Steyermark 52786 (F, NY, P). EL ORO: Balslev et al. 62526 (AAU, COL, QCA). BOLIVAR: Balsapamba, T. Lockwood 825 (GH). ESMERALDAS: Fila de Bilsa, A. Gentry et al. 72867 (MO); Coronel C. Concha, P. Maas et al. 2920 (U); Esmapaidas, P. Maas et al. 2020 (U); Rio Mira, M.G. Patwa s.n. (US). GUAYAS: Naranjal, G. Harling & L. Andersson 19417 (GB); F. Lehmann 5292 (K). LOS RIOS: Jaunche, C. Dodson & A. Gentry 12698, 7991 (MO, SEL); C. Dodson et al. 7991 (MO, SEL); Rio Palenque, A. Gentry & C. Dodson 18045 (MO); K. Norstog 80–5 (FTG). PICHINCHA: Congoma Grande, L. Kvist 40203 (AAU, MO, NY); Manabí, G. Harling & L. Andersson 24751 (GB); Toache-Las Pampas, C. Dodson & A. Gentry 9715, 13694 (MO, SEL). PERU. AMAZONAS: Bagua, T. Plowman 5536 (GH). HUÁNUCO: Tingo Maria, T. Plowman et al. 7575 (F, GH, NY), 11232 (F, GH, INPA, NY); LORETO: Lower Rio Huallaga, L. Williams 5373 (F, US); Maynas, L. Williams 3794 (F). MADRE DE DIOS: Tambopata, M. Alexiades 1322 (NY); Cocha Cashu Station, R. Foster 5852 (F). SAN MARTIN: Campanilla, J. Schunke 4200 (F); Tarapoto, F. Montes 57 (F, NY); T. Plowman 7601 (F); M. Rimachi Y. 5185 (NY), 5356 (MO, NY); Tocache Neuvo, A. Gentry et al. 25710 (MO, NY); T. Plowman & J. Schunke 11543 (F). TUMBES: Tumbes, C. Díaz et al. 5117 (MO); Matapalo, C. Díaz et al. 7500 (MO); D. Simpson & J. Schunke 428 (COL, F, GH, NY, US). DISTRIBUTION

ETYMOLOGY The specific epithet honours Eduard Poeppig, who first collected the species in Peru. DISTINGUISHING FEATURES Zamia poeppigiana is readily identified by its falcate linear leaflets with evenly spaced teeth at nearly right angles to the margin. Zamia poeppigiana and Z. lindenii Regel ex André are here considered conspecific. The types of both are identical but the former is from the lower Pacific Andean slopes of Ecuador whereas the latter is from the lower Amazonian slopes of Peru and Colombia. The seeds of Z. poeppigiana are unique within Zamia because of their somewhat flattened oblong shape. By contrast, the seeds of Z. lindenii are reported to be unflattened and oval in shape, as in all other known species of Zamia, but observations on both fresh seeds and herbarium material show a flattened oblong shape.

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Zamia poeppigiana is widely but sporadically distributed. Local populations exhibit good seed set and seedling establishment. Unlike Z. obliqua, Z. poeppigiana appears to produce seed cones when the stems are not yet arborescent, thus reducing the threat from habitat destruction. Not yet listed in the 1997 IUCN Red List of Threatened Plants.

CONSERVATION STATUS

9. ZAMIA ROEZLII Linden, (1873) Linden Catalogue des Plantes Nouvelles No. 90, 10 NEOTYPE: Planches 133–134 in L’Illustration Horticole 20 of 1873, (fide Stevenson and Sabato, 1986). Aulacophyllum roezlii (Linden) Regel, (1876) Gartenflora 25, 141. Stem arborescent, to 7 m tall. Leaves 5–10, 1–3 m long; petiole 0.5–1 m long, sparsely to densely prickled; rachis with 10–20 pairs of leaflets, occasionally with a few prickles in the lower third. Leaflets linear-lanceolate, grooved between the veins on the adaxial surface, cuneate basally, acute apically, margins entire, 30–50 cm long, 12–15 cm wide. Pollen strobili cream to tan, cylindrical to elongate-cylindrical, 20–30 cm long, 4–6 cm in diameter. Ovulate strobili brown, short pedunculate, cylindrical to ovoid-cylindrical, 30–60 cm long, 10–20 cm in diameter. Seeds red, ovoid, 1.5–2.5 cm in diameter. 2n = 22, 24, 25, 26 (Norstog, 1981). DISTRIBUTION Along coastal Chocó, Colombia, and contiguous coastal Ecuador (Fig. 14.2). ECUADOR. ESMERALDAS: Zapollo Grande, A. Barfod & F. Skov 60116 (AAU, NY, QCA, QNA); San Lorenzo, C. Dodson 19622 (RPSC); C. Dodson & A. Gentry 19048 (RPSC); C. Dodson & T. Neudecker 19083 (QCNE, RPSC); H.E. Luther s.n. (MO); David Neill et al. 11792 (MO, QCNE); F Nicolalde & J. Palacios 234 (QCNE); Reserva Awa, G. Tipaz et al. 2242 (0MO, QCNE); Cotacachi Cayapas, G. Tipaz et al. 2255 (MO, QCNE); M. Tirado et al. 646 (QCNE); Communa Corriente Grande, A. Yanez 1413 (QCNE). NAPO: Jatun Sacha, cultivated from seed from Reserva Awa, Esmeraldas, D. Neill 11160 (MO, QCNE). ETYMOLOGY The specific epithet honours Benedict Roezl, prodigious plant collector who travelled throughout Mexico, Central America and South America in the latter half of the 19th century and who first collected the species.

Zamia roezlii is the largest of the South American Zamia plants and is unmistakable with its massive trunk, leaves and strobili. This species appears to be part of a complex composed of Z. dressleri D.W. Stevenson, Z. neurophyllidia D.W. Stevenson and Z. skinneri in Panama, Z. amplifolia hort. Bull ex Masters and Z. roezlii in the Chocó of Colombia and adjacent Ecuador, and Z. wallisii A. Braun in northern Antioquia, Colombia. This grouping is based upon the common feature of a plicate appearance of the leaflets. This character,

DISTINGUISHING FEATURES

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along with simultaneous rather than sequential leaf production, prompted Regel (1876) to erect the segregate genus Aulacophyllum. However, no other synapomorphies have been found to support Aulacophyllum as a genus (Sabato, 1990). Moreover, the distinction between simultaneous and sequential leaf production in Zamia seems problematic at best. However, Z. roezlii is readily distinguishable from other species with deeply grooved leaflets by its falcate, linear and entire leaflets. Zamia roezlii is locally abundant and produces very large seed cones and numerous seeds and seedlings. However, seed cones are produced only by arborescent plants and, under continual disturbance, seed production will be severely diminished, resulting in high vulnerability for the species. 1997 IUCN Red List of Threatened Plants Category R,II,V.

CONSERVATION STATUS

10. ZAMIA ULEI Dammer, (1907) Verhandlungen des Botanischen Vereins der Provinz Brandenburg 47, 117–118 TYPE: BRAZIL. Cachoeira oberer Rio Jura, May 1901, E. Ule 5523 (LECTOTYPE: HBG; ISOLECTOTYPES: L, G, MG, K, F-fragment; fide Stevenson and Sabato, 1986). Z. cupatiensis Ducke, (1922) Archivos do Jardim Botânico do Rio de Janeiro 3, 20 and Planche 1. LECTOTYPE: Planche 1 as above. Stem subterranean and tuberous, tapering distally, 4–6 cm in diameter. Leaves 2–4, 1–1.5 m long, broadly ovate; petiole to 1 m long, terete, generally armed with numerous prickles; rachis to 50 cm long, with 3–6 pairs of subopposite leaflets, often armed with prickles in the lower third. Leaflets sessile, papyraceous to subcoriaceous, oblong-elliptic to elliptic-ovate, sometimes slightly falcate, obtuse and constricted at base, acute to short-acuminate at apex, 12–15 teeth on each margin in the upper one-half, the median ones 12–20 cm long, 6–10 cm wide. Pollen strobili usually 2–5, tan, cylindrical, 6–10 cm long, 1–2 cm in diameter; peduncle 6–8 cm long. Ovulate strobili usually solitary, brown, cylindrical, 18–20 cm long, 4–6 cm in diameter; peduncle 8–10 cm long. Seeds red, ovoid to oblong, 15 mm long, 8 mm in diameter. 2n = 26 (Caputo et al., 1996). North of the Amazon River in Pará and Rio Branco, Brazil and disjunct to the bordering regions of western Brazil and eastern Colombia, Ecuador and Peru (Fig. 14.7). ECUADOR. NAPO: Pastaza, D. Neill et al. 11136 (QCNE). PERU. LORETO: A. Gentry et al. 77429 (MO); Maynas, I. Cabrera 3351 (GH); T. Croat 18675 (MO); D. Daly et al. 6189 (AMAZ, NY); D. Simpson & J. Schunke 800 (F, GH, US); R. Schultes 8366 (GH); J. Schunke 14029 (F); R. Vásquez 1536, 17594 (MO), R. Vásquez & N. Jarmillo 15955 (MO); D. Stevenson 1161 (AMAZ, FTG, MO, NY, U). DISTRIBUTION

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MADRE DE DIOS: Iberia, R. Seibert 2158 (US); Tambopata, V.P. Baca et al. 143 (MO). ETYMOLOGY The specific epithet honours Eduard Ule, an Amazonian plant collector of the latter half of the 19th century, who first collected the species in Brazil.

Zamia ulei is similar to Z. obliqua but the latter always has obliquely inserted and basally falcate leaflets while Z. ulei always has symmetrical leaflets. Moreover, adult plants of Z. obliqua are arborescent in contrast to the acaulescent Z. ulei.

DISTINGUISHING FEATURES

Zamia ulei is fairly common in sporadic populations throughout its range. Seed set and seedling establishment appear to be high. Not yet listed in the 1997 IUCN Red List of Threatened Plants but the status throughout its range would be R,II,R.

CONSERVATION STATUS

11. ZAMIA UREP Wallnöfer, (1996) Linzer Biologische Beiträge 28(2), 1056–1058 and Fig. 1 TYPE: PERU. HUÁNUCO: Pachitea, Llullapichis, B. Wallnöfer 112–15788 (HOLOTYPE: W; ISOTYPES: LZ, USM). Stem subterranean, to 20 cm long, 2.5–5 cm in diameter. Cataphylls narrowly lanceolate, 3–4 cm long, 5–8 mm wide. Leaves 1–4, 40–70 cm long; petiole smooth, 20–40 (48) cm long, canaliculate adaxially at the base and flat distally; rachis without prickles, 8–15 cm long, 2–5 pairs of leaflets. Leaflets broadly lanceolate to elliptic, coriaceous, obliquely cuneate basally, acuminate apically, margins sharply serrulate in upper third, median leaflets 10–20 cm long, 3–6 cm wide. Pollen strobili 1–2, tan to light brown, cylindrical, 3–6 cm long, 0.6–1 cm in diameter; peduncle 18–22 cm long, 2–3 mm in diameter; microsporophylls with sterile tip composed of six steeply inclined facets surrounding a centrally depressed terminal facet, sporangia present on both the adaxial and abaxial surfaces of the fertile region. Ovulate strobili tan to light brown, cylindrical to ovoidcylindrical, 3.5–5 cm long, 1.5–2.5 cm in diameter; peduncle 13–16 cm long, 3–5 mm in diameter. Seeds unknown. Zamia urep is endemic to Peru (Fig. 14.2) and known only from the vicinity of the type locality where it occurs, from 250 to 750 m on stony hillsides with thin soils. PERU. HUÁNUCO: Pachitea, Llullapichis, Listabarth 11–11589, 12–11589, 14–1293 (USM, W); B. Wallnöfer 15–241188 (LZ, USM, W).

DISTRIBUTION

ETYMOLOGY

An anagram for Peru.

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DISTINGUISHING FEATURES Zamia urep can be distinguished by the combination of symmetrical almost perfectly elliptic to broadly lanceolate leaflets with sharply serrated margins, acuminate apices and unarmed petioles and rachis. In general appearance, Z. urep is most similar to Z. obliqua and looks like a smaller version of the latter. It differs from Z. obliqua in being a smaller plant with subterranean stems, lacking prickles on the petiole and rachis, and having more prominently toothed leaflet margins. Similarly, the cones are much smaller and with longer peduncles. Zamia urep also resembles Z. ulei in having elliptic leaflets and a subterranean stem, but differs from that species in having longer cone peduncles and no prickles on the petiole or rachis. CONSERVATION STATUS Zamia urep is known from only seven collections, all from essentially the same locality, even though over the past 50 years many expeditions have collected in the area where it is found. Neither seeds nor seedlings of this species have been seen so nothing is known of its reproductive capacity. Thus it is assumed that the species is quite rare. Not yet listed in the 1997 IUCN Red List of Threatened Plants.

Conclusions As yet there are very few collections of Zamia from Peru. Consequently, of the eight species known from Peru, six (Z. amazonum, Z. disodon, Z. hymenophyllidia, Z. lecointei, Z. macrochiera and Z. urep) are each known basically from single localities or small areas. Of these six species, two (Z. amazonum and Z. lecointei) are widespread in the upper Amazon basin in Brazil, Colombia and Venezuela. It is expected that they are much more widespread in Amazonian Peru. Zamia machrochiera and Z. urep are endemic to Peru and from poorly collected areas in terms of general botanical exploration. Although Z. hymenophyllidia is known also from Colombia, it is in a contiguous relatively unexplored area botanically and is found in only four small populations from a relatively small area. Again, it is expected that with more exploration this species will be found to have a wider distribution than current data indicate. The presence of Z. disodon in Peru represents a trans-Andean disjunct from the Darien of Colombia. It has been collected only twice in Peru and both collections are from the same locality, and perhaps, population. In Colombia, Z. disodon is known from only two collections from nearby localities. Because of the paucity of material from both Colombia and Peru, along with the disjunct distribution of Z. disodon, it is difficult to know if the materials from Colombia and Peru are truly conspecific. Until further material is collected, including cone material which is unknown at present, this species will remain enigmatic. The conservation status of Zamia disodon, Z. urep, Z. macrochiera and Z. hymenophyllidia is difficult to assess because of the lack of collections and population information. Moreover, there are very few plants of these species in cultivation so that information from this source concerning coning and growth patterns is not currently available.

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At present, Zamia boliviana is the only species of the genus known from Bolivia, where it is widely distributed in the Beni, Cochabamba and Santa Cruz Provinces. Not only are there numerous collections of Z. boliviana but many of these have cones, indicating that reproduction in these localities is good. It is expected that Z. poeppigiana and Z. ulei will be found in Bolivia in the poorly collected areas contiguous with Brazil and Peru where both species are well known. Ecuador has been more extensively explored in terms of cycad collections than either Bolivia or Peru. As a result more is known about population sizes, distribution and coning frequencies of Zamia species in Ecuador; much of this knowledge is the result of the interest and work of Dodson (1994, 1998). From his work we have a concept of successful reproduction and seedling establishment of Z. roezlii, Z. gentryi and Z. poeppigiana in Ecuador (Z. poeppigiana as treated here includes Z. lindenii). Zamia poeppigiana occurs on both sides of the Andes in Ecuador and Peru. The type for Z. poeppigiana is from the eastern side of the Andes whereas the type for Z. lindenii is from the western side of the Andes. Both types are of sterile material. However, in terms of leaf and leaflet morphology, all material from both sides of the Andes is identical and, in fact, unique within Zamia in having very uniformly and spreading marginal teeth on distinctly basally falcate leaves. Cones, as far as known, also appear identical in all plants assigned here to Z. poeppigiana. On the other hand, Calaway Dodson (USA, 2000, personal communication) has noted differences in seed shape, with seeds of eastern Andean plants being distinctly flattened and elongate in shape as compared with the oval to more or less spherical shape of the seeds of western Andean plants. There is a paucity of reproductive material, particularly seeds, in herbarium collections. The seed morphology question needs further study but could provide support, along with molecular sequence data, for the recognition of two species. If so, this would most likely represent a vicariant trans-Andean species pair, because the cycads were there long before the Andes.

Acknowledgements I offer my sincere gratitude to my cycad colleagues, without whose help this work would not have been possible. In particular, I would like to thank those who accompanied me in the field: Aldo Moretti, Luciano Gaudio and Jean-Pierre Sclavo. I also thank Rupert Barneby for help with the Latin diagnosis. I am deeply grateful to Amy Melson and Cynthia Armstrong for their excellent illustrations of the taxa included here. This work was made possible in part as a result of National Science Foundation Grants BSR-8607049 and BSR-8796279 awarded to the author. This chapter is dedicated to the memory of my friend, colleague and mentor, Knut J. Norstog.

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References Brako, L. (1993) Cycadaceae. In: Brako, L. and Zarucchi, J. (eds) Checklist of the Plants of Peru. Missouri Botanical Garden Press, St Louis, Missouri, p. 1. Caputo, P., Cozzolino, S., Gaudio, L., Moretti, A. and Stevenson, D.W. (1996) Karyology and phylogeny of some Meso-American species of Zamia (Zamiaceae). American Journal of Botany 83, 1513–1520. Dammer, U. (1907) Cycadaceae. Verhandlungen des Botanischen Vereins der Provinz Brandenburg 47, 117–118. Dodson, C. (1994) The Zamias of Equador. The Cycad Newsletter 18(3), 2–5. Dodson, C. (1998) A new species of Zamia (Zamiaceae) from Ecuador. Novon 8, 12–14. [Zamia gentryi.] Ducke, A. (1915) Plantes nouvelles ou peu connues de la région Amazonienne. Cycadaceae. Archivos do Jardim Botânico do Rio de Janeiro 1, 9–10. Ducke, A. (1922) Plantes nouvelles ou peu connues de la région Amazonienne. Cycadaceae. Archivos do Jardim Botânico do Rio de Janeiro 3, 20. Ducke, A. (1935) Plantes nouvelles ou peu connues de la région Amazonienne. Archivos do Jardim Botânico do Rio de Janeiro, Series 8a, 2, 27–28. Norstog, K.J. (1980) Chromosome numbers in Zamia (Cycadales). Caryologia 33, 419–428. Norstog, K.J. (1981) Karyotypes of Zamia chigua (Cycadales). Caryologia 34, 255–260. Norstog, K.J. and Nicholls, T.J. (1997) The Biology of the Cycads. Cornell University Press, Ithaca, New York, 363 pp. Regel, E. (1876) Die Cycadeen, deren Gattungen und Arten. Gartenflora 25, 140–144. Sabato, S. (1990) West Indian and South American cycads. In: Stevenson, D.W. (ed.) The Biology, Structure, and Systematics of the Cycadales. Proceedings of the Symposium CYCAD 87. Memoirs of the New York Botanical Garden 57, pp.179–180. Schultes, R. (1953) Notes on Zamia in the Colombian Amazon. Mutisia 15, 1–6. Schuster, J. (1932) Cycadaceae. In: Engler, A. (ed.) Das Pflanzenreich, Fascicle 99, Vol. 4, Part 1, pp. 1–168. Stevenson, D.W. (1990) Morphology and systematics of the Cycadales. In: Stevenson, D.W. (ed.) The Biology, Structure, and Systematics of the Cycadales. Proceedings of the Symposium CYCAD 87. Memoirs of the New York Botanical Garden 57, pp. 8–55. Stevenson, D.W. (1991) Zamiaceae. Flora of the Guianas, Series A, Fascicle 9, 7–11. Stevenson, D.W. (1993) The Zamiaceae in Panama with comments on phytogeography and species relationships. Brittonia 45, 1–16. Stevenson, D.W. (1999) Zamiaceae. In: Jorgensen, P.M. and León-Yánez, S. (eds) Catalogue of the Vascular Plants of Ecuador. Missouri Botanical Garden Press, St Louis, Missouri, pp. 189–190. Stevenson, D.W. (2001) Cycadales. Flora de Colombia 21, 1–92. Stevenson, D.W. and Sabato, S. (1986) Typification of names in Zamia L. and Aulacophyllum Regel (Zamiaceae). Taxon 35, 134–144. Walter, K. and Gillett, H. (1998) 1997 IUCN Red List of Threatened Plants. IUCN – The World Conservation Unit, Gland, Switzerland. Wrinkle, G. (1993) A new species of Zamia from amazonian Peru. Encephalartos 36, 20–22.

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In Search of the True Tree: Guidelines for Classification

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Roy Osborne1 and Terrence Walters2 1PO Box 244, Burpengary, Queensland, Australia; 2Montgomery Botanical Center, Miami, Florida, USA

Abstract The central goal in cycad systematics is to uncover the ‘true tree’ that correctly represents the hierarchy of relationships within the Cycadales. Consensus reached at the Cycad Classification Concepts Workshop in Miami in April 2002 is that the cycads are a monophyletic group, that a species is the smallest practical unit which should be used at the present time, that species descriptions should be field-based with as wide a suite of characters as possible and that taxonomic descriptions of the highest standard are essential to avoid past deficiencies in the literature. The identification of facilities, the sharing of resources and a vigorous interaction between all cycad systematics will collectively facilitate progress towards the ‘true tree’. Data in this respect are presented in the form of a number of schedules.

Introduction This chapter is based on discussions by participants at the Cycad Classification Concepts (CCC) Workshop held at the Montgomery Botanical Center on 7–9 April 2002. It commences with a summary of the core philosophy held by all participants, as has been more fully detailed in Chapter 1 of this volume, and then progresses to specific guidelines recommended during the workshop sessions.

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Further work in cycad systematics is constrained by the availability of resources and a number of schedules listing various facilities available to cycad research workers have therefore been included.

Core Philosophy There exists an underlying coherent natural order within the Cycadales. The objective of those working in cycad systematics is to construct hypotheses that will ultimately reveal the phylogeny of the group, i.e. the ‘true tree’ for the Cycadales. This tree comprises a hierarchy of recognizable categories that can be arranged systematically in an order descending towards the smallest taxonomic unit. At the present time, the smallest unit that is practically useful is our concept of a species, this being a geographically and morphologically distinct entity that is reproductively isolated from any other such entity. Variations in interpretation of such entities will inevitably occur and are recognized as part of the process in striving towards stability. The work presented in Chapters 2–14 of this volume shows that considerable progress has been made in understanding relationships between the cycads as presently circumscribed, but it is clear that a wealth of data remains to be captured and further botanical exploration is necessary. The data exist in a broad range of forms that encompass much more than classical taxonomic descriptions based solely on plant morphology. The continuous exchange of information and sharing of resources is vital to ensure further meaningful progress.

Guidelines for Taxonomic Descriptions Inadequate taxonomic descriptions for cycads (and other plants) in the 17th to 20th centuries have led to much confusion and have inhibited progress in cycad systematics (references throughout, Chapters 2–14 this volume). It is vital that new taxonomic treatments are of the highest standard and, while concise, provide a sound basis for critical evaluation and elucidation of relationships between taxa. The requirements for naming species are provided in the principles, provisions, articles and recommendations given in the codes of botanical nomenclature, the current of which is the St Louis Code (Greuter et al., 2000). Apart from the mandatory requirements, a proposal from the CCC Workshop is that authors should, as far as possible, include the following in their treatments, and that manuscript reviewers should be cognisant of the following guidelines. ●

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Full details, qualitative and quantitative where appropriate, of vegetative and reproductive morphological characters should be presented in all texts. Geographical data, such as climatic data, distribution range and profile, GPS latitude and longitude coordinates (except where such information may prejudice conservation of the taxon) and altitude, should be included in the descriptions.

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Ecological data, including edaphic and topographical data, habitat details and plant associations and symbiotic associations, should be given. Life history aspects, such as coning phenology, pollinating and seed dispersal agents, plant predators, plant abundance and population dynamics, and evidence of possible hybridization, should be included. Micromorphological and anatomical details should be given where significant. Cytological details, such as chromosome number and morphology and details of chromosome satellites, should be provided if available. Chemical data, such as details of primary and secondary plant metabolites, isoenzyme analyses and DNA investigations, should be included where possible. Ethnobotanical commentary, especially as may relate to past distribution patterns, local names and human usage of plant material, should be given. Ex situ experimental results (e.g. where trials have been made to access the plasticity of discriminatory characters) should be provided.

Guidelines for Presenting Reports In addition to the above features, which relate directly to the comprehensiveness of the taxonomic description for any particular taxon, the following ancillary guidelines are proposed by the CCC Workshop participants. ●

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Species are recognized as the basic evolutionary unit; until cycad classification becomes more stable, the designation of infraspecific units (subspecies, varieties, etc.) is discouraged. Taxonomic descriptions should be submitted only to widely recognized, international and refereed journals. A distribution map (or descriptive text) should be provided to show the extent of the known range and that of associated and/or closely related taxa. Taxonomic keys using discriminatory characters should be included where appropriate. The conservation status of the taxon should be given, or an appropriate conservation status proposed (see Donaldson, Chapter 2 this volume). Where data are derived from ex situ plants, the source of such material should be clearly identified. Epithets chosen for species names should be simple and relevant, and an etymology should be provided. Authors’ names associated with plant species should follow internationally recognised guidelines (e.g. Brummit and Powell, 1992; see also the IPNI website listed in Schedule 15.9). Cycad taxonomists are encouraged to send their draft publication to peers for critical evaluation before submission for publication. Major advances in cycad classification will follow from in-depth monographic treatments based on geographical zones or monophyletic groupings.

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Guidelines for Collection of Field Data Much of the past information about individual cycad taxa has been based on single ‘typical’ specimens. The necessity for data that best represent a plant population, rather than single specimens, has only recently been recognized as being paramount. Recommended guidelines for fieldworkers are as follows. ●

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Sample size is critical in data collection and must be appropriate both for the variation within the population and for the nature of the analysis. Cognisance must be made of changes that occur on a seasonal basis, or with the passage of time, which may affect the data collected. Photographic evidence should be used to complement field notes. Standardized data collection sheets (see Hill, Chapter 3 this volume) are extremely useful in providing rigour and structure to field data collection; a uniform character checklist for each cycad genus is highly desirable.

Guidelines for Herbarium Specimen Collecting and Processing The need for quality herbarium specimens goes hand in hand with the concept of quality taxonomic publications. Many of the ‘older’ cycad specimens are sadly inadequate in terms of both material and collector annotations (references throughout, Chapters 2–14 this volume). Guidelines for fieldworkers are as follows. ●

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Herbarium specimens should include both vegetative and reproductive material where possible. A type specimen should be carefully selected so that it best represents the population being described. Since cycads are dioecious, the type will necessarily represent only a single male or female plant. Additional vouchers should be made to represent the other sex. The herbarium sheets should be informatively documented. Photographs should be used to illustrate points that will not be evident in preserved specimens. Duplicate herbarium sheets should be deposited in at least three institutions.

Availability of Resources In parallel with the distribution patterns of the extant cycads, workers in cycad taxonomy and systematics are geographically dispersed and often isolated. Their work is often inhibited by limited financial and infrastructural resources. Since sharing of resources is an obvious way to eliminate duplication of effort and to increase efficiency, it is appropriate to list resources that may be useful to cycad workers.

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Personnel resources. Schedule 15.1 gives the names and addresses of workers actively engaged in cycad studies. Facilities. Schedules 15.2–15.6 give lists of cycad-orientated herbaria, ex situ plant collections, fossil collections, insect collections and molecular laboratories. Software packages for cladistics. See Schedule 15.7. Cycad societies and magazines. See Schedule 15.8. Electronic information. Schedule 15.9 gives a list of other cycad-oriented websites.

Remaining Issues to be Resolved As would be expected in any long-term multi-disciplinary scientific project, there are several issues that can be identified but which could not be resolved at the CCC Workshop. Among these are the following. ●

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Terminology. A need has been identified for the standardization of cycad terminology. Examples of inconsistency are seen at present in the use of terms such as leaflet vs. pinna, the distinction between spines, pinnacanths (as modified leaflets) and prickles (as epidermal structures), the use of the terms rachis (rachis) vs. leaf stalk (petiole), cone vs. strobilus, seed vs. omnule etc. It is recommended that an authoritative taxonomic glossary to be used as a guideline for cycad workers is prepared and distributed; the glossary developed for this volume (see Osborne and Walters, Appendix 2 this volume) may be useful as a starting point in this project. Archiving of data. A great deal of information resides in personal literature collections, plant material, photographs/slides, field notebooks, etc. which often represent a lifetime’s work in cycad studies. No provision exists for the archiving of such material for posterity. International Conferences on Cycad Biology. Commenced in 1987, these immensely valuable meetings have been organized every 3 years on an ad hoc basis, with no provision for continuity. It is recommended that a coordinating role in this planning is given to the Cycad Specialist Group of the IUCN. The World List of Cycads. Several versions of a cycad world list have been published in paper and electronic forms with the format and choice of ‘acceptable’ species in the hands of the authors. A single and authoritative world list, timeously updated, is a vital data source for numerous and diverse users. It is recommended that the Cycad Specialist Group of the IUCN be given a monitoring responsibility for this list, with a brief to secure its long-term continuation and to resolve points of conflict if necessary. A listing of the cycad flora of the world, excluding synonyms, was compiled in 2003 by three of the participants as another reference source for this volume (see Hill et al., Appendix 1 this volume).

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Conclusions The revelation of a single tree, which correctly and fully represents the phylogeny of all Cycadales, remains as an ultimate, but probably unattainable, objective in cycad biology. During the foreseeable future, it is important for cycad workers to strive towards resolution of at least an approximate tree for the extant cycads. Adherence to the proposed guidelines in this chapter, diligent use of resources, quality of workmanship, timely dissemination of information and participation in international meetings are seen as key factors in making progress towards this goal.

Acknowledgements This chapter is based on the input from all who attended the Cycad Classification Concepts Workshop held at Montgomery Botanical Center on 7–9 April 2002. Participants were invited to review this text during its preparation, and the authors believe that the contents of this chapter correctly represent the consensus view of all Workshop participants.

Schedules Schedule 15.1: Active cycad workers This list comprises names and addresses of workers at present active in cycadoriented research projects. It is drawn up from the lists of regular participants in the International Conferences on Cycad Biology, those who attended the Cycad Classification Concepts Workshop in Miami in 2002, and authors of recently published cycad work. We are aware that this list may be incomplete and that address details may change with the passage of time. Avendaño, Sergio Instituto de Ecología A.C., Apdo Postal 63, Xalapa, Veracruz 91000, Mexico [email protected] Beentje, Henk Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AE, UK [email protected] Bonta, Mark Division of Social Sciences, 203B Kethley Hall, Delta State University, Cleveland, Mississippi 38733, USA [email protected] Broome, Tom The Cycad Jungle, PO Box 325, Polk City, Florida 33868-0325, USA [email protected]

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Calonje, Alvaro Carrera 28 5B-102, Cali, Colombia [email protected] Calonje, Michael 770 East Saginaw Way, Fresno, California 93704, USA [email protected] Capela, Pedro Plantas de Mozambique, Apartado No. 293, Chimoio, Mozambique [email protected] Caputo, Paolo Dipartimento di Biologia Vegetale, Università degli Studi di Napoli Federico II, Via Foria 223, Napoli 80139, Italy [email protected] Chaves, Ramiro Calle 46 No. 904, Playa, La Habana, CP 11300, Cuba [email protected] Chavez, Victor M. Universidad Nacional Autónoma de Mexico, Jardin Botanico del Instituto de Biologia, DF 04510, Mexico [email protected] Chaw, Sha-Miaw Institute of Botany, Academia Sinica, #128 Academy Road Sec. 2, Taipei 11529, Taiwan [email protected] Chemnick, Jefferey Lotusland Foundation, 695 Ashley Road, Santa Barbara, California 93108, USA [email protected] Chen, Chia-Jui Institute of Botany, Chinese Academy of Sciences, 20 Nanxincum, Xiangshan, Beijing 100093, China [email protected] Clos, Lynne M 1185 Claremont Drive, Boulder, Colorado 80303, USA [email protected] Connell, Stephen 3 Glenbank Crescent, Kalloroo, Western Australia 6025, Australia Cozzolino, Salvatore Dipartimento di Biologia Vegetale, Università degli Studi di Napoli Federico II, Via Foria 223, Napoli 80139, Italy [email protected] Dalzell, Chris Durban Botanic Gardens, PO Box 3720, Durban 4000, South Africa [email protected]

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De Laubenfels, David J. 107 Will-O-Wind Drive, Jamesville, New York 13078, USA Dehgan, Bijan Horticultural Systematics Laboratory, Department of Environmental Horticulture, University of Florida, Gainesville, Florida 32611, USA [email protected] Donaldson, John Kirstenbosch Research Center, National Botanical Institute, Private Bag X7, Claremont 7735, South Africa [email protected] Forster, Paul I. Queensland Herbarium, Environmental Protection Agency, Brisbane Botanic Gardens, Mt Coot-tha Road, Toowong, Queensland 4066, Australia [email protected] Francisco-Ortega, Javier Florida International University/Fairchild Tropical Garden, 11935 Old Cutler Road, Miami, Florida 33156, USA [email protected] Gaudio, Luciano Dipartimento di Genetica, Biologia Generale e Molecolare, Facoltà di Scienze, Università degli Studi di Napoli Federico II, Napoli, Italy [email protected] Gonzáles, Dolores Instituto de Ecología A.C., Apdo Postal 63, Xalapa, Veracruz 91000, Mexico [email protected] González-Geigel, Lutgarda Jardín Botánico Nacional, Universidad de La Habana, Carretera ‘El Rocío’, Km 31/2, Calabazar, Boyeros, CP 19230, C. Habana, Cuba [email protected] Goode, Douglas 10 Hudson Bennett Crescent, Gillitts 3610, South Africa Gorelick, Root Department of Biology, Arizona State University, Tempe, Arizona 852871501, USA [email protected] Gregory, Timothy J. Montgomery Botanical Center, 11901 Old Cutler Road, Miami, Florida 33156, USA [email protected] Grobbelaar, Nathanaël PO Box 15357, Lynn East 0039, South Africa [email protected]

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Hall, John Department of Entomology, University of Queensland. Correspondence to 11/26 Lang Parade, Auchenflower, Queensland 4066, Australia [email protected] Hayes, Virginia Lotusland Foundation, 695 Ashley Road, Santa Barbara, California 93108, USA [email protected] Haynes, Jody Montgomery Botanical Center, 11901 Old Cutler Road, Miami, Florida 33156-4242, USA [email protected] Hill, Ken D. Royal Botanic Gardens, Mrs Macquaries Road, Sydney, New South Wales 2000, Australia [email protected] Hurter, P. Johan H. Lowveld National Botanic Gardens, PO Box 1024, Nelspruit 1200, South Africa [email protected] Jones, David 13 Saville Close, Melba, ACT 2615, Australia [email protected] Kennedy, Paul 21 Sierra Road, Engadine, New South Wales 2233, Australia Kokubugata, Goro Tsukuba Botanical Garden, National Science Museum, Tokyo, Amakubo 4, Tsukuba, Ibaraki 305-0005, Japan [email protected] Ladd, Philip G. School of Environmental Science, Murdoch University, Murdoch, Western Australia 6150, Australia [email protected] Lazcano, Julio Jardín Botánico Nacional, Universidad de La Habana, Carretera ‘El Rocío’, Km 31/2, Calabazar, Boyeros, CP 19230, C. Habana, Cuba [email protected] Lindström, Anders Nong Nooch Tropical Garden, 34/1 Sukhumvit Highway, Najomtien, Sattahip, Chonburi 20250, Thailand [email protected] Liu, Nian South China Botanical Garden, Academia Sinica, Guangzhou 510650, Guangdong, China

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Litz, Richard E. University of Florida, Tropical Research and Education Center, 18905 SW 280 Street, Homestead, Florida 33031, USA [email protected] Loc, Phan Ke Department of Botany, University of Science, Vietnam National University, Hanoi, Vietnam [email protected] Meerow, Alan W. USDA-ARS-SHRS, National Germplasm Laboratory, 13601 Old Cutler Road, Miami, Florida 33158, USA [email protected] Moon, Pamela A. University of Florida, Tropical Research and Education Center, 18905 SW 280 Street, Homestead, Florida 33031, USA [email protected] Moretti, Aldo Dipartimento di Biologia Vegetale, Università degli Studi di Napoli Federico II, Via Foria 223, Napoli 80139, Italy [email protected] Musial, Kathy Huntington Botanical Gardens, 1151 Oxford Road, San Marino, California 91108, USA Nan, Li Fairy Lake Botanical Garden, Lian-Tang, Shenzhen, Guangdong 518004, China [email protected] Nguyen, Tien Hiêp Institute of Ecology and Biological Resources, Nghia Do, Cau Giay, Hanoi, Vietnam [email protected] Nicholls, Trevor J. University of Bristol, Bristol, UK Oberprieler, Rolf CSIRO Entomology, GPO Box 1700, Canberra, ACT 2601, Australia [email protected] O’Brien, Charles Center for Biological Control, 105 [South] Perry-Paige Bldg, Florida A&M University, Tallahassee, Florida 32307-4100, USA [email protected] or [email protected] Osborne, Roy PO Box 244, Burpengary, Queensland 4505, Australia [email protected]

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Peña, Esperanza Calle 2 No. 464, Plaza, CP 10400, La Habana, Cuba [email protected] Pérez-Farrera, Miguel Angel Escuela di Biología, Universidad de Ciencias y Artes de Chiapas (UNICACH), Calzada Samuel León Brindis 151, Tuxtla Gutiérrez, Chiapas 29000, Mexico [email protected] or [email protected] Richardson, Peter (Mick) Missouri Botanical Garden, PO Box 299, St Louis, Missouri 63166-0299, USA [email protected] Salas-Morales, Silvia Sociadad para el Estudio de Recursos Bióticos de Oaxaca (SERBO), Calle Porfirio Diaz, No. 211, Centro, Oaxaca, Mexico [email protected] Seawright, Alan A. National Research Center for Environmental Toxicology, University of Queensland, PO Box 594, Archerfield, Queensland 4108, Australia [email protected] Schutzman, Bart University of Florida, Environmental Horticulture Department, 1525 W.M. Fifield Hall, Gainesville, Florida 32611-0670, USA [email protected] Scott-Shaw, C. Rob Biodiversity Research Division, KwaZulu-Natal Conservation Service, PO Box 13053, Cascades 3202, South Africa [email protected] Siniscalco Gigliano, Gesualdo Dipartimento di Biologia Vegetale, Università degli Studi di Napoli Federico II, Via Foria 223, Napoli 80139, Italy Stevenson, Dennis Wm. Institute of Systematic Botany, New York Botanical Garden, Bronx, New York 10458, USA [email protected] Tang, William Fairchild Tropical Garden, 11935 Old Cutler Road, Miami, Florida 33156, USA [email protected] Taylor, Alberto Universidad de Panama, 6-4957 El Dorado, For Z6, Panama [email protected] Terry, Irene Department of Biology, University of Utah, 257 South 1400 East, Salt

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Lake City, Utah 84112, USA [email protected] Thompson, Craig PO Box 140, Sylvania, New South Wales 2224, Australia Vázques Torres, Mario Centro de Investigaciones Biologicas, Universidad Veracruzana, Apdo Postal 294, Xalapa, Veracruz 91000, Mexico [email protected] Visser, Jan-Maarten Hortus Botanicus Amsterdam, Plantage Middenlaan 2a, 1018 DD, Amsterdam, The Netherlands [email protected] Vorster, Piet Botany Department, University of Stellenbosch, Private Bag X1, Matieland 7602, South Africa [email protected] Vovides, Andrew P. Instituto de Ecología A.C., Apdo Postal 63, Xalapa, Veracruz 91000, Mexico [email protected] Walters, Terrence Montgomery Botanical Center, 11901 Old Cutler Road, Miami, Florida 33156-4242, USA [email protected] Whitelock, Loran M. 4524 Toland Way, Los Angeles, California 90041, USA [email protected] Wilson, Gary W. Department of Tropical Plant Sciences, James Cook University, Smithfield, Cairns, Queensland 4870, Australia [email protected] Wink, Michael Institut für Pharmazeutische Biologie, Universität Heidelberg, Im Nuwnhwimwe Feld 364, D-69120 Heidelberg, Germany [email protected] Wijnants, Jeff 42 Oudstrijderstraat, Merchtem 1785, Belgium Schedule 15.2: Major herbaria with cycad accessions A number of herbaria with important cycad accessions are listed below. Many of the European herbaria have vouchers from the days of colonial exploration; more recent collections will generally be found in herbaria in the USA and in the countries of origin of the material. As names and addresses may change in time, a useful website for more permanent access is the Index Herbariorum, http://www.nybg.org/bsci/ih

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Australian National Herbarium (CANB) Center for Plant Biodiversity Research, GPO Box 1600, Canberra, ACT 2601, Australia Website: http://www.anbg.gov.au/cpbr Contact: Jim Croft, [email protected] Botanischer Garten und Botanisches Museum Berlin-Dahlem (B) Zentraleinrichtung der Freien Universität Berlin, Königin Luise Strasse 6-8, D-14191 Berlin, Germany Contact: Director, [email protected] Botany Department (BM) The Natural History Museum, Cromwell Road, London SW7 5BD, UK Website: http://www.nhm.ac.uk Contact: R. Huxley, [email protected] Chinese National Herbarium, Institute of Botany, Chinese Academy of Sciences (PE) 20 Nanxincun, Xiangshan, Beijing 100093, China Website: http://www.ibcas.ac.cn Contact: Hai-Ning Qin, [email protected] Conservatoire et Jardin Botaniques de la Ville de Genève (G) Case postale 60, CH-1292 Chambésy/Genève, Switzerland Contact: Fernand Jacquemoud, [email protected] Compton Herbarium (NBG) National Botanical Institute, Private Bag X7, Claremont 7735, South Africa Website: http://www.nbi.ac.za Contact: Koos Roux, [email protected] Fairchild Tropical Garden (FTG) 11935 Old Cutler Road, Miami, Florida 33156, USA Website: http://www.virtualherbarium.org Contact: Gerald Guala, [email protected] Field Museum of Natural History (F) 1400 south Lake Shore Drive, Chicago, Illinois 60605-2496, USA Contact: Chair, [email protected] Gray Herbarium (G) and Arnold Arboretum (A) Harvard University Herbaria, 22 Divinity Avenue, Cambridge, Massachusetts 02138, USA Contact: Emily Wood, [email protected] Herbario, Departamento de Botánica, Instituto Nacional de Biodiversidad (INB) Apdo Postal 22-3100, Santo Domingo de Heredia, Costa Rica Website: http://www.inbio.ac.cr Contact: Nelson Zamora, [email protected]

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Herbario, Instituto de Ecología (XAL), A.C. Apdo Postal 63, 2.5 Km sobre carretera antigua a Coatepec, Cong El Haya 351, Xalapa, Veracruz 91000, Mexico Website: http://www.ecologia.edu.mx Contact: Francisco G. Lorea-Hernández, [email protected] Herbario, Instituto de Investigação Científica Tropical (LISC) Travessa Conde da Ribeira 9, P-1300-142, Lisbon, Portugal Contact: Maria Adélia Diniz, [email protected] Herbarium Jardin Botanique National de Belgique (BR) Domein van Bouchout, B-1860 Meise, Belgium Website: http://www.br.fgov.be Contact: Elmar Robbrecht, [email protected] Herbarium Neapolitanum (NAP) Dipartimento di Biologia Vegetale Università degli Studi di Napoli Federico II, Via Foria 223, 80139 Napoli, Italy Contact: Annalisa Santangelo, [email protected] Herbarium, University of Coimbra (COI) Acros do Jardim, P-3001-401, Coimbra, Portugal Contact: Fátima Sales, [email protected] Missouri Botanical Garden Herbarium (MO) PO Box 299, St Louis, Missouri 63166-0299, USA Website: http://www.mobot.org Contact: James Solomon, [email protected] Muséum national d’histoire naturelle, Herbier (P) 16 rue Buffon, F-75005 Paris, France Contact: Philippe Morat, [email protected] Nationaal Herbarium Nederland, Leiden University Branch (Rijksherbarium) (L) Postbus 9514, 2300 RA Leiden, The Netherlands Website: http://www.nationaalherbarium.nl Contact: Pieter Baas, [email protected] Nationaal Herbarium Nederland, Utrecht University Branch (U), Heidelberglaan 2, 3584 CS Utrecht, The Netherlands. Website: http://www.bio.uu.nl/~herba Contact: Paul Maas, [email protected] National Herbarium (PRE) National Botanical Institute, Private Bag X101, Pretoria 0001, South Africa Website: http://www.nbi.ac.za Contact: Marinda Koekemoer, [email protected] National Herbarium of New South Wales (NSW) Royal Botanic Gardens, Mrs Macquaries Road, Sydney 2000, Australia Website: http://www.rbgsyd.gov.au Contact: Barry Conn, [email protected]

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National Herbarium of Zimbabwe (SRGH) Botanic Garden, PO Box CY 550, Causeway, Harare, Zimbabwe Contact: Nozipo Nobanda, [email protected] New York Botanical Garden Herbarium (NY) Bronx, New York 10458-5126, USA Website: http://www.nybg.org Contact: Barbara Thiers, [email protected] Northern Territory Herbarium (DNA) Parks and Wildlife Commission of the Northern Territory, PO Box 496, Palmerston, Northern Territory 0831, Australia Contact: Gregory Leach, [email protected] Queensland Herbarium (BRI) Brisbane Botanic Gardens, Mt Coot-tha Road, Toowong, Queensland 4066, Australia Contact: Gordon Guymer, [email protected] Royal Botanic Gardens Herbarium (K) Kew, Richmond, TW9 3AE, UK Website: http://www.rbgkew.org.uk Contact: Simon Owens, [email protected] South China Institute of Botany (IBSC) Academia Sinica, Guangzhou 510650, Guangdong, China Contact: Hai-Shan Chen, [email protected] United States National Herbarium (US) Botany Section, MRC-166, Smithsonian Institution, PO Box 37012, Washington, DC 20013-7012, USA Website: http://nmnh.si.edu/sysbiology Contact: Collections Manager, [email protected] V.L. Komarov Botanical Institute Herbarium (LE) Prof. Popov Street 2, Saint Petersburg 197376, Russia Contact: Rudolf Kamelin, [email protected]

Schedule 15.3: Major ex situ cycad collections Darwin Botanic Gardens Northern Territory Parks and Wildlife Commission, Geranium Street, Stuart Park, Darwin, PO Box 496, Palmerston, Northern Territory 0831, Australia Website: http://www.nt.gov.au/paw Contact: Greg Leach, [email protected] Durban Botanic Gardens PO Box 3720, Durban 4000, South Africa Contact: Chris Dalzell, [email protected] Fairchild Tropical Garden 10901 Old Cutler Road, Miami, Florida 33156, USA

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Website: http://www.fairchildgarden.org Contact: Jack Fisher, [email protected] Fairy Lake Botanical Garden Lian-Tang, Shenzhen, Guangdong 518004, China Website: http://www.szbg.org/eng/cont.htm Contact: Li Nan, [email protected] Ganna Walska Lotusland Foundation 695 Ashley Road, Santa Barbara, California 93108, USA Website: http://www.lotusland.org/general.html Contact: Virginia Hayes, [email protected] Hortus Botanicus Amsterdam Plantage Middenlaan 2a, 1018 DD, Amsterdam, The Netherlands Contact: Jan-Maarten Visser, [email protected] Huntington Botanical Gardens 1151 Oxford Road, San Marino, California 91108, USA Website: http://www.huntington.org Contact: Kathy Musial Jardín Botánico FCO J. Clavijero, Instituto de Ecología, A.C. Apdo Postal 63, 2.5 Km sobre carretera antigua a Coatepec, Cong El Haya 351, Xalapa, Veracruz 91000, Mexico (Mexican National Cycad Collection) Website: http://www.ecologia.edu.mx E-mail: [email protected] Kirstenbosch National Botanical Garden Private Bag X7, Claremont 7735, South Africa Contact: Philip le Roux, [email protected] Lowveld National Botanic Gardens PO Box 1024, Nelspruit 1200, South Africa Website: http://www.nbi.ac.za/lowveld/mainpage.htm Contact: Johan Hurter, [email protected] Montgomery Botanical Center 11901 Old Cutler Road, Miami, Florida 33156-4242, USA Website: http://www.montgomerybotanical.org Contact: Jody Haynes, [email protected] Nong Nooch Tropical Garden 34/1 Sukhumvit Highway, Najomtien, Sattahip, Chonburi 20250, Thailand Contact: Anders Lindström, [email protected] Orto Botanico Dipartimento di Biologia Vegetale, Università degli Studi di Napoli Federico II, Via Foria 223, Napoli 80139, Italy Contact: Salvatore Cozzolino, [email protected] Pretoria National Botanical Garden National Botanical Institute, Private Bag X101, Pretoria 0001, South Africa

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Website: http://www.nbi.ac.za/pretoria/mainpage.htm Contact: Gideon Smith, [email protected] Quail Botanic Gardens 230 Quail Gardens Drive, Encinitas, California 92024, USA Website: http://www.qbgardens.com Contact: Julian Duval, [email protected]

Schedule 15.4: Major cycad fossil collections Details of a limited number of institutions with important fossil cycad collections are given below. A useful generic website is: http://uni-wuerzburg.de/mineralogie/palbot1.html Bernard Price Institute for Palaeontology University of Witwatersrand, Private Bag X3, Johannesburg 2050, South Africa Contact: Marion Bamford, [email protected] Burke Museum of Natural History and Culture PO Box 353010, University of Washington, Seattle, Washington 98195, USA Contact: Wes Wehr, [email protected] Denver Museum of Nature and Science 2001 Colorado Blvd., Denver, Colorado 80205, USA. Website: http://www.dmns.org Contact: Kirk Johnson, [email protected] Florida Museum of Natural History Museum Road and Newell Drive, University of Florida, Gainesville, Florida 32611-7800, USA Website: http://www.flmnh.ufl.edu/natsci/paleobotany/paleobotany.htm Contact: Steven Manchester, [email protected] Herbarium of Paleobotany Institute of Botany, the Chinese Academy of Sciences, Xiangshan, Beijing 100093 Website: http://www.ibcas.ac.cn Contact: Yu-Fan Hu. Instituto de Geología, Universidade Nacional Autónoma de México Ciudad Universitaria, 04510 Mexico, DF, Mexico Contact: Reinhard Weber, [email protected] Museo Argentino de Ciencias Naturales ‘B. Rivadavia’ Av. A. Gallardo 470, 1405 Buenos Aires, Argentina Contact: Sergio Archangelsky, [email protected]

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Museo de La Plata Paseo del Bosque s/n. 1900, La Plata, Argentina Contact: Analia Artabe Museo Paleontológico Egidio Feruglio 9100 Trelew, Chubut, Argentina Contact: Ruben Cúneo, [email protected] Museum Victoria PO Box 666e, Melbourne, Victoria 3001, Australia Website: http://www.museum.vic.gov.au Contact: Dermot Henry, [email protected] National Herbarium Fossil Collection National Botanical Institute, Private Bag X101, Pretoria 0001, South Africa Website: http://www.nbi.ac.za Contact: John Anderson, [email protected] Natural History Museum Department of Palaeontology, Cromwell Road, London SW7 5BD, UK Website: http://www.nhm.ac.uk/palaeontology Contacts: Paul Kenrick, [email protected] and Paul Davis, [email protected] Peabody Museum of Natural History Yale University, PO Box 208118, 170 Whitney Avenue, New Haven, Connecticut, USA Website: http://www.peabody.yale.edu Contact: Leo Hickey, [email protected] Petrified Forest National Park PO Box 2277, Petrified Forest, Arizona 86028, USA Website: http://www.nps.gov/pefo/index.htm Smithsonian National Museum of Natural History (Department of Palaeobiology) Website: http://www.mnh.si.edu Contact: Scott Wing, [email protected]

Schedule 15.5: Insect collections with significant cycad-associated specimens Albany Museum Somerset Street, Grahamstown 6139, South Africa Website: http://www.ru.ac.za/departments/am Contact: F.W. Gess, [email protected] Australian National Insect Collection CSIRO Entomology, GPO Box 1700, Canberra, ACT 2601, Australia Website: http://www.ento.csiro.au/research/natres/natres.html Contact: Rolf Oberprieler, [email protected]

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Charles W. O’Brien (Private) Collection Florida A&M University, Tallahassee, Florida 32307-4100, USA Contact: Charles O’Brien, [email protected] or [email protected] Iziko Museums of Cape Town (South African Museum) PO Box 61, Cape Town 8000, South Africa Website: http://www.nhm.org/~lorquin/evans/a2collections.html Contact: Simon van Noort, [email protected] National Collection of Insects Plant Protection Research Institute, Private Bag X134, Pretoria 0001, South Africa Website: http://www.sciref.org/netc/netc1-2/dit2c.htm Contact: Riaan Stals, [email protected] The Natural History Museum Department of Entomology, Cromwell Road, London SW7 5BD, UK Website: http://www.nhm.ac Contact: Chris Lyal, [email protected]

Schedule 15.6: Molecular laboratories carrying out cycad-related work The list below gives details of some laboratories that are active in molecular analyses. It must be remembered that this work is time-consuming and expensive – fees may be requested on a ‘per sample’ basis for any work done. However, most universities with botany, biology or biochemistry departments would have access to equipment for carrying out molecular studies and the possibility of a joint project is worth considering; such projects are usually dependent on the interest of students and supervisors and on funding availability. Cold Spring Harbor Laboratories PO Box 100, Cold Spring Harbor, New York 11724, USA Website: http://www.cshl.org Dipartimento di Biologia Vegetale Università degli Studi di Napoli Federico II, Via Foria 223, Napoli 80139, Italy Contact: Paolo Caputo, [email protected] Institut für Pharmazautische Biologie Universität Heidelberg, Im Neuenheimer Feld 364, D-69120, Heidelberg, Germany Website: http://Pharm-Biologie.uni-hd.de Contact: Michael Wink, [email protected] Institute of Botany, Academia Sinica #128 Academy Road Sec. 2, Taipei 11529, Taiwan Contact: Shu-Miaw Chaw, [email protected]

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Institute of Systematic Botany, New York Botanical Garden Bronx, New York 10458, USA Website: http://www.nybg.org Contact: Dennis Stevenson, [email protected] Instituto de Ecología, Sistemática Vegetal Apdo Postal 63, Xalapa, Veracruz 91000, Mexico Website: http://www.ecologia.edu.mx Contact: Andrew Vovides, [email protected] Jodrell Laboratory Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3DS, UK Website: http://www.rbgkew.org.uk Contact: Mark Chase, [email protected] Fairchild Tropical Garden 11935 Old Cutler Road, Miami, Florida 33156, USA Website: http://www.fiu.edu/~biology/hmpgs/jfo.html Contact: Javier Francisco-Ortega, [email protected] Fairy Lake Botanical Garden Lian-Tang, Shenzhen, Guangdong 518004, China Website: http://www.szbg.org/eng/cont.htm Contact: Li Nan, [email protected] National Herbarium of New South Wales Royal Botanic Gardens, Mrs Macquaries Road, Sydney 2000, Australia Website: http://www.rbgsyd.nsw.gov.au Contact: Ken Hill, [email protected] USDA-ARS-SHRA National Germplasm Repository 13601 Old Cutler Way, Miami, Florida 33158, USA Contact: Alan Meerow, [email protected] Schedule 15.7: Software packages for cladistic analysis A large number of software packages is available as tools for cladistic analyses, the more popular of which amongst cycad systematists are listed below. Particularly useful generic information is found on the ‘Phylogeny Programs’ website: http://evolution.genetics.washington.edu/phylip/software.html. BIOSYS2 Author: W.C. Black. A modified version of Swofford and Selander’s BIOSYS program for the analysis of allelic variation in genetics. File transfer site: ftp://lamar.colostate.edu/pub/wcb4 HENNIG86 Author: J.S. Farris. Current version 1.5. Reference manual and software published by the author, Port Jefferson Station, New York, USA. Website: http://www.cladistics.org

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MACCLADE Authors: D. and W. Maddison. Current version 4. Published by Sinauer Associates. Website: http://phylogeny.arizona.edu/macclade/macclade.html NONA Author: P.A. Goloboff. Current version 2.0. Instruction manual distributed by the author, INSUE – Fundación e Instituto Miquel Lillo, Miquel Lillo 205, 4000 S. M. de Tucumán, Argentina. Website: http://www.cladistics.com PAUP – Phylogenetic Analysis Using Parsimony Author: D.L. Swofford. Current version 4.0. Smithsonian Institute, Washington, DC, USA. Website: http://www.paup.csit.fsu.edu PHYLIP – Phylogeny Inference Package Author: J. Felsenstein. Current version 3.5c. Distributed by the author, Department of Genetics, University of Washington, Seattle, USA. Website: http://evolution.genetics.washington.edu/phylip/software.html WINCLADA Author: K.C. Nixon. Current version 1.00.08. Published by the author, Ithaca, New York, USA. Website: http://www.cladistics.com

Schedule 15.8: Cycad societies and magazines The Cycad Society (USA) c/o Montgomery Botanical Center, 11901 Old Cutler Road, Miami, FL 33156, USA Magazine: The Cycad Newsletter Website: http://www.cycad.org The Cycad Society of China c/o Institute of Botany, Chinese Academy of Sciences, 20 Nanxincum, Xiangshan, Beijing 100093, China Contact: Chia-Jui Chen, [email protected] The Cycad Society of South Africa PO Box 1790, Groenkloof, Pretoria 0027, South Africa Magazine: Encephalartos Website: http://www.cycadsociety.org Contact: Guillaume Theron, [email protected] Palm and Cycad Societies of Florida, Inc. (PACSOF) 9525 Jamaica Drive, Miami, Florida 33189, USA Contact: Jody Haynes, [email protected] The Palm and Cycad Societies of Australia Limited (PACSOA) PO Box 1134, Milton, Queensland 4064, Australia Magazine: Palms & Cycads

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Website: http://www.pacsoa.org.au E-mail: [email protected] The Palm and Cycad Society of New Zealand PO Box 3871, Auckland, New Zealand Quarterly magazine E-mail: [email protected] Contact: Gary Coleman, [email protected] West Coast Cycad Society PO Box 754, Bonsall, California 92028-0754, USA Website: http://www.home.earthlink.net/~wccshome/index/htm Contact: Bruce Ironmonger, [email protected] Schedule 15.9: Other cycad-associated websites Gymnosperm Database Christopher J. Earle (ed.) Website: http://www.geocities.com/RainForest/Canopy/2285 Harvard University Herbaria A site including the Gray Herbarium Index, the International Plant Names Index and other useful information Website: http://www.huh.harvard.edu/databases Q’taxa – University of California at Riverside Website: http://maya.ucr.edu/pril/PRIL.html The Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) Website: http://www.cites.org The Cycad Pages Ken Hill (ed.), Royal Botanic Gardens, Sydney, Australia. This includes the current World List of Cycads Website: http://plantnet.rbgsyd.nsw.gov.au/PlantNet/cycad The International Association for Plant Taxonomy (IAPT) This gives details of the journal Taxon and the Codes of Botanical Nomenclature Website: http://www.bybm.org/iapt/default/htm The International Plant Names Index (IPNI) This gives names and authors to plant species Website: http://www.ipni.org/index.html The International Union for the Conservation of Nature and Natural Resources (IUCN) Website: http://www.iucn.org The IUCN Red List of Threatened Species Website: http://www.redlist.org The Species Survival Commission (SSC) Including details of the various specialist groups Website: http://www.iucn.org/theme/ssc

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The University of California, Los Angeles (Berkeley) Website: http://www.ucmp.berkeley.edu/seedplants/cycadophyta/cycads Virtual Cycad Encyclopedia Jody Haynes (ed.), Palm and Cycad Societies of Florida Website: http://www.plantapalm.com

References Brummit, R.K. and Powell, C.E. (1992) Authors of Plant Names. Royal Botanic Gardens, Kew, England, 732 pp. Greuter, W., McNeill, J., Barrie, F.R., Burdet, H.M., Demoulin, V., Filgueiras, T.S., Nicolson, D.H., Silva, P.C., Skog, J.E., Trehane, P., Turland, N.J. and Hawksworth, D.L. (2000) International Code of Botanical Nomenclature (Saint Louis Code). Koeltz Scientific Books, Köningstein, Germany, 474 pp. Norstog, K.J. and Nicholls, T.J. (1997) The Biology of the Cycads. Cornell University Press, Ithaca, New York, 363 pp.

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Appendix 1: The World List of Cycads Ken D. Hill,1 Dennis Wm. Stevenson2 and Roy Osborne3 1Royal

Botanic Gardens, Sydney, Australia; 2New York Botanical Garden, Bronx, New York, USA; 3PO Box 244, Burpengary, Queensland, Australia

Introduction Updates of the ‘World List’ of extant cycad taxa have been published regularly, generally appearing as part of the Proceedings of the various International Cycad Conferences on Cycad Biology (see References). These reports list taxa accepted by the compilers as currently valid, country of occurrence, dates, authors and journals of publication, often together with much useful commentary about recent taxonomic changes, synonymity and anticipated new species. The list is also now available as a periodically updated searchable database on the internet (http://plantnet.rbgsyd.nsw.gov.au/PlantNet/cycad). This Appendix lists the names of all extant cycads (considered valid as at April 2003), authors, dates and publication journals. Legitimately published species names have been excluded when, in our judgement, they represent species considered synonymous with those having priority under the International Code of Botanical Nomenclature. Compilation is alphabetical by genus. Authors’ names are abbreviated in accordance with Brummit and Powell (1992) and the International Plant Names Index (IPNI website: http://www.ipni.org/index.html). Journals are abbreviated according to the Botanico-Periodicum-Huntianum standard (Lawrence et al., 1968); other reference material follows the style of Stafleu and Cowan (1976–1983) and page numbers are given as the first and last numbers of the taxonomic treatment within the relevant publication. The type species for each genus is indicated by an asterisk. The total number of species, validly published or known to be in press, in our list, not including synonyms, species dubia, or taxa below specific rank, is 303. ©CAB International 2004. Cycad Classification: Concepts and Recommendations (eds T. Walters and R. Osborne)

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Compared with the 130 species recorded in the first such list (Osborne and Hendricks, 1985), this is testimony to the very considerable progress that has been made in cycad taxonomy over the past two decades.

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The World List BOWENIA Hook. ex Hook. f. (1863) (2 species, Australia) Australia (Qld) Australia (Qld)

1912 1863

C. latifolia Miq. C. matudae Lundell *C. mexicana Brongn. C. microstrobila Vovides & J.D. Rees C. miqueliana H. Wendl. C. mirandae Vovides, Pérez-Farr. & Iglesias

Ann. Sci. Nat. Bot., ser. 3, 5: 7–9, t. 1 1999 xxxx 1986

Novon 9(3): 410–413 In review Brittonia 38(1): 17–26

Mexico Mexico (Querétaro, San Luis Potosi) Mexico (Veracruz)

1878 1979 2003

Sci. Proc. Roy. Dublin Soc., ser. 2: 113–114 Brittonia 31(3): 422–424, fig. 1 Bot. J. Linn. Soc. 141: 395–398

Mexico (Tamaulipas)

1857

Mexico (Hidalgo, Querétaro, San Luis Potosi) Guatemala, Mexico (Chiapas, Oaxaca) Mexico (Hidalgo, Puebla, Veracruz) Mexico (San Luis Potosi) Mexico (Chiapas, Tabasco, Veracruz) Mexico (Chiapas)

1848

Bull. Soc. Imp. Naturalistes Moscou 30: 186–188, t. 3, fig. 6, t. 4. fig. 22 Tijdschr. Wis-Natuurk. Wetensch. Eerste Kl. Kon. Ned. Inst. Wetensch. 1: 197–209 Lloydia 2(2): 75–76 Ann. Sci. Nat. Bot., ser. 3, 5: 7–9, t. 1 Madroño 30(1): 39–42 Index Palm.: 49–54, 68 Bot. J. Linn. Soc. 137(1): 81–85, fig. 1–2, as C. mirandai continued

1939 1846 1983 1854 2001

221

Mexico (Chiapas) Mexico (Tabasco) Mexico (Oaxaca, Veracruz)

Page 221

C. alvarezii Pérez-Farr., Vovides & Iglesias C. becarrae Pérez-Farr., Vovides & Schutzman C. euryphyllidia Vázq. Torres, Sabato & D. W. Stev. C. fusco-viridis D. Moore C. hildae G.P. Landry & M.C. Wilson C. huastecorum S. Avendaño, Vovides & Cast.Campos C. kuesteriana Regel

Bot. Gaz. 54 : 419 Bot. Mag. 89: sub t. 5398 Appendix 1: The World List of Cycads

CERATOZAMIA Brongn. (1846) (21 species; Mexico, Guatemala & Belize)

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B. serrulata (W. Bull) Chamb. *B. spectabilis Hook. ex Hook. f.

Bot. Mag. 89: sub t. 5398

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Mexico (Oaxaca) Mexico (San Luis Potosi) Mexico (Chiapas)

1995 1963 2001

Phytologia 79(1) (publ. 1996): 51–57 Brittonia 15: 175–176 Bot. J. Linn. Soc. 137(1): 77–80 , fig. 1

C. bernalii D.W. Stev. *C. restrepoi D.W. Stev.

Colombia Colombia

CYCAS L. (1753) (98 species, Asia, Australia, Indian and SW Pacific Ocean countries) C. aculeata K.D. Hill & Hiêp N. Vietnam C. angulata R. Br. Australia (NT, Qld) C. apoa K.D. Hill New Guinea C. arenicola K.D. Hill Australia (NT) C. armstrongii Miq. Australia (NT) C. arnhemica K.D. Hill Australia (NT) subsp. muninga Chirgwin & K.D. Hill Australia (NT) subsp. natja K.D. Hill Australia (NT) C. badensis K.D. Hill Australia (Qld) C. balansae Warb. China (Guangxi), N. Vietnam

Mem. New York Bot. Gard. 57: 169–172 1990 1990

Mem. New York Bot. Gard. 57: 169–172 Mem. New York Bot. Gard. 57: 169–172

xxxx 1810 1994 1993 1868 1994 1996 1996 1996 1900

Sp. Pl.: 1188. Mem. New York Bot. Gard. (in press) Prodr. 1: 348 Austral. Syst. Bot. 7: 553–554, fig. 9 Telopea 5(2): 419–422 Arch. Néerl. Sci. Exact. Nat. 3(5): 235–236 Telopea 5(4): 693–696, fig. 1 Telopea 7(1): 44–46, fig. 20 Telopea 7(1): 46–47, fig. 21 Telopea 7(1): 20–21, fig. 9 Monsunia 1: 179

K.D. Hill et al.

CHIGUA D.W. Stev. (1990) (2 species, South America)

Page 222

Mexico (Veracruz) Mexico (Chiapas, Oaxaca) Belize, Guatemala, Mexico (Chiapas, Oaxaca, Veracruz) Mexico (Hidalgo, Querétaro)

Phytologia 83(1) (publ. June 1998): 47–52 Novon 8(1): 87–90, fig. 1 Brittonia 34: 181–184 Tijdschr. Wis-Natuurk. Wetensch. Eerste Kl. Kon. Ned. Inst. Wetensch. 1: 33–44 Novon 3(4): 502–504

3:52 pm

1997

28/11/03

C. sabatoi Vovides, Vázq. Torres, Schutzman & Iglesias C. whitelockiana Chemnick & T.J. Greg. C. zaragozae Medellin-Leal C. zoquorum Pérez-Farr., Vovides & Iglesias

Mexico (Oaxaca)

222

C. mixeorum Chemnick & T.J. Greg. & SalasMorales C. morettii Vázq. Torres & Vovides C. norstogii D.W. Stev. C. robusta Miq.

X00app1.qxd

1883

C. bifida (Dyer) K.D. Hill C. bougainvilleana K.D. Hill

China (Guangxi), N. Vietnam Bougainville, New Britain, Solomon Islands N. Vietnam Australia (NT, Qld) Australia (Qld) Australia (NT) New Guinea Australia (NT) Australia (NT) Australia (Qld) Thailand China (Hainan) C. Vietnam India (Andhra Pradesh, Karnataka, Kerala, Maharashtra, Tamil Nadu) Malaysia, Thailand Cambodia, Thailand, S. Vietnam N. Vietnam S. Vietnam Australia (NT) Australia (Qld) Australia (Qld) Philippines (Palawan) China (Guangxi)

xxxx 1994 xxxx 1992 1876 1978 1994 1994 1994 xxxx 1999 1998 1931 1753

Mem. New York Bot. Gard. (in press) Telopea 5(1): 200–201, fig. 15 Fragm. 10: 63, 121 J. Adelaide Bot. Gard. 1(3): 175–178, fig. 1 Austral. Syst. Bot. 7: 538–540 Telopea 5(4): 698–700, fig. 4a-d Telopea 5(4): 699–700, fig. 4e-g Telopea (in press) Brittonia 51(1): 58, fig. 6 Acta Phytotax. Sin. 36(6): 552–554, fig. 1 in Lecompte, Fl. Indo-Chine 5(10): 1092 Sp. Pl.: 1188

1999 1999 xxxx xxxx 1993 1992 2002 1995 1997

Brittonia 51(1): 62–63, fig. 8a-d, g-h Brittonia 51(1): 64, fig. 8e,f,i Mem. New York Bot. Gard. (in press) Mem. New York Bot. Gard. (in press) J. Adelaide Bot. Gard. 15(2): 147 Telopea 5(1): 197–198, fig. 13 Austrobaileya 6: 153 Proc. Third Int. Conf. Cycad Biol.: 150 Acta Phytotax. Sin. 35(6): 571

C. brachycantha K.D. Hill, Hiêp & P.K. Loc C. brunnea K.D. Hill C. cairnsiana F. Muell. C. calcicola Maconochie C. campestris K.D. Hill C. canalis K.D. Hill subsp. carinata K.D. Hill C. candida K.D. Hill C. chamaoensis K.D. Hill C. changjiangensis N. Liu C. chevalieri Leandri *C. circinalis L. C. clivicola K.D. Hill subsp. lutea K.D. Hill C. collina K.D. Hill, Hiêp & P.K. Loc C. condaoensis K.D. Hill & S.L. Yang C. conferta Chirgwin ex Chirgwin & Wigston C. couttsiana K.D. Hill C. cupida P.I. Forst. C. curranii (J. Schust.) K.D. Hill C. debaoensis Y.C. Zhong & C.J. Chen

continued

Page 223

India (Andhra Pradesh)

3:52 pm

C. beddomei Dyer

Bull. Woods Forests Dept., Western Australia 32: 31 Trans. Linn. Soc. London, Bot., ser. 2, 5: 85–86, pl. 17 Mem. New York Bot. Gard. (in press) Austral. Syst. Bot. 7: 557–560, fig. 11

28/11/03

1923

223

Australia (WA)

Appendix 1: The World List of Cycads

C. basaltica C.A. Gardner

X00app1.qxd

1997 1999 1996 1996 1996 1854 1810 1996 1996

Telopea 7(1): 48–49, fig. 22 Telopea 7(1): 49–51 Telopea 7(1): 51–52. fig. 23 Not. Pl. Asiat. 4: 11–14, pl. 362, fig. 2 Prodr. 1: 348 Telopea 7(1): 15–16 Telopea 7(1): 14–15, fig. 6

C. maconochiei Chirgwin & K.D. Hill subsp. lanata K.D. Hill subsp. viridis K.D. Hill C. macrocarpa Griff. C. media R. Br. subsp. banksii K.D. Hill subsp. ensata K.D. Hill

Page 224

S. Vietnam Malaysia, Myanmar, Sumatra Thailand, S. Vietnam Australia (NT) Australia (NT) Australia (NT) Malaysia, Thailand Australia (Qld) Australia (Qld) Australia (Qld)

3:52 pm

C. lindstromii S.L. Yang, K.D. Hill & Hiêp C. litoralis K.D. Hill

Austrobaileya 4(3): 345–352, fig. 1–5 Sichuan Forestry & Design 1995: 1 Mem. New York Bot. Gard. (in press) in De Laub. & Adema, Blumea 43: 372 Brittonia (in press) Cycads China: 51, as C. elonga Cycads China: 54 Kew Bull. 54(1): 209 Guihaia 14: 300 Mem. New York Bot. Gard. (in press) J. & Proc. Roy. Soc. Western Australia 3: 108 Comm. Phytog.: 127 Acta Phytotax. Sin. 21(2): 209–210 Acta Phytotax. Sin. 13(4): 82, t. 2, fig. 5–6 Mem. New York Bot. Gard. (in press) in D.Y. Wang, Cycads China: 62 Fl. Cochinch., ed. 2, 2: 776–777 in D.Y. Wang, Cycads China: 65 Bull. Woods Forests Dept., Western Australia 32: 30–32, fig. E Novon 7: 213–215, fig. 1 Brittonia 51(1): 70–72, fig. 11

28/11/03

1995 1995 xxxx 1998 xxxx 1996 1996 1999 1994 xxxx 1918 1840/41 1983 1975 xxxx 1996 1793 1996 1923

K.D. Hill et al.

Australia (Qld) China (Yunnan) China (Yunnan), N. Vietnam Philippines (Sulu) Thailand S. Vietnam China (Guangdong) Indonesia China (Guangxi) N. Vietnam Australia (WA) East Timor, Indonesia China (Guanxi, Guizhou, Yunnan) China (Hainan) N. Vietnam China (Yunnan) S. Vietnam Indonesia Australia (WA)

224

C. desolata P.I. Forst. C. diannanensis Z.T. Guan & G.D. Tao C. dolichophylla K.D. Hill, Hiêp & P.K. Loc C. edentata de Laub. C. elephantipes A. Lindström & K.D. Hill C. elongata (Leandri) D. Yue Wang C. fairylakea D. Yue Wang C. falcata K.D. Hill C. ferruginea F.N. Wei C. fugax K.D. Hill, Hiêp & P.K. Loc C. furfuracea W. Fitzg. C. glauca hort. ex Miq. C. guizhouensis K.M.Lan & R.F. Zou C. hainanensis C.J. Chen C. hoabinhensis K.D. Hill, Hiêp & P.K. Loc C. hongheensis S.Y. Yang & S.L. Yang C. inermis Lour. C. javana (Miq.) de Laub. C. lane-poolei C.A. Gardner

X00app1.qxd

New Guinea China (Yunnan), India, Laos, Myanmar, Thailand Thailand Australia (Qld) Thailand

1876 1826 xxxx 1992 1999

Australia (WA) Japan (Ryukyu Islands)

1978 1782 1863 1839

C. saxatilis K.D. Hill & A. Lindström C. schumanniana Lauterb.

Philippines (Luzon) S. Borneo, E. Indonesia, NE Java, Moluccan Islands, New Guinea, Sulawesi Philippines (Palawan) New Guinea

C. scratchleyana F. Muell.

New Guinea

1885

C. petraea A. Lindström & K.D. Hill C. platyphylla K.D. Hill C. pranburiensis S.L. Yang, W. Tang, K.D. Hill & Vatacharakorn C. pruinosa Maconochie C. revoluta Thunb. C. riuminiana Porte ex Regel C. rumphii Miq.

xxxx 1901

J. Adelaide Bot. Gard. 1(3): 177–178, fig. 2. Verh. Holl. Maatsch. Weetensch. Haarlem 20(2): 424, 426–427 Gartenflora 12: 16–17 Bull. Sci. Phys. Nat. Néerl. 2: 45 In preparation Fl. Schutzger. Sudsee (publ. Nov. 1900): 154–155 Victorian Naturalist 2(2): 18–19

225

continued

Page 225

C. papuana F. Muell. C. pectinata Buch.-Ham.

Telopea 5(1): 188–189, fig. 5 Gard. Chron., ser. 3, 38: 142–144, fig. 48–49 Austral. Syst. Bot. 7: 554–557, fig. 10 Acta Phytotax. Sin. 32: 239, 480–481 Pflanzenr. 99: 76, fig. 10E Brittonia 51(1): 60–62, fig. 7 Telopea 5(1): 190–191, fig. 7 Telopea 5(4): 696–697, fig. 3 Mem. New York Bot. Gard. (in press) Acta Phytotax. Sin. 19(3): 335, t. 10, fig. 1–6, t.11, fig. 1–10 Descr. Notes Papuan Pl. 4: 71–72 Mem. Wern. Nat. Hist. Soc. 2(2): 322– 323, fig. 3,5 Brittonia (in press) Telopea 5(1): 193–194, fig. 9 Brittonia 51(1): 44–47, fig. 1

3:52 pm

1992 1905 1994 1994 1932 1999 1992 1994 xxxx 1981

28/11/03

Australia (Qld) E. Laos, Central Vietnam Micronesia (Marianas Islands) China (Yunnan) Sri Lanka Thailand Australia (Qld) Australia (NT) S. Vietnam China (Sichuan, Yunnan)

Appendix 1: The World List of Cycads

C. megacarpa K.D. Hill C. micholitzii Dyer C. micronesica K.D. Hill C. multipinnata C.J. Chen & S.Y. Yang C. nathorstii J. Schust. C. nongnoochiae K.D. Hill C. ophiolitica K.D. Hill C. orientis K.D. Hill C. pachypoda K.D. Hill C. panzhihuaensis L. Zhou & S.Y. Yang

X00app1.qxd

Telopea 5(1): 181–182, fig. 1 Proc. Third Int. Conf. Cycad Biol.: 150

1832 xxxx 1975

Fl. Ind.: 747 In preparation Acta Phytotax. Sin. 13(4): 81, t. 1, fig. 7–8

Taiwan

1994

Bot. Bull. Acad. Sin. 35: 135–138

China (Guangdong) China (Yunnan) Thailand E. Africa, Indian Ocean Islands N. Vietnam Australia (Qld) Philippines (Culion) Australia (Qld) Australia (Qld) Sri Lanka

1893 1996 1999 1829 xxxx 1996 1936 1996 1996 xxxx

J. Bot. 31: 1–3, pl. 331 Cycads of China: 134 Brittonia 51(1): 65–66 Voy. Uranie, Bot: 434 Mem. New York Bot. Gard. (in press) Telopea 7(1): 20–23, fig. 10 Phillipp. J. Sci. 60(3): 234–236, pl. 1–4 Telopea 7(1): 32–33, fig. 15 Telopea 7(1): 18–19, fig. 8 Novon (in press)

Page 226

1992 1995

3:52 pm

Sitzungdber. Ges. Naturf. Freunde Berlin: 114–115 Encephalartos 43: 11–14 Telopea 7(1): 23–25, fig. 11 Guihaia 16: 1 Bot. Zeitung Berlin 21: 334

K.D. Hill et al.

C. sphaerica Roxb. C. sundaica K.D. Hill & A. Lindström C. szechuanensis C.Y. Cheng, W.C. Cheng & L.K. Fu C. taitungensis C.F. Shen, K.D. Hill, C.H. Tsou & C.J. Chen C. taiwaniana Carruth. C. tanqingii D. Yue Wang C. tansachana K.D. Hill & S.L. Yang C. thouarsii R. Br. ex Gaudich. C. tropophylla K.D. Hill & P.K. Loc C. tuckeri K.D. Hill C. wadei Merrill C. xipholepis K.D. Hill C. yorkiana K.D. Hill C. zeylanica (Schuster) K.D. Hill & A. Lindström

1876 1995 1996 1996 1863

28/11/03

C. silvestris K.D. Hill C. simplicipinna (Smitinand) K.D. Hill

SW Pacific islands China (Guanxi, Guizhou, Yunnan) Australia (Qld) China (Guangxi), Vietnam Cambodia, Laos, Myanmar, Thailand, S. Vietnam Australia (Qld) China (Yunnan), Laos, Myanmar, Thailand, N. Vietnam India (Orissa) Indonesia China (Fijian, Guangdong)

226

C. seemannii A. Braun C. segmentifida D. Yue Wang & C.Y. Deng C. semota K.D. Hill C. sexseminifera F.N. Wei C. siamensis Miq.

X00app1.qxd

Biol. J. Linn. Soc. 80 (in press) Bot. J. Linn. Soc. 141: 471–476

Mexico (Oaxaca, Puebla) Mexico (Oaxaca, Puebla) Mexico (Veracruz) Mexico (Oaxaca) N. Honduras, Nicaragua Mexico (Oaxaca, Chiapas) Mexico (Oaxaca) Mexico (Oaxaca)

1979 1980 1843 1981 1950 1981 1909 1980

Brittonia 31(1): 170–172 Brittonia 32(1): 44–46 Edward’s Bot. Reg. 29: misc. 59–60 Brittonia 33(4): 552–554 Ceiba 1: 36–38 Brittonia 33(2): 180–184 Contr. U.S. Natl. Herb. 12(7): 260–261 Brittonia 32(2): 225–229

Mexico (NW coast)

1997

Phytologia 83(1) (publ. 1998): 1–6

Mexico (Oaxaca, Veracruz) Mexico (SW coast)

1883 1984

in Eichler, Gart. Zeit. 2: 411–413, fig. 80 Brittonia 36: 225–227

ENCEPHALARTOS Lehm. (1834) (65 species, Africa) South Africa (KwaZulu-Natal) South Africa (E. Cape) Swaziland South Africa (E. Cape) Benin, Ghana, Nigeria Nigeria South Africa (Limpopo) Kenya, Tanzania

1990 1834 1996 1956 1868 1978 1996 1957

S. African J. Bot. 56(2): 239–243 Pugill. 6: 11, t. 4 & 5 S. African J. Bot. 62: 57–60 J. S. African Bot. 22(1): 1–4 Arch. Néerl. Sci. Exact. Nat. 3: 243 J. Linn. Soc. Bot. 77: 125–129 S. African J. Bot. 62(1): 61–64 Kew Bull. 1957: 252

continued

227

E. aemulans Vorster E. altensteinii Lehm. E. aplanatus Vorster E. arenarius R.A. Dyer E. barteri Carruth. ex Miq. subsp. allochrous L.E. Newton E. brevifoliolatus Vorster E. bubalinus Melville

Pugill. 6: 14

Page 227

2003 2003

3:52 pm

Mexico (Nuevo Leon, Tamaulipas) Mexico (Oaxaca)

Appendix 1: The World List of Cycads

D. angustifolium Miq. D. argenteum T.J. Greg., Chemnick, Salas-Mor. & Vovides D. califanoi De Luca & Sabato D. caputoi De Luca, Sabato & Vázq. Torres *D. edule Lindl. D. holmgrenii De Luca, Sabato & Vázq. Torres D. mejiae Standl. & L.O. Williams D. merolae De Luca, Sabato & Vázq. Torres D. purpusii Rose D. rzedowskii De Luca, A. Moretti, Sabato & Vázq. Torres D. sonorense (De Luca, Sabato & Vázq. Torres) Chemnick, T.J. Greg. & Salas-Mor. D. spinulosum Dyer D. tomasellii De Luca, Sabato & Vázq. Torres

Edward’s Bot. Reg. 29: misc. 59–60

28/11/03

DIOON Lindl. (1843) (13 species; Honduras, Mexico, Nicaragua)

X00app1.qxd

Pugill. 6: 8, T. 1–3 Ill. Hort. 14, misc.: 80 Bull. Misc. Inform.: 181 Bothalia 10(4): 539–546 Ind. Sem. Hort. Berol.: 8 S. African J. Bot. 62(1): 46–48, fig. 1 Pugill. 6: 14 Bothalia 6: 220–241, pl. 3 Bothalia 8(2): 169–170 Mem. New York Bot. Gard. 57: 152–155 Utafiti 2(1): 7–10 Fl. Transvaal & Sw. 1: 40, 99

1926 1837–38

Fl. Transvaal & Sw. 1: 40, 90, Fig. 4D Tijdschr. Natuurl. Gesch. Physiol. 4: 424, T. 9

Page 228

1834 1867 1916 1972 1874 1996 1834 1951 1964 1990 1989 1926

3:52 pm

Pugill. 6: 14 Durban Mus. Novit. 14: 153–156 Kirkia 7: 147–158 Kirkia 7: 147–158 Bothalia 10(2): 379–383 Pugill. 6: 13 Ann. Gembloux 98: 153 Bull. Jard. Bot. Belg. 58: 219–224 Bull. Jard. Bot. Belg. 58: 219–224 S. African J. Bot. 61(4): 226–229 J. S. African Bot. 11(1): 1–3 Mem. Reale Accad. Sci. Ist. Bologna 3: 264

28/11/03

E. lanatus Stapf & Burtt Davy E. latifrons Lehm.

1834 1989 1969 1969 1971 1834 1992 1988 1988 1995 1945 1851

K.D. Hill et al.

*E. friderici-guilielmi Lehm. E. ghellinckii Lem. E. gratus Prain E. heenanii R.A. Dyer E. hildebrandtii A. Braun & Bouché E. hirsutus P.J.H. Hurter E. horridus (Jacq.) Lehm. E. humilis I. Verd. E. inopinus R.A. Dyer E. ituriensis Bamps & Lisowski E. kisambo Faden & Beentje E. laevifolius Stapf & Burtt Davy

South Africa (E. Cape) South Africa (KwaZulu-Natal) Mozambique, Zimbabwe Zimbabwe South Africa (Mpumalanga) South Africa (E. Cape) Tanzania South Africa (Limpopo) South Africa (Limpopo) Uganda South Africa (Limpopo) Mozambique, South Africa (KwaZulu-Natal) South Africa (E. Cape, KwaZulu-Natal) South Africa (E. Cape, KwaZulu-Natal) Malawi, Mozambique South Africa (Mpumalanga), Swaziland Kenya, Tanzania South Africa (Limpopo) South Africa (E. Cape) South Africa (Mpumalanga) South Africa (Limpopo) Dem. Rep. of Congo, Uganda Kenya South Africa (E. Cape, KwaZulu-Natal, Limpopo Province, Mpumalanga), Swaziland South Africa (Mpumalanga) South Africa (E. Cape)

228

E. caffer (Thunb.) Lehm. E. cerinus Lavranos & D.L. Goode E. chimanimaniensis R.A. Dyer & I. Verd. E. concinnus R.A. Dyer & I. Verd. E. cupidus R.A. Dyer E. cycadifolius (Jacq.) Lehm. E. delucanus Malaisse, Sclavo & Crosiers E. dolomiticus Lavranos & D.L. Goode E. dyerianus Lavranos & D.L. Goode E. equatorialis P.J.H. Hurter E. eugene-maraisii I. Verd. E. ferox Bertol. f.

X00app1.qxd

Pugill. 6: 14 Pugill. 6: 14 Bot. J. Linn. Soc. 140: 187–192, fig. 1–6 Encephalartos 50: 13–17, figs. 1, 2 Proc. Rhodesia Sci. Assoc. 37: 133–134 Bull. Soc. Roy. Bot. Belgique 91: 104–10 S. African J. Bot. 55: 122–126 S. African J. Bot. 62(2): 67–70 Kirkia 7: 147–158 Bothalia 6(1): 205–211, pl. 1–3 Fl. Pl. Africa 27: pl. 1053, 1054

1995 1926 1878 1965 1969 2001 1993 1969 1989 1996

Phytologia 78(6): 409–410, fig. 1 Fl. Transvaal & Sw. 1: 40 & 99, fig. 4A Verh. Bot. Vereins Prov. Brandenburg 20: 35–36 J. S. African Bot. 31(2): 111–112, pl. 19 Kirkia 7: 147–158 Bothalia 31(2): 197–199 Bull. Jard. Bot. Belg. 62: 215–219 Bull. Jard. Bot. Belg. 39: 401–406 Delpinoa 29–30: 3–5 S. African J. Bot. 62(2): 76–79

1871 1957 1999

Bot. Zeitung Berlin 29: 334 Kew Bull. 1957: 249 J. East African Nat. Hist. 88: 35

continued

Page 229

1834 1834 2002 1997 1939 1958 1989 1996 1969 1951 1949

229

E. septentrionalis Schweinf. E. tegulaneus Melville subsp. powysii Miringu & Beentje

Etudes Fl. Bas et Moy – Congo 1: 10, T. 25 Fl. Pl. Africa 27: pl. 1078–1079

3:52 pm

E. nubimontanus P.J.H. Hurter E. paucidentatus Stapf & Burtt Davy E. poggei Asch. E. princeps R.A. Dyer E. pterogonus R.A. Dyer & I. Verd. E. relictus P.J.H. Hurter E. schaijesii Malaisse, Sclavo & Crosiers E. schmitzii Malaisse E. sclavoi De Luca, D.W. Stev. & A. Moretti E. senticosus Vorster

1903 1949

Appendix 1: The World List of Cycads

E. lehmannii Lehm. E. longifolius (Jacq.) Lehm. E. mackenziei L.E.Newton E. macrostrobilus S. Jones & Wynants E. manikensis (Gilliland) Gilliland E. marunguensis Devred E. middelburgensis Vorster E. msinganus Vorster E. munchii R.A. Dyer & I. Verd. E. natalensis R.A. Dyer & I. Verd. E. ngoyanus I. Verd.

Angola, Dem. Rep. of Congo Mozambique, South Africa (KwaZulu-Natal), Swaziland South Africa (E. Cape) South Africa (E. Cape) Sudan N. Uganda Mozambique, Zimbabwe Dem. Rep. of Congo South Africa (Mpumalanga) South Africa (KwaZulu-Natal) Mozambique South Africa (KwaZulu-Natal) South Africa (KwaZulu-Natal), Swaziland South Africa (Limpopo) South Africa (Mpumalanga), Swaziland Dem. Rep. of Congo South Africa (E. Cape) Mozambique Swaziland Dem. Rep. of Congo Dem. Rep. of Congo, Zambia Tanzania South Africa (KwaZulu-Natal), Swaziland Sudan, Uganda Kenya Kenya

28/11/03

E. laurentianus De Wild. E. lebomboensis I. Verd.

X00app1.qxd

Fl. Transvaal & Sw. 1: 40, 99, fig. 4B J. S. African Bot. 31(2): 112–116, pl. 20 Garcia de Orta, sér. Bot. 7: 11–14 Fl. Pl. Africa 28: pl. 1100 Ill. Hort. 14, misc.: 79; 15: T. 557

1995 1908

Phytologia 78(6): 410–411, fig. 3 Gard. Chron.: 257

Australia (Qld) Australia (NSW, Qld)

1876 1857

MACROZAMIA Miq. (1842) (40 species, Australia) M. cardiacensis P.I. Forst. & D.L. Jones M. communis L.A.S. Johnson M. concinna D.L. Jones M. conferta D.L. Jones & P.I. Forst. M. cranei D.L. Jones & P.I. Forst. M. crassifolia P.I. Forst. & D.L. Jones M. diplomera (F. Muell.) L.A.S. Johnson M. douglasii W. Hill ex F.M. Bailey M. dyeri (F. Muell.) C.A. Gardner M. elegans K.D. Hill & D.L. Jones M. fawcettii C. Moore M. fearnsidei D.L. Jones

Australia (Qld) Australia (NSW) Australia (NSW) Australia (Qld) Australia (Qld) Australia (Qld) Australia (NSW) Australia (Qld) Australia (WA) Australia (NSW) Australia (NSW) Australia (Qld)

Gartenflora 25: 3–6 Bull. Soc. Imp. Naturalistes Moscou 30: 184 Monogr. Cycad.: 35

1998 1959 1998 1994 1994 1994 1959 1883 1930 1998 1884 1991

Fl. Australia 48: 717 Proc. Linn. Soc. New South Wales 64: 98 Fl. Australia 48: 718 Austrobaileya 4: 271–273, fig. 1 Austrobaileya 4: 273–275, fig. 2 Austrobaileya 4: 275–276, fig. 3 Proc. Linn. Soc. New South Wales 84: 98 Syn. Qld Fl. 500 Enum. Pl. Austral. Occid.: 3 Fl. Australia 48: 718 J. & Proc. Roy. Soc. New South Wales 17: 120 Austrobaileya 3: 481

K.D. Hill et al.

L. hopei Regel *L. peroffskyana Regel

Bull. Soc. Imp. Naturalistes Moscou 30: 182

Page 230

LEPIDOZAMIA Regel (1857) (2 species, Australia)

3:52 pm

1926 1965 1985 1951 1867

28/11/03

E. whitelockii P.J.H. Hurter E. woodii Sander

South Africa (Limpopo) South Africa (E. Cape) Mozambique Mozambique, Swaziland South Africa (E. Cape, KwaZulu-Natal), Swaziland Uganda South Africa (KwaZulu-Natal) (extinct in the wild)

230

E. transvenosus Stapf & Burtt Davy E. trispinosus (Hook.) R.A. Dyer E. turneri Lavranos & D.L. Goode E. umbeluziensis R.A. Dyer E. villosus Lem.

X00app1.qxd

231

continued

Page 231

J. & Proc. Roy. Soc. New South Wales 17: 121 Monogr. Cycad.: 37 Fl. Australia 48: 718 J. & Proc. Roy. Soc. New South Wales 17: 122 Fl. Australia 48: 719 Telopea 5(1): 31 Austrobaileya 3: 483 Fl. Australia 48: 717 Proc. Linn. Soc. New South Wales 84: 102 Prodr. 16(2): 537 Arch. Néerl. Sci. Exact. Nat. 3(5): 250 Prodr. 16(2): 535 Fl. Australia 48: 717 Austral. Chem. Drugg. 4: 84 Syn. Qld Fl., suppl. 1: 50 Austrobaileya 4: 278, fig. 5 Austrobaileya 4: 279–281, fig. 6 Fragm. 1: 86 Qld Agric. J. 3: 356 Austrobaileya 3: 484 Fl. Australia 48: 718 Fl. Australia 48: 718 Enum. Pl. Austral. Occid.: 3 J. & Proc. Roy. Soc. New South Wales 17: 122 Austrobaileya 6(1): 90–92, fig. 20–21 Monogr. Cycad.: 36 Proc. Linn. Soc. New South Wales 84: 106 Austrobaileya 4: 281–283, fig. 7

3:52 pm

1884 1842 1998 1884 1998 1992 1991 1998 1959 1868 1868 1868 1998 1881 1886 1994 1994 1859 1898 1991 1998 1998 1930 1884 2001 1842 1959 1994

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Australia (NSW) Australia (WA) Australia (NSW) Australia (NSW) Australia (NSW) Australia (NSW) Australia (Qld) Australia (Qld) Australia (NSW, Qld) Australia (NT) Australia (Qld) Australia (Qld) Australia (NSW) Australia (Qld) Australia (Qld) Australia (Qld) Australia (Qld) Australia (Qld) Australia (Qld) Australia (NSW, Qld) Australia (NSW) Australia (NSW) Australia (WA) Australia (NSW) Australia (Qld) Australia (NSW) Australia (NSW) Australia (Qld)

Appendix 1: The World List of Cycads

M. flexuosa C. Moore M. fraseri Miq. M. glaucophylla D.L. Jones M. heteromera C. Moore M. humilis D.L. Jones M. johnsonii D.L. Jones & K.D. Hill M. lomandroides D.L. Jones M. longispina P.I. Forst. & D.L. Jones M. lucida L.A.S. Johnson M. macdonnellii (F. Muell. ex Miq.) A. DC. M. macleayi Miq. M. miquelii (F. Muell.) A. DC. M. montana K.D. Hill M. moorei F. Muell. M. mountperriensis F.M. Bailey M. occidua D.L. Jones & P.I. Forst. M. parcifolia P.I. Forst. & D.L. Jones M. pauli-guilielmi W. Hill & F. Muell. M. platyrhachis F.M. Bailey M. plurinervia (L.A.S. Johnson) D.L. Jones M. polymorpha D.L. Jones M. reducta K.D. Hill & D.L. Jones *M. riedlei (Gaudich.) C.A. Gardner M. secunda C. Moore M. serpentina D.L. Jones & P.I. Forst. M. spiralis (Salisb.) Miq. M. stenomera L.A.S. Johnson M. viridis D.L. Jones & P.I. Forst.

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1868

STANGERIA T. Moore (1853) (1 species, Southern Africa) South Africa (E. Cape, kwaZulu-Natal)

Hook. Kew J., misc. 5: 228–229 1892

ZAMIA L. (1763) (58 species, South, Central & North America)

Sp. Pl., ed. 2, 2: 1659

Costa Rica, Nicaragua, N. Panama Brazil, Colombia, (Amazonas, Chocó), Ecuador, Peru, S. Venezuela Cuba, Jamaica, Puerto Rico Colombia (Valle) Bahamas N. Bolivia, Brazil. Colombia (Chocó), Panama (Chiriqui) Mexico (Tabasco) Panama Colombia (Antioquia), Peru (Huánuco) Panama Panama

1884 2001

in Hemsl., Biol. Cent.-Amer., Bot. 3: 190–195 Fl. Colombia 21: 33

1987 1878 1789 1868 1854 1988 1993 2001 1993 1998

Fairchild Trop. Gard. Bull. 42(3): 26 Gard. Chron., ser. 2, 10(261): 810 Collectanea 3: 263–265, pl. 636 Prodr. 16(2): 540 Bot. Voy. Herald 6: 201–203, t. 43 Bot. Gaz. 149(3): 351–354, fig. 4–5 Brittonia 45(1): 5–6 Fl. Colombia 21: 38 Brittonia 45(1): 6 Phytologia 85(3) (publ. Apr. 2000): 137–145

Colombia (Santander) Costa Rica, Panama Mexico (Querétaro, San Luis Potosi) Mexico (Veracruz) Ecuador

2001 1982 1845 1789 1998

Fl. Colombia 21: 40 Phytologia 50: 401–404 in Lem., Hort. Vanhoutt. 1: 20 in Aiton, Hortus Kew. 3: 477 Novon 8(1): 12–14, fig. 1a-f

K.D. Hill et al.

Z. amblyphyllidia D.W. Stev. Z. amplifolia hort. Bull ex Mast. Z. angustifolia Jacq. Z. boliviana (Brongn.) A. DC. Z. chigua Seem. Z. cremnophila Vovides, Schutzman & Dehgan Z. cunaria Dressler & D.W. Stev. Z. disodon D.W. Stev. & Sabato Z. dressleri D.W. Stev. Z. elegantissima Schutzman, Vovides & R.S. Adams Z. encephalartoides D.W. Stev. Z. fairchildiana L.D. Gómez Z. fischeri Miq. Z. furfuracea L. f. Z. gentryi Dodson

Hist. Pl. 12: 68

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*Microcycas calocoma (Miq.) A. DC.

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MICROCYCAS (Miq.) A. DC. (1868) (1 species, Cuba)

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Z. lucayana Britton Z. macrochiera D.W. Stev. Z. manicata Linden ex Regel Z. melanorrhachis D.W. Stev. Z. montana A. Braun Z. monticola Chamb. Z. muricata Willd. Z. neurophyllidia D.W. Stev. Z. obliqua A. Braun

Guatemala Colombia (Boyacá, Guajira, Meta, Santander),Venezuela (Guarico) Costa Rica, S. Nicaragua, N. Panama Colombia (Antioquia, Chocó, Valle), S. Panama Mexico

Fl. Colombia 21: 43 Flora de Veracruz 26: 22–24

1789

in Aiton, Hortus Kew. 3: 477–479

1993 1842 1998 1915

Brittonia 45(1): 7–9 Monogr. Cycad.: 71, t. 8 Novon 8(4): 441–446, fig. 1–3 Arch. Jard. Bot. Rio de Janeiro 1: 9–10, pl. 1–2 Tijdschr. Natuurl. Gesch. Physiol. 10: 72–73

1843 1907 2004 1876 2001 1875 1926 1806 1993 1875 1916

Bull. New York Bot. Gard. 5(18): 311–318 [see Stevenson, Chapter 14 this volume] Trudy Imp. S.-Petersburgsk. Bot. Sada 4: 310, t. 926, fig. e Fl. Colombia 21: 55 Monatsber. Königl. Preuss. Akad. Wiss. Berlin: 376 Bot. Gaz. 81: 219, 223, fig. 1–3 Sp. Pl. ed. 4, 4: 847–848 Brittonia 45(1): 10, fig. 5 Monatsber. Königl. Preuss. Akad. Wiss. Berlin: 376 American Fossil Cycads 2: 212, fig. 86 continued

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Colombia (Amazonas, Cordoba, Santander) Colombia (Antioquia)

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Z. ipetiensis D.W. Stev. Z. kickxii Miq. Z. lacandona Schutzman & Vovides Z. lecointei Ducke

Bahamas, Cayman Islands, Cuba, USA (Florida, Georgia) Panama Cuba Mexico (Chiapas) Brazil, Colombia (Amazonas, Antioquia), Peru (Loreto), S. Venezuela Guamemala, Mexico (Hidalgo, Oaxaca, Veracruz) Bahamas (Long Island) Peru Colombia (Antioquia), Panama (Darien)

1924

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Z. hymenophyllidia D.W. Stev. Z. inermis Vovides, J.D. Rees & Vázq. Torres Z. integrifolia L. f.

El Salvador, Guatemala, Honduras, Mexico (Chiapas) Colombia (Amazonas), Peru (Loreto) Mexico (Veracruz)

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Z. herrerae Calderón & Standl.

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Delpinoa n.s. 37–38 (publ. 1998): 3–8, fig. 1

1899 1881 1982 1854 1763 1983 1815 1873

Symb. Antill. 1: 291 Retail List: 20 Phytologia 50(6): 401–404 Bot. Voy. Herald 6: 201–203, 253 Sp. Pl., ed. 2, 2: 1659 Flora de Veracruz 26: 28–31 Bot. Mag. 43: t. 1741 Catalogue des Plantes Nouvelles 9: 10

1851 1988 1868 1989 1903 1907

Allg. Gartenzeitung 19: 146, fig. s.n. Bot. Gaz. 149(3): 347–351 Prodr. 16(2): 539 Syst. Bot. 14(2): 214–219 Bot. Gaz. (Crawfordsville) 35(1): 8, pl. 1 Verh. Bot. Vereins Prov. Brandenburg 47: 117–118 Linz. Biol. Beitr. 28(2): 1056 Allg. Gartenz. 32: 252–253 Delpinoa n.s. 37–38 (publ. 1998): 9–17

1996 1845 1995–96

Mexico (Chiapas)

1870

Z. wallisii A. Braun

Colombia (Antioquia)

1875

Verh. Kon. Ned. Akad. Wetensch., Afd. Natuurk. 2(4): 31 Monatsber. Königl. Preuss. Akad. Wiss. Berlin: 376

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Peru Guatemala, Mexico (Chiapas) Mexico (Veracruz)

Z. skinneri Warsz. ex A. Dietrich Z. soconuscensis Schutzman, Vovides & Dehgan Z. spartea A. DC. Z. standleyi Schutzman Z. tuerckheimii Donn. Sm. Z. ulei Dammer

in Hemsl., Biol. Cent.-Amer., Bot. 3: 194 Fl. Bras. 4(1): 414–416, pl. 108–109

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Z. urep Walln. Z. variegata Warsz. Z. vazquezii D.W. Stev., Sabato, A. Moretti & De Luca Z. verschaffeltii Miq.

Z. polymorpha D.W. Stev., A. Moretti & Vázq. Torres Z. portoricensis Urban Z. prasina Bull Z. pseudomonticola L.D. Gómez Z. pseudoparasitica Yates in Seem. *Z. pumila L. Z. purpurea Vovides, J.D. Rees & Vázq. Torres Z. pygmaea Sims Z. roezlii Linden

1884 1863

K.D. Hill et al.

Guatemala, Mexico (Chiapas) Brazil, Colombia (Huila, Meta, Tolima), Ecuador, Peru Belize, Mexico (Campeche, Quintana Roo, Yucatan) Puerto Rico Belize W. Costa Rica N. Panama Cuba, Dominican Republic, Puerto Rico Mexico (Oaxaca, Veracruz) Cuba (W. Cuba, Isla de la Juventud) Colombia (Amazonas, Chocó, Nariño, Valle), Ecuador C. Panama, N. Panama Mexico (Chiapas) Mexico (Oaxaca) Honduras Guatemala W. Brazil, Colombia, Ecuador, Peru

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Z. picta Dyer Z. poeppigiana Mart. & Eichler

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References and Further Reading Brummit, R.K. and Powell, C.E. (1992) Authors of Plant Names. Royal Botanic Gardens, Kew, UK, 732 pp. Hill, K.D. and Stevenson, D.W. (2004) The world list of cycads. In: Stevenson, D.W. (ed.) Proceedings of the Fifth International Conference on Cycad Biology. Memoirs of the New York Botanical Garden (in press). Lawrence, G.H.M., Buchheim, A.F.G., Daniels, G.S. and Dolezal, H. (eds) (1968) BotanicoPeriodicum-Huntianum. Hunt Institute for Botanical Documentation, Pittsburgh, Pennsylvania, 1063 pp. Osborne, R. and Hendricks, J. (1985) A world list of cycads. Encephalartos 3, 13–17. Osborne, R. and Hendricks, J. (1986) A world list of cycads – supplement. Encephalartos 5, 27. Osborne, R. Stevenson, D.W. and Hill, K.D. (1999) The world list of cycads. In: Chen, C.J. (ed.) Biology and Conservation of Cycads. Proceedings of the Fourth International Conference on Cycad Biology. International Academic Publishers, Beijing, China, pp. 224–239. Stafleu, F.A. and Cowan, R.S. (1976, 1979, 1981, 1983) Taxonomic Literature, Second Edition, Vols 1–4. (Regnum Vegetabile 94, 98, 105, 110). Stevenson, D.W. and Osborne, R. (1993a) The world list of cycads. In: Stevenson, D.W. and Norstog, K.J. (eds) The Biology, Structure, and Systematics of the Cycadales. Proceedings of the Second International Conference on Cycad Biology, Palm & Cycad Societies of Australia Limited, Milton, Queensland, Australia, pp 354–364. Stevenson, D.W. and Osborne, R. (1993b) The world list of cycads. Encephalartos 33: 19–25. Stevenson, D.W., Osborne, R. and Hendricks, J. (1990) A world list of cycads. In: Stevenson, D.W. (ed.) The Biology, Structure, and Systematics of the Cycadales. Proceedings of the Symposium CYCAD 87. Memoirs of the New York Botanical Garden 57, pp. 200–206. Stevenson, D.W., Osborne, R. and Hill, K.D. (1995) The world list of cycads. In: Vorster, P. (ed.) Proceedings of the Third International Conference on Cycad Biology. Cycad Society of South Africa, Stellenbosch, South Africa, pp. 55–64.

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Appendix 2: Glossary of Terms Encountered in Cycad Systematics Roy Osborne1 and Terrence Walters2 1PO Box 244, Burpengary, Queensland, Australia; 2Montgomery Botanical Center, Miami, Florida, USA

Introduction A large number of terms is encountered in the literature relating directly or indirectly to cycad systematics. Many are technical terms found generally in botanical descriptions but some (e.g. omnule, omnel, corruptule, corruptel) are exclusive to cycad literature. Other terms (e.g. bulb, endosperm, frond) are used commonly but incorrectly with reference to cycads. Most terms are understood by readers in context, but many have a precise definition that is not readily found in general reference texts. Many terms encountered do not relate to plant descriptions per se, but to techniques of statistical and chemical analysis and to the relation of cycads to their environment. This glossary attempts to list and define all such terms, with cycad-specific examples where appropriate. Common acronyms, abbreviations and some Latin phrases are included.

Glossary Notes: Primary entries and relevant cross-references are indicated by bold type. Terms of the opposite meaning are indicated by ‘Cf.’ abaxial. Side of an organ facing away from a central axis, e.g. the lower side of a leaf or leaflet. Cf. adaxial. abscission. Process in which a corky cell layer forms across an axis, cutting off water and nutrient supply to the distal portion and resulting in its loss, as in 237 ©CAB International 2004. Cycad Classification: Concepts and Recommendations (eds T. Walters and R. Osborne)

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loss of a leaf, leaflike organ or section of stem. acaulescent. Without any evident trunk or stem. Cf. caulescent. acropetal. Progressing in direction from promixal to distal zone; from base to apex, e.g. as for the pollen dehiscence sequence in most cycad cones. Cf. basipetal. actinomorphic. Of a radially symmetric structure that can be halved in more than one plane to give two halves that are mirror images of each other; of seeds, radiospermic. Cf. zygomorphic. actran optimization. Optimization technique used in cladistics, based on ‘accelerated transformation’ and favouring acquisition of characters, with subsequent homoplasy accounted for by reversal. Cf. deltran optimization. aculeate. Having sharp prickles, as for the petiole of Cycas aculeata. acuminate. Tapering to a protracted point, with sides somewhat concave, as for the leaflets of Zamia acuminata. See also acute. acute. Narrowing to end in a sharp point, as for the leaflets of many cycad species. See also acuminate. Adansonian. Using as many unweighted characters as possible to arrive at a natural classification; 18th century naturalist Michel Adanson’s philosophy predated modern computer-aided numerical taxonomy. adaxial. Side of an organ facing towards a central axis, e.g. the upper side of a leaf or leaflet. Cf. abaxial. adventitious bud. Vegetative growth arising on a cycad stem, giving rise to suckers at the base or to offsets on the stem. affinis, affin., aff. Akin or allied to; used in reference to a specimen similar to a known species, but showing some differences. allele. One of two or more alternative forms of a gene at a given locus. allopatric. Of two or more taxa not overlapping in their distribution. Cf. sympatric. alpha-taxonomy. Descriptive taxonomy, based exclusively on morphological parameters. amphistomatic. Of leaves and leaflets with stomata on both surfaces. Cf. hypostomatic. anatomy. Study of the internal structure of organisms and their component parts. anemophily. Wind-effected pollen transfer. Cf. entomophily. angle(s) of insertion. See leaflet angle(s) of insertion. ANOVA. Analysis of variance, a tool used in statistics to apportion observed variance into probable causes. antherozoid (more commonly spermatozoid). Motile male gamete of lower plants, cycads, Ginkgo, etc. apex. Tip; proximal or distal end of an organ such as a shoot, leaf or root. apical meristem. Zone of actively dividing but as yet undifferentiated tissue at a shoot or root apex. apogeotropic, ageotropic, apogravitropic. Negatively geotropic; nega-

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tively gravitropic; developing in an orientation contrary to gravitational force, as with cycad coralloid roots. apomixis. Production of viable seeds without any apparent fertilization process. apomorphy. Derived character or character state. See also autapomorphy, homology, plesiomorphy, symplesiomorphy, synapomorphy. arborescent. Tree-like in habit. armed. Having spines or prickles. Cf. inerm. articulate. Separated by a node or joint; e.g. leaflets of Ceratozamia, Chigua, Microcycas and Zamia are articulated at their base. auctoris, auctorum, auct. Obsolete term previously used in taxonomy when an author had applied an incorrect name. autapomorphy. Derived character state unique to a terminal taxon in a particular data set. Note that an autapomorphy at a given hierarchical level may be a synapomorphy at a less inclusive level. See also apomorphy, homology, plesiomorphy, symplesiomorphy, synapomorphy. author, authority. Person who first publishes a valid name for a taxon. The author’s or authors’ name accompanies the taxonomic name, usually in abbreviated form, e.g. Carl Peter Thunberg in Cycas revoluta Thunb. autonym. Taxonomic name automatically established when a subdivision of a taxon such as a genus or species is published. The infrageneric or infraspecific taxon containing the type of the genus or species carries the same name or epithet as the respective genus or species, e.g. the publication of varieties within Dioon edule established the autonym Dioon edule var. edule. axis. Central line of development of a plant; the main stem. basionym. Combination of a name in the same rank as first validly published, e.g. genus and specific epithet in case of a species name, or generic name and infrageneric epithet in case of an infrageneric name. Basionyms are cited only when there is a recombination of genus name and epithet, e.g. the basionym in the publication of Encephalartos caffer (Thunb.) Lehm. is Zamia caffra Thunb. basipetal. Progressing in direction from distal to proximal; from apex to base. Cf. acropetal. bifid. Deeply notched or cleft for more than half the length. bifurcate. Forked in a Y-shaped manner, usually applying to leaves, leaflets or stems. binomial. Genus name and specific epithet for any species. biome. Broad vegetational subdivision of some biogeographical realm, e.g. forest, grassland, desert. bipinnate. Twice pinnate; of a compound leaf having both first order and second order divisions, i.e. pinnae and pinnules, as in both Bowenia species and some Cycas species. See also multipinnate. BMAA. β-n-methylamino-L-alanine, a neurotoxin found in cycad tissues. bootstrap value. Statistical estimate of confidence in a dendrogram or phylogenetic tree, obtained from repeated tree calculations by randomly eliminating selected characters while duplicating others to keep the total number

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of characters constant. bract. Leaf-like structure subtending an axillary bud or shoot, usually with a protective function. Occasionally misapplied to cycad cataphylls. bulb. Storage stem of limited longitudinal growth enveloped in fleshy leaf bases; misapplied to the bulbous trunks of some Cycas species; occasionally misapplied to cycad suckers. bulbous. Swollen to an almost spherical shape, as for the trunk base of Cycas pachypoda and several other Asian cycads. bulla (plural bullae). Bubble, blister or vesicle. Commonly also used in reference to the expanded shield-like distal portion of some cycad sporophylls such as Encephalartos megasporophylls. Although the derivation is technically incorrect, this term has become widely entrenched in cycad literature and its continued use is recommended. caducous. Deciduous at an early stage or prematurely. caespitose. Turf-shaped and forming a clump, as in many suckering cycads, e.g. Encephalartos cupidus. callous (adjective). Of the distinctive swollen tissue, often coloured, formed at the point of insertion of Macrozamia leaflets on to the rachis. Often confused with callus. callus (noun). Mass of hardened, thickened or undifferentiated parenchymatous tissue, e.g. as formed at the base of a cutting prior to root formation; undifferentiated cellular mass arising in tissue culture. See also callous. cataphyll. Modified leaf, much reduced and thickened, serving to protect the apical meristem in cycads and usually produced in flushes preceding the emergence of cones or leaves. caudex. Thick stem or trunk, often at least partially subterranean. caulescent. Having a trunk or stem. Cf. acaulescent. centromere. Region of a chromosome where spindle microtubules are attached during nuclear division. See also satellite. chalaza. Proximal end of a seed; its point of attachment. Cf. micropyle. channelled. With raised longitudinal edges to form a channel, as in the adaxial petiole surface of many cycads. character. Identifiable and hereditable trait which can be used in comparing one taxon with another. character states. Changeable attribute of any given character, e.g. if sarcotesta colour is a character, then red and yellow are character states. Many character states are simply recorded as present or absent. chartaceous. Papery in texture. See also membranous, papyraceous. chlorophyll. Green plant pigment in the cells of some bacteria and in plant chloroplasts, which captures energy from sunlight; an electron donor in photosynthesis. chloroplast. Plant cellular organelle in which photosynthesis occurs. See also chlorophyll. chromatid. One of the pair of threadlike forms of each chromosome. chromosome. Submicroscopic filamentous strand of DNA and associated pro-

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teins in the nucleus of all cells, by which hereditary information is transmitted from generation to generation. See also centromere, chromatid. CI. Consistency index, a measure of the amount of homoplasy for a character in a cladogram. See also RC, RI. circinate. Rolled in a coil-like manner with the apex innermost, as in leaflets of emerging leaves of Cycas species, hence C. circinalis. See also conduplicate, inflexed, ptyxis, reflexed, vernation. CITES. Convention on International Trade in Endangered Species, a United Nations treaty which sets out a conservation regulatory process between the signatory countries. clade. One particular monophyletic branch in a cladogram. cladistics. Method of classification that groups taxa hierarchically and parsimoniously into nested sets according to their synapomorphies; the output conventionally presented in the form of a cladogram. cladogram. Tree diagram based on parsimony analysis showing taxa grouped hierarchically in nested sets according to their synapomorphies. A cladogram has no connotation of ancestry and has no implied time axis. See also dendrogram, phenogram, phylogram. classification. Grouping of taxa or taxonomic groups into categories according to an overall plan. clone. Set of genetically identical individuals produced vegetatively from the same progenitor. coevolution. Concurrent evolution of two different but interdependent organisms, as in the case of a cycad and its insect pollinator. collar. In cycads, a coloured or textured band at base of a rachis, e.g. as seen in Encephalartos lehmannii leaves; a glandular swelling at the base of a leaflet, e.g. as seen in Zamia manicata leaves. combinatio nova, comb. nov. Nomenclatural new combination usually made by transferring a specific epithet from one genus to another, e.g. Dyerocycas micholitzii (Dyer) Nakai was a combinatio nova from Cycas micholitzii Dyer. community. Total of all living species in a particular habitat. conduplicate. Folded together lengthwise, usually in two equal halves, as in leaflets of emergent Stangeria leaves. See also circinate, inflexed, ptyxis, reflexed, vernation. cone. Reproductive structure of gymnosperms; organized collection of sporophylls on a central axis. See also strobilus, megasporangiate and microsporangiate strobili. confer, cf. Latin, meaning ‘compare’. congeneric. Belonging to the same genus; e.g. it is now thought that Epicycas is congeneric with Cycas. consensus tree. Cladogram representing the clades found in all the most parsimonious trees of an analysis, often from a large number of possible resolutions. conspecific. Belonging to the same species; e.g. some workers believe that

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Encephalartos altensteinii and E. natalensis are conspecific. contiguous. Touching or neighbouring, as in a common border between two countries. contractile. Of roots, and occasionally stems, which contract so as to pull the stem apex lower into the ground. convergence. Evolutionary process where dissimilar organs or organisms show strong superficial similarities. coralloid root. Club-shaped apogravitropic (apogeotropic) root with the potential for hosting symbiotic Cyanobacteria. coriaceous. Leathery in texture, as for the leaflets of many cycad species. corruptel. Kernel of a corruptule (Grobbelaar, 2002). corruptule. Unfertilized ovule that is superficially indistinguishable from a true seed (Grobbelaar, 2002). See also omnule. CSG. Cycad Specialist Group, a conservation-based group within the IUCN. cuneate. Wedge-shaped and attached at the narrow end. Curculionidae. Weevil family of insects. cuticle. In plants, the outer waxy layer of an epidermis, comprising mainly cutin with lesser amounts of overlaying waxes and polysaccharides. cutin. Complex polymeric mixture of fatty acids and phenolic compounds; the main component of a plant cuticle. Cyanobacteria. Group of bacteria capable of photosynthesis, previously known as blue-green algae, found in coralloid roots of cycads. Cycad Action Plan. Series of proposals for cycad conservation drafted by the CSG. Cycadales. Gymnosperm plant order containing all extant and extinct cycads. cycads. Members of the plant order Cycadales. cycasin. Toxic MAM glycoside found only in cycad tissue; methylazoxymethanol-β-D-glucopyranoside. See also macrozamin. cymbiform. Boat-shaped. cytology. Study of the structure, physiology and reproduction of cells. DAF. DNA amplification fingerprinting, a technique used in DNA analysis. decumbent. Of stems, lying along the ground but turning upwards distally. See also procumbent, prostrate. decurrent. Extending basipetally from the point of insertion, as for Lepidozamia leaflets where the leaflet base extends downwards along the rachis. dehiscence. Rupturing process where the contents of a plant structure are released, as in pollen shedding. deltran optimization. Optimization technique used in cladistics, based on ‘delayed transformation’ and favouring independent gains rather than acquisition and reversal. Cf. actran optimization. dendrogram. Generic term for any kind of tree diagram, including cladogram, phenogram and phylogram. dentate. Having sharp indentations or teeth along the edge of a structure and perpendicular to its margin. See also serrate. denticulate. Finely dentate. See also serrate, serrulate.

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determinate. With growth of an axis ceasing at a particular stage. Cf. indeterminate. dichotomous. Branching into two equal parts, as in forked branching of stems of Cycas elongata, leaflets of Macrozamia stenomera or megasporophyll lobes of Cycas segmentifida. Also used in reference to branching patterns in dendrograms. dimorphic. Having two different forms. See also homomorphic, monomorphic, polymorphic. dioecious. Having male and female reproductive parts on different plants. All extant cycads are dioecious. diploid. Having a pair of chromosomes of each kind. Cf. haploid. discriminant analysis. Statistical technique used in separating discrete sets of objects. disjunct. Separated geographically, pertaining to populations of the same taxon occurring in more than one geographical area. distal. Furthest away from the centre of a structure or, more commonly, furthest from its point of attachment; terminal; apical. Cf. proximal. DNA. Deoxyribonucleic acid; desoxyribonucleic acid, the molecule in which an organism’s genetic definition is determined by the sequence of nitrogenous bases projecting along a ‘backbone’ of sugar moieties linked by phosphodiester bonds. ecology. Study of relationships of living organisms to each other and to their physical and chemical environment. ecosystem. Sum of all biological, chemical and physical components of an area and their interaction. edaphic. Relating to the soil environment, e.g. soil quality, pH. electrophoresis. Analytical technique in which an electrical gradient is used to separate compounds, especially proteins, according to their charge and molecular mass. elliptic. Of a two-dimensional structure that is widest near the middle but narrowed towards each rounded end. See also obovate, ovate. elongate. Lengthened or drawn out, e.g. as for the megasporophyll apical spines of Cycas elongata. embryo. In seeds, diploid tissue arising from the zygote, until the time of germination. embryology. Study of the morphology and development of embryos, pollen, megagametophytes and microgametophytes. endemic. Restricted in occurrence to a particular area; e.g. Microcycas calocoma is endemic to Cuba. endocarp. Internal layer of a fruit wall; misapplied to the endotesta in cycads. endosperm. Triploid (or more) nutritive tissue within angiosperm seeds; misapplied to the megagametophyte of cycad seeds. endotesta. Inner layer of a seed coat. ensiform. Sword-shaped, as approximated by the leaflets of some cycads, e.g. Cycas media subspecies ensata.

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entire. With a continuous margin; not toothed or lobed; without incisions of any kind. entomophily. Pollen transfer brought about by insects. Cf. anemophily. eophyll. First leaf produced by a seedling. See also euphyll. epidermis. Outermost primary cellular layer of an organism. Cf. hypodermis. epigeous. Occurring above soil level, as for the stems of arborescent cycads. Cf. hypogeous. epiphytic. Growing on another plant non-parasitically, or on some other elevated support. epithet. Second word of a botanical binomial; the specific or subspecific epithet. etymology. Dealing with the origin of words. Species descriptions commonly give the etymology for the specific epithet. eukaryote. Organism having cells with a true nucleus, as for all plants and animals. euphyll. Conventional foliage leaf, not modified in any way. See also eophyll. ex situ. Of plants or plant collections in cultivation outside their natural habitat. exclamation mark (!). Used in taxonomic literature to signify that a particular herbarium specimen has been examined by the writer. Cf. non visus. exsiccatum (plural exsiccata). Dried specimen material; plantae exsiccatae refers to herbarium specimens. extant. Existing at the present time. Cf. extinct. extinct. No longer existing; e.g. Encephalartos woodii is believed to be extinct in the wild. Amongst the very many extinct cycad genera are: Ceratozamites, Crossozamia, Dioonites, Eostangeria, Palaeocycas, Pseudoctenis, Ticoa and Zamites. Cf. extant. facet. Flattened terminal, median or lateral section of a sporophyll bulla defined by ridges; in cycads the terminal facet is often rhombic in outline. falcate. Curved in a sickle shape, as for the leaflets of Cycas falcata. family. Taxonomic rank below order but above genus. Cycad families comprise the Cycadaceae, Stangeriaceae and Zamiaceae, with some authors separating Boweniaceae as a fourth family. farinaceous. Having the texture of flour or similar starchy material; sometimes referring to a dusty covering. fasciculate. Arranged in a whorl, as for the leaflets of the common form of Ceratozamia hildae. ferrugineous. Rusty brown in appearance, as for the tomentum at the stem apex of Cycas ferruginea. fertilization. Union of male and female gametes resulting in a zygote. fide. According to; by the assurance of. See also sensu. filius, fil.or f. Son of, used in reference to father-and-son authors of taxa. flabellate. Fan-shaped, as in the megasporophyll blade of some Cycas species. flavonoid. Large range of plant secondary metabolites comprising specific phenolic compounds, usually occurring as glycosides, often coloured as in many

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plant pigments. flexuose. In a zig-zag shape, as used in allusion to the much twisted rachis of Macrozamia flexuosa leaves. floccose. Bearing soft, uneven hairs. foliiform. Leaf-like. Fourier transformation. Mathematical process converting state space to frequency space, usually applied to time series data to find periodic signals. frond. Having the form of a fern leaf; commonly misapplied to other pinnately compound leaves, as in palms and cycads. funiculus (plural funiculi). Attachment stalk of an ovule. furfuraceous. Covered with bran-like scales or powder, as for the emergent foliage of Cycas furfuracea and Zamia furfuracea. fusiform. Spindle-shaped; narrowed at each end and swollen centrally. gamete. Mature male (sperm) or female (egg) cell able to take part in reproduction. gametophyte. Haploid structure or tissue; that component of the life cycle which produces gametes. gene. Specific part of the DNA molecule which comprises the basic unit of inheritance, each prescribing a code for the synthesis of a specific protein. genealogy. Line of descent from an ancestor through its derivatives; the ‘pedigree’ of an organism. See also lineage. genetics. Study of genes and genetic processes. genome. Entire genetic complement of an organism or clone, as defined by its haploid chromosome complement. See also genotype. genotype. Genetic constitution of an organism or clone. See also genome. Cf. phenotype. genus (plural genera). Taxonomic rank below family but above species. Extant cycad genera comprise Bowenia, Ceratozamia, Chigua, Cycas, Dioon, Encephalartos, Lepidozamia, Macrozamia, Microcycas, Stangeria and Zamia. Aulacophyllum is now considered congeneric with Zamia while Dyerocycas and Epicycas are congeneric with Cycas. genus novum, gen. nov. Citation at the time a new genus is first described. See also species nova. glabrous. Of a smooth surface, without hair of any kind. glaucous. Of a surface covered by a bluish grey waxy or powdery bloom, as for the foliage of Macrozamia glaucophylla. See also pruinose. GPS. Global Positioning System; worldwide electronic satellite-linked system for establishing latitude, longitude and altitude. gymnosperms. Loosely-related (polyphyletic) group of seed-bearing but non-flowering plants, including cycads, conifers, Ephedra, Ginkgo, Gnetum, Welwitschia together with various extinct taxa. All bear ovules, later seeds, without any enveloping pericarp. habit. Growth form of an organism. habitat. Environment where a plant or animal exists naturally. haploid. Having only one set of chromosomes. Cf. diploid.

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hirsute. Covered with short coarse hairs, as for the leaves of Encephalartos hirsutus. See also lanate, pilose, pubescent, sericeous, tomentose. histology. Study of biological tissues. holotype, holo. Single herbarium specimen or illustration of the type collection used or designated by the author of the name. See also isotype, lectotype, neotype, paratype. homology. Features having a common origin but not necessarily the same function, e.g. cycad leaves, cataphylls and sporophylls. See also apomorphy, autoapomorphy, homoplasy, plesiomorphy, symplesiomorphy, synapomorphy. homomorphic. Of a population, uniform in morphology. See also dimorphic, monomorphic, polymorphic. homoplasy. Mistaken homology; superficial similarity between characters or character states due to convergent or parallel evolution or by reversal; e.g. the occurrence of bipinnately compound leaves in Bowenia and Cycas. hybrid. Natural or artificially produced plant resulting from a cross of genetically dissimilar parents, commonly between two different species. hypocotyl. Embryonic axis at the time of seed germination; that part from which the first leaf emerges. See also radicle. hypodermis. Cellular layer immediately internal to an epidermis. hypogeous. Occurring below soil level; subterranean, as for the stems of Stangeria eriopus, many Zamia species and most Macrozamia Section Parazamia species. Cf. epigeous. hypostomatic. Of leaves and leaflets with stomata on the abaxial surfaces only. Cf. amphistomatic. ICBN. International Code of Botanical Nomenclature, e.g. St Louis Code of 2000. idioblast. Specialized cell with inclusions, in cycads storing toxins possibly as a herbivore deterrent; a cell without known function. imbricate. Overlapping, as for leaflets of many Encephalartos species. See also incubous, succubous. imparipinnate. Of a leaf or leaflet where the rachis or rachilla terminates in a solitary pinna or pinnule. Cf. paripinnate. incertae sedis. Of uncertain placement in a classification system. incubous. Arrangement in which a leaflet partially shields the leaflet above (the next distal leaflet) when viewed from above (adaxially). Cf. succubous. incurved. With apex bent or curving adaxially. Cf. recurved. indeterminate. With growth of the axis continuing indefinitely. Cf. determinate. indumentum. Covering of trichomes or scales. See also tomentum. ineditus, ined. Unpublished, often in reference to an anticipated new species description. inerm. Without spines or prickles; unarmed, as for the leaves of Zamia inermis. Cf. armed. inflexed. Bent longitudinally inwards (adaxially) as in emerging leaves of many

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Zamia species. See also circinate, conduplicate, inflexed, ptyxis, reflexed, vernation. insertion angle(s). See leaflet angle(s) of insertion. integument. Outer covering of an ovule, forming the layers of seed coat at maturity. See also sarcotesta, sclerotesta. interstitial region. Intervening zone between areas of defined structure. involute. With margins rolled inwards (adaxially). Cf. revolute. isoenzymes, isozymes. Differing molecular forms of an enzyme that serve the same function. isotype, iso. Herbarium specimen that is a duplicate of (having the same collection details as) the holotype. This term also has other applications, e.g. in immunology. See also lectotype, neotype, paratype. ITS. Internal transcribed spacer region of a gene. ITS2 is often used for cycad DNA analysis. IUCN. The World Conservation Union. Originally, the International Union for Conservation of Nature and Natural Resources, a United Nations organization. juvenile. Not fully developed; not yet capable of sexual reproduction. Cf. mature. karyology. Dealing with the characteristics of chromosomes, commonly in terms of their number and morphology. lamina (plural laminae). Flattened and expanded portion of a leaf, sporophyll or similar structure; blade. lanate. Woolly with long, intertwined curly hairs, as for the stem apex, emergent leaves and cones of Encephalartos lanatus. See also hirsute, pilose, pubescent, sericeous, tomentose. lanceolate. Lance-shaped, much longer than broad, with a wide base, tapered apex and widest below the centre. See also oblanceolate. lateral. At or on the side of an organ. leaf stalk. Stalk of a leaf; petiole. leaflet. Primary division of a compound leaf; pinna. leaflet angle(s) of insertion. Pinna–pinna (pp) angle: angle on adaxial side of a compound leaf subtended by leaflets on opposite sides of the rachis. Pinna–rachis (pr) angle: distal angle between leaflet and rachis. Shielding (s) angle: angle by which a leaflet is transversely twisted often resulting in overlapping. If leaflets overlap incubously, the s-angle is nominally positive; if leaflets overlap succubously, the s-angle is nominally negative (Grobbelaar, 2002). lectotype, lecto. Herbarium specimen chosen from the original material to replace a missing holotype or isotype. A duplicate of a lectotype is an isolectotype (isolecto.). See also isotype, neotype, paratype. Lepidoptera. Order of insects that includes moths and butterflies. lignified. Of cell walls impregnated with lignin. lignin. Complex insoluble polysaccharide mixture serving to strengthen and protect cell walls. See also xylem.

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lineage. Line of descent of an organism; ancestry. See also genealogy. linear. Long and narrow, the sides parallel or nearly so. lit(t)oral. Of the coast or shore, as for the habitat for Cycas litoralis. lobe. Deeply incised segment of a flattened organ such as a leaf, leaflet or sporophyll. macrozamin. Toxic MAM glycoside found only in cycad tissue; methylazoxymethanol-β-primeveroside. See also cycasin. MAM. Methylazoxymethanol, the toxic principle found as its glycoside in cycasin, macrozamin and structurally related compounds in cycad tissues. manoxylic. Having a small amount of secondary xylem or woody tissue with relatively abundant parenchyma, as in cycad stems. masting. Simultaneous reproductive activity by all or most plants in a particular area, typically seasonal and separated by long periods of low reproductive activity. mature. Capable of sexual reproduction. Cf. juvenile. megagametophyte. Mass of haploid cellular tissue surrounding the embryo in a gymnosperm seed; analogous in function but not in origin to the endosperm of angiosperm seeds. megasporangiate strobilus (less correctly megastrobilus). Female strobilus; female cone; seed cone, ovulate cone. Cf. microsporangiate strobilus. megaspore. Spore that gives rise to a female gametophyte. Cf. microspore. megasporophyll. Sporophyll bearing one or more ovules or later seeds, or potentially so. Cf. microsporophyll. membranous (less commonly membranaceous). Thinly textured, as in a membrane. See also chartaceous, papyraceous. micropyle. Orifice in the integuments and later seedcoats, at the distal end of a cycad ovule, through which the pollen or pollen tube enters. Cf. chalaza. microsporangiate strobilus (less correctly microstrobilus). Male strobilus; male cone; pollen cone. However, in Ceratozamia microstrobila the allusion is to the small size of cones. Cf. megasporangiate strobilus. microsporangium (plural microsporangia). Structure on the abaxial surface of microsporophylls containing microspores; pollen sacs. microspore. Spore that gives rise to a male gametophyte; pollen grain. Cf. megaspore. microsporophyll. Sporophyll bearing microsporangia. Cf. megasporophyll. monomorphic. Having only one form. See also dimorphic, homomorphic, polymorphic. monophyletic. Derived from a single ancestor. See also paraphyletic, polyphyletic. monospecific. Of a genus with only one species, as for Microcycas and Stangeria. monothetic. Of a group sharing all features. See also polythetic.

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monotypic. Of a family with only one genus, or a genus with only one species. Cycadaceae is a monotypic family while Microcycas and Stangeria are monotypic (and monospecific) genera. montane. Of mountains or high places, as for the localities for Macrozamia montana and Zamia montana. morphogeographic. Combining aspects of shape and distribution, i.e. morphology and geography. morphology. Study of the external architecture of any entity. morphometric. Involved with the measurement of morphological characters. mucilage canal. Passage within an organ which allows for the transport of mucilage. mucilage. Gelatinous substance; in cycads comprising complex water-soluble carbohydrates and produced in response to stress, e.g. to wounding. mucronate. Ending abruptly in a sharp point or spur known as a mucro. multipinnate. Of a compound leaf, having more than two orders of division, as in Cycas multipinnata. See also bipinnate. multivariate analysis. Simultaneous statistical analysis of two or more variables. mycorrhiza (plural mycorrhizae). Web of root-like structures arising from a symbiotic association of a fungus and a plant, and facilitating nutrient uptake by the host plant. neotype, neo. New material designated to replace a missing holotype when no original material remains in a herbarium collection. See also isotype, lectotype, paratype. nomen dubium, nom. dub. Name of doubtful taxonomic validity, e.g. the name Encephalartos tridentatus (Willdenow) Lehmann (Pugillus 6, 1834) is a nomen dubium which may refer to several species of Encephalartos or Macrozamia. nomen illegitimum, nom. illeg. Name published in contravention of the rules of nomenclature, e.g. Zamia brongniartii Weddell is a nomen illegitimum, being a superfluous name for Ceratozamia boliviana Brongniart. nomen novum, nom. nov. New name designated when a name cannot be used for nomenclatural purposes and no type or original material exists. nomen nudum, nom. nud. or nomen solum, nom. sol. Avowed new name unaccompanied by a description or diagnosis, e.g. Linden’s name Cycas neocaledonica (L’Illustration Horticiole 28, 1881). nomenclature. Assignment of names to taxa; in botany in accordance with the International Code of Botanical Nomenclature. non visus, n.v. In reference to an item not seen, as in the case of a herbarium specimen that could not be examined. Cf. exclamation mark (!). nucleus. Core part of any eukaryotic cell, a membrane-encased organelle containing the genetic material. oblanceolate. Lance-shaped, much longer than broad, with a wide apex, tapered base and widest above the centre. See also lanceolate. obligate. Restricted to only one taxon or activity, as in an obligate pollinator.

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obovate. Of a two-dimensional structure that is egg-shaped in outline but broadest above the middle. See also elliptic, ovate. obovoid. Of a three-dimensional structure that is obovate in longitudinal section. See also ovoid. obtuse. Blunt or rounded at the apex. offset. Vegetative axis arising from an adventitious bud laterally on a cycad trunk. See also sucker. omnel. Kernel of an omnule; a ‘cleaned cycad seed’ (Grobbelaar, 2002). omnule. Collective term for mature cycad seeds and fully expanded unfertilized ovules that are externally indistinguishable; ‘cycad seed’ (Grobbelaar, 2002). ontogeny. Developmental cycle or ‘life history’ of an individual from its inception until its sexual maturity. opere citado, op. cit. In reference to a publication already cited. This phrase is no longer used in modern scientific writing. order. Taxonomic rank below division or class but above family. orthostichy (plural orthostichies). Row created by intersection of contact parastichies. Sporophylls in Ceratozamia and Zamia cones show welldefined orthostichies in a near-vertical arrangement. OTU. Operational taxonomic unit. Any convenient taxonomic unit used in cladistics and phenetics. outgroup. In cladistics, an organism or group, closely related to but not included within the group under analysis, and used for comparative purposes with respect to character polarity determination. See also sister group. ovate. Of a two-dimensional structure that is egg-shaped in outline but broadest below the middle. See also elliptic, ovate. ovoid. Of a three-dimensional structure that is ovate in longitudinal section. See also obovoid. ovulate cone/strobilus. Female cone; megasporangiate strobilus. ovule. Female reproductive structure; in seed plants comprising a megaspore, or megaspore-derived tissue, one or more integuments and an attachment stalk (funiculus). pachycaulous. Thick-stemmed and columnar but without any substantial secondary wood, as for the stems of arborescent cycads. paleoendemic, palaeoendemic. Referring to a taxon that is a geographical remnant of a taxon formerly of much wider geographical distribution. paleontology, palaeontology. Study of organisms from former geological periods, typically fossilized plants or animals or their parts. palynology. Study of all aspects of pollen from extant and extinct plants. papyraceous. Papery in texture. See also chartaceous, membranous. paraphyletic. Of an artificial group comprising a single ancestor and some, but not all, of its descendants. See also monophyletic, polyphyletic. parastichy (plural parastichies). Spiral arrangement of leaves on an axis (or sporophylls in a cone). Encephalartos, Lepidozamia and Macrozamia cones show well-defined clockwise and anticlockwise parastichies. See also orthostichy. paratype, para. Herbarium specimen cited in a description together with the

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holotype and any isotypes. See also lectotype, neotype. parenchyma. Thin-walled cells in storage tissues such as the cortex zone between the epidermis and vascular tissue. The starch-rich stems of Stangeria eriopus and similar cycads are mainly parenchymatous. paripinnate. Even-pinnate; of a leaf or leaflet where the rachis or rachilla does not terminate in a solitary pinna or pinnule. Cf. imparipinnate. PCR. Polymerase chain reaction, a technique for duplicating a small amount of DNA into a large number of DNA fragments of identical sequence, selectively controlled by a chosen DNA primer. See also RAPD. pectinate. Comb-like; with closely spaced, narrow segments, as in the megasporophyll of Cycas pectinata. pedicel. Supporting stalk of a flower or gymnosperm sporophyll. See also peduncle. peduncle. Supporting stalk of an inflorescence or gymnosperm cone. See also pedicel. peltate. With a stalk positioned centrally on the surface of a lamina or sporophyll, as for most cycad bullae. pendent, pendulous. Hanging downwards, as for the female cones of many Dioon species. petiole. Stalk of a leaf; in a compound leaf, that part of the axis below the lowermost leaflets, pinnacanths or spines. See also rachis. petiolule. Stalk of a leaflet, that part of the axis below the leaflet blade, as seen clearly in Zamia manicata. See also rachilla. phenetic. Condition of an overall similarity of chosen characters between taxa but without regard to whether the characters are derived or due to convergence. phenology. In plants, the study of recurrent phenomena, such as episodes of reproduction, in relation to seasonal patterns. phenogram. Tree diagram showing taxa arranged hierarchically on the basis of phenotypic similarities without any regard for ancestry. See also cladogram, dendrogram, phylogram. phenotype. Sum total of morphological or other characters defining an organism or group. Cf. genotype. pheromone. Volatile chemical substance emitted by an organ and acting as a signal to other organisms, as in cycad cone emissions attracting insect pollinators. photosynthesis. Fundamental process in biosynthesis, by which carbon dioxide and water are converted to simple sugars using sunlight as an energy source. See also chlorophyll. phylogeny. Evolutionary history of an organism or group. phylogram, phylogenetic tree. Cladogram where branch lengths are proportional to the number of changes that occur at each branch. See also dendrogram, phenogram. physiographic. Relating to physical geography. physiology. Study of the functioning of organisms and their parts.

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phytochemistry. Study of plant chemistry, particularly in relation to secondary metabolites. phytogeography. Study of plants and their distribution in relation to geographical factors. pilose. With soft hairs. See also lanate, hirsute, pubescent, sericeous, tomentose. pinna (plural pinnae). Primary division of a compound leaf; leaflet. pinnacanth. Sharply pointed structure intermediate between a leaflet and a spine, usually green and hence photosynthetic, as seen in on the rachises of some species of Dioon, Encephalartos and Macrozamia. See also prickle, tooth. pinnate. Feather-shaped; typically a leaf with leaflets or pinnae on either side of a rachis. See also bipinnate, multipinnate, pinnule. pinnule. Secondary division of a compound leaf. See also pinna. planche. French term used in some of the older botanical literature to denote illustrative plate. See also tabula. platyspermic. Of seeds, flattened so as to be not radially symmetrical, as in Cycas seeds. See also actinomorphic, zygomorphic. Cf. radiospermic. plesiomorphy. Ancestral or underived character or character state. Note that a plesiomorphy at a given hierarchical level may be an apomorphy at a more inclusive level. See also autapomorphy, homology, symplesiomorphy, synapomorphy. plicate. Pleated or folded longitudinally to give a corrugated appearance, as for the leaflet surface of Zamia roezlii. plumose. Feathery in a whorled appearance. pollen. Fine powdery material (microspores) shed from the microsporangia of seed plants; in cycads sometimes referred to as prepollen; microspores containing a male gametophyte (microgametophyte). pollen cone/strobilus. Male cone; microsporangiate strobilus. pollination. Transfer of pollen towards ovules. See also anemophily, entomophily. polymorphic. Persistently variable in form, as for populations of Macrozamia polymorpha and Zamia polymorpha. See also dimorphic, homomorphic, monomorphic. polyphyletic. Of an artifical group comprising members that have originated independently from more than one ancestor. See also monophyletic, paraphyletic. polythetic. Referring to a group sharing many, but not all, features. See also monothetic. population. Group of individuals of a species occupying a particular area. prepollen. Microspore with a proximal aperture but without a distal aperture. Cycad pollen is considered an intermediate form between prepollen and ‘conventional’ pollen. prickle. Small sharp protuberance of epidermal origin, usually green, usually somewhat irregularly distributed, as seen on the petioles of most Ceratozamia and Zamia species. Pinnacanths in Encephalartos have also been called prick-

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les, but they are not epidermal in origin. See also spine, tooth. procumbent, prostrate. Trailing or lying along the ground but not rooting; typically referring to stems. See also decumbent. proximal. Nearest to the point of attachment of a structure; basal. Cf. distal. pruinose. With surface covered by a waxy bloom, as for the foliage of Cycas pruinosa. See also glaucous. ptyxis. Manner of folding of a leaf and leaflets at emergence. See also circinate, conduplicate, inflexed, reflexed, vernation. pubescent. Densely covered with fine short hairs. See also lanate, hirsute, pilose, sericeous, tomentose. pungent. Terminating in a stiff, sharp point. r(h)achilla (plural r(h)achillae). A diminutive of rachis; a secondary axis, in particular, in the grasses or sedges, the axis that bears the florets. Sometimes used in reference to the axis along which pinnules are attached in cycads having compound leaflets, e.g. Bowenia. r(h)achis (plural r(h)achides, r(h)achises). That portion of the axis of a compound leaf where leaflets are attached and excluding the petiole, as alluded to in the flattened rachis of Macrozamia platyrachis and the dark purple rachis of Zamia melanorrhachis. radicle. Embryonic root; often misapplied to the emergent hypocotyl in germinating cycad seeds. radiospermic. Of seeds, radially symmetric as for seeds of cycad genera except Cycas. See also actinomorphic, zygomorphic. Cf. platyspermic. RAPD. Random amplified polymorphic DNA; a technique in DNA analysis based on patterns obtained in electrophoresis after PCR amplification using randomly selected primers. See also RFLP. RC. Rescaled consistency index, the product of the consistency index (CI) and the retention index (RI) for a character in a cladogram. recruitment. Increase in a population due to migration, vegetative proliferation or reproduction from seed. recurved. Bent or curving abaxially. See also reflexed. Cf. incurved. Red List. IUCN-published listing of plant and animal taxa in terms of perceived threatened status. reflexed. Abruptly recurved or bent sharply abaxially, as in the emerging leaves of some Dioon species. See also circinate, conduplicate, inflexed, ptyxis, vernation. relictual. Remaining relatively small portion of a previously larger population or taxon, as for Encephalartos relictus. revolute. With margins rolled downwards (abaxially), as in leaflets of Cycas revoluta and Encephalartos ghellinckii. Cf. involute. RFLP. Restriction fragment length polymorphism; a technique used in DNA analysis based on pattern of bands obtained in electrophoresis of DNA fragments produced after digestion of sample material by restriction endonuclease enzymes. See also RAPD. RI. Retention index, a measure of the amount of similarity in a character that

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can be interpreted as a synapomorphy in a given cladogram. See also CI, RC. ribosome. Cellular organelle in which protein synthesis occurs. sarcotesta (plural sarcotestae). Fleshy outer layer of the integument of a cycad seed, brightly coloured in many cycad genera. See also sclerotesta. satellite. Minute chromosome portion separated from the main body by the centromere or primary constriction. sclerotesta (plural sclerotestae). Hard or stony inner layer of the integument of a cycad seed. See also sarcotesta. scurfy. Covered with small papery scales. section, subsection, series. Taxonomic ranks used within some genera, e.g. the genus Macrozamia comprises two sections, Macrozamia and Parazamia, while the genus Cycas has the four sections Asiorientales, Stangerioides, Indosinensis and Cycas, the last having one or more subsections within which may be one or more series. seed. Fully mature ovule after fertilization, with an embryo, storage tissue and all integuments. See also omnule, corruptule. SEM. Scanning electron microscope (instrument) or micrograph (image produced by the instrument). senescence. Natural ageing processes leading to the death of an organ or organism. sensu. According to; in the sense of. See also fide. sensu lato. In a broad or all-encompassing sense. sensu stricto. In the narrow or restricted sense. sericeous. With fine hairs giving a silky texture. See also lanate, hirsute, pilose, pubescent, tomentose. series. See section. serrate. With a margin of saw-toothed, sharply tipped protrusions pointing forwards apically. See also dentate, tooth, serrulate. serrulate. Minutely serrate, as for leaf margins in Bowenia serrulata. sessile. Without any apparent stalk, as for the cones of many cycads; also used in reference to cycad leaves without petioles, e.g. Encephalartos villosus. sine numero, s.n. Of a herbarium or other specimen accession that is without any collector’s accession number. sister group. In cladistics, the group most closely related to a specific individual or group. See also outgroup. sorus (plural sori). Cluster of fern sporangia; term misapplied to groups of microsporangia sharing a common vascular supply in some cycads. speciation. Evolutionary process in which taxa accumulate sufficient genetic change to be recognized as individual species. species, sp. (plural species, spp.). Basic taxonomic rank; taxonomic rank below genus but above subspecies and varietas. A working definition for cycads is ‘one or more populations where individuals are morphologically similar, interfertile, but sometimes geographically and hence reproductively isolated from other such populations’. [See also the discussions of species

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concept in this volume.] species complex. Variable group of closely related members known or suspected to represent different species but often difficult to circumscribe; usually resolved as a discreet clade in taxonomic analysis; e.g. the Ceratozamia norstogii complex comprises C. norstogii, C. alvarezii and C. mirandae. species nova, sp. nov. Citation at the time a new species is first described, e.g. Zamia macrochiera D.W. Stevenson species nova (Chapter 14 this volume). (Species novum, whilst often seen in the literature, is grammatically incorrect). See also genus novum. spermatophyte. Any seed-bearing plant, including all gymnosperms and angiosperms. spermatozoid (sometimes antherozoid). Motile male gamete of lower plants, cycads, Ginkgo, etc. spine. Hard, sharp and non-photosynthetic protuberance with vascular connections and not of epidermal origin. Spines on many cycad rachises and sporophylls are reduced leaflets. See also pinnacanth, prickle, tooth. spinescent. Terminating in a sharp point. spinulose. With many small spines, as incorrectly alluded to in reference to the leaflet margins of Dioon spinulosum – which are in fact teeth. sporophyll. Modified leaf bearing reproductive structures. See megasporophyll, microsporophyll. SSC. Species Survival Commission, an agency of the IUCN. staminate cone/strobilus. Incorrectly derived term for male cone; pollen cone; microsporangiate strobilus. status novus, stat. nov. New status or rank. For example, Encephalartos manikensis (Gilliland) Gilliland was a status novus for the taxon previously named E.gratus Prain var. manikensis Gilliland. stipule. Appendage at the base of a petiole. In Stangeria, a hood-like stipule subtends each leaf base. stoma (sometimes stomate, plural stomata). Orifice allowing gaseous exchange across a plant epidermis, structurally defined by guard and subsidiary cells. striate. With longitudinal lines, grooves or ridges. striolate. Finely striate. strobilus (plural strobili). Reproductive structure of gymnosperms and some cryptogams such as Selaginella; organized collection of sporophylls on a central axis. See also cone, megasporangiate strobilus, microsporangiate strobilus. subspecies, subsp. Taxonomic rank immediately below species; group of individuals which differ morphologically from another group but insufficiently so as to justify separate specific status, e.g. Cycas media subsp. banksii. Subspecies are reproductively compatible but are reproductively isolated from each other. The usefulness of infraspecific taxonomic categories in cycads is questioned in this volume. See also varietas. succubous. Arrangement in which a leaflet partially shields the leaflet below

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(the next proximal leaflet) when viewed from above (adaxially). Cf. incubous. sucker. Vegetative axis arising from an adventitious bud at the base of a cycad trunk. See also offset. sulcate. Having a longitudinal groove or furrow. Cycad pollen grains are characteristically monosulcate. suture. Line of opening or dehiscence of a closed structure such as a cycad microsporangium. symbiont. Organism living in a symbiotic relationship with another, e.g. the cyanobacteria in cycad coralloid roots. sympatric. Of two or more taxa which exist naturally together in the same geographical area. Cf. allopatric. symplesiomorphy. Ancestral or underived character state shared by several members of a monophyletic group that does not define a monophyletic subset of that more inclusive group and has not experienced reversal. See also apomorphy, autapomorphy, plesiomorphy, synapomorphy. synapomorphy. Shared derived character state that unites two or more members of a monophyletic group. For example, the presence of a glandular collar at the leaflet base is a synapomorphy for a monophyletic group comprising Zamia macrochiera and Z. manicata. A synapomorphy at one level is an autoapomorphy at a more inclusive level. See also apomorphy, plesiomorphy, symplesiomorphy. systematics. Description and classification of life forms and the study of their relationships. tabula. Latin term used in some of the older French botanical literature to denote a black and white plate. See also planche. taxon (plural taxa). Any group of individuals, in any rank, having characteristics in common and of the same evolutionary origin. taxonomy. Circumscription, classification and naming of organisms; in plants, systematic botany. terete. Solid structure which is circular in transverse section; cylindrical or nearly so. thermogenesis. Self-heating through respiratory activity, as in cones, especially male cones, of many cycads. threatened status. Perceived degree of threat, determined by conservation agencies, to the continued natural existence of individual taxa, e.g. in categories such as Critically Endangered, Endangered and Vulnerable. tomentose. Densely woolly in a finely matted fashion. See also lanate, hirsute, pilose, pubescent, sericeous. tomentum. Covering of fine hairs. See also indumentum. tooth. Sharply tipped protrusion along a leaf or leaflet (or analogous structure) margin pointing away at an angle of 90o. See also serrate. topographic. Relating to physical features, usually of the landscape but also used in reference to the surfaces of structures such as pollen grains, leaves etc.

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trichome. Small hair or scale of epidermal origin. trnL-F. Spacer region of the maternally inherited chloroplast genome. truncate. With an abrupt ending, as though cut off terminally. t-test, Student’s t-test. Statistical tool to access if the mean values from two sets of data are the same or not. tuberculate. Covered with small raised protuberances, as for the bulla surface of some cycad megasporophylls. See also verrucose. type, T. Herbarium specimen or other element (e.g. illustration) to which the name of a taxon is permanently attached, whether as a correct name or a synonym. The type is not necessarily the most typical or representative element of a taxon. See also holotype, isotype, lectotype, neotype or paratype. undulate. With wavy margins, usually of leaflets. variegated. Having two or more colours in a blotched or mottled pattern, as for the leaflets of Zamia variegata. varietas, variety, var. Taxonomic rank below species; group of individuals which differ morphologically from another group but insufficiently so to justify separate specific status, e.g. Dioon edule var. angustifolia. Varieties are reproductively compatible, not reproductively isolated from each other and may occur together in mixed stands. The usefulness of infraspecific taxonomic categories in cycads is questioned in this volume. See also subspecies. vascular plant. Plant having phloem or xylem as conducting tissues, i.e. any Pteridophyte (ferns and their allies) or Spermatophyte (gymnosperms and angiosperms). venation. Pattern of veins in a leaf or leaflet. vernation. Manner of folding of a leaf prior to emergence. See also circinate, conduplicate, inflexed, reflexed, ptyxis. verrucose. Warty in appearance, as for the bulla surface of many cycad sporophylls. See also tuberculate. Wilks lambda test. Statistical test comparing the centroids of a distribution of means; a multivariate analysis of variance. See also ANOVA. xylem. Water-conducting tissue in vascular plants, comprising vessels and tracheids, dead at maturity and having a secondary layer of lignin. zygomorphic. Of a bilaterally symmetric structure that can be halved only in one plane to give two halves that are mirror images of each other; of seeds, platyspermic. Cf. actinomorphic. zygote. Cell resulting from the fusion of male and female gametes; the first cell of an embryo.

Acknowledgements We thank Giancarlo Contrafatto, Root Gorelick, Nat Grobbelaar, Lou Randall and contributors to this volume for much helpful assistance in the compilation of this glossary.

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References and Further Reading Grobbelaar, N. (2002) Cycads – with Special Reference to the Southern African Species. Published by the author, Pretoria, South Africa, 331 pp. Jackson, B.D. (1971) A Glossary of Botanical Terms with their Derivation and Accent, 4th edn. Gerald Duckworth & Co., London, 481 pp. Jones, D.J. (2002) Cycads of the World – Ancient Plant in Today’s Landscape, 2nd edn. Reed New Holland, Sydney, Australia, 456 pp. Lawrence, G.H.M. (1989) Taxonomy of Vascular Plants. MacMillan, New York, 823 pp. Norstog, K.J. and Nicholls, T.J. (1997) The Biology of the Cycads. Cornell University Press, Ithaca, New York, 363 pp. Schuh, R.T. (2000) Biological Systematics – Principles and Applications. Cornell University Press, Ithaca, New York, 261 pp. Stearn, W.T. (1992) Botanical Latin, 4th edn. Timber Press, Portland, Oregon, 546 pp.