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A Chronology of Middle Missouri Plains Village Sites Smithsonian Institution Scholarly Press smithsonian contributions to botany • number 95 Smithsonian Institution Scholarly Press A EcologyChronology of the of MiddlePodocarpaceae Missouri Plainsin TropicalVillage Forests Sites By CraigEdited M. Johnsonby Benjamin L. Turner and withLucas contributions A. Cernusak by Stanley A. Ahler, Herbert Haas, and Georges Bonani SERIES PUBLICATIONS OF THE SMITHSONIAN INSTITUTION Emphasis upon publication as a means of “diffusing knowledge” was expressed by the first Secretary of the Smithsonian. In his formal plan for the Institution, Joseph Henry outlined a program that included the following statement: “It is proposed to publish a series of reports, giving an account of the new discoveries in science, and of the changes made from year to year in all branches of knowledge.” This theme of basic research has been adhered to through the years by thousands of titles issued in series publications under the Smithsonian imprint, com- mencing with Smithsonian Contributions to Knowledge in 1848 and continuing with the following active series: Smithsonian Contributions to Anthropology Smithsonian Contributions to Botany Smithsonian Contributions to History and Technology Smithsonian Contributions to the Marine Sciences Smithsonian Contributions to Museum Conservation Smithsonian Contributions to Paleobiology Smithsonian Contributions to Zoology In these series, the Institution publishes small papers and full-scale monographs that report on the research and collections of its various museums and bureaus. The Smithsonian Contributions Series are distributed via mailing lists to libraries, universities, and similar institu- tions throughout the world. Manuscripts submitted for series publication are received by the Smithsonian Institution Scholarly Press from authors with direct affilia- tion with the various Smithsonian museums or bureaus and are subject to peer review and review for compliance with manuscript preparation guidelines. General requirements for manuscript preparation are on the inside back cover of printed volumes. For detailed submissions require- ments and to review the “Manuscript Preparation and Style Guide for Authors,” visit the Submissions page at www.scholarlypress.si.edu. smithsonian contributions to botany • number 95 Ecology of the Podocarpaceae in Tropical Forests Edited by Benjamin L. Turner and Lucas A. Cernusak WASHINGTON D.C. 2011 ABSTRACT Turner, Benjamin L., and Lucas A. Cernusak, editors. Ecology of the Podocarpaceae in Tropical Forests. Smithsonian Contributions to Botany, number 95, viii + 207 pages, 70 figures, 18 tables, 2011.—The emergence of angiosperms in tropical forests at the expense of the gymnosperms, their ancestral relatives, was one of the most important events in the evolutionary history of terrestrial plants. Gymnosperms were nearly eliminated from the tropics after the evolution of angiosperms in the early Cretaceous, yet conifers of the Podocarpaceae are among the few gymnosperm families that persist in tropical forests worldwide. Podocarps are often considered to be restricted to montane sites in the tropics, a feature of their biogeography that is used by paleo ecologists to reconstruct past forest communities. However, podocarps also occur in the lowland tropics, where they can be the dominant component of forest canopies. Podocarps have proved to be remarkably adaptable in many cases: members of the family have a semi-aquatic lifestyle, exhibit drought tolerance and resprouting, and include the only known parasitic gymnosperm. Other intriguing aspects of podocarp physiology include the mechanism of water transport in the leaves and the conspicuous root nodules, which are not involved in nitrogen fixation but instead house arbuscular mycorrhizal fungi. Perhaps most surprising, paleobotanical evidence indicates that far from being ‘relict’ members of tropical forest communities, podocarps have been dispersing into the tropics since the late Eocene epoch more than 30 million years ago. These and other aspects of the Podocarpaceae explored in this volume have far-reaching implications for understanding the ecology and evolution of tropical rain forests. Cover images: Left, nodules and root hairs on Prumnopitys ferruginea (see chapter 11); center, seed- lings of Podocarpus guatemalensis growing in a shadehouse in Panama (see chapter 3); right, the semi- aquatic podocarp Retrophyllum minus growing in a stream in New Caledonia (see chapter 4). Photo credits, left to right: I. A. Dickie, A. W. Cheesman, and J. W. Dalling. Published by SMITHSONIAN INSTITUTION SCHOLARLY PRESS P.O. Box 37012, MRC 957 Washington, D.C. 20013-7012 www.scholarlypress.si.edu Text and images in this publication may be protected by copyright and other restrictions or owned by individuals and entities other than, and in addition to, the Smithsonian Institution. Fair use of copyrighted material includes the use of protected materials for personal, educational, or noncommercial purposes. Users must cite author and source of content, must not alter or modify content, and must comply with all other terms or restrictions that may be applicable. Users are responsible for securing permission from a rights holder for any other use. Library of Congress Cataloging-in-Publication Data Ecology of the podocarpaceae in tropical forests / Benjamin L. Turner and Lucas Cernusak, editors. p. cm.—(Smithsonian contributions to botany ; no. 95) Includes bibliographical references and index. 1. Podocarpaceae. 2. Tropical plants. I. Turner, Benjamin L. II. Cernusak, Lucas. III. Series: Smithsonian contributions to botany ; no. 95. QK494.5.P73P63 2011 585’.31734—dc22 2010042376 ISSN: 0081-024X (print); 1938-2812 (online) The paper used in this publication meets the minimum requirements of the American National Standard for Perma- nence of Paper for Printed Library Materials Z39.48–1992. Contents PREFACE v ACKNOWLEDGMENTS vii SECTION I – EVOLUTIONARY HISTORY 1 Podocarp Evolution: A Molecular Phylogenetic Perspective 1 Edward Biffin, John G. Conran, and Andrew J. Lowe 2 Dispersal and Paleoecology of Tropical Podocarps 21 Robert J. Morley SECTION II – DISTRIBUTION AND ECOLOGY OF TROPICAL PODOCARPS 3 Ecology and Distribution of Neotropical Podocarpaceae 43 James W. Dalling, Phoebe Barkan, Peter J. Bellingham, John R. Healey, and Edmund V. J. Tanner 4 Ecology and Distribution of the Malesian Podocarps 57 Neal J. Enright and Tanguy Jaffré 5 Podocarps in Africa: Temperate Zone Relicts or Rainforest Survivors? 79 Hylton Adie and Michael J. Lawes 6 The Ecology of Podocarps in Tropical Montane Forests of Borneo: Distribution, Population Dynamics, and Soil Nutrient Acquisition 101 Kanehiro Kitayama, Shin-ichiro Aiba, Masayuki Ushio, Tatsuyuki Seino, and Yasuto Fujiki iv • SMITHSONIAN CONTRIBUTIONS TO botany SECTION III – A TEMPERATE PERSPECTIVE 7 Temperate and Tropical Podocarps: How Ecologically Alike Are They? 119 David A. Coomes and Peter J. Bellingham 8 Ecology of Fire-Tolerant Podocarps in Temperate Australian Forests 141 Philip G. Ladd and Neal J. Enright SECTION IV – ECOPHYSIOLOGY AND ENVIRONMENT 9 Conifer–Angiosperm Interactions: Physiological Ecology and Life History 157 Christopher H. Lusk 10 A Functional Analysis of Podocarp Ecology 165 Timothy J. Brodribb 11 Podocarp Roots, Mycorrhizas, and Nodules 175 Ian A. Dickie and Robert J. Holdaway SECTION V – SYNTHESIS 12 Podocarpaceae in Tropical Forests: A Synthesis 189 Lucas A. Cernusak, Hylton Adie, Peter J. Bellingham, Edward Biffin, Timothy J. Brodribb, David A. Coomes, James W. Dalling, Ian A. Dickie, Neal J. Enright, Kanehiro Kitayama, Philip G. Ladd, Hans Lambers, Michael J. Lawes, Christopher H. Lusk, Robert J. Morley, and Benjamin L. Turner SUBJECT INDEX 197 INDEX OF SCIENTIFIC NAMES 203 Preface he emergence of angiosperms in tropical forests at the expense of the gymnosperms, their ancestral relatives, was one of the most important events in the evolutionary history of terrestrial plants. Although gym- Tnosperms were an important component of the flora on the supercon- tinent of Gondwana, they were virtually eliminated from the tropics following the evolution of angiosperms in the Early Cretaceous. Modern tropical forests are overwhelmingly dominated by angiosperms, yet a few gymnosperms persist. What can they tell us about the ecology of tropical forests? Conifers of the Podocarpaceae are one of the few gymnosperms that inhabit tropical forests worldwide, although they remain the least well known of the three large conifer families. Podocarps occur throughout the Malesian, African, and neotropics and are common in temperate regions of Africa, Australasia, and South America. Tropical podocarps are often considered to be restricted to montane sites, a feature of their biogeography that is used by paleoecologists to reconstruct past forest communities. Yet they also occur in the lowland tropics, usually as rare individuals, but sometimes forming the dominant component of forest canopies. In many cases podocarps have proved to be remarkably adaptable: mem- bers of the family have a semiaquatic lifestyle (Retrophyllum minus), exhibit drought tolerance and resprouting (Podocarpus drouynianus), and include the only known parasitic gymnosperm (Parasitaxus usta). Other intriguing aspects of their physiology include the mechanism of water transport in the leaves and the conspicuous root nodules, which are not involved in nitrogen fixation, but instead house arbuscular mycorrhizal fungi. Perhaps most surprising, paleobo- tanical evidence indicates that
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