Piper: A Model Genus for Studies of Phytochemistry, Ecology, and Evolution

Piper: A Model Genus for Studies of Phytochemistry, Ecology, and Evolution

Edited by

Lee A. Dyer Tulane University, New Orleans, Louisiana

and

Apama D. N. Palmer Mesa State College, Grand Junction, Colorado

Kluwer Academic / Plenum Publishers New York Boston Dordrecht London Moscow

Library of Congress Cataloging-in-Publication Data

Piper: a model genus for studies of phytochemistry, ecology, and evolution / edited by Lee A. Dyer and Apama D.N. Palmer.

p. cm. Includes bibliographical references and index.

1. Piper (Genus) I. Dyer, Lee A. II. Palmer, Apama D. N. QK495.P67P562004 583'.25-dc22

ISBN 978-1-4757-1008-3 ISBN 978-0-387-30599-8 (eBook) DOI 10.1007/978-0-387-30599-8

© 2004 by Kluwer Academic/Plenum Publishers, New York

Softcover reprint ofthe hardcover I st edition 2004

233 Spring Street, New York, New York 10013

http://www.kluweronline.com

10 9 8 7 6 5 4 3 2

A c.I.P. record for this book is available from the Library of Congress

All rights reserved

2004042122

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Contributors

Donald P. Briskin Department of Natural Resources and

Environmental Sciences University of Illinois at Urbana/Champaign Urbana, IL 61801 USA

Ricardo Callejas Departamento de Biologia Universidad de Antioquia Apartado Aereo 1226 Medellin, Colombia

Rodolfo Antonio de Figueiredo Centro Universitano Central Paulista Rua Sebastiao de Abreu Sampaio, 1234 13083-470 Sao Carlos, Brazil

Craig D. Dodson Deparment of Chemistry Mesa State College Grand Junction, CO 81501 USA

LeeA.Dyer Deparment of Ecology and Evolutionary Biology 310 Dinwiddie Hall Tulane University New Orleans, LA 70118 USA

v

Theodore H. Fleming Department of Biology University of Miami Coral Gables, FL 33124 USA

Karin R. Gastreich Organization for Tropical Studies Apdo. 676-2050 San Pedro, Costa Rica

Margaret Gawienowski Department of Natural Resources and

Environmental Sciences University of Illinois at Urbana/Champaign Urbana, IL 61801, USA

Grant L. Gentry Deparment of Ecology and Evolutionary

Biology 310 Dinwiddie Hall Tulane University New Orleans, LA 70118 USA

Nancy Greig Cockrell Butterfly Center Houston Muserum of Natural Science One Hermann Circle Drive Houston, TX 77030-1799 USA

vi

M. Alejandra Jaramillo Departmento de Bioqufmica Medica, CCS-ICB, Universidade Federal do Rio de Janeiro, C. P. 68041,2194-590 Rio de Janeiro, RJ, Brazil

Hideka Kobayashi Department of Natural Resources and

Environmental Sciences University of Illinois at Urbana/Champaign Urbana, IL 61801 USA

Deborah K. Letourneau Department of Environmental Studies Interdisciplinary Sciences Building University of California Santa Cruz, CA 95064 USA

Mary Ann Lila Department of Natural Resources and

Environmental Sciences University of Illinois at Urbana/Champaign Urbana, IL 61801 USA

Robert J. Marquis Department of Biology University of Missouri-St. Louis 8001 Natural Bridge Road St. Louis, Misssouri 63121-4499 USA

Aparna D.N. Palmer Department of Biology Mesa State College

CONTRIBUTORS

Grand Junction, CO 81501 USA

Joe Richards Deparment of Chemistry Mesa State College Grand Junction, CO 81501 USA

Marlies Sazima Departamento de Botanica Universidade Estadual de Campinas 13083-970 Sao Paulo, Brazil

EricJ. Tepe Department of Botany Miami University Oxford, OH USA

Michael A. Vincent Department of Botany Miami University Oxford, OH USA

Linda E. Watson Department of Botany Miami University Oxford, OH USA

Preface

This book offers a glimpse into the world that exists within, and revolves around, a remark­able group of tropical plants. Although it does not synthesize all of the scientific work that has been gathered on Piper, it is a significant advance in our understanding. This advance represents only the tip of the iceberg in terms of the scientific inquiry that will undoubtedly continue to accumulate on this group of organisms. Not unlike other model genera (e.g., Drosophila, Escherichia, Arabidopsis, Neurospora), Piper possesses several attributes that are essential for successful scientific work: it is readily accessible, easily manipulable, and strikingly diverse. For these reasons, it is a model system that will become important to many areas of science beyond chemistry, ecology, and evolutionary biology. Regrettably, as we compiled this volume, we could not cover all aspects of Piper biology that have been studied to date; most notably, this book lacks insight into the developmental genetics, physiology, anatomy, and invasion ecology of Piper. And, although it makes a substantial contribution to our knowledge of the Neotropical pipers, it does not do justice to the Pa­leotropical meJIlbers of the genus. ~evertheless, this book strives to create a resource for investigators searching for a"body of information with which they can plan future studies on and around this extraordinary group of organisms.

We would like to thank many people and organizations for making this book possible. Helpful comments and thorough reviews were provided by a skilled group of anonymous reviewers. We are especially grateful to Christine Squassoni "for reading the entire book several times and helping to edit the final version. Other thoughtful comments and editing remarks were kindly provided by the authors of the chapters in this book and by the following individuals: J. Stireman, R. Matlock, T. Walla, I. Rodden, M. Singer, W. Carson, M. Olson, T. Floyd, R. M. Fincher, A. Smilanich, C. Pearson, M. Tobler, and D. Bowers. LAD thanks N. Greig, R. Marquis, O. Vargas, and D. Letourneau for first introducing him to Piper in Costa Rica. ADNP thanks LAD for infecting her with the same enthusiasm he has for Piper, asking her to collaborate with him, and inviting her to share in the editing of this book. Finally, we would like to thank W. Kelley, who has been a source of inspiration to both of us with his continual enthusiasm for Piper anatomy and evolution.

vii

viii PREFACE

We are grateful for an enonnous amount of help in the field and laboratory for our own research on Piper, especially from G. Vega Chavarria, H. Garcia Lopez, and M. Tobler. In addition to the authors in this book, we also thank the following individuals for their collaborative work in the field and laboratory: A. Barberena, R. Krach, C. Squassoni, O. Vargas, D. Rath, H. Rosenberg, A. Smilanich, R. M. Fincher, A. Hsu, T. Walla, H. Greeney, W. Williams, M. Rathbone, A. Schaefer, J. Sorenson, H. Kloeppl, J. Searcy, Z. Wright, J. Jay, T. Brenes, G. Brehem, N. Bishop, hundreds of Earthwatch volunteers, and many undergraduate students at Tulane University and Mesa State College. Funding for the editors' research on Piper and some of the expenses incurred in compiling this book came from Earthwatch Institute, the National Science Foundation (DEB 9318543 and DEB 0074806), the United States Department of Agriculture (CSREES 35316-12198), the Department of Energy (Southcentral Regional Center of NIGEC), Tulane University, and Mesa State College.

We dedicate this book to the Eois caterpillars that are the true Piper specialists. The book is also dedicated to the Antisana-Sumaco conservation axis in Northeast Ecuador in hopes that the ecosystems there will always offer a safe haven for wild pipers. Viva la abundancia de las bosques del Piper.

LEE. A. DYER

APARNA D. N. PALMER

Contents

CHAPTER 1. Introduction............ ...................................................... 1

N. Greig

CHAPTER 2. Mutualism, Antiherbivore Defense, and Trophic Cascades: Piper Ant-Plants as a Mesocosm for Experimentation.................... 5

D. K. Letourneau

2.1. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 2.2. Study Sites .................................................................... 8 2.3. Plants........................................................................... 8 2.4. Herbivores..................................................................... 9 2.5. Ant Mutualists ................................................................ 10 2.6. Top Predators ................................................................. 11 2.7. Other Endophytic Arthropods, Nematodes, and Annelids ........... 12 2.8. Mutualism Experiments .................................................... 13

2.8.1. Evidence for Nutrient Procurement by Pheidole bicomis Plant-Ants .. ................... ....... ........... .... ... .... ......... 15

2.8.2. Evidence for Defense against Folivores by Pheidole bicomis Plant-Ants ................................................ 16

2.8.3. Evidence for Higher Fitness in Establishing Fragments via Defense against Folivores ........................................ 17

2.8.4. Evidence for Additional Plant Fitness Advantages Afforded by Ph. Bicomis Plant-Ants... .... ... ............ ...... ........... 18

2.9. Tritrophic Interactions and Antiherbivore Defense .................... 18 2.10. Trophic Cascades ............................................................ 22

2.10.1. Experimental Test I: Do Trophic Cascades Operate on the Four Trophic Level System Associated with P. cenocladum Ant-Plants? ..................................... 23

ix

x CONTENTS

2.10.2. Experimental Test II: Can Top-Down and Bottom-Up Forces Affect Animal Diversity in the Endophytic Community of P. Cenocladum Ant-Plants? ................. 24

2.10.3. Experimental Test ill: Can Indirect Effects of Top Predators Extend to Other Plants in the Understory Community of Piper Ant-Plants? .............. 26

2.11. Conclusions................................................................... 27 2.12. Acknowledgments ........................................................... 29

CHAPTER 3. Pollination Ecology and Resource Partitioning in Neotropical Pipers........................................................... 33

Rodolfo Antonio de Figueiredo and MarHes Sazima

3.1. Introduction ................................................................... 33 3.2. Pollination and Resource Partitioning in Piper ......................... 34

3.2.1. Study Site and Species of the Brazilian Study................ 35 3.2.2. Habit and Habitat Utilization .................................... 36 3.2.3. Vegetative Reproduction .......................................... 37 3.2.4. Reproductive Phenology.......................................... 38 3.2.5. Pollination and Visitors ........................................... 41

3.3. Conclusions: Pollination and Resource Partitioning of Pipers in Light of Evolutionary and Conservative Ecology ...................... 49

3.4. Guidelines for Future Research on the Pollination of Pipers ........ 52 3.5. Acknowledgments........................................................... 52

CHAPTER 4. Dispersal Ecology of Neotropical Piper Shrubs and Treelets .... 58

Theodore H. Fleming

4.1. Introduction............................................................. ...... 58 4.2. The Piper Bats ............................................................... 59 4.3. Piper Fruiting Phenology and Dispersal Ecology ..................... 62

4.3.1. Fruiting Phenology ................................................ 62 4.3.2. Patterns of Seed Dispersal ......•............................ ..... 64 4.3.3. Fates of Seeds ...................................................... 65 4.3.4. Postdispersal Distribution Patterns .......................... ~.. 67

4.4. Coevolutionary Aspects of Bat-Piper Interactions .................... 72 4.5. Conclusions ................................................................... 74 4.6. Acknowledgments........................................................... 75

CHAPTER 5. Biogeography of Neotropical Piper..................................... 78

Robert J. Marquis

5.1. Introduction ...................................... ............................. 78 5.2. Methods ....................................................................... 79

CONTENTS Xl

5.3. Results......................................................................... 84 5.3.1. Biogeographic Affinities and Regional Species Pools ...... 84 5.3.2. Correlates of Local Species Richness.......................... 86 5.3.3. Variation in Growth Fonn and Habitat Affinity .............. 88

5.4. Discussion.............................. .... .... .............. ....... .......... 91 5.5. Acknowledgments ........................................................... 94

CHAPTER 6. Faunal Studies in Model Piper spp. Systems, with a Focus on Spider-Induced Indirect Interactions and Novel Insect-Piper Mutualisms ................................................................... 97

Karin R. Gastreich and Grant L. Gentry

6.1. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97 6.2. The Case of Piper obliquum ............................................... 99 6.3. The Case of Piper urostachyum ........................................... 102

6.3.1. Plant Characteristics that Encourage Mutualism ............. 103 6.3.2. Resident Arthropods ...................................... ......... 103

6.3.2a. Herbivores........ .... ... ................................ 103 6.3.2b. Mutualist predators .......................... ........... 105 6.3.2c. Parasites of the mutualism? ........................... 106 6.3.2d. Top predators ............................................ 106

6.3.3. Possible Mutualisms and the Effects of Spiders .............. 107 6.4. Summary and Conclusions................................................. 112 6.5. Acknowledgments............ ................. .... ..... ... ..... .... .... ..... 114

CHAPTER 7. Isolation, Synthesis, and Evolutionary Ecology of Piper Amides.............................................................. 117

Lee Dyer, Joe Richards, and Craig Dodson

7.1. Introduction to Piper Chemistry .......................................... 117 7.2. Isolation and Quantification of Piper Amides .......................... 120 7.3. Synthesis of Piper Amides and Their Analogs ......................... 121 7.4. Ecology of Piper Chemistry ............................................... 128 7.5. Evolution of Piper Chemistry ............................................. 131 7.6. Applied Piper Chemistry ................................................... 132 7.7. Future Research on Piper Chemistry ..................................... 133 7.8. Acknowledgments ........................................................... 134

CHAPTER 8.. Kava (Piper methysticum): Growth in Tissue Culture and In Vitro Production ofKavapyrones.................................... 140

Donald P. Briskin, Hideka Kobayashi, Mary Ann Lila, and Margaret Gawienowski

8.1. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 140 8.2. Origins of Kava Use and Discovery by Western Cultures ........... 141

xu CONTENTS

8.3. Description of Kava (Piper methysticum) and Its Growth for Use in Kava Production ................................................... 141

8.4. Active Phytochemicals Present in Kava Extracts ..................... 142 8.5. Issues Regarding the Potential Hepatotoxicity of

Kava Extracts .......................................................... ..... 143 8.6. Significance of Tissue Culture Growth in Kava Production

and Phytochemical Research ............................................. 144 8.7. Establishment of Kava Cell Cultures and the Determination of

In Vitro Kavapyrone Production ......................................... 146 8.8. Regeneration of Viable Kava Plants from Kava Cell Cultures..... 151 8.9. Summary and Perspective ................................................ 151

CHAPTER 9. Phylogenetic Patterns, Evolutionary Trends, and the Origin of Ant-Plant Associations in Piper Section Macrostachys: Burger's Hypotheses Revisited.... ...................................... 156

Eric. J. Tepe, Michael A. Vincent, and Linda E. Watson

9.1. Introduction ................................................................. 156 9.2. Taxonomic History of Piper sect. Macrostachys

(MIQ.) C.DC. ................................... ........ .................... 158 9.3. Natural History of Piper sect. Macrostachys ...... ..... ... ......... ... 159 9.4. Phylogenetic Relationships in Piper sect. Macrostachys ..... ...... 162 9.5. Burger's Hypotheses Revisited.......................................... 165

9.5.1. Systematic Relationships .................................... ... 165 9.5.2. Evolutionary Trends ............................................. 167

9.6. Ant-Plant Associations in Piper sect. Macrostachys ................ 168 9.6.1. Origins and Evolutionary Trends .............................. 168 9.6.2. Evolution of the Mutualism .................................... 169

9.6.2a. Obligate associations and hollow stems .......... 169 9.6.2b. Petiolar domatia and facultative associations .... 172 9.6.2c. Pearl Bodies ............................................ 173 9.6.2d. Origin of ant-associated plant structures .......... 173

9.7. Conclusions ................................................................. 174 Appendix 9.1 ................................................................ 174

CHAPTER 10. Current Perspectives on the Classification and Phylogenetics of the Genus Piper L. ..................................................... 179

M. Alejandra Jaramillo and Ricardo Callejas

10.1. Introduction ................................................................. 179 10.2. Classification................................. ............................... 180

10.2.1. Getting Cluttered ...................................... ... ...... 180 10.2.2. Getting Articulated ............................................. 181

10.3. Phylogeny .................................................................... 181

CONTENTS Xlll

10.3.1. Phylogenetic Relationships of the Piperales: A Test of Piper's Monophyly ............................................. 181

10.3.2. Infrageneric Relationships of Piper ......................... 183 1O.3.2a. Neotropical Taxa ...................................... 183 1O.3.2b. South Pacific and Asian taxa ........................ 188

10.4. Evolutionary Aspects ...................................................... 189 10.4.1. Flower Morphology............................................ 189 10.4.2. Plant Architecture .............................................. 191

10.5. Acknowledgments ......................................................... 192 Appendix 10.1 .............................................................. 194

CHAPTER 11. Future Research in Piper Biology ..................................... 199

M. Alejandra Jaramillo and Robert Marquis

11.1. Introduction. . . . . . . . . . .. . . . . . .. . .. . .. . .. . . .. . . . . . .. . . .. .. . .. . .. .. . . . .. . . .. .. . 199 11.2. Plant-Animal Interactions ................................................ 199 11.3. Abiotic Factors ............................................................. 201 11.4. Geographical Distribution ................................................ 201 11.5. Summary ..................................................................... 202

Index.......................................................................... 205

Piper: A Model Genus for Studies of Phytochemistry, Ecology, and Evolution