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Primates in Fragments Ecology and Conservation

Primates in Fragments Ecology and Conservation

Edited by

Laura K. Marsh Los Alamos National Laboratory

Los Alamos, New Mexico

SPRINGER SCIENCE+BUSlNESS MEDIA, LLC

ISBN 978-1-4757-3772-1 ISBN 978-1-4757-3770-7 (eBook) DOI 10.1007/978-1-4757-3770-7

©2003 Springer Science+Business Media New York Originally published by Kluwer AcademiclPlenum Publishers, New York in 2003

Softcover reprint of the hardcover I st edition 2003

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No part of this book may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written

permission from the Publisher, with the exception of any material supplied specifically for the purpose of being entered and executed on a computer system, for exclusive use by the purchaser of the work

This book is dedicated to my mom, Janet G. Marsh, for going with me to Kenya when I was 14 and

for sending me by myself when I was 18 to meet strangers in Panama to do primate research.

Her unending support has been truly appreciated.

PREFACE

This volume was created initially from a symposium of the same name presented at the International Primatological Society's XVIII Congress in Adelaide. South Australia. 6-12 January 2000. Many of the authors who have contributed to this text could not attend the symposium. so this has become another vehicle for the rapidly growing discipline of Fragmentation Science among primatologists. Fragmentation has quickly become a field separate from general ecology. which underscores the severity of the situation since we as a planet are rapidly losing habitat of all types to human disturbance.

Getting ecologists. particularly primatologists. to admit that they study in fragments is not easy. In the field of primatology. one studies many things. but rarely do those things (genetics. behavior. population dynamics) get called out as studies in fragmentation. For some reason "fragmentation primatologists" fear that our work is somehow "not as good" as those who study in continuous habitat. We worry that perhaps our subjects are not demonstrating as robust behaviors as they "should" given fragmented or disturbed habitat conditions. I had a colleague openly state that she did not work in fragmented forests. that she merely studied behavior when it was clear that her study sites. everyone of them. was isolated habitat. Our desire to be just another link in the data chain for wild primates is so strong that it makes us deny what kinds of habitats we are working in. However. the time has come to embrace Fragmentation Science as a field and to pursue it vigorously within primatology. We as scientists have chosen to study in undesirable habitats as our field of concern. This is unfortunate because habitats are degraded. and unfortunate because we aU enjoy pristine habitats. But frankly. it is a good thing we chose the "less desirable" path since the future of primate conservation may depend on it.

One of the primary goals of this book is to be a reference not only in the primate literature. but in Fragmentation Science. The contributors to this volume realize the significance of working within fragments as a whole no matter how disturbed and that these systems respond to and depend upon the matrix they are embedded within. Given that many of the researchers in this volume are also fluent in botany and general ecology. we endeavor to make the text accessible to students and feUow fragment biologists who are interested in this field.

This volume seeks to address several key questions regarding primates in fragments. We attempt to clarify some of the issues. but perhaps in trying we bring to light the complexity of the situation with primates in disturbed habitats. There are few clear

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viii PREFACE

patterns that have emerged demonstrating how primates respond to fragmentation. This volume introduces possible trends for some species, but predictive powers for species other than those discussed in the literature are less reliable. There was no attempt to standardize nomenclature across the volume, but within each chapter nomenclature is consistent.

The book is divided into sections based on broad categories of research on primates in fragments. In the Genetics and Population Dynamics section, the authors cover topics in viability, metapopulation, and species that remain in remnant forests. In the Behavioral Ecology section, authors take a closer look at feeding, ranging, and other behaviors that allow primates to remain in or disperse between fragments. In Conservation and Management, authors bring knowledge of species who remain in fragments together with plans to implement strategies for their long-term viability. And, finally, in the Integration and Future Directions section, authors synthesize the information in this volume and make recommendations for future and continued work in this field. We hope this volume will provoke more research and inquiry to this quickly developing discipline in primatology.

One of the greatest challenges we have facing conservation today is apathy. We encounter this in the consumers of industrialized countries as well as villagers in source nations. Engaging all people, but especially those in tropical nations, to become interested and dedicated as scholars, researchers, teachers, and supporters of conservation efforts within their native countries is vitall. This volume represents work conducted in 10 countries. It is remarkable that out of 51 authors, 37 (75%) are native to the countries they work in. It is my personal hope that this is a growing global trend. If it is, then perhaps primates will have a future in the wild.

Given the recent increase in books published on various aspects of Fragmentation Science, I have provided a list as a supplement to this volume. We no longer have the luxury of studying a single species without having a complete understanding of its habitat and its place within it. These references have become the staples within the discipline.

I would like to express my thanks to all of the authors contributing to this volume. I think we have accomplished a tremendous effort. In particular, without the participants of the International Primatological Society Symposium in Adelaide this volume would never have come into being. I would especially like to thank all of the authors for contributing references and text to the introduction and summaries before each chapter. I hope I represented all of our similar thoughts. Funding for my travel to Australia would not have been possible without the support and encouragement from Fairley Barnes. Without her persistence, I could never have done this project. I thank Andrea Macaluso for asking me to do this book in the first place. Huge thanks must be given to Los Alamos National Laboratory, particularly Tim Haarmann, Ted Doerr, and Diana Webb for their internal support. I cannot thank Teresa Hiteman and Hector Hinojosa enough. They will continue to be richly rewarded for all of their amazing work and dedication to editing and preparing the entire volume (camera ready copy!) before submission to Kluwer. I would also like to thank Winters Red Star, Julie Hill, Rhonda Robinson, and Marjorie Wright for help with maps, figures, and slides for talks having to do with this volume. Many thanks to Bill Laurance and Colin Chapman for great advice and constant inspiration. Special love and thanks to Sal for being a feathery support. Since this is my first edited

There are obvious regions missing from this volume that suffer from severe fragmentation, such as Madagascar and Southeast Asia. It is my hope that in future volumes these countries will be included.

PREFACE

book, I would also like to thank Thelma Rowell, Marina Cords, Tsingalia Mugatsia, and Dennis Rasmussen for their support and encouragement during my formative years as a young primatologist. Look guys, I finally did something! And finally, I thank Jeanne Fair for enduring the painful process of the first book and for all of the helpful comments throughout.

Santa Fe, New Mexico May 2002

LKM

FOREWORD: PRIMATES AS ICONS FOR CONSERVATION

William F. Laurance *

I'm not a primatologist, but in my career I've been dazzled by many primates in the wild, from orangutans and gibbons in Borneo to white-faced sakis and spider monkeys in Central America and the Amazon. I've been equally intrigued by their ecological analogs-the possums, cuscuses, and tree-kangaroos-that I've studied in the rain forests of Australia and New Guinea.

I'm not alone, of course. The apes, monkeys, and lemurs-our closest living relatives in the world-hold a special magic for most people, perhaps rivaled only by whales and dolphins in their ability to capture the popular imagination. In the 1980s, the World Wildlife Fund discovered that the public was far more strongly galvanized by exhortations to "Save the Primates!" than "Save the Rain Forests!" despite the fact that these goals overlap considerably.

Primates are icons for conservation because we identify with them, empathize with them, and feel for their plight. And so many primates are direly threatened. Of 600 primate species in the world, fully a fifth are seriously endangered, and half of those are at imminent risk of extinction.

Primates are imperiled by the same forces that threaten much of the world's biodiversity-habitat destruction and fragmentation, logging and fires, and over hunting. They are icons for conservation because they reside in many of the world's most megadiverse regions. Of the 25 most gravely endangered primate species in the world, 24 are found exclusively in recognized "biodiversity hotspots"-regions such as Madagascar, Indochina, Sundaland (Borneo, Java, Sumatra), Brazil's Atlantic forest, and the Guinean forests of West Africa that sustain a disproportionate fraction of the world's biological diversity and have been ravaged by human activities. To conserve viable populations of wild primates is to protect many of the world's most critically endangered ecosystems.

Primates are icons for conservation because they play vital roles in ecosystem structure and functioning. They disperse fruits and seeds; play integral roles in food webs as consumers of insects, fruits, and foliage and as prey for mammalian carnivores,

Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Republic of Panama, and Biological Dynamics of Forest Fragments Project, National Institute for Amazonian Research (INPA), Manaus, AM 69011-970, Brazil. Correspondence to W. Laurance (email: [email protected]).

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xli W. F. LAURANCE

snakes, and raptors; and participate in a diverse array of coevolved relationships with other species (in the Amazon, for example, certain dung beetles rely exclusively on the droppings of howler monkeys, and, in burying the seed-rich dung to feed their larvae, greatly increase the germination and survival of some plant species). A forest that has lost its primates is an unhealthy, dysfunctional forest.

For these and many other reasons, primates are special, and this book is a timely and impressively comprehensive effort to describe the myriad impacts of habitat fragmentation on their survival, population dynamics, genetic structure, ecological interactions, biogeography, and behavior. It is an unquestionably important contribution, following upon earlier books such as Tropical Forest Remnants (Laurance and Bierregaard, 1997) and Lessons from Amazonia: Ecology and Conservation of a Fragmented Forest (Bierregaard et aI., 2001) that provide more general insights into the ecological consequences of habitat fragmentation.

Primates are icons for conservation because, throughout much of the world, their formerly intact habitats are in desperate retreat. These captivating and intelligent creatures are figureheads for conservation-as they should be-and our success or failure in conserving their rapidly dwindling populations may presage the fate of much of the natural world.

REFERENCES

Bierregaard, Jr., R. 0., Gascon, C., Lovejoy, T. E., and Mesquita, R., 2001, Lessollsfrom Amazollia: The Ecology ofCollservatioll of a Fragmellted Forest, Yale University Press, New Haven.

Laurance, W. F., and Bierregaard, Jr., R. 0.,1997, Tropical Forest RellUlallts: Ecology, Mallagemellt alld COllservatioll of Fragmellted Commullities, University of Chicago Press, Chicago.

CONTENTS

THE NATURE OF FRAGMENTATION ..................................................................... 1

Laura K. Marsh

1. INTRODUCION ............................................................................................... 1 2. FRAGMENTATION SCIENCE ..................................................................... 2

2.1. Edge Effect .................................................................................................. 3 2.2. Matrix .......................................................................................................... 3 2.3. Landscape Patterns ...................................................................................... 4 2.4. Cumulative Pressures ................................................................................... 5

3. PRIMA TES IN FRAGMENTS ........................................................................ 6 4. SUMMARY ....................................................................................................... 7 S. REFERENCES .................................................................................................. 8

SECTION I: GENETICS AND POPULATION DYNAMICS

Laura K. Marsh

1. INTRODUCTION .......................................................................................... 11 2. GENETICS AND VIABILITY ...................................................................... 13 3. CHRONOLOGY OF FRAGMENTATION ................................................. 13 4. METAPOPULATIONTHEORY .................................................................. 13 S. CASE STUDIES .............................................................................................. 14 6. SUMMARY ..................................................................................................... 15 7. REFERENCES ................................................................................................. 15

EFFECTS OF HABITAT FRAGMENTATION ON THE GENETIC VARIABILITY OF SILVERY MARMOSETS, MICO ARGENTATUS ... 17

Evonnildo C. Gon¥alves, Stephen F. Ferrari, Artur Silva, Paulo E.G. Coutinho, Elytania V. Menezes, and Maria Paula C. Schneider

1. INTRODUCTION .......................................................................................... 17 2. STUDY AREA ................................................................................................. 18

idv CONTENTS

3. THE STUDY SPECIES .................................................................................. 19 4. PROCEDURES ............................................................................................... 20

4.1. Fieldwork ................................................................................................... 20 4.2. Genetic Analyses ....................................................................................... 21

5. RESULTS ........................................................................................................ 22 5.1. Population Parameters ................................................................................ 22 5.2. Genetic Variability ..................................................................................... 23

6. DISCUSSION .................................................................................................. 25 7. SUMMARY ..................................................................................................... 26 8. ACKNOWLEDGMENTS .............................................................................. 26 9. REFERENCES ................................................................................................ 27

CHANGES IN DISTRIBUTION OF THE SNUB-NOSED MONKEY IN CHINA. 29

Baoguo Li, Zhiyun Jia, Ruliang Pan, and Baoping Ren

1. INTRODUCTION .......................................................................................... 29 2. GEOCHRONOLOGICAL DISTRIBUTION .............................................. 31

2.1. Fossil Records and Paleoecology ............................................................... 31 3. CHANGES AND HISTORICAL DISTRIBUTION .................................... 32

3.1. Appellations in Historical Text .................................................................. 32 3.2. Distribution Records Based on Provincial and County Anuals ................. 32

4. CURRENT DISTRIBUTION AND HABITATS ......................................... 35 4.1. Sichuan Snub-Nosed Monkey CR. roxellana) ............................................ 36 4.2. Guizhou Snib-Nosed Monkey CR. brelichi) ............................................... 36 4.3. Yunnan Snub·Nosed Monkey CR. bieti) ..................................................... 38

5. REASONS FOR CHANGES IN DISTRIBUTION ...................................... 38 5.1. The Effect of Himalayan Orogenesis ......................................................... 38 5.2. The Effect of Glacial Climate in the Quaternary Period ............................ 39 5.3. The Effect of Historical Changes in Climate ............................................. 39 5.4. The Strong Impact from Human Activity in the Last 400 Years ............... 40

6. PRESENT STA TUS ........................................................................................ 43 6.1. Survival of the Sichuan Snub-Nosed Monkey in the Qinling Mountains .. 43 6.2. The Main Threat to the Guizhou Snub-Nosed Monkey ............................. 46 6.3. Survival of the Yunnan Snub-Nosed Monkey ........................................... 47

7. SUMMARY ..................................................................................................... 49 8. ACKNOWLEDGMENTS ............................................................................... 49 9. REFERENCES ................................................................................................ 49

ANALYSIS OF THE HYPOTHETICAL POPULATION STRUCTURE OF THE SQUIRREL MONKEY (SAIMIRI OERSTEDII) IN PANAMA. ................. 53

Ariel R. Rodrfguez-Vargas

1. INTRODUCTION .......................................................................................... 53 1.1. Taxonomy, Distribution, and Natural History ........................................... 53

CONTENTS xv

2. STUDY AREA ................................................................................................. 55 3. METHODOLOGY ......................................................................................... 55

3.1. Determination of the Metapopulations and Subpopulations ...................... 55 4. RESULTS ........................................................................................................ 57 5. DISCUSSION .................................................................................................. 58 6. CONCLUSION ............................................................................................... 60 7. SUMMARY ..................................................................................................... 60 8. ACKNOWLEDGMENTS .............................................................................. 61 9. REFERENCES ................................................................................................ 61

PRIMA TE SURVIVAL IN COMMUNITY -OWNED FOREST FRAGMENTS: ARE METAPOPULATION MODELS USEFUL AMIDST INTENSIVE USE? ................................................................................................................. 63

Colin A. Chapman, Michael J. Lawes, Lisa Naughton-Treves, and Thomas Gillespie

1. INTRODUCTION .......................................................................................... 63 2. METHODS ...................................................................................................... 65

2.1. Study Site ................................................................................................... 65 2.2. Surveying Primate Fragment Occupancy .................................................. 67 2.3. Environmental Factors and Forest Use by Local Landowners .................. 67 2.4. The Incidence-Function Model .................................................................. 69

3. RESULTS ........................................................................................................ 70 3.1. Forest Use .................................................................................................. 70 3.2. Primate Population Change ....................................................................... 71 3.3. Mainland-Island Incidence-Function Model .............................................. 72

4. DISCUSSION .................................................................................................. 74 5. SUMMARY ..................................................................................................... 76 6. ACKNOWLEDGMENTS .............................................................................. 76 7. REFERENCES ................................................................................................ 76

RELA TIONSHIPS BETWEEN FOREST FRAGMENTS AND HOWLER MONKEYS (ALOUATTA PALLIATA MEXICANA) IN SOUTHERN VERACRUZ, MEXICO ................................................................................. 79

Erika M. Rodriguez-Toledo, Salvador Mandujano, and Francisco Garcia-Orduna

1. INTRODUCTION .......................................................................................... 79 2. PROJECT OBJECTIVES .............................................................................. 80 3. META POPULATION BACKGROUND ...................................................... 81 4. POSSIBLE MET APOPULA TION SCENARIO IN LOS TUXTLAS ....... 82 5. STUDY AREA ................................................................................................. 83 6. METHODOLOGY ......................................................................................... 83

6.1. Landscape Description ............................................................................... 83 6.2. Alouatta Sampling ..................................................................................... 85

7. RESULTS AND DISCUSSION ..................................................................... 86

xvi CONTENTS

7.1. Fragment Characterizations ....................................................................... 86 7.2. Howler Population ..................................................................................... 90

8. COMPARISON WITH OTHER STUDIES ................................................. 92 9. HOWLERS AND FRAGMENT CHARACTERISTICS ............................ 94 10. SUMMARY ..................................................................................................... 95 11. ACKNOWLEDGMENTS .............................................................................. 96 12. REFERENCES ................................................................................................ 96

PRIMATES OF THE BRAZILIAN ATLANTIC FOREST: THE INFLUENCE OF FOREST FRAGMENTATION ON SURVIVAL ......................................... 99

Adriano G. Chiarello

1. INTRODUCTION .......................................................................................... 99 1.1. Atlantic Forest and Fragmentation ............................................................. 99 1.2. Other Main Threats .................................................................................. 100 1.3. Goals of this Chapter ............................................................................... 10 1

2. MATERIAL AND METHODS .................................................................... 101 2.1. Study Sites ............................................................................................... 101 2.2. Data Collection ........................................................................................ 105 2.3. Data Analysis ........................................................................................... 106

3. RESULTS ...................................................................................................... 106 3.1. Populations in Fragments ......................................................................... 106 3.2. Effects of Fragment Size and Hunting ..................................................... 108

4. DISCUSSION ................................................................................................ 109 4.1. Forest Fragmentation and Disturbance .................................................... 109 4.2. Illegal Hunting ......................................................................................... 114 4.3. Population Sizes ....................................................................................... 115

5. CONCLUDING REMARKS ....................................................................... 116 6. SUMMARY ................................................................................................... 117 7. ACKNOWLEDGMENTS ............................................................................ 118 8. REFERENCES .............................................................................................. 118

DYNAMICS OF PRIMATE COMMUNITIES ALONG THE SANTAREMCUIABA. HIGHWAY IN SOUTH-CENTRAL BRAZILIAN AMAZONIA .................................................................................................. 123

Stephen F. Ferrari, Simone Iwanaga, Andre L. Ravetta, Francisco C. Freitas, Belmira A. R. Sousa, Luciane L. Souza, Claudia G. Costa, and Paulo E. G. Coutinho

1. INTRODUCTION ........................................................................................ 123 2. STUDY AREA ............................................................................................... 124 3. THE PRIMATE FAUNA ............................................................................. 127 4. PROCEDURES ............................................................................................. 128

4.1. Selection of Study Sites ........................................................................... 128 4.2. Data Collection ........................................................................................ 129

CONTENTS xvii

5. RESULTS ...................................................................................................... 131 5.1. Communities ............................................................................................ 131 5.2. Abundance ............................................................................................... 134

6. DISCUSSION ................................................................................................ 140 7. SUMMARY ................................................................................................... 142 8. ACKNOWLEDGMENTS ............................................................................. 142 9. REFERENCES .............................................................................................. 142

PRIMATES AND FRAGMENTATION OF THE AMAZON FOREST ............... 145

Kellen A. Gilbert

1. INTRODUCTION ........................................................................................ 145 1.1. Background .............................................................................................. 146 1.2. Study Site ................................................................................................. 146 1.3. History of Primate Studies in the BDFFP Reserves ................................. 148

2. SURVEY METHODS ................................................................................... 148 3. PRIMATES IN FRAGMENTS .................................................................... 149

3.1. 1-ha Reserves ........................................................................................... 149 3.2. 10-ha Reserves ......................................................................................... 150 3.3. 100-ha Reserves ....................................................................................... 152 3.4. Continuous Forest Reserve ...................................................................... 152 3.5. Primates in Fragments ............................................................................. 152 3.6. Fragments and Secondary Growth ........................................................... 152

4. DISCUSSION ................................................................................................ 154 5. SUMMARY ................................................................................................... 155 6. ACKNOWLEDGMENTS ............................................................................ 155 7. REFERENCES .............................................................................................. 156

SECTION II: BEHAVIORAL ECOLOGY

Laura K. Marsh

1. INTRODUCTION ........................................................................................ 159 2. LANDSCAPE AND DEMOGRAPHy ........................................................ 159 3. FEEDING ECOLOGY AND BEHAVIORAL PLASTICITy .................. 160 4. SEED DISPERSAL ....................................................................................... 161 5. COMPILATION ........................................................................................... 161 6. SUMMARY ................................................................................................... 161 7. REFERENCES .............................................................................................. 162

xviii CONTENTS

IMPACTS OF FOREST FRAGMENTATION ON LION-TAILED MACAQUE AND NILGIRI LANGUR IN WESTERN GHATS, SOUTH INDIA ....... 163

Govindasamy Umapathy and Ajith Kumar

1. INTRODUCTION ........................................................................................ 163 1.1. The Western Ghats .................................................................................. 163 1.2. Loss and Fragmentation of Forests .......................................................... 164

2. STUDY SITE ................................................................................................. 164 2.1. Forest Fragments ..................................................................................... 167 2.2. Matrix Around the Fragments .................................................................. 169

3. METHODS .................................................................................................... 169 3.1. Study Animals ......................................................................................... 169 3.2. Estimation of Primate Abundance ........................................................... 171 3.3. Estimation of Habitat Parameters ............................................................ 171 3.4. Demographic Data ................................................................................... 172 3.5. Analysis of Data ...................................................................................... 173

4. RESULTS ...................................................................................................... 173 4.1. Fragment Dynamics ................................................................................. 173 4.2. Landscape Parameters .............................................................................. 173 4.3. Habitat Parameters ................................................................................... 175 4.4. Occurrence of Primates ............................................................................ 176 4.5. Population Density ................................................................................... 178 4.6. Demography ............................................................................................ 179

5. DISCUSSION ................................................................................................ 182 6. SUMMARY ................................................................................................... 185 7. ACKNOWLEDGMENTS ............................................................................ 186 8. REFERENCES .............................................................................................. 186

POPULATION SIZE AND HABITAT USE OF SPIDER MONKEYS AT PUNTA LAGUNA, MEXICO .................................................................................... 191

Gabriel Ramos-Fernandez and Barbara Ayala-Orozco

1. INTRODUCTION ........................................................................................ 191 2. STUDY AREA ............................................................................................... 192 3. POPULATION DENSITY ........................................................................... 195 4. VEGETATION ............................................................................................. 195 5. DEMOGRAPHY AND SOCIAL ORGANIZATION ................................ 196 6. HOME RANGES .......................................................................................... 198 7. DIET ............................................................................................................... 199 8. DISCUSSION ................................................................................................ 204 9. SUMMARY ................................................................................................... 207 10. ACKNOWLEDGMENTS ............................................................................ 208 11. REFERENCES .............................................................................................. 208

CONTENTS

CHANGES IN FOREST COMPOSITION AND POTENTIAL FEEDING TREE AVAILABILITY ON A SMALL LAND-BRIDGE ISLAND IN LAGO

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GURI, VENEZUELA ................................................................................... 211

Marilyn A. Norconk and Brian W. Grafton

1. INTRODUCTION ........................................................................................ 211 2. PRIMATES IN FOREST FRAGMENTS ................................................... 212 3. METHODS .................................................................................................... 213

3.1. Study Site ................................................................................................. 213 3.2. Sampling Methods ................................................................................... 217 3.3. Analysis ................................................................................................... 217

4. RESULTS ...................................................................................................... 218 4.1. Wind Data ................................................................................................ 218 4.2. Structural Changes in the Forest .............................................................. 218 4.3. Plant Species Diversity and Impact on Primate Feeding ......................... 220

5. DISCUSSION ................................................................................................ 222 5.1. Edge Effects on Forest Composition on Isla Redondo ............................ 222

6. SUMMARy ................................................................................................... 224 7. ACKNOWLEDGMENTS ............................................................................ 225 8. REFERENCES .............................................................................................. 225

FORAGING STRATEGY CHANGES IN AN ALOUATTA PALLIATA MEXICANA TROOP RELEASED ON AN ISLAND ...................................................... 229

Ernesto RodrIguez-Luna, Laura E. DomInguez-DomInguez, Jorge E. Morales-Mavil, and Manuel MartInez-Morales

1. INTRODUCTION ........................................................................................ 229 1.1. Daily Acitvity Pattern .............................................................................. 230 l.2. Feeding Preferences ................................................................................. 230 1.3. Home Range ............................................................................................ 231 1.4. Feeding Habits and Foraging Strategies .................................................. 231

2. METHODOLOGY ....................................................................................... 232 2.1. Group Study ............................................................................................. 232 2.2. Study Area ............................................................................................... 232 2.3. Sampling and Recording Methods ........................................................... 233

3. RESULTS ...................................................................................................... 234 3.1. Pattern of Daily Activities ....................................................................... 234 3.2. Feeding Preferences ................................................................................. 237

4. DISCUSSION ................................................................................................ 242 5. SUMMARy ................................................................................................... 244 6. ACKNOWLEDGMENTS ............................................................................ 245 7. REFERENCES .............................................................................................. 245 APPENDIX ........................................................................................................... 249

CONTENTS

DIETARY FLEXIBILITY, BEHAVIORAL PLASTICITY, AND SURVIVAL IN FRAGMENTS: LESSONS FROM TRANSLOCATED HOWLERS ...... 251

Scott C. Silver and Laura K. Marsh

1. INTRODUCTION ........................................................................................ 251 2. FORAGING CHALLENGES IN UNFAMILIAR AREAS ....................... 251 3. SPECIES COMPOSITION OF DIET ........................................................ 252 4. PLANT PART COMPOSITION OF DIET ................................................ 252 5. STUDY SITES AND METHODS ................................................................ 253

5.1. Community Baboon Sanctuary ................................................................ 253 5.2. Cockscomb Basin Wildlife Sanctuary ..................................................... 253 5.3. Vegetation Transects ............................................................................... 254 5.4. Study Troops and Behavioral Data Collection ........................................ 254 5.5. Dietary Comparisons ............................................................................... 254 5.6. Statistical Analyses .................................................................................. 255

6. RESULTS ...................................................................................................... 255 6.1. Vegetation and Food Abundance ............................................................. 255 6.2. Dietary Diversity and Overlap ................................................................. 255 6.3. Consumption of Novel Foods .................................................................. 257 6.4. Differences in Plant Part Composition of Diet ........................................ 257 6.5. Activity Budgets ...................................................................................... 259

7. DISCUSSION ................................................................................................ 259 7.1. Novel Food Consumption ........................................................................ 259 7.2. Learning Processes and Seasonality ........................................................ 260 7.3. Patterns of Food Abundance and Diet Composition ................................ 261 7.4. Differences in Activity ............................................................................. 263

8. SUMMARY ................................................................................................... 264 9. ACKNOWLEDGMENTS ............................................................................ 264 10. REFERENCES .............................................................................................. 264

HOWLER MONKEYS (ALOUAITA PALLIATA MEXICANA) AS SEED DISPERSERS OF STRANGLER FIGS IN DISTURBED AND PRESERVED HABITAT IN SOUTHERN VERACRUZ, MEXICO ...... 267

Juan Carlos Serio-Silva and Victor Rico-Gray

1. INTRODUCTION ........................................................................................ 267 1.1. Figs and Primates ..................................................................................... 267 1.2. Figs and Mexican Howler Monkeys ........................................................ 268

2. MATERIALS AND METHODS ................................................................. 269 2.1. Description of Study Sites ....................................................................... 269 2.2. Study Troops ............................................................................................ 271 2.3. Seed Collection and Selection ................................................................. 271 2.4. Controlled Germination Trials ................................................................. 271 2.5. Planter Box Experiment ........................................................................... 271 2.6. Dispersal Distances .................................................................................. 272

CONTENTS

3. STATISTICAL ANALYSES ....................................................................... 273 4. RESULTS ...................................................................................................... 273

4.1. Controlled Experiment ............................................................................. 273 4.2. Field Experiment (Planter Boxes) ............................................................ 273 4.3. Light, Temperature, and Humidity .......................................................... 273 4.4. Dispersal Distance ................................................................................... 276

5. DISCUSSION ................................................................................................ 276 5.1. Dispersal Distances .................................................................................. 277


HOW DO HOWLER MONKEYS COPE WITH HABITAT FRAGMENTATION? .................................................................................. 283

Julio Cesar Bicca-Marques

1. INTRODUCTION ........................................................................................ 283 2. METHODOLOGICAL APPROACH ......................................................... 284 3. HABITAT FRAGMENTATION AND HOWLER MONKEYS .............. 287

3.1. Use of Space ............................................................................................ 287 3.2. Diet .......................................................................................................... 287 3.3. Activity Budget ........................................................................................ 292

4. DISCUSSION ................................................................................................ 293 5. SUMMARY ................................................................................................... 295 6. ACKNOWLEDGMENTS ............................................................................ 296 7. REFERENCES .............................................................................................. 296 APPENDIX I ........................................................................................................ 299 APPENDIX II ....................................................................................................... 301 APPENDIX III ..................................................................................................... 303

SECTION III: CONSERVATION AND MANAGEMENT

Laura K. Marsh

1. INTRODUCTION ........................................................................................ 305 2. AGRICULTURAL MATRIX ...................................................................... 305 3. MULTIPLE ENCROACHMENTS ............................................................. 306 4. COMPILA TION ........................................................................................... 306 5. SUMMARY ................................................................................................... 306 6. REFERENCES .............................................................................................. 307

CONTENTS

FRAGMENTS, SUGAR, AND CHIMPANZEES IN MASINDI DISTRICT, WESTERN UGANDA .................................................................................. 309

Vernon Reynolds, Janette Wallis, and Richard Kyamanywa

1. INTRODUCTION ........................................................................................ 309 2. FRAGMENTATION OF THE BUDONGO FOREST .............................. 309 3. ADD SUGAR: THE DEVELOPMENT OF AN INDUSTRy ................... 311 4. THE CHIMPANZEES OF KASOKWA FOREST .................................... 312

4.1. The Kasokwa Chimpanzee Project .......................................................... 313 4.2. Data Collection Techniques ..................................................................... 313 4.3. Subjects and Community Composition ................................................... 314 4.4. Preliminary Information of the Kasokwa Chimpanzees' Behavior and

Diet ..............•........................ : ................................................................... 315 4.5. Chimpanzee-Human Interactions ............................................................. 315

5. SOLUTIONS: PLANNING FOR THE FUTURE ...................................... 317 6. SUMMARY ................................................................................................... 318 7. ACKNOWLEDGMENTS ............................................................................ 319 8. REFERENCES .............................................................................................. 319

SHADE COFFEE PLANTATIONS AS WILDLIFE REFUGE FOR MANTLED HOWLER MONKEYS (ALOUA1TA PALLIATA) IN NICARAGUA ..... 321

Colleen McCann, Kimberly Williams-Guillen, Fred Koontz, Alba Alejandra Roque Espinoza, Juan Carlos Martinez Sanchez, and Charles Koontz

1. INTRODUCTION ........................................................................................ 321 1.1. Forest Fragmentation and Ecological Corridors in Central America ....... 321 1.2. The Agroforestry of Coffee ..................................................................... 322 1.3. Managing Habitat on Coffee Plantations .................................................. 324 1.4. The Status of Primates in Nicaragua ........................................................ 324 1.5. Howler Monkey Behavioral Ecology ...................................................... 325 1.6. Conservation Issue .................. ' ................................................................. 327

2. METHODS .................................................................................................... 327 2.1. Study Site ................................................................................................. 327 2.2. Habitat Reconnaissance of Mombacho Coffee Plantations ..................... 327 2.3. Howler Monkey Census ........................................................................... 329 2.4. Local Interviews ...................................................................................... 330

3. ANALYSIS .................................................................................................... 330 4. RESULTS ...................................................................................................... 331

4.1. Habitat Reconnaissance ........................................................................... 331 4.2. Howler Monkey Census ........................................................................... 332 4.3. Howler Monkey Distribution ................................................................... 332 4.4. Howler Monkey Density and Habitat Quality ......................................... 334 4.5. Local Interviews ...................................................................................... 335

5. DISCUSSION ................................................................................................ 335 6. CONCLUSION ............................................................................................. 337

CONTENTS


EFFECTS OF HABITAT FRAGMENTATION ON THE CROSS RIVER GORILLA (GORILLA GORILLA DIEHLI): RECOMMENDATIONS FOR CONSERVATION ........................................................................................ 343

Edem A. Eniang

1. INTRODUCTION ........................................................................................ 343 1.1. The Nigerian Tropical Moist Forest and Primate Conservation .............. 343 1.2. Impacts of Dwindling Economic and Sociopolitical Stability ................. 345 1.3. Cross River Gorillas ................................................................................ 346

2. STUDY AREA ............................................................................................... 348 2.1. Mbe Mountain Range .............................................................................. 348 2.2. Afi River Forest Reserve ......................................................................... 349 2.3. The Cross River National Park ................................................................ 350

3. CURRENT THREATS ................................................................................. 351 3.1. Hunting and Poaching .............................................................................. 351 3.2. Habitat Fragmentation .............................................................................. 354 3.3. Land Rights, Tenure, and Ownership ...................................................... 354 3.4. Logging/Agricultural Projects ................................................................. 355 3.5. Trapping and Collection of Non-Timber Forest Products (NTFP) .......... 355 3.6. Bush Fires ................................................................................................ 356 3.7. Illiteracy, Poverty, and Lack of Basic Resources of Livelihood .............. 356 3.8. Pet Trade .................................................................................................. 356 3.9. Inadequate Scientific Knowledge ............................................................ 356

4. STRA TEGIES FOR CONSERVATION .................................................... 357 4.1. Adapting Traditional Conservation Strategies ......................................... 357 4.2. Update and Enforce Wildlife Laws .......................................................... 357 4.3. Immediate Demarcation of Boundaries ................................................... 357 4.4. Alternatives to Bushmeat ......................................................................... 358 4.5. Creation of Corridors ............................................................................... 358 4.6. Creation of Eco-ductslPortal Gates .......................................................... 358 4.7. Core Conservation Zone .......................................................................... 359 4.8. Closing Some Portion ofthe Ikom-Obudu Highway ............................... 359 4.9. Translocation ........................................................................................... 359 4.10. Exchange Gorillas for Conservation .................................................... 360 4.11. Relocation of Enclave Communities .................................................... 360 4.12. Optimize Conservation Options ........................................................... 360


xxiv CONTENTS

WILD ZOOS: CONSERVATION OF PRIMA TES IN SITU ................................. 365

Laura K. Marsh

1. INTRODUCTION ........................................................................................ 365 2. CURRENT PRIMATE MANAGEMENT STRATEGIES ........................ 366

2.1. Preservation ............................................................................................. 366 2.2. Reintroduction ......................................................................................... 367 2.3. Translocation ........................................................................................... 368

3. VALUE OF SMALL FRAGMENTS (<100 HA) ........................................ 368 4. MANAGEMENT OF PRIMATES IN FRAGMENTS .............................. 370

4.1. General ..................................................................................................... 370 4.2. Wild Zoos ................................................................................................ 371


IV: INTEGRATION AND FUTURE DIRECTIONS

FRAGMENTATION: SPECTER OF THE FUTURE OR THE SPIRIT OF CONSERVATION? ...................................................................................... 381

Laura K. Marsh, Colin A. Chapman, Marilyn A. Norconk, Stephen F. Ferrari, Kellen A. Gilbert, Julio Cesar Bicca-Marques, and Janette Wallis

1. INTRODUCTION ........................................................................................ 381 1.1. Semantics ................................................................................................. 382

2. ISSUES OF MANAGEMENT: AN INTEGRATION ............................... 383 2.1. Primate Responses ................................................................................... 383 2.2. Primate Persistence .................................................................................. 385 2.3. Land Tenure ............................................................................................. 386 2.4. Conservation Measures ............................................................................ 387

3. FUTURE DIRECTIONS .............................................................................. 388 3.1. Ranking Fragments .................................................................................. 388 3.2. Research ................................................................................................... 390

4. POLITICS ..................................................................................................... 394 5. SUMMARY ................................................................................................... 395 6. REFERENCES .............................................................................................. 395

SUGGESTED READING ........................................................................................... 399

INDEX .......................................................................................................................... 401

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