NEW PERSPECTIVES IN THE STUDY OF MESOAMERICAN PRIMATES. Distribution, Ecology, Behavior, and Conservation

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1 NEW PERSPECTIVES IN THE STUDY OF MESOAMERICAN PRIMATES Distribution, Ecology, Behavior, and Conservation i

2 DEVELOPMENTS IN PRIMATOLOGY: PROGRESS AND PROSPECTS Series Editor: Russell H. Tuttle University of Chicago, Chicago, Illinois This peer-reviewed book series melds the facts of organic diversity with the continuity of the evolutionary process. The volumes in this series exemplify the diversity of theoretical perspectives and methodological approaches currently employed by primatologists and physical anthropologists. Specific coverage includes: primate behavior in natural habitats and captive settings; primate ecology and conservation; functional morphology and developmental biology of primates; primate systematics; genetic and phenotypic differences among living primates; and paleoprimatology. ALL APES GREAT AND SMALL Volume I: African Apes Edited by Birute M.F. Galdikas, Nancy Erickson Briggs, Lori K. Sheeran, Gary L. Shapiro and Jane Goodall THE GUENONS: DIVERSITY AND ADAPTATION IN AFRICAN MONKEYS Edited by mary E. Glenn and Marina Cords ANIMAL MINDS, HUMAN BODIES By W. A. Hillix and Duane Rumbaugh COMPARATIVE VERTEBRATE COGNITION Edited by Lesley J. Rogers and Gisela Kaplan ANTHROPOID ORIGINS: NEW VISIONS Edited by Callum F. Ross and Richard F. Kay MODERN MORPHOMETRICS IN PHYSICAL ANTHROPOLOGY Edited by Dennis E. Slice BEHAVIORAL FLEXIBILITY IN PRIMATES: CAUSES AND CONSEQUENCES By Clara B. Jones NURSERY REARING OF NONHUMAN PRIMATES IN THE 21 ST CENTURY Edited by Gene P. Sackett, Gerald C. Ruppenthal and Kate Elias NEW PERSPECTIVES IN THE STUDY OF MESOAMERICAN PRIMATES: DISTRIBUTION, ECOLOGY, BEHAVIOR, AND CONSERVATION Edited by Alejandro Estrada, Paul A. Garber, Mary S. M. Pavelka, and LeAndra Luecke ii

3 NEW PERSPECTIVES IN THE STUDY OF MESOAMERICAN PRIMATES Distribution, Ecology, Behavior, and Conservation Edited by Alejandro Estrada Universidad Nacional Autónoma de México Mexico City, Mexico Paul A. Garber University of Illinois Urbana, IL, USA Mary S. M. Pavelka University of Calgary Calgary, Alberta, Canada LeAndra Luecke Washington University St. Louis, MO USA iii

4 Alejandro Estrada Paul A. Garber Estación de Biología Los Tuxtlas, Instituto de Biología Department of Anthropology UNAM Apdo. Pos. 176 University of Illinois San Andrés Tuxtla Urbana, IL Veracruz, USA Mexico Mary S. M. Pavelka LeAndra Luecke Department of Anthropology Department of Anthropology University of Calgary Washington University Calgary, AB T2N 1N4 St. Louis, MO Canada USA Library of Congress Control Number: ISBN-10: X e-isbn ISBN-13: Printed on acid-free paper. C 2006 Springer Science+Business Media, Inc. All rights reserved. This work may not be translated or copied in whole or in part without the written permission of the publisher (Springer Science+Business Media, Inc., 233 Spring Street, New York, NY 10013, USA), except for brief excerpts in connection with reviews or scholarly analysis. Use in connection with any form of information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden. The use in this publication of trade names, trademarks, service marks, and similar terms, even if they are not identified as such, is not to be taken as an expression of opinion as to whether or not they are subject to proprietary rights. Printed in the United States of America. (TB/MVY) springeronline.com iv

5 For Alex, Erika, and Ximena. Alejandro Estrada For Sara, Jenni, Seymour, and Sylvia. Paul A. Garber For Drew and Cameron, and my mother, Sari Lynn. LeAndra Luecke v

6 ACKNOWLEDGMENTS We are grateful to each contributing author for their efforts and enthusiasm in translating ideas, data, theories and perspectives into a single volume. We also are grateful to the American Society of Primatologists. The ASP played an important role in supporting the symposium from which the book project originated, at their annual meetings at the University of Wisconsin-Madison in June of We also acknowledge the scholarship of participants at the ASP symposium on Mesoamerican primates, some of whom, although not contributors to the volume, nonetheless provided important intellectual insights. We acknowledge the efforts of several graduate students who participated as coauthors in some of the chapters in this book. The quality of their contributions attests to their high level of scientific investigation and to their enthusiasm in conducting field research in the spirit of great primatologists such as C. R. Carpenter and Ch. Southwick. As always, PAG thanks Sara and Jenni for their love, and for just being Sara and Jenni. AE is grateful to Dr. Karen Strier of the Department of Anthropology, University of Wisconsin-Madison, for hosting the sabbatical year during which this book was developed. AE would also like to acknowledge the economic support of the National Autonomous University of Mexico and of the Scott Neotropic Fund in the development of the ASP symposium and book project. Karla Harmon provided help in printing out the final drafts of each chapter. We are grateful to Melanie Luinstra for assistance in formatting the final drafts of all manuscripts. vii

7 CONTENTS List of Contributors xiii 1. Overview of the Mesoamerican Primate Fauna, Primate Studies, and Conservation Concerns 1 Alejandro Estrada, Paul A. Garber, Mary S. M. Pavelka, and LeAndra Luecke PART 1 TAXONOMY AND BIOGEOGRAPHY 23 Introduction Taxonomy and Distributions of Mesoamerican Primates 29 Anthony B. Rylands, Colin P. Groves, Russell A. Mittermeier, Liliana Cortés-Ortíz, and Justin J. H. Hines 3. The Biogeographic History of Mesoamerican Primates 81 Susan M. Ford PART 2 POPULATION RESPONSES TO DISTURBANCE 115 Introduction Demographic Features of Alouatta pigra Populations in Extensive and Fragmented Forests 121 Sarie Van Belle and Alejandro Estrada 5. Population Structure of Black Howlers (Alouatta pigra) in Southern Belize and Responses to Hurricane Iris 143 Mary S. M. Pavelka and Colin A. Chapman 6. The Effects of Forest Fragment Age, Isolation, Size, Habitat Type, and Water Availability on Monkey Density in a Tropical Dry Forest 165 Holly Noelle DeGama-Blanchet and Linda Marie Fedigan ix

8 x Contents 7. Forest Fragmentation and Its Effects on the Feeding Ecology of Black Howlers (Alouatta pigra) from the Calakmul Area in Mexico 189 Andrómeda Rivera and Sophie Calmé 8. Intestinal Parasitic Infections in Alouatta pigra in Tropical Rainforest in Lacandona, Chiapas, Mexico: Implications for Behavioral Ecology and Conservation 215 Kathryn E. Stoner and Ana González Di Pierro PART 3 BEHAVIOR AND ECOLOGY 241 Introduction Average Body Weight for Mantled Howling Monkeys (Alouatta palliata): An Assessment of Average Values and Variability 247 Kenneth E. Glander 10. An Exploratory Analysis of Developmental Plasticity in Costa Rican Mantled Howler Monkeys (Alouatta palliata palliata) 265 Clara B. Jones 11. Travel Patterns and Spatial Mapping in Nicaraguan Mantled Howler Monkeys (Alouatta palliata) 287 Paul A. Garber and Petra E. Jelinek 12. Use of Landmark Cues to Locate Feeding Sites in Wild Capuchin Monkeys (Cebus capucinus): An Experimental Field Study 311 Paul A. Garber and Ellen Brown 13. Leap, Bridge, or Ride? Ontogenetic Influences on Positional Behavior in Cebus and Alouatta 333 Michelle F. Bezanson 14. Food Choice by Juvenile Capuchin Monkeys (Cebus capucinus) in a Tropical Dry Forest 349 Katherine C. MacKinnon

9 Contents xi 15. Why Be Alpha Male? Dominance and Reproductive Success in Wild White-Faced Capuchins (Cebus capucinus) 367 Katharine M. Jack and Linda M. Fedigan 16. Post-conceptive Mating in White-Faced Capuchins, Cebus capucinus : Hormonal and Sociosexual Patterns of Cycling, Noncycling, and Pregnant Females 387 Sarah D. Carnegie, Linda M. Fedigan, and Toni E. Ziegler PART 4 CONSERVATION AND MANAGEMENT POLICIES 411 Introduction Growth of a Reintroduced Spider Monkey (Ateles geoffroyi) Population on Barro Colorado Island, Panama 417 Katharine Milton and Mariah E. Hopkins 18. Primates in Agroecosystems: Conservation Value of Some Agricultural Practices in Mesoamerican Landscapes 437 Alejandro Estrada, Joel Saenz, Celia Harvey, Eduardo Naranjo, David Muñoz, and Marleny Rosales-Meda 19. Primate Populations in the Protected Forests of Maya Archaeological Sites in Southern Mexico and Guatemala 471 Alejandro Estrada, Sarie Van Belle, LeAndra Luecke, and Marleney Rosales-Meda 20. Mapping Primate Populations in the Yucatan Peninsula, Mexico: A First Assessment 489 Juan Carlos Serio-Silva, Víctor Rico-Gray, and Gabriel Ramos-Fernández 21. A Metapopulation Approach to Conserving the Howler Monkey in a Highly Fragmented Landscape in Los Tuxtlas, Mexico 513 Salvador Mandujano, Luis A. Escobedo-Morales, Rodolfo Palacios-Silva, Victor Arroyo, and Erika M. Rodríguez-Toledo

10 xii Contents 22. Quantifying Fragmentation of Black Howler (Alouatta pigra) Habitat after Hurricane Iris (2001), Southern Belize 539 Shelley M. Alexander, Mary S. M. Pavelka, and Nicola H. Bywater PART 5 SYNOPSIS AND PERSPECTIVES New Perspectives in the Study of Mesoamerican Primates: Concluding Comments and Conservation Priorities 563 Paul A. Garber, Alejandro Estrada, and Mary S. M. Pavelka Species Index 585 Subject Index 593

11 LIST OF CONTRIBUTORS Shelley M. Alexander, Department of Geography, University of Calgary, Alberta, Canada T2N 1N4. Victor Arroyo, División de Posgrado, Instituto de Ecología A. C., km 2.5, Carretera Antigua a Coatepec Nro. 351, Congregación del Haya, Xalapa, Veracruz 91070, México. victorarroyo rodriguez@hotmail.com Michelle Bezanson, Department of Anthropology, Northern Arizona University, Campus Box 15200, Flagstaff, AZ , USA. michelle.bezanson@nau.edu Ellen Brown, Yale University School of Forstry and Environmental Studies, M.E.M., New Haven, CT 06511, USA. ellen.l.brown@yale.edu Nicola H. Bywater, Department of Geography, University of Calgary, Alberta, Canada T2N 1N4. nhbywater@yahoo.com Sophie Calmé, Colegio de la Frontera Sur, Avenida Centenario, km 5.5, Chetumal, Quintana Roo 77900, México. scalme@ecosur-qroo.mx Sarah D. Carnegie, Department of Anthropology, University of Calgary, 2500 University Drive NW, Calgary, Alberta, Canada T2N 1N4. sdcarneg@ucalgary.ca Colin A. Chapman, Anthropology Department and McGill School of Environment, 855 Sherbrooke St. West, McGill University, Montreal, Canada H3A 2T7. colin.chapman@mcgill.ca Liliana Cortés-Ortiz, Centro de Investigaciones Tropicales, Universidad Veracruzana, Xalapa, Veracruz 91070, México. citro@uv.mx Holly Noelle DeGama-Blanchet, Department of Anthropology, University of Calgary, Calgary, AB, Canada T2N 1N4. Holly.DeGammaBlanchet@ natureconservancy.ca xiii

12 xiv List of Contributors Luis A. Escobedo-Morales, División de Posgrado, Instituto de Ecología A. C., km 2.5, Carretera Antigua a Coatepec Nro. 351, Congregación del Haya, Xalapa, Veracruz 91070, México. escobedo@ecologia.edu.mx Alejandro Estrada, Estacion de Biología Los Tuxtlas, Instituto de Biología, Universidad Nacional Autónoma de México, Apartado Postal 176, San Andrés Tuxtla, Veracruz, México. aestrada@primatesmx.com Linda Marie Fedigan, Department of Anthropology, University of Calgary, Calgary, Alberta, Canada T2N 1N4. fedigan@ucalgary.ca Susan M. Ford, Department of Anthropology and Center for Systematic Biology, Southern Illinois University, Carbondale, IL , USA. sford@siu.edu Paul A. Garber, Department of Anthropology, University of Illinois at Urbana-Champaign, 109 Davenport Hall, Urbana, IL 61801, USA. p-garber@uiuc.edu Kenneth E. Glander, Biological Anthropology and Anatomy, Duke University, Durham, NC 27708, USA. glander@duke.edu Ana Marie González Di Pierro, Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Apartado Postal 27-3, Morelia, Michoacán 58089, México. agdipierro@yahoo.com. mx Colin P. Groves, School of Archaeology and Anthropology, Australian National University, Canberra, A.C.T. 0200, Australia. colin. groves@anu.edu.au Celia Harvey, Departmento de Agricultura y Agroforestería, Centro Agronómico Tropical de Investigación y Enseñanza (CATIE), Turrialba 7170, Costa Rica. charvey@catie.ac.cr Justin J. H. Hines, School of Archaeology and Anthropology, Australian National University, Canberra A.C.T. 0200, Australia. justin.hines@ anu.edu.au Mariah E. Hopkins, Department of Environmental Science, Policy & Management, Division Insect Biology, University of California, Berkeley, CA 94720, USA. mhopkins@nature.berkeley.edu

13 List of Contributors xv Katharine M. Jack, Department of Anthropology, Tulane University, 1021 Audubon Street, New Orleans, LA Petra E. Jelinek, Department of Anthropology, University of Illinois at Urbana-Champaign, 109 Davenport Hall, Urbana, IL 61801, USA. Clara B. Jones, Department of Psychology, Fayetteville State University, Fayetteville, NC , USA. s: LeAndra Luecke, Department of Anthropology, Washington University, St. Louis, MO 63130, USA. Katherine C. MacKinnon, Department of Sociology and Criminal Justice and Center For International Studies, Saint Louis University, 210 Fitzgerald Hall, 3500 Lindell Blvd., St. Louis, MO, USA. Salvador Mandujano, Departamento de Biodiversidad y Ecología Animal, Instituto de Ecología A. C., km 2.5, Carretera Antigua a Coatepec Nro. 351, Congregación del Haya, Xalapa, Veracruz 91070, México. mandujan@ecologia.edu.mx Katharine Milton, Department of Environmental Science, Policy & Management, Division Insect Biology, University of California, Berkeley, CA 94720, USA. kmilton@berkeley.edu Russell A. Mittermeier, Conservation International, 1919 M Street NW Suite 600, Washington, DC 20036, USA. r.mittermieir@conservation.org David Muñoz, Colegio de la Frontera Sur, San Cristóbal de las Casas, Chiapas, México. aullador@primatesmx.com Eduardo Naranjo, Colegio de la Frontera Sur, San Cristóbal de las Casas, Chiapas, México. enaranjo@sclc.ecosur.mx Rodolfo Palacios-Silva, División de Posgrado, Instituto de Ecología A. C., km 2.5, Carretera Antigua a Coatepec Nro. 351, Congregación del Haya, Xalapa, Veracruz 91070, México. palacior@ecologia.edu.mx Mary S. M. Pavelka, Department of Anthropology, University of Calgary, 2500 University Drive NW, Calgary, Alberta, Canada T2N 1N4. pavelka@ucalgary.ca

14 xvi List of Contributors Gabriel Ramos-Fernández, Pronatura Península de Yucatán A. C., Calle 32 Nro. 269, Colonia Pinzón II, Mérida, Yucatán 97207, México. Víctor Rico-Gray, Departamento de Ecología Funcional, Instituto de Ecología, A. C., Apartado Postal 63, Xalapa, Veracruz 91070, México. Andrómeda Rivera, Colegio de la Frontera Sur, Avenida Centenario km 5.5, Chetumal, Quintana Roo 77900, México. primatesmx.com Erika M. Rodríguez-Toledo, División de Posgrado, Instituto de Ecología A. C., km 2.5, Carretera Antigua a Coatepec, No. 351, Congregacion del Haya, Xalapa 91070, Veracruz, México. rodrigt@ecologia.edu.mx Marleny Rosales-Meda, Escuela de Biología, Edificio T-10, Ciudad Universitaria, Zona 12, Ciudad de Guatemala, Guatemala. marleny rm@yahoo.com.mx Anthony B. Rylands, Center for Applied Biodiversity Science, Conservation International, 1919 M Street NW, Suite 600, Washington, DC 20036, USA. a.rylands@conservation.org Joel Saenz, Programa Regional de Manejo de Vida Silvestre, Universidad Nacional Autónoma (UNA), Heredia, Costa Rica. jsaenz@una.ac.cr Juan Carlos Serio-Silva, Departamento de Biodiversidad y Ecología Animal, Instituto de Ecología, A. C., Apartado Postal 63, Xalapa, Veracruz 91070, México. serioju@ecologia.edu.mx Kathryn E. Stoner, Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Apartado Postal 27-3, Morelia, Michoacán 58089, México. kstoner@oikos.unam.mx Sarie Van Belle, Department of Zoology, University of Wisconsin-Madison, 250 N Mills Street, Madison, WI 53706, USA. sarievanbelle@ primatesmx.com

THE BLACK HOWLER MONKEY (ALOUATTA PIGRA) AND SPIDER MONKEY (ATELES GEOFFROYI) IN THE MAYAN SITE OF YAXCHILÁN, CHIAPAS, MEXICO: A PRELIMINARY SURVEY

THE BLACK HOWLER MONKEY (ALOUATTA PIGRA) AND SPIDER MONKEY (ATELES GEOFFROYI) IN THE MAYAN SITE OF YAXCHILÁN, CHIAPAS, MEXICO: A PRELIMINARY SURVEY Neotropical Primates 10(2), August 2002 89 Parr, L., Matheson, M., Bernstein, I. and de Waal, F. 1997. Grooming down the hierarchy: Allogrooming in captive brown capuchin monkeys, Cebus apella. Anim. Behav.