Th e Mind of the Chimpanzee Th e Mind of the Chimpanzee Ecological and Experimental Perspectives Elizabeth V. Lonsdorf, Stephen R. Ross, & Tetsuro Matsuzawa Th e University of Chicago Press Chicago and London Elizabeth V. Lonsdorf is the director of the Lester E. Fisher Center for the Study and Conservation of Apes at the Lincoln Park Zoo in Chicago and a faculty member of the Committee on Evolutionary Biology at the University of Chicago. Stephen R. Ross supervises behavior and cognitive research at the Fisher Center and chairs the Chimpanzee Species Survival Plan of the Associa- tion of Zoos and Aquariums. Tetsuro Matsuzawa directs the Primate Research Institute at Kyoto University in Japan. Th e University of Chicago Press, Chicago 60637 Th e University of Chicago Press, Ltd., London © 2010 by Th e University of Chicago All rights reserved. Published 2010 Printed in the United States of America 18 17 16 15 14 13 12 11 10 1 2 3 4 5 ISBN-13: 978-0-226-49278-0 (cloth) ISBN-13: 978-0-226-49279-7 (paper) ISBN-10: 0-226-49278-8 (cloth) ISBN-10: 0-226-49279-6 (paper) Library of Congress Cataloging-in-Publication Data Th e mind of the chimpanzee : ecological and experimental perspectives / [orga- nized by] Elizabeth V. Lonsdorf, Stephen R. Ross, and Tetsuro Matsuzawa. p. cm. Based on the papers presented at a conference held in Chicago in 2007. Includes bibliographical references and index. ISBN-13: 978-0-226-49278-0 (cloth : alk. paper) ISBN-13: 978-0-226-49279-7 (pbk. : alk. paper) ISBN-10: 0-226-49278-8 (cloth : alk. paper) ISBN-10: 0-226-49279-6 (pbk. : alk. paper) 1. Chimpanzees— Behavior—Congresses. 2. Chimpanzees—Psychology—Congresses. 3. Chimpanzees—Ecology—Congresses. 4. Chimpanzees— Conservation—Congresses. 5. Cognition in animals—Congresses. 6. Social behavior in animals—Congresses. I. Lonsdorf, Elizabeth. II. Ross, Stephen R. III. Matsuzawa, Tetsuro, 1950– IV. Goodall, Jane, 1934– ql737.p96m57 2010 599.885′15—dc22 2009042882 Th e paper used in this publication meets the minimum requirements of the American National Standard for Information Sciences—Permanence of Paper for Printed Library Materials, ANSI Z39.48-1992. Contents Foreword Jane Goodall vii Acknowledgments xi 1 Th e Chimpanzee Mind: Bridging Fieldwork and Laboratory Work Tetsuro Matsuzawa 1 Part I. Cognitive Mechanisms 2 Early Social Cognition in Chimpanzees Masako Myowa-Yamakoshi 23 3 Using an Object Manipulation Task as a Scale for Comparing Cognitive Development in Chimpanzees and Humans Misato Hayashi 32 4 Do the Chimpanzee Eyes Have It? Masaki Tomonaga 42 5 Understanding the Expression and Classifi cation of Chimpanzee Facial Expressions Lisa A. Parr 52 6 Behavioral and Brain Asymmetries in Chimpanzees William D. Hopkins, Jared Taglialatela, David A. Leavens, Jamie L. Russell, and Steven J. Schapiro 60 7 Trapping the Minds of Apes: Causal Knowledge and Inferential Reasoning about Object-Object Interactions Josep Call 75 Part II. Tool Use and Culture 8 A Coming of Age for Cultural Panthropology Andrew Whiten 87 9 Th e Cultural Mind of Chimpanzees: How Social Tolerance Can Shape the Transmission of Culture Victoria Horner 101 10 How Are Army Ants Shedding New Light on Culture in Chimpanzees? Tatyana Humle 116 11 Th e Complexity of Chimpanzee Tool-Use Behaviors Crickette M. Sanz and David B. Morgan 127 12 Tools, Traditions, and Technologies: Interdisciplinary Approaches to Chimpanzee Nut Cracking Dora Biro, Susana Carvalho, and Tetsuro Matsuzawa 141 13 Ubiquity of Culture and Possible Social Inheritance of Sociality among Wild Chimpanzees Michio Nakamura 156 14 New Th eaters of Confl ict in the Animal Culture Wars: Recent Findings from Chimpanzees W. C. McGrew 168 Part III. Social Minds: Ecological Perspectives 15 Chimpanzee Minds in Nature John C. Mitani, Sylvia J. Amsler, and Marissa E. Sobolewski 181 16 Vocal Communication in Chimpanzees Katie Slocombe and Klaus Zuberbühler 192 17 Th e Function and Cognitive Underpinnings of Post-Confl ict Affi liation in Wild Chimpanzees Roman M. Wittig 208 18 Th e Role of Intelligence in Group Hunting: Are Chimpanzees Diff erent from Other Social Predators? Ian C. Gilby and Richard C. Connor 220 Part IV. Social Minds: Empirical Perspectives 19 Chimpanzee Social Cognition Michael Tomasello and Josep Call 235 20 Intentional Communication and Comprehension of the Partner’s Role in Experimental Cooperative Tasks Satoshi Hirata, Naruki Morimura, and Koki Fuwa 251 21 Collaboration and Helping in Chimpanzees Alicia P. Melis, Felix Warneken, and Brian Hare 265 22 Inequity and Prosocial Behavior in Chimpanzees Sarah F. Brosnan 282 23 Th e Need for a Bottom-Up Approach to Chimpanzee Cognition Frans B. M. de Waal 296 Part V. Ethics, Care, and Conservation 24 How Cognitive Studies Help Shape Our Obligation for the Ethical Care of Chimpanzees Stephen R. Ross 309 25 Positive Reinforcement Training, Social Learning, and Chimpanzee Welfare Jaine E. Perlman, Victoria Horner, Mollie A. Bloomsmith, Susan P. Lambeth, and Steven J. Schapiro 320 26 Chimpanzee Orphans: Sanctuaries, Reintroduction, and Cognition Benjamin B. Beck 332 27 Human-Chimpanzee Competition and Confl ict in Africa: A Case Study of Coexistence in Bossou, Republic of Guinea Kimberley J. Hockings 347 28 Chimpanzee Mind, Behavior, and Conservation Elizabeth V. Lonsdorf 361 Aft erword: Meanings of Chimpanzee Mind Richard Wrangham 370 Appendix: Major Chimpanzee Research Sites 375 Index 377 Foreword Jane Goodall Th is volume is based on the papers presented at the third immigrant females. Th ese papers and the resulting discus- conference in the spirit of “Understanding Chimpanzees.” sions provided a great deal of information about the behav- What a lot has happened since Paul Heltne and I began ior of our closest relatives in the wild. An i mportant—and discussing ideas for the fi rst of these conferences! Held in exciting—aspect of the conference was the opportunity 1986, it was to mark the publication of Th e Chimpanzees of for dialogue between Western researchers from the vari- Gombe: Patterns of Behavior, in which I brought together ous African study sites and our colleagues from Japan. some of the results from the fi rst 20 years of observations Only one African scientist was present at that conference: at Gombe National Park, Tanzania, set against an over- Gilbert Isabirye-Basuta, from Uganda. view of published data from other chimpanzee studies in Some of the fi eld biologists present, the “old timers” or the wild and in captivity. We planned to bring together, “silverbacks” as we referred to ourselves, had been consis- for the fi rst time, all (or as many as possible) of the fi eld tently in the fi eld since the sixties. In addition to myself biologists from the diff erent chimpanzee study sites across there were Adriaan Kortlandt, Junichiro Itani, Yukimaru Africa, along with some of the scientists conducting non- Sugiyama, and Toshisada Nishida studying the com- invasive studies on captive groups. Back then it was a novel mon chimpanzee. Bonobo fi eld studies had begun in the idea to have a conference on the behavior of one species. In 1970s and Takayoshi Kano, Suehisa Kuroda, and Nancy fact, at the time we included those working with bonobos, Th ompson-Handler joined us at that fi rst conference. Pan paniscus, which were still known as pygmy chimpan- Th ere were a number of silverbacks in the fi eld of cap- zees; the others were called common chimpanzees. tive studies also: Emil Menzel, Allen and Beatrix (Trixie) Gardner, Duane Rumbaugh and Sue Savage-Rumbaugh. First Conference: Understanding Chimpanzees Th roughout the conference there were many animated conversations about diff erences between chimpanzees and Th at fi rst conference was held in Chicago and organized bonobos—and I remember making a passionate plea for and supported by the Chicago Academy of Sciences. In- dropping the name “pygmy chimpanzee” since, clearly, vited speakers presented papers about research results they were so very diff erent. Th is was substantiated not from the fi eld sites of Gombe and Mahale Mountains in only by the work of Frans de Waal with captive bonobos, Tanzania, Bossou in Guinea, and Kibale in Uganda. Th e but also by the research at fi eld sites in the Democratic Re- topics included population dynamics, feeding ecology, vo- public of Congo (known at that time as Zaire). cal communication, and interactions between resident and A fascinating session that focused on the mind of the viii Goodall chimpanzee opened with a discussion of that great pio- Richard Wrangham, Bill McGrew, and Suehisa Kuroda neer, Wolfgang Köhler. Emil Menzel discussed his work discussed the various new sites across Africa where chim- on chimpanzee intelligence in a variety of captive experi- panzees and bonobos were being observed, and summed mental situations. Language acquisition research, involv- up the status of the research there. Much new research ing the teaching of American Sign Language to chim- was presented, including the work of Colin Chapman and panzees, was discussed by Allen and Trixie Gardner (who John Mitani in Kibale National Park, of Christophe and pioneered this work) and by Roger and Deborah Fouts. Hedwidge Boesch in Taï Forest, and of Caroline Tutin in Duane Rumbaugh and Sue Savage-Rumbaugh reported Gabon. Th ere was a section on the ecology of chimpanzees on their research teaching chimpanzees and bonobos to and bonobos that included speculation on the role of the use lexigrams, which comprised a language they called Yer- environment in determining party size, types of tools and kish. And it was at this conference that the accomplish- purposes for which they were used, diff erent hunting strat- ments of chimpanzee Ai in Japan were presented by Tet- egies and so on that had been observed in diff erent popu- suro Matsuzawa. He called her “his partner in exploring lations. Many of the papers discussed diff erences in social the upper limits of chimpanzee intellect” and her abilities organization and social interactions between chimpanzees at the keyboard amazed most of those present. and bonobos—and for the fi rst time gorilla research was Th ere were two sessions that, for me, were extremely sig- also included. nifi cant. One of these was on the plight of chimpanzees in During this second conference there were more pa- Africa, and the second was on the treatment of chimpan- pers resulting from studies of chimpanzees in zoo popu- zees in a variety of captive situations. Th ese two sessions lations, including comparisons between behavior seen in changed the course of my life, and I shall return to them at wild and in captive situations (stemming in part from the the end of this foreword. Here let me say that Understand- Jane Goodall Institute’s ChimpanZoo program which I ing Chimpanzees was a landmark conference for many of had briefl y discussed in 1986). Th ere had been major de- us; it revealed the rich diversity of chimpanzee behavior velopments in captive research in cognitive and cultural in diff erent areas, and reinforced my long-held conviction behaviors, and Matsuzawa and his students were not only that chimpanzees have their own primitive cultures. By the working on cognitive issues in his lab in Inuyama, but had end of the four days there was one thing we all agreed on: begun observing tool-using behavior in the Bossou popu- the conference was a huge success, greatly increasing our lation in Guinea. Th e explosion of research into many as- understanding of chimpanzees. In fact, so many new stud- pects of behavior since the fi rst conference meant that it ies were underway that we unanimously decided it would would be possible to investigate cultural variation in much be of great value for us to get together again aft er fi ve years greater detail than before. And as we had predicted, the to share and review the new data that would then be avail- many video sessions on diff erent aspects of behavior— able. Th e book Understanding Chimpanzees, an outcome ranging from tool use to social interactions—made it pos- of the conference, was published in 1989. sible to compare behaviors that truly diff ered from one study site to another. Second Conference: Chimpanzee Cultures Increasing collaboration between wild and captive studies was valuable in many ways. For one thing, the ever- Th is second conference, organized by Paul Heltne and increasing understanding of behavior in the wild meant Linda Marquardt, also took place in Chicago in 1991. It fo- that the adaptive value of certain behaviors long observed cused on variation in chimpanzee behavior from one study in captivity became apparent. Behaviors seen in the wild site to another. We had felt that video taken in the fi eld as rare events could, in some cases, be further investigated would provide a signifi cant way of evaluating such diff er- through noninvasive testing in captive situations. And, ences, and all participants had been asked to bring fi lm of course, captive chimpanzees can be encouraged to use with them. Among the most remarkable aspects of this their minds in new situations. Th is ever-increasing un- conference were the proliferation of behavioral and eco- derstanding of the cognitive abilities of chimpanzees and logical studies, the number of new study sites across Africa, bonobos helped to give credence to anecdotal examples of and of course the many new young researchers who were i ntelligent behavior in the wild. Th e book Chimpanzee Cul- working in the fi eld of chimpanzee ecology and behavior. tures, an outcome of the conference, was published in 1994. Foreword ix Th ird Conference: Th e Chimpanzee Mind As I mentioned earlier in this introduction, there had been a session on conservation in the fi rst Understanding Th is most recent conference, held in 2007 in Chicago Chimpanzees conference, organized by Geza Teleki and and organized by Elizabeth Lonsdorf and Steve Ross of Richard Wrangham. Th e picture painted by the various re- the Lincoln Park Zoo, focused on the chimpanzee mind. searchers was grim: from across Africa there were reports Since 1985, when I wrote the chapter on this subject for of human population growth, habitat destruction, forest Th e Chimpanzees of Gombe, a positive explosion of fasci- fragmentation, chimpanzees caught in wire snares, and nating studies on animal minds has taken place. At this the hunting of chimpanzees for the wild animal trade and third conference there were, in addition to scientists who the “bushmeat trade”—the commercial hunting of wild had participated in one or both of the fi rst two (some of animals for food. All this had clearly had a major impact whom during the intervening years had changed from on chimpanzee numbers across their range. No one really “blackback” to “silverback”—that is, from students to knew how many there were, but it was clear that the more professors), there were many new, young researchers rep- than one million who had ranged across 25 African nations resenting the diff erent study sites in Africa and captive at the turn of the century had been reduced to fewer than research around the world. Early observations of tool use 300,000 by 1986. In four countries they were already ex- in the Goualougo Triangle chimpanzees had been greatly tinct. Photographs by Karl Ammann and Michael “Nick” expanded through the use of camera traps by Crickette Nichols showed agonizing images of chimpanzees who Sanz and Dave Morgan. While Ai, whose scientifi c debut had lost a hand or a foot aft er being caught in a wire snare, in the United States had so amazed the participants in chimpanzees and gorillas butchered for food, and infants 1986, continued to perform brilliantly a variety of extraor- whose mothers had been shot being off ered for sale in the dinarily complex tasks, she was all but overshadowed by marketplace or by the roadside. her six-year-old son, Ayumu, with his astounding photo- Another signifi cant session at the 1986 conference had graphic memory. Th e advance of technology was enabling been on the treatment of chimpanzees in medical research new studies of the kind scarcely envisioned when I had laboratories, zoos, and the entertainment industry. Again, begun in 1986. For example, DNA profi ling from fecal images obtained by Nick and others showing the stark samples enabled researchers to determine the paternity of conditions in research labs (followed up by secretly fi lmed particular chimpanzees for the fi rst time, and geographic footage at the SEMA lab in Rockford, Maryland) made a information systems and satellite imagery were helping us deep impression on many of those present. to better understand ranging patterns. Moreover, there It was those two sessions that had such an impact on my was much better collaboration between researchers from own life. In 1986 I was planning to continue collecting data diff erent sites and diff erent universities, and more willing- at Gombe, and I had already begun work on a sequel to ness to share information. Andrew Whiten, who had been Th e Chimpanzees of Gombe—a volume that was to include zealously polling the various study sites as to the presence analysis of my own particular interest, the mother-infant or absence of a whole variety of proposed cultural behav- study (infant development, the changing relationship be- iors, was able during the conference to corner recalcitrant tween mother and her child, the development of relations respondents and get the fi nal data that would enable him between siblings), and changes in behavior over the life to complete his survey of chimpanzee diversity in these re- cycle. Instead I became an activist, determined to do my spects. Th is volume presents all these fi ndings and more. share to raise awareness about the plight of the chimpan- zees and their forests. Conservation, Ethics, and Well-Being Today, as I travel some 300 days a year, I seldom get the chance to spend more than three or four days twice a In this third conference, major concerns for many par- year at Gombe. But the research continues. It is clear that ticipants were conservation issues in the wild, and ethical in many countries there are increasing numbers of young issues regarding captive situations in laboratories, non- people determined to work with chimpanzees, not only accredited zoos, and entertainment as well as in the Afri- as scientists pursuing diff erent aspects of behavior but also can sanctuaries for orphaned great apes. Th e fi nal session as conservationists fi ghting for the protection of the rain of the conference was dedicated to these concerns. forests and the delineation of new national parks and re-
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