COMPARATIVE VERTEBRATE COGNITION: ARE SUPERIOR TO NON-PRIMATES? DEVELOPMENTS IN : PROGRESS AND PROSPECTS

Series Editor: Russell H. Tuttle University ofChicago, Chicago, Illinois

This peer-reviewed book series will meld the facts of organic diversity with the continuity of the evolutionary process. The volumes in this series will exemplify the diversity of theo• retical perspectives and methodological approaches currently employed by primatologists and physical anthropologists. Specific coverage includes: behavior in natural habi• tats and captive settings: primate ecology and conservation; functional morphology and developmental biology ofprimates; primate systematics; genetic and phenotypic differences among living primates; and paleoprimatology.

ALL APES GREAT AND SMALL VOLUME 1: 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 BODIES, HUMAN MINDS: APE, DOLPHIN, AND PARROT LANGUAGE SKILLS William A. Hillix and Duane M. Rumbaugh

COMPARATIVE VERTEBRATE COGNITION: ARE PRIMATES SUPERIOR TO NON-PRIMATES? Lesley J. Rogers and Gisela Kaplan COMPARATIVE VERTEBRATE COGNITION: ARE PRIMATES SUPERIOR TO NON-PRIMATES?

Edited by

Lesley J. Rogers and Gisela Kaplan Centre tor Neuroseienee and Animal Behaviour Sehool o[ Biologieal, Biomedieal and Moleeular Seienees University o[ New England Armidale, NSW 2351, Australia

SPRINGER-SCIENCE+BUSINESS MEDIA, LLC Library ofCongress Cataloging-in-Publication Data

Comparative vertebrate cognition: are primates superior to non-primates? / edited by Lesley ]. Rogers and Gisela Kaplan. p. cm. Includes bibliographical references and index. ISBN 0-306-47727-0 1. Cognition in animals. 2. Primates-Psychology. 3. Vertebrates-Psychology. I. Rogers, Lesley J. II. Kaplan, Gisela T. QL785.C537 2003 596.1513-dc22 2003060171

ISBN 978-1-4613-4717-0 ISBN 978-1-4419-8913-0 (eBook) DOI 10.1007/978-1-4419-8913-0

© 2004 Springer-Science+Business Media New York Originally publishcd by Kluwer Academic/Plenum Publishers, New York in 2004 Softcover reprint of the hardcover 1st edition 2004

10 9 8 7 6 5 4 3 2 1 A C.I.P record for this book is available from the Library of Congress

All rights reserved 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. PREFACE

Primates have featured in human cultural history for a long time. Adventurers, hunters, and travelers described them in their diaries. Even before Darwin, there was some recognition that they were different and fascinating, although not necessarily likeable. Rennie, in his observation oforangutans in 1838 con• demned orangutans as slovenly and useless creatures: "Their deportment is grave and melancholy, their disposition apathetic, their motions slow and heavy, and their habits so sluggish and lazy, that it is only the cravings of appetite, or the approach of imminent danger, that can rouse them from their habitual lethargy, or force them to active exertion." (cit. in Yerkes, R. M., and Yerkes, A. W. (1929) The Great Apes. A Study of Anthropoid Life, Yale University Press, New Haven). Starting with Darwin, interest in primates became scientific and, tragically, led to the first major holocaust of apes, who were killed by their thousands in short spans of time to supply museums with specimens. Gradually zoos also captured them in increasing numbers for "exhibits." Because of their relatedness to humans, primates were then also regarded as good test subjects in biomedical research and the beginning ofthe trade and supply of monkeys commenced, taking them from the wild in uncontrolled and ever growing numbers for use in medical laborarories throughout the best part of the 20th century. Against this background, the efforts that were made in the 1960s and throughout the 1970s to say that primates and, in particular great apes, were "special" was a much needed and radical departure from the poor practice and derogatory attitudes that had gone before. Attitudes began to change along with the sudden rise to fame of the great apes, thanks to the extremely devot• ed research work done by a number of researchers, many of whom are now household names. These changes resulted in questioning the ethics ofhow we treated primates. Export and import of many primates is now banned in most countries; hence, taking them from the wild is often no longer an option, no matter how justifiable the purpose may be. Poaching is usually punishable by law (although

v VI Preface not always enforceable) and use ofprimates for frivolous research purposes has been curbed over the years. Overall, primates are now better protected in the wild and are generally treated better in captivity than they were in the 1950s. Such new appreciation can be attributed in no small measure to primatology's own hard work in disseminating the persistent take-home message that primates are special, deserving of our interest, protection and moral support. As a result of these sustained efforts in the last 50 years or so, the image of great apes gradually changed from that of brutes like King Kong (gorilla), the silly clown (chim• panzee), or the slovenly imbecile (orangutan) to that of creatures worthy of appreciation or, less needed, we believe, ofsome kind of new "noble savage" perhaps even with a mind ofits own. So what are we doing here in Primatology by publishing a book seemingly questioning the very essence on which we have finally achieved some change in moral status for primates? There are two points to be made in reply. The appalling past treatment ofprimates and their depletion in the wild had to be fought by political means and discourses in the political realms ofhuman soci• eties. The claim that primates are special was an important political point of argument; and so was the evolving concept ofgreat apes as flagship species. This book, voicing the opinions ofsome leading primatologists, ethologists, psychobiologists, neuroscientists and anthropologists, is not speaking from the standpoint ofa political engagement with primates but ofa scientific engage• ment with primates in relation to all other species. The extremely lively and seminal primatological debates of the 1970s, especially on the cognitive skills ofapes, have carried us almost through to this day. Thirty years later, it is time to take stock and revise what we know, casting the net wider than the primate order to see what we have achieved theoretically and what is sustainable scien• tifically. Such stock taking exercises help us to adjust our research directions, reflect on our practices, and perhaps also give rise to new and different questions. Often inadvertently, but sometimes deliberately, we make statements imply• ing superiority ofthe behavior or cognitive abilities ofapes compared to mon• keys, or primates compared to nonprimates. Yet recent evidence shows that at least some of the characteristics that we thought made primates unique and superior are also seen in some species ofnon-primates. Thus we are beginning to become aware of the risks of moving in one intellectual milieu and choos• ing to work on a species instead ofchoosing a problem and then testing it on Preface vii a range of species. With this recognition has come another motivation for editing this book. Each contributor has addressed the question "Are the cog• nitive abilities ofprimates simply different from other mammals or are they an evolutionary advance on them?" or, more generally, "Are primates special?" Each contributor has approached the question from a different perspective and considered a range ofdifferent species. We have covered in this book research findings about a wide span ofvertebrate species, all relevant to understanding primates. Of course, we recognize that there are differences in cognition between all species, including the various primates, but we have examined whether there is any substance behind the often stated or hinted assumption that primates are some sort of improved cognitive design and that, amongst primates, the apes are a further improvement that foregrounded the evolution ofthe human brain and mind. We have approached this topic fully aware ofthe difficulties in defining what we mean by higher cognition, or "intelligence," but by our various ways ofdealing with this uncertainty as we compare primate and nonprimate species we believe we will lead to a change in thinking. The aim of the book is to explore afresh the long-standing interest, and emphasis on, the "special" capacities of primates. Some of the recent discov• eries of the higher cognitive abilities of other mammals and also birds challenge the concept that primates are special and even the view that the cog• nitive ability ofapes is more advanced than that ofnon-primate mammals and birds. It is therefore timely to ask whether primates are, in fact, superior to non-primates, and to do so from a broad range ofperspectives. It will become apparent to the reader that researchers are only at the beginning of the search to find out whether primates are special and, ofcourse, by "special" is meant not just different, which applies to all biological categories, but "better" in the ephemeral sense of being more like us and being cognitively superior to all other species. Some of the contributors conclude that all primates (or some primate species) do, indeed, have abilities that separate them from other mammals and that these abilities are clearly special. Others argue that primates as a group are no more special than a range ofother species, or they are special only because they are seen in relation to human primates. Our aim has not been to down• play studies on primates, or to simply criticize them, in comparison to studies on nonprimates, but to present the results of similar studies on primates and nonprimates to see whether any or many of the known cognitive abilities of primates are shared by some of the nonprimate taxa. V1ll Preface

Divided into five sections this book deals with topics about higher cogni• tion and how it is manifested in different species, and also considers aspects of brain structure that might be associated with complex behavior. One important theme of this book is, of course, the evolution of higher cognition and another is the applicability of different testing methods to dif• ferent species. We would fall short if we attempted here to summarize the breadth ofareas covered by the chapters, since each one is a complete essay in itself. We hope they will be read to enlighten scientifically, rather than in any sense to lessen our respect for primates politically. At the very least, or perhaps the most, we hope that this volume will stimulate comparative research on behavior and so ensure that future dividing lines between species are erected only when their foundations are in science and not the result ofeither cultural distortions or political gain. We would like to express our gratitude to Russell Tuttle, editor ofthe series, and Andrea Macaluso, editor with Kluwer, whose invitation to us to proceed with this book gave us the opportunity to explore our ideas further, and to thank Richard Andrew, Dario Maestripieri, and Michael Beran for their valuable comments on an earlier draft of the manuscript. We thank Leanne Stewart for assistance in preparing the index. We are most grateful to all ofthe contributors for adding so many ideas and giving us so many enjoyable pages to read. Lesley J. Rogers and Gisela Kaplan April, 2003 CONTENTS

Contributors xv

PART I: COMPLEX COGNITION 1. Comparing the Complex Cognition of Birds and Primates 3 Nathan]. Emery and Nicola S. Clayton Introduction 3 Why Might Primates be Superior to Non-Primates? 4 Comparing Birds and Primates 5 Primates have a Neocortex Larger than Predicted for their Body Size 5 Primates have an Expanded Prefrontal Cortex 8 Primates Demonstrate Social Learning and Imitation 9 Primates Understand Others' Mental States 14 Primates Display Insight, Innovation, and they Construct and Use Tools 23 Insight and Innovation 23 Manufacture and Use ofTools 25 Primates Utilize Symbolic and Referential Communication 27 Primates Demonstrate Elements ofMental Time Travel 29 The Retrospective Component-Episodic Memory 30 Do Animals have Episodic-like Memory? 31 Episodic-like Memory in Scrub-Jays 32 The Prospective Component-Future Planning 33 Is there any Evidence ofFuture Planning in Animals? 35 Food Caching by Scrub-Jays: A Candidate for Future Planning in Animals? 36 The Perils of Primatocentrism and "Scala Naturae" 36 Uses and Abuses ofthe Ecological/Ethological Approach to Cognition 38

IX x Contents

Species Differences in Ecology and Cognition 39 Ethologicaily Relevant Stimuli are Difficult to Control 40 How Far can the Natural Behavior of an Animal be Translated to the Laboratory? 41 The Great Divide: Awareness of "Self' 41 Is there a Case for Convergent Cognitive Evolution and Divergent Neurological Evolution? 45 Acknowledgments 46 References 46

2. Visual Cognition and Representation in Birds and Primates 57 Giot;gio Vallortigara Introduction 57 Integration and Interpolation ofVisual Information in the Spatial Domain 58 Integration and Interpolation ofVisual Information in the Temporal Domain 69 Representing Objects 72 Objects in Space: Use of Geometric and Nongeometric Information 77 Conclusions 84 Acknowledgments 85 References 85

PART II: SOCIAL LEARNING 3. Socially Mediated Learning among Monkeys and Apes: Some Comparative Perspectives 97 Hilary O. Box and Anne E. Russon Introduction 97 Socially Mediated Learning 98 Imitation 106 Imitation in Monkeys 106 Imitation in Great Apes UO Primate Imitation in Broader Perspective U5 Culture U8 Behavioral Traditions among Monkeys U9 Behavioral Traditions among the Great Apes 121 Contents xi

Facilitating Influences on Behavioral Traditions among Great Apes 123 References 127

4. Sodal Learning, Innovation, and Intelligence in Fish 141 Yfke van Bet;gen) Kevin N. Laland) and William Hoppitt Introduction 141 Traditions and Social Learning in Guppies 144 Innovation in Guppies-Is Necessity the Mother ofInvention? 148 Conformity and Social Release 152 Primate Supremacy Reconsidered 156 Conclusions 163 Acknowledgments 164 References 164

PART III: COMMUNICATION 5. The Primate Isolation Call: A Comparison with Precodal Birds and Non-primate Mammals 171 John D. Newman Introduction 171 The Mammalian Isolation Call 172 The Primate Isolation Call 174 Isolation Call Development 175 A Well-Studied Primate 176 Neurochemical (Pharmacological) Control ofIsolation Call Production 177 Neural Mechanisms ofIsolation Call Production 177 Neural Mechanisms ofIsolation Call Perception 179 Conclusions 181 References 181

6. Meaningful Communication in Primates, Birds, and Other Animals 189 Gisela Kaplan Introduction 189 Communication from the Point ofView ofthe Receiver 191 Xli Contents

Referential Signaling 191 Vocal Signaling in General 191 Motivational versus Referential Signals 192 Attributing Meaning in Alarm and Food Calling 194 Deception in Vocal Signaling 197 Nonvocal Communication 199 Human Language and Animal Studies 201 Co-evolutionary Events 204 Complex Communication, Social Organization, and the Hunt 205 Advantages ofLiving Together 207 Hierarchy, Group Complexity, and Feeding 212 Conclusion 214 References 215

PART IV: THEORY OF MIND 7. Theory of Mind and Insight in Chimpanzees, Elephants, and Other Animals? 227 Moti Nissani Elephant Cognition 228 Do Elephants and Chimpanzees know that People See? 231 Experiment 1: Do Elephants know that People See? 240 Experiment 2: Do Chimpanzees know that People See? 245 Insight in Animals? 248 Retractable Cord-Pulling in Elephants 251 Do Elephants know when to Suck or Blow? 254 Conclusion 257 Acknowledgments 257 References 258

8. The Use of Social Information in Chimpanzees and Dogs 263 Josep Call Reading Attention 265 What can Others See 266 What Organ is Responsible for Vision 269 Following Attention 271 Attention Following into Distant Space 272 Contents xiii

Attention Following in Object Choice 272 Directing Attention 275 Discussion 278 References 283

PART V: BRAIN, EVOLUTION, AND HEMISPHERIC SPECIALIZATION 9. Increasing the Brain's Capacity: Neocortex, New Neurons, and Hemispheric Specialization 289 Lesley Rogers Introduction 289 Brain Size Relative to Body Weight 290 Neocortex/Isocortex 296 Frontal Lobes 299 Relative Differences in the Size ofDifferent Regions ofthe Brain 299 Coordinated Size Change 300 Mosaic Evolution 302 Linking the Size ofBrain Regions to Specific Behavior 304 Correlations between Brain Size and Behavior 305 Foraging for Food 305 Social Intelligence 306 Social Learning, Innovation, and Tool Use 308 Hemispheric Specialization 310 Corpus Callosum 312 Experience and Brain Size 314 Assumptions/New Neurons 316 Conclusion 317 References 318

10. The Evolution of Lateralized Motor Functions 325 Michelle A. Hook Whole-body Turning 327 Lower Vertebrates: Fish, Amphibians, and Reptiles 327 Birds 329 Non-Primate Mammals: Rodents, Dolphins, Cats, and Dogs 329 Non-Human Primates 331 XlV Contents

Summary ofTurning Biases 331 Hand Preferences for Simple Actions 332 Lower Vertebrates 332 Birds 333 Non-Primate Mammals: Rodents 333 Non-Primate Mammals: Cats and Dogs 334 Non-Human Primates 335 Summary ofHand Preferences for Simple Actions 338 Complex Visuospatial Tasks 339 Non-Primate Mammals: Cats 339 Non-Human Primates 340 Summary of Complex Visuospatial Tasks 342 Manipulation and Tool Use 343 Birds 343 Non-Human Primates 344 Summary ofManipulation and Tool Use 345 Foot Preferences in Locomotion 346 Birds 346 Non-Human Primates 347 Summary ofFoot Preferences in Locomotion 348 Production ofEmotional Responses and Vocalizations 348 Lower Vertebrates: Fish, Amphibians, and Reptiles 348 Birds 349 Non-Primate Mammals: Rodents 351 Non-Human Primates 352 Summary 354 Are Primates Special? 355 Acknowledgments 359 References 359

Epilogue 371

About the Editors 375

Index 377 CONTRIBUTORS

Josep Call, Max Planck Institute for Evolutionary Anthropology, , Nicola S. Clayton, Department of Experimental Psychology, University of Cambridge, Cambridge, UK Nathan J. Emery, Sub-department of Animal Behaviour, University of Cambridge, Cambridge, UK Michelle A. Hook, Department of Psychology, Texas A&M University, College Station, TX, USA William Hoppitt, Sub-Department of Animal Behaviour, University of Cambridge, Madingley, UK Gisela Kaplan, Centre for Neuroscience and Animal Behaviour, School of Biological, Biomedical and Molecular Sciences, University ofNew England, Armidale, NSW, Australia Kevin N. Laland, Sub-Department of Animal Behaviour, University of Cambridge, Madingley, UK John D. Newman, Laboratory of Comparative Ethology, NICHD, National Institutes of Health, Department of Health and Human Services, Poolesville, Maryland USA Moti Nissani, Department of Interdisciplinary Studies, Wayne State University, Detroit, MI, USA Hilary O. Box, Department ofPsychology, University ofReading, Reading, UK Lesley Rogers, Centre for Neuroscience and Animal Behaviour School of Biological, Biomedical and Molecular Sciences, University ofNew England, Armidale, NSW, Australia Anne E. Russon, Department of Psychology, Glendon College of York University, Toronto Ontario, Canada Giorgio Vallortigara, Department of Psychology and B.R.A.I.N. Centre for Neuroscience, University ofTrieste, Trieste, Italy Yfke van Bergen, Sub-Department of Animal Behaviour, University of Cambridge, Madingley, UK

xv COMPARATIVE VERTEBRATE COGNITION: ARE PRIMATES SUPERIOR TO NON-PRIMATES?