T. Matsuzawa, M. Tomonaga, M. Tanaka (Eds.)Cognitive Development in Chimpanzees

T. Matsuzawa, M. Tomonaga,M. Tanaka (Eds.)

CognitiveDevelopment inChimpanzees

With 237 Figures, Including 26 in Color

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Tetsuro Matsuzawa, Ph.D.Professor, Primate Research Institute, Kyoto University 41 Kanrin, Inuyama, Aichi 484-8506, Japan

Masaki Tomonaga, Ph.D.Associate Professor, Primate Research Institute, Kyoto University 41 Kanrin, Inuyama, Aichi 484-8506, Japan

Masayuki Tanaka, Ph.D.Assistant Professor, Primate Research Institute, Kyoto University 41 Kanrin, Inuyama, Aichi 484-8506, Japan

Spine: Ayumu, Ai’s son, 1 year, 3 months. Photo by Akihiro HirataFront cover:Upper left: Ayumu stacks blocks in front of Tetsuro Matsuzawa. Photo by Etsuko NogamiUpper right: Sharing food. Ayumu watches as his mother, Ai, peels an orange. Photo by Etsuko NogamiCenter: Ai embraces her son, Ayumu. Photo by Tokufumi Inagaki (AERA, Asahi Newspaper Co.)Back cover, from the top:#1. Two infants in the Bossou community. Photo by Rikako Tonooka-Tomonaga#2. A chimpanzee family in Bossou: Jire (mother), Jeje (51/2-year-old male), and Jimato (21/2-month-oldmale who died in the 2003 epidemic) in January 2003. Photo by Tetsuro Matsuzawa#3. A juvenile chimpanzee in Bossou eating the fruit of a huge fig tree. Photo by Tetsuro Matsuzawa#4. Ayumu (left, 4 years, 11 months) and Pal (right, 4 years, 8 months) on top of the climbing frames,April 9, 2005. Photo by Tomomi Ochiai#5. In a computer-controlled finger drawing task, Ai learned to trace symbols used for writing (collab-orative work by Iversen and Matsuzawa). Photo by Tetsuro Matsuzawa#6. Pal examines the remnants of macadamia nuts that her mother, Pan, has cracked with stones. Photoby Etsuko Nogami#7. Ayumu wears a big smile while playing. Photo by Akihiro Hirata (Mainichi Newspaper Co.)

This book was financially supported by the Japan Society for the Promotion of Science (Grant-in-Aid forPublication of Scientific Research result: Grant No. 175332).

Library of Congress Control Number: 2006920239

ISBN-10 4-431-30246-8 Springer-Verlag Tokyo Berlin Heidelberg New YorkISBN-13 978-4-431-30246-9 Springer-Verlag Tokyo Berlin Heidelberg New York

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Foreword by Jane Goodall

This book describes, firstly, the unfolding of an imaginative and brilliantly con-ceived research project; secondly, the development of the fascinating relation-ship between the principal collaborators, Tetsuro Matsuzawa and Ai—a humanbeing and a chimpanzee (subsequently a third major player was recruited:Ayumu, Ai’s son, born in 2000); and thirdly, the journey of Matsuzawa the laboratory scientist into the African wilderness, where he adapted the labresearchers’ methodology to a completely new environment: in the wild it is onlythe methods of data collection that can be controlled; the movements and behav-ior of the subjects cannot.

I first met Matsuzawa in 1986 at a conference “Understanding chimpanzees”in Chicago, where I was most impressed with the paper he presented on theaccomplishments of a chimpanzee named Ai. The following year I met Ai herself.When I first saw her she was in her enclosure with other chimpanzees. We madeeye contact, and I gave the soft panting grunts that chimpanzees utter when theygreet each other. She did not reply.An hour later I was crouched, looking througha small pane of glass, so that I could watch her at her computer. Matsuzawawarned me: “She hates to make a mistake, and especially if a stranger is watch-ing. She will bristle up and charge towards you and hit the glass window. Butdon’t worry — it’s bulletproof glass!”

For some time Ai made one correct response after another. Then came thefirst mistake. Sure enough, Ai glared at me, bristled, and charged towards me.But at the last moment she stopped, her hair sleeked, and, looking at me intently,she pressed her lips to the glass. I kissed in return. She made a total of three mis-takes, and each time the same result—a mutual kiss through glass. Matsuzawatold me that had never happened before, and I don’t think it has happened since!On my next visit I was allowed to spend an hour sitting with Ai in her room, justthe two of us. It was a memorable experience, looking into her wise eyes, groom-ing her a little, playing for a while.

I first saw Ayumu when he was a small infant. When he was two and a halfyears old I was allowed to go into his room but was warned that he was quiterough with strangers. As I am familiar with boisterous chimpanzee youngstersin our African sanctuaries (orphans whose mothers have been shot by hunters),I was prepared to have my hair pulled and my hands and arms bitten throughmy clothing. But it wasn’t like that at all. Ayumu was so gentle, grooming me,

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(Photo: Jane and Ayumu, November 2002)

laughing softly as I tickled him, climbing all over me, and repeatedly kissing me.It reminded me of my first contact with his mother.Afterwards I watched Ayumuworking with his computer. Like Ai, he seemed to have great concentration andloved to press the right panels for a small reward.

This book reveals sometimes surprising aspects of chimpanzee intelligence,discovered I believe because Matsuzawa’s sensitivity for his primate collabora-tor allowed him to ask the right questions in the right way. His intuitive and sen-sitive reading of chimpanzee nature, coupled with the meticulous methodologyand quick intellect of the true scientist, made him the perfect partner for Ai—herself a remarkably intelligent chimpanzee. One of the reasons she is able tomaster very complex tasks is because she has an incredible power of concentra-tion, and because she truly wants to succeed. Indeed, if she gets a bad score afterone 20-minute test session, she may actually ask for another session so that shecan try to do better.

One incident illustrates how these qualities enhance her success. Ai wasworking at a difficult task that involved memorizing a sequence of numbers onone computer screen so that she could replicate it on a second screen. A filmcrew was present, as well as myself. Ai, who is used to peace and quiet whilst sheworks, began to lose her concentration as first one and then another member ofthe team moved to get a better view, often bumping into the cage. She began tomake mistakes—and after a few minutes her hair began to bristle. I was sure shewas about to vent her frustration in a stamping display. Instead, she suddenlystopped working altogether, her hair sleeked, she sat very still and seemed to bestaring at a point midway between the two screens. For at least 30 seconds, andmaybe longer, she remained motionless. Then she started to work again. For theremainder of the session she paid no further attention to her noisy humanobservers. It was exactly as though she had decided that she must either give upor else pull herself together and get on with the job! At any rate, whatever thatpause meant, she made no further mistakes!

This book represents an important contribution to our overall understandingof the intelligence of our closest living relatives, and the development of a varietyof mental and social skills, in some remarkable individuals. And it provides avaluable bridge between research conducted in the controlled conditions of thelaboratory and that which takes place in the natural environment. Finally, it will,I believe, help many to understand the role that can be played by empathybetween scientist and subject, especially when there is such a close evolutionaryrelationship between the two.

VI Foreword by Jane Goodall

Preface

Humans and chimpanzees last shared a common ancestor about 5 to 6 millionyears ago. Single-nucleotide substitutions occur at a mean rate of 1.23% betweencopies of the human and chimpanzee genome. Chimpanzees are our closestliving evolutionary relatives, and therefore it is reasonable to suggest that under-standing them may provide us with clues to understanding human nature.The present book focuses on cognition and its development in chimpanzees,providing a window through which the reader can glimpse the cognitive worldof another species. Across the 28 chapters, a large variety of topics are covered,including perception, cognition, emotion, memory, face recognition, folkbiology, categorization, concept formation, object manipulation, tool manu-facture and use, decision making, learning, possible instances of teaching,education by master–apprenticeship, communication, origin of speech, gaze following, mutual gaze, smiling, social referencing, food sharing, neophobia,mother–infant bonds, parental care, self-awareness, intentionality, imitativeprocesses, understanding others’ minds, cooperation, deception, altruism, reci-procity, personality, social networks, culture, social learning, and ecological constraints.

The approach advocated in this book clearly sets our work apart from previ-ous studies. The so-called ape-language paradigm has focused on single home-raised subjects: isolated apes were taught human-like skills and were forced toadapt to human ways of communication and the human environment. In con-trast, we study chimpanzees in a captive, yet much more natural, setting. Infantsare reared by their own mothers, and live within a community comprising threegenerations of chimpanzees in an enriched outdoor environment. In our “par-ticipation observation” method, the infants take part in tests run by humanexperimenters with the assistance of chimpanzee mothers. These studies in thelaboratory have already illuminated developmental changes in chimpanzee cog-nition over the first 5 years of life through intensive observation and many con-trolled experiments.

In addition, in parallel with our laboratory work we also conduct field studiesin Africa with the aim of learning more about chimpanzees in their naturalhabitat. Long-term research at Bossou, in Guinea, West Africa, has just enteredits fourth decade. Field experiments on tool use have created a logical bridgebetween field observations and laboratory experiments—drawing together

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evidence from these distinct sources, we aim to elucidate chimpanzee cognitionas a whole.

Each human community has its own unique cultural traditions. According tothe Christian calendar, I am writing this in 2006, but in Japan the year is 2666,which, incidentally, is also the year of the dog. The Japanese calendar begins withthe first emperor, Jimmu (660 b.c.), whose 125th successor rules today. West-erners use 26 letters of the alphabet (plus some additional variants) to expressideas and communicate with one another in written form. In contrast, Japaneseprimary schoolchildren have to learn the basic 45 letters of the kana script toexpress information phonetically, as well as 1006 kanji (Japanese and Chinese)characters, each of which has a unique shape and meaning. The Japanese use apair of chopsticks to eat sashimi, but it does not follow that all humans use apair of sticks as a pinching device to eat raw fish. Each culture is unique, differ-ent, but at the same time each shares some characteristics common to all humancultures. Chimpanzees also have a rudimentary form of culture. Researchers nowrecognize that, similarly to the human examples just given, each community ofwild chimpanzees has its unique set of behavioral traditions. For example, chim-panzees in Gombe are well known to fish for termites, while those in Bossou donot perform this behavior. Bossou chimpanzees eat termites that emerge fromtheir mound, but seldom use fishing tools to reach those that cannot be seenfrom the outside. They do, however, have ways of obtaining other hidden foods:Bossou chimpanzees use a pair of stones as hammer and anvil to crack openhard-shelled oil-palm nuts. Gombe chimpanzees do not use stone tools for nutcracking even though both oil-palm trees and stones are readily available. Theyinstead eat only the outer red, soft tissue of oil-palm nuts, leaving behind thekernel concealed inside the hard shell. Each community of chimpanzees has itsown unique culture, not only in terms of tool use but also for such matters asgreetings and possibly dialects.

In many living organisms, genetic channels are important for the transmis-sion of information from one generation to the next. However, in both humansand chimpanzees, the cognitive-learning channel also plays an essential role inthe cross-generational transfer of knowledge, skills, and values. Chimpanzeessurvive 40 to 50 years, or even longer. Infants continue to suckle for the first 4to 5 years of life. Details of how, when, what, where, and from whom to whominformation is transmitted between generations is a fundamental issue forunderstanding chimpanzee behavior. Chapters in this book focus on variousaspects of chimpanzee cognition and the developmental changes associated withthem. The core part of the book is the collaborative product of the three editors,their postdoctoral assistants, graduate students, and Japanese and foreign collaborators, working at the Primate Research Institute of Kyoto University(KUPRI), Japan. The research project we refer to as “Cognitive Development inChimpanzees” (CDC) began in 2000, with the birth of three chimpanzee infantsin the KUPRI community.

This book has a sister volume entitled Primate Origins of Human Cognitionand Behavior, published in 2001 by Springer. It covers various topics related to

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comparative cognitive science in chimpanzees and more than 90 species of non-human primates, in an attempt to synthesize fieldwork and laboratory work. Iencourage readers to consult the earlier book for a broader perspective and his-torical background.

The following Internet sites provide useful information about our ongoingprojects:

Laboratory work: http://www.pri.kyoto-u.ac.jp/ai/index-E.htmFieldwork: http://www.pri.kyoto-u.ac.jp/chimp/index.htmlReferences: http://www.pri.kyoto-u.ac.jp/koudou-shinkei/shikou/index.htmlGreen Corridor Project: http://www.phytoculture.co.jp/greenbelt-top-E.htmlHOPE International Collaboration: http://www.pri.kyoto-u.ac.jp/hope/index.htmlSAGA for conservation and welfare: http://www.saga-jp.org/

I deeply thank all the contributors for their efforts to make this book possi-ble. Each of the authors may have his or her own long list of acknowledgments,as all research requires help from many people. The three editors wish especiallyto express their thanks to Kiyoko Murofushi, who began the chimpanzee project(now known as the “Ai Project”) at the Primate Research Institute in 1978. Wealso thank Toshio Asano, Shozo Kojima, Kisou Kubota, Tetsuya Kojima, KazuoFujita, Nobuo Masataka, Shinichi Yoshikubo, Jyunichi Yamamoto, Takao Fushimi,Shoji Itakura, Koji Hikami, Rikako Tonooka-Tomonaga, Noriko Inoue-Nakamura, Kazuhide Hashiya, So Kanazawa, Akira Satoh, Shuji Suzuki, andAkihiro Izumi for their collaboration in running the laboratory. SumiharuNagumo developed computer programs to assist our cognitive research.Masuhiro Suzuki tended the plants in the compounds and orchards for the chim-panzees. Special thanks are due to the veterinarians and caretakers: Kiyoaki Matsubayashi, Shunji Gotoh, Satoru Oda, Junzo Inagaki, Juri Suzuki, YoshikazuUeno, Norikatsu Miwa, Nobuko Matsubayashi, Masamitu Abe, YoshiroKamanaka, Mayumi Morimoto, Chihiro Katsuta-Hashimoto,Akino Kato,AkihisaKaneko, Kiyonori Kumazaki, Norihiko Maeda, Yoshitaka Fukiura, ShinoYamauchi, Shohei Watanabe, and Takashi Kageyama. We also thank MichikoSakai for many years of secretarial work. We are grateful to the group of GifuUniversity veterinary students who looked after the chimpanzees every Sundayfor the past 4 years: Akihisa Kaneko, Masato Kobayashi, Atsushi Kodama, NamiNakayama, Shino Tanaka, Tomoya Kaneko, and Mami Kondo.

The research project CDC 2000 was originally set up by the three editors of this book together with two postdoctoral researchers, Masako Myowa-Yamakoshi (Shiga Prefectural University at present) and Satoshi Hirata(Hayashibara GARI), and help from the following people: Shozo Kojima, AkihiroIzumi, Noriko Inoue-Nakamura, Tomomi Ochiai-Ohira, Chisato Douke-Inoue,Cláudia Sousa, Maura Celli, Dora Biro,Ari Ueno,Yuu Mizuno, Makiko Uchikoshi,Gaku Ohashi, Sanae Okamoto-Barth, Noe Nakashima, Tomoko Imura, MidoriUozumi, Toyomi Matsuno, and Misato Hayashi. Many other collaborators havemade unique contributions to the project, and without their efforts and dedica-tion we would not have been able to put together such a comprehensive picture

Preface IX

of chimpanzee cognition. In particular, we appreciate the cooperation of our collaborators from other disciplines, such as morphology, neuroscience,and genomics: Osamu Takenaka, Akichika Mikami, Yuzuru Hamada, TakeshiNishimura, Kaoru Chatani, Hirohisa Hirai, Motoharu Hayashi, Keiko Shimizu,and Miho Inoue-Murayama. The following researchers outside KUPRI areinvolved in collaborative studies with us: Kazuo Fujita, Shoji Itakura, KazuhideHashiya, Nobuyuki Kawai, Hideko Takeshita,Yukuo Konishi, Gentaro Taga, RiekoTakaya, Tatsushi Tachibana, Satoru Ishikawa, Daisuke Kosugi, Yuko Kuwahata,Chizuko Murai, So Kanazawa, Masami Yamaguchi, Naruki Morimura, SumirenaSekine, Toshiko Uei-Igarashi, Naoki Horimoto, Seiichi Morokuma, ShoheiTakeda, Orie Nakagawa, Reiko Oeda, Kikuko Tsutsui, Yusuke Moriguchi, MasakoMatsuzawa, and Aya Saitoh. Our collaborators abroad are also numerous: IverIversen, Joel Fagot, James Anderson, Dorothy Fragaszy, Kim Bard, ElisabettaVisalberghi, Celine Devos, Amelie Dreiss, Nadege Bacon, Carol Betsch, DinaStolpen, Pan Jing, Sanha Kim, Mariko Yamaguchi, Patrizia Pozi, and Jessica Crast.The ongoing project continues to be assisted by Sana Inoue, Tomoko Takashima,Etsuko Nogami, Suzuka Hori, Shinya Yamamoto, Yoshiaki Sato, and Laura Martinez.

Fieldwork at Bossou over the past three decades has been carried out in col-laboration with Institut de Recherche Environnementale de Bossou (IREB) andDirection Nationale de la Recherche Scientifique et Technique (DNRST) of theRepublic of Guinea. We thank Kabine Kante, Fode Soumah, Coullibaly Bakary,Jeremie Koman, Tamba Tagbino, Momoudou Diakite, and Makan Kourouma, aswell as other staff from these organizations. We also thank our local assistantsand the villagers at Bossou who have given us their support over the many yearssince the project began in 1976. Special thanks are due to the two oldest guideswho have been working with us since the 1970s: Guano Goumy and TinoZogbila. The Bossou-Nimba project is currently run by the following membersof the KUPRI international team: Yukimaru Sugiyama, Tetsuro Matsuzawa, GenYamakoshi, Hiroyuki Takemoto, Shiho Fujita, Satoshi Hirata, Gaku Ohashi,Misato Hayashi, Kazunari Ushida, Shinya Yamamoto, Asami Kabasawa, GentaroUenishi, Ryutaro Goto, Ryo Hasegawa, Tatyana Humle, Dora Biro, Cláudia Sousa,Kathelijne Koops, Kim Hockings, Nicolas Granier, and Susana Carvalho.

Our research activity both in the wild and in the laboratory has been filmedby ANC (Miho Nakamura and Tamotsu Aso), NHK, and the Mainichi Newspa-per Company (Daisuke Yamada and Akihiro Hirata). Chukyo TV (MichiyoOwaki) has also kept a long-term film record, through periodic visits to our lab-oratory. We thank these people for their collaboration in documenting ourresearch. The color photos reproduced in the book were provided by AkihiroHirata (1c, 2ab, 3b–f, 4ab), Hiroki Sameshima (3a), Tomomi Ochiai (5ab), GakuOhashi (7a–e,g), Tatyana Humle(6b, 7f, 8b), and Tetsuro Matsuzawa (1ab, 6a, 8a).

Our studies in the laboratory and the field were financially supported bygrants from MEXT (12002009, 16002001 to Tetsuro Matsuzawa; 11710035,13610086, 16300084 to Masaki Tomonaga; and 12710037, 15730334 to MasayukiTanaka) and from JSPS (21COE program for biodiversity A14, and 21COE

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program for psychological studies D10). Additional support came from thecooperative research program of KUPRI. The project HOPE (an anagram of“Primate Origins of Human Evolution”), a core-to-core program financially sup-ported by JSPS, began on February 1, 2004, and encouraged us to publish ourstudies in English. HOPE aims to build an international network of collabora-tions to promote the study of nonhuman primates with the aim of understand-ing human nature. I thank the following scholars for their leadership and rolein setting up the collaboration: Michael Tomasello, Josep Call, Svante Pääbo,Christophe Boesch, Jean-Jacques Hublin, Richard Wrangham, Marc Hauser,Frans de Waal, William McGrew, and Elisabetta Visalberghi. Conservation inAfrica has been supported by the following agencies and organizations: Japan-ese Embassy in Guinea, Japan Fund for Global Environment, U.S. Fish andWildlife Services, Conservation International (Primate Action Fund), HoustonZoo (USA), CCCC-Japan, SAGA, GRASP-Japan, Phytoculture Control Co.,Nippon Keidanren, and Toyota.

In closing, I would like to express our gratitude to our publisher, Springer. Ithank Tatiana and Dieter Czeschlik for their friendship and continued support.Thanks are also due to Aiko Hiraguchi, Akemi Tanaka, and Motoko Takeda fortheir editorial work, and to Susan Kreml and Winston Priest for the copyedit-ing. Because this book is the result of a collaboration among such a large andvaried group of people, I hope that it will provide stimulating reading to all thoseinterested in human origins and our evolutionary neighbors.

Tetsuro Matsuzawa

Preface XI

Contents

Foreword by Jane Goodall . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . V

Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . VII

List of Authors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . XV

Color Plates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . XIX

Part 1 Introduction to Cognitive Development inChimpanzees

1 Sociocognitive Development in Chimpanzees: A Synthesis ofLaboratory Work and Fieldwork

T. Matsuzawa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

Part 2 Behavioral and Physical Foundation2 A New Comparative Perspective on Prenatal Motor Behaviors:

Preliminary Research with Four-Dimensional UltrasonographyH. Takeshita, M. Myowa-Yamakoshi, S. Hirata . . . . . . . . . . . . . 37

3 Cognitive Abilities Before Birth: Learning and Long-Lasting Memory in a Chimpanzee Fetus

N. Kawai . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 48

4 Spindle Neurons in the Anterior Cingulate Cortex of Humans and Great Apes

M. Hayashi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64

5 Descent of the Larynx in Chimpanzees: Mosaic and Multiple-StepEvolution of the Foundations for Human Speech

T. Nishimura . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75

6 Understanding the Growth Pattern of Chimpanzees: Does It Conserve the Pattern of the Common Ancestor of Humans andChimpanzees?

Y. Hamada, T. Udono . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 96

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7 The Application of a Human Personality Test to Chimpanzees and Survey of Polymorphism in Genes Relating to Neurotransmitters and Hormones

M. Inoue-Murayama, E. Hibino, T. Matsuzawa, S. Hirata,O. Takenaka, I. Hayasaka, S. Ito, Y. Murayama . . . . . . . . . . . . . . 113

Part 3 Communication and Mother–Infant Relationship

8 Evolutionary Origins of the Human Mother–Infant RelationshipT. Matsuzawa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127

9 Development of Facial Information Processing in Nonhuman Primates

M. Myowa-Yamakoshi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 142

10 Development of Joint Attention in Infant ChimpanzeesS. Okamoto-Barth, M. Tomonaga . . . . . . . . . . . . . . . . . . . . . . . . . 155

11 Food Sharing and Referencing Behavior in Chimpanzee Mother and Infant

A. Ueno . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 172

12 Development of Chimpanzee Social Cognition in the First 2 Years of Life

M. Tomonaga . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 182

Part 4 Social Cognition: Imitation and Understanding Others13 Chimpanzee Learning and Transmission of Tool Use to Fish for

HoneyS. Hirata . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 201

14 How and When Do Chimpanzees Acquire the Ability to Imitate?M. Myowa-Yamakoshi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 214

15 Yawning: An Opening into Empathy?J.R. Anderson, T. Matsuzawa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 233

16 How Social Influences Affect Food Neophobia in Captive Chimpanzees: A Comparative Approach

E. Addessi, E. Visalberghi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 246

17 Tactical Deception and Understanding of Others in Chimpanzees

S. Hirata . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 265

Contents XIII

Part 5 Conceptual Cognition18 Early Spontaneous Categorization in Primate Infants—

Chimpanzees, Humans, and Japanese Macaques—with the Familiarization-Novelty Preference Task

C. Murai . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 279

19 Processing of Shadow Information in Chimpanzee (Pan troglodytes) and Human (Homo sapiens) Infants

T. Imura, M. Tomonaga, A. Yagi . . . . . . . . . . . . . . . . . . . . . . . . . . . 305

20 Color Recognition in Chimpanzees (Pan troglodytes)T. Matsuno, N. Kawai, T. Matsuzawa . . . . . . . . . . . . . . . . . . . . . . . 317

21 Auditory–Visual Crossmodal Representations of Species–SpecificVocalizations

A. Izumi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33022 Spontaneous Categorization of Natural Objects in Chimpanzees

M. Tanaka . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 340

23 Cognitive Enrichment in Chimpanzees: An Approach of Welfare Entailing an Animal’s Entire Resources

N. Morimura . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 368

Part 6 Tools and Culture24 Cognitive Development in Apes and Humans Assessed by Object

ManipulationM. Hayashi, H. Takeshita, T. Matsuzawa . . . . . . . . . . . . . . . . . . . 395

25 Token Use by Chimpanzees (Pan troglodytes): Choice, Metatool,and Cost

C. Sousa, T. Matsuzawa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 411

26 Behavioral Repertoire of Tool Use in the Wild Chimpanzees at Bossou

G. Ohashi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 439

27 Ant Dipping in Chimpanzees: An Example of How MicroecologicalVariables, Tool Use, and Culture Reflect the Cognitive Abilities ofChimpanzees

T. Humle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 452

28 Ontogeny and Cultural Propagation of Tool Use by Wild Chimpanzees at Bossou, Guinea: Case Studies in Nut Cracking and Leaf Folding

D. Biro, C. Sousa, T. Matsuzawa . . . . . . . . . . . . . . . . . . . . . . . . . . . 476

Subject Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 509

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List of Authors

Addessi, Elsa (Chapter 16)Unit of Cognitive Primatology, Institute of Cognitive Sciences and Technologies,CNR, Via Ulisse Aldrovandi 16/b, 00197 Rome, Italy

Anderson, James R. (Chapter 15)Department of Psychology, University of Stirling, Stirling FK9 4LA, Scotland,UK

Biro, Dora (Chapter 28)Department of Zoology, University of Oxford, South Parks Road, Oxford OX13PS, UK

Hamada, Yuzuru (Chapter 6)Primate Research Institute, Kyoto University, 41 Kanrin, Inuyama, Aichi 484-8506, Japan

Hayasaka, Ikuo (Chapter 7)Kumamoto Primate Park, Sanwa Kagaku Kenkyusho, 990 Ohtao, Misumi-cho,Uki, Kumamoto 869-3201, Japan

Hayashi, Misato (Chapter 24)Primate Research Institute, Kyoto University, 41 Kanrin, Inuyama, Aichi 484-8506, Japan

Hayashi, Motoharu (Chapter 4)Primate Research Institute, Kyoto University, 41 Kanrin, Inuyama, Aichi 484-8506, Japan

Hibino, Emi (Chapter 7)Faculty of Applied Biological Sciences, Gifu University, 1-1 Yanagito, Gifu 501-1193, Japan

Hirata, Satoshi (Chapters 2, 7, 13, 17)Great Ape Research Institute, Hayashibara Biochemical Laboratories, 952-2 Nu,Tamano, Okayama 706-0316, Japan

Humle, Tatyana (Chapter 27)Department of Psychology, University of Wisconsin, Madison, 250 N. Mills St.,Madison, WI 53706, USA

XV

Imura, Tomoko (Chapter 19)Department of Integrated Psychological Science, Kwansei Gakuin University,1-1-155 Uegahara, Nishinomiya, Hyogo 662-8501, Japan

Inoue-Murayama, Miho (Chapter 7)Faculty of Applied Biological Sciences, Gifu University, 1-1 Yanagito, Gifu 501-1193, Japan

Ito, Shin’ichi (Chapter 7)Faculty of Applied Biological Sciences, Gifu University, 1-1 Yanagito, Gifu 501-1193, Japan

Izumi, Akihiro (Chapter 21)National Institute of Neuroscience, National Center of Neurology and Psychiatry, 4-1-1 Ogawa-Higashi, Kodaira, Tokyo 187-8502, Japan

Kawai, Nobuyuki (Chapters 3, 20)Graduate School of Information Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan

Matsuno, Toyomi (Chapter 20)Primate Research Institute, Kyoto University, 41 Kanrin, Inuyama, Aichi 484-8506, Japan

Matsuzawa, Tetsuro (Chapters 1, 7, 8, 15, 20, 24, 25, 28)Primate Research Institute, Kyoto University, 41 Kanrin, Inuyama, Aichi 484-8506, Japan

Morimura, Naruki (Chapter 23)Great Ape Research Institute, Hayashibara Biomedical Laboratories, 952-2 Nu,Tamano, Okayama 706-0316, Japan

Murai, Chizuko (Chapter 18)Brain Science Research Center, Tamagawa University Research Institute, 6-1-1 Tamagawa Gakuen, Machida, Tokyo 194-8610, Japan

Murayama, Yuichi (Chapter 7)National Institute of Animal Health, Tsukuba, Ibaraki 305-0856, Japan

Myowa-Yamakoshi, Masako (Chapters 2, 9, 14)School of Human Cultures, The University of Shiga Prefecture, 2500 Hassaka-cho, Hikone, Shiga 522-8533, Japan

Nishimura, Takeshi (Chapter 5)Laboratory of Physical Anthropology, Department of Zoology, Graduate Schoolof Science, Kyoto University, Kitashirakawa Oiwake-cho, Sakyo-ku, Kyoto 606-8502, Japan

Ohashi, Gaku (Chapter 26)Primate Research Institute, Kyoto University, 41 Kanrin, Inuyama, Aichi 484-8506, Japan

XVI List of Authors

Okamoto-Barth, Sanae (Chapter 10)Department of Cognitive Neuroscience, Faculty of Psychology, Maastricht University, P.O. Box 616, 6200 MD Maastricht, The Netherlands

Sousa, Cláudia (Chapters 25, 28)Department of Anthropology, Faculty of Social and Human Sciences, New University of Lisbon, Avenida de Berna, 26–c, 1069-061 Lisbon, Portugal

Takenaka, Osamu (Chapter 7)Primate Research Institute, Kyoto University, 41 Kanrin, Inuyama, Aichi 484-8506, Japan

Takeshita, Hideko (Chapters 2, 24)School of Human Cultures, The University of Shiga Prefecture, 2500 Hassaka-cho, Hikone, Shiga 522-8533, Japan

Tanaka, Masayuki (Chapter 22)Primate Research Institute, Kyoto University, 41 Kanrin, Inuyama, Aichi 484-8506, Japan

Tomonaga, Masaki (Chapters 10, 12, 19)Primate Research Institute, Kyoto University, 41 Kanrin, Inuyama, Aichi 484-8506, Japan

Udono, Toshifumi (Chapter 6)Kumamoto Primate Park, Sanwa Kagaku Kenkyusho, 990 Ohtao, Misumi-cho,Uki, Kumamoto 869-3201, Japan

Ueno, Ari (Chapter 11)Center for Evolutionary and Cognitive Sciences, Graduate School of Arts andSciences, The University of Tokyo, 3-8-1 Komaba, Meguro-ku, Tokyo 153-8902,Japan

Visalberghi, Elisabetta (Chapter 16)Unit of Cognitive Primatology, Institute of Cognitive Sciences and Technologies,CNR, Via Ulisse Aldrovandi 16/b, 00197 Rome, Italy

Yagi, Akihiro (Chapter 19)Department of Integrated Psychological Science, Kwansei Gakuin University,1-1-155 Uegahara, Nishinomiya, Hyogo 662-8501, Japan

List of Authors XVII

1a. (Upper left): Pal (left) and Ayumu (right) on October 23, 2001

1b. (Upper right): Cleo (left) and Ayumu (right) on October 23, 2001

1c. (Lower): The Ayumu-Cleo-Pal trio on February 1, 2002

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2a. First calligraphy of the New Year by the chimpanzee Ai. January 1, 2000

2b. Participation observation based on the triadic relationship of the chimpanzee mother, theinfant, and the tester. Ai’s son, Ayumu, shown here at the age of 7 months, clings to TetsuroMatsuzawa. December 4, 2000

3c. Pan and her daughter, Pal, withMasayuki Tanaka. May 16, 2002

3a. Ai and her son, Ayumu, with T.Matsuzawa. January 17, 2002

3b. Chloe and her daughter, Cleo, withMasaki Tomonaga. February 20, 2002

3d. Testing a human child, Mimori, withher mother

3e. Pan and Pal, cracking macadamia nuts 3f. Ayumu at the age of 2 years and 3months already has started honey fishing

4b. At the age of 10 months Ayumu touches the image of an apple on the touch-sensitivemonitor

4a. Ayumu watching Ai carrying out a matching-to-sample task at the computer. Ai knowsthe names of 11 colors. As the lexigram (visual symbol) meaning “blue” is presented in the bottom center of the screen, she chooses the corresponding kanji (Japanese-Chinese)character

5b. Pal at the age of 1 year and 8 months on the rope with an old female, Reiko. May 7, 2002

5a. Outdoor compound for the KUPRI community in April 2005. During the daytime, chim-panzees spend about 80% of their time on the 15-m-high “triple towers”

6b. The chimpanzee Jire (estimated age, 47 years) and her children, Jeje (7-year-old male bornin December 1997) and Joya (1-year-old female born in September 2004)

6a. Chimpanzees cracking oil-palm nuts at Bossou, Guinea. The infant closely watches hermother cracking nuts

7a. Kai, an old woman (estimated age, 52years), died in 2003

7b. Tua, the former alpha male of theBossou community

7c. Poni, an adolescent male, taking a napon the ground

7d. Yolo, the current alpha male of theBossou community eating Myrianthusarboreus

7e. Yo, the mother of Yolo

7f. Jire with Joya, her 1-year-old daughter

7g. Veve (left) and Jimato (right), bothinfants, died in the flu-like epidemic of 2003

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8a. Veve died on December 31, 2003, watched over by her mother, Vuavua, and grandmother,Velu. The mother continued to carry Veve’s body even after it mummified

8b. The Nimba Mountains and savanna, located to the southeast of Bossou. To connect the Bossou community with groups of chimpanzees in the Nimba Mountains, the Green Corridor project was launched in 1997