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The Pygmy Evolutionary and Behavior Hal Coolidge on the Asiatic Primate Expedition, 1937. The Pygmy Chimpanzee Evolutionary Biology and Behavior

Edited by Randall L. Susman School of Medicine State University of New York at Stony Brook Stony Brook, New York

PLENUM PRESS • NEW YORK AND LONDON Library of Congress Cataloging in Publication Data Main entry under title: The Pygmy chimpanzee. Includes bibliographical references and index. I. Pygmy chimpanzee. I. Susman, Randall L., 1948- QL737.P96P94 1984 599.88'44 84-13236 ISBN 978-1-4757-0084-8 ISBN 978-1-4757-0082-4 (eBook) DOl 10.1007/978-1-4757-0082-4

©1984 Plenum Press, New York Softcover reprint of the hardcover 15t edition 1984 A Division of Plenum Publishing Corporation 233 Spring Street, New York, N.Y. 10013 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 To Hal Coolidge Contributors

Alison Badrian Department of , State University of New York at Stony Brook, Stony Brook, New York 11794

Noel Badrian Department of Anthropology, State University of New York at Stony Brook, Stony Brook, New York 11794

Harold Jefferson Coolidge Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts 02138

Raymond C. Heimbuch Department of Medical Biostatistics, Ortho Pharmaceutical Company, Raritan, New Jersey 08869

William L. Jungers Department of Anatomical Sciences, School of Med• icine, State University of New York at Stony Brook, Stony Brook, New York 11794

Kabongo Ka Mubalamata lnstitut de Recherche Scientifique, Centre de Recherche de Lwiro, Bukavu, Zaire

Takayoshi Kano Department of , College of Medicine, University of the Ryukyus, 207 Uehara, Nishihara, Okinawa, Japan

Warren G. Kinzey Department of Anthropology, City College of New York, City University of New York, New York, New York 10031

Suehisa Kuroda Laboratory of Physical Anthropology, Faculty of Sci• ence, Kyoto University, Sakyo-ku, Kyoto, 606 Japan

vii viii CONTRIBUTORS

Jeffrey T. Laitman Department of Anatomy, Mount Sinai School ofMed• icine of the City University of New York, New York, New York 10029 Richard K. Malenky Department of Ecology and , State Uni• versity of New York at Stony Brook, Stony Brook, New York 11794

Henry M. McHenry Department of Anthropology, University of Cali• fornia at Davis, Davis, California 95616

Mbangi Mulavwa Institut de Recherche Scientifique, Centre de Mabali, B.P. 36 Bikoro, Equateur, Zaire

Vincent M. Sarich Departments of Anthropology and Biochemistry, U ni• versity of California, Berkeley, California 94720

E. S. Savage-Rumbaugh Research Center, Yerkes Regional Primate Research Center, Emory University, and Georgia State Uni• versity, Atlanta, Georgia 30322

Brian T. Shea Department of Anthropology, American Museum of Nat• ural History, New York, New York 10024. Present address: De• partments of Anthropology and Cell Biology and Anatomy, North• western University, Evanston, Illinois 60201

Wladyslaw W. Socha Primate Blood Group Reference Laboratory and WHO Collaborating Centre for Haematology of Primate , Laboratory for Experimental Medicine and Surgery in Primates (LEMSIP), New York University School of Medicine, New York, New York 10016

Randall L. Susman Department of Anatomical Sciences, School ofMed• icine, State University of New York at Stony Brook, Stony Brook, New York 11794

Nancy Thompson-Handler Department of Anthropology, Yale Univer• sity, New Haven, Connecticut 06520

Dirk F. E. Thys Van den Audenaerde Section, Musee Royale de I'Afrique Centrale, B-1980 Tervuren, Belgium

Adrienne L. Zihlman Department of Anthropology, University of Cali• fornia at Santa Cruz, Santa Cruz, California 95064 Foreword Historical Remarks Bearing on the Discovery of paniscus

Whether by accident or by design, it was most fortunate that Robert M. Yerkes, the dean of American primatologists, should have been the first scientist to describe the characteristics of a pygmy chimpanzee, which he acquired in August 1923, when he purchased him and a young female companion from a dealer in New York. The came from somewhere in the eastern region of the Belgian Congo and Yerkes esti• mated the male's age at about 4 . He called this young male Prince Chim (and named his female, com• mon chimpanzee counterpart Panzee) (Fig. I). In his popular book, Almost Human, Yerkes (1925) states that in all his experiences as a student of behavior, "I have never met an animal the equal of this young chimp ... in approach to physical perfection, alertness, adaptability, and agreeableness of disposition" (Yerkes, 1925, p. 244). Moreover,

It would not be easy to find two infants more markedly different in bodily traits, temperament, , vocalization and their varied expressions in action, than Chim and Panzee. Here are just a few points of contrast. His eyes were black and in his dark face lacked contrast and seemed beady, cold, expressionless. Hers were brown, soft, and full of emotional value, chiefly because of their color and the contrast with her light complexion. Chim's were small, set close to his head and fringed with black hair, whereas Panzee's stood out conspicuously, and were light in color and hairless. Their foreheads, , lips and head conformations also differed noticeably. (Yerkes, 1925, p.245.)

When it comes to animal temperament, we are at a loss for descriptive terms. Little Chim was notable for his bold, aggressive manner, his constant alertness

ix x FOREWORD

Figure 1. A portrait of Prince Chim. FOREWORD xi

and eagerness for new experiences. Seldom daunted, he treated the mysteries of as philosophically as any man. Panzee was timid, nervous, hesitant before anything novel or new. When there was anything to learn by "trial and error," he took the lead and she followed at an eminently safe distance. Chim also was even-tempered and good-natured, always ready for a romp; he seldom resented by word or deed unintentional rough handling or mishap. Never was he known to exhibit jealousy .... [By contrast,] Panzee could not be trusted in critical situations. Her resentment and anger were readily aroused and she was quick to give them expression with and teeth. (Yerkes, 1925, p. 246.) Everything seems to indicate that Chim was extremely intelligent. His sur• prising alertness and interest in things about him bore fruit in action, for he was constantly imitating the acts of his human companions and ,esting all objects. He rapidly profited by his experiences .... Never have I seen a man or beast take greater satisfaction in showing off than did little Chim. The contrast in intellectual qualities between him and his female companion may briefly, if not entirely adequately, be described by the term "opposites." (Yerkes, 1925, p. 248.) In group behavior studies his actions "contrasted almost as markedly with that of his chimpanzee associates as did his appearance, for he was a little black-face with rather conspicuous , small ears, and a heavy coat of fine black hair, whereas most of them were white-face specimens with the typical chimpanzee nose, large, conspicuous ears, and much coarser and generally less thick coat of hair" (Yerkes, 1925, p. 251). Sadly, Prince Chim died of pneumonia while visiting Madam Abreu's colony in Havana in July 1924. Professor Yerkes states that he was ac• tually a prince of his kind and his "behavior even in death goes far to justify the title of this story, Almost Human. Prince Chim seems to have been an intellectual genius. His remarkable alterness and quickness to learn were associated with a cheerful and happy disposition which made him the favorite of all, and gave him a place of distinction not only in their regard but in their memories" (Yerkes, 1925, p. 255). I recall with great pleasure meeting Prince Chim at the Yerkes' farm in Franklin, New Hampshire, and remember his greeting me with a firm handshake. Little did I realize that he would open the way to the important studies to be described in this volume 60 years later. It was my good fortune to have my own interest in the anthropoid and particularly , in a large measure sparked by my distin• guished friend, Robert M . Yerkes, for many years professor of psychology at Yale University. I was fortunate to have served as assistant zoologist on the Harvard Medical School African Expedition in 1926-1927, where I collected and documented a good-sized mountain in the mountains of the eastern Belgian Congo for the Museum of Comparative Zoology at Harvard. This expedition was followed by a survey of gorilla material xii FOREWORD

in European and U. S. museums and publication of a revision of gorilla classification (Coolidge, 1927-1929). While visiting European museums to gather data for my gorilla study in 1928, I noticed a specimen that was described to be from south of the Congo River and was somewhat smaller than other chimpanzee specimens. I shall never forget, late one afternoon in Tervuren, casually picking up from a storage tray what clearly looked like a juvenile chimp's from south of the Congo and finding, to my amazement, that the epiphyses were totally fused. It was clearly adult. I picked up four similar in adjoining trays and found the same condition, which I measured for a future paper on the revision of chimpanzees. Just then, Dr. Schouteden, the museum director, came to tell me that it was time to close and I showed him what I had discovered. He seemed most interested. Two weeks later Dr. Ernst Schwarz, who was aware that chimps on either side of the Congo differed, visited the Congo Museum and Dr. Schouteden told him about my discovery. In a flash Schwarz grabbed a pencil and paper, measured one small skull, wrote up a brief description, and named a new pygmy chimpanzee race: Pan satyrus paniscus. He asked Schouteden to have his brief account printed without delay in the Revue Zoologique (April 1929) of the Congo Museum (Schwarz, 1929). I had been taxonomically scooped. When I learned about this article and read a further paper by Schou• tenden on the chimps from the left bank of the Congo, I intensified my study of the pygmy chimpanzee and its distribution. In 1931 I undertook a comprehensive survey of chimpanzee museum collections with a view to revising their classifications as I had done for gorillas. My survey of skeletal material included collections in the American Museum of Natural History, the Riksmuseum in Stockholm, the British Museum in London, the Berlin Museum, the Paris Museum of Natural History, the Royal Museum in Brussels, and the Congo Museum in Tervuren, which made me feel very much at home with the rich chimp and gorilla collec• tions from the Belgian Congo. In the American Museum of Natural History I found a skin and skull that had been collected by Jim Chapin near Lukolela on the southeast bank of the Congo in 1930. It clearly belonged to this small race. I also found the skin and of Dr. Yerkes' Prince Chim, No. 54336, American Museum of Natural History. Although I had no juveniles to compare it with, its dark skin and small ears clearly indicated that it also was a "." The Chapin skeleton was compared with specimens of Pan, carefully measured by Dr. Adolph Schultz, and characteristics of possible taxonomic significance listed. Most consistent are the small bones FOREWORD

throughout. There seems to be more evidence from the external appear• ance of the skeleton collected by Chapin that it is closer to Pan schwein• furthii than to Pan satyrus, as Schwarz had stated. I believed that the pygmy chimpanzee had a sufficient difference in degree as well as in variation from other chimpanzees that it should be classified as a full , making it Pan paniscus instead of Pan satyrus paniscus. This classification was documented in my report in the Amer• ican JournaL of Physical AnthropoLogy (Coolidge, 1933). It is highly gratifying that the greatly needed further studies of this important ape are being carried out by primatologists in many countries in cooperation with the Zaire government, and also that one or more national parks, including the pygmy chimps' present principal habitat south of the Congo River, will hopefully be established and protected with adequate guards to save the species from extinction, for the benefit of future generations, as well as the welfare of the animals themselves. Some believe that this true paedomorphic species is the most im• portant of the chimpanzees for the study of the phylogeny and relation• ships of the apes and man. This possibility makes this volume of particular significance. The research reported here and future studies will no doubt help us answer the question of whether or not the pygmy chimpanzee approaches most closely the common ancestor of chimpanzee and man.

Harold J. Coolidge Museum of Comparative Zoology Harvard University Cambridge. Massachusells

References

Coolidge. H. J .• 1927-1929. Memoirs of the Museum of Comparative Zoology at Harvard College. Volume L, Museum Publication. Cambridge. Massachusetts. Coolidge, H. J., 1933, Pan paniscus: Pygmy chimpanzee from south of the Congo River. Am. J. Phys. Anlhropol. XVIII(I):1-57. Schwarz, E .. 1929, Das Vorkommen des Schimpansen auf den Iinken Kongo-Ufer. ReI'. Zool. Bot. Afr. XVI(4):425-426. Yerkes, Robert M., 1925, Almost Human. The Century Co .• New York. Preface

On August 9th, 1982, a symposium entitled The Evolutionary Morphol• ogy and Behavior of the Pygmy Chimpanzee was held in Atlanta in conjunction with the IXth Congress of the International Primatological . The symposium honored Harold Jefferson Coolidge, a man who has had a lifelong devotion to the study of primates and primate conser• vation. Hal Coolidge played a key role in the discovery and description of the pygmy chimpanzee in the late 1920s, and in 1933 it was he who elevated Pan paniscus to species status consequent on his detailed mor• phological study. All of us who participated in this symposium were ho• nored to present the results of our respective work in the presence of one of the major figures in in this century, the man who, over 50 years ago, brought Pan paniscus to the attention of the scientific world. Hal Coolidge began his lifelong association with the Harvard Museum of Comparative Zoology (MCZ) at the beginning of his sophomore . In 1926 Richard Strong and George Shattuck invited Hal to accompany them (in the role of assistant mammalogist) on the Harvard Medical Ex• pedition across (1926-1927). As a result of this experience Hal decided on a career in . Under the tutelege of Prof. of Yale (Harvard did not have a primatologist at this time), Hal was advised to pursue an interest in the biology of gorillas, which had been sparked by his prior travels in the eastern Congo in 1927. The result was a comprehensive work, A Revision of the Genus Gorilla, published by Coolidge in 1929. From 1929 through 1940 Hal was an assistant curator of at the MCZ. During this time he worked principally with primates, and conducted research on gorillas, pygmy chimpanzees, and . Beginning in 1931 Hal taught a course on the evolution of animal sociology with William Morton Wheeler, and he lectured on primatology in courses offered by Ernest Hooton. xv xvi PREFACE

In 1937 Hal organized, funded, and led the legendary Asiatic Primate Expedition (APE), which was sponsored by the MCZ, Columbia Uni• versity, and Johns Hopkins. The members of the APE included, in ad• dition to Hal, Clarence Ray Carpenter (who by this time had pioneered studies of howling monkeys and spider monkeys in Panama), Sherwood Washburn (a student of Hooton), Adolph Schultz (a preeminent physical anthropologist and anatomist), J. Augustus Griswold (zoologist and prep• arator interested in small mammals and birds), and John Coolidge (pho• tographer and illustrator) (Fig. 1). This distinguished group spent 9 months in northern Siam (now Thailand), North , and Sumatra. Their work focused on primates, and their scientific legacy was profound. From the APE, Carpenter published his classic work, "A Field Study in Siam of the Behavior and Social Relations of the "; Washburn obtained the specimens for his thesis, "A Preliminary Metrical Study of the Skel• eton of Langurs and "; and Schultz acquired wet specimens and skeletal material that served him in his manifold publications over

Figure 1. Members of the Asiatic Primate Expedition (APE). Front row (left to right): Augustus Griswold, Sherwood Washburn. Back row: Harold Coolidge, Adolph Schultz, Clarence Carpenter. PREFACE xvii the next 35 years. Other legacies of the expedition included extensive collections of monkeys and gibbons, most of which are housed in the MCZ, field notes, films, and photographs. All constitute a priceless re• source for students of primatology. Following the expedition, Hal toured the United States giving popular lectures, which helped pay the remaining cost of the expedition. The success of the APE also resulted, in part, in the establishment of the laboratory of primatology at Harvard (1938-1939). Hal, working in cooperation with Carpenter and Washburn, and with advice from Robert Yerkes, was instrumental in planning the primate laboratory. Hal's work at the MCZ represented only a small part of his profes• sional activity. In 1930 Hal established the American Committee for In• ternational Protection (now the Committee for International Conservation). This was the earliest international conservation organi• zation in the United States and it helped draft the London Convention on African Wildlife Protection; the Committee also sponsored many other publications. The Committee took part in the establishment of the Inter• national Union for the Conservation of and Natural Resources (lUCN), which was established in 1948 with the assistance of the French Government and then Director-General of UNESCO, Julian Huxley. (To• day the IUCN has over 50 member governments and 250 member insti• tutions in over 90 countries.) Hal founded IUCN's Survival Service and Parks Commission. He was IUCN's first Vice President until 1954, was President from 1966 to 1972, and is now Honorary President. In 1961 Hal helped to found the IUCN's sister organization, the World Wildlife Fund, which finances the IUCN and other conservation projects. Hal was a director of WWF -International until 1976 and a founding director of WWF• US Hal's specific contributions to wildlife conservation are manifested in the establishment of national parks in Japan, Korea, Taiwan, the Phil• lipines, New Caledonia, Vietnam, Malaysia, and Indonesia. He organized the First World Conference on National Parks (held in Seattle in 1962). His contributions to conservation in third world countries has earned him over 25 major honors, including the J. Paul Getty Wildlife Conservation Prize for 1979. Hal was the first American so honored. Hal began the pygmy chimpanzee symposium with personal remarks and recollections of his first encounter with Prince Chim, a captive pygmy chimpanzee owned by Prof. Yerkes (but not known at the time to be a pygmy chimpanzee) (see Coolidge, Foreword to this volume). Hal also related his meeting with Dr. Ernst Schwarz in Berlin and the sequence of events leading to Schwarz' announcement of Pan paniscus. Following the symposium a reception sponsored by the L. S. B. Leakey Foundation and the World Wildlife Fund-US was held in honor of Hal Coolidge. xviii PREFACE

A great many people and organizations are responsible, both directly and indirectly, for the present volume. The Musee Royale de I'Afrique Centrale at Tervuren (now the Tervuren Museum) has provided all of those interested in the comparative anatomy of Pan paniscus with the only sizable collection of skeletal material available. Over the years the scientific and technical staff of the Museum has provided many a visiting scientist with a warm and friendly atmosphere, and one of the most hos• pitable working environments to be found anywhere. We are deeply in• debted to the past and present staff of the Tervuren Museum. Those of us who have had the privilege of studying Pan paniscus in the field are deeply indebted to the Government of the Republic of Zaire. In particular, we are indebted to the Institut de Recherche Scientifique (IRS) in Kinshasa for its unwavering support. We are grateful to Dr. Iteke Bochoa, Dr. Kankwenda M'Baya, the present Director, Dr. Nkanza Ndolumingu, and the staff of the IRS for their advice, help, and colleagueship. The editor would like to thank the authors who have contributed to this volume. Divergent perspectives and methods characterize the con• tributions that follow. Despite this and the controversy that has attended discussions of the phylogenetic affinities and relevance of Pan paniscus for modeling early , the papers presented in Atlanta rep• resent a relatively uniform and consistent view. In some ways pygmy chimpanzees closely resemble the earliest hominids, but in others the common chimpanzee and other apes provide us with important compar• ative data for phylogeny reconstruction and functional inference. As editor I have chosen to retain the common name of "pygmy chimpanzee" for Pan paniscus. I have done so largely for historical reasons and for reasons of familiarity. Also, I personally do not feel that the present alternatives, bonobo or bonobo chimpanzee, are any more justified. Recent work, including the published body weights for common and pygmy chimpan• zees, shows that in fact the eastern long-haired chimpanzee Pan troglod• ytes schweinfurthii has a mean body weight that is similar to that of Pan paniscus (Jungers and Susman, this volume). It is also true that, as judged by criteria for mammalian drawfs, Pan paniscus does not follow the trend for accelerated negative scaling of the skeleton relative to the postcanine . However, it must also be noted that Schwarz, Coolidge, and later workers have demonstrated that Pan paniscus has a relatively small skull for its body size or trunk length. Remembering that the skull was the basis on which the taxon was diagnosed and that Coolidge in 1933 had only a single small (female) specimen with which to describe the postcranial skeleton, it is understandable that this species was considered to be a dwarf or pygmy form. It was not until the 1960s that additional of Pan paniscus became available, through the efforts of PREFACE xix

Vandebroek (see van den Audernaerde, this volume). It was not until very recently that enough body weights of free-ranging common and pygmy chimpanzees have been available to allow for intergroup comparisons among the varieties of chimpanzees. Thus it seems that in historical perspective the term "pygmy chim• panzee" is not an inappropriate one. From our present perspective it is preferable to the cumbersome term "bonobo chimpanzee" or "bonobo." The word bonobo itself is problematic. It most likely is the mispronoun• ciation of the word Bolobo, which is a town on the Zaire River, between Kinshasa and Lukolela, from which specimens of Pan paniscus were collected (see van den Audernaerde, this volume). It is interesting to note that the Lingala word for the pygmy chimpanzee is "Mokumbusu"; the Limongo name is "Eja" or "Engombe." Last of all for those concerned, it seems that, in any event, the name "pygmy chimpanzee" is at least as appropriate as the common name Celebes "black ape" given to Macaca nigra and the other Celebes macaques, or the name "barbary ape" given to Macaca sylvanus. I expect that the systematics of the genus Pan will be a subject of discussion for some time to come (see chapters by Socha and Sarich, this volume); different preferences for common names will, no doubt, also remain. Finally, it should be noted that at the very time that we are beginning to learn about the behavior and ecology of free-ranging pygmy chimpan• zees, the species and its environment have become threatened with dis• ruption and elimination. Whether we will continue to learn about pygmy chimpanzees in the wild depends on the political and economic situation in central Africa. At present commercial interests threaten the rain forest and the survival of its unique fauna. The only hope for the long term is an international conservation effort under the leadership of the Zairian government, with the help of scientists and conservationists. In the Lo• mako Forest and at Wamba the threat is primarily from foreign commercial logging. In other areas of Equateur the pygmy chimpanzee is threated by hunting and by human encroachment in the form of shifting, slash-and• burn agriculture. As late as the 17th century pygmy chimpanzees may have ranged into northwestern Angola and as far south as the Quanza River (V. Reynolds, 1967, The Apes, Dutton, New York). With the col• onization of the Congo, the Belgians installed roads and river transport systems, which led to the formation of population centers. Since 1900 the large mammals that once were found throughout much of Zaire have been decimated. Today vast areas along the major waterways and roads and near the population centers of Lukolela, Mbandaka, Boende, Befale, Bas• ankusu, and Lisala are devoid of pygmy chimpanzees and significant numbers of other large mammals. Salonga National Park, in lower Equa- PREFACE teur, is also devoid of Pan paniscus. If we are to continue our field studies, the first fruits of which are seen in the present volume, then a major conservation effort must be made to establish a reserve free from the inevitable perturbations of human encroachment. Already the government of the Republic of Zaire has expressed an interest in preserving its rich natural history. With help from the international scientific and conser• vation communities we are hopeful that the establishment of a protected area for pygmy chimpanzees will take place before it is too late.

Randall L. Susman Contents

Part I. Molecular Biology, Systematics, and Morphology

Chapter 1 The Tervuren Museum and the Pygmy Chimpanzee ...... 3 Dirk F. E. Thys Van den Audenaerde References ...... 11

Chapter 2 Blood Groups of Pygmy and Common Chimpanzees: A Comparative Study...... 13 Wladyslaw W. Socha 1. Introduction ...... 13 2. Methodology of Blood Grouping and General Classification of Blood Groups of Primates ...... 14 3. The A-B-O Blood Group System...... 16 3.1. Subgroups of A ...... 17 3.2. The H Specificity...... 20 3.3. Secretion of A-B-H Substances ...... 21 3.4. Serum Isoagglutinins ...... 22 4. The M-N Blood Group System ...... 23 5. The V-A-B-D Blood Group System ...... 26 6. The Rh-Hr Blood Group System...... 27 7. The R-C-E-F Blood Group System...... 28 8. Other Blood Group Systems ...... 33 9. Genealogical Studies ...... 34 10. Summary and Conclusions ...... 35 References ...... 39 xxi xxii CONTENTS

Chapter 3 Pygmy Chimpanzee Systematics: A Molecular Perspective 43 Vincent M. Sarich I. Introduction ...... 43 2. Results ...... 44 2.1. Further Electrophoretic Studies ...... 44 2.2. Immunology ...... 44 2.3. Restriction Endonuclease Comparisons of Mitochondrial DNA ...... 44 3. Phylogenetic Implications of the Molecular Data...... 45 4. Origin and Adaptive Radiation of the African Apes (Including Hominids) ...... 46 4. I. Developing an Understanding of Organismal Evolution.. 46 4.2. The Role of the Pygmy Chimpanzee in Telling Us about Hominid Origins ...... 47 References ...... 48

Chapter 4 A Measure of Basicranial Flexion in Pan paniscus, the Pygmy Chimpanzee...... 49 Jeffrey T. Laitman and Raymond C. Heimbuch I. Introduction ...... 49 2. Methods and Materials ...... 50 2. I. Craniometric Measurements and Statistical Methods ..... 50 2.2. Pan paniscus Specimens ...... 54 3. Results ...... 55 4. Discussion...... 61 References ...... 63

Chapter 5 The Dentition of the Pygmy Chimpanzee, Pan paniscus 65 Warren G. Kinzey I. Introduction ...... 65 2. Materials and Methods ...... 66 3. Results ...... 67 3.1. Upper Morphology...... 67 3.2. Lower Molar Morphology ...... 70 3.3. Metrical Data ...... 72 3.4. Roots of Teeth ...... 79 3.5. Sequence of Eruption ...... 81 CONTENTS xxiii

4. Discussion ...... 83 4.1. Distribution of Advanced and Primitive Traits ...... 83 4.2. Functional Differences between Chimpanzee Species .... 84 References ...... 87

Chapter 6 An Allometric Perspective on the Morphological and Evolutionary Relationships between Pygmy (Pan paniscus) and Common (Pan troglodytes) Chimpanzees ...... 89 Brian T. Shea 1. Introduction ...... 89 2. The Types and Meanings of Allometry ...... 92 3. Allometry and Heterochrony ...... 97 4. Proportion and Size Differences between Pan paniscus and Pan troglodytes ...... , ...... 98 5. Postcranial Allometry ...... 103 6. Cranial Allometry ...... 109 7. Dental Allometry ...... ll5 8. Heterochrony and Morphology ...... 119 9. Interspecific Dissociations ...... 121 10. Conclusions ...... 123 References 125

Chapter 7 Body Size and Skeletal Allometry in African Apes ...... 131 William L. Jungers and Randall L. Susman I. Introduction ...... 131 2. Materials and Methods ...... 136 2.1. Sources of Body Weights ...... 136 2.2. Skeletal Sample...... 137 2.3. Analytical Methods...... 138 3. Results and Discussion ...... 142 3.1. Body Size of African Apes ...... 142 3.2. Interspecific Allometry...... 151 3.3. Intraspecific Allometry ...... 161 References ...... 171

Chapter 8 Body Build and Tissue Composition in Pan paniscus and Pan troglodytes, with Comparisons to Other Hominoids ...... 179 Adrienne L. Zihlman xxiv CONTENTS

1. Introduction 179 2. Pan paniscus and Pan troglodytes: A Comparison of Body Builds...... 182 3. Methods ...... 183 4. Results ...... 184 5. Body Build and Locomotor Pattern: Case Studies ...... 187 5.1. Symphalangus ...... 188 5.2. Pongo ...... 191 5.3. Pan troglodytes and Pan paniscus ...... 191 5.4. sapiens ...... 193 6. Pan paniscus: Its Place among the Hominoids ...... 193 References ...... 198

Chapter 9 The Common Ancestor: A Study of the Postcranium of Pan paniscus, , and Other Hominoids ...... 201 Henry M. McHenry 1. Introduction ...... 201 2. Materials and Methods ...... 202 3. Results ...... 204 3.1. ...... 204 3.2. Distal Humerus ...... 207 3.3. Ulna ...... 209 3.4. Capitate ...... 210 3.5. ...... 211 3.6. Proximal Femur ...... 212 3.7. Distal Femur...... 213 3.8. Foot ...... 214 3.9. Proportions...... 215 4. Discussion...... 216 5. Conclusions ...... 222 References ...... 223

Part II. Behavior of Pan paniscus

Chapter 10 Feeding Ecology of the Pygmy Chimpanzees (Pan paniscus) of Wamba ...... 233 Takayoshi Kano and Mbangi Mulavwa CONTENTS ~

1. Introduction ...... 233 1. 1. Subjects and Methods ...... 234 1.2. Study Area...... 236 2. Results ...... 238 2.1. Food Repertoire ...... 238 2.2. Dietary Proportions ...... 244 2.3. Annual and Seasonal Variations in Diet...... 247 2.4. Food Preferences ...... 249 2.5. Food Diversity ...... 252 2.6. Food Provisioning ...... 253 2.7. Feeding Techniques...... 256 2.8. Habitat Utilization ...... 259 2.9. Routine Activities ...... 261 2.10. Daily Range and Party Size ...... 263 2.11. Competition ...... 264 3. Discussion ...... 266 4. Summary ...... 271 References ...... 273

Chapter 11 Feeding Ecology of Pan paniscus in the Lomako Forest, Zaire ..... 275 Noel Badrian and Richard K. Malenky 1. Introduction ...... 275 2. Study Area ...... 275 3. Study Population...... 277 4. Methods ...... 277 5. Plant Foods...... 278 6. Seasonal Patterns ...... 288 7. Feeding Patterns and Group Size ...... 289 8. Animal Foods...... 290 9. Discussion...... 293 References ...... 298

Chapter 12 Interaction over Food among Pygmy Chimpanzees 301 Suehisa Kuroda 1. Introduction ...... 301 2. Subjects and Methods ...... 302 xxvi CONTENTS

2.1. Subjects and Data Collection ...... 302 2.2. Terminology ...... 302 3. Results ...... 303 3.1. Interaction over Naturally Occurring Food...... 303 3.2. Interaction over Artificially Provided Food ...... 307 4. Discussion ...... 320 4.1. Food Sharing Behavior in Pygmy and Common Chimpan- zees ...... 320 4.2. Food Division...... 321 4.3. Begging and Sharing...... 322 4.4. Cofeeding ...... 322 4.5. Hypothesis of Preadaptation to Systematic Food Sharing ...... 323 References ...... 324

Chapter 13 Social Organization of Pan paniscus in the Lomako Forest, Zaire 325 Alison Badrian and Noel Badrian 1. Introduction ...... 325 2. Methods ...... 326 3. Results ...... 328 3.1. Population Density and Group Size ...... 328 3.2. Group Composition...... 331 3.3. Agonistic Behavior ...... 334 3.4. Grooming Interactions ...... 335 3.5. Food Sharing ...... 336 3.6. Sociosexual Behavior ...... 336 4. Discussion ...... 337 5. Conclusion...... 342 References ...... 344

Chapter 14 Sexual Behavior of Pan paniscus under Natural Conditions in the Lomako Forest, Equateur, Zaire...... 347 Nancy Thompson-Handler, Richard K. Malenky, and Noel Badrian I. Introduction ...... 347 2. Methodology ...... 348 CONTENTS xxvii

3. Results...... 351 3.1. Male-Female Sexual Behavior ...... 351 3.2. Female-Female Genital Contact ...... 355 3.3. Male-Male Genital Contact...... 358 4. Discussion ...... 359 4.1. Menstrual Cycles and Sexual Swellings ...... 360 4.2. Distribution of Copulations across Swelling Phases ...... 362 4.3. Lactational Amenorrhea ...... 363 5. Conclusion...... 364 References ...... 366

Chapter 15 The Locomotor Behavior of Pan paniscus in the Lomako Forest ... 369 Randall L. Susman 1. Introduction ...... 369 2. Methods ...... 371 3. Results ...... 373 3.1. Terrestrial Locomotion ...... 373 3.2. ...... 374 4. Discussion ...... 383 5. Comparison of Pygmy Chimpanzees in the Lomako and at Other Sites...... 386 6. Comparisons of the Locomotion of Pygmy and Common Chim- panzees ...... 388 7. Conclusion ...... 389 References ...... 392

Chapter 16 Pan paniscus and Pan troglodytes: Contrasts in Preverbal Commu- nicative Competence ...... 395 E. S. Savage-Rumbaugh 1. Introduction ...... 395 2. History of Subjects ...... 396 3. Research Environment ...... 397 4. Development of Nonverbal Communicative Competence in Kanzi ...... ,...... 403 5. Conclusion...... 411 References ...... 412 xxviii CONTENTS

Chapter 17 Will the Pygmy Chimpanzee Be Threatened with Extinction as Are the and the White Rhinoceros in Zaire? ...... 415 Kabongo Ka Mubalamata References ...... 419

Author Index ...... 421 Subject Index ...... 427