Primates of South Asia: Ecology, Sociobiology, and Behavior [Reprint 2014 ed.] 9780674432215, 9780674432208

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OF SOUTH ASIA

HARVARD UNIVERSITY PRESS CAMBRIDGE, MASSACHUSETTS LONDON, ENGLAND • 1977

M. L. Roonwal S. M. Mohnot

OF SOUTH ASIA Ecology, Sociobiology, and Behavior

Copyright © 1977 by the President and Fellows of Harvard College All rights reserved Printed in the United States of America Library of Congress Cataloging in Publication Data Roonwal, M L Primates of South Asia. Bibliography: p. Includes index. 1. Primates—South Asia. 2. Primates—Behavior. 3. Mammals—Behavior. 4. Mammals—South Asia. I. Mohnot, S. M., joint author. II. Title. QL737.P9R65 599'.8'0954 76-28309 ISBN 0-674-70485-1

To the memory of Karm Narayan Bahl

Contents

Foreword, by Irven DeVore Preface xiii Introduction 1 TUPAIIDAE (Tree Shrews)

xi

35

Anathana ellioti (Madras tree shrew) Tupaia glis (Common tree shrew) Tupaia nicobarica (Nicobar tree shrew) LORISIDAE (Lorises and Galagos)

47

Loris tardigradus (Slender loris) Nycticebus coucang (Slow loris) CERCOPITHECIDAE (Macaques, Langurs or Leaf Monkeys, and Baboons) 63 Macaca arctoides (Stump-tailed macaque) Macaca assamensis (Assamese macaque)

Macaca fascicularis (Long-tailed macaque)

88

Macaca mulatta (Rhesus macaque)

97

Macaca nemestrina (Pig-tailed macaque)

175

Macaca radiata (Bonnet macaque)

191

Macaca silenus (Lion-tailed macaque)

217

Macaca sinica (Toque macaque)

223

Presbytis cristatus (Silvered leaf monkey)

227

Presbytis entellus (Hanuman langur)

234

Presbytis geei (Golden langur)

271

Presbytis johnii (Nilgiri langur)

278

Presbytis melalophos (Banded leaf monkey)

292

Presbytis obscurus (Spectacled leaf monkey)

295

Presbytis phayrei (Phayre's leaf monkey)

298

Presbytis pileatus (Capped langur)

301

Presbytis senex (Purple-faced langur)

304

Rhinopithecus roxellanae (Snub-nosed monkey)

310

HYLOBATIDAE (Gibbons and Siamangs)

313

Hylobates hoolock (Hoolock gibbon)

315

Hylobates lar (Lar gibbon)

319

Appendix

330

Bibliography Index

413

337

Figures 1. Map of South Asia.

1

2.

World distribution of living primates.

6

3.

South Asian mean daytime temperatures, January.

24

4.

South Asian mean daytime temperatures, July.

25

5.

South Asian mean annual rainfall.

26

6.

South Asian forest types.

27

7.

Sites of recent field observations of Tupaia and Presbytis, India and Ceylon.

32

Sites of recent field observations of Macaca, India and Ceylon.

33

8.

9. Approximate geographical distribution of South Asian members of the family Tupaiidae.

35

10. Approximate geographical distribution of South Asian members of the family Lorisidae.

47

11. Approximate geographical distribution of South Asian members of the genus Macaca.

64

12. Approximate geographical distribution of South Asian members of the genus Presbytis.

65

13. Approximate geographical distribution of South Asian members of the genus Rhinopithecus.

66

14. Approximate geographical distribution of South Asian members of the family Hylobatidae.

313

Foreword

Nowhere has the ancient relationship between human and nonhuman primates been more intimate and complex than on the Indian subcontinent. Protected for centuries by the Hindu belief that all creatures carry a spark of divinity and must not be killed, and abetted by the Hindu legend that the monkey god Hanuman and his monkey army helped Prince Rama recapture his bride Sita, macaques and langurs still swarm through the parks, temples, and bazaars of many Indian cities with the impunity of pigeons in Central Park or Trafalgar Square. This much is known by any tourist who has fed an importunate rhesus beggar, or watched a group of monkeys harassing a fruit merchant. In the following pages, however, the reader will also learn that even the tree shrew (Tupaia glis) may forsake its traditional forest habitat to live in human dwellings. Other species show similar evidence of their long association with humans; stump-tailed macaques, for example, who are normally quite noisy while feeding, may resort to "adaptive silence" for as long as an hour while raiding orchards that are guarded. Residents of Western cities, whose opportunities to observe animal behavior are usually confined to sparrows and pigeons, squirrels and rats, can only envy our Indian colleagues' ready access to such a fascinating and varied fauna. We join them in the hope that, as the needs of the human population increase and the traditional protection afforded by religious belief wanes, new methods will be found to conserve and protect this rich heritage.

This volume on the primates of South Asia is timely and welcome, the result of collaboration between two scholars eminently qualified to undertake it. M. L. Roonwal, formerly Professor of Zoology, Jodhpur University, and Director of the Zoological Survey of India, is well known for his decades of research and numerous publications on the mammals of India and Burma. His colleague at Jodhpur, S. M. Mohnot, has conducted field research on primates in India since 1967, especially on langur behavior in the Rajasthan region. Together they have produced an exhaustive and authoritative survey. A compendium such as this, with summaries of the key references on the behavior and ecology of South Asian primates (including many that are not readily available in American libraries), has long been needed by field workers, laboratories, and research libraries. The authors are to be especially congratulated for circulating drafts of the various chapters to appropriate scholars and incorporating current, sometimes unpublished, information. The result, as the authors acknowledge, is as much an index of our ignorance as our knowledge of most species and many aspects of primate behavior. Not surprisingly, descriptions of the frequently studied rhesus and common (hanuman) langurs occupy a disproportionate amount of space, while information on, for example, the toque and lion-tailed macaques is very sparse—this despite the fact that the latter is seriously threatened by extinction. It is also ironic that much of our understanding of even rhesus macaque behavior still depends to a great extent on the many studies carried out on Cayo Santiago, Puerto Rico, a transplanted, protected, and provisioned colony with a population density at least an order of magnitude greater than rhesus populations in the Indian forests. This book will not only help focus field work on the remaining lacunae in the oft-studied primates such as rhesus, but should also stimulate research on the many South Asian species on which work has scarcely begun. Such research will necessarily require the work of many. International collaboration can greatly enrich such projects; a recent example is the understanding gained by the different perspectives on hanuman langur behavior contributed by Japanese, Indian, British, and American primatologists. For this summary of our present knowledge, and for their many efforts to facilitate primate research by the international community, we are greatly in the debt of our colleagues in India. Cambridge, Massachusetts January 1977

Irven DeVore

Preface

Within the present-day geographical range of primates (mainly the tropical and subtropical belts, comprising South America, Africa, and Asia), nowhere is there a greater concentration of a variety of species and forms than in the relatively small area known as South and Southeast Asia. In South Asia, which includes the landmasses of Afghanistan, Pakistan, India, Bhutan, Nepal, Ceylon, Bangladesh, and Burma, there are as many as twenty-five different species of living primates. This number includes three treeshrews (Tupaiidae) and two lorises (Lorisidae) and, if we exclude these, twenty species of monkeys and lesser apes. Few branches of biology have excited greater interest in the last fifteen or twenty years than the study of behavior, and within this field the study of primate behavior and sociobiology has perhaps attracted the greatest attention. These studies require investigations both in the wild state as well as in captivity under controlled or semicontrolled laboratory conditions. Investigations in large, free-ranging colonies, sometimes comprising several hundred individuals, of exotic species introduced in suitable and favorable habitats (as, for example, colonies of the rhesus macaque, Macaca mulatto., introduced from India to the Cayo Santiago Island in the West Indies) have also proved to be highly successful for such studies. The reasons for this heightened interest are many. Primate

Preface / xiv

studies affect many disciplines of science such as biology, psychology, anthropology, physiology, and medicine. They also throw light on both the ontogeny and phylogeny of the behavior of primitive and modern man. For instance, the urge to dominate, or to be aggressive—a basic requirement for maintaining a home range or territory (extended in many cases to a home country)—may be traced back to its origin in our primate progenitors. As a consequence of this interest in the study of primates, the increasing flood of published literature—papers, books, proceedings of international and regional conferences, and so on—is overwhelming. This enormous mass of literature, published in many different places and languages and in diverse ways, makes it difficult to get a consolidated picture, and that is one of the justifications for writing this book. We have restricted this volume to South Asia partly because it is a rich representative region in itself and also because of our greater familiarity with this region than with others. A word of explanation on the general arrangement of this book is called for. The object of the Introduction is to present not an exhaustive discussion but a short introduction to selected topics, such as primate characters and classification, geographical distribution, aspects of reproduction, social organization, and mother-infant relations, so that the more detailed accounts of individual species which follow the Introduction are not seen in isolation but understood against a more general background. In the main body of the book the twenty-five species occurring in South Asia are dealt with one by one in some detail. For each species we have given the first published valid name and authority as well as vernacular names, followed by the alternative names used by various authorities, to facilitate consultation of the older literature. Full synonymies are not given; however, they may be found in the works of the authorities mentioned under each species. Even the most recent literature contains controversies over correct names. To those who are not familiar with the complexities of taxonomic nomenclature, the alternative names given here should prove helpful. While changes of well-established and familiar names might appear maddening to some, it should be remembered that the aim of these changes is to arrive at stability. To take an example: Pocock has done a great deal for the elucidation of the taxonomic problems of South Asian macaques and langurs (his Cercopithecidae and Colobidae respectively), and his

Preface / xv

findings are s u m m a r i z e d in the first volume (1939) of his f a u n a l work on the Indian m a m m a l s . However, his conclusions on the colobid genera require substantial changes. He assigns the I n d i a n colobids to four genera, namely, Semnopithecus Desmarest (the entellus group), Trachypithecus Reichenbach (the pileatus-group, or the cristatus-group of some authors), Kasi Reichenbach (the senex group) a n d Presbytis Eschscholtz (the aygula group). Recent authorities, however, agree in placing all these groups of species u n d e r the single genus Presbytis Eschscholtz. Even in recent publications some mixing u p continues to occur, though for different reasons—mainly ignorance or oversight of simple taxonomic rules a n d practices. Thus, in a recent account of the noninsect pests of agriculture in India, Srivastava (1964, p. 419) refers to the rhesus m a c a q u e , Macaca mulatta, as two species: " T h e c o m m o n monkeys of N o r t h e r n India, (Rhesus macaque a n d Macaca mulatta Z i m m e r m a n ) . " Following the taxonomic references are brief particulars regarding the external characters (including size a n d weight) a n d geographical distribution, as well as a systematic note listing the subspecies occurring in South Asia. Next follows a detailed account of ecology, sociobiology, behavior, which is generally divided into two sections, "In the Field" and "In Captivity." The purpose of this division is to emphasize the intrinsic importance of distinguishing between social behavior in a n a t u r a l or wild state and artifacts t h a t often develop u n d e r confined a n d u n n a t u r a l conditions in the laboratory even in relatively large cages. One should not, however, suppose that observations u n d e r confined conditions are of no value. For certain aspects of social relations, especially where dyads are involved, such as m o t h e r - i n f a n t relations, these observations in confined conditions have yielded valuable clues to behavior mainly because the desired experiments can be designed a n d carried out w i t h m u c h greater ease a n d precision t h a n is possible in the wild state. In each section, the topics dealt with are h a b i t a t , food, and drink; daily r h y t h m of activity; territory and h o m e range; movements; social groups and their composition; reproduction and reproductive behavior; breeding seasons; interaction within groups (including such aspects as m o t h e r - i n f a n t relations a n d relations between other m e m b e r s of a group); f o r m s of social communication such as vocalization, expressions, gestures, a n d postures; dominance hierarchies; grooming; play activities; interac-

Preface / xvi

tions with other groups of the same species, primates of other species, and other animals including predators; hybridization; and longevity. Under a small "Miscellaneous" section, mention is made of information on topics such as anatomy and biomedical aspects, especially diseases occurring in the wild state. In the literature on primate behavior, to express the organized and more or less permanent assemblies of individuals usually composed of a few to a hundred or more individuals of various types and frequently with an established dominance hierarchy, a number of terms have been used: troups, troupes, troops, groups, schools, bands, parties, and so on. For these more or less stable and semipermanent assemblies we have used the word "group" throughout. In the present state of our knowledge a species-wise approach was considered more appropriate and profitable than a purely comparative account. Depending upon the amount of published information available, each species has been dealt with briefly or extensively. Lacunae in our knowledge are thus highlighted. One of the best general accounts of primate life, including behavior, is the small book Primates by Eimerl and DeVore (1966) in the Life Nature Library series. In that same series is a work which is appropriately complementary, the equally well-written and illustrated volume, Early Man by Howell (1966), in which the evolution of man from the nonhuman primates is traced. The account of primates in Grzimek's Animal Life Encyclopedia, edited by B. Grzimek, volume 10 (1972), also provides a very readable and entertaining yet authoritative account of the life of living primates. For the more specialized reader, the review of primates, including their classification, in the chapter entitled "An introduction to primates" by Buettner-Janusch (1963) in the book Evolutionary and Genetic Biology of Primates, volume 1 (edited by the same author), and the more massive volume, the Handbook of Primates by Napier and Napier (1967), will be helpful. The completion of this book would not have been possible but for the generous and unstinted help we received from a large number of persons and institutions. The prompt and altogether generous service rendered by the Primate Information Centre at the University of Washington deserves mention. Without its weekly publication, Current Primate References, which lists current literature, it would have been most diffi-

Preface / xvli cult to keep abreast of the enormous amount of recent work that is being published on primates all over the world. Also, a large number of active research workers promptly supplied us reprints of their recent works, sometimes undergoing considerable trouble and expense in doing so. To the authorities of the libraries of the following institutions we are obliged for the generous loan of books and for other facilities: the libraries of the Jodhpur University, especially the Central Library (Mr. K. L. B. Rai, Librarian), and the Zoology Department Library (Professor S. D. Misra); the Library of the Zoological Survey of India, Calcutta (Mr. S. Ghoshal, Head Librarian), and the Library of the Desert Regional Station, Zoological Survey of India, Jodhpur (Dr. P. D. Gupta, and Dr. T. G. Vazirani, Officersin-Charge). To all of them we express our indebtedness. We are grateful to the following primatologists for their kindness and generosity in reading through some of the sections dealing with individual species and offering comments. We have benefited greatly from their experience, though we must emphasize that the responsibility for the correctness of the statements made, and for any omissions or errors, is entirely ours. Dr. Suzanne Ripley (City College, New York), for the section on Presbytis entellus; Lord Medway (Saxmundham, Suffolk, England; formerly Professor of Zoology, University of Malaya, Kuala Lumpur) for the sections on Macaca arctoides, M. fascicularis, M. nemestrina, Presbytis cristatus, P. melalophos, and P. obscurus; Dr. F. E. Poirier (Ohio State University, Columbus, Ohio) for the section on Presbytis johnii; Dr. I. S. Bernstein (Yerkes Field Station, Lawrenceville, Georgia) for the sections on Macaca nemestrina and Presbytis cristatus; Dr. Mireille Bertrand (Faculté de Médicine de Paris Ouest, Pkris) for the section on Macaca arctoides; Professor C. H. Southwick (The Johns Hopkins University, Baltimore, Maryland) for the field portion of the section on Macaca mulatta; Dr. P. E. Simonds (University of Oregon, Eugene, Oregon) for the section on Macaca radiata; and Dr. Steven Green (The Rockefeller University, New York) for the section on Macaca silenus. Dr. G. H. Manley (Unit of Primate Biology, Birkbeck College, London) generously allowed us the use of his unpublished field observations on Presbytis senex in Ceylon. To Dr. R. W. Thorington (Director of the Primate Biology Program, Smithsonian Institution, Washington) we are indebted for assistance with current bibliographies. Professor G. P. Sharma (Punjab University, Chan-

Preface / xviii

digarh) kindly supplied us useful information on p r i m a t e chromosomes. To the following zoologists, all of the Zoological Survey of India, we are grateful for assistance w i t h literature a n d in o t h e r ways: Dr. B. Biswas, Dr. H. K h a j u r i a , Dr. V. C. Agrawal, Dr. R. P. Mukherjee, Mr. G. D. Mukherjee, a n d Mr. S. Chakraborty. To Dr. P. K. S e n - S a r m a (Forest Research Institute, Dehra Dun) we are obliged for assistance w i t h some references. Finally, we sincerely thank Mr. P a d a m Singh C h a u h a n , J o d h p u r University, for assistance with the m a p s a n d Mr. Ishaq Moh a m m e d , J o d h p u r University, for the o t h e r illustrations. Jodhpur

M. L. Roonwal S. M. Mohnot

OF SOUTH ASIA

Introduction

FIG. 1. Map of South Asia (shaded area). A, Afghanistan; P, Pakistan; I, India; Cy, Ceylon; N, Nepal; Bh, Bhutan; Bd, Bangladesh; Bm, Burma; Ch, China; L, Laos; T, Thailand; V, Vietnam; Cb, Cambodia; M, Malaysia; S, Sumatra; Bn, Borneo.

This book is concerned with the primates of the landmass that we have designated South Asia, extending approximately from 6° to 38° north latitude and from 61° to 100° east longitude (fig. 1). It has an area of about 5,797,018 km 2 and includes the following countries: Afghanistan, Pakistan, India, Bhutan, Nepal, Bangladesh, Burma, and Ceylon (now Sri Lanka). Primates are found all over South Asia except in very high altitudes (above about 2,500 m) and extremely arid regions (the western part of the Thar Desert).

Primates of South Asia / 2 GENERAL PRIMATOLOGY From the evolutionary point of view primates constitute the highest order of mammals. Members of this order are best identified by a combination of characters rather than by one or more unique or exclusive ones. The primates, having evolved from arboreal ancestors, in general retain this characteristic; a few species have, secondarily, returned to a terrestrial habitat. A feature of arboreality is prehensile hands and feet, with thumb and big toe opposable to the other digits, although opposability is absent in tree shrews. Primates usually have five digits on both hands and feet, and each is usually tipped with a flat nail, but some families have a claw on one or two digits. Arboreality has led to a great reduction in the olfactory functions; the snout is reduced and the face relatively flattened. Both eyes look forward and have developed stereoscopic vision. Other evolutionary trends include an increase in the size and complexity of the brain, especially the cerebral hemispheres; progressively more upright stance, with facultative bipedalism; and prolongation of postnatal life. Primates have a complete bony rim around the orbit. The dentition is generally much reduced from the primitive mammalian formula (three incisors, one canine, four premolars, and three molars in each half of the upper and lower jaws). The clavicles are well developed. The stomach is generally simple. The testes descend into a scrotal sac. There are usually only two teats in the thoracic region. Primates range in size from marmosets, which weigh less than a kilogram and can be held in the palm of the hand, to gorillas, which stand almost 200 cm high and may weigh as much as 350 kgClassification Authorities have divided primates into two suborders, the more primitive Prosimii and the more advanced Simiae (or Anthropoidea). The Prosimii, which include tree shrews, lemurs, lorises, and tarsiers, are confined today to Africa, Madagascar, and South and Southeast Asia. Most are nocturnal and arboreal. Their cerebral hemispheres are not highly developed and do not completely overlap the cerebellum. The posterior bony rim of the orbit is a narrow bar beneath which the orbit and the temporal fossa com-

Introduction / 3

m u n i c a t e freely. The lachrymal f o r a m e n is situated outside the m a r g i n of the orbit. The inner incisors of the u p p e r j a w are generally separated by a space. In addition to the thoracic pair, a p a i r of teats m a y be present on the a b d o m e n . All digits are provided w i t h flat nails except the second toe, which h a s a claw. The u t e r u s is two-horned, the placenta diffuse. Tree shrews (Tupaiidae) were formerly placed in the o r d e r Insectívora. Carlsson (1922), the first to emphasize their similarity to primates, regarded t h e m as Prosimii, a n d this view has been accepted by m a n y recent authorities, including Clark (1959), S i m p s o n (1962), Buettner-Janusch (1963b), Napier a n d Napier (1967), a n d Sorensen (1970). A few, however, including E l l e r m a n a n d Morrison-Scott (1951) and Grassé (1955), continue to place tree shrews a m o n g the Insectívora. S t r a u s (1949) m a i n t a i n e d that tree shrews have u n i q u e characters of their own a n d should be placed in an independent order, the Tupaioidea. Recently Luckett (1968, 1969, 1971), on the basis of the morphogenesis of the placenta a n d the fetal m e m b r a n e s of some m e m b e r s of the Tupaiidae, h a s concluded that the family is not closely related to p r i m a t e s b u t " t o the basal stock t h a t gave rise to all the unguiculate orders of e u t h e r i a n m a m m a l s " (1969, p. 419). For recent reviews of the subject, see van Valen (1965), Campbell (1966), a n d Haines a n d Swindler (1972). To discuss the respective merits of these views of the taxonomic position of tree shrews is beyond the scope of the present work; we should say, however, t h a t we regard tree shrews as primitive p r i m a t e s . The Simiae, which include monkeys, apes, a n d man, are higher p r i m a t e s . They are more widespread today t h a n the Prosimii, being found in South a n d Central America, Africa, a n d Asia. They are chiefly diurnal a n d arboreal. Their cerebral hemispheres are usually richly convoluted and cover the cerebellum completely. The orbit is separated f r o m the temporal fossa by a b r o a d vertical plate. The lachrymal f o r a m e n is situated within the m a r g i n of the orbit. The inner incisors of the u p p e r j a w are not separated by a space. There is one p a i r of thoracic teats, none on the a b d o m e n . All digits are provided with flat nails, except in the marmosets, whose digits, except for the big toe, all carry a claw. The u t e r u s is not horned. The placenta is deciduate a n d metadiscoidal. Both suborders of primates, the Prosimii a n d the Simiae, are represented in South Asia. Of the 12 known families (excluding the Hominidae, man), 4 occur in South Asia: Tupaiidae, Lorisidae,

Primates of South Asia / 4

Cercopithecidae, and Hylobatidae. Of the 55 known genera (excluding Homo), 8 occur in South Asia: (Tupaiidae) Tupaia, Anathana; (Lorisidae) Loris, Nycticebus; (Cercopithecidae) Macaca, Presbytis, Rhinopithecus; and (Hylobatidae) Hylobates. Of some 200 known species of recent primates, 25 are found in South Asia. For a classification of living primates, see appendix table A. For more details and discussion, see Simpson (1945, 1962), Ellerman and Morrison-Scott (1951), Fiedler (1956), Buettner-Janusch (1963b), Napier and Napier (1967), Schultz (1969; 1970, Cercopithecoidea), Thorington and Groves (1970a, Cercopithecoidea), Schrier and Stollnitz (1971a), and Chiarelli (1972a). Nuclear cytology has a bearing on genetic and taxonomic differentiation, but the information available on the chromosomes of South Asian primates is limited. It is hoped that cytologists favorably situated for such studies will give more attention to this group. Earlier information is reviewed by Bender and Chu (1963) and summarized by Napier and Napier (1967). More recent works are those of Hsu and Benirschke and of Sharma and his coworkers. The diploid chromosome numbers of primates (including man) vary from 26 to 80. There seems to be no evolutionary relationship, and in the same genus the number may vary widely (Galago senegalensis, 38; G. crassicaudatus, 62), though some generic tendencies appear. Among South Asian primates, diploid chromosome numbers are known for 15 species (see appendix table B). They vary from 42 (Macaca) to 62 (Loris tardigradus). Experimental Use of Primates That the study of nonhuman primates has a close bearing on the understanding of human social and psychological problems is widely realized. Indeed, students of primate behavior have perhaps more often been social scientists, anthropologists, and psychologists than zoologists. In addition to its relevance to the study of social evolution, the study of primates is important in a number of other fields, such as medicine (human and veterinary) and agriculture (protecting crops from primate pests). Biologically, primates provide superb material for the understanding of the morphological, physiological, and even behavioral aspects of h u m a n evolution, especially of early man before the advent of agriculture.

Introduction / 5

Primates have value in experimental research as stand-ins for h u m a n beings. The selection of primates for biomedical experiments depends upon the nature of the experiment, availability of animals, and conditions in the laboratory. To a certain extent, the choice of a species for particular experiments may be guided by its taxonomic and evolutionary position. Ultimately, as Washburn and Harding (1970) pointed out, some strains of laboratory primates may have to be developed. They suggest that the following species would be particularly useful for such purposes: among the primitive primates (prosimians), a species of the genus Lemur; among the Old World monkeys, Macaca mulatto., a cold-adapted macaque (probably M. arctoides), and a species of Cercopithecus (probably C. talapoin)-, among the New World monkeys, Saimiri, Cebus, and Callithrix. Some of the nutritional problems involved in the feeding and maintenance of primates in the laboratory have been discussed by Moreland (1970), Portman (1970), Greenberg (1970), Newberne (1970), Harris (1970), Lang (1970), and Navia (1970). A useful summary of the diseases of primates commonly used for toxicological studies has been given by Vickers (1969). Ecology Primates are confined today to the tropical and subtropical regions of both the Old and the New World, roughly between 40° north latitude and 40° south latitude (fig. 2). This region includes Central and South America, Africa, Madagascar, and South and Southeast Asia. Some monkeys are found in the eastern temperate zone (Japan and China) as well. The Barbary ape in Gibraltar is a relatively recent introduction (sometime before 1704). The Sahara Desert, the Arabian Desert (except for a few coastal areas), the extreme western portion of the Thar Desert, and the southern part of South America are devoid of primates. Primate fossils have been found in Europe and North America. The only areas in which there is no evidence of primates are Australia and the adjacent islands of New Guinea and the islands of Oceania in the Pacific. Early man is an exception—his fossils have been found not only in the temperate region but also in Australia. The habitats of living primates range from almost exclusively arboreal to almost exclusively terrestrial, with many species between these two extremes. The primitive primates—tree

Primates of South Asia / 6

shrews, lemurs, and lorises—are almost exclusively arboreal. Among the higher primates (monkeys and apes), some arboreal species live in the higher levels of forest trees, seldom if ever coming down to the ground, while others live in the lower levels. For convenience, monkeys and apes may be grouped, on the basis of habitat, into the following categories, which on the whole have, however, no phylogenetic significance. (1) Arboreal in higher tree levels: spider monkeys, howler monkeys, orangutans, gibbons, and most of the colobuses and mangabeys. (2) Arboreal in lower tree levels (no higher than about 7 m), only occasionally, if ever, descending to the ground: capuchins (South America), red-tail monkeys, and olive colobuses (Africa). (3) Intermediate, both arboreal and terrestrial, and equally at home in both habitats: langurs and leaf monkeys, chimpanzees, and vervets. (4) Mainly terrestrial (though able to climb trees readily): baboons, macaques, and patas monkeys. Most primates are vegetarians. Some are exclusively so, while others supplement a vegetable diet with animal food such as insects, crabs, mollusks, birds, bird eggs, and even mammals. In addition, several species are known to eat earth, evidently to provide minerals; for the same reason, apparently, hanuman langurs sometimes eat bones from cremation grounds.

Introduction / 7

Generally they choose a wide range of vegetable foods; in fact, many species eat whatever is edible and available in their area during a particular season. But narrow preferences are occasionally seen in the various groups of a species (as, for example, in the Japanese macaque). The eating, seemingly with relish, of the fruit pulp and poisonous seeds of Strychnos nux-vomica, the strychnine tree, by the h a n u m a n langur in India and Ceylon is a case of remarkable adaptation (Troup 1921, Finn 1929, Oboussier and Maydell 1960). In captivity, primates readily adapt to raw and cooked foods with which they are not naturally familiar, such as cow's milk and bread. All primates drink water regularly, but some of them can go without direct drinking for weeks and even months. Food is generally plucked with the hands and then transferred to the mouth, but sometimes it is taken directly by the mouth.

Sociobiology and Behavior The areas to which primate groups are usually attached are broadly of three kinds: a home range, a core area, and a territory. A m a m m a l ' s home range has been defined as " t h a t area about its established home which is traversed by the animal in its normal activities for food-gathering, mating and caring for the young" (Burt 1940). It remains constant, though often overlapping the home range of another group, at least for a time, and does not include the areas traversed during occasional exploration. It often extends vertically as well as horizontally, especially in the arboreal species. Its horizontal extent varies from a few hectares to 20 or more km 2 . Relations between groups occupying neighboring home ranges are generally peaceful, though there are spacing mechanisms such as specific vocalizations. Occasionally there are mutual attacks and severe fights, which sometimes result in social changes such as the defeated group's splitting up. In some species that have large home ranges (baboons and some langurs), one or more smaller areas, core areas, are reserved for more intensive occupation. Here the groups or subgroups mostly live, feed, and rest, and the remaining part of the range is used for occasional foraging or for transit. While home ranges may overlap, core areas do not. Only when a home range or part of it is actively defended can we speak of a territory, a concept originally developed from the study of birds. The existence of territoriality in a strict sense has not been clearly established in primates, though in some cases we may

Primates of South Asia / 8

perhaps speak of an incipient territory. The word "territory," however, continues to be used rather loosely in primate literature. Social Organization Primates live in groups of varying sizes and have varying degrees of social organization. Examples may be found of solitary individuals, of a single pair and its offspring, and of herds as large as two hundred individuals. DeVore (1968, p. 353) lists six main types of primate social groups as follows, although in cases indicated by a question mark, field data are insufficient for assignment to particular types, and in other cases changes occur either during the annual cycle (as in the galago) or during the daily cycle (as in the gelada Theropithecus gelada and the baboon Papio hamadryas) or there is geographical variation (as in some langurs, the baboon Papio hamadryas, and the chimpanzee). 1. Solitary (usually nocturnal and crepuscular). Examples: tree shrews, some lemurs, lorises, tarsiers, galagos (?), orangutans, and preagricultural man. 2. Mated pair with offspring. Examples: indris, avahis, galagos (?), aotes, marmosets, gibbons, and man (family stage). 3. Group with only one male. Examples: patas, geladas, and some baboons. 4. Group generally oriented to one male. Examples: spider monkeys (?), colobuses (?), some langurs, and gorillas. 5. Group with multiple adults of both sexes. Examples: some lemurs, howler monkeys, spider monkeys (?), capuchins, squirrel monkeys (?), macaques, savannah baboons, vervets, mangabeys (?), colobuses, some langurs, geladas, chimpanzees, and man (bands). 6. Unstructured aggregation. Examples: galagos, geladas, some baboons, chimpanzees, and man. In type 1 (solitary), the consort relationship occurs only for the short period when the female is receptive. In type 2, the offspring ultimately separate from the parents and form their own family groups. The larger groups (types 3, 4, and 5) are basically of two kinds, unisexual and bisexual. Unisexual groups may be all-male, as in hanuman langurs, or all-female, as in Nilgiri langurs and occasionally in hanuman langurs, though all-female groups are not common. Unisexual groups consist of adults, subadults, and juveniles but never infants. Tiger (1971) has called attention to the formation of male groups, or male bonding, among humans, but the existence of any evolutionary relationship between such tempo-

Introduction / 9

rary groupings among humans and the more long-lasting all-male (and, rarely, all-female) groups in nonhuman primates is doubtful. Bisexual groups consist of animals of various ages, including infants. Two types (4 and 5) are recognizable: a unimale group, with a single adult male, a number of adult females, and juveniles and infants of both sexes; and a multimale group, with several adult males, a number of adult females, and young of both sexes. Among bisexual groups a further distinction is to be noted. In some species of baboons, unimale units associate with each other to form larger groups, while in others multimale groups may be divided into subgroups (of which one may be central and others peripheral) on a more or less long-term basis, as in rhesus macaques, or for a shorter period (a day or more) because of changed environmental conditions. In some species, as in hanuman langurs, a group forms a single, indivisible social unit. In others, a group is divisible into a core or central population and a peripheral population. This division is largely linked to dominance structure among the various adults, both male and female; those living at the periphery generally are subordinates. From time to time individuals at the periphery and the center may exchange positions as a result of fights, but as long as the stability lasts the division is more or less firm. These social groups are stable for long periods (for several months at least) but even then are not absolutely rigid, and periodically changes take place, especially in large groups, by splitting, coalescence, or desertion; the groups are thus best regarded as dynamic, though not fluid. In some cases, as in rhesus macaques (Lindburg 1969), groups are not closed social units but experience a seasonal exchange of a portion of the adult male population; this male shifting, though socially disruptive, assists in the exchange of genetic material between various groups. In other cases males may desert and live alone. In southern India, Sugiyama (1971) observed that occasionally a bonnet macaque male deserts his group for no apparent reason and may rejoin the group a few months later. In the same species, Simonds (1972a, 1973) noted that a few deserting males may form their own small, virtually permanent cohort of two or three individuals. We may well regard this situation as an incipient stage in the evolution of larger and well-established all-male groups in some primates. Why males desert is difficult to explain. Simonds (1972a) stated

Primates of South Asia / 10

that societies with strong male-male bonds accommodate their growing males better than those with highly individual males. The socialization of young males differs in the two kinds of societies. Where strong adult male associations (which depend on the cooperation of adult males) prevail, young males are integrated into the group's social network, which includes the dominant males. Where very individualistic males predominate, however, young males develop avoidance relationships with the dominant male(s). Among some primates (as in chimpanzees) the basic social unit is a loose association that is highly flexible and is continually reorganized into small associations or bands of varying structures. These form DeVore's type 6. Grouping into societies has some obvious advantages, since it leads to more effective joint defense against enemies and also provides greater mating opportunities and greater communal strength for attack, food gathering, and other such purposes. The groupings are often associated with mutual adjustments between individuals composing a group or subgroup, as the case may be, and result in dominance hierarchies. Strong or absolute dominance, however, does not appear to be a universal feature among primates. Thus, while the existence of dominance has been well established in macaques and baboons, it is weak in leaf monkeys and perhaps absent in the higher apes. Generally the more arboreal Old World monkeys, such as some of the Asian langurs and the African colobus, have smaller groups than the ground-living monkeys, such as baboons and macaques (Jay 1965a). In baboons and some macaques the group may contain as many as 180 individuals, as in rhesus macaques in Afghanistan (Puget 1971). Apart from two or more species of primates living in the same habitat and sometimes feeding on the same trees (sometimes friendly and at other times avoiding each other or actively agonistic, which results in fights), there is a type of interesting interspecies association in which one member of a species attaches itself to a group of another species. The stranger is accepted fully, and the association may last for years. Such a case was observed at Jodhpur, where a male rhesus macaque lived with a group of hanuman langurs for several years. Quantitative studies of contacts and relationships between individuals in a group should yield interesting results. Bernstein (1971c) listed some of the more important features of social

Introduction

/II

responses. These pertain to proximity, contact, social grooming, play, agonistic responses, sexual responses, lip smacking, and maternal care. Individual activity patterns can be studied with respect to inactivity, location, demonstration displays, traveling, eating, object manipulation, and self-directed activity. These patterns apply to studies in the field as well as in captivity. Some aspects of the bearing of sexual selection, dimorphism, and sociosexual signals on primate social organization have been discussed by Wickler (1966, 1967) and Crook (1972); and some general aspects of primate socialization, including theoretical considerations, by Poirier (1972a,b) and Williams (1972). Reproduction Reproductive behavior has considerable bearing on social life, especially in those species in which large groups are formed. Let us first consider the problem of the seasonality of the reproductive cycle. During the last three decades there has been considerable evolution of thought in regard to primates' reproductive cycles. Zuckerman (1930, 1931, 1932a,b, 1933, 1937, 1953) maintained that there is an uninterrupted sexual cycle in monkeys and apes and, further, that this characteristic distinguishes the higher primates, including man, from other mammals. More recently, Bullough (1961) has asserted the same thing. These conclusions were based largely on observations of animals in captivity, and recent work in the field does not support them. An increasing body of field evidence suggests that the reproductive cycle in several species of monkeys, though not in all, is seasonal, and that females are not receptive year-round. Since mutually contradictory definitions of the breeding season are prevalent in the literature, it is advisable to follow a uniform terminology; the terms provided by Lancaster and Lee (1965), given below, are recommended. Annual reproductive cycle: the seasonal distribution of copulations, conceptions, and births in a population. Mating season: the period of the year to which fertile copulations are confined. Birth season: the period of the year to which all births are confined (if there are some months in which no births occur). Birth peak: the period of the year in which a high proportion of births, but not all births, are concentrated. It is important to emphasize that data from confined animals, such as those caged in zoos, where conditions such as space and feeding are highly artificial, cannot properly be utilized for determining a species's annual reproductive cycle. For this purpose

Primates of South Asia / 12

populations living in a wild state and subsisting on natural food should be used primarily. Observations of a large sample should be made throughout the year and repeated for as many years as feasible. When birth dates are based on estimates of the age of young infants (rather than on direct observation of births), they should be accurate at least within a few weeks. (For this purpose, the change of coat color in infants is often useful.) All groups of macaques studied so far show a marked birth season, lasting two to seven months, and some groups exhibit complete cessation of copulation for long periods of the year. Langurs and baboons have been studied less thoroughly, but here also there is some evidence of a seasonality in births, which may also vary geographically within a species. (For a fuller discussion, see Lancaster and Lee 1965.) Dukelow (1970, 1971) has given a summary of some reproductive parameters—such as gestation period, age of maturity, birth season, and length of estrous cycle—of a large number of primates, though in many cases only the genus is mentioned. In view of what has been said above about the reproductive seasonality of several primates, Zuckerman's (1932a) postulate, that the year-round sexual activity of primates is mainly responsible for the stability of primate social groups, is no longer sustainable. It has also been pointed out (Altmann 1962a, 1967b) that the sociability of "prepubescent individuals" on the one hand and the nonsociability of adult females (except during short periods of sexual activity) on the other are additional factors that militate against the acceptance of Zuckerman's postulate. Other aspects of primate reproduction that are of general and comparative interest are the role of dominance and consort arrangements and sex ratios. Dominance plays an important role in the reproductive behavior of individuals within a group. As a rule, the most dominant male has the first choice for copulation, as in rhesus macaques. Males denied access to receptive females may lose rank and regress to inferior, or even infantile, status, and "breeding hierarchies" may arise in which females take part (Chance 1956). Since dominance, large size, and aggression are often positively correlated, these factors play a role in reproductive success (see Trivers 1972, p. 160). They also have a bearing on the flow of genetic characters in a population. In group-living primates, consort arrangements may vary from none, as in bonnet macaques, where the male and the female separate immediately

Introduction / 13

after copulation, to those lasting from a few hours to a few days, as in rhesus macaques. Except for rhesus macaques, information on sex ratios in South Asian primates is very meager. For some theoretical considerations regarding sex ratios, see Trivers (1972) and Trivers and Willard (1973). Much has been written on the nonseasonal, year-round breeding habits of man as opposed to the seasonal breeding of several nonhuman primate species, among which the female is receptive only for very short estrous periods. Comparisons with human beings are always tempting but not necessarily valid, since human social evolution has been complex and has involved not merely biological and physiological factors but also psychological, legal, economic, and religious ones. Maternal and Paternal Relationships That early care of the infant by the mother and other members of the group varies widely among primates is now well established. (For a general discussion, see Chalmers 1972.) Among the cercopithecids, colobus (leaf monkey) mothers are "permissive"—they allow their infants to be freely handled by other members of the group, especially females, while among the cercopithecines, macaque mothers are strict and possessive and do not permit their infants to be handled by others. Again, some primates, like chimpanzees, care intimately for their infants for many years, while bush babies care for them for a few days only. Both maternal and paternal relationships form a part of a series of interactions, known as the affectional system, which constitute the greater part of the social life of primates, and of which five principal types have been recognized: infant-to-mother, motherto-infant, age-mate or peer, heterosexual, and paternal (Harlow and Harlow 1965a, Harlow 1966). Perhaps the most intense and long-lasting of the relationships within a primate society is the maternal one, of which there are two complementary and sometimes hardly separable components, the infant-to-mother and the mother-to-infant relationships, the nomenclature being determined largely by whichever partner plays the active role—for example, the infant's clinging and the mother's holding with her protective arm. Both components are established in the first few months of the infant's life. An infant clings to its mother for its physiological and psychological needs

Primates of South Asia / 14

(milk, body contact, and comfort) and for protection from external threat. All these needs are supplied by a normal mother in abundance and for a long period. The second stage in this relationship is the emancipation stage. Generally after three to five months the infant, because of its curiosity and need to explore the space around it, tends to move away from its mother. The mother encourages this process but always maintains contact with the infant, sometimes physical (for example, by keeping hold of its tail and even pulling it back), sometimes merely visual, and is always ready to come to its aid if need be. In some species the mother may temporarily leave the infant in the care of some other female while she herself is busy feeding or doing some other essential task. Weaning time seems to vary considerably with the species. In rhesus macaques, for example, it begins when the infant is about ten to twelve weeks old, while in hanuman langurs, at eleven to fifteen months; and the process may last for several months. This is a stage of rejection by the mother, which adopts various strategies for the purpose, ranging from simply withdrawing the nipple to putting a finger in the infant's mouth, vocally threatening, and even slapping. For the infant this is a very painful period. Again and again it tries to come to the denying mother. It screams, throws tantrums, jumps in desperation, and indulges in all sorts of tricks. The mother sometimes relents and sometimes remains unmoved. Once the long and painful process of weaning is over, the mother has nothing further to do with her infant, and after a time perhaps does not even recognize it, particularly after a sibling is born, though occasionally the first infant remains with the mother for a time along with the sibling. The rare occurrence of a mother's mating with her son has been recorded, but this is not a case of recognition of their old relationship. A useful review of the ontogeny of mother-infant relationships in macaques may be found in Rosenblum (1971b). By "paternal" relationships among primates we generally mean the interactions taking place in a group between infants and juveniles on the one hand and all adult and subadult males, not necessarily the father alone, on the other. These interactions, which vary widely, have been discussed by Mitchell and Brandt (1972). The following types of interactions have been noticed: No interaction or contact. Examples: tree shrews, bush babies, some lemurs, some New World monkeys (probably squirrel mon-

Introduction / 15

keys at least), and some Old World monkeys (patas monkeys, bonnet macaques, lion-tailed macaques, and to a certain extent hanuman langurs; the last have no interest in newborn infants). Tolerance (no active interaction, but proximity of the young and even contact are tolerated by the adult males). Examples: squirrel monkeys, capuchins, and some Old World monkeys (stump-tailed macaques, long-tailed macaques, Japanese macaques, rhesus macaques, pig-tailed macaques, hanuman langurs, some baboons, lar gibbons, chimpanzees, and gorillas). Friendly interactions (such as approaching, touching, carrying, retrieving, grooming, playing, caring for, and adopting). Such interactions occur in several species, those of the Old World being stump-tailed macaques, long-tailed macaques, Tapanese macaques, rhesus macaques, bonnet macaques, barbary macaques, hamadryas baboons, and chimpanzees. Aggressive interactions (ranging from mildly threatening to chasing, biting, and even killing). Examples: some tree shrews, bush babies, some New World monkeys (howler monkeys, marmosets), and some Old World monkeys and apes (stump-tailed macaques, long-tailed macaques, rhesus macaques, hanuman langurs, and chimpanzees). The various factors that may govern paternal relationships include, for example, infant variables (such as sex, age, and orphaned or defective infants), the paternal variables (such as age and dominance rank of males, number of males in a group, familiarity with the mother, conflict between males, and hormonal factors), the maternal variables (mother's dominance rank, consort relationships, time of year in relation to birth season, mother's state of estrus, social change in a group), ontogenic variables ("identification" or "transference," interest in the group's center, early experience), and other variables, such as "cultural propagation," state of captivity or crowding, kinship, and the ecological nature of the species (terrestrial or arboreal). For a discussion of these factors, see Mitchell and Brandt (1972).

Social Communication Group structure, as well as intragroup and intergroup interactions, is maintained by established forms of social communication, each species having as a rule its own repertoire. These communications are achieved by various sensory means or signals—olfactory, tactile, auditory, and visual. The

Primates of South Asia / 16

signals are used both within the group, for maintaining dominance structure, agonistic interactions, affectional systems, and other social and biological relationships, and between different groups in the area. Though territoriality in the strict sense hardly occurs, home ranges are maintained, and for this purpose social communication is achieved largely by signals; severe fights are not common. Some general aspects of social communication systems of various kinds—such as chemical, optical, tactile, and acoustic—have been discussed by Sebeok (1967). Rioch (1967) wrote about the agonistic behavior of individuals in relation to the social environment, while Fady (1970) has discussed some general considerations of cooperation and communication between primates. Apart from the usual signals, spacing mechanisms between individuals and between groups play an important role in the maintenance of social organization and the development of social behavior (Kummer 1970). Regarding the sensory responses it may be stated that primates, especially the higher ones, differ from many other mammals in that they depend more on visual than on olfactory signals both for orientation in space and for recognition of objects. A very large proportion of the input into the central nervous system comes through the optic nerve. A good deal of communication among primates is done by means of visual signals without any accompanying vocalization or other sounds. Such signals include grimacing, wrinkling and smacking the lips, and baring the teeth. Recent experimental studies on vision have been summarized by De Valois and Jacobs (1971). Hearing is also of considerable importance to primates. Several field and laboratory observations have been made in recent years on primates, especially macaques, to study such problems as the range of hearing, threshold values, and discrimination of frequencies, and a summary of some of these results is given by Stebbins (1971). In all modes of communication except the tactile one, the individual maintains a space around itself. In this total process, ranging from undirected signals such as alarm calls, tactile communication forms the last and most intimate step, since only here must individual space be renounced. The maintenance or renouncing of individual space between two individuals acquires a sharper meaning under special social situations such as domi-

Introduction / 17

nance where the leader, usually a male, maintains around itself a "social space" which normally no group member (except infants and consort females) dares violate; others approach this space with appropriate subordinate gestures. Play Play is a highly significant activity in primates, especially in the younger age groups. Apart from being an outlet for energy, it is an important element in the process of learning. Play activity can be either locomotive or manipulative and often persists even when there is no food reward. While the motor patterns seen during play may be similar to those occurring in other functional contexts, the motivation differs. Play activities occur in the absence of the longlasting motivational factors that normally cause those activities. Thus, when a juvenile mounts another individual in play, the action may have no sexual motivation and does not lead to intromission or ejaculation. Play behavior is sometimes accompanied by the inhibition of certain activities. For example, fighting (which occurs with considerable intensity among primates) is a friendly affair during play, and, while mild biting may occur, severe biting is inhibited. The factors that initiate and control play are complex and far from well understood. But play should not be interpreted merely as a nonmotivational activity, that is, as an activity indulged in only when there is nothing better to do. It exercises an important role in the psychological adjustment of individuals, especially in the younger stages, to various social situations. Play is also a means of learning skills of all sorts, including those required for vital biological functions such as the proper method of mounting a female for achieving successful copulation. Peer-deprived infants, having no chance for play mountings, are unable to mount and copulate normally as adults. The development of learning skills, as in the use of weapons such as stones and sticks, is of interest because these processes may, to a considerable extent, depend on the development of the brain. A good deal of work has been done on the development of learning skills in the higher apes, both in the field and in the laboratory, and the results have been summarized by Rumbaugh (1970). Work done so far on monkeys and the lower primates is limited. Investigative activities, whether in play or otherwise, have considerable bearing on the learning and development of skills and on the achievement of end goals of behavior. These aspects have been discussed by Butler (1965). Reviews by Fantz (1965) on the ontogeny

Primates of South Asia / 18

of perception and by Z i m m e r m a n n and Torrey (1965) on the ontogeny of learning are also of interest for the study of behavior. Anatomical features of species certainly account for similarities as well as differences in the process of learning. For instance, actions that are natural for man and apes may be difficult for monkeys. For apes, which walk on their knuckles, underhand grasping and throwing are easy, while for baboons and macaques, which walk on flat soles, they are difficult. Consequently apes can easily pick u p stones and throw them, but baboons and macaques cannot. Again, brain capacities and specialized structures inhibit the acquisition of certain skills such as the use of tools and speech. The use of the stick by the chimpanzee for collecting termites from mounds in Africa is about the m a x i m u m use of a tool by a nonh u m a n primate, and because of the serious limitations of its brain capacity the chimpanzee may lack the capacity to learn h u m a n language. Thus, as Oakley (1954) and Jay (1968c) emphasized, there are biological limitations in the development of skills. Apes and even small-brained early man used primitive tools, but it was not until the late Pleistocene that large-brained man appeared on the scene and started using tools more skillfully. Perception of Death Whether higher primates have a level of understanding at which they can perceive at least the importance and irreversibility, if not the inevitability, of biological death is a m a t t e r of speculation. It has often been observed that when death occurs, especially when it is sudden, monkeys perceive it at once as an unusual happening, and the group members near the dead one often behave in a somewhat unusual manner. They may give out wails or howls and tend to stay near the corpse. But within a few minutes to an hour, they give up and go away. The mother, however, shows strong attachment to her dead infant, and several cases are known, as for example in h a n u m a n langurs and rhesus macaques, of a mother's continuing to carry her dead infant in spite of its fetid smell, sometimes for as long as a month, when the infant is nothing but dry skin and bones. Studying Primate Behavior The understanding of behavior, whether in individuals or in a society, involves first of all simple, unbiased observations of animals in the natural state or in captivity, as the case may be, followed by

Introduction / 19

appropriate interpretation. To go deeper into the nervous, physiological, psychological, and other mechanisms involved in the expression of a particular behavior pattern, additional study, especially experimental, is necessary. An understanding of the evolutionary background is also helpful. In general animals increase in complexity with progressive evolutionary status, in the following order: lower invertebrates, higher invertebrates, lower vertebrates, higher vertebrates, man. The development of social organization, however, does not strictly follow that pattern. During the several hundred million years that life has been evolving on earth, the problem of social organization has been solved in two different ways—one based on instinct (in the higher invertebrates, such as ants, bees, wasps, and termites, and the simpler vertebrates, from fish to the lower mammals), and the other based on reasoning and symbolic capacities (in at least some subhuman primates and man). There are many books and monographs on the subject. Animal Behaviour: Its Evolutionary and Neurological Basis, by Dethier and Stellar (1963), is a good introduction; the more advanced student will find Manning's An Introduction to Animal Behaviour (1972) extremely informative. The study of behavior in nonhuman primates, particularly in monkeys and apes, has always excited man's interest, probably because these creatures look so human. For this very reason there is always the danger of interpreting their behavior in anthropomorphic terms, a temptation that the researcher must constantly be on guard against. Another temptation is to consider behavior in captivity as normal; this too must be resisted. To start with, we must, as far as possible, endeavor to distinguish between elemental and compound patterns of behavior and utilize the better techniques for studying them when available. Altmann (1965, 1967c) analyzed the principles of study of both elemental and compound patterns, partly with the aid of computers. Compound behavioral patterns are those, whether two or more, that are displayed simultaneously by one monkey and that would otherwise be recorded as elemental. They may not have exactly the same significance as the elemental patterns of which they are composed. An elemental pattern is independent of the occurrence of any compound pattern into which it is incorporated. Two examples help make this clear. A single attack by a rhesus macaque is compounded of elements of locomotion, posture, movements of

Primates of South Asia / 20

the head and face, and vocalization, and these elements may be combined in different degrees of intensity (Sade 1967). In the squirrel monkey, chirping is a compound sound made of two elements, squeaking and twittering, which are constantly heard together (Ploog 1967). Almost all behavioral studies of primates have to be made in the social context. The most important of course are studies of animals in a wild or natural state. Field work is not easy—it demands that the observer stay in the natural haunts of the animals for prolonged periods, and this requires time, money, and sacrifice of comfort. Furthermore, these haunts may be in dense forests or in rocky and desert areas, far away from human habitation. While conducting field studies, one has to keep in mind a whole gamut of phenomena without which the study would be barren or even misleading: adaptation, evolutionary patterns, survival values of actions, causal and triggering mechanisms, reflexes, and so on. As Washburn and Hamburg (1965a) pointed out, such a simple phenomenon as the clinging of the infant to the mother may, as in the gibbons, which jump high in the trees from branch to branch and drop several meters in each jump, have more than ordinary significance. Similarly, fear may be an important element in an animal's actions. Monkeys drinking water from a pool or stream where there are no carnivores or other enemies drink slowly and leisurely, but those drinking from a puddle in the summer that may be the single waterhole for miles around for all animals (including carnivores) do so quickly and with great caution. There are two ways to carry out field observations. One is to record meticulously detailed observations of social groups of a species on whatever behavior is presented to the observer from day to day and hour to hour and then to classify and analyze the observations carried out over a reasonably long period of time—a few months, a year, or even several years. The other method is to focus on a narrow, specific problem—such as mating behavior, vocalization, or mother-infant relations—and direct one's observations to that end, more or less excluding observations on other aspects. In all observations efforts should be made to utilize the best available technique—though it may be emphasized that faithful recording in an ordinary notebook has by no means lost its primary importance. Nevertheless, the camera, the movie camera, and the tape recorder are extremely useful. Another approach that is expected to yield valuable results is to devise field experiments in order to secure answers to specific

Introduction / 21

problems. Such experimentation is necessarily simpler than that undertaken in the laboratory, but conclusions derived from it will have greater relevance to natural behavior than experiments on animals in captivity. Various aspects of these methods of field work have been discussed in recent years by a number of observers—Jay (1968b, analysis of behavior), Hall (1968, social learning), Mason (1968, significance of aggregation, dispersal, and space), Lancaster (1968, social communication), and Washburn and Hamburg (1968, aggressive behavior). Hinde (1973) discussed the design of various types of check sheets for recording field observations. All primates, especially the higher ones, are wary of strangers. In order to study their natural behavior, the observer should become as inconspicuous and familiar as possible so that the animals will treat him as a normal part of the environment. In achieving these aims, the following hints will, we hope, be helpful; other techniques will no doubt be evolved by the observer as experience is gained. The observer should go to the observation site either alone or with one helper at the most, wearing dull-colored clothes. If the local population is capturing or shooting the animals, it is important to avoid dressing like the natives, of whom the animals have learned to be wary. It is best to sit in an elevated position, easily visible, so that the animals can satisfy their curiosity about the stranger in the belief that they are hidden. Since it makes animals uncomfortable to be stared at, one should gaze at other objects as well and try not to point cameras or binoculars at them for extended periods but rather include them in a sweep. One must not pursue the animals directly but walk as if totally unconcerned, and when sitting one should pretend to be immersed in some personal activity such as reading, writing, or eating. If animals are stalked from natural hideouts and the observer is discovered there, they may desert the area; if one sits in the open, one soon ceases to be a suspected stranger, and the animals will eventually come closer. At first one may—if it is necessary—use artificial food such as peanuts or chick-peas to attract the animals and make them feel at home. But constantly supplying food may alter their natural reactions. Although field work is of primary importance, useful information on some specific aspects of behavior can also be obtained, and analyses made, from primates in captivity in the laboratory under controlled conditions. A large amount of experimental work has

Primates of South Asia / 22

been done on the behavior of various primates, including the South Asian species, particularly the rhesus macaques. A summary of the knowledge gained in recent years has been given in four volumes in Behavior of Nonhuman Primates—the first two edited by Schrier, Harlow, and Stollnitz (1965a,b), the third and fourth by Schrier and Stollnitz (1971a,b). While observations of animals in captivity and experimental work designed to provide answers to specific questions can provide invaluable additional information, conclusions should be drawn with caution, for the results may sometimes become distorted because of the unnatural conditions of confinement. In behavioral studies one must often take note of the developmental stage of the individual concerned, especially in infants and juveniles. The designation and grouping of the various developmental stages obviously vary from group to group, and perhaps from species to species, a point emphasized by Hinde (1971). Thus, for example, we may on the basis of Jay's classification (1963a,b; summarized by Hinde, 1971) designate and characterize the following stages in monkeys. Newborn infant (up to 1 month old): goes only a few meters from its mother. Infant I (1-3 months old): wanders up to about 3 m from its mother. Transitional infant (3-5 months old): undergoes color changes; spends less time with its mother, more with peers. Infant II (5-11 months old): plays with peers for several hours each day; eats by itself. Weaning. Young juvenile (second year of life): spends most of its time with peers. In this connection the ontogenic study of Moltz (1971) on vertebrates in general, including primates, is of interest. Behavioral patterns of primates can be (to varying degrees) either individualor group-conditioned. They may be genetically determined (in which case the patterns are likely to have at least some bearing on taxonomic assignment) or they may, at least in part, be correlated with ecology and environment as learned responses. Communication between individuals in a social group is achieved by a variety of means, such as vocalization, expressions of the eyes or of the face as a whole, gestures, movements, and even attitudes and postures, the purpose in all cases being to communicate a message by signals that are understood by the addressee. On the whole, there are broad basic similarities in these signals among the major groups of primates. At the same time, the signals undergo evolution and change, some of them being retained if they have adaptive value and others dropped. Consequently it is to be expected that species that are closely related taxonomically would

Introduction / 23

also show similar signal repertoires and the more distantly related ones would show greater divergences. Studying all these signal repertoires in the field, where opportunities for prolonged, continuous observation are obviously limited, would be difficult and very time-consuming. Fortunately, recent primate studies have shown that behavior in the laboratory under confined conditions is far more similar to field behavior than might ordinarily be expected. It would be useful to distinguish between broad categories of signals and responses that are widely prevalent among primates and those that are more restricted and even group-specific or species-specific. Such behavior patterns as lip smacking, staring, and attacking (slapping, hitting, pushing, biting) are widely prevalent and have a social purpose. Responses such as erecting the penis, ingesting genital secretion, scratching, self-grooming, and masturbating are also widely prevalent but are individual activities and have no apparent social context. Sometimes a behavior pattern may be fairly widespread in a large taxonomic group (a subfamily or a tribe) but absent in some of the species of that group. Thus, grinding or gnashing of the teeth is widely prevalent in macaques, baboons, and other cercopiths but is said to be absent in one species, bonnet macaques (Simonds 1965). It is interesting and not altogether unprofitable to speculate on the lessons that we might learn from the study of the behavior and social life of nonhuman primates for understanding human social evolution and behavior—even of modern man. While fossils give fairly accurate information on early man's body size, brain capacity, state of erectness, and so forth, inferences on behavior patterns, because they leave no mark or hardly any, are much more tenuous. Such inferences have been discussed by Barnett (1957), Hamburg (1963), Jay (1968c), Washburn and Hamburg (1968), Eimerl and DeVore (1968), and Howell (1970). More and more one is led to the conclusion that some of the basic patterns of human behavior—such as aggression, the affectional systems, dominance, and group behavior—require biological and physiological rather than purely psychological and emotional explanations. GEOGRAPHY OF SOUTH ASIA A broad crown of high mountains forms the northern edge of this landmass, comprising the Hindu Kush in Afghanistan and the Himalayas in Pakistan, India, Bhutan, and Nepal. Afghanistan and the

Primates of South Asia / 24

FIG. 3. South Asian mean daytime temperatures (°C), January.

western half of Pakistan are mountainous, as are Nepal (except for the wet southern Terai) and Burma (except for its coastal areas and river valleys). In eastern Pakistan and northwest India lie the great Indo-Gangetic Plains, including the Thar Desert. South of this, jutting into the Indian Ocean, is peninsular India, with its coastal plains and central uplands (the Deccan Plateau). And still farther south lies the island of Ceylon, which also has coastal plains and a central region of highlands. Bangladesh, next to India on the Bay of Bengal, is largely plains, which are often marshy and intersected by rivers and streams. Much of the coastal areas of India, Ceylon, Bangladesh, and Burma lie below sea level and are subject to periodic tidal flooding. The climate of South Asia varies considerably—from temperate to subtropical to tropical (figs. 3, 4). Temperate, even snowbound in many areas, are Afghanistan, western Pakistan, and India along the northern crown from Kashmir eastward through Nepal to Assam. The temperature is cold or very cold in winter (often sev-

Introduction / 25

FIG. 4. South Asian mean daytime temperatures (°C), July.

eral degrees below zero centigrade) and pleasantly cool in summer. The rest of India may be divided into two parts. The northern, continental half is cold in winter, with temperatures often at the freezing point or a little below, and hot in summer, with maximum temperatures as high as 50°C. The southern, peninsular part is almost uniformly hot throughout the year. Except in the mountains, Bangladesh, Burma, and Ceylon are hot and tropical. The climate of South Asia, with the exception of Afghanistan, is profoundly conditioned by the monsoon (fig. 5). Afghanistan, Pakistan, and India west of Delhi (including the Thar Desert) have little rainfall, less than 500 mm per annum. The remainder of the landmass is an area of moderate to heavy rainfall, the heaviest being 10,700 mm in Cherrapunji in the Assam region. However, there are large portions of this area, such as the Deccan Plateau, that should be classified as dry rather than wet. The plains portion of the landmass is cultivated, especially along

Primates of South Asia / 26

FIG. 5. South Asian mean annual rainfall (mm).

river basins and valleys, where there are canal systems, and where underground water is tapped by means of artesian and tube wells and springs. The natural forest cover is being progressively depleted. Hardly a fourth of India can be classed as forest, and this includes considerable portions of open scrub, which is only by courtesy considered forest. The main forest types range from alpine to temperate to tropical deciduous to tropical wet evergreen (fig. 6). (The last has an almost closed canopy and is difficult to penetrate.) There are tidal mangrove forests along the coastline and in the Sundarbans, in the delta of the Ganges and the Brahmaputra rivers.

SOUTH ASIAN PRIMATES A perusal of the published literature, both recent and old, shows that primates are frequently referred to only by their common English names, of which several species have more than one. To

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