Handbook of the Mammals of the World - Volume 3 by Lynx Edicions

INTRODUCTION

Over the course of the past two centuries, there have been a number of publications dedicated to reviews of the Order Primates. The most noteworthy of these were Forbes’s two-volume series of 1896–1897, the monumental work of D. G. Elliot in three volumes in 1913, and the greatest of them all, the eight volume series of monographs by W. C. O. Hill, published from 1953 to 1974, but sadly never completed. More recently, there have been individual volumes that have provided overviews of the primates, of which J. R. Napier and P. H. Napier’s A Handbook of Living Primates of 1967 was the most noteworthy, and inspired many of us in the early days of our careers. Beginning in 1980, Anthony Rylands and I, both of us working on the monkeys of the Atlantic forest region of Brazil at the time, decided we needed a modern volume covering all primates, lavishly illustrated with photos and drawings and covering all aspects of the taxonomy, distribution, behavior, ecology, and conservation of these animals. A year later, in 1981, Rylands was contacted by Stephen Nash, a student of Natural History Illustration at the Royal College of Art, London, who had a passion for primates. Nash had just completed a painting “Darwin and Friends”—Charles Darwin surrounded by representative prosimians, monkeys, and apes—that was commissioned by Professor Robert D. Martin, then at the Anthropology Department of University College London. With a callitrichid field guide in mind, Nash had produced a series of remarkable sketches of marmosets and tamarins. Martin introduced him to Rylands, who in turn contacted me, and I found him a job with the World Wildlife Fund – US, where I was Director of the Primate Program, and we were off and running. Although we have produced a great variety of primate publications and educational material over the years, we never did get around to doing a comprehensive volume on the primates—in large part because we were engaged in so many different primate conservation and research activities under the auspices of the International Union for Conservation of Nature (IUCN) Species Survival Commission (SSC)’s Primate Specialist Group (PSG), which I have chaired since 1977 and for which Anthony Rylands has been Deputy Chair since 1996. In the interim, in 1996 Noel Rowe produced an excellent book on the Order Primates, entitled The Pictorial Guide to the Living Primates, and later, in 2010, converted it into a website called “All the World’s Primates.” In 2004, Matthew Richardson, a Canadian writer fascinated with primates, contacted us with the idea of doing an encyclopedia of primates. We encouraged him and provided modest support to enable him to move this project forward. But our good intentions to produce such an ambitious volume continued to be sidetracked by our many other responsibilities. As it turned out Matt Richardson helped to lay the groundwork for this volume, and he is one of the principal contributing editors. When Josep del Hoyo contacted me in 2005 to discuss a mammal series to parallel his epic, 16-volume Handbook of the Birds of the World, I was intrigued with the possibility, and helped to find the core funding that would enable Lynx to jumpstart the new series. But always in the back of my mind was that this series would provide an impetus to us and a deadline to finally produce the comprehensive primate volume, and, as a bonus, to situate it within the broader context of the mammals as a whole. With Don Wilson and myself as Chief Editors, Lynx produced the first two volumes on the carnivores and the ungulates, and here we are, at long last, with “Volume 3: Primates.” The nonhuman primates are our closest living relatives, with some, the great apes, sharing more than 98% of our DNA. What is more, primates are a prominent and essential component of the fauna of a very large part of the world’s tropical forests. Field studies that provide us with an understanding of their diversity, their habits and habitats, and their role in the maintenance and ecological dynamics of tropical forest ecosystems began in earnest in the 1970s. However, it is only today that we are beginning to understand the importance of primates as seed dispersers and pollinators, as leaf eaters, predators, and prey in the extraordinarily rich and complex environments in which

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Introduction

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INTRODUCTION

they live. Early studies provided us with a rudimentary understanding of the diverse niches they occupy and insights into the adaptive patterns replicated by different species in Asia, Africa, and the Neotropics. In recent years, and especially in the last 15–20 years, we have made enormous progress in our understanding of the diversity of this mammalian Order. Back in the 1980s, there was a general consensus that there were in total about 160 species of primates worldwide. The most recent compilation by the IUCN/SSC Primate Specialist Group, which is reflected in this book, recognizes 16 families, 77 genera, 479 species, and 681 taxa of primates, a dramatic increase that reflects both our rapidly growing understanding as well as our surprising ignorance of this important group of animals. Primates can be divided into the prosimians, monkeys, and apes. The prosimians include the African galagos and bushbabies of the family Galagidae (five genera, 18 species, and 34 taxa), the African and Asian lorises and pottos in the family Lorisidae (four genera, twelve species, and 18 taxa), the lemurs of Madagascar (five families, 15 genera, 98 species, and 102 taxa), and the tarsiers of the family Tarsiidae (three genera, eleven species, and 16 taxa). Monkeys are divided into those from Neotropics, also called the New World monkeys (five families, 20 genera, 156 species, and 204 taxa), and those from Africa and Asia, the Old World monkeys (one family, 23 genera, 159 species, and 270 taxa). The apes, all from the Old World, include the gibbons or lesser apes of the family Hylobatidae (four genera, 19 species, and 24 taxa) and the great apes, the orangutans, Chimpanzee, Bonobo and gorillas of the family Hominidae (three genera, six species, and 13 taxa in all), and of course our own worldwide species, Homo sapiens. The majority of primates are monkeys (70% of the taxa), with the next most diverse group being the prosimians (25% of the taxa) with 15% contributed by the lemurs of Madagascar. Great apes account for only about 2% of all taxa, even though they are the primates that the public knows best. Family

Genus

Species

% of species

Taxa

% of taxa

Africa

110

23%

197

29%

Madagascar

20%

102

15%

Asia

116

24%

179

26%

Neotropics

156

33%

204

30%

African prosimans

Asian prosimians

Malagasy prosimians

20%

102

15%

All prosimians

139

29%

170

25%

Neotropical monkeys

156

33%

204

30%

African monkeys

17%

147

22%

Asian monkeys

16%

123

18%

All monkeys

315

66%

473

70%

Gibbons

3·5%

African apes

Asian apes

Great Apes

All apes

All primates

77*

479**

681**

Prosimians, monkeys and apes in Africa, Madagascar, Asia and the Neotropics.

*The column for the regions, Africa, Asia, Madagascar, and Neotropics, adds up to one more than the total given because Asia and Africa share one genus: Macaca. **The column for the regions, Africa, Asia, Madagascar, and Neotropics, adds up to one more than the total given because Asia and Africa share one species: Papio hamadryas.

The number of recognized primate species has increased dramatically since the 1970s for several reasons. One has been the increasing application of molecular genetic techniques that have modified our perceptions of “differentness”—allowing us not only to detect strong genetic differences poorly manifested in outward appearances and morphology but also when two forms diverged from a common ancestor—thus providing us with a map and chronology of the evolution of the different groups. Forms considered just varieties (races) or even synonyms have now been found to be clearly distinct populations that we can call species. Another reason has been an increasing effort to study primates (and mammals as a whole) because of the devastation of tropical forests that began largely in the 1970s—global demands for timber, crops (e.g. soy and oil palm), and development (e.g. ranching, mining, dams, and settlements) targeting the great tropical forest wilderness areas of South-east Asia (Indochina, Peninsular Malaysia, East Malaysia and Brunei, Indonesia, and the Philippines), Central and West Africa, and Amazonia. In 1970, about 1% of the Amazon forest had been destroyed. Estimates now indicate 20%. Such destruction inspired a search for new primates to better understand the extent of their geographic distributions and to document and save species which might otherwise never even be known to humans. Paradoxically, the destruction of the forests and the construction of highways into remote regions have facilitated this search, providing access to parts of Amazonia and the Congo forests, for example, that were previously inaccessible. As a result of this increased field research and the ever more sophisticated genetic techniques available, 96 primate species and subspecies have been discovered and described since 1990: 47 from Madagascar, eleven from Africa, 16 from Asia, and 22 from the Neotropics. Fifty-five of the primates described since 1990 are prosimians, 40 are monkeys, and one of them is a gibbon. Sixtysix primates have been described since 2000, and many more possibly new species are under study. Even more remarkable, it is not just new species and subspecies that are being discovered, but even new genera, the Dwarf Marmoset Callibella from the Central Amazon in 2003 and the Kipunji Rungwecebus (an arboreal primate with affinities to the terrestrial baboons) from Tanzania in 2006. What is more, increasingly sophisticated genetic data combined with morphological studies has also enabled us to demonstrate relationships among primate genera, and not just species. This has resulted in a number of taxonomic adjustments. Recent examples include: the recognition of the African monkey genera Allochrocebus and Chlorocebus, separating them out from the guenons of the

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INTRODUCTION

Top Countries for Non-human Primate Species Diversity

Primate Endemism in the Most Diverse Countries – SPECIES

Primate Endemism in the Most Diverse Countries – TAXA

Country

Families

Genera

Species

Taxa

Brazil

116

139

Madagascar

102

Indonesia

DR Congo

Colombia

Peru

Country

Families

Genera

Species

Endemism

Madagascar

5/5

15/15

98/98

100%

Indonesia

0/5

2/10

38/56

68%

Brazil

0/5

4/19

61/116

53%

Colombia

0/5

0/13

12/45

27%

DR Congo

0/4

0/18

10/49

20%

Peru

0/5

1/14

6/44

14%

Country

Families

Genera

Taxa

Endemism

Madagascar

5/5

15/15

102/102

100%

Indonesia

0/5

2/10

55/71

77%

Brazil

0/5

4/19

83/139

60%

Colombia

0/5

0/13

17/52

32%

DR Congo

0/4

1/18

15/66

23%

Peru

0/6

1/14

7/50

14%

Our improved understanding of the evolution and diversity of our own mammalian order and its fundamental role in the ecological dynamics of tropical forests (and in the case of baboons, green monkeys, and Patas Monkeys in that of tropical savannas) underlines the importance of protecting primate species not just as components of our evolutionary history but as fundamental components of the health of these ecosystems and consequently the health and wellbeing of human communities in the regions in which they occur. The most recent assessment of the conservation status of the world’s 5487 mammals in 2008 produced alarming results even for those of us who know the situation well and have been working on extinction avoidance for decades. The assessment of the conservation status of primates, carried out by the Species Survival Commission of IUCN and its Primate Specialist Group, in close collaboration with Conservation International (CI), involved a prolonged and exhaustive compilation of relevant information on each species, finalized and discussed in four regional expert workshops held between 2005 and 2008 (Africa, Madagascar, Asia, and Africa, involving more than 150 specialist participants). The IUCN Red List assessment covered 634 primate species and subspecies, and found that 303 were threatened—fully 48%, nearly half of all living primates! Almost 11% were in the category of Critically Endangered (imminent extinction if conservation measures are not taken immediately), including several species that are down to only a few dozen or a few hundred individuals, but which can be saved; 21% were Endangered, and 15% Vulnerable. Sixteen percent were classed as Data Deficient. Many of the species for which information was lacking were those described only recently. Taking into account the dramatic deterioration in the conservation measures for and the protection of wildlife in Madagascar since the change in government in early 2009, and the fact that numerous species were classified as Data Deficient, the PSG held a Lemur Red-Listing and Conservation Planning Workshop in Antananarivo, 9–15 July 2012. Ninety-six lemur taxa were reassessed and a further seven taxa were assessed for the first time against The IUCN Red List criteria. The preliminary results of the Red List assessments were as follows: 23 taxa Critically Endangered, 52 taxa Endangered, 19 taxa Vulnerable, 2 taxa Near Threatened, 3 taxa Least Concern, and 4 taxa Data Deficient. With 91% of all lemurs listed in one of the three categories of threat, this makes lemurs the most endangered larger mammal group worldwide. Overall it resulted in increasing the number of taxa assessed as threatened to 358, an alarming 52% of all primates worldwide. Habitat destruction (including degradation, fragmentation, and outright loss) and hunting are the two major threats to primates. A third factor, of immense significance especially for the African great apes, is disease—the Ebola virus, for example, has devastated populations of gorillas and chimpanzees in Central Africa. These threats vary from region to region. In the Neotropics, deforestation—habitat loss—is the principal threat, but hunting for some of the larger species (for example, spider monkeys, genus Ateles, and woolly monkeys, genus Lagothrix) can eliminate populations even in areas of intact forest such as those that can still be found in western Amazonia. When forests are

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genus Cercopithecus; the division of tarsiers into three genera, Tarsius, Carlito, and Cephalopachus in South-east Asia; and the New World capuchins into two genera, Sapajus and Cebus. The primates are mostly tropical in distribution, with more than 90% occurring north of the Tropic of Capricorn and south of the Tropic of Cancer. Native wild populations occur in 91 countries in four major regions: tropical and subtropical South and Central America and Mexico; mainland Africa; tropical, subtropical, and some parts of south temperate Asia; and the island of Madagascar, which stands as a primate region in its own right. A few countries can be highlighted for their extraordinarily rich diversity of primate species. They are Brazil, Madagascar, Indonesia, and the DR Congo. Brazil is the richest country in primates with 116 species and 139 taxa. Sixty percent of them are endemic, but Brazil has only four endemic genera out of the 19 that occur there. Madagascar’s rich primate fauna is second on the list and is composed of five families, 15 genera, 98 species, and 102 taxa, all of which are endemic. They are all packed into a land area that is only about 7% the size of Brazil and that has already lost more than 90% of its original natural vegetation.

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INTRODUCTION

reduced to fragments surrounded by farms, roads, and towns, hunting and the challenges faced by very small population sizes (e.g. inbreeding, disease, and chance disasters) become the major threats. Thirty-nine percent of all Neotropical primates are now threatened. In East and West Africa, forests are now heavily fragmented, and hunting is a major factor in the once primate-rich forests of West Africa’s Upper Guinean region. Indeed, the first primate extinctions in modern times could occur in Ghana and Ivory Coast, where several regional endemics are down to tiny remaining populations. In both heavily fragmented West Africa and still largely intact Central Africa, there is a widespread and insidious commerce in bushmeat, which has increased enormously over the last two decades, facilitated and encouraged by the gradual penetration of logging companies into formerly remote and inaccessible forests. The phenomenon of the “empty forest” is increasingly common and widespread in West and Central Africa. Thirty-seven percent of Africa’s primates are now threatened with extinction, most of them in the remnant forests of East and West Africa. In Asia, the situation is very severely aggravated by the massive trade in animals, not just for their meat but also their tissues and body parts as essential components of a widespread and deeply rooted culture of traditional medicine and talismans. In the past, this was largely artisanal or at least relatively small-scale; today it has become a major commerce of export and import, with much of it going to an increasingly affluent China. Asia brings together all the major threats: widespread forest loss, degradation, and fragmentation (e.g. timber, rice, oil palm, forest fires), and hunting, both subsistence and commercial—all in the context of a region with the highest human population densities on Earth. Seventy-one percent of the Asian primates are now ranked as threatened with extinction, and quite a few, especially in countries such as Vietnam, Indonesia, and China, hang on only in tiny populations. The forests of Madagascar have suffered a 2000-year history of devastation since the arrival of humans. For the most part, they are now reduced to minuscule patches, and the lemurs that occur there all have small to very small geographic ranges, especially when viewed in global terms. The loss of even a tiny patch of forest there can result in the loss of the remaining habitat of an entire species. Surviving forests are being constantly whittled away and degraded by local populations, which are highly dependent on natural resources for their subsistence—a situation exacerbated still more by the political instability following a coup in early 2009. As already mentioned, the reassessment of the conservation status of the lemurs in 2012 resulted in the finding that 91% are threatened, which is indicative of the severity of the crisis there. Madagascar is also a clear example of the fact that large-scale primate extinctions are not a figment of our imagination, and that they have taken place as a result of human activity in just the past few hundred years. Indeed, since human arrival on Madagascar just 2000 years ago, a minimum of eight genera and at least 17 species of “giant” lemurs (all of them larger than the extant species) have disappeared, some of them perhaps as recently as the late 1800s. IUCN’s Species Survival Commission (SSC) is a knowledge network of some 7000 volunteer members working in almost every country of the world, with more than 120 Specialist Groups and Task Forces. Members of the SSC and the Primate Specialist Group include government officials, protected area managers, wildlife biologists, anthropologists, zoo specialists, and veterinarians. The Primate Specialist Group has been in existence since the early 1960s, and in its current form since 1977. Its principal activities include: 1) the development of action plans and synthetic analyses to review the conservation needs of a species or species group and to recommend conservation action sufficient to ensure long-term survival; 2) the promotion of measures to facilitate the implementation of action plan recommendations; 3) the establishment and maintenance of primate conservation networks, especially through the publication of regional newsletters (Neotropical Primates, Asian Primates Journal, African Primates, and Lemur News) and a journal (Primate Conservation) to divulge information (research, field surveys, taxonomy, biogeography, and analyses of conservation status and threats) vital for conservation measures; 4) the publication of field guides and pocket guides to promote primate ecotourism and an understanding of primate diversity and biogeography; 5) the publication of a series “Best Practice Guidelines” for primate conservation in general, and particularly for great ape conservation (so far aspects have included logging, reintroduction, population survey methods, great ape/human conflict, and great ape tourism); 6) the organization of workshops and meetings to discuss program activities and aspects such as taxonomy and the regional coordination of conservation measures; 7) the compilation and organization of pertinent data and the assessment of the conservation status of all primate species and subspecies through The IUCN Red List process (see www.iucnredlist.org); 8) the biennial production of a list of the world’s 25 Most Endangered Primates, in collaboration with Conservation International and the International Primatological Society (IPS), accompanied by a report explaining the plight of each, and general media outreach to ensure that primate conservation remains in the news; 9) the maintenance of a website that serves as a resource for PSG members, researchers, and the general public, providing information on primate diversity, threat status and current conservation efforts (see www.primatesg.org); 10) the management of a Primate Action Fund fed by an annual grant of US$ 135,000 from the Margot Marsh Biodiversity Foundation, and providing awards of up to US$ 5000 to support and promote primate conservation activities worldwide, through direct conservation action, field research, and publications, as well as supporting workshops and other relevant events; and 11) the continual search for additional resources to fund primate conservation in the field. The PSG is chaired by Russell A. Mittermeier and the Deputy Chair is Anthony B. Rylands, both at Conservation International, and there are two Red List Focal Points, Christoph Schwitzer from the Bristol Zoo Gardens, UK, and Sanjay Molur from Zoo Outreach Organization (ZOO) in Coimbatore, India. There is a section of 115 members which deals specifically with great apes (coordinated by Liz Williamson, Stirling University, UK) and a recently created section on gibbons (coordinated by Benjamin Rawson, Fauna and Flora International, Cambridge, UK), and an additional nine sections for regions in which primates occur (i.e. Brazil and the Guianas, the Andean region of South America, Mesoamerica, Madagascar, West and Central Africa, East and Southern Africa, South Asia, Southeast Asia, and China), each of them with at least one regional vice-chair. The total number of members exceeds 400.

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Much of the work of the Primate Specialist Group over the past 24 years has been made possible by Conservation International, which has housed the Chair and the Deputy Chair over that period and has provided for and facilitated many activities on behalf of primates. These include those mentioned above, and also large-scale protection of many areas of primate rainforest habitat through the Global Conservation Fund (GCF), the Critical Ecosystem Partnership Fund (CEPF), and the Centers for Biodiversity Conservation (CBCs) in South America and Madagascar. It is no exaggeration to say that this support has been instrumental in maintaining the diversity of the Order Primates worldwide, with not a single species or subspecies having gone extinct over that period and indeed over the past century. Now, however, the time has come to begin ramping up our efforts. The more we learn, the more we see how important primates are—as flagship species for education and awareness efforts for rainforests, as pollinators, and as seed dispersers that may even be instrumental in maintaining high carbon sequestration capacity in the forests of Amazonia, Central Africa, and South-east Asia. What is more, as the need grows to evaluate, verify, and monitor the long-term health of tropical forests as part of a new wave of REDD+ projects, a number of primate species will serve as some of the best indicators of forest health (for example, woolly monkeys and spider monkeys in Amazonia; gorillas, chimps, guenons, and colobus monkeys in Africa; and orangutans and langurs in Asia). We know how to keep primates from going extinct. We have developed the methods and have both the experience and the trained personnel to put the right projects in place. What we have lacked thus far is sufficient funding to deploy these experts into the highest priority places with the greatest extinction risk. This differs from many other less studied groups of organisms where either the manpower or the expertise, or both, are still in short supply. For the primates, we have the people and we have the knowledge; what we need over the next five years is at least an order of magnitude additional funding to make it all happen. We are hopeful that this book, published as part of such a prestigious series, will make great strides in helping to stimulate interest in primates, and, in so doing, make a major contribution to the conservation of this important group of animals. With regard to presentation, we organize this volume by family, beginning with the prosimians, which comprise 25% of the living primates. Most of them are lemurs, an extraordinary and diverse radiation of five families—Cheirogaleidae, Lepilemuridae, Lemuridae, Indriidae, and Daubentoniidae—from the infraorders Lemuriformes and Chiromyiformes with 98 living species and 102 taxa inhabiting the island of Madagascar. What is remarkable about the lemurs is that we continue to find new species in spite of the fact that at least 90% of Madagascar’s forests have already been lost, and what remains of their natural habitat covers no more than 50,000–60,000 km2. Indeed, the known lemur fauna has doubled over the past 20 years and the largest number of primates that have been discovered since 1990 have been from Madagascar; 47 of the 96 thus far, and we are aware of at least half a dozen new species that await description. The Cheirogaleidae includes five genera of very small to small nocturnal forest-dwelling species, all of them arboreal. The mouse lemurs (Microcebus) include the smallest of all primates; Madame Berthe’s Mouse Lemur, (Microcebus berthae), which weighs only about 30 g. Most have been discovered only recently. In 1998, only four species were recognized; a further 15 species have been discovered and described since then, and this is one of the genera in which quite a few new species are expected to be described in the next few years. Mouse lemurs range in weight from 30 g to 65 g. In contrast, there is just one species of Hairy-eared Dwarf Lemur (Allocebus). A little larger than the mouse lemurs (c.85 g), it is rare and remains very poorly known. The Giant Mouse Lemurs (Mirza) also show little variation, being represented thus far by just two species, one of which was discovered and described just eight years ago. They are also nocturnal and arboreal, and occur patchily only in the western dry forest region of Madagascar. These lemurs are more than four times the weight of the mouse lemurs, ranging from 290 g to 320 g. The dwarf lemurs of the genus Cheirogaleus, are still very poorly understood. Although we recognize five species in this volume, there are several clades within three of them, and it is highly likely that more species will be recognized in the years to come. They are larger than Microcebus and Allocebus, ranging in weight from 135 g to 458 g. They are also unusual among the primates in that they fatten up and go into torpor during the cold season; at least two species store a large quantity of fat in the tail, increasing their body weight by up to 30%. The last of the cheirogaleid genera is Phaner, the fork-marked lemurs, represented by at least four species, with one more in the process of being described. These are highly active gum specialists, and range in size from 300 g to 460 g. The second family, the Lepilemuridae, is represented by only one genus, Lepilemur. With 26 species it is the most diverse lemur genus, and the second most diverse of all primates, beaten only by the titi monkeys (Callicebus) with 31. Twenty years ago, only five to seven species were recognized but, like the mouse lemurs, many have been described only recently, and several more probably remain to be discovered. They are the smallest of the folivorous primates, weighing from c.600 g to 1·2 kg, and are found throughout the remaining forested areas of Madagascar, where, if not hunted, they can reach very high densities. The Lemuridae has five genera that range from small to medium-large. The family includes the famous Ring-tailed Lemur (Lemur catta), the best known lemur and the primate species most widely kept in captivity, the “typical” lemurs of the genus Eulemur, the ruffed lemurs (Varecia) and the bamboo lemurs (Hapalemur and Prolemur). Lemur catta is the only member of its genus, weighs c.2·2 kg, has a wide range in southern Madagascar, and is the most terrestrial of the lemurs, although it is also very much at home in the trees. The genus Eulemur is widespread in remaining forests in Madagascar. The twelve species are quadrupedal, arboreal, and frugivorous; some of them are diurnal, some cathemeral (regularly active for parts of the day and night). The two species of ruffed lemurs are the largest members of the family, weighing from 3 kg to 3·7 kg, and they are restricted to the eastern rainforests. The most frugivorous of the lemurs, they are among the most heavily hunted, and are Critically Endangered. The two genera of bamboo lemurs, Hapalemur and Prolemur, are very interesting in that bamboo specialists like them are rare among the mammals. The smaller Hapalemur includes five species and are found in the east, the north and parts of the

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INTRODUCTION

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INTRODUCTION

northwest; they range in size from 800 g to 1·5 kg. One species, H. alaotrensis, is the only primate restricted to the reed beds of a single lake. The monotypic Prolemur, the most specialized, is larger than the Hapalemur, weighing in at 2·2–2·5 kg. It is one of the two most endangered primate genera in the world (the other being Rungwecebus from Tanzania), and down to around 200 individuals in patches of the eastern rainforest. The family Indriidae is composed of three genera, and includes the largest of the living lemurs that are among the most spectacular of all mammals. The monotypic genus Indri is the largest, with individuals weighing up to 9 kg, and is the only lemur with a very short tail. It is diurnal and arboreal, only occasionally descending to the ground, and largely folivorous. The Indri’s flagship value for Madagascar is comparable to that of the Giant Panda in China. The genus Propithecus, the sifakas, is composed of nine diurnal, arboreal species that range in weight from 2·6 kg to 7 kg. In contrast to the Indri, all the sifakas have long tails. The third genus is Avahi, the woolly lemurs, of which there are nine species. They are also fully arboreal but, unlike the Indri and the sifakas, are entirely nocturnal and, at 830 g to 1·2 kg, are much smaller. All of the indriids are “vertical clingers and leapers,” jumping from tree to tree in a vertical posture. Their legs are much longer than their arms, and when on the ground they move by bipedal jumps. The family Daubentoniidae is the most divergent of all primates. Although related to the lemurs and, like them, restricted to Madagascar, it is placed in a separate Infraorder Chiromyiformes. Genetic studies have shown that it was the first of the extant forms to split from the other lemurs, early in their evolutionary history, c.66 million years ago. There is only one living species, the Aye-aye (Daubentonia madagascariensis), that weighs c.2·5 kg, but a giant species, the 13- to 14kg D. robusta, may have survived until AD 891–1027 ad. Aye-ayes have a number of very unusual features, including continuously growing incisor teeth (as is found in rodents), huge ears, a very reduced dentition, and a special, skeleton-like, long, middle finger on a ball-and-socket joint that is used to extract insect larvae from tree holes and under bark. The Galagidae and Lorisidae make up the Infraorder Lorisiformes. They are very small to small, nocturnal, arboreal species found in mainland Africa and South and South-east Asia. The Galagidae is composed of five genera, 18 species, and 34 taxa of galagos and bushbabies found in subSaharan Africa, all of them arboreal and nocturnal. There are seven species and 13 taxa of dwarf galagos (Galagoides), some of which are among the smallest of the primates, with weights ranging from 35 g to 200 g. The widespread genus Galago (galagos and bushbabies) has four species and seven taxa that are somewhat larger, ranging from 110 g to 300 g. The two species and four taxa of the needle-clawed galagos (Euoticus) range in size from 200 g to 360 g, while the three species of squirrel galagos (Sciurocheirus) are somewhat larger, with weights from 200 g to 500 g. The largest members of the family are the two greater galagos of the genus Otolemur, which can weigh as much as 1·8 kg. Although most of the Galagidae inhabit tropical rainforest, members of the genus Galago are also found in woodland-savanna habitats, and Otolemur is found mainly in drier biomes. With the exception of a handful of species, the Galagidae remain relatively poorly studied, especially in the rainforest regions of Central Africa. A number of species still await description, and we expect that quite a few more will come to light in the next decade. The Lorisidae are found in both sub-Saharan Africa and tropical Asia, and are represented by four genera, twelve species, and 18 taxa. All are arboreal, nocturnal and insectivorous. The three species and six taxa of pottos (Perodicticus), ranging in weight from 850 g to 1·6 kg, are found in the rainforests of West, Central and East Africa. There are just two species of the smaller Angwantibo (Arctocebus); they weigh 230–465 g. They are restricted to the rainforests of West Africa. All of these animals remain relatively poorly known in the wild. In Asia, the family is represented by two genera: Loris (slender lorises) and Nycticebus (slow lorises). Loris is restricted to south India and Sri Lanka and has two species and six taxa, ranging in size from 85 g to 294 g. The more widespread slow lorises (Nycticebus) range from northeastern India through mainland tropical Asia to Java, Borneo, and Sumatra. There are five species in this genus, but several more have yet to be described. The tarsiers, family Tarsiidae, are a highly distinctive group of very small primates (50–150 g) found only in insular South-east Asia, on the islands of Borneo, Sumatra, Sulawesi, and the Philippines. Although for long classified as prosimians, allied with the non-anthropoid lemurs, galagos, and lorises, they have a number of features which place them with the monkeys and apes, the most pertinent being the lack of a rhinarium, the moist tip to the nose. Lorises, pottos, angwantibos, galagos, and lemurs all have a wet nose, whereas monkeys, apes, and humans do not. Other features which ally tarsiers with the monkeys and apes include the loss of the ability to produce Vitamin C, aspects of the fetal membranes, a mobile upper lip free from the gum, a postorbital plate, and the absence of a tapetum lucidum behind the retina (the membrane that results in eyeshine), which has, rather, a macula lutea (an oval, yellow spot near the center of the retina) and fovea centralis (a small pit in the macula), which provide for sharp central vision. This confounded the classificatory notion of “pre-monkey” primates (the prosimians) and “monkey-like” primates (us, apes and monkeys), and led to a reclassification of the extant species into two suborders: the Strepsirrhini (wet-nosed primates—infraorders Lemuriformes, Chiromyiformes, and Lorisiformes) and the Haplorrhini (dry-nosed primates—the tarsiers, Tarsiiformes, and the monkeys, apes, and humans, the Simiiformes). It has now been shown that tarsiers diverged from other haplorrhines about 87 million years ago, soon after the haplorrhines split from the strepsirrhines. Until recently, they were all included under a single genus Tarsius. However, in 2010, C. P. Groves and M. Shekelle split them into three genera, Tarsius from Sulawesi, Cephalopachus from Borneo, Sumatra, Bangka Island, the Natuna Islands, and Belitung Island, and Carlito from the Philippines. In all there are eleven species and 16 taxa currently described, but this number will increase over the next few years; several other species of the Sulawesi (eastern) tarsiers have already been discovered and await description. The monkeys and apes are divided into two groups: the New World monkeys and the Old World monkeys with the apes, referred to as platyrrhines and catarrhines, respectively. The platyrrhines are so called because of the broad, flat shape of the nose; the catarrhines have narrow nostrils, close together. The Platyrrhini have a number of other features which distinguish them, notably: three premolar teeth (the primitive condition), no bony ear tube, and the zygomatic and parietal

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bones meet at a symphysis on the side of the brain case. Catarrhini have two premolar teeth, an ear tube, and the zygomatic and parietal bones do not fuse, being separated by a symphysis between the frontal and sphenoid bones. Forty years ago, when many of us first became involved in primatology, the Platyrrhini were classified into just two families: the Callitrichidae for the small, clawed marmosets and tamarins, and the Cebidae for the remaining larger New World monkeys. Since the early 1980s, numerous studies in comparative morphology, molecular genetics, and cytogenetics have focused on discerning a more precise and phylogenetically coherent taxonomy at the family level. The number of families recognized has varied from three to five. The Callitrichidae, Pitheciidae (titis, sakis and uacaris), and Atelidae (howlers, spider and woolly monkeys) have been consistently recognized as natural groupings, as have the squirrel monkeys and capuchins in a redefined Cebidae. The callitrichids are closest to the Cebidae and some place them as a subfamily of the same, the Callitrichinae. The origins and evolutionary relations of the titi monkeys and night monkeys are rather more obscure. The titi monkeys have now been settled as being closest to the sakis and uacaris and are placed in the Pitheciidae. The night monkeys have been placed by some as members of the Cebidae, and by others as a tribe, the Homunculini, of the Pitheciidae. The arrangement that we have settled on here recognizes five families, the Callitrichidae (seven genera), the Cebidae (three genera), the Aotidae (one genus), the Pitheciidae (four genera), and the Atelidae (five genera). The family Callitrichidae includes the smallest of the New World monkeys. All have claws rather than nails on all digits except the hallux (big toe), and, with the exception of the very unusual Callimico, all have two molars in each quadrant of the jaw (not the typical platyrrhine three), and twin births. There are seven genera, 47 species, and 62 taxa in total, with a very high likelihood that several remain to be discovered, especially in the vast Amazon region. They are all highly insectivorous and frugivorous, with some specializing on eating plant gums and even including fungi in their diets. The Pygmy Marmoset (Cebuella) has just one species with two subspecies that are widely distributed in western Amazonia. It is the smallest of all monkeys, weighing only c.125 g, and with Callithrix, Mico, and Callibella, it has the “short-tusked condition,” and is perhaps the most specialized gummivore of all Neotropical primates. The monotypic Callibella, the dwarf marmoset, was only discovered in 1996. Callibella humilis is the second smallest of the simian primates, weighing in at 150–185 g, and is found only in a tiny area of the central Brazilian Amazon. Until recently, the Amazonian marmosets (Mico) were lumped with Callithrix. They are mostly Amazonian, with just one species, M. melanurus, extending south into the Brazilian Cerrado (woodland savannah) and Pantanal and into the neighboring countries of Bolivia and Paraguay. They range in weight from 250 g to about 400 g. They eat gums, although their degree of dependence on this food source is less than that of the Atlantic forest marmosets (Callithrix). Fourteen species are currently recognized, and this is one of the genera where new species discoveries are highly likely. The marmosets (Callithrix) are found in the Atlantic forest region of Brazil and the neighboring “Cerrado” and “Caatinga” (i.e. dry forest and scrub). Six species are recognized, ranging in size from 230-450 g. These four genera of marmosets are characterized by a high percentage of gums in their diet, with a specialized dentition (“the short-tusked condition,” with elongated lower incisors) that enables them to gouge holes in trees and lianes to cause the flow of gums. With 20 species and 34 taxa in all, the tamarins (Saguinus) make up one of the larger genera among the primates. They are found over a wide area of Amazonia, with three species extending north-west into non-Amazonian Colombia and Panama. They have a more normal incisor to canine relationship, “the long-tusked condition,” with longer canines and shorter incisors. They also eat gums, but only opportunistically when they are readily available; exuded, for example, due to damage or attack by such as wood-boring beetles. Many of the tamarins are slightly larger than marmosets, they range in weight from 230 g to 630 g, and, as with all the callitrichids, they are diurnal and arboreal. The genus Leontopithecus includes the famous lion tamarins of Brazil. Endemic to Brazil’s Atlantic forest, they are among South America’s most important flagship species and an example of a great success story in primate conservation, having been brought back from the brink of extinction in the 1970s through a concerted international effort that continues to this day. There are four species, one of which, the Black-faced Lion Tamarin (L. caissara), eluded discovery until 1990. They are the largest of the callitrichids, ranging in weight from about 630 g to nearly 800 g. The last member of the Callitrichidae is the enigmatic Goeldi’s Monkey, Callimico goeldii, a monotypic genus found only in small, widely scattered populations in the western Amazon. Since it shares certain features with the larger New World monkeys (it has three molar teeth and gives birth to singletons not twins), it once resided in its own family, the Callimiconidae, and was believed to be ancestral. The findings of a number of genetic studies, however, have placed it as a member of the Callitrichidae; and even show that it is more closely related to the marmosets than are the tamarins. Goeldi’s Monkey is comparable in size to other callitrichids, weighing c.360 g. It is a specialist in its habitat preferences, spending most of its time low in the forest and near the ground in dense foliage, particularly favoring dense patches of bamboo. The family Cebidae includes the capuchins and squirrel monkeys, now in three genera: seven species and eleven taxa of squirrel monkeys (Saimiri); eight species and nine taxa of the robust or tufted capuchins (Sapajus); and 14 species and 16 taxa of the gracile or untufted capuchins (Cebus). All capuchins were considered to belong to the one genus Cebus until 2011, when genetic studies showed that the gracile and robust forms, the former with an ancestry from the Amazon, the latter from the Atlantic forest, had diverged some 6 million years ago. With their distinct morphological differences (the more robust skeleton of Sapajus associated with its destructive foraging and adaptations for durophagy), it became appropriate to classify them as distinct genera. Sapajus has the second-largest range of any New World genus, being found over much of Amazonia, northwestern Colombia, the Atlantic forest region of Brazil, and drier forest formations such as the Caatinga, the Cerrado, and forested portions of the Pantanal, extending as far south as northern Argentina and Paraguay. Cebus is found mainly in Amazonia, but also crosses the Andes into Pacific coastal South America and extends into Central America as far as Honduras. The capuchins are

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INTRODUCTION

the most omnivorous of the platyrrhines, eating a wide variety of plant foods, invertebrates, and small vertebrates. All are diurnal and mainly arboreal, although they go to the ground more than any other New World genera. They are comparable in weight: about 2 kg to nearly 5 kg for the big males. They are also among the seven genera of New World monkeys with prehensile tails, but lack the large pad of volar skin on the tail that is found in the Atelidae. The highly insectivorous squirrel monkeys are the smallest of the non-callitrichid New World monkeys, ranging in weight from 550 g to 1·4 kg. They live in large to very large groups and are widespread in Amazonia extending to central Colombia, and with one species and two subspecies having a disjunct distribution in Costa Rica and Panama. The cebids have large brains in relation to their body sizes. The capuchins are considered the most intelligent of the New World monkeys and some members of the genus Sapajus have a complex tool-use technology, otherwise shown only by the great apes. The night monkeys, family Aotidae, are all of one genus (Aotus), with eleven species, and 13 taxa. Their phylogenetic position amongst the platyrrhines is difficult to discern, and they have been placed in various families over the years. Today, some experts place them with the titi monkeys (Callicebus) in the Pitheciidae. We maintain them as a separate family. These are the only nocturnal New World monkeys, although in some parts of their ranges, for example, in Paraguay and northern Argentina, they are also partially diurnal. They range in size from c.600 g to c.1·45 kg, and are distributed widely over much of Amazonia (but not the Guianas), extending north into Panama and south as far as Paraguay and northern Argentina (but absent from the Atlantic forest). The fourth family of the New World monkeys is the Pitheciidae. Previously including only the sakis (Chiropotes and Pithecia) and uacaris (Cacajao), there is morphological and genetic evidence that also places the titis (Callicebus) in this family. Discoveries of eight previously undescribed titis since 1990 have resulted in this now being the most diverse genus in the world in terms of species. At present, there are 31 of them, and more are likely to be described in the near future. (The African genus Cercopithecus is more diverse overall, having 23 species but 58 recognized taxa when subspecies are included.) Titis range in weight from about 800 g to 1·65 kg. They are diurnal and arboreal, and live in small family groups of a single adult pair. They are found over a wide area of the Amazon basin (but not north of the lower Amazon, or in the Guianas) and the Atlantic forest, and extend into non-Amazonian parts of Colombia, Bolivia, and Paraguay. The sakis (Pithecia) and the bearded sakis (Chiropotes) are strictly Amazonian in distribution. Pithecia is found over much of Amazonia, but Chiropotes occurs only in the eastern part of this vast forest, east of the Rio Negro and north of the middle and lower Amazon on the Guiana Shield. Five species and eight taxa of Pithecia are currently recognized, but a systematic revision currently underway will likely more than double this number. They range in size from 1·4 kg to 3 kg with the largest species, the Buffy Saki (P. albicans) probably reaching 3·5 kg. The sakis are elusive and little known primates. They are frugivores and seed predators, are particularly fond of liane fruits, and are generally found in small groups of 2–4, sometimes six or seven individuals. The bearded sakis (Chiropotes) have five species. Somewhat larger than Pithecia and Callicebus, they range in weight from 2 kg to 4 kg. They live in large groups of as many as 20–30, and are specialized seed predators, with wedge-shaped canines and powerful jaw muscles to break open fruits of the Brazil nut family (Lecythidacae) and the tough fruits of many other tree and liane species. The uacaris, or uakaris (Cacajao) are the only New World monkeys with a short tail. They are exclusively Amazonian in distribution, being found mainly in western Amazonia in an area largely complementary to that of Chiropotes. The uacaris are similar to the bearded sakis in many ways, being comparable in size (2–4·5 kg), living in large groups, and specializing on the seeds of unripe fruits. Three species and seven taxa are currently recognized, but several more may be discovered in the near future. The last of the New World families, Atelidae, includes the largest of the South and Central American monkeys and is currently divided into five genera: the howlers (Alouatta), with twelve species and 19 taxa; the spider monkeys (Ateles), with seven species and 15 taxa; the woolly monkeys (Lagothrix), with three species and five taxa; the Peruvian Yellow-tailed Woolly Monkey (Oreonax), with only one species; and the muriquis (Brachyteles), with two species. All five genera have a prehensile tail with a pad of volar skin on the ventral surface of the tip, and all but the howlers are brachiators, moving through the trees both quadrupedally and by swinging by their arms below branches. The difference between the brachiation of these Neotropical genera and that of the gibbons is in their use of the prehensile tail. Alouatta also has a strongly prehensile tail, but locomotion is mainly quadrupedal and above branch, with the tail used mainly in postural behavior while feeding. By far the largest of the New World monkeys, these animals weigh from c.4 kg to c.10 kg, with the muriqui, which reportedly can reach 14–15 kg, being the largest non-human primate in the Neotropics. All are diurnal and arboreal, with Alouatta descending to the ground to move between patches of forest more often than the other genera. Alouatta is also a good swimmer and regularly crosses rivers; the other four genera cannot swim, so rivers form barriers delimiting the ranges of the species. The howlers (Alouatta) are quite different from the other Atelidae in their locomotion and morphological features. They have an enlarged hyoid bone that forms a voice box and enables them to produce loud roaring vocalizations. They are the most folivorous member of the family and also the most wide-ranging of any Neotropical monkey genus, being found from southern Mexico through Central America and the west (Pacific) coast of South America as far south as northern Peru, through the Venezuelan Llanos (Orinoco savannas), Amazonia, the Atlantic forest, all of the Cerrado and Pantanal of Brazil, to Bolivia, Paraguay, and northern Argentina. Howlers are highly adaptable and able to survive in a much wider range of habitats, and are more resistant to hunting and forest degradation and fragmentation than other atelids. The more agile, long-limbed spider monkeys (Ateles) have not been subjected to an in-depth taxonomic revision since 1944, and there are almost certainly new species to be described. The genus has a wide range that includes most of Amazonia, the forests of the Pacific coast of Ecuador and Colombia, and all of Central America, extending north as far as the Mexican state of Tamaulipas, the northernmost distribution of any Neotropical monkey. Spider monkeys are the most frugivorous of the New World monkeys. In Amazonia, they are found almost exclusively in intact

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tropical rainforest, but in Central America and Mexico they occupy a wider range of habitats, including tropical dry forests. Like Ateles, the taxonomy of Lagothrix is in need of a modern revision, and new species of woolly monkeys will likely be described. Woolly monkeys are found in western Amazonia, with one species extending north along the foothills of the Eastern Cordillera of the Andes into central Colombia. Spider monkeys and woolly monkeys are heavily hunted for food and for pets in Amazonia, and have been wiped out in many forests that are otherwise still largely pristine. The distinctive Peruvian Yellow-tailed Woolly monkey (Oreonax), was included in the genus Lagothrix until 2001. It has a very limited range in the mountains of the northern Peruvian Andes, and is the largest mammal endemic to Peru and an extremely important flagship species for wildlife conservation in that country. The muriquis (Brachyteles) are restricted to the Atlantic forest region of Brazil between the states of Bahia and Paraná. At one point, the muriqui was considered monotypic, but it was divided into two species in 1993. Being the largest of the Neotropical primates and the largest mammals endemic to Brazil, they, like the Peruvian Yellow-tailed Woolly Monkey in Peru, are extremely important flagship species for the Atlantic forest and for the country as a whole. The family Cercopithecidae, the Old World monkeys or Catarrhini, is the largest of all primate families, with 23 genera, 159 species, and 270 taxa. It is divided into two subfamilies, the Cercopithecinae and the Colobinae, which some authors prefer to recognize as separate families in their own right. The Cercopithecinae includes the macaques, the baboons, drills, and mangabeys, the green monkeys, and the very diverse guenons (13 genera in all), while the Colobinae has within it the the Asian langurs and the African colobus monkeys (ten genera). The macaques (Macaca) are divided into 22 species and 37 taxa, and have the widest range of any non-human primate genus; from Pakistan and Afghanistan through all of tropical and subtropical Asia, and a significant part of temperate Asia as well, extending well into China and as far north as Japan. They occur in the greatest variety of habitat types; from high mountains above 4000 m to dense tropical rainforests, to large cities. It is one of the two non-human primate genera that occur on two continents (actually three if you count Gibraltar, where it once occurred naturally), and the only primate genus that crosses Wallace’s Line into eastern Indonesia, with a radiation of macaque species on the island of Sulawesi and the crab-eating macaque ranging as far east as Halamahera and the Nusa Penida-Timor Island chain, where they may have been introduced. Introduced populations of one species, the crab-eating macaque, are also now established on Mauritius, on Palau in the Pacific, and even around Jayapura on the island of New Guinea. The one African species, the Barbary macaque, occurs in Morocco and Algeria and on the Rock of Gibraltar, and in Africa is the only non-human primate found north of the Sahara. The macaques are sexually dimorphic and medium to large in size, with females ranging in weight from c.4 kg to 9 kg, but males in some species being as large as 18 kg. They are diurnal, strongly omnivorous, and all are at home in the trees; some spend most of their time on the ground, whereas others only go to the ground occasionally to forage. In Asia, they are the most ubiquitous and adaptable of primates, with some species such as the Rhesus and the Crab-eating macaques even living in urban environments. The mangabeys are entirely sub-Saharan in distribution. Until 1978, they were considered to all belong to a single genus, but in 1978 they were split into two: Cercocebus (the capped mangabeys) and Lophocebus (the crested mangabeys). Moreover, genetic studies in the early 1990s showed that the two genera had different phylogenetic relationships with other members of the tribe Papionini: the Gelada, the baboons, the Mandrill, and the Drill. Cercocebus is most closely related to the Mandrill and the Drill whereas Lophocebus is most closely related to the Gelada and baboons. The Kipunji (Rungwecebus) was first described in 2005 as a large (15 kg) member of the genus Lophocebus, but subsequent genetic and morphological studies found that it was quite different and more closely aligned with baboons (Papio) and the Gelada (Theropithecus) than with either of the mangabeys. Mangabeys are medium-sized to large monkeys, ranging in weight from c.4 kg to 14 kg; males are larger than females. The mangabeys and the Kipunji are diurnal and arboreal, although most species regularly descend to the ground to forage. There are seven species of capped mangabeys (Cercocebus), found mainly in Central and West Africa, with two species extending into widely separated forest islands in Kenya and Tanzania. The six species of crested mangabeys (Lophocebus) occur over much the same area. The Kipunji occurs in Tanzania, and has the smallest range of any primate genus; just two tiny forest fragments. The forest baboon genus Mandrillus, the Mandrill and the Drill, has only two species and three taxa and is found only in West Africa, in the countries of Cameroon, Gabon, and Equatorial Guinea. These are the among the weightiest of the living monkeys; large males reach 33 kg, the females are much smaller at 6–13 kg. Mandrills also form the largest social groups of any primate, with more than 1000 animals having been recorded in the forests of Gabon. The baboons (Papio) are one of the most widespread and successful of all primates. They are found throughout sub-Saharan Africa, with one species, the Hamadryas Baboon, crossing over into Yemen and extreme southern Saudi Arabia. Six species and nine taxa are currently recognized. They are found in a wide variety of different woodland savanna and other open country habitats. Opportunistic omnivores, they are generally diurnal and largely terrestrial, but are also at home in the trees. Baboons are large to very large monkeys, and large males of the Chacma Baboon (P. ursinus) can weigh as much as 35 kg. The very unusual genus Theropithecus, the Gelada, has only one species and two taxa, and is restricted to Ethiopia. A diurnal, terrestrial grazer that lives in high altitude grasslands, it too forms very large multimale groups that can reach 260 or more animals; sometimes groups merge to form temporary herds of up to 1000. Like the baboons and mandrills, it is quite large, with adult males weighing as much as 30 kg. Next come the guenons and their relatives, which are now divided into six genera, one of them, Cercopithecus, very large, with 23 species and 58 taxa, and the other five with just one to four species. Until recently, Cercopithecus was even larger. In a review of the taxonomy of the African primates by P. Grubb and coworkers published in 2003, the six species of green monkeys (the so-called Cercopithecus aethiops group) and three terrestrial guenons (the Cercopithecus preussi group) were

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maintained as members of the genus Cercopithecus. However, C. P. Groves in his earlier 2001 review entitled Primate Taxonomy recognized Chlorocebus as a distinct genus, and a molecular genetic study in 2007 showed that they, the Patas Monkey (Erythrocebus), and (separately) the terrestrial guenons of the C. preussi group (Allochrocebus) formed a clade that was basal to the remaining guenons (Cercopithecus) and the talapoins (Miopithecus). His separation of the genus Cercopithecus intro three genera, Cercopithecus, Chlorocebus, and Allochrocebus, is followed here. Allen’s Swamp Monkey (Allenopithecus) is basal to all other guenons, terrestrial and arboreal, and is found mainly in riparian and swamp forest in the DR Congo, Republic of the Congo, and possibly Angola. The two species of Miopithecus, the talapoins, are the smallest of the Cercopithecidae; females weigh 750–1100 g and males weigh 1·2–1·4 kg. They occupy a similar ecological niche to the squirrel monkeys of South and Central America. The Patas Monkey (Erythrocebus) with one species and three taxa is a large (females reach 7 kg, males 13 kg), long-limbed, savanna dweller. It is largely terrestrial, and occurs in a wide band across sub-Saharan Africa, mainly in the Sahelian region. Chlorocebus, the green monkeys, are widespread and highly adaptable woodland savanna dwellers that often occupy the same habitats as Papio. Like baboons, they are diurnal, spend a lot of time on the ground, and are opportunistic omnivores, but they are much smaller; females range in weight from about 1·5 to 5 kg, and males from 3 kg to 6·4 kg. Six species and twelve taxa are currently recognized and they have a wide distribution in the drier habitats of sub-Saharan Africa, but are absent from tropical rainforest, except for the very unusual C. djamdjamensis from Ethiopia. One species, C. sabaeus, is also well-established on several Caribbean islands, including St. Kitts and Nevis and Barbados, having been introduced there early in the colonial period. The terrestrial guenons of the genus Allochrocebus (just three species and four taxa) are found in two widely separated parts of tropical Africa. A. preussi has a restricted and patchy range in the western portion of Central Africa in Nigeria, Cameroon and Equatorial Guinea (including Bioko). A. lhoesti occurs on the eastern side of the rainforest in Uganda, Rwanda, Burundi, and the eastern part of the DR Congo, and the Sun-tailed Monkey (A. solatus) in a small area of central Gabon. These monkeys are medium in size: females range from about 3 kg to 4·5 kg, males 4·7–10 kg. They spend much more time on the ground than other guenons, although they are equally at home in the trees. Cercopithecus, the typical guenons, are found mainly in the tropical rainforests of Central and West Africa, with several species extending into eastern and southern Africa, where they occupy both rainforest isolates and drier forest formations. One species, C. mona, is also established on the Caribbean island of Grenada, having been introduced there during the colonial period. They are generally medium to large monkeys, with females ranging in weight from about 2 kg to 4 kg, and males 3 kg to 7·5 kg. All are diurnal and largely arboreal, with some species spending more time on the ground than others. They are opportunistic omnivores, and often form multispecies associations with other members of the genus and with other primate genera as well. These guenons make up the most diverse genus of African monkeys and are also the most diverse primate genus overall, with 23 species and 58 taxa. Next is the subfamily Colobinae, the folivorous monkeys of Africa and Asia. In all, there are three genera, 23 species, and 38 taxa in sub-Saharan Africa and seven genera, 55 species, and 87 taxa in Asia. Their taxonomy is complex and much discussed, with animals sometimes being placed in one genus and sometimes in another and with some experts splitting genera and others lumping them. The arrangement we present here is based on our interpretation of the best information available at this time, but there may well be changes in the future. The African colobines can be divided into three groups, the black-and-white colobus monkeys, the red colobus monkeys, and the monotypic Olive Colobus. At various times in the past, these have all been lumped together in one genus, Colobus, listed as three subgenera of one genus, divided into two genera, Colobus and Procolobus, or split into three genera with the black-and-white colobus monkeys in the genus Colobus, the red colobus monkeys in the genus Piliocolobus, and only the Olive Colobus in the genus Procolobus. We believe that the last-mentioned arrangement, with three distinct genera, best reflects the diversity of these monkeys, and that is the arrangement we use here. The black-and-white colobus monkeys, genus Colobus, are the most widespread and adaptable of the African colobines, and, like all colobines, are largely folivorous. They are diurnal and arboreal and occur across tropical and subtropical Africa, in a wide variety of habitats from tropical rainforest to drier forest types. Black-and-white colobus are large monkeys, females ranging in weight from 5·5 kg to 11 kg, and males 7·6 kg to 13·5 kg. Most are black and white; just one species (C. satanas) is entirely black. Five species and 20 taxa are currently recognized. The red colobus monkeys, genus Piliocolobus, are mainly found in the tropical rainforests of West and Central Africa, with several species occurring in isolated formations in Kenya and Tanzania, and one species on the island of Zanzibar. They are similar in size to the black-and-white colobus monkeys; females weigh 6–9 kg, males 8–12·5 kg. Following a revision by C. P. Groves in 2007, we recognize 17 species and no subspecies. These monkeys are particularly vulnerable to hunting and are even the favorite target monkey for chimpanzee hunting parties; they are in a dire situation in many parts of their range. Indeed, we may already have lost one species, Miss Waldron’s Red Colobus (P. waldronae) from the border area between Ghana and Cote d’Ivoire, which has not been seen in the wild by primatologists in several decades. The last of the African colobine genera is Procolobus, the Olive Colobus, a monotypic species found only in the forests of Upper Guinean West Africa. It is smaller than other colobus monkeys, weighing only 3–5·7 kg. The seven genera of Asian colobines are more diverse than their African counterparts, and their taxonomy has also been in a state of flux over several decades. There are four less diverse genera, sometimes referred to as the “odd-nosed monkeys,” all of them having unusual pointed, upturned, or even pendulous noses. Their taxonomy has been relatively stable over the past few decades, although there has been some lumping and some splitting. The most famous is the Proboscis Monkey (Nasalis) from Borneo, a monotypic genus found in the Nipa palm and mangrove swamps around the coast of Borneo and sometimes extending inland along the larger rivers. This unusual animal is characterized by a long pendulous nose in the males, which is used as a resonating chamber for loud, honking vocalizations. A large species, with males weighing as much as 24 kg, it is also an adept

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swimmer and regularly crosses rivers and even swims out in the ocean to reach nearby islands. There has been much discussion as to whether the smaller genus Simias, the Pig-tailed Langur endemic to the tiny Mentawai Islands off the west coast of Sumatra, should be included as a member of the genus Nasalis or as a separate genus, as has been the case for most of the last few decades. Not even the authors of this book are in agreement as to where Simias should be placed. Although genetically close to Nasalis, it occupies a different niche, being found in tropical rainforest, has a short tail (unlike the long tail of the Proboscis Monkey), exhibits an unusual color dimorphism, and is not markedly sexually dimorphic in size. It is also much smaller, the males weighing only 8·5–8·8 kg (females a little less at 7·0–7·2 kg). For the present, we have taken a conservative position, leaving the one species and two subspecies of Pig-tailed Langur in the separate genus Simias. The other two odd-nosed Asian colobines are found in China and Indochina. The five species and seven taxa of snub-nosed monkeys (Rhinopithecus) are found mainly in isolated montane habitats in temperate and subtropical China (four species and six taxa), with one species found in the montane forests of northern Vietnam, and the last, the recently discovered R. strykeri, also being found in Myanmar and across the border in China. These are quite large monkeys, with males weighing 14–19 kg, and the females 6–10 kg. They live in some of the most extreme conditions occupied by non-human primates. Yunnan Snub-nosed Monkeys (R. bieti), for example, live at altitudes above 4000 m where it snows for a months at a time; in winter they feed largely on pine needles, lichens and bark. The doucs (Pygathrix) are found only in Vietnam, Cambodia and Laos. There are three species, they live in tropical rainforest, and are somewhat smaller than the Rhinopithecus, males weighing in at 8 kg to 12·5 kg, females 4·7 kg to 11·7 kg. All of the odd-nosed monkeys are diurnal and arboreal, with the Chinese Rhinopithecus occasionally going to the ground to forage. The three larger genera of Asian colobines have undergone much taxonomic revision over the past three decades, and there is still no final consensus among taxonomists. Initially these animals were all included in the genus Presbytis. Presbytis was then divided into four genera or four subgenera: Presbytis, Trachypithecus, Semnopithecus, and Kasi. The species within them were moved around as well, some shifting from one genus to another depending on the opinion of the experts involved. The latest arrangement, which we present here, recognizes three genera, Presbytis, Trachypithecus, and Semnopithecus, with the two species previously in Kasi now being included under Semnopithecus. The genus Presbytis is very diverse, with 16 species and 28 taxa. They are the langurs, sometimes called surilis, of tropical South-east Asia, both on the mainland and on the islands of Sundaland, west of Wallace’s line. They are medium to large monkeys, ranging in weight from 4·3 kg to 8·2 kg, and the sexes are generally not dimorphic in size. The genus Trachypithecus, the species sometimes referred to as lutungs, is even more diverse, with 18 species and 32 taxa, and is found from Northeast India, Bhutan, and Bangladesh through mainland South-east Asia and onto the same islands as Presbytis. Langurs of the genus Presbytis are now restricted to Malaysia and western Indonesia. Presbytis differs from Trachypithecus by a number of dental and cranial features (thick enamel, short faces, no supraorbital ridge, and relatively small larynx), and they are distinct genetic clades. Trachypithecus infants have distinct bright-orange-colored infants. The langurs of these two genera are all diurnal and arboreal, and occupy a wide range of forest habitats. Last we have the genus Semnopithecus, which is found in South Asia, including India, Nepal, Bhutan, Bangladesh and Sri Lanka. At one time, all the gray langurs were subspecies of Presbytis entellus, the Hanuman or Bengal Sacred Langur, but this wide-ranging group has now been divided into a number of different species and subspecies, with each taxonomist working on them having a somewhat different breakdown of taxa. The arrangement that we follow here follows the molecular genetic studies of K. P. Karanth and colleagues, who recognize eight species and 15 taxa. The Nilgiri Langur (S. johnii) from southern India, and the Purple-faced Langurs (S. vetulus) from Sri Lanka that have been placed in a separate genus Kasi in the past, are now lumped with the Hanuman or gray langur group in Semnopithecus. For the most part, the Semnopithecus species are large monkeys. The Hanuman or gray langurs exhibit size dimorphism, with males of the Himalayan species reaching nearly 21 kg in weight and females ranging from 9·5 kg to 17·7 kg. So does the Nilgiri Langur of the Western Ghats, with males weighing c.12 kg to nearly 14 kg, and females 10–11 kg. S. vetulus from Lanka, however, is a smaller species with no dimorphism (males and females weigh 3·8– 9·4 kg). All the Semnopithecus species are diurnal. The Hanuman group spends a lot of time on the ground whereas S. johnii and S. vetulus are largely arboreal. Many of the taxa of the Hanuman group are also very adaptable and often live in close proximity to humans and even in cities and temples. The apes are divided into lesser and great apes. The gibbons of the family Hylobatidae constitute the lesser apes, and are found mainly in continental and insular South-east Asia as far east as Java and Borneo, and in North-east India, Bangladesh, Myanmar, Indochina, and extreme southern China. Four genera, 19 species and 24 taxa are currently recognized, and they include some of the most endangered primates on Earth, best symbolized by the Hainan Crested Gibbon, which is restricted to a very small area of the island of Hainan, China, and is down to about 20 individuals in the wild. Largely frugivorous, pair-living, diurnal and arboreal, all gibbons lack tails and are the ultimate brachiators among the primates, moving from tree to tree by swinging by their arms. The three smaller genera can also move by “ricochetal brachiation,” a rapid form of brachiation that has them literally flying through the trees, and is among the most spectacular of all forms of animal locomotion. The much heavier Siamang (Symphalangus) brachiates, but does not display ricochetal brachiation. The genus Hoolock is composed of two small species (c.6–7 kg) found in northeastern India, Bangladesh, and Myanmar. Nomascus has seven species and eight taxa, and is restricted to mainland South-east Asia and extreme southern China (including Hainan). Nomascus gibbons range from 5 kg to 10 kg. Hylobates is the largest genus ranging from southern China through mainland South-east Asia to the islands of Java, Sumatra, and Borneo. There are nine species and 13 taxa, and they range in size from 4 kg to 7·5 kg. The fourth genus, Symphalangus (the Siamang), is monotypic and restricted to Malaysia and Sumatra. It is by far the largest member of the family, weighing in at 9 kg to nearly 13 kg. Last we have the great apes of the family Hominidae—three genera, six species, and 13 taxa— and our own species, Homo sapiens, with just one genus and species and a wide range of variation

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INTRODUCTION

around the world. The Chimpanzees and the Bonobo (Pan), the gorillas (Gorilla), and the orangutans (Pongo) are by far the best known primates, and are among the world’s most important flagship species. The Bonobo (P. paniscus), also sometimes called the Pygmy Chimpanzee (although it is not a pygmy in any sense of the word), is also becoming very well known. The Chimpanzees (P. troglodytes) and the Bonobo are our closest living relatives, sharing with us roughly 98% of our DNA, and the gorillas and the orangutans are not far behind. The gorillas are by far the largest living primates, with males reaching 209 kg and females 98 kg, and are divided into two species and four taxa. They are found in two widely separated parts of Africa, one in the eastern part of the DR Congo (G. beringei graueri) and in the Virunga Volcanoes of extreme eastern DR Congo, Rwanda, and in the Bwindi (Impenetrable) Forest of Uganda (G. beringei beringei), and the other in western equatorial Africa in Gabon, Equatorial Guinea, Cameroon, Republic of the Congo, DR Congo, and the Cabinda enclave of Angola (G. gorilla gorilla), with an isolated subspecies on the Cameroon/Nigeria border (G. gorilla diehlii). Gorillas are diurnal and largely terrestrial, although they are capable of climbing into the trees. The one species of Chimpanzee is divided into four subspecies and occurs from western Uganda and Tanzania across Central and western equatorial Africa, up into the Guinean forests of West Africa and even into drier habitats in Senegal and Mali. Males range in size from 28 kg to 70 kg and females 20–50 kg. The Bonobo, by contrast, is restricted to the “Cuvette Centrale” of DR Congo, south of the bend of the Congo River, and is found only in tropical rainforest. Though sometimes referred to as a “Pygmy Chimpanzee,” it is comparable in size to the Chimpanzee, males weighing from 37 kg to 60 kg and females 27–38 kg. Chimpanzees and Bonobos are diurnal, and are equally at home in the trees and on the ground. The orangutans are found only on the islands of Sumatra and Borneo, with the Sumatran populations belonging to the species P. abelli and the Bornean populations being divided into three subspecies of P. pygmaeus. Males weigh up to 85 kg and females up to 45 kg. They are found only in tropical rainforest, are largely frugivorous, and are the largest arboreal animals on Earth, although they periodically move on the ground. Last, but certainly not least, we have ourselves, Homo sapiens, a single species that occurs on all continents except Antarctica, and is the most adaptable, successful, and destructive mammal on Earth. Given that we would need volumes to describe the amazing behavioral, ecological, cultural, and technological diversity of our own species, we have decided to exclude it from this volume, and to focus instead only on the non-human members of the Order of which we are a part. What should be obvious to the reader after he or she has pored through this extensive text is that it is no longer easy to make generalizations about behavior and ecology, nor to easily categorize primate species and genera into discrete categories, monogamous vs. polygamous, permanently pair-bonded vs. opportunistic, one male vs. multimale groups, folivore vs. frugivore, frugivore vs. omnivore, nocturnal vs. diurnal… and the list goes on. The more we learn about different species in different habitats, and even different populations of the same species, the more we see that there is a great deal of flexibility in their behavior and ecology and the ways in which this fascinating Order of mammals adapts to different environmental conditions. Perhaps this is not surprising, given the great adaptability of our own primate species, Homo sapiens, but it only adds to the overall appeal of the primates. Much of primatology in the early days was based on a desire to learn more about our own evolution by studying our closest living relatives, and certainly such research has provided many extraordinary and exciting results and insights. But as we have progressed in primate studies over the decades, we have found that these animals are extremely interesting in their own right, and worthy of study beyond their value as surrogates for our early ancestors. We hope that this book gives you at least some understanding of how exciting and interesting the primates are, and that it stimulates you to become more involved in their study and their conservation.

Acknowledgements As with all such publications, this has been a collaborative effort involving many contributors and a variety of funding sources, and I would like to recognize them all here. First, I would like to acknowledge those people and organizations that provided the institutional support to make this all possible. My organization, Conservation International (CI), has provided me with the flexibility to work on this project amid all my other responsibilities, and has given both Anthony Rylands and Stephen Nash, also CI staff members, the time to enable them to dedicate themselves to this project over the past three years. My long-term assistants Ella Outlaw and Jill Lucena also provided backup in many different ways, and photo editors Paula Rylands and later Luana Luna were instrumental in locating images for this book from my 40 years of primate field work. I would also like to recognize the IUCN Species Survival Commission in the person of its current Chair, Simon Stuart, and its Senior Scientific Officer, Michael Hoffmann, for their early support of the Handbook of the Mammals of the World (HMW) series, and to Simon and all previous chairs of the SSC going back to Sir Peter Scott, Grenville Lucas, George Rabb, David Brackett, and Holly Dublin for their confidence in maintaining me as Chair of the Primate Specialist Group of this distinguished Commission for such a long time. With regard to financial support from other donors, I first have to acknowledge the late Doris Swanson, of Hayden Lake, Idaho, USA, whose commitment to species conservation over the first decade of this century enabled us to provide the resources to start HMW in the first place and to cover a lot of the field work that is referenced in the species accounts in this book. I would also like to acknowledge the support of the Margot Marsh Biodiversity Foundation, named after another wonderful woman, Margot Marsh from La Jolla, California, USA, whose dedication to primate conservation has resulted in the support of well over a thousand researchers and field projects over three decades and particularly since the creation of the foundation named after her in 1996. The Margot Marsh Biodiversity Foundation provided core support for the production of this volume, without which it would have been impossible to complete. Special thanks to Shawn Concannon of

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Chicago, Illinois, USA, for his long-term support of our species conservation work, now going back 35 years, some of which went into the research behind this volume. Thanks also to Rick Barongi and Peter Riger of the Houston Zoo for their support at a critical moment, to Thomas E. Lacher Jr of Texas A&M University for support to the series as a whole, and to the Department of Anatomical Sciences at the Health Sciences Center of Stony Brook University for providing office space to Stephen Nash for the last three decades, as well as the invaluable opportunity for him to interact on a daily basis with some of the world’s most distinguished physical and behavioral anthropologists, palaeontologists, and comparative anatomists and their students. Over the years, they have included William L. Jungers, Jack T. Stern, Randall L. Susman, Susan Larson, David Krause, Brigitte Demes, Diane Doran, Frederick Grine, Maureen O’Leary, Erik Seiffert, Nathan Kley, Callum Ross, Dan Schmitt, Pierre Lemelin, Christine Wall, Patricia Wright, and especially John G. Fleagle. Concerning the actual writing of this volume, I have to first and foremost recognize the extraordinary commitment of Anthony Rylands, Deputy Chair of the IUCN/SSC Primate Specialist Group and Senior Researcher in Conservation International, who has worked day and night over the the past three years to help complete this book, using his vast knowledge of both primates in the wild and the primate literature. Very special thanks also to Matt Richardson for all the effort that he put into the preparation of multiple drafts of his “Encyclopedia of Living Primates,” which has served us so well in the preparation of this volume. We are also grateful to Colin P. Groves of the Australian National University, Canberra, whose synthesis Primate Taxonomy, published in 2001 by the Smithsonian Institution Press, Washington, DC, provided the backbone for this volume. He has freely given us his immense wisdom and knowledge in dealing with numerous taxonomic issues from the very beginning of this work. Dietmar Zinner and Christian Roos of the German Primate Center (DPZ), Göttingen, Germany, together with Colin Groves, oversaw the largest and taxonomically most complex of the primate families, the Cercopithecidae, and edited, fact checked, and strengthened the species accounts, making us current with the taxonomy and our understanding of the distributions of the 159 species and 270 taxa in the family. Dietmar Zinner, Christian Roos, and Gisela Fikenscher (also in the German Primate Center), most generously and heroically, also took on the task of writing the introduction to the Cercopithecidae very much at the eleventh hour, and for that we will forever be in their debt. The same is true for Stephen F. Ferrari of the Federal University of Sergipe, Sergipe, Brazil, Liliam P. Pinto of the Centro Nacional de Pesquisa e Conservação da Biodiversidade Amazônica, Manaus, Brazil, and Laura K. Marsh, Director of the Global Conservation Institute, Santa Fe, New Mexico, USA, who most kindly agreed to write the introduction and species accounts for the Pitheciidae; again very late in the day did we call on their immense knowledge of the family and their good will in contributing to the volume. Our most sincere thanks also to the other contributors to this book: Madagascar lemurs – Christoph Schwitzer, Bristol Zoo Gardens, UK, and Edward Louis, Jr, Omaha’s Henry Doorly Zoo, Omaha, Nebraska, USA; Galagidae, Lorisidae – Anna Nekaris, Oxford Brookes University, Oxford, UK; Tarsiidae – Myron Shekelle of Bellingham, Washington, USA, and Sharon Gursky, Texas A&M University, Texas, USA; Cebidae – Fernanda Paim and Helder Queiroz, both of the Mamirauá Institute for Sustainable Development, Tefé, Brazil; Aotidae – Eduardo Fernandez-Duque, Margaret Corley and Andrea Spence-Aizenberg, of the Owl Monkey Project, University of Pennsylvania, Philadelphia, USA; Atelidae – Kenneth Glander, Duke University, Durham, North Carolina, USA; William R. Konstant, Flourtown, Pennsylvania, USA, Thomas R. Defler, Universidad Nacional de Colombia, Letícia, Colombia, Fanny Cornejo, Research Program, Yunkawasi, Lima, Peru, and Maurício Talebi, Universidade Federal de São Paulo, Diadema, São Paulo, Brazil; Cercopithecidae – Siân Waters, Moroccan Biodiversity Conservation & Research, Tetouan, Morocco, Martina V. Anandam and Sanjay Molur, Wildlife Information Liaison Development, Coimbatore, India, Antje Engelhardt, German Primate Center, Göttingen, Germany, Erin Riley, San Diego State University, California, USA, Danielle Whittaker, Michigan State University, East Lansing, Michigan, USA, Ardith Eudey, Upland, California, USA, Lori Sheeran, Central Washington University, Ellensburg, Washington, USA, Elizabeth Gadsby, Pandrillus Foundation, Portland, Oregon, USA, Tim Davenport, Wildlife Conservation Society, Mbeya, Tanzania, Aoife Healy, Oxford Brookes University, Oxford, UK, Nicola Davies, Bristol Zoo Gardens, UK, Janette Wallis, University of Oklahoma, Oklahoma, USA, Kate Detwiler, New York University, New York, USA, Nelson Ting, University of Oregon, Eugene, Oregon, USA, Tilo Nadler, Endangered Primate Rescue Center, Cuc Phuong National Park, Vietnam, Elizabeth Bennett, Wildlife Conservation Society, Bronx, New York, USA, and K. Praveen Karanth, Indian Institute of Science, Bangalore, Karnataka, India; Hylobatidae – David J. Chivers, Selwyn College, University of Cambridge, UK, and Benjamin Rawson, Fauna and Flora International, Cambridge, UK; Hominidae – Liz Williamson, University of Stirling, Stirling, UK, Fiona Maisels, Wildlife Conservation Society, Bronx, New York, USA, Blake Morton, University of Stirling, Stirling, UK, Anne Russon, Glendon College of York University, Toronto, Canada, Ian Singleton, PanEco Foundation, Medan, North Sumatra, Indonesia, Tatyana Humle, University of Kent, Canterbury, UK, and Barbara Fruth, Max-Planck-Institute for Evolutionary Anthropology, Leipzig, Germany. On behalf of the individual authors of HMW Volume 3—for help in reviewing early drafts, providing unpublished data, identifying the species in the photographs, providing suggestions for the illustrations, and support in numerous other ways—we would like to extend our sincerest thanks to: Christophe Abegg, Marc Ancrenaz, Christos Astaras, Sirley Baião, Simon K. Bearder, Elizabeth Bennett, Douglas Brandon-Jones, Kelly Boyer, Thomas Breuer, Terry Brncic, Thomas M. Butynski, Genevieve Campbell, Nicola Campbell, J. Bryan Carroll, Susana Carvalho, S. Roy Choudhury, Marina Cords, Jasmine Craig, Nicola Davies, Constance Dubuc, Will Duckworth, Ardith Eudey, Gisela Fickenscher, Denisse Goffard, Maryke Gray, Valerie Hardman, John Hart, Tanja Haus, Gail Hearn, Kimberley Hockings, Jason Hon, Lynne Isbell, Clifford Jolly, Yvonne de Jong, William L. Jungers, Cecília Kierulff, Kathelijne Koops, Hjalmar Kuehl, William C. McGrew, Fanny Mehl, Erik Meijaard, Fabiano Rodriguez de Melo, Bethan Morgan, Stuart Nixon, Felicity Oram, Lisa Paciulli, Jennifer Peers, Elizabeth R. Pimley, Carlito Pizzaras, Andrew Plumptre, Tabitha Price, Rodrigo Cambará Printes, John G. Robinson, Eva Johanna Rode, Heidi Ruffler, Felicia Ruperti, Christina Salibay,

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INTRODUCTION

Sasimar Sangchantr, Crickette Sanz, Carel van Schaik, Nora Schwitzer, Melanie Seiler, Joanna M. Setchell, Arif Setiawan, Christopher Shaffer, Lori Sheeran, Volker Sommer, José de Sousa e Silva Jr, Tara Stoinski, Jacqueline Sunderland-Groves, Jatna Supriatna, Brandon Wheeler, Tony Whitten, Christopher Whittier, and Serge Wich. Anthony Rylands is particularly grateful to Ella Outlaw, Jill Lucena, Stephen Nash, Liz Williamson, and Matt Richardson, who have been a constant source of support, inspiration, kindness, encouragement, and superlative friendliness. In closing, I want to thank the entire team of Lynx Edicions for all that they do to further our understanding of biodiversity in general and of birds and mammals in particular. Josep del Hoyo is an amazing visionary and leader, and his Handbook series on birds, his many other bird publications, his website, and his knowledge and commitment to birds, have made major contributions to conservation. And now, with this Handbook of the Mammals of the World, he is extending his considerable influence to this important Class of vertebrates as well. We particularly thank Albert Martínez-Vilalta, Amy Chernasky, Ana Conesa Parellada, David M. Leslie Jr, José Luis Copete, and Marc Olivé, whose efficiency, expertise, and kindness always impressed, but none so much as their patience. The Lynx team would also like to express their gratitude for the assistance received with the foreign and scientific names for the volume. Normand David and Michel Gosselin (Canadian Museum of Nature) provided the French names. The Spanish names came from the Sociedad Española para la Conservación y Estudio de los Mamíferos (SECEM), for which they would like to especially thank Luis Javier Palomo Muñoz. Gustav Peters and Rainer Hutterer, who provided the German common names, would like to thank Eckhard W. Heymann, Christian Matauschek, Stefan Merker, Ute Radespiel, and Christian Roos for suggestions in this matter. Lynx would also like to thank Jordi Bas for the photo on the front cover of the volume. Lastly, I would like to pay tribute to the late Liza M. Veiga, a researcher at the Museu Paraense Emílio Goeldi (MPEG) and the Federal University of Pará, Belém, Brazil. She was one of the Regional Vice-Chairs for the Neotropics for the IUCN/SSC Primate Specialist Group and a contributor to the Pitheciidae section of this volume. She sadly passed away in late October, 2012. She was much admired and loved by her many friends and colleagues, and she will be missed. Russell A. Mittermeier President, Conservation International; and Chair, IUCN/SSC Primate Specialist Group

References

Brandon-Jones, D., Eudey, A.A., Geissmann, T., Groves, C.P., Melnick, D.J., Morales, J.C., Shekelle, M. & Stewart C.-B. (2004). Asian primate classification. Int. J. Primatol. 25: 97–164. Elliot, D.G. (1913). A Review of the Primates. Monograph Series. Three volumes. American Museum of Natural History, New York. Forbes, H.O. (1896-1897). A Hand-Book to the Primates. Two volumes. Edward Lloyd, London. Groves, C.P. (1978). Phylogenetic and population systematics of the mangabeys (Primates: Cercopithecoidea). Primates 19: 1–34. Groves, C.P. (1989). A Theory of Human and Primate Evolution. Oxford University Press, New York. Groves, C.P. (2001). Primate Taxonomy. Smithsonian Institution Press , Washington, DC. Groves, C.P. (2007). The taxonomic diversity of the Colobinae of Africa. J. Anthropol. Sci. 85: 7–34. Grubb, P., Butynski, T.M., Oates, J.F., Bearder, S.K., Disotell, T.R., Groves, C.P. & Struhsaker, T.T. (2003). Assessment of the diversity of African primates. Int. J. Primatol. 24: 1301–1357. Hill, W.C.O. (1953). Primates Comparative Anatomy and Taxonomy I. Strepsirrhini. Edinburgh University Press, Edinburgh. Hill, W.C.O. (1955). Primates Comparative Anatomy and Taxonomy II. Haplorrhini: Tarsioidea. Edinburgh University Press, Edinburgh. Hill, W.C.O. (1957). Primates Comparative Anatomy and Taxonomy III. Pithecoidea Platyrrhini (Families Hapalidae and Callimiconidae). Edinburgh University Press, Edinburgh. Hill, W.C.O. (1960). Primates Comparative Anatomy and Taxonomy IV. Cebidae Part A. Edinburgh University Press, Edinburgh. Hill, W.C.O. (1962). Primates Comparative Anatomy and Taxonomy V. Cebidae Part B. Edinburgh University Press, Edinburgh. Hill, W.C.O. (1966). Primates Comparative Anatomy and Taxonomy VI. Catarrhini, Cercopithecoidea, Cercopithecinae. Edinburgh University Press, Edinburgh. Hill, W.C.O. (1970). Primates Comparative Anatomy and Taxonomy VIII – Cynopithecinae, Papio, Mandrillus, Theropithecus. Edinburgh University Press, Edinburgh. Hill, W.C.O. (1974). Primates Comparative Anatomy and Taxonomy VII –Cynopithecinae, Cercocebus, Macaca, Cynopithecus. Edinburgh University Press, Edinburgh. Mittermeier, R.A., Ganzhorn, J.U., Konstant, W.R., Glander, K., Tattersall, I., Groves, C.P., Rylands, A.B., Hapke, A., Ratsimbazafy, J., Mayor, M.I., Louis Jr, E.E., Rumpler, Y., Schwitzer, C. and Rasoloarison, R.M. (2008). Lemur diversity in Madagascar. Int. J. Primatol. 29: 1607–1656. Napier, J.R, & Napier, P.H. (1967). A Handbook of Living Primates. Academic Press, London. Rowe, N. (1996). The Pictorial Guide to the Living Primates. Pogonias Press, East Hampton, New York. Rylands, A.B., Schneider, H., Langguth, A., Mittermeier, R.A., Groves, C.P. and Rodríguez-Luna, E. (2000). An assessment of the diversity of New World primates. Neotrop. Primates 8: 61–93.

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FAMILY HOMINIDAE Great Apes

CLASS MAMMALIA ORDER PRIMATES SUBORDER HAPLORRHINI PARVORDER CATARRHINI SUPERFAMILY HOMINOIDEA

Family HOMINIDAE (GREAT APES) • Large apes with relatively short trunk, broad chest, long arms, robust canine teeth, simple molar teeth, long hands and feet, and no external tail; males larger than females. • 70–200 cm.

• Afrotropical and Indo-Malayan Regions. • Lowland to montane equatorial forests, swamps, savanna-woodland mosaic. • 3 genera, 6 species, 13 taxa (excluding humans). • 2 species Critically Endangered, 4 species Endangered; none Extinct since 1600.

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Systematics The anthropoids or great apes are for the most part confined to the equatorial regions of Africa and South-east Asia. Although there has been some controversy regarding their nomenclature at the family level, there is no question that they are the closest living relatives of modern humans. For many years, the superfamily Hominoidea was split into three families, Hylobatidae (gibbons or lesser apes), Pongidae (great apes), and Hominidae (humans and their ancestors). The Pongidae consisted of three genera: Pongo (orangutans), Pan (Chimpanzees), and Gorilla (gorillas). The late M. Goodman in 1963 was first to propose placing African great apes in the family Hominidae, along with modern humans (and their fossil ancestors), and C. P. Groves incorporated the orangutan into this family in 1986. In the arrangement proposed by Groves, the Hominidae comprised the subfamily Ponginae, with Pongo, and the subfamily Homininae, with Gorilla, Pan, and Homo. This phylogenetic arrangement, which is now widely accepted and followed here, is supported by a variety of genetic data showing that Gorilla, Pan, and Homo are more similar to one another than any of them is to Pongo. Thus, the superfamily Hominoidea contains only two living families, Hominidae and Hylobatidae, together with several known only as fossils. In a review published in 1978, P. Andrews concluded that the family Pongidae (here, family Hominidae) originated in the earliest Oligocene about 35 million years ago, at which time a series of genera, from Oligopithecus to Aegyptopithecus, were present in the Jebel Qatrani Formation of the Al Fayyûm, Egypt. More recent information, however, suggests that this Formation may actually be late Eocene, and that these fossil genera represent the very earliest catarrhines, well before the ancestors of the Hominoidea separated from those of the Old World monkeys (Cercopithecoidea). By the early Miocene about 18 million years ago, several species of Proconsul had developed in Africa, and although this genus is no longer thought to represent the ancestral line of both the modern great apes and humans, much of what is known about the morphology of early Miocene hominoids is based on it. Like Old World monkeys and gibbons, Proconsul had thin tooth enamel and a narrow chest. Like Old World monkeys, it had short forelimbs and a light build—suggesting primarily quadrupedal living on soft fruits, but it also shared some similarities with apes, especially in having no tail. Proconsul and its relatives are now placed in a separate family, Proconsulidae.

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The evolutionary line leading to African apes and humans separated from the Proconsulidae and Hylobatidae some time during the Early or Middle Miocene, more than 13 million years ago when the ancestors of the orangutan and the African apes are recognizable in the fossil record. The split between the ancestors of Pan and Homo took place in the Late Miocene, perhaps about seven million years ago, but genetic evidence suggests a phase of interbreeding between the two lines about four million years ago. It is commonly thought that Pan is the closest living relative of Homo and that the ancestral stock of Gorilla split off considerably earlier. Nevertheless, in 1993, J. Rogers suggested that the lines leading to all three genera diverged over a relatively brief period. There is a minority view, supported by certain morphological evidence, that Pongo is the closest living relative of Homo. Under the presently accepted taxonomic arrangement, the two subfamilies of the Hominidae have been further divided accordingly: the Ponginae with its single living genus (Pongo) and currently comprising two species and the Homininae with its three genera (Gorilla, Pan, and Homo) comprising five species. Subdivision of the Hominidae

HOMINIDAE

[Figure: Stephen Nash]

PONGINAE

HOMININAE

orangutans 2 species (Pongo)

African apes and Humans 5 species (Gorilla, Pan, Homo)

FAMILY SUBFAMILY

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FAMILY HOMINIDAE Great Apes

Fully mature adult male orangutans have flaps of fatty tissue called flanges on either side of their faces. These flanged males are twice the size of females and continue to get heavier as they get older, sometimes exceeding 100 kg. The Bornean Orangutan (subspecies wurmbii, “Central Bornean Orangutan,” shown here) tends to be stouter and stockier than the Sumatran Orangutan (Pongo abelii, below right), with a darker coat and somewhat stringy hair. Fossil evidence indicates that orangutans once had a much wider distribution, and occurred on the mainland of South-east Asia in early recent times. Pongo pygmaeus wurmbii Camp Leaky, Tanjung Puting National Park, S Borneo. Photo: Thomas Marent/ardea.com

Pongo abelii Gunung Leuser National Park, N Sumatra. Photo: Konrad Wothe

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“North-west Bornean Orangutan” (P. p. pygmaeus), the “Northeast Bornean Orangutan” (P. p. morio), and the “Central Bornean Orangutan” (P. p. wurmbii). In contrast to the Bornean species, the Sumatran Orangutan is monotypic. The subfamily Homininae includes the African great apes (gorillas, Chimpanzees, Pan troglodytes, and Bonobos, Pan paniscus) and modern humans. All are broadly similar from a morphological standpoint. Although not directly descended from living apes, as is sometimes assumed, humans do share a common ancestor from which the two lines split off. It was first proposed by Goodman in 1963 that a genus should have a time depth of at least four to five million years, and using this criterion, it is evident that one should recognize Pan as a separate genus from Homo. On the other hand, if one adopts

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Orangutans’ arms are one and a half times as long as their legs, and reach to the ankles when an individual is standing. Their legs are short and relatively weak. The Bornean (Pongo pygmaeus, photo above) and Sumatran Orangutan were formerly considered subspecies of the single species P. pygmaeus, because of superficial external similarities. After 1·1–1·5 million years of separation, the two island populations have become genetically and behaviorally different. Sumatran Orangutans are slimmer, with longer hair, especially on their arms, and have longer, more oval faces. Both sexes have long beards. Orangutans are thought to have diverged from the African great apes around 13 million years ago.

The last common ancestor of all living Ponginae and Homininae is probably the genus Kenyapithecus, which lived about 14 million years ago in the middle Miocene of eastern Africa, although some hold fast that this genus was already on the African ape/human lineage. In 1982, Andrews and J. Cronin suggested that Sivapithecus and Pongo are closely related and in an evolutionary line completely separate from that leading to Pan, Gorilla, and Homo. In his 1978 paper, Andrews also considered that in the late Miocene Sivapithecus gave rise to Gigantopithecus, a genus containing one particularly large ape (G. blacki) that survived at least until the middle Pleistocene in Asia. It was first discovered by G. H. R. von Koenigswald, the German-Dutch geologist, who collected its teeth during his travels in China and Java from 1934 to 1939. He found teeth while wandering through Chinese pharmacies to study fossil bones used as traditional medicines; three mandibles and hundreds of isolated teeth have since been discovered in limestone caves in southern China and northern Vietnam. There has been some suggestion that Gigantopithecus, thought to have been a relative of Pongo, may actually represent an aberrant branch of the line leading to Homo, but this is a minority view. Gigantopithecus blacki was the largest known primate—estimated to have been 2·5–3 m tall and weighing up to 300 kg. Its latest known occurrence, in a cave in northern Vietnam, dates to 475,000 years ago. It is believed to have been terrestrial and may have eaten bamboo like the Giant Panda (Ailuropoda melanoleuca). The genus Pongo is confined today to the islands of Borneo and Sumatra. Pleistocene fossils from southern China, northern Vietnam, Laos, and Java indicate that orangutans once had a much greater distribution. Remains discovered in northern Vietnam, as well as traditional beliefs in Peninsular Malaysia, suggest that they still occurred on the mainland of South-east Asia in early recent times. Orangutans are thought to have diverged from African great apes between ten and 16 million years ago, probably around 13 million years ago. Because of geographic isolation and a time-separation of 1·1–1·5 million years, the two remaining island populations have become chromosomally, morphologically, and behaviorally different (most markedly in the case of adult males). Historically, because of superficial external similarities, Sumatran and Bornean orangutans were both considered subspecies of Pongo pygmaeus. The taxonomic review proposed by Groves in 2001 supported the acceptance of the Sumatran Orangutan (Pongo abelii) as distinct from its Bornean relative, the Bornean Orangutan (Pongo pygmaeus), and this classification has now been widely adopted. Three subspecies of Bornean Orangutans are recognized according to differences in overall size and skull morphology: the

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FAMILY HOMINIDAE Great Apes

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a time depth criterion of seven million years, as has also been proposed, then there are possible grounds for uniting the two genera (for which the earlier name would be Homo). Gorillas were unknown to science until 1847 when the first skulls were analyzed, and they remained little known for almost a century. At that time, the exploration of the great Central African rainforest had only just begun, and it was not until about 1880 that the major museums first stocked up with gorilla skins and skeletons. A dozen or more species and subspecies were named and described during the next 30 years, sometimes from single specimens. During the 20th century, the trend went the other way, with only a single species and its two subspecies recognized. Gorillas are patchily distributed in Central and Western Equatorial Africa, separated by the Congo River and its tributaries. Until relatively recently, only one species of Gorilla was recognized, with three subspecies: G. gorilla gorilla in the west and G. g. beringei and G. g. graueri in the east. These widely separated east and west populations were formally split into two species, the Western Gorilla (Gorilla gorilla) and the Eastern Gorilla (Gorilla beringei), in 2000 because they are consistently different in quite a large number of morphological features and DNA sequences. There is a striking divergence in mitochondrial DNA between G. g. gorilla, on the one hand, and G. b. graueri and G. b. beringei, on the other, and indeed Western and Eastern gorillas are at least as genetically distant from one another as are Chimpanzees and Bonobos. There are currently two recognized subspecies of Western Gorilla. The “Western Lowland Gorilla” (G. g. gorilla) occurs in lowland rainforest areas from southern Cameroon (south of the Sanaga River) to the mouth of the Congo River and east to the Ubangi River. The “Cross River Gorilla” (G. g. diehli), first described in 1904, was not recognized as distinct until 2000 after its unexpected rediscovery two years earlier; its skull is strongly different, on average though not 100%, from that of other western gorillas, although its mitochondrial DNA haplotypes are generally nested within those of western gorillas. A population of gorillas first discovered in 2002 in the Ebo Forest of western Cameroon is geographically intermediate between Western Lowland and Cross River gorillas. These “Ebo Gorillas” may be in some way distinct, with measurements from a single skull indicating that this may be a relict population of a previously more widespread form living north of the Sanaga River; their taxonomic status awaits clarification.

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Gorillas are the biggest and most powerful living primates. In 2000, the gorilla populations to either side of Congo River and its tributaries were split into two species, the Eastern (Gorilla beringei) and the Western Gorilla. The standing height of a male gorilla is up to 180 cm, and the span of the outstretched arms is far greater, at 200–275 cm. Gorillas’ bodies are covered in dark hair, except for the chests of adult males, which become bare as they age. Dominant males also develop a bony (sagittal) crest on their heads to which their massive jaw muscles are attached, and the hair on their backs becomes “silver.” Some “Western Lowland Gorillas” (G. g. gorilla), like this one, have a rich chestnut-colored crown. Gorilla gorilla gorilla Dzanga-Sangha Forest Reserve, Dzanga-Ndoki National Park, SW Central African Republic. Photo: Matthias Dehling

The Eastern Gorilla is found in eastern DR Congo, northwestern Rwanda, and south-western Uganda. There are two subspecies, the “Mountain Gorilla” (G. b. beringei) and “Grauer’s Gorilla” (G. g. graueri), and these are strongly distinct from one another. Most individuals can be allocated to one or the other subspecies by external characters alone, and most skulls can also be allocated without error. Their mitochondrial DNA haplotypes appear, based on current information, to be fully distinct, and with such evidence, they would be recognized as separate species if they were mouse lemurs or shrews, but without additional study of DNA segments and morphological characters, it would seem a rather large step to take in the case of near-human taxa; nonetheless, it is possible that taxonomic status is underestimated. A population of gorillas in the Bwindi Impenetrable National Park of south-western Uganda may prove to be either a distinct subspecies, or even a population of Grauer’s Gorilla after further research, although most available evidence, both morphological and mitochondrial DNA, supports the provisional conclusion that it should continue to be treated under the Mountain Gorilla. Indeed, it may be that until a few hundred years ago, or even less, their populations formed a continuum. The remaining two species of great ape come closest to Homo sapiens in both physiology and genetics: they share 98·5% of their total DNA with modern humans, and more than 99% if only active genes are considered. Some authorities have gone so far as to argue that Chimpanzees, Bonobos, and humans should all be categorized in the same genus, Homo, because it is believed that Chimpanzees and humans diverged only 7–6 million years ago and taking the viewpoint that a genus should have a time depth of about seven million years (although more usually the minimum time depth is set at five million). The implications of changing the taxonomical categorization could have enormous impacts on how Chimpanzees are perceived, and the rights extended to them. For example, by categorizing Chimpanzees as Homo, it would certainly be considered unethical to keep them in zoos or use them in research; there is already a strong movement to ban biomedical research on Chimpanzees in the last two countries that still permit it (USA and Gabon), even without them being considered species of our own genus. There has been considerable controversy in the past regarding the technically proper generic name. Until the 1950s, various names were used—Troglodytes, Anthropopithecus, Chimpansee [sic],

Gorillas’ feet resemble those of humans, although with an opposable, grasping big toe, which is more divergent in the Western Gorilla. Gorillas’ toes are relatively shorter than those of Chimpanzees (Pan troglodytes), but gorillas’ hands are large and wide, with comparatively longer thumbs than the other non-human apes. Gorillas’ hands and feet are hairless, like their faces and ears. Gorilla gorilla gorilla Batéké Plateau National Park, SE Gabon. Photo: Martin Harvey/DRK

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FAMILY HOMINIDAE Great Apes

When walking on all fours, gorillas support their weight on the backs of their third and fourth fingers (“knuckle-walking”). The Eastern Gorilla is larger than the Western Gorilla (Gorilla gorilla), with shorter arms and a stockier build. “Mountain Gorillas” (G. beringei beringei) like these have larger jaws and a wider facial skeleton than other gorillas, and their hair is thick and long, particularly on the arms of adult males. There are physical and behavioral differences between the two subspecies, the Mountain and “Grauer’s Gorillas” (G. b. graueri). Regardless of individual size, Western Gorillas climb much more than Mountain Gorillas. Gorilla beringei beringei Volcanoes National Park, NW Rwanda. Photo: Thomas Marent/ardea.com

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While the appropriate taxonomic labels for different populations of Chimpanzees remain unresolved, the relative importance of different threats faced by Chimpanzees varies across Africa, making a regional approach valuable for conservation purposes, recognizing that future work may lead to a consensus recognizing more or fewer subspecies. The Bonobo is still the least known of the great apes in terms of its ecology. Indeed, its very existence was not even recognized until 1929 when Schwarz decided to investigate a handful of “aberrant” skins and skeletons of Chimpanzees in a museum and found them to be distinct. Although at first Schwarz classified them as another subspecies of P. troglodytes, it was not long before H. Coolidge, in 1933, realized that it was in fact a thoroughly distinct species.

Morphological Aspects The great apes are, without exception, large barrel-chested animals, with larger brains and bigger bodies than other nonhuman primates. All three great ape genera contain individuals that exceed many human beings in size. All are sexually dimorphic, with the males being bigger than the females. Like humans, they lack a tail. The pelage is generally short, shaggy, and coarse. The face is nearly naked, and the ears are round and naked. The form of the skull is variable, but it is nearly always longer than broad. The dental formula for members of this family is I 2/2, C 1/1, P 2/2, M 3/3 (×2) = 32. The incisors are nearly equal in size in gorillas and Chimpanzees but different in size in orangutans, the canines are large, the anterior lower premolars have one primary cusp and one more-rudimentary one, the other premolars are bicuspid, and the molars are wide-crowned and supplied with four tubercles in the upper jaw and five in the lower. In general, form and structure of the brain of great apes closely resemble that of Homo sapiens. Average brain capacities in adult Hominidae are: Pongo 411 cm3; Pan 394 cm3; and Gorilla 506 cm3. Great apes can distinguish colors, and their best-developed senses are vision and hearing. The two species of orangutans are essentially similar in size. There is considerable individual variation in both species, although in general all adults have coarse, dark-gray skin, which on the face in particular tends to be quite pimply. Pelage color ranges from reddish-orange through dark rufus and reddish-

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and others, but none of them were acceptable for a variety of reasons. Although the name Pan was proposed by the eccentric L. Oken in 1816 in a book that used scientific nomenclature in a completely bizarre and idiosyncratic manner and is generally banned as a source of new generic names, primatologists had more or less settled on the generic name Pan by about 1950, and this is the name that is now formalized in nomenclature. The Bonobo has sometimes been considered a subspecies of the Chimpanzee, although modern evidence confirms that the two are diagnosably distinct. They are now invariably taken separately in both morphological and behavioral studies, although it should be kept in mind that Bornean and Sumatran orangutans, and Western and Eastern gorillas, are about as distinct as Chimpanzees and Bonobos, one gets the impression that the separate treatment always awarded to Bonobos is simply because they have their own name. The taxonomy of the Chimpanzee as a species remains an active area of research. E. Schwarz, the zoologist who in 1932 proposed the basis of the still-used modern classification, distinguished subspecies troglodytes (“Central Chimpanzee”), verus (“Western Chimpanzee”), and schweinfurthii (“Eastern Chimpanzee”) by such characters as the shape of the head, the form of the beard, and the changes in the color of the facial skin with age. Four subspecies are currently recognized, because in the last ten years, Chimpanzees occurring between the Sanaga and Niger rivers have been accepted to form the subspecies P. t. ellioti (“Nigeria-Cameroon Chimpanzee”). Based on a craniometric study, Groves proposed that the Eastern Chimpanzee currently classified as P. t. schweinfurthii be split in two, creating a fifth subspecies, P. t. marungensis; however, geneticists do not support this division. DNA studies have shed new light on the interrelationships of the Chimpanzee taxa. On the basis of mitochondrial DNA, it would appear that the Western Chimpanzee has been distinct from other Chimpanzees for perhaps 1·5 million years (compared to 2·5 million years for the time of separation of the Bonobo) and that the Nigeria-Cameroon Chimpanzee is also consistently distinct, whereas the other three share some haplotypes. Accordingly, there is a minority view that the two that are distinct in mitochondrial DNA should be recognized as the species Pan verus and P. ellioti, while schweinfurthii and marungensis should become subspecies of the Central Chimpanzee. Based on recent nuclear DNA work, A. Fischer and colleagues have argued that differences between any of the populations of Chimpanzees are too small to warrant subspecific designation.

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FAMILY HOMINIDAE Great Apes

Four subspecies of the Chimpanzee are currently recognized. Chimpanzees are broadly similar to gorillas (Gorilla), but smaller, and like gorillas, move mainly on the ground by “knuckle-walking.” Males are larger than females, although not by as much as in orangutans (Pongo) and gorillas. They lack the gorillas’ heavy brows and protruding jaws, although some large individuals of either sex may have a small sagittal crest. Both sexes have white beards. Males like this one develop a triangular bald patch behind the brow, while the hair of females recedes in a straight line and their crowns may become completely bald. Pan troglodytes schweinfurthii Mahale Mountains National Park, W Tanzania. Photo: Konrad Wothe

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brown to black. The hairy coat is rather thin and shaggy. They are large apes, weights being 60–85 kg for fully adult males and 30–45 kg for adult females. There is a high degree of sexual dimorphism, and it may be that males are larger because of male–male competition for females; large males displace small males for access to females for mating. Head-to-body length of an average adult is about 1·2–1·5 m. The powerful arms are one-half again as long as the legs, reach to the ankles when an individual is standing erect, and have a spread of about 2·2 m. The legs, by contrast, are short and relatively weak. The hands and feet are virtually indistinguishable from each other, and both are ideal for grasping, despite having relatively short thumbs and big toes.

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The skull profile in orangutans is more sloping and the face more dished than those of Chimpanzees and gorillas, and the skull of orangutans exhibits little of the brow ridging that is so prominent in other genera. The forehead is high and the jaws prognathous (jutting out), with thin lips. the small ears are devoid of hair and have no lobes. Fully adult males have flaps of fatty tissue (called flanges) on both sides of the face, which develop with full maturity. These represent localized deposits of subcutaneous fat bound by connective tissue and covered by unmodified skin with scant and irregularly distributed hairs. Flanged males are twice the size of females; they have a long coat of dark hair on the back, a facial disk, and a throat sac used in the production of “long calls.” These males are rather intolerant and aggressive toward other adult males. Unflanged males do not possess these secondary sexual characteristics; they are the size of an adult female, do not emit long calls, or show intolerance. Diverging genetically 1·5 million years ago, phenotypic differences between the two species of orangutans are apparent. Sumatran Orangutans are thinner than their Bornean relatives, and they usually have paler red coats, longer hair especially on the arms, and longer more oval faces. Adult males have moustaches and their flanges are covered with fine white hair. Both genders have long beards. Bornean Orangutans have coarse hair that can be orange, brown, or maroon. Males have large, pendulous throat pouches and, compared with the Sumatran species, their flanges are markedly larger and are covered in short, often nearly invisible, hair. The face of Bornean Orangutans has a more figure-eight shape because of deeper infraorbital fossae. Infants are born with pink faces, but the pigment changes to dark brown or almost black as they age. There is little external difference between the three subspecies of Bornean Orangutans. The North-west Bornean Orangutan is medium in size with a relatively broad palate; the Central Bornean Orangutan is very large with a narrow palate; and the North-east Bornean Orangutan is very small with a relatively small brain size, which has been argued to be an adaptation to its drier, less predictable environment. Orangutans are by far the world’s largest tree-dwelling mammals and, with the exception of adult Bornean males, rarely descend to the ground in the wild. Normal movements are mainly by climbing and walking through large trees and swinging from branch to branch, using any combination of both hands, both feet, or one hand and a foot to hold onto branches as they

The Chimpanzee and the Bonobo (Pan paniscus) have prominent ears, protrusive lips, arms that are longer than their legs, and long hands with short thumbs. The ears, nose, hands, and feet of young Chimpanzees like this one are flesh-colored, and the skin color darkens in older individuals (above). Young Chimpanzees have a parting along the center of their crowns, which is more pronounced in some subspecies than in others. The thickness of the hair on the scalp also varies. Although mainly terrestrial, Chimpanzees are capable of some suspensory movement, and young ones often swing by their arms between branches and vines. Pan troglodytes troglodytes Bakoumba Private Reserve, near Franceville, SE Gabon. Photo: Cyril Ruoso

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FAMILY HOMINIDAE Great Apes

Pan paniscus Lola ya Bonobo Sanctuary, W DR Congo. Photo: Christian Ziegler/Bios

The hands of the Chimpanzee (Pan troglodytes) and the Bonobo are long and narrow, with a short thumb set well below the other fingers. This is probably an adaptation for climbing, allowing them to grasp wide-diameter supports. But both species are also capable of precision grips, such as “pinching” small objects between the pad of the thumb and the middle joint of the index finger. Like humans, the great apes can use their left and right hands simultaneously for different aspects of a task and also control their fingers independently. Chimpanzees and Bonobos are often right-handed. While supporting themselves on the knuckles of one hand, they tend to reach for objects with their palms upward, whereas when standing upright, they usually reach with the palm down. Pan paniscus Lola ya Bonobo Sanctuary, W DR Congo. Photo: Tony Camacho

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move horizontally through the rainforest canopy (quadrumanous climbing or clambering). The positions of their very short thumbs and big toes make it possible to move hand-overhand through the trees, grasping branches with their feet as well; their fingers and toes act like hooks. Nevertheless, they are extremely cautious and deliberate climbers and commonly use a method of passing from tree to tree known as “tree swaying,” in which a relatively thin tree (usually sapling) is swayed in ever widening circles, until the orangutan has narrowed the space to the next tree sufficiently to grab hold and cross over. Because of their large size, orangutans must be careful in choosing supports when traveling, which may, at least partially, explain why they move slowly. Terrestrial movement, when it occurs, is cautious; when on the ground, orangutans will normally use a quadrupedal gait, with their hands either clenched into a fist or with their palms flat (but not on their knuckles as is seen in African great apes). They can walk more or less upright but rarely do so because their legs are poorly designed for this purpose. Nevertheless, for some reason, they readily adopt an upright gait in zoos, and it is a delightful sight to see two youngsters, hand-in-hand, walking upright, stiff-legged, and rocking from side-to-side as they go. J. MacKinnon in 1971 and H. Rijksen in 1978 suggested that the orangutan’s arboreal mode of life and dispersed social structure may have resulted, in part, from many thousands of years of human hunting pressure. Moreover, Pleistocene remains from China and Sumatra suggest that some orangutans were considerably larger than those of today, possibly even exceeding gorillas in size, although this conclusion is based mainly on tooth size, which may be a poor indicator of body size. B. Galdikas in 1988 concluded that the solitary nature of orangutans was mainly due to the association of their large size and frugivorous diet and the consequent competition of opportunistic food sources; she doubted that Pleistocene orangutans had been terrestrial. This latter hypothesis seems most plausible, although the question of why body size grew so large in the first place is not answered; the huge size of flanged males undoubtedly relates to sexual selection, but even adult females are well above the size of any other arboreal species. Gorillas are the biggest and most powerful living primates, with an extremely compact and sinewy build and a wide pelvis. The average weight is 57–98 kg for females and 120–209 kg for males. Males are 138–196 cm when standing upright, and females are 109–152 cm. The various taxa are roughly equal in size, and although on average Grauer’s Gorilla is largest, but alltime size records come from the Mountain Gorilla. The shoul-

der breadth of this powerful primate is nearly twice that of the Chimpanzee, and the chest is as much as 50 cm across, with a circumference of 125–175 cm in the adult male. The span of the outstretched arms, about 200–275 cm, is far greater than the standing height. The hands are large and wide, with comparatively longer thumbs than the other non-human apes. The feet of Mountain Gorillas are very much like those of humans, although the great toe is somewhat more divergent in Western and Grauer’s gorillas. The forearm is much shorter than the upper arm; the forelimbs are relatively long, and the hindlimbs are relatively short. The skull of the gorilla is characterized by a markedly prognathous face in most individuals, rectangular and widely sepa-

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The Bonobo shows a greater predisposition for bipedal walking than other great apes, due to its longer thighbones, longer feet, and differential distribution of body weight. Although formerly known as the Pygmy Chimpanzee, the Bonobo is comparable in size to the more familiar and widespread Chimpanzee (Pan troglodytes). Bonobos have smaller and rounder heads than Chimpanzees. Overall, they are more slender, with longer limbs and narrower chests. They are more agile and arboreal than Chimpanzees, climbing, swinging, and leaping between branches, although like the other African great apes, they also walk quadrupedally, supporting themselves on their knuckles.

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FAMILY HOMINIDAE Great Apes

Orangutans are by far the world’s heaviest tree-dwelling mammals, and the care they must take to choose branches and lianas that can support them may explain why they travel so slowly. They move by climbing and walking through large trees, and swinging from branch to branch, using any combination of hands and feet, with their fingers and toes acting like hooks. “Tree swaying” (swaying a slender tree in ever widening circles) is used to narrow the gaps between trees, and orangutans will also swing on lianas, like Tarzan, to reach the next supporting branch or trunk. Orangutans of different ages and sexes often follow the same route to reach fruit trees, but females and youngsters can travel at higher levels to take advantage of more slender supports. But they may need to sway them more often than the much heavier males to gain sufficient amplitude to cross a gap. The Sumatran Orangutan spends a larger proportion of its day traveling than its Bornean counterpart (Pongo pygmaeus). The heavier male uses the upper surfaces of larger branches more often than the female, and sits, stands, and walks on them, while females use suspensory under-branch locomotion more often. Adult female Sumatran Orangutans have frequently been observed hanging from a few strands of vertical foliage when feeding. However, females that have borne at least one baby tend to avoid small single supports and favor more robust ones, to a greater extent than the larger males. It has been suggested that the experience of raising offspring makes them more cautious than other age and sex classes.

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Pongo abelii Gunung Leuser National Park, N Sumatra. Photo: Cyril Ruoso

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FAMILY HOMINIDAE Great Apes

Knuckle-walking, which is unique to the African great apes among primates, is the most common form of locomotion in the Chimpanzee. After sitting (which occupied 61% of waking time in a study in Mahale Mountains National Park, Tanzania), it is also the ape’s second most common positional behavior. Many aspects of the African ape wrist and hand that had been supposed to be adaptations to swinging from branches have been shown to be knuckle-walking adaptations. When moving within food patches, Chimpanzees also walk on their palms. African apes do not swim, and barriers formed by rivers too deep for wading are thought to have played a part in the separation of the Chimpanzee and the Bonobo (Pan paniscus), and some Chimpanzee subspecies.

rated orbits, and sagittal and nuchal crests in almost all males and sometimes (much smaller) in females. The pronounced brow ridges are heavier and more rounded than those of Chimpanzees. A pad of skin and connective tissue, relatively dense and fibrous in nature, is present on the crown. The nostrils are large, tending to be different in shape in different taxa; Western Gorillas have heavily padded nostrils, giving their nose its characteristic “squashed tomato” appearance. The nostrils of Eastern Gorillas lack this padding, and their noses are more angular and protrude less above the surface of the upper lips. Interestingly, individual gorillas can be distinguished by their noses; each has a unique pattern, much like the human fingerprint. The eyes are small, and the tiny ears lie close to the head. The teeth have high crests that help break down the leaves that make up a large proportion of their diet. The lower molar teeth increase in size toward the rear. Gorillas have dark brown to black fur and black skin. The face, ears, hands, and feet of the gorilla are bare, and the chest of mature males lacks hair. There is no beard in most individuals, but some—males in particular—develop bushy side whiskers; these may be especially noticeable in Mountain and Cross River gorillas. Dominant adult male gorillas, popularly known as silverbacks, have a prominent fat-padded sagittal crest (much larger than that of the female) and are so-named for the striking silver color that extends from their shoulders to their rump (extending to different degrees in the two species). It is often mistakenly thought that silverbacks are a race or even a species of gorilla, but they are simply mature males with silver to white hair on their backs. To some extent, even an inexperienced observer can distinguish the Eastern and the Western gorillas from one another, but there are few striking physical differences between subspecies, although differences in dentition and craniometric analyses do reveal distinguishing morphological characteristics of each. Generally, Eastern Gorillas have longer faces and broader chests than Western Gorillas and lack the patches of red-brown hair on the head that characterize the latter. The Western Lowland Gorilla is generally brownish-black, often with a reddish crown. The male’s white saddle extends onto his thighs and grades more into the body color. The Cross River Gorilla is the smallest member of the genus and differs from other gorillas genetically and in the shape of the skull. The color of both the skin and hair of both Eastern Gorilla subspecies is jet black, with the adult male developing a silvery-

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white saddle on the back between the shoulders and rump and not extending onto the sides until senility. The Mountain Gorilla can be easily distinguished from Grauer’s Gorilla, however, by its much longer silkier hair, especially on the arms. The facial skeleton is wide, with large jaws and strong sexual dimorphism in the upper canines. There is a prominent sagittal crest, and the pelage on the scalp is long and shaggy. The nostrils of the Mountain Gorilla are quite broad but angular and clearly outlined above. Its arms are relatively short. Grauer’s Gorilla has shorter hair (less shaggy on the scalp and arms). Its head is smaller, with a notably long and thin face and a strongly padded upper lip, and its nostrils are rounded and not clearly outlined above. There is also less sexual dimorphism in the upper canines. The so-called “Bwindi Gorillas” are not different from those inhabiting the Virunga Volcanoes in terms of their mitochondrial DNA, but they do differ somewhat in morphology, being slightly smaller and more narrow in the body than the typical Mountain Gorilla, with shorter hair and, in many cases, relatively longer limbs, hands, and feet. The teeth are also slightly smaller, and the thumbs and big toes, on average, are shorter. All these differences are “on average” or “at the most,” and characteristics such as smaller size and shorter hair, for example, may simply be a matter of phenotypic plasticity in response to different climates and vegetation. For the most part, gorillas are terrestrial but quite capable of climbing. Due to the quadrupedal gait and the arms being considerably longer than the legs, the body is inevitably put into a semi-erect configuration. Surface locomotion is by a quadrupedal walk, with the soles of the feet and the middle phalanges of the fingers placed on the ground. Gorillas support their weight on the dorsal surface of the third and fourth digits of the curled hands, known as knuckle-walking. A limited amount of time is spent standing on two legs, and a few bipedal steps may be taken. When they travel through trees, they climb but are unable to move by suspensory behavior. The two species of Chimpanzees are characterized by prominent ears, protrusive lips, arms that are longer than the legs, and long hands but short thumbs. The digits are narrow and curved. The facial skeleton is only moderately prognathic, with the orbits frontally directed and surmounted by prominent supraorbital crests, which are not strongly rounded and do not protrude like those of gorillas. A good rule of thumb to distinguish large Chimpanzee skulls from small or young gorilla

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Pan troglodytes schweinfurthii Mahale Mountains National Park, W Tanzania. Photo: Günter Ziesler

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FAMILY HOMINIDAE Great Apes

Gorillas rarely walk upright for more than a few steps. The maximum distance they have been observed walking bipedally is around 20 m. Gorillas, Chimpanzees (Pan troglodytes), and humans are fully plantigrade; that is, unlike other primates, their entire foot, including the heel, is in contact with the ground when they walk. The male Western Gorilla tends to be more terrestrial than the female because his greater weight limits the parts of trees he can climb, particularly the smaller outer branches. This can result in differences in diet, with less fruit being available to the male. Gorilla gorilla gorilla Dzanga-Sangha Forest Reserve, Dzanga-Ndoki National Park, SW Central African Republic. Photo: Maximilian Dehling

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skulls is that gorillas have a ridge running down the center of the nasal bones, whereas the nasals are flat in Chimpanzees. A small sagittal crest is seen only occasionally in large male and female Chimpanzees, and there is little or no nuchal crest. The molars are large and decrease in size toward the rear; they lack the intercuspal crests of those of gorillas. Males Chimpanzees have large canines. The Chimpanzee may be called the “Common Chimpanzee” by those who call the Bonobo the “Pygmy Chimpanzee,” although the term “common” is no longer really accurate. Chimpanzees are broadly similar to gorillas, but smaller and more active in their movements. A relatively heavy-built ape,

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Chimpanzees have some sexual dimorphism, with males weighing 28–70 kg and females 20–50 kg. There is a great deal of geographic variation in size; the largest Chimpanzees are those of Cameroon and the northern DR Congo, which weigh up to 60 kg or more, while the famous Chimpanzees of Gombe Stream National Park, Tanzania, are remarkably small; both genders weigh 30–40 kg. The arms extend below the knees when an individual is standing and have a spread that is about 50% greater than an individual’s height. The palms are long and narrow, and the thumbs are comparatively short, all of which are probably adaptations for climbing. The face is usually bare and generally black. The ears, nose, hands, and feet of young Chimpanzees are flesh-colored, and there is a white patch of fur near the rump. Infant Western Chimpanzees have a slightly darker, often bluish-tinged, “mask” across the upper face around the eyes, traces of which may survive even in black-faced adults. In Central and Eastern chimpanzees, facial darkening is more often accompanied by the development of freckles, which enlarge and fuse. At maturity, their overall skin color is dark, and the pelage varies from deep black to light brown, becoming gray with extreme age. The hair on the head may grow in any direction, although in Western Chimpanzee youngsters, there is often a central crown parting, and both genders are prone to partial baldness early in maturity. Balding starts behind the brows, and in males, it tends to form a triangular patch, which gradually enlarges. In females, the crown hair recedes in more of a straight line, so that eventually the crown baldness is more complete than in most males. Both males and females have short white beards and have markedly pronounced genitalia, with the vulva being backwardly placed. There is little difference between Chimpanzee “subspecies” in terms of morphology, although mitochondrial DNA analysis indicates that they are quite distinct from one another. The Central Chimpanzee is a notably large and sexually dimorphic form. The head is very broad with a concave facial profile, and the facial skin becomes pink in juveniles but freckled with tan spots and darkening to a deep black with maturity. The white beard is long and sparse, and the sideburns are long and hang downward. The scalp is thinly haired from an early age and becomes bald in adulthood (especially in females, on whom the bald patch often extends onto the temples), with the scalp parting poorly marked. The brow ridge runs straight across. The Western Chimpanzee is small and thinly haired, with a broad flat-topped head. The pelage is black but may range from brown to ginger. The jaws are broad, and the brow ridges may

Orangutans rarely stand fully bipedally. Even when fully erect, they usually use at least one of their forearms for support. Their feet are adapted for clambering and grasping, and when standing, their heels are not in contact with the ground. On the rare occasions when it comes to the ground, the Bornean Orangutan generally uses a quadrupedal gait, walking on its wrists/fists or palms, but not on its knuckles. In a study of Sumatran Orangutans (Pongo abelii), the gait and climbing capabilities of females carrying infants were not found to differ significantly from those of unencumbered females. Pongo pygmaeus Kalimantan, S Borneo. Photo: Cyril Ruoso

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FAMILY HOMINIDAE Great Apes

African apes are highly gregarious. The Chimpanzee (Pan troglodytes) and the Bonobo live in multimale–multifemale communities, of which the membership changes only with births, deaths, and permanent transfers. Bonobo communities comprise 10–120 individuals, which meet every day, and often feed and travel together. They break up into mixed-sex parties of 5–23 individuals when foraging. Bonobos enter water more readily than Chimpanzees, which are said to dislike doing so, although one population is known to immerse themselves in shallow pools when the weather is extremely hot.

be arched and laterally flared over each eye. Juveniles have a butterfly-shaped “mask” of dark skin covering the upper part of the otherwise pinkish-colored face (although the skin around the mouth and nose has a tendency to darken with age) and a parting on the scalp. Traces of this mid-facial mask remain in adult Western Chimpanzees. A thick, full, and rounded white beard is present in adults of either sex, and the sideburns are long and directed downward. Both males and females have a triangular bald spot, beginning as a widening of the parting; in the female, it is very wide, extending down onto the temples. The Nigeria-Cameroon Chimpanzee is genetically different from the Western Chimpanzee (with which it was formerly included), although not distinctly different in appearance. M. K. Gonder and colleagues resurrected this subspecies (it was first described a century ago), but there has been no study of its morphological differences. The name vellerosus has since been discarded in favor of ellioti. Finally, the head of the Eastern Chimpanzee is rounder than in other subspecies, and the brow ridges are thinner and run straight across, while the lower face is narrow and the facial profile is fairly straight. The hair is dark, long, and exceedingly dense, and the beard is full but straggly. The facial skin of juveniles is pink, with no freckling, and it becomes dark (bronze or coppery but not deep black) in adults. The scalp parting is poorly defined in juveniles, and the scalp hair gradually becomes thinner all over in adult males. The bald spot in adult females is never very wide and never extends down onto the temples. The sideburns are full and swept backward. There is considerable morphological variation, and Groves suggested that the Eastern Chimpanzee may in fact represent two subspecies: the very large schweinfurthii and the much smaller (and more familiar) marungensis. Mitochondrial DNA haplotypes of these two forms and the nominate form troglodytes are intermixed, some being unique to one or other of the three and others being common to two or all of them. Haplotypes of verus and ellioti form distinct, exclusive clades, such that it has been proposed that they should be considered distinct species. More study, particularly morphological, is required to ascertain if these differences are truly diagnostic. Chimpanzees are both terrestrial and arboreal, with the amount of time spent on the ground varying between study sites and genders. Modes of locomotion include quadrupedal walking, running, and occasional bipedalism, particularly during displays of dominance and aggression. Bipedal walking is rather stooped, with the toes turned inward. Unless carrying something, Chimpanzees prefer to walk on all fours. Quadrupedal move-

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ment is by knuckle-walking, with the hindlegs slightly flexed, the body inclined forward, and the arms straight. The soles of feet and the backs of middle phalanges of the fingers are placed on the ground. In this position, individuals may proceed at a rapid gallop. In the trees, Chimpanzees move in a quadrupedal manner, but they will use suspensory behavior to move around. Leaping and limited brachiation also are used, particularly by young individuals. Movement in the canopy, however, seldom proceeds very far, and most travel takes place on the ground. Bonobos are similar in size to Chimpanzees. Adult coloration in both species is about the same, but unlike infant Chimpanzees, infant Bonobos are black-faced from birth, with just a thin pink area around the mouth. Bonobos have longer limbs than Chimpanzees, the head is smaller, and chest girth is small relative to height. Overall, Bonobos have a more gracile, or slender, build than Chimpanzees. They exhibit moderate sexual dimorphism, with adult males weighing 37–61 kg and measuring 77–96 cm tall and adult females weighing 27–38 kg and measuring 70–76 cm tall. These figures are within the range of variation of Chimpanzees, so the name “Pygmy Chimpanzee” for the Bonobo is inaccurate. The skull of the Bonobo is more gracile than the Chimpanzee and absolutely smaller; the two species can be unfailingly discriminated by skull size. The arms of Bonobos are longer than the legs but not much; the intermembral index (arm:leg ratio ×100) may be only 100, or slightly more. The feet are designed more for grasping than walking, and the second and third toes are partially fused. The thumbs are short. The vulva is more forwardly placed in Bonobos than in Chimpanzees. There is sexual dimorphism in the canines, which are longer in males than in females. The pelage is entirely black, although it may turn more of a grayish color with age, and the young are born with a white rump tuft, which is retained later in life than in Chimpanzees. Bonobos have relatively small ears and a relatively high forehead. They have long hair on the head that looks as if it is parted, and they do not go as bald as Chimpanzees until reaching old age. Bonobos are lighter and more compactly built than Chimpanzees, which allows them to be much more arboreal and agile. Movement is mainly quadrupedal climbing and suspensory swinging through the trees, with occasional leaping between branches. On the ground, individuals move quadrupedally by means of knuckle-walking. Bonobos show a greater predisposition for bipedal walking than other great apes due to a more centrally positioned foramen magnum, longer thighbones, longer feet, and differential distribution of body weight.

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Pan paniscus Lola ya Bonobo Sanctuary, W DR Congo. Photo: Russell A. Mittermeier/ Conservation International

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FAMILY HOMINIDAE Great Apes

About 40% of groups of “Mountain Gorilla” (as the beringei subspecies of the Eastern Gorilla is known) contain more than one adult (silverback) male, and some as many as nine, along with females and their infant, juvenile, and subadult offspring. The typical group size is ten weaned individuals, although up to 65 have been recorded. The Mountain Gorilla is not territorial, and there is extensive overlap in the home ranges of different groups. Changes in the composition of the group, such as the loss of the dominant male, may cause them to change their core ranges. Neither males nor females show any great fidelity to a site. The daily and annual home ranges seem to vary in size with elevation and therefore with the subspecies. Fruit availability decreases with increasing elevation, and with less fruit in their diet, gorillas move shorter distances. Groups of Mountain Gorilla in the Virunga Mountains use areas as small as 6 km2, but as large as 34 km2 over a year. They remain in the parts of their home range where the quality and abundance of food are currently highest, traveling more when less food is available and returning to areas where the foods they exploit are most quickly renewed. Mountain Gorillas spend as little as 6·5% of their daylight hours traveling and 55% foraging, with long rest periods accounting for most of the remaining time.

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Gorilla beringei beringei Virunga National Park, NE DR Congo. Photo: Konrad Wothe/ Minden Pictures/ASA

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FAMILY HOMINIDAE Great Apes

Pan paniscus Kokolopori Bonobo Reserve, NC DR Congo. Photo: Christian Ziegler

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Habitat Most great apes live in closed, moist, mixed forest in the tropics of the Old World, which is probably the most complex ecosystem in which primates occur. The heterogeneity of these forests moved the 19th century traveler M. Kingsley to declare, “Unless you are interested in it and fall under its charm, it is like being shut up in a library whose books you cannot read, all the while tormented, terrified, and bored. But if you do fall under its spell it takes all the color out of other kinds of living.” The great apes exploit this phenomenal biodiversity and occupy a multitude of forest types—mixed lowland, swamp, seasonally inundated, secondary, gallery, coastal, submontane, and montane among them. Great apes are found between sea level and 3800 m above sea level. Chimpanzees occur throughout much of the geographical range of both Eastern and Western gorillas, and they can be sympatric at all but the highest elevations. The largest populations of all great ape species are found below 500 m in the vast terra firma and swamp forests of Africa and Asia, where canopy cover is maintained year-round and rhythms of production are determined by fluctuations in rainfall, with little discernable change in temperature. Mature lowland forest typically has a 30–40 m high canopy, and where it is continuous, ground vegetation is sparse. However, tropical forests are intrinsically dynamic, and tree falls create gaps where an understory of palatable herbs flourishes, and these are particularly important to the African apes. Semi-deciduous forests are a mix of evergreen and deciduous trees, where the production of leaves and flowers tends to peak biannually. Many tropical trees produce fleshy fruits adapted to mammalian dispersion, and these are the preferred foods of great apes. Fruiting patterns of any particular species may be synchronous or asynchronous, and crops may be large or small. Bornean forests are renowned for their irregular supply of food for fruit-eating animals. Forests dominated by Dipterocarpaceae are characterized by synchronized production of massive crops of wind-dispersed seeds at irregular intervals of two to ten years. In the years between mast fruiting, there is a paucity of food for orangutans, rendering dipterocarp forest relatively inhospitable. The second major forest type on Borneo is peat swamp, which develops where lowland forest has become established on flooded soils. Water inhibits the decomposition of fallen vegetation and peat accumulates, creating an acidic environment that many tree species cannot tolerate. Nonetheless, peat swamps are an important habitat for orangutans and harbor perhaps 40% of Borneo’s surviving great apes. Sumatra’s predominantly volcanic soils are more fertile than soils on Borneo, and the lowland swamps, plateaus, and mountainous regions are generally better habitat for orangutans, principally because dipterocarps are not so widespread and preferred fruit trees occur at higher densities. This is particularly true of figs, noted as keystone species for primates in both Asia and Africa, due to their general year-round availability of their fruit. There can be more tree species in a single square kilometer of tropical rainforest than are native to all of North America. Although less species rich than South-east Asia, the Congo Basin is more diverse than other regions of Africa. The semideciduous Guineo-Congolian lowland forests grow on welldrained soils and are largely evergreen. Western Lowland Gorillas, Central Chimpanzees, and Bonobos are all found in Central Africa, where thousands of kilometers of undulating forest remain intact and uninhabited by humans. Food for great apes is widely available in the heterogeneous tropical African forests, with hundreds of tree species occurring at low densities, except where Gilbertiodendron dewevrei (Fabaceae) occurs in monodominant stands clearly marked by a lack of herbs. Great apes avoid these relatively poor areas except during mast fruiting, which occurs every four to five years. In mixed forest, where the canopy is broken, monocotyledonous plants dominate the understory. The arrowroot (Marantaceae) and ginger (Zingiberaceae) families are important sources of food for gorillas, Chimpanzees, and Bonobos. In the so-called Marantaceae forests of Central Africa, Aframomum (Zingiberaceae) and species such as Haumania liebrechtsiana and Megaphrynium macrostachyum can form dense thickets. Gorillas are surprisingly abundant in swamps of Raphia palm (Arecaceae) and reach their highest numbers in a mosaic of

swamp and Marantaceae forest, frequenting mineral rich, swampy clearings (locally called “bais”), where aquatic and semi-aquatic plants in the families Hydrocharitaceae, Cyperaceae, and Poaceae (or Gramineae) form a floating mat. A mosaic of swamp and terra firma lowland forest with a lush understory of terrestrial or aquatic herbs is also a key habitat for Bonobos. The upper elevational limit at which orangutans are regularly found is 500 m in Borneo and 1000 m in Sumatra. Occasionally, lone “wandering” males are seen in the montane highlands, but many trees with fruits preferred by orangutans disappear above 750 m. African apes occupy a much wider elevational range. Although the vast majority of gorillas, Chimpanzees, and Bonobos are found below 700 m, smaller populations of gorillas and Chimpanzees can be found at higher elevations. Forest often remains on mountaintops that are too steep to cultivate. Submontane and montane forests differ in character compared with lowland forest: trees are lower in stature, canopy heights drop to 15–25 m, and diversity of woody plants and tree density decrease. In the mountainous regions of West Africa, montane forests give way to grassland plateaus crisscrossed by gallery forests. Much of the Albertine Rift Highlands of eastern DR Congo, Rwanda, and western Uganda are steep hills and valleys, oscillating between elevations of 600 m and 1300 m. Submontane and montane forests are interspersed with areas of Cyperus (Cyperaceae) swamp and peat bog. Above 2100 m, bamboo (Arundinaria alpina, Poaceae) appears in the forest. Above 2500 m, bamboo is interspersed with dwarf forest and subalpine scrub, and where it succeeds in impeding the establishment of other plant species, bamboo forms an elevational belt. Where the canopy is discontinuous, lianas and woody vines flourish; Mimulopsis arborescens (Acanthaceae) and Sericostachys scandens (Amaranthaceae) are common. The peaks of the Virunga Volcanoes reach elevations of 4507 m and have distinct strata. Above the bamboo zone is woodland characterized by Hagenia abyssinica (Rosaceae), Hypericum revolutum (Clusiaceae), and a dense herbaceous layer.

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Chimpanzee (Pan troglodytes) and Bonobo parties travel in single file, with the adult females and young in the middle of the line. These traveling parties can be noisy, and Bonobos are particularly vocal. Male Bonobos also drag branches to initiate and coordinate group travel and to herd females while traveling. Chimpanzees also adopt the singlefile formation when patrolling their boundaries and hunting monkeys, but at these times, they are mostly silent. Bonobos do not patrol their boundaries and are far less aggressive than Chimpanzees toward members of other groups.

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FAMILY HOMINIDAE Great Apes

The subalpine zone features stands of Dendrosenecio erici-rosenii (Asteraceae), Lobelia giberroa, and L. mildbraedii (Campanulaceae), grading into an alpine zone above 3600 m, where woody plants are sparse. The elevational limits of great ape distribution are not easy to establish, but a Western Lowland Gorilla nest was recorded at c.620 m, and a Central Chimpanzee nest at c.740 m in Equatorial Guinea, and a Western Chimpanzee nest was observed above 1600 m in Liberia. Cross River Gorillas and Nigeria-Cam-

eroon Chimpanzees range to 2000 m in the volcanic uplands of the Cameroon Highlands, but only the eastern taxa occur above 2000 m. The presence of Eastern Chimpanzees has been confirmed at elevations of 2790 m in southern Rwanda. Only Mountain Gorillas have adapted to elevations above 2900 m, and they range up to 3800 m. Chimpanzees and Bonobos are not confined to dense forest and are capable of occupying a wider range of habitat types than other great apes. Chimpanzees are notable for their use of mosaics of savanna woodland, gallery forests, and relatively impoverished dry forests at the geographic extremes of their distribution in Guinea, Mali, Senegal, and Tanzania. The extensive miombo woodlands in Tanzania were created by forest clearance and are maintained by fire and grazing. The western and southernmost populations of Bonobos inhabit mosaics of swamp forest, dry forest, marshy grassland, and savanna woodland. In these open habitats, Chimpanzees and Bonobos depend heavily on any available tree cover for shade and nesting, but only about 2% of these ecosystems is evergreen forest, usually occurring as gallery forests. Large-scale conversion of forest to alternative land-uses is accelerating, and great apes are rapidly losing ground. Great apes can persist in disturbed areas, such as those that have been moderately logged, albeit at lower densities and only in mixed landscapes. South-east Asian forests are being cleared to make way for oil palm (Elaeis guineensis, Arecaceae), pulpwood plantations, and logging concessions. Orangutans leave forest being logged to seek refuge in surrounding areas, but they will return as the forest regenerates. Degraded forests do not meet all of the orangutans’ biological requirements; they need a mosaic of habitat types, as is found in the highly fragmented Kinabatangan floodplain of Malaysia, where riparian and mixed lowland dipterocarp forest are still found along the riverbanks. Recently, orangutans have been found to persist in Acacia (Fabaceae) and Eucalyptus (Myrtaceae) plantations, although the long-term viability of these individuals is unknown. Chimpanzees also seem able to adapt to moderate habitat disturbance, such as selective logging. Remarkably, some Chimpanzees survive in landscapes dominated by agriculture and in close proximity to humans. A recent survey in Sierra Leone revealed that one-half of the Chimpanzee population lives outside protected areas, traveling between the few remaining forest patches, finding food and shelter in farmbush (secondary growth and scrub on farmland) and secondary forest, and relying heavily on crops growing in cultivated fields. It is not yet clear if these individuals are just remnants of a dwindling population, but every other known population of great apes requires some access to forest for food and shelter. Great apes in modified habitats depend on resources elsewhere in the landscape, and habitat connectivity via networks of forest corridors must be maintained if they are to survive.

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General Habits

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Much of the preferred food of great apes is found in the canopy, and all age classes feed above ground. Even the largest great apes occasionally climb as high as 40 m to forage. Because of their large size, adult male gorillas and orangutans usually stay near the main trunk or on major branches, sitting or standing while they eat. Orangutans are almost exclusively arboreal, and only flanged male Bornean Orangutans often travel on the ground. Orangutans use lianas to move through the canopy, particularly for vertical climbing and descent. Adult females use more suspensory behavior than do flanged males, but less than juveniles. One of the most common postures adopted by feeding adults is “forelimb-hindlimb suspend.” The African apes are semi-terrestrial. Ascension of trees and movement in the canopy are by quadrumanous climbing and scrambling and quadrupedal walking along branches. Suspensory underbranch postures are usually used only by smaller individuals, and brachiation is rare. They descend feet first, and some individuals transfer into smaller trees or saplings on the way down, or use lianas or vines to reach the ground. If startled, they slide rapidly down the trunk like firemen on a pole, sometimes jumping the last few meters to the ground. Smaller individuals are able to transfer between canopies by swaying

Between the ages of eight and 15 years, the male Chimpanzee (Pan troglodytes) shows an increase in muscle mass, testicular volume, and aggression. Testosterone levels are positively associated with both dominance rank and rates of aggression directed at others. Although closely related to Chimpanzees, Bonobos are much mellower and show dominance relations among themselves with less aggression, and they react to stress by sharing, playing, and engaging in sexual activity. Pan paniscus Lola ya Bonobo Sanctuary, W DR Congo. Photo: Régis Cavignaux

Dominance in the Chimpanzee is expressed primarily through ritualized displays rather than physical aggression. Male Chimpanzees rock from side to side while standing upright. They sometimes snap saplings and branches, and drag large objects and throw smaller ones. They raise the hair on their bodies to make themselves appear bigger. Sometimes a displaying Chimpanzee runs apparently at random, but it may direct its aggression at a subordinate male, or a unreceptive female that it has taken a dislike to. Challenges to dominant males can be more serious in their outcomes. On the rare occasions when encounters turn to violence, the large canine teeth can inflict serious wounds, including torn ears and bitten-off fingers and toes. Pan troglodytes Photo: Gerard Lacz/VWPics

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FAMILY HOMINIDAE Great Apes

African apes sometimes stand upright when displaying, probably to make themselves appear more conspicuous. Adult male gorillas, like the Eastern Gorilla shown here, adopt a variety of postures to intimidate rivals, including strutting with stiff legs, and beating their chests rhythmically with alternating cupped hands. Aggressive encounters between two male gorillas can include blood-curdling roars, or hoots that build in pitch and volume, with or without a punctuating chest-beat. The displays become more emphatic as the gorillas close the distance between them. Chest-beating may be followed by a charge on all fours, during which the gorilla may slap and tear at anything in his path. Females, juveniles, and even infants beat their chests, but they lack the amplifying air-sacs of adult males. Gorilla beringei beringei Virunga National Park, NE DR Congo. Photo: Konrad Wothe

Multimale reproductive groups are rare in the Western Gorilla, and groups generally include only one silverback male. Young sexually mature males, which have not yet developed their silver backs, are known as blackbacks. The dominant silverback maintains his position by displays of aggression, which are intended to impress and reassure females as much as to intimidate other males. Many males leave their natal groups as blackbacks or young silverbacks and become solitary.

ently on branches, but usually hesitantly and always within arm’s reach of their mother. Juveniles often dangle by one limb in play. The amount of time that African apes spend above ground varies between species and age classes; for example, adult female Chimpanzees average 60% of daytime in trees and adult male Chimpanzees about 40%. Bonobos spend 44% of daylight hours in trees and do much of their feeding and resting at 30 m or more above the ground. Mountain Gorillas are the least arboreal. Although bulky adult male Mountain Goril-

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back and forth until they can reach a neighboring tree. Chimpanzees and Bonobos are more agile in the trees than gorillas, and Bonobos display more arboreal leaping and diving movements than Chimpanzees do. Great apes not only feed but also rest and socialize in trees, and all age-sex classes rest supine on branches. Mothers carry their infants while climbing. Infants slide round from a dorsal position to rest between their mothers’ thighs when she sits. Even normally ventrally riding infants may move independ-

Gorilla gorilla gorilla Photo: Konrad Wothe

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FAMILY HOMINIDAE Great Apes

Male infant gorillas play more than female infants. Males are practicing the skills that they will need when they are mature, while by playing with immature males, females begin to adopt the patterns of proximity and affiliation with males that will be characteristic of their adulthood. Adult females develop strong bonds with the silverback, and they rely on him to protect their infants from unrelated males. Because there is no potential alternative dominant male in Western Gorilla groups, a group may disintegrate when the silverback dies. In such cases, females join another group or form a new one with a solitary silverback, but the new silverback may kill their unweaned offspring. Gorilla gorilla gorilla Photo: Konrad Wothe

las are excellent climbers, but only 3% of their daily activity takes place in trees. African apes travel all but the shortest distances on the ground. Terrestrial locomotion is by quadrupedal knucklewalking, whereby weight is borne on the backs of the fingers (dorsal surfaces of knuckles and medial phalanges) and the soles of the feet, which are in contact with the ground. Knuckle-walking requires morphological adaptations that only the African apes have; orangutans do not. During the rare instances that orangutans are on the ground, they walk on their fists or exhibit hand-assisted bipedality. African apes tend to use bipedalism in short bursts: gorillas and Bonobos adopt an upright posture to wade in water, and Chimpanzees and Bonobos stand to peer over vegetation, or to carry objects in their hands. Goril-

las, Chimpanzees, and Bonobos use bipedal locomotion when displaying. Bonobos inhabiting savanna woodland are thought to be the most bipedal of the great apes. Great apes are diurnal and need long periods of sleep. Every night, all weaned individuals build a nest to sleep in—bending, breaking, and weaving leafy branches around and under their bodies. These beds are usually constructed high in the trees, and there is apparent uniformity of nest-building across great ape species and populations. It seems to be an innate behavior, refined by social learning and lots of practice. Infants sleep with their mothers for several years until they are weaned, and nests built by juveniles are often crude. Various anti-predator, anti-parasite, and anti-disease functions have been ascribed to nest-building behavior, particularly

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The social organization of the Bonobo is unique among nonhuman primates, in that females are strongly bonded, whether or not they are related. As a result of these supportive coalitions, female social status is roughly equal to that of males. Older, high-ranking females are the preferred grooming partners of newly immigrated females. However, grooming between Bonobos of the opposite sex is more frequent and prolonged than grooming between same sex pairs. This is partly because the strong bond between the mother and her son continues into his adulthood, but adult males also form friendly pair-relationships with unrelated adult females. Grooming is reciprocated, and “groomer” and “groomee” may switch roles.

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Pan paniscus Kokolopori Bonobo Reserve, NC DR Congo. Photo: Russell A. Mittermeier/ Conservation International

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FAMILY HOMINIDAE Great Apes

Related female gorillas maintain close proximity and groom each other. But there is little affiliative behavior between unrelated females, and relations between them range from neutrality to hostility. Most aggression within the group is between adult females, although this involves more screaming than physical contact and is often ended by the intervention of an adult male. Younger silverbacks in multimale Eastern Gorilla groups are more supportive of unrelated immigrant females than the dominant silverback, and they may use grooming to develop mating relationships with them. Gorilla beringei beringei Virunga National Park, NE DR Congo. Photo: Konrad Wothe

The female Chimpanzee spends most of the time alone with her dependent offspring, but she sometimes joins other mother– infant units. Juveniles and adolescents also associate with their mothers. Grooming in Chimpanzees serves the practical purpose of removing dead skin and parasites, but it is also used to maintain cohesion, repair relationships after conflicts, and reestablish bonds after absence. Most adult females have at least one preferred female partner, and these relationships may be ended only by death. Grooming-partner preferences are less long-lasting and are associated with short-term advantage such as support in conflict and food-sharing. Pan troglodytes schweinfurthii Mahale Mountains National Park, W Tanzania. Photo: Günter Ziesler

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branches into the nest. Last, branches are braided until the nest has a strong structure. All of this takes fewer than ten minutes. Nest materials come from the immediate surroundings. Ordinarily, Chimpanzees use materials from only one tree in each nest, and several Chimpanzees may sleep in the same large tree. Bonobos’ night nests are often more elaborate, and a single nest may incorporate the branches and foliage from several trees. If nests are constructed in the tops of small trees or saplings that have no substantial branches, the small branches are folded in toward the crown or two small trees are locked together. Orangutans and Bonobos sometimes place loose leafy twigs on top of their bodies while lying in their nests. Gorillas usually nest on the ground, on cushions of vegetation made of the large ground herbs (Marantaceae and Zingib-

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because nest reuse is uncommon. It is most likely that nests provide comfort during sleep and that nesting above ground is a way to avoid predators and large forest mammals that are active at night, such as bushpigs and elephants. The basic requirements of nest trees are a firm base, abundant foliage, and pliable branches. Trees with fruit crops that will attract nocturnal feeders, such as fruit bats, tend to be avoided. A detailed description of the orangutan’s nest-building sequence by D. Prasetyo and colleagues is abridged here: first, a tree is carefully selected among the many available. Second, orangutans usually stand in a fixed location and are precise and selective in choosing branches for the foundation, which is formed by pulling some big branches together and uniting them under the body. Third, a mattress is made by bending smaller leafy

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FAMILY HOMINIDAE Great Apes

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eraceae) and prevent direct contact with damp soil, although Western Lowland Gorillas sometimes sleep on bare ground. In the swamps, Raphia fronds are a popular building material. Both gorilla species often build nests on fallen tree trunks, a few feet off the ground. Seasonal trends have been detected in several populations of Western Gorilla, whereby fewer nests are constructed on the ground during the wettest months. The difference is striking for Cross River Gorillas at relatively high elevations where night-time temperatures are low: the proportion of ground nests is 31% in wettest months compared to 81% in drier months. Chimpanzees in south-eastern Guinea have a proclivity for ground nesting, as do a few Chimpanzees in some other populations. Nest size tends to correlate with the arm’s reach of the builder, because great apes form nests around their bodies. Height of nesting varies with habitat type, substrate, tree morphology, availability of suitable materials, and body size. Immature great apes tend to make nests at higher levels in the canopy than do adults. Conversely, adult male gorillas build the fewest tree nests. The range of heights of Chimpanzees’ nests is predictably greater in mature forest than in savanna woodlands. Bonobos usually nest 15–30 m above ground. Where gorillas and Chimpanzees are sympatric, there is significant overlap in the heights at which they nest, but on average, gorillas build lower tree nests (9·6 m compared to 17·3 m). Great apes also rest in nests during daylight hours. Day nests serve for short periods and tend to be structurally simpler than night nests. Orangutans, Chimpanzees, and Bonobos usually make day nests in trees. Gorillas, and occasionally Chimpanzees, mould simple resting places on the ground between bouts of feeding. Orangutans have been observed covering their nests with leaves when it rains and holding vegetation above their heads as shade from the sun. H. Bingham in 1932 commented that nest-site selection was a matter of expediency, rather than foresight, and it is likely that the most important factor influencing where great apes spend the night is usually no more important than where they were feeding at the end of the day. Nest-building techniques and preferences are similar across populations of great apes, and most variation is environmentally determined; for example, plant materials used in construction depend on local availability. Nevertheless, location is critical for populations vulnerable to poachers. Western Lowland Gorillas in Cameroon and Grauer’s Gorillas in eastern DR Congo are known to nest in steep locations that humans would find difficult to reach. To prevent themselves from sliding down steep inclines during the

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night, gorillas anchor and level off the nest vegetation, or prop the nest against the base of a tree, demonstrating intelligence and engineering skill. In the tropics, daylength changes little during the year. Great apes leave their nests soon after sunrise, maybe later if it is raining, and are active for 10–12 hours until sunset. Their main activities are foraging, resting, traveling, and socializing. They tend to feed intensively in the early morning and then alternate periods of foraging, resting, and traveling throughout the day. On average, orangutans spend 32–61% of active time foraging, 19–54% resting, 10–17% traveling, and 2% in other activities. Bornean Orangutans generally spend more time resting and less time foraging than Sumatran Orangutans, but differences in activity budgets are more clear-cut when comparing habitat types; orangutans in peat-swamp forests spend more time foraging (more than 50%) and traveling than orangutans in most mixed-dipterocarp forests, which spend more time resting and less than 50% foraging. Low levels of activity seem to be a strategy for energy conservation on a poor-quality diet. Similarly, Western Gorillas forage and travel more and rest less (67% foraging, 21% resting, and 12% traveling) than Mountain Gorillas, which have long rest periods in the middle of the day (55% foraging, 34% resting, and 7% traveling, 4% in other activities). Activity budgets of Chimpanzees vary between sites: 43–55% foraging, 25–39% resting, and 12–14% traveling. Bonobos spend 35–61% of their day foraging, 13–37% resting, and 15–25% traveling. On a daily basis, great apes travel is between food patches, mainly searching for fruit and leaves. Finding enough food in diverse tropical forest is a challenge. Although dozens of species produce fruit in any given year, individual trees bear crops for only a few days or weeks. Foraging in such environments requires spatial memory and mental mapping, and Chimpanzees have been shown to have both. Chimpanzees have sophisticated mental representations of their home range and are capable of memorizing the individual locations of thousands of trees over many years. This phenomenal cognitive capacity is likely to be shared by orangutans, gorillas, and Bonobos, enabling them not only to find ephemeral fruit but also to travel directly and efficiently between resources. The other great apes do not show the Chimpanzee’s propensity for tool-use. Chimpanzees are extraordinarily proficient at manufacturing and using tools, and are, with some populations of robust capuchin monkeys (Sapajus) in northeastern Brazil, the only living non-human primates to do so habitually. Individuals in all known populations of Chimpanzees

A high-ranking male Chimpanzee may sometimes demand grooming from a subordinate without offering to groom in return, but grooming is usually reciprocated. Male–male grooming among Chimpanzees is relatively more common than grooming between males and females or among females. Males use alliances to bolster their position in the hierarchy, and mutual grooming is thought to service the relationships and coalitions that can lead to higher status. Immature males spend increasing amounts of time with other males as they grow up, despite frequent aggression from older males. When they mature, at about 15 years of age, they are integrated into the male networks and are dominant to all females and immature individuals. Pan troglodytes schweinfurthii Mahale Mountains National Park, W Tanzania. Photo: Günter Ziesler

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FAMILY HOMINIDAE Great Apes

The flanged male Sumatran Orangutan rests the most, and travels the least, of all age and sex classes in this species. Flanged male orangutans are extremely aggressive to other adult males and are able to monopolize a high-quality home range, into which they can attract receptive females. Unflanged males are more tolerant of other males, and females are more gregarious still. Females sometimes associate with familiar or related females and their offspring, and travel together, as do adolescents of both sexes. Forests on Sumatra produce abundant fruit, and Sumatran Orangutans have higher population densities than Bornean Orangutans (Pongo pygmaeus). Consequently, social interactions occur at higher rates in the Sumatran species, from group-formation to aggression. Pongo abelii Gunung Leuser National Park, N Sumatra. Photo: Cyril Ruoso

The adult male Chimpanzee spends an average of 40% of the day in trees, compared to 60% for female Chimpanzees. African great apes not only feed in trees, but also relax and socialize in them. All age and sex classes, including the heavier males, rest on their backs or sides on branches. The amount of time Chimpanzees spend resting varies among populations and sites, from 25 to 39%. In Tai National Park, Ivory Coast, Chimpanzees of the verus subspecies sometimes make day nests in trees during long rest periods, and on the very cold days in December when the Harmattan wind blows, they build day nests on the ground. Pan troglodytes schweinfurthii Mahale Mountains National Park, W Tanzania. Photo: Günter Ziesler

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Most Chimpanzees excel at extractive foraging for aggressive ants and termites, luring them from arboreal nests or earthen mounds. Tools are adapted for specific tasks: flexible probes to gather termites (Macrotermes, Termitidae) and carpenter ants (Camponotus, Formicidae); stiff vegetation to dip for army ants (Dorylus, Formicidae); and puncturing sticks to perforate termite mounds. Again, the techniques take years to perfect. Chimpanzees across their geographic range make “sponges” by chewing leaves or fiber that they use to extract drinking water from tree hollows. Chimpanzees in hot-dry regions use their hands to dig wells in sandy riverbeds when drinking water runs short. Chimpanzees also dig up tubers, with (Tanzania) or without (eastern DR Congo) the aid of sticks or pieces of bark. Tool

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use tools, and more than one-half of the tool types recorded are used in a feeding context, to extract insects or to smash open hard-shelled fruits (percussive technology). Nut cracking is one of the most sophisticated of these behaviors, taking years to learn. Western Chimpanzees specialize in using sticks and stones as hammers and anvils. The only other population that is known to crack nuts this way is the Nigeria-Cameroon Chimpanzee in Ebo Forest, south-western Cameroon. Western Chimpanzees in Guinea have developed a pestle-and-mortar system, whereby they climb to the top of oil palms and use palm fronds to pound and soften the apical growth tip, which can then be scooped up with the hands. In Senegal, they use stones to break open baobab fruit (Adansonia digitata, Bombacaceae).

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FAMILY HOMINIDAE Great Apes

When compared with the “Mountain Gorilla” (Gorilla beringei beringei), the Western Gorilla spends more time feeding and traveling, but less time resting (21% versus 34%). This disparity may be explained by the more scattered nature of the foods exploited by Western Gorillas. Western Gorillas eat more fruit than is available to Mountain Gorillas, who eat more leaves. Fruit is also more easily digested than leaves, so Western Gorillas may not need to spend so long resting while waiting for their stomachs to clear. Gorilla gorilla gorilla Batéké Plateau National Park, SE Gabon. Photo: Martin Harvey/DRK

use may be critical to the survival of Chimpanzees in marginal habitats, enabling them to exploit otherwise inaccessible foods. Non-food uses of tools include using leaves to clean their own bodies, such as using handfuls of leaves to wipe hair or body surfaces and dabbing wounds. Chimpanzees also use objects as weapons, throwing them at conspecifics or dangerous animals. Each community has its own repertoire of tools and techniques, developing a kit of tools (8–22 types), and crosspopulation differences have emerged. Bornean Orangutans rarely use tools. Sumatran Orangutans in dryland forests have not been seen to use tools, but those living in swamp forests have. They use sticks to exploit termites, ants, or stingless bees (Trigona, Apidae) living in tree holes by hammering to break open nests, poking to stir the adult insects

to exit, and scraping to obtain eggs, larvae, or adults. Some Sumatran Orangutans use leaf “padding” to protect their hands when handling spiny fruits or thorny branches. Similarly, Chimpanzees in Sierra Leone make stick “sandals” to protect their feet from Kapok thorns (Ceiba pentandra, Bombacaceae). Bonobos rarely use tools in the acquisition of food; however, they do make moss sponges, napkins, and tooth picks and drape vegetation over their head and shoulders as hats or umbrellas during heavy rains. Great apes generally show discomfort in heavy rain. Gorillas stop feeding and bed down in day nests during heavy rain, and some orangutans use vegetation as umbrellas. Few great apes are challenged by thermoregulation because the temperature range in lowland forest is relatively narrow and humidity is always high. The extremes faced by great apes

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The vocal activity, mostly grunts, of the “Mountain Gorilla” (as the beringei subspecies of the Eastern Gorilla is known) increases significantly toward the end of rest periods and may be used to assess the readiness of group members to depart and coordinate group movements. Among Eastern Gorillas, the proportions of time spent resting, moving, and feeding vary little among adult females, black-backed males, and juveniles. Although silverbacks feed for longer and spend less time moving, the difference in feeding time between silverbacks and females is small in comparison to the two-fold disparity in their body weights.

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Gorilla beringei beringei Virunga National Park, NE DR Congo. Photo: Russell A. Mittermeier/ Conservation International

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FAMILY HOMINIDAE Great Apes

Every night, all weaned individuals of every great ape species build a nest to sleep in. The Bornean Orangutan takes less than ten minutes to pull several big branches together, bend smaller branches into a mattress, and bind the structure together by braiding more supple branches through it. In rainy weather, Bornean Orangutans sometimes add a second structure (a roof) above the nest. Nests are often built in, or close to, the last feeding site of the day, and may help the ape to guard good feeding resources. Bornean Orangutans sometimes build cruder “day nests” for the noonday rest period, but less often than the Sumatran Orangutan (Pongo abelii), which does so almost every day. Pongo pygmaeus wurmbii Gunung Palung National Park, West Kalimantan, W Borneo. Photo: Tim Laman

are in the Mountain Gorillas’ volcanic peaks where night-time temperatures frequently fall to 0°C and in south-eastern Senegal where maximum temperatures exceed 40°C in the dry season. Chimpanzees cope by seeking shade in caves to escape the heat of the day, immersing themselves in rainwater pools during the hot and humid early rainy season and foraging and traveling on moonlit nights.

Communication Great apes communicate with a broad range of vocalizations that are usually specific to particular contexts, such as mating, fear, threat, and appeasement. Numbers of call types described

range from 16 for Mountain Gorillas to 32 for orangutans; however, many calls grade into one another, so describing a discrete number can be subjective. Close calls are categorized as those used for short distance communication, usually within 25 m, and are frequent and quieter. These are used to signal location and maintain contact in dense vegetation where individuals are unable to see each other, particularly if they disperse while foraging. Intragroup calls also seem to facilitate coordination of group travel. Infants of all the great apes whimper, cry, and scream in situations of fear, distress, frustration, and protest; the pitches of these calls increase with the level of anxiety and agitation. Long-distance calls are loud, audible over distances of several hundred meters, and used primarily by adult males to announce their presence and location, or in response to

Pan troglodytes ellioti Drill Ranch Afi Mountain, Cross River State, S Nigeria. Photo: Cyril Ruoso/JH Editorial/ Minden Pictures/ASA

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The Chimpanzee generally uses materials from only one tree in each nest. Nests are normally built between 6 m and 25 m above the ground, depending on the types of trees available. The range of heights is greater in mature forest, where trees are taller, than in savanna woodlands. Lighterbodied immature Chimpanzees can build higher nests than adults. Nest-site preference also varies among populations. Chimpanzees usually make arboreal nests, but some grassland/savannah populations, and also the Chimpanzees of the West African subspecies verus in the Nimba Mountains, Guinea, build an unusually high percentage of nests on the ground.

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FAMILY HOMINIDAE Great Apes

A Bonobo will sometimes cover its body with loose leaves while lying in its nest, perhaps for warmth or for shelter from heavy rain. Bonobos’ nests often are more elaborate than those of the Chimpanzee (Pan troglodytes). The branches of several trees are sometimes folded in to make the foundation of the nest, or two or more saplings that could not support a Bonobo alone are locked together. Bonobo nests are commonly found close together, in groups of two to twelve or more, whereas the majority of Chimpanzee sleeping sites consist of only one nest. Pan paniscus Kokolopori Bonobo Reserve, NC DR Congo. Photo: Christian Ziegler

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potential danger, such as a rival male or a human. The most conspicuous calls are described below. The orangutan’s “long call” is one of the loudest and most frequently produced vocalizations in its repertoire, often audible to humans up to 1500 m away. Only flanged adult males and males undergoing the transition to full maturity are capable of these bellowing calls, produced using a throat pouch that is inflated and acts as a resonance chamber, amplifying the sound. Long calls build over one to two minutes into a full-blown roar in three stages: a grumbling introduction, a pulsing climax, and a gradually subsiding repetitive gurgling. Speed and duration of the call may convey information such as the signaller’s condition and fighting ability. High-ranking males call two to four

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times a day; call frequency increases where local density of orangutans is high. They often call in the direction in which they are traveling, and it has been suggested that flanges help recipients to determine the direction of a caller. Orangutans use long calls as a spacing mechanism—their calls allow other males to space themselves out and avoid conflicts. Long calls discourage subordinate males from coming into a dominant male’s domain. Conversely, a dominant male will approach calling subordinates and displace them. Males also use long calls to attract receptive females and coordinate range use with adult females. Females can distinguish familiar from unfamiliar males if they are within 400 m of the caller, and they may keep track of a particular male’s location via his calls. The “kiss squeak” is a common sound made by orangutans of both genders and all ages to indicate social tension or potential danger. It is a sharp intake of air through pursed-lips, which may be enhanced using a hand, wrist, or leaves. Immature individuals practice kiss squeaking during play. Orangutans that are not habituated to human presence will kiss squeak at human observers. Many components of the gorilla’s vocal repertoire are produced by adult males and are very loud, usually emitted during encounters with another group or a lone male. Various short barks convey mild alarm or curiosity. Roars are aggressive bursts of sound that can be blood curdling. Low-pitched “hoo” sounds build in pitch in a “hoot series.” Hoot series are given with or without a punctuating chest-beat. All age and sex classes of gorillas give mildly aggressive grunts and shrill, prolonged screams, particularly during squabbles. Members of a Mountain Gorilla group exchange vocalizations and generally increase their call rate before leaving a resting site, which might play a role in coordinating departure. Most Chimpanzee vocalizations are variants of four call types: grunts, barks, screams, and hoots. The “pant-hoot” is loud and distinctive and consists of four phases: (1) the introduction begins as repeated soft hoos, (2) the build-up is a series of increasingly louder hoos voiced on both inhalation and exhalation, which comes to (3) a climax of screams and sometimes barks and is followed by (4) a post-climax of soft hoos similar to the build-up but decreasing in pitch. Adult and adolescent males and females pant-hoot, but high-ranking males do so most often, and parties of males exchange pant-hoot choruses. Pant-hoots are given in a variety of circumstances, such as meeting up with other community members, arriving at fruiting trees, traveling, and early in the morning and late in the afternoon. Chimpanzees can differentiate between individuals by their pant-hoots, demonstrating that information about the callers’ identities is

Orangutans show none of the Chimpanzee’s (Pan troglodytes) dislike of water. Younger orangutans, especially, use water when playing. The young Sumatran Orangutan begins to play by itself at around three years old, swinging exuberantly by its hands or feet. However, it continues to associate with its mother every day until it is 7–9 years old, and social play (with other juveniles and adolescents, and unflanged males) does not begin until around this age. Pongo abelii Gunung Leuser National Park, N Sumatra. Photo: Konrad Wothe

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FAMILY HOMINIDAE Great Apes

Although preferring to keep dry, orangutans occasionally enter water to depths of around 60 cm (chest height). Although rarely, the Bornean Orangutan will wade across rivers, adopting an upright posture, as do gorillas (Gorilla) and Bonobos (Pan paniscus) when wading across streams and feeding on aquatic plants. Rather than avoiding water, Western Lowland Gorillas (G. gorilla gorilla) in northern Congo spend hours sitting in waist-deep water while they feed. Bonobos forage in streams and do not hesitate to wade waist-deep into pools to gather algae. Some Chimpanzees (P. troglodytes) use sticks to scoop floating algae from the surface of ponds without entering the water, but most avoid water completely. Pongo pygmaeus wurmbii Tanjung Puting National Park, S Borneo. Photo: Mitsuaki Iwago/ Minden Pictures/ASA

For some months of the year, Bonobos living in seasonally inundated forests spend much of their foraging time wading bipedally in water. Orphaned Bonobos at Lola ya Bonobo Sanctuary are similarly at home in water. They use sticks for support and perhaps also to gauge the depth before taking a step. Similar use of sticks when wading has been reported in gorillas (Gorilla) and at least once in wild orangutans (Pongo). Unlike Chimpanzees (Pan troglodytes), Bonobos rarely use sticks to acquire food (for example, by digging) and are not known to use them as weapons. Pan paniscus Lola ya Bonobo Sanctuary, W DR Congo. Photo: Martin Harvey/DRK

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day by most or all members of a party, in contexts similar to the Chimpanzee’s pant-hoot. There are two peaks in call rate: one in the morning when arriving at feeding sites and another in late afternoon when prospecting for nest sites. Individuals synchronize their calling and can sound like echoes of one another. F. de Waal described high-hoots as ear-piercingly shrill and explosive at close range and a common group response when Bonobos are excited. M. Bermejo and A. Omedes considered the vocal repertoire of Bonobos to be more complex than that of Chimpanzees and thus to have the potential to express a wider range of meanings. Adult male great apes perform iconic displays, usually designed to intimidate, and they throw objects to assert domi-

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encoded in the call and the size of a vocalizing group is likely to be conveyed in pant-hoot choruses. Pant-hoots seem to play a role in territorial behavior because Chimpanzees pay close attention to pant-hoots from neighboring communities and often respond to them. Interestingly, Chimpanzees reduce their call rate when crop raiding. Chimpanzees use barks in different contexts (for example, to alert neighbors to a snake). High-pitched screams can be long and intense and are given by Chimpanzees of any age when fearful, frustrated, or excited. Bonobo vocalizations have been described as “incessant chatter.” Their frequent, high-pitched dialogues are often accompanied by pointing gestures and facial expressions. The “high-hoot” is a long-distance call, produced throughout the

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FAMILY HOMINIDAE Great Apes

In the forests of Central Africa, the Western Gorilla comes to swampy clearings known as “bais” to eat mineral-rich aquatic plants. Gorillas’ diets are often low in sodium, which other populations remedy by eating decaying wood. Bais are also important sources of minerals for large mammals like the African Forest Elephant (Loxodonta cyclotis) and Forest Buffalo (Syncerus nanus) seen here. Several gorilla groups may use the same bai simultaneously and within sight of one another, without any sign of aggression among the males. Solitary males visit bais more regularly than groups and may stay there longer. Some groups with home ranges distant from the bais may visit less than twice a month. Gorilla gorilla gorilla Langoué Bai, Ivindo National Park, EC Gabon. Photo: Nick Garbutt

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nance. Male orangutans display by bristling their hair and shaking branches vigorously while loud calling. In fearful situations, female and immature orangutans shake or throw branches and kiss squeaking at the same time. Adult male gorillas adopt an array of postures intended to impress rivals, such as strutting with stiff legs, elbows bent outward, and hunched shoulders. Chest-beating is the rapid, rhythmic beating of the chest with alternating, cupped hands. Chest-beating is performed in many contexts from play to communication between groups, and by both genders of all ages of gorilla, but female and juvenile chest-beats lack resonance. Only in mature males is the sound amplified by laryngeal air

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sacs in the chest cavity. A full silverback display can incorporate charges, chest-beats, strutting, ground-thumping, and vegetation throwing. A charge alone by these powerful individuals is highly intimidating, particularly with the added emphasis of a scream or roar. Adult male gorillas emit a pungent odor from glands in the armpit when aroused by the sight or sound of other males. Male Western Lowland Gorillas in the Republic of the Congo have devised an unusual water display, leaping into streams to make a dramatic splash. Male Chimpanzees “drum” by rapidly and rhythmically striking buttress roots or tree trunks trees with their hands or feet. The low-frequency sound of buttress-drumming conveys information about the timing and direction of travel, carries a kilometer or more, and is often combined with pant-hoots. Some males perform dramatic “rain dances” before or during a storm, running back and forth, swinging on lianas, bending and sometimes breaking saplings. More generalized aggressive displays involve bipedal rocking, stamping, slapping other Chimpanzees, branch waving, throwing or dragging, and noisy charging. Their spectacular displays are emphasized by piloerection—the body hair standing on end. Chimpanzees use objects as clubs to strike another individual or as missiles to fling randomly (for example, rocks and broken-off branches). They are also capable of aimed throwing and will target conspecifics or other animals, such as baboons and humans. Bonobos show some behaviors similar to those of Chimpanzees. Males buttress-drum and make charging displays when excited, sometimes incorporating high hooting, branch dragging, or bending and then releasing saplings. They rock their upper body and adopt bipedal postures to walk or run short distances. Mature and immature individuals show antagonism by shaking branches or throwing objects at other Bonobos or humans. Males also use branch dragging to coordinate group travel. E. Ingmanson described how adult males seem to direct their branch dragging at adult females and called this “herding” behavior. Rather than being aggressive, noisy branch dragging focuses the group’s attention and is used to initiate movement in a specific direction.

Food and Feeding All great apes have similar dietary requirements and are fundamentally frugivorous. They have simple globular stomachs and lack fermentation chambers, so they are unable to digest large

The Sumatran Orangutan (Pongo abelii) and the Bornean Orangutan use leaves as umbrellas in heavy rain. Sumatran Orangutans also make a “gloves” out of leaves when handling spiny fruits or thorny branches. Such behavior is probably learned by watching others. Tool use is more common in swampforest populations of Sumatran Orangutan, where population densities are higher. Bornean Orangutans rarely use tools in the wild, but in captivity, they display complex cognitive behaviors including tool use. They have a slightly smaller average brain size than Sumatran Orangutans, which may be related to the greater sociality of the Sumatran species. Pongo pygmaeus Kalimantan, S Borneo. Photo: Cyril Ruoso

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FAMILY HOMINIDAE Great Apes

Gorilla beringei graueri Kahuzi-Biéga National Park, E DR Congo. Photo: Russell A. Mittermeier/ Conservation International

The Bornean Orangutan is generally less frugivorous than the Sumatran Orangutan (Pongo abelii). Borneo experiences extreme fluctuations in fruit production due to poor soils, seasonal changes, and the impact of El Niño temperature oscillations, which cause drought and food scarcity in some years. Bornean Orangutans supplement their diet with leaves, plant pith, and bark. Their teeth are adapted to more fibrous, tougher, and harder foods than eaten by Sumatran Orangutans and therefore have thicker enamel, and more crenulated upper surfaces to their molars. Pongo pygmaeus morio Wanariset Orangutan Reintroduction Project, E Kalimantan, SE Borneo. Photo: Konrad Wothe

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quantities of mature leaves or unripe fruit. They are largely restricted to eating plant parts that are not chemically defended and are easy to digest—succulent pulp, new leaves, shoots, and herbs. Large body size enables great apes to eat lower quality foods than most other primates, and the largest of them all—orangutans and gorillas—incorporate more poor-quality fibrous foods into their diets than do the smaller Chimpanzees and Bonobos. Diets of great ape are of course a function of what is available, but they are shaped by a strong preference for ripe, sugary fruit. When fruit is abundant, it forms more than 50% of feeding records, feeding time, or fecal samples. Bornean Orangutans are generally less frugivorous than Sumatran Orangutans because they experience more extreme fluctuations in food availability, with months when fruit consumption falls as low as 16% of their diet to highs of up to 99% when they gorge themselves during infrequent mast fruiting events. Sumatran Orangutans face less difficulty locating fruit because some high-quality crops are usually available. In Africa, interannual variation in fruit production is less dramatic. African apes in lowland habitats average 62–85% fruit in their diet, with marked changes throughout the year, but fruit shortages are less severe and less prolonged than in Asia. Seasonality and fruit availability decline with increasing elevation, and the degree of frugivory exhibited by gorillas is on a continuum: highest in Western Lowland Gorillas, lower but still an important component of diets of Grauer’s and Bwindi gorillas, and falling to negligible in Virunga Mountain Gorillas. The Chimpanzee’s degree of frugivory shows no such correlation with elevation; Chimpanzees do not occur at elevations such as those where fruit drops out of the gorilla’s diet. Groups of apes can deplete a ripe crop in an hour or so, but solitary individuals can spend several hours feeding in a single tree. Sitting, squatting, and standing positions are adopted during feeding, shifting position every few minutes; fruits and leaves are plucked by hand or with the lips. The tremendous strength of adult male orangutans and gorillas enables them to break fruit-laden branches and retreat with them to a safer position, usually closer to the main trunk. Smaller apes bend terminal branches within reach, without breaking them. Because they consume enormous numbers of ripe fruits and rarely damage the seeds, great apes are excellent seed dispersers. Much is known about this aspect of great ape ecology in the more terrestrial African apes. Some large seeds are

extracted with the fingers and others are spat out, but most seeds are swallowed passively with pulp. C. Tutin and M. Fernandez described how fruit is manipulated in the mouth by an extraordinarily mobile lower lip, separating and ejecting some fruit skins and large seeds. Chimpanzees also use their muscular lip used to compress food against the teeth and gums, before spitting out a wad of indigestible fruits parts—skin, some fiber, and very small seeds, such as those of Ficus (Moraceae) infructescences. Great apes disperse intact and viable seeds over far greater distances than smaller primates; thus, they are important highquality dispersers. They also eat large fruits that the smaller

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Fruit is seasonal and scarce in the submontane forests of Kahuzi-Biéga National Park, DR Congo, where the Eastern Gorilla (graueri subspecies “Grauer’s Gorilla,” shown here) and the Chimpanzee (Pan troglodytes) occur together. During the course of the year, the gorillas move more widely and eat from a much wider variety of plant species than the Chimpanzees, including many kinds of leaves and bark. The number of fruit species eaten by these Chimpanzees was similar to that for Chimpanzees in lowland habitats, but the gorillas ate a much smaller variety of fruit than their lowland counterparts.

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FAMILY HOMINIDAE Great Apes

Twice a year, at the beginning of each rainy season, “Mountain Gorillas” (as the beringei subspecies of the Eastern Gorilla is known) in the Virunga Mountains move into the bamboo zone and feed almost exclusively on new bamboo shoots for two to three weeks. Similarly, when in season, bamboo shoots form 70–90% of the diet of “Grauer’s Gorillas” (Gorilla beringei graueri) living in montane areas. Otherwise, there is little seasonality in the Mountain Gorilla’s diet. Fruit is very scarce in the Virunga Mountains, a chain of volcanoes that spans the borders of DR Congo, Rwanda, and Uganda. The gorillas’ diet is overwhelmingly dominated by leaves and stems, with just three species, bedstraw (Galium ruwenzoriense), wild celery (Peucedanum linderi), and thistles, making up threequarters of what they eat. These and other foods are abundant and available throughout the year across much of their habitat. But a group of gorillas can quickly deplete and trample a feeding area, and Mountain Gorillas have been found to move around their home ranges, allowing their food plants to regenerate. They also revisit areas more often, the higher the biomass and nutritional quality of food there. The plant species in the diet of Mountain Gorillas in the Virunga region are very different to those eaten by Mountain Gorillas in Bwindi Impenetrable Forest, Uganda. The Bwindi gorillas eat more fruit, tree leaves, bark, and wood and fewer herbaceous plants. But the nutritional content of the diets of the two populations has been found to be remarkably similar in terms of crude protein, fiber, and carbohydrate.

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Gorilla beringei beringei Volcanoes National Park, NW Rwanda. Photo: Russell A. Mittermeier/ Conservation International

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FAMILY HOMINIDAE Great Apes

The Bonobo appears to depend more on terrestrial herbaceous vegetation, including aquatic plants, than does the Chimpanzee (Pan troglodytes), and it frequently forages in marshy grasslands and streams. In one study, about 18% of foraging was in swamps or on the ground, searching for pith or leaves. The Bonobos sat down to process a stem or shoot on average every 10 m. The home ranges of the Bonobos of Wamba, DR Congo, consist mainly of intact dry forest, but the Bonobos visit swamp forest and disturbed forest almost every day because of the abundant proteinrich herbaceous plants that are constantly available.

grasslands on plants in the families Alismataceae, Arecaceae, and Cyperaceae. Bonobos do not hesitate to wade waist-deep into pools to gather algae. Chimpanzees, on the other hand, very rarely enter water; instead, they use sticks to scoop floating algae from the surface of ponds. Food is collected and processed with dextrous hands, strong jaws, and teeth. Great apes have developed elaborate techniques to avoid stings and sharp hooks on leaves. Orangutans, for example, avoid their lips coming into contact with stinging nettles Dendrocnide (Urticaceae), and Mountain Gorillas carefully fold or roll thistles Carduus nyassanus (Asteraceae) before putting the leaves in their mouths. One population of Sumatran Orangutans uses sticks to dislodge the seeds of Neesia cf. malayana (Bombacaceae), avoiding contact with the irritant hairs in which the seeds are embedded. Western Chimpanzees use tools to crack open the nuts of Coula edulis (Olacaceae), Detarium senegalense (Fabaceae), Panda oleosa (Pandaceae), Parinari excelsa (Chrysobalanaceae), Sacoglottis gabonensis (Humiriaceae), and oil palms. Dietary flexibility is crucial during periods of food scarcity. Fallback foods are always available but of relatively poor nutritional quality. They include bark and unripe fruit that are ignored when ripe succulent fruits are available. Some orangutans rely heavily on inner bark (cambium and phloem, the wafer-thin growth layers under the bark) and strangling figs that produce large crops year-round. In parts of Borneo, the giant fan palm (Borassodendron borneense, Arecaceae) becomes an important food. Western Lowland Gorillas eat the dry fibrous fruits of Duboscia macrocarpa (Tiliaceae) and Klainedoxa gabonensis (Irvingiaceae), and both subspecies of Western Gorilla increase their consumption of herbaceous and woody vegetation, such as the inner bark of Milicia excelsa (Moraceae). Chimpanzees maintain a relatively high fruit intake by eating figs, oil palm kernels, and fruit of the parasol tree Musanga cecropioides (Moraceae) in disturbed areas. Chimpanzees also ingest more fiber, including shoots, young leaves, and bark. Oil palm hearts, pith, and petioles and the pith of Cyperus papyrus (Cyperaceae) are known fallbacks for some populations of Chimpanzees. Fallback foods available to African apes are thought to be of higher quality than those available to orangutans. In addition to fruit, leaves, herbs, and inner bark, great apes eat a wide variety of minor vegetal items, including algae, aerial roots, bracts, flowers, fungi, leaf galls, mushrooms, orchids, roots, tree gum, tubers, truffles, vine tendrils, and wood.

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monkeys are unable to break into. Western Lowland Gorillas excel as the sole dispersers of Cola lizae (Sterculiaceae), one of the dominant tree species in central Gabon. Thousands of Cola seeds are deposited at gorilla nest sites in a substrate of fecal matter suitable for germination, and they have high rates of germination and survival. Nonetheless, great apes are seeds predators of a few species and consume vast quantities of fatrich seeds during mast fruiting events: Western Lowland Gorillas, Chimpanzees, and Bonobos eat the seeds of Gilbertiodendron dewevrei (Fabaceae). Orangutans eat unripe fruit and seeds, and they both destroy and disperse seeds of about one-third of the species they eat. When feeding on dipterocarp seeds, orangutans increase their calorie intake by 50–70%, storing the excess energy as fatty tissue reserves to be metabolized in times of nutritional stress. To meet their protein needs, great apes consume structural plant parts. New leaves, petioles, buds, and shoots are preferred; mature leaves are eaten selectively, and species high in secondary metabolites, such as tannins and alkaloids, are avoided. These make up 15–36% of the orangutan diet. African apes forage at all levels in the forest, and although much of their food is harvested arboreally, they specialize on the abundant terrestrial herbaceous vegetation, popularly known as THV. Plants from the monocotyledonous Marantaceae family provide a dependable supply of tender stems, shoots, and new leaves throughout the year. Marantaceae genera that are eaten frequently include Megaphrynium and Haumania. Fibrous stems of gingers (Aframomum) are consumed in large quantities, especially by Western Gorillas. Cross River Gorillas face four to five months of fruit scarcity when their diet becomes predominately THV, pith, and leaves. Western Lowland Gorillas in northern Republic of the Congo make extensive use of seasonally inundated swamp forests where sodium-rich herbaceous vegetation abounds. In Raphia swamps, their staple foods are the fronds of Raphia palms and Pandanus candelabrum (Pandanaceae). In bais (swampy clearings), their preferred foods are aquatic and semi-aquatic Hydrocharis chevalieri (Hydrocharitaceae), Rhynchospora corymbosa, and Cyperus sedges. Rather than avoiding water, gorillas sometimes spend hours sitting waist-deep in water while they feed. Although highly digestible and high in protein, many bai plants have a high water content, which limits the quantities that gorillas can ingest in a single sitting. Bonobos also consume aquatic plants throughout the year, foraging in streams and marshy

Pan paniscus Photo: Terry Whittaker/FLPA

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FAMILY HOMINIDAE Great Apes

Flood-prone forests and peatswamps produce more regular, larger fruit crops than dry dipterocarp forests, and so they harbor the highest densities of the Bornean Orangutan. This orangutan appears to be retrieving a fallen fruit floating in the water. Bornean Orangutans are strongly opportunistic foragers, and the composition of their diet varies markedly from month to month. During a four-year study, Bornean Orangutans in the swampy lowlands of Tanjung Puting spent over 60% of their foraging time on fruit, but ate a total of 317 different food types, including leaves, bark, small vines, fungus, insects, and honey. Pongo pygmaeus Borneo. Photo: Jeffrey Oonk/Foto Natura/ Minden Pictures/ASA

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Overall diversity of the plant part of the diet is high, reflecting the floristic diversity of tropical habitats. The number of food items in the diet of any one population in lowland forest ranges from about 100 to more than 300 food items, harvested from as many as 200 plant species. Dietary breadth of Chimpanzees in hot and arid savanna environments is much narrower (60 food items from 47 plant species) because plant species diversity of the habitat is low. Sympatric gorillas and Chimpanzees use very similar resources, and there is considerable overlap in their diets (50– 84% of the fruit species eaten). Competition between them is limited by mutual avoidance and niche differentiation, which

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becomes more evident when fruit is scarce. Gorillas always consume large amounts of herbaceous foliage; Chimpanzees are more specialized and require year-round access to fruit. Chimpanzees exploit lipid rich fruits that are avoided by gorillas, but they also have a social adaptation. Instead of altering their diet, they reduce the size of feeding parties: fission–fusion of Chimpanzee communities makes it easier for them to continue to exploit fruit resources (see Movements, Home range and Social organization). Mountain Gorillas are an exception to all of the above. Because plant species richness decreases with elevation, their diet is rather impoverished and includes only 62 species. Fruit is very scarce in the mountains of the border region of DR Congo, Rwanda, and Uganda, and their diet is overwhelmingly dominated by leaves and stems of herbs, vines, and shrubs (93% food intake), supplemented with bark, roots, and decaying wood (a source of sodium). Three-quarters of their diet comprises the leaves and stems of just three species: bedstraw (Galium ruwenzoriense, Rubiaceae), wild celery (Peucedanum linderi, Apiaceae), and thistles. The only pronounced seasonality in food availability is bamboo shoots, a highly preferred food that grows at the beginning of each rainy season. Twice a year, Mountain Gorillas move into the bamboo zone and feed almost exclusively on new shoots for two to three weeks. Similarly, when in season, bamboo shoots form 70–90% of the diet of Grauer’s Gorillas living in montane areas. Great apes usually avoid areas where people are active, but they may persist in areas that were originally forest. Increasingly, humans are clearing great ape habitat and replacing forest trees with cultigens (species resulting from artificial selection by humans). Cash crops are usually very palatable and nutritious. When great apes range onto land that not long ago formed part of their home range and find tasty food growing there, it is not surprising that they eat it. Globalization means that wildlife populations are increasingly exposed to non-native plant species, and great apes are developing a liking for cultivated foods that have not been part of their natural diet. Orangutans subsisting in plantations kill acacia and eucalyptus trees by bark stripping. Mountain Gorillas live in national parks, but some groups wander out onto land abutting the parks that was part of their home range less than three generations ago. Here they help themselves to eucalyptus bark, potatoes, and maize and tear apart banana trees to eat the pithy interior (never the fruit). Some orangutans and Chimpanzees may find themselves in forest patches surrounded by small-scale slash-and-burn ag-

Measured in time spent feeding, the diet of the Bonobo is 70–80% fruit. The majority of the remainder of their diet consists of other vegetable foods, with a small quantity of vertebrate and invertebrate animals. Bonobos prefer ripe, sugary fruits. Although they feed regularly on higher-protein leaves and herbs, they are unable to subsist on bulky quantities of lower-quality, fibrous foods, as the much larger gorillas (Gorilla) are able to do. In primary forests, Bonobos feed mainly high in the canopy and on the peripheral branches of trees. They rarely suspend themselves by their hands or feet while feeding; they sit on large branches and pull fruiting branches toward themselves. Pan paniscus Kokolopori Bonobo Reserve, NC DR Congo. Photo: Russell A. Mittermeier/ Conservation International

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FAMILY HOMINIDAE Great Apes

The Chimpanzee is an opportunistic feeder, but shows a strong preference for fruit, which it seeks out even at times and in places where it is not abundant. Unlike the Bonobo (Pan paniscus), Chimpanzees disperse when they are feeding and rarely feed close together or in the same tree, as they are doing here. The Chimpanzeeâ&#x20AC;&#x2122;s fissionfusion social system is thought to minimize feeding competition because communities break up into parties to exploit ephemeral, dispersed patches of ripe fruit. This population of Chimpanzees at Mahale Mountains National Park, Tanzania, has been recorded eating 328 food items from 198 plant species, plus others not yet identified. However, 46 these items were recorded only once, and more than 40 were eaten fewer than ten times, suggesting that the Chimpanzees were experimenting with items not previously used as food. Diet composition at Mahale changes from year to year, and some foods almost neglected in one year might be harvested in great amounts in another. When one fruit is abundant, they may concentrate on it to the exclusion of others, while at other times they forage more widely, and they have been recorded eating 20 different foods in the course of a single day. Chimpanzees appear to be able to tolerate higher tannin levels than other sympatric primates, although given the choice they prefer highersugar, lower-tannin fruits.

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Pan troglodytes schweinfurthii Mahale Mountains National Park, WÂ Tanzania. Photo: GĂźnter Ziesler

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FAMILY HOMINIDAE Great Apes

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riculture. These individuals have little choice but to raid crops, which causes conflict with people. Chimpanzees in fragmented farm-forest mosaics steal cassava, cacao, guava, lemons, mangos, papaya, sugarcane, and pineapples, depending on availability. Some orangutans spend 21% of feeding time devouring cultivated fruits (see Relationship with Humans). Great apes practice geophagy, that is, they eat earth, generally a few times each year. Soils ingested are rich in sodium, iron, potassium, or calcium, and they usually have a high clay content. Clay neutralizes secondary plant compounds in the

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gut and may absorb stomach acids, soothing the stomach. Great apes are attracted to specific caves, cliffs, and riverbanks, and even orangutans sometimes descend to the ground to visit natural salt licks. Social insects (ants, bees, and termites) can be exploited without disproportionate effort and are excellent sources of protein, fat, and energy. Bornean Orangutans use their hands to break into terrestrial nests and even split open standing dead trees housing insect colonies, and they extract the insects by sucking. Sumatran Orangutans tend to be more insectivorous; one Sumatran population eats at least 17 invertebrate species, using tools to do so and spending an average of 12% of its feeding time consuming insects. Most African apes (with the exception of Cross River Gorillas) eat ants or termites, plus the occasional caterpillar, grub, or larvae found in dead wood. In Central Africa, the bulk of insects that great apes consume are weaver ants (Oecophylla longinoda, Formicidae) and termites (Cubitermes, Termitidae). Insects are eaten year-round when availability and opportunity permit. Weaver ants come in convenient packets of leaves, bound into compact arboreal nests. Each nest contains a few grams of eggs, larvae, and adults, which are immobilized when crushed by the apes’ hands. Ants and termites are eaten frequently (recorded in 31–42% fecal samples) but not in large volumes, forming just 1–5% diet, but direct observations have revealed that Western Lowland Gorillas in the Central African Republic feed on termites 91% of days. Like orangutans, Western Lowland Gorillas use their brute strength to split open termite mounds and rip apart rotting wood. Chimpanzees across their geographic range use tools to prey on a variety of termites, army ants, carpenter ants, and various beetles. Different communities choose to incorporate different insect species into their diet; a species eaten at some sites may be ignored at others. Bonobos eat ants, termites, and earthworms, and there is one record of them eating colonial spiders. Bonobos can be seen walking quadrupedally in streams, slapping the water, and searching for invertebrates. Because insect availability decreases with increasing elevation, Mountain Gorillas feed on army ants just a few times per year. Orangutans, Chimpanzees, and Bonobos eat honey, bird eggs, and occasionally birds. Only orangutans and Chimpanzees use tools to gather honey, usually that made by stingless bees (Trigona, Apidae). When Chimpanzees raid nests of honeybees (Apis, Apidae), they spit-out chewed and sucked wedges of honeycomb.

Fruit-eating can present problems for the Bornean Orangutan. The animal is heavy, and fruit is often found on the terminal slender branches. Flanged males solve this problem by sitting or standing on strong branches and pulling the fruit toward them, sometimes breaking the fruiting branches off. Females, unflanged males, and juveniles suspend themselves by any combination of up to three hands and feet and reach for the fruit with whatever is left. This individual is handling what appears to be a typical “primate fruit,” which is large, with an inedible husk that must be peeled before the fruit can be eaten. Fruits preferred by orangutans tend to have soft pulp that is rich in digestible carbohydrate (mostly sugars), but contain little protein and virtually no fats. Pongo pygmaeus morio Sabah, NE Borneo. Photo: Konrad Wothe

Loss of forest habitat in southern Gombe has driven one Chimpanzee community to raid banana, mango, and palm fruit orchards at the forest edge. But adult Chimpanzees can be conservative in their feeding habits and slow to adopt novel foods. After villagers left the area of Mahale Mountains National Park, Tanzania, when it was created in 1978, it took the Chimpanzees 7–8 years until they began to taste the guava, mango, and lemon crops that had been left behind. Comparisons of food lists at Gombe and Mahale have revealed clear differences in the frequency of eating plants and fruits common to both areas. The two populations’ feeding habits also differ in at least three commonly eaten food types. Pan troglodytes schweinfurthi Gombe Stream National Park, W Tanzania. Photos: Cyril Ruoso

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FAMILY HOMINIDAE Great Apes

Individuals in all known Chimpanzee populations use tools, and more than half the tool-types recorded are used when feeding. Nut-cracking is one of the most sophisticated of these behaviors. Chimpanzees at Bossou, Guinea, begin to acquire the techniques needed to crack nuts with stones at 2·5 years old, but do not combine them in the appropriate sequence (picking the nut, putting the nut on the anvil stone, and holding the hammer stone) until they are around 3·5 years old. They learn by observing older Chimpanzees that have mastered the sequence. Nut-cracking appears to be confined to western Chimpanzee populations, implying that the technique is socially transmitted rather than innate. Pan troglodytes troglodytes Bakoumba Private Reserve, near Franceville, SE Gabon. Photo: Cyril Ruoso/Bios

The Eastern Gorilla (beringei subspecies “Mountain Gorilla,” shown here) supplements its diet with roots and also with bark and rotting wood, a source of sodium. Roots eaten include those of the giant groundsel (Dendrosenecio johnstonii) and torch lobelia (Lobelia wollostonii), and more rarely, of their primary food plants such as wild celery (Peucedanum linderi) and thistles. Although gorillas use their great strength to obtain most of their foods, they are also capable of processing it in quite complex ways. Thistle leaves, for example, may be rolled or folded to mask the prickles. When eating stinging nettles, the stems are broken, and the tender contents pinched clear from the skin, with its stinging hairs. The tough outer layers of bamboo and elephant grass are also stripped off to obtain the pith. Gorilla beringei beringei Virunga National Park, NE DR Congo. Photo: Konrad Wothe

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Baboons (Papio anubis), Yellow Baboons (P. cynocephalus), Hamadryas Baboons (P. hamadryas papio), Patas Monkeys (Erythrocebus patas), Vervet Monkeys (Chlorocebus aethiops), duikers (Cephalophus), bushbucks (Tragelaphus), Banded Mongoose (Mungos mungo), and Common African Pangolins (Manis tricuspis). Chimpanzees in Senegal are known to use sharp sticks to skewer bushbabies asleep in tree holes. Most hunting by Chimpanzees is the arboreal pursuit of monkeys, and it is usually opportunistic but organized and cooperative. Prey are usually chased, captured, and killed by the adult males of a commu-

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Gorillas do not eat meat, and there are only nine known cases of meat-eating by a few individual Sumatran Orangutans. They have been seen to slap nocturnal slow lorises to the ground, thus knocking them unconscious and avoiding a venomous bite. The lorises are killed with a bite to the head and then eaten. Chimpanzees are renowned hunters and the most carnivorous great ape, eating over 30 species of small and medium-sized mammals, mainly colobus monkeys and guenons. Where sympatric, Red Colobus (Piliocolobus badius) are their primary prey. They have also succeeded in killing Olive

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FAMILY HOMINIDAE Great Apes

Orangutans use sheer strength to break into termite nests and tear apart dead trees and rotten branches housing termite colonies. The Sumatran Orangutan also uses sticks as tools to exploit termites, ants, and stingless bees living in tree holes. The sticks are employed in a number of ways, including hammering to break nests open, poking to stir up the adult insects so that they pour out into the open, and scraping inside the holes to obtain eggs, larvae, and adults. Female orangutans are considerably more insectivorous than males, but tool-based feeding in both sexes is much less frequent than direct manual methods of reaching the insects. Pongo abelii Gunung Leuser National Park, N Sumatra. Photo: Suzi Eszterhas/ardea.com

nity and success during group hunts varies with the number of male participants. Males often control the carcasses and share meat with other members of their community. Youngsters typically acquire scraps through begging. Nonetheless, meat forms only a small portion of the Chimpanzee diet (about 3% of time spent feeding). Patterns of meat-eating vary among populations of Bonobos, which do not hunt frequently but occasionally consume small mammals. Recent records include Northern Black Crested Mangabey (Lophocebus aterrimus), Red-tailed Monkey (Cercopithecus ascanius), Wolf’s Monkey (Cercopithecus wolfi), Demidoff’s Dwarf Galago (Galagoides demidovii), and duikers. Adult female Bonobos usually control meat-sharing. In summary, all great apes are opportunistic frugivore-folivores. The main differences between them are that Mountain Gorillas are compelled to eat herbs and fall at the folivore (herbivore) end of the spectrum, and Chimpanzees are omnivores, habitually eating meat.

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Breeding Mating systems differ strikingly between the great ape genera. Orangutans and gorillas are usually polygynous; Chimpanzees, Bonobos, and gorillas in multimale groups are polygynandrous. There is no monogamy, only temporary consortships by pairs of orangutans and Chimpanzees. Slow rates of reproduction are common to all great apes, due to a high investment in single offspring and their slow maturation. The process of bimodal maturation (bimaturation) in male orangutans is unique. Males reach sexual maturity between the ages of eight and 16 years. Some remain “unflanged” for many years—capable of reproducing, but they are smaller and lack the fibrous, fatty cheek adornments. Not all individuals make the testosterone-driven transition to a fully mature form, the achievement of which seems to be determined by social context and is manifested by impressive flanges, a pronounced throat pouch, long hair on the back and arms, and aggressive behavior. There are thus two adult male morphs, displaying differing degrees of development in secondary sexual characteristics. S. Wich and colleagues suggested that 35 years is the average minimum age of entry into the flanged stage. In relative terms, there are more flanged Bornean Orangutans and fewer flanged Sumatran Orangutans. Male gorillas start to show secondary sexual characteristics at ten to eleven years

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of age. These “blackbacks” are sexually but not physically mature. Western Gorilla males reach full maturity at 18 years and Eastern Gorilla males slightly earlier at 15 years, developing a prominent sagittal crest and a covering of short white hairs on the middle back, which gives the appearance of a silver saddle resulting in the popular name “silverback.” Between the ages of eight and 15 years, male Chimpanzees show increases in muscle mass, testicular volume, and aggression. They are fully grown by about 25 years of age. The body and testes of male Bonobos increase in size at eight to nine years, and they are thought to reach sexual maturity by ten years old. Female great apes reach sexual maturity at similar ages: orangutan females begin to display sexual behavior at ten to eleven years of age, Chimpanzees have their first swellings at about eight years, and Bonobos start cycling at nine to twelve years. Onset of menarche occurs slightly earlier in gorillas, at six to seven years of age. The length of the menstrual cycle is about 28 days in orangutans and Eastern Gorillas, about 35 days in Chimpanzees, and probably about 36 days in Bonobos; it is about 32 days in captive Western Gorillas. The first menses is followed by two to three years of adolescent infertility. Female orangutans have no external signs of ovulation, and only nulliparous gorillas show a slight swelling of the labia at mid-cycle. In contrast, Chimpanzees and Bonobos have striking, pink perineal swellings around the time of ovulation, advertising their fecundity to potential mates. In Chimpanzees, sexual swellings are irregular for the first two years of cycling, becoming larger and regular only at ten to eleven years of age. The sexual swellings of Chimpanzees and Bonobos vary in firmness and attractiveness to males during the cycle, reaching maximum volume and turgidity around ovulation. In Chimpanzees, the swelling persists for ten to twelve days, collapsing abruptly after ovulation, so that the labia are flat during nonfertile phases of the cycle. Swellings of female Bonobos are sustained for slightly longer, about 14 days. Female great apes are most receptive at the mid-point of their cycle when estrogen concentrations peak and conception is probable. Female orangutans actively seek contact with prime adult males at this time. Female gorillas are receptive throughout their menstrual cycle, but proceptivity is restricted to only one to four days. Female Chimpanzees are both proceptive and receptive during peak swelling, and they copulate frequently and promiscuously. Conception is most likely during the last four days of the cycle when possessive mating by

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FAMILY HOMINIDAE Great Apes

Most Chimpanzee populations use tools to extract termites from mounds and subterranean nests. In East and West Africa, they use sticks as probes to dip or “fish” for the termites They remove them from the stick either with their mouths (as here), or by picking termites from the sides of their fists after having swept a closed hand up the length of the tool. Chimpanzees have also been seen fishing with grass-blades and flexible vines. In the forests of the Goualougo Triangle, Republic of the Congo, however, they use a set of two distinct tools. A stout, straight stick is used to perforate the termite nest, and a more slender, brush-ended stick is dipped in to extract the termites. After brushing away surface debris with its hands, the Chimpanzee leans over the stout stick and uses its weight to push it into the ground, while grasping it around the middle with both hands. It chooses old holes that have been repaired with soil by the termites, rather than trying to break through the hard cement of the nest wall. It pulls the stick out, inspects or sniffs the hole or the end of the stick to ensure than the nest has been penetrated and then pushes in the brush-ended stick. It first wets the brush tip with saliva and pulls it through its hand to straighten it, actions that are repeated every time the “brush” is pushed into the hole. In some Chimpanzee populations, there is no difference between sexes in the frequency of tool-use to extract termites. In other populations, females depend more on termites in their diet than males do and fish for them more often. Young female Chimpanzees have been found to be more patient in watching and imitating their mothers than young males they and hence learn the technique earlier.

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Pan troglodytes schweinfurthii Ngamba Island Chimpanzee Sanctuary, Lake Victoria, S Uganda. Photos: Suzi Eszterhas/ Minden Pictures/ASA

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FAMILY HOMINIDAE Great Apes

The Chimpanzees of Mahale Mountains National Park, Tanzania, fish with twigs for arboreal ants, but they have not been seen fishing on the ground for driver ants. Chimpanzees at Gombe Stream National Park, Tanzania, on the other hand, eat driver ants so regularly and in such quantities (up to 20 g per session) that some researchers regard them as a significant dietary component. The Mahale Chimpanzees use fewer tools for fewer purposes than some other populations. They modify the tool as they use it, whereas the Chimpanzees of Tai Forest, Ivory Coast, make modifications in advance. Pan troglodytes schweinfurthii Mahale Mountains National Park, W Tanzania. Photo: Günter Ziesler

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dominant males also occurs. Bonobos do not limit their sexual activity to time of ovulation because females are more-or-less permanently proceptive and receptive, but most copulations take place during maximum swelling. Orangutans and gorillas are among the most sexually dimorphic primates, reflecting intense physical competition between adult males. Some flanged male orangutans are extremely aggressive to any other adult males in the vicinity, and they are able to monopolize a home range into which they attract receptive females. R. Delgado described a signaling male as creating a protective sphere for the females associating with him. When multiple females are cycling, they may converge around a dominant flanged male. He is selective about mates and often ignores adolescent females that are likely to

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be “subfertile.” Other males are nomadic and mate opportunistically, especially unflanged males that are unable to make long calls so they must search for a mate. Copulations may be forced upon females that resist advances of unfamiliar males or those they find unattractive. Forced copulations seem to be more prevalent in Bornean populations, where both flanged and unflanged males resort to this tactic, restraining and often biting females who resist. Unflanged males often copulate without using aggression, but larger males can displace them. Dominant males of both species and some unflanged Sumatran males form consortships with receptive females. At this time, a male–female pair travels together for several consecutive days or weeks, and the male will fend off many potential competitors. Unflanged males follow consort pairs closely Rehabilitated Bornean Orangutans will scavenge for fish, and also catch fish, marooned in small pools and in mud. Wild great apes do not scavenge and are highly unlikely to catch or eat fish, although Bonobos (Pan paniscus) may be seen walking quadrupedally in streams, slapping the water, and searching for aquatic insects. Bonobos do not hunt frequently, but occasionally they consume small mammals and invertebrates. Gorillas (Gorilla) do not eat meat, and there are only nine known cases of meat-eating by a few individual Sumatran Orangutans (Pongo abelii). In contrast to the other great apes, Chimpanzees (Pan troglodytes) are renowned hunters and the most carnivorous great ape, eating over 30 species of small and mediumsized mammal, mainly colobus monkeys (Colobus) and arboreal guenons (Cercopithecus). Pongo pygmaeus Palas II Island, Nyaru Menteng Rehabilitation Centre, C Borneo. Photo: Alain Compost/Bios

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FAMILY HOMINIDAE Great Apes

The Chimpanzee is the most carnivorous great ape, eating over 30 species of small and mediumsized mammals, primarily colobus monkeys (Colobus) and arboreal guenons (Cercopithecus). Red Colobus (Piliocolobus badius) are their primary prey in areas where they occur together. A long-term study of the Kanyawara Chimpanzees in Kibale National Park, Uganda, recorded 152 hunts of red colobus monkeys between 1990 and 2003. Around 13% of encounters with Red Colobus resulted in a hunt, and 49% of hunts resulted in the capture of at least one monkey. Up to seven monkeys were killed in a single hunt. Studies of different populations have suggested various explanations for hunting by Chimpanzees. At Gombe, Tanzania, they hunt more frequently during the dry season, when body mass tends to be low, and they may be seeking an additional source of food. But at Ngogo in Kibale National Park, Uganda, and at Mahale Mountains National Park, Tanzania, hunting frequency is highest when ripe fruit is plentiful. One possible reason for an increase in hunting at times of plenty is that Chimpanzee parties tend to be larger when food is abundant, and hunts tend to be more successful when more Chimpanzees are involved. Hunts usually involve adult males, and at Gombe, some males withhold meat from females until after copulation. But in West Africa, hunting tends to be less frequent when sexually receptive females are present, and males often choose to guard their mates rather than join in the hunt. One or more males control the carcasses. Some, such as the Gombe Chimpanzees, share the meat with certain members of their community and withhold it from others. Some element of bonding or alliance-building may be involved, although no evidence of this has been found in studies of other populations.

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Pan troglodytes schweinfurthii Mahale Mountains National Park, WÂ Tanzania. Photos: GĂźnter Ziesler

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FAMILY HOMINIDAE Great Apes

and copulate surreptitiously if the consort male is unable to monopolize the female. Most gorillas live in unimale polygynous groups, and gorillas are usually described as having a one-male mating system; however, there are many multimale groups (about 40% of groups) in populations of Eastern Gorillas. In unimale groups, one male performs all the mating and usually have access to several females, whereas solitary males have access to none. In multimale gorilla groups, dominant males enjoy most copulations, although females often mate with more than one male, not always by choice. Subordinate males succeed in copulating clandestinely, but they are harassed if detected by a more domi-

nant male. Opportunities to mate are relatively infrequent even for dominant males because adult female gorillas are usually pregnant or lactating and therefore infertile. Chimpanzees and Bonobos are only slightly sexually dimorphic, but the huge testes of males indicate a high level of sperm competition. Both species live in promiscuous communities, where mating is opportunistic. Receptive female Chimpanzees can attract large numbers of males and copulate frequently with numerous males without provoking obvious conflict among them. High-ranking males may use aggression to guard a swollen female. Alternatively, a pair may enter into a consortship and avoid other community members for days or weeks. In Bonobo communities, a greater proportion of females are receptive at any given time, so it would be difficult for males to monopolize mating opportunities, and Bonobos do not form consortships. Male Bonobos rarely fight over access to females; instead, dominant males establish amicable relationships with their mates. During peri-ovulation females of all great ape species preferentially mate with high-status, fully developed males in their prime. For a female orangutan, this will be a locally dominant flanged male, with whom she will seek encounters and may choose to initiate a consortship. The male solicits by posturing and displaying his penis, and copulation will take place repeatedly during a consortship. Around the time of ovulation, females often mate with more than one male. When the chances of becoming pregnant are low, they may submit to the advances of unflanged or past prime males. Mating between gorillas can be initiated by either sex. At the time of ovulation, females solicit by approaching a male and staring, sometimes reaching out and touching him with her hand. Males use a specific vocalization when approaching a female as an invitation to mate. Chimpanzee copulations are usually initiated through male displays—bipedal swaggering with an erect penis, sometimes stamping, nodding of the head, or shaking branches. Female Chimpanzees solicit by crouching to present their swollen genitalia. Sexual behavior of Bonobos is less constrained, and pairings occur between many different members of the community, although rarely between mothers and sons. Most copulations are brief (for example, Mountain Gorillas 30–310 seconds) and are dorso-ventral; orangutans, gorillas, and Bonobos sometimes adopt a ventro-ventral position. Female mate selectivity during her most fertile period and male reproductive tactics determine paternity. Genetic stud-

These pictures are taken from a video sequence of a Sumatran Orangutan eating a slow loris (Nycticebus). This is the only vertebrate prey recorded for the Sumatran Orangutan and perhaps the only primate prey likely to be captured by these slow-moving great apes. The capture started when the orangutan, a female with an infant, slapped the loris out of the tree, knocking it unconscious and hence avoiding its venomous bite. The orangutan went to the ground, where she killed the loris with a bite to the skull. The mother did not actively share the meat with the infant, which helped itself from her hands or mouth. The mother sometimes resisted these attempts. Pongo abelii Gunung Leuser National Park, N Sumatra. Photos: Madeleine Hardus

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Forest ungulates, particularly duikers and Red River Hogs (Potamochoerus porcus), are hunted by all the East African Chimpanzee populations studied, but they do not appear to be regarded as prey by West African Chimpanzees. The piglets must be taken without risking an encounter with the more formidable adult hogs. At Gombe, Chimpanzees have been described using stealth to seize piglets. They also use aggressive displays to panic the adults and capture the piglets in the confusion, or when they are left behind by the fleeing herd. Although female Chimpanzees do hunt, in two decades of data from Gombe, adult males were responsible for 91·5% of all kills. Males often snatch carcasses from successful females, which may explain their reluctance to join the hunts.

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Pan troglodytes schweinfurthii Gombe Stream National Park, W Tanzania. Photo: Cyril Ruoso/JH Editorial/ Minden Pictures/ASA

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FAMILY HOMINIDAE Great Apes

Gorilla gorilla gorilla Photo: Roland Seitre

When free-standing water is not available, or not easily accessible, the Chimpanzee uses a variety of techniques to obtain it. Chimpanzees across their distribution make “sponges” by chewing leaves, or use handfuls of moss, to soak up water from tree hollows. At Bossou, Guinea, they make a kind of container by folding leaves to scoop out water, a method that young Chimpanzees begin to copy at around 2·5 years old. In drier areas, Chimpanzees will use their hands to scoop wells in sandy river beds, or dig up roots containing water. Pan troglodytes troglodytes Bakoumba Private Reserve, near Franceville, SE Gabon. Photo: Cyril Ruoso

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ies show that orangutan and Chimpanzee consortships have a high chance of producing offspring. Paternity studies indicate that high-ranking Chimpanzees father most offspring, perhaps because dominant males are capable of mate-guarding during the peri-ovulatory period. DNA analyses have also revealed that subordinate Mountain Gorillas occasionally sire offspring, and unflanged Sumatran Orangutans reproduce at a similar rate to flanged males, although with nulliparous rather than parous females. The length of gestation in orangutans is 8·5–9 months (about 254 days in captivity). The mean gestation is about 255 days (8·4 months) in Mountain Gorillas and about 230 days (7·5 months) in Chimpanzees. The length of pregnancy in wild Bonobos is unknown, but averages 224–239 days (7·3–7·8 months) in captivity. Age at first parturition in orangutans is 15–16 years, ten years in gorillas (range of averages: 8–14 years), 13·5 years in Chimpanzees (mean at different sites 10·9–15·4), and 13–15 years in Bonobos. Females usually give birth to a single infant at night. During the handful of births that have been witnessed, obvious labor lasted several hours, during which females were restless and frequently changed position. They built multiple nests and gave birth in an arboreal (gorillas and Chimpanzee) or a terrestrial nest (gorillas). New mothers bite through the umbilical cord and eat the placenta. Twin births are known in orangutans, gorillas, and Chimpanzees but are rare. For example, only one set of twins was recorded among 135 Chimpanzee births. It is difficult for females to carry both twins and feed herself, so usually one or both of the twins die. A single pair of twins has survived to adulthood during long-term studies of Chimpanzees in western Tanzania and Mountain Gorillas in Rwanda. Mean birthrate in gorillas and Chimpanzees is 0·2–0·3 births per adult female per year, or one birth per adult female every 3·3–5 years. Neonates are estimated to weigh 1–2·5 kg. Mother–infant bonds are strong and long-lasting, and females are extremely protective of their young, carrying them close to their bodies. Newborns cling to their mothers’ hair and are carried ventrally in the early months. Infants begin to travel dorsally (on the mothers’ back) within a few weeks. African apes display a characteristic white pygal tuft. Suckling inhibits post-partum cycling and great apes undergo three to four years of lactational amenorrhea. Lactation drops off gradually as solid foods are incorporated into the infant’s diet. Offspring share their mothers’ night nests until they are weaned or the next sibling is born. Much information on age of weaning is preliminary: Bornean Orangutans five to six years, Sumatran Orangutans about seven years, Western Lowland Gorillas four to five years, Mountain Gorillas a mean of 3·6 years, Chimpanzees four to five years, and Bonobos about five years. For the African great apes, weaning marks the end of infancy, and gorillas are weaned early in relation to their body weight. Infant orangutans do not become fully independent until seven to nine years of age, despite having similar rates of development to the other apes. Species differences are also evident in interbirth intervals, which average four to six years in African apes but eight years in orangutans (Bornean Orangutans means 6·1–8·2 years, Sumatran Orangutans 9·3 years, Western Lowland Gorillas four to six years, Mountain Gorillas four years, Chimpanzees 4·6–7·2 years, and Bonobos about 4·8 years). The exceptionally long interbirth intervals of orangutans are thought to be a consequence of their solitary lifestyle. This investment by female orangutans seems to pay off; Wich and colleagues have shown that mortality in the first year of life is three times lower for orangutans than for Chimpanzees and 2·5 times lower than for gorillas. Furthermore, mortality of infant orangutans in their second and third years is zero compared to 7% for gorillas and 19% for Chimpanzees. About 90% of orangutans survive infancy compared to 73% of Mountain Gorillas and only 50% of Chimpanzees in western Tanzania. Infanticide is the killing of unweaned offspring and results in early resumption of the mother’s menstrual cycle. Adult males can gain reproductive benefits through infanticide of unrelated infants by shortening the time to impregnate their mothers, which is adaptive in species with prolonged post-partum amenorrhea. The mother is usually able to conceive again within a few months of losing her dependent infant. It has been

established that infanticide occurs in populations of gorillas and Chimpanzees, but it is unknown in orangutans. Female orangutans’ lack of visual indicators of ovulation means they are able to conceal it, which may be to their advantage in “creating confusion” about paternity, hence their strategy of mating with multiple “potentially infanticidal” males outside of their most fertile period. Some female orangutans also mate during their pregnancy, and this too is believed to be an infanticide avoidance tactic. The extended receptivity and proceptivity of Chimpanzees with sexual swellings helps them to mate with a large number of potential sires. Female gorillas use a similar strategy, and they may succeed in reducing the number of infants killed

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Gorillas obtain much of their water from the moisture in fruit and plants. Some populations are believed to drink rarely, or by some accounts, not at all. However, both the Eastern (Gorilla beringei) and the Western Gorilla have been seen to drink. Gorillas have also been seen drinking rain by extending their lower lips, and they are said to obtain water by dipping their hands and sucking it from their hair.

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FAMILY HOMINIDAE Great Apes

Some populations of orangutans show a preference for using their left hands for tasks such as scooping up water to drink, whereas the majority of Chimpanzees (Pan troglodytes), gorillas (Gorilla), and Bonobos (P.Â paniscus) favor their right hands for such tasks. Although their diet has a high water content, orangutans drink regularly, perhaps daily. Water is available to them in the tree canopy, in the form of rainwater pools in hollows and large leaves. They also lick rainwater from their hair. Perhaps because of the presence of Tigers (Panthera tigris) on the island, the female Sumatran Orangutan avoids coming down to the ground to drink, although the more powerful flanged males come to the ground more often. Orangutans of both sexes, however, visit salt licks, places where mineral-rich water seeps to the surface. The minerals may be needed because of imbalances in their diet or to counteract the effects of toxins in fruits, seeds, and leaves. In Sabah, Malaysian Borneo, Bornean Orangutans (Pongo pygmaeus) are among the most frequent large mammal visitors to mineral licks. A camera-trapping study found that the orangutans drank the water, rather than eating soil or clay, and sometimes moved stones to reach it. Female orangutans paid the shortest visits to the mineral licks, usually less than 15 minutes. Flanged males stayed the longest, sometimes for more than an hour and, in one case, longer than two hours. All age and sex classes of orangutans visited the licks during the course of a single day, and several were sometimes present at the same time, suggesting that the licks have a secondary function as a communications hub for this otherwise mostly solitary species.

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Pongo abelii Gunung Leuser National Park, NÂ Sumatra. Photo: Konrad Wothe

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FAMILY HOMINIDAE Great Apes

Gorilla beringei beringei Virunga National Park, NE DR Congo. Photo: Konrad Wothe

Gestation in the Sumatran Orangutan (Pongo abelii) and the Bornean Orangutan lasts around 254 days. The average age at first pregnancy is 14–15 years. On average, a female will give birth to 4–5 offspring during her lifetime, and the mean interval between births is 7–9·3 years. Pregnant females greatly increase their intake of energy-rich and protein-rich foods such as honey and insects. In Sumatra, they can spend almost two hours a day hunting insects, at the expense of time spent feeding on fruit. Insect consumption drops in lactating females, who are perhaps too encumbered by dependent young to hunt insects successfully. Lactating females spend more time eating fruit than females in any other reproductive state. Pongo pygmaeus Gunung Palung National Park, West Kalimantan, W Borneo. Photo: Tim Laman

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by adult males. Nonetheless, infanticide is responsible for 26% of the deaths of infant Mountain Gorillas. Male Bonobos have no indication of whether or not they sired any particular offspring, and so infanticide is unlikely to be adaptive and indeed seems to be absent in Bonobos. The lack of clarity over paternity seems to translate into generalized paternalism, and adult male Bonobos are caring and affectionate toward infants, sharing both food and nests. Great apes give birth throughout the year and generally have no birth season; however, cycling and conception are energetically demanding and may be determined by seasonal patterns in fruit production. Given that some populations of Bornean Orangutans experience periods of negative energy balance during food shortages, it is not surprising that female reproduction is influenced by food availability and rates of conception increase during mast fruiting events. Sumatran Orangutans do not face such severe constraints (see Food and Feeding). Chimpanzees and Bonobos have birth peaks during particular months that correlate with resource availability. When fruit is abundant, females are more likely to start or to restart (post-partum) cycling, so there are peaks in numbers of female Chimpanzees and Bonobos ovulating and conceiving, with contingent peaks in birth rate. Gorillas are somewhat less dependent on fruit, and there is no seasonality in their reproduction. Great apes live a long time and precise information about their longevity is limited. Two populations of Chimpanzees have been studied for over 50 years, orangutans and Mountain Gorillas for over 40 years, and a study of Bonobos began in the 1970s. Although known individuals from these studies are thought to be in their late 40s and even their 50s, the oldest individuals were born before the studies began, so their dates of birth are estimates. Nonetheless, long-term studies indicate that a few great apes will have life spans of over 50 years. Average life spans are shorter; male Chimpanzees that reach maturity are expected to live to 29 years in a Tanzanian population and 41 years in a Ugandan population. Male gorillas die relatively young, perhaps because of fierce competition among them. In Rwanda, four times as many males as females die between the ages of 24 years and 30 years (32% versus 8%). Female lifetime reproductive success (LRS) has been estimated using the results of long-term research on Mountain Gorillas and Chimpanzees. On average, female Chimpanzees give birth to four offspring during their lifetimes, but only 1·5–3·2 sur-

vive beyond infancy. Female Mountain Gorillas produce 3·6 offspring during their lifetimes, indicating a growing population in contrast with other great ape taxa. In 2009, Wich and colleagues demonstrated that orangutans have the slowest breeding rate of any mammal, and later age at first reproduction, longer interbirth intervals, and longer generation time than the African apes. Of all the great apes, orangutans have the slowest life history, followed by Chimpanzees and gorillas. Documenting the biology of these long-lived species takes decades of study, and interpopulation differences are only now coming to light.

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Copulation in the Eastern Gorilla (beringei subspecies “Mountain Gorilla,” shown here) lasts an average of 1·5 minutes, and it can occur at intervals of three hours during the 2–4 days the female is proceptive. The female usually initiates copulation, although the male may also display when he wishes to mate. This display has in the past been misread as aggression toward the female, although there is little evidence of forced copulation or coercion by male gorillas, in contrast to orangutans (Pongo). The female mates up to ten times during one cycle, mainly with the dominant male in multimale groups. Subordinate males may sneak copulations, but they are harassed by the dominant silverback if detected. However, young males that remain in a multimale group can have higher lifetime reproductive success than those that leave and try to form their own groups.

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FAMILY HOMINIDAE Great Apes

The newborn Bornean Orangutan is estimated to weigh between 1·25 kg and almost 2 kg, and males tend to be around one-fifth heavier than females. In one observed birth, the newborn orangutan began breathing after 30 seconds, showed considerable alertness, and was suckling within four hours. The mother exhibited great care, licking and sucking it, and breathing into its mouth. Other, perhaps younger, mothers can be less attentive to their infant young. The youngster clings to its mother’s chest and belly for its first year of life. Orangutan twins are rare, and usually only one survives, perhaps because of the difficulty in managing two babies while traveling and feeding in the tree canopy. Pongo pygmaeus Sepilok Orang Utan Rehabilitation Centre, Sabah, NE Borneo. Photo: Günter Ziesler

Movements, Home range and Social organization

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Ranging is influenced by many factors, not only by feeding ecology and the physical environment but also aspects of the social environment, such as group size, avoidance of other social units, and searching for potential mates. The distance traveled between consecutive nest sites is referred to here as

the day range or day journey. With a life in the canopy, orangutans do not travel far in a day. Female Bornean Orangutans and flanged males rarely cover more than 200 m/day, although unflanged males travel faster and range about 430 m/day. Sumatran Orangutans move a little farther, with mean day journeys of 680 m (females) and 939 m (males), but still less than one kilometer. Seasonal changes in orangutan movements tend to be site-specific rather than species-specific. The semi-terrestrial African apes move considerably farther, and the most frugivo-

Mother gorillas provide most of the care for their offspring, but fathers hug, carry, and play with them. However, infanticide by unrelated male gorillas is one of the primary causes of infant mortality. An infant is most vulnerable when the protector male (its likely father) is absent or when a new silverback takes over a group. Observations of Western Gorilla (gorilla subspecies “Western Lowland Gorilla” shown here) in KahuziBiéga National Park, DR Congo, suggest the infanticidal male may discriminate between infants to accept and those to kill according to his previous interactions with their mothers. Infanticide by male gorillas was not reported in Kahuzi for more than 20 years, but it occurred three times within a few months soon after the large-scale killing of gorillas during a war in the late 1990s. Gorilla beringei gorilla Photo: Gerard Lacz/VW Pics

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FAMILY HOMINIDAE Great Apes

Pan paniscus Lola ya Bonobo Sanctuary, W DR Congo. Photo: Cyril Ruoso/JH Editorial/ Minden Pictures/ASA

The infant Bornean Orangutan spends its first 6–8 months clinging firmly to its mother. By the age of about one year, it is only spending a quarter of its time in contact with its mother, although she is never far away and she continues to carry it while traveling. By two years old, the infants climbing and swinging skills are better developed, but its mother may hold its hand when traveling and pull together branches to create a bridge to help it cross gaps in the canopy. At three years old, the infant has largely reached locomotory independence and can build its own nest, but it continues to sleep in its mother’s nest until weaning, at around seven years old. Pongo pygmaeus wurmbii Tanjung Puting National Park, S Borneo. Photo: Konrad Wothe

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rous roam widely between fruiting trees. Chimpanzees journey two to three kilometers each day, with occasional ten-kilometer excursions. When fruit is scarce, Chimpanzees not only reduce travel, but they split into smaller feeding parties, because larger groups must travel greater distances to obtain sufficient food. Bonobos and Western Lowland Gorillas average about two kilometers each day, but they range up to five to six kilometers when feeding on patchily dispersed resources. During seasons when gorillas rely on low-quality but more evenly distributed foods, their day journeys become considerably shorter. Eastern and Western gorillas in lowland areas move similar distances (Eastern Gorillas about 1·5 km/day), but because day journey length decreases with elevation and a more folivorous diet, Mountain Gorillas in the salad bowl of the Virunga Volcanoes usually travel less than 0·6 km/day. The 4–8 km2 annual home ranges of male Bornean Orangutans are small compared with Sumatran males, whose home ranges in swamp forest exceed 25 km2. Females use smaller areas: 0·4–3·5 km2 in Borneo and 2–8·5 km2 in swamps in Sumatra. Home range overlap is usually extensive, although this varies with orangutan density, which is contingent upon food availability. Male orangutans disperse when they reach sexual maturity. Some flanged and most unflanged males are nomadic and have large home ranges. High-status adult males are able to monopolize both food and females, and so they are able to reside in a relatively small area. Establishment of a circumscribed home range secures access to the resources within it, and male home ranges may encompass several female home ranges. Flanged male orangutans are fiercely intolerant of one another, but rather than actively defending ground, they use long calls to establish personal space. They may tolerate subadult males because they are not agile enough to chase them. Males occasionally aggregate around a favorite food source. As long as distance is maintained, physical conflicts are rare; however, close encounters trigger aggressive displays that sometimes lead to fights on the ground. When males do battle and inflict serious injuries, infection of the wounds can result in casualties. Such deaths have been known among male Bornean Orangutans. Annual home range estimates for Western Gorillas are 10·6–15·4 km2. Eastern Gorillas range over areas of 6–34 km2 annually. Gorillas are not territorial, and home range overlap between neighboring groups is substantial (24–72% in one population). Encounters between groups using the same area can occur without the gorillas being able to establish eye contact, due to the poor visibility in forest habitats. Dominant males may exchange vocalizations and chestbeats hundreds of meters apart, sometimes for hours, until one group moves away. Some groups remain silent and leave the area without engaging the other group. Groups ignore each other under particular conditions, such as in swampy clearings (bais) in the Congo Basin, where good visibility allows adult males to monitor potential competitors from a safe distance. These males sometimes display, but physical contact between them has not been seen. In addition to increased tolerance in bais, it has been suggested that aggression between neighboring groups of Western Lowland Gorillas is infrequent because the dominant males are likely to be related. Male Mountain Gorillas engage in contact aggression during 17% of group encounters. Serious aggression is rare, but when contests escalate, fighting is intense and the outcome sometimes fatal. Deaths from septicemia have followed injuries sustained during intergroup interactions. It should be noted that such conflicts are not over territory but to guard females. Chimpanzees living in forest habitats have annual home ranges varying between 6·8 km2 and 32 km2. In the savanna woodlands of Senegal, they use areas greater than 65 km2 during one year. Females use smaller core areas within a community home range that is defended by the males. Males are highly territorial and patrol the boundaries of their home range, which may border on another community’s home range. Small groups of males move quietly, looking and listening for other Chimpanzees and may attack members of neighboring communities. Some populations are renowned for their aggression. A recent study of lethal conflicts by M. Wilson and colleagues, published in 2012, reported that communities and patrols with large numbers of males launched most attacks

and victims were usually adult males and infants. The protagonists may gain females or extend their home ranges with these combative tactics. Bonobo communities share annual home ranges of 22–58 km2, and the overlap between community home ranges is 40–66%. Encounters between parties from different communities are frequent and characterized by highpitched excitement rather than conflict. Some encounters are aggressive but not lethal. Bonobos do not exhibit territorial defense or cooperative patrolling.

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The female Bonobo suckles her infant more frequently, but for shorter periods, than the female Chimpanzee (Pan troglodytes). She also leaves the infant alone more often during its first two years, which may reflect the lower risk of infanticide in Bonobo groups. Unlike the Chimpanzee, the female Bonobo tends to have priority at feeding sites, which may help her meet the energy costs of pregnancy and lactation. The lactating female Chimpanzee rests more than non-reproductive females. She also spends less time feeding by choosing higher-quality foods. The fat she is able to store by conserving her energy through lower rates of activity helps her through lactation, which lasts 4–5 years for each infant in both species.

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FAMILY HOMINIDAE Great Apes

Very young gorillas suckle around once an hour, in bouts of around three minutes, during the course of which they may change nipples. By 18 months old, they suckle an average of only once every two hours, but the duration of the bouts remains the same. “Mountain Gorillas” (Gorilla beringei beringei) are weaned at 3–4 years old, but the Western Gorilla continues to suckle for another year, until 4·5–5 years old. This may be related to fluctuations in the Western Gorilla’s primary foods. Succulent fruits, likely to be the preferred weaning foods, are not always available. The herbs and other plants eaten by Mountain Gorillas are not seasonal and are constantly available. Gorilla gorilla gorilla Batéké Plateau National Park, SE Gabon. Photo: Cyril Ruoso

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Where gorillas and Chimpanzees are sympatric, they occasionally meet at the same fruiting trees. Observations of interactions between the two species are rare, but encounters can be peaceful or result in agonistic contests. In Uganda, a gorilla was seen feeding in a fig tree within meters of several adult male Chimpanzees, although at the same site a party of Chimpanzees temporarily prevented a gorilla group from entering the tree they occupied. In the Republic of the Congo, eight incidents of cofeeding have been witnessed, each lasting up to 150 minutes. Both species may be more tolerant when they are mutually attracted to a highly preferred food source, especially

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in times of fruit scarcity. Aggressive encounters between gorillas and Chimpanzees have not been observed. Social organization differs considerably among great ape genera. Orangutans are semi-solitary, while the African apes are highly gregarious. Orangutans have loosely defined communities that are not socially bounded but where residents know other orangutans in the neighborhood. Adults and adolescents of both genders usually forage alone, but individuals sometimes congregate at food sources. Foraging in groups is costly due to competition for limited resources. Fruit scarcity and arboreal locomotion impose solitude on Bornean Orangutans, and flanged males are alone 91% of the time. When not alone, they are associating with females. Unflanged males are comparatively tolerant of other males and spend 41–45% of their time in association with other males or females. Mean party size is less than two individuals, and mother–infant pairs are the main social unit (20% of Bornean populations). Adult female orangutans are more gregarious than adult males, and they appear to be philopatric. They tend to remain within the areas where they were born, sometimes forming clusters with other familiar or related females and travel together, as do adolescents. If individuals converge on large food sources, they may depart separately but occasionally continue traveling together between fruiting trees. These parties are most likely to be composed of females, but association with a dominant male provides females with refuge from harassment by other males. The forests on Sumatra produce abundant food and, as a consequence, Sumatran Orangutans have higher population densities than do populations of Bornean Orangutans. With increased opportunities for interaction among Sumatran Orangutans, social behaviors occur at higher rates, from party formation to aggressive encounters. Mast fruiting allows for periodic sociality. African apes are unusual among primates in that they exhibit female-biased dispersal and male dispersal is rare. Gorillas, Chimpanzees, and Bonobos live in two types of society: stable mixed-sex gorilla groups or dynamic communities of Chimpanzees and Bonobos. The latter vary in their group size through the fissioning and fusing of subunits according to their activity and availability of resources. Their large size and folivorous tendencies enable gorillas to cope with fruit shortages and reside in cohesive social units. Gorilla groups are polygynous or polygynandrous, with one or more adult silverback males, several females, and their offspring forming the core of relatively stable groups. Immature individuals account for

The milk of the Eastern Gorilla (beringei subspecies “Mountain Gorilla,” shown here) is lower in fat and total energy than that of other hominids, including humans, but higher in crude protein. Male infant gorillas suckle more than females, as would be expected because of their greater eventual size. However, research suggests that when mothers are in poor condition and the chances of raising a male to weaning are lower, those with daughters invest more time ingesting food and suckling than those with sons. Maternal skills improve with age: first time mother gorillas have a 50% higher offspring mortality rate than those giving birth for second and subsequent times. Gorilla beringei beringei Volcanoes National Park, NW Rwanda. Photo: Suzi Eszterhas/Bios

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FAMILY HOMINIDAE Great Apes

Comparisons with orphan orangutans have shown the importance of a competent mother in the development of the young orangutan’s locomotion skills. The very young Sumatran Orangutan clings to its mother while she travels. As it begins to make its own way, she helps by pushing or pulling it, or dragging branches together to narrow the gap between them. Between the ages of two and three years, the youngster begins to travel independently, although it never goes more than a meter or two away from its mother. At this early age, the mother may move more slowly to enable the infant to keep up with her, but increasingly it is the infant, rather than the mother, who maintains the close distance between them. Somewhere between the ages of three and six, the young orangutan reaches full locomotory independence and can travel as fast, or even faster, than its mother. Being so much lighter, it is able to use more slender and ﬂexible supports than she can. It clings to its mother far less and is increasingly found beyond the reach of her arms, although still rarely out of her sight. It starts to leave its mother during part of the day at seven years old, but it is not usually found traveling alone until it is ten or eleven. Above: Pongo abelii Gunung Leuser National Park, N Sumatra. Photo: Art Wolfe

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Below: Pongo abelii Gunung Leuser National Park, N Sumatra. Photo: Cyril Ruoso

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FAMILY HOMINIDAE Great Apes

The young Chimpanzee or Bonobo (Pan paniscus) is carried clinging to its mother’s belly for its first few months. But within a few weeks it is also capable of riding on its mother’s back when she walks quadrupedally (see also the pictures of Bonobos below). Twin Chimpanzee births are rare, and the survival of both twins even rarer. It is difficult for females to carry twins and feed herself, so usually one or both of the twins die. On average, female Chimpanzees give birth to four offspring during their lifetimes, but only 1·5–3·2 survive beyond infancy. Infant survival increases with the social rank of the mother. Pan troglodytes Drill Ranch Afi Mountain, Cross River State, S Nigeria. Photo: Cyril Ruoso

40–50% of group members. A proportion of all populations are solitary adult males or “lone silverbacks” that either left their natal groups voluntarily or were ousted. Group size, composition, and patterns of dispersal are similar across populations of all gorilla taxa; the main difference between species is that about 40% of Eastern Gorilla groups contain multiple adult males. Median group size of both species is ten individuals, but maximum group size of the Eastern Gorilla is double that of the Western Gorilla (65 members versus 32 members). The dominant male in any group is the center of attention. One of his main roles is to use his strength, size, and intimidat-

ing displays to defend females from other males. Among great apes, only female gorillas live in permanent association with males, relying on male protection of their infants against infanticide. Adult females therefore develop strong bonds with their group leader. A female that transfers to another group with an infant faces the risk of her offspring being killed by the dominant male of her new group. Hierarchies exist among adult male gorillas, competition between them is intense, and aggression is common when females are sexually receptive. There is little affiliative behavior between adult males or between unrelated females. Related

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The infant Bonobo gradually learns how to position its body and hands in ways that facilitate and seem to encourage being picked up and carried by its mother. The mother can then sweep it up as she moves, while keeping her eyes on her destination. The mean interbirth interval of Bonobos is shorter than that of Chimpanzees (Pan troglodytes), and females can simultaneously carry and nurse two offspring if one is born before the older one is weaned. Based on 20 years of research at Wamba, DR Congo, Bonobo infant mortality is much lower than that reported for Chimpanzees. This seems to be related to abundant fruit and herbaceous foods, larger food patch size, female feeding priority, and the absence of infanticide. Left: Pan paniscus Lola ya Bonobo Sanctuary, W DR Congo. Photo: Régis Cavignaux. Right: Pan paniscus Photo: Martin Harvey/DRK

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FAMILY HOMINIDAE Great Apes

Pongo pygmaeus wurmbii Tanjung Puting National Park, S Borneo. Photo: Hanne & Jens Eriksen

Play between the mother Eastern Gorilla and her offspring begins when the infant is about twelve weeks old. At this age, mother and infant are in constant physical contact. The infant watches its mother’s movements and begins to manipulate objects. From eight months of age, the infant spends less time in direct physical contact, but remains within its mother’s reach and whimpers if she moves away. Gorilla beringei beringei Volcanoes National Park, NW Rwanda. Photo: Art Wolfe

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females maintain close proximity and often groom each other. Most intragroup aggression is between adult females, involves more screaming than physical contact, and often ends with the intervention of an adult male, thereby limiting the effectiveness of female coalitions. Both males and females may be philopatric, but about one-half disperse from their natal groups upon reaching sexual maturity. Some females remain and reproduce within their natal group. Emigrating males will not be accepted into another reproductive unit, so they become solitary for a number of years, sometimes for the rest of their lives. A few young males are accompanied by females when they emigrate, thus splitting off as a social unit. Solitary males will try to attract females from groups and establish a new group. If the leader of a unimale group dies, his group will disintegrate. Emigrating females have the choice of joining a solitary male, but they more often transfer to another group. Multimale groups evolve when a maturing male is tolerated by the dominant male and is able to stay with his natal group. Genetic studies have confirmed that such males are often, but not always, related. Adult males in multimale groups cooperate during intergroup encounters and actively prevent females from leaving by herding them. When the leader dies, a subordinate takes over, and the group remains intact. Multimale groups are therefore more stable and may persist for generations. Non-reproductive gorilla groups form when adult and adolescent males become a social unit, usually for a number of months rather than years. Chimpanzees and Bonobos live in multimale–multifemale communities. The community is a closed social network; membership changes only with births, deaths, and permanent transfers. Females emigrate from their natal group when they reach sexual maturity, but philopatric males remain. There are no cohesive groups; the community fissions into temporary parties of varying size and composition within the larger, more stable whole. Social relationships within communities are hierarchical and relatively affiliative, but antagonistic between them. The mean size of Chimpanzee communities is 35 individuals, ranging from 16 to 82, with one especially large unit of about 150 members known in Uganda. In forest habitats, party size is usually five to ten individuals, or about 15% of the community. In the savanna woodlands of Senegal, mean party size is larger than elsewhere at 15 individuals and about 50% of community members. Single-sex parties are common, but the

most common aggregations are a mix of males and females with immature offspring. Parties usually build around large food patches, although entire communities rarely if ever come together at the same time. Female Chimpanzees usually range with any dependent offspring, sometimes with other mother–infant units, rarely joining large parties when they are sexually receptive. Juveniles and adolescents associate with their mothers. Immature males spend increasing amounts of time with other males as they grow up, despite frequent aggression from older males. When they mature, at about 15 years of age, males are integrated into

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The mother Bornean Orangutan does not actively teach the infant what to eat. Instead, the young one watches her attentively and imitates her as it begins to feed itself. Studies of immature orangutans have found that their diets are often different from one another, but usually identical to what their mothers eat. Although they are competent foragers by the age of four, there will still be important foods they have not yet encountered because many south-eastern Asian trees fruit at long, irregular intervals. This may explain the young orangutan’s uniquely long period of “ecological dependency” on its mother, 10–11 years for Sumatran Orangutans (Pongo abelii) but shorter in Bornean Orangutans.

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FAMILY HOMINIDAE Great Apes

By one year old, Chimpanzee play becomes more vigorous and includes play-biting and wrestling. As the youngster grows, it spends less time playing with its mother and more time playing with its siblings, peers, and other adults. It plays most frequently with those of its own age and size. Play becomes steadily rougher as youngsters grow, particularly when well-matched partners are playing together. Older and larger juveniles play more gently when their partners are smaller or younger. Juvenile male Chimpanzees play more frequently than females, and their play is more likely to involve wrestling and mock-fighting. Young female Bonobos (Pan paniscus), by contrast, play more frequently together than males, which may be related to the close bonds between adult females in Bonobo communities. Adult female Chimpanzees associate less with other females and spend most time with their offspring, so play that establishes and maintains bonds between females may be less important to them. Play that identifies the stronger and weaker individuals helps to establish dominance relationships and helps the youngsters recognize their own place in the hierarchy. The relaxed open-mouth expression, or play face, is similar to the bared-teeth display used by adults when appeasing an aggressor, and it may help to prevent play escalating into real fighting.

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Pan troglodytes schweinfurthii Gombe Stream National Park, W Tanzania. Photo: Cyril Ruoso

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FAMILY HOMINIDAE Great Apes

Pongo pygmaeus Sepilok Orang Utan Rehabilitation Centre, Sabah, NE Borneo. Photo: Konrad Wothe

The young Chimpanzee begins to sample solid food at around three months old, and is eating regularly by 6–10 months. It continues to suckle until 3–4 years old, but from the age of two, the long process of weaning begins. The mother holds the infant away from her or blocks access to her nipple with an arm or leg. She is patient and gentle throughout weaning, even when the youngster responds with temper tantrums, and will attempt to distract it with play and grooming. The young Chimpanzee temporarily shows elements of depression as the nipple is progressively withheld, playing less, losing its appetite, huddling alone, and attempting to resume its close infantile contact with its mother. Pan troglodytes schweinfurthii Mahale Mountains National Park, W Tanzania. Photo: Günter Ziesler

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male networks and are dominant to all females and immatures. Male Chimpanzees are more gregarious than females, develop strong bonds, groom one another frequently, and participate in cooperative activities such as boundary patrols and hunting. Linear dominance hierarchies among males are dynamic and maintained by aggression toward subordinate individuals. Males use alliances to bolster their position in the hierarchy, and mutual grooming is thought to service the relationships and coalitions that can lead to higher status. Dominance relationships among females are correlated with age. Bonobo communities comprise 10–120 individuals. Most members meet every day, and feeding and travel may involve entire communities. When foraging on the ground, Bonobos splinter into mixed-sex parties that tend to be more cohesive and larger than Chimpanzee parties, averaging 4·8–22·7 individuals. Male Bonobos are more peaceable than male Chimpanzees; they interact less, compete less, and are not aggressive to males from other communities. Bonds among adult male Bonobos are weaker than among male Chimpanzees, but they retain strong ties with their mothers throughout their lives, which may influence their position in the dominance hierarchy. Female Bonobos are strongly bonded, whether or not they are related. Forming coalitions helps females to offset their size disadvantage, and they support each other against (infrequent) male aggression; therefore, female social status is roughly equal to that of males. Adult males form friendly pair-relationships with unrelated adult females, and high-ranking males invest more in these relationships than do lower-ranking individuals. Grooming between Bonobos of the opposite sex is more frequent and prolonged than grooming between same sex pairs. Bonobos are famous for their non-conceptive sexual behavior, which occurs between almost all age and sex categories, females with females, males with males, and adults with individuals of any age. Only sexual contacts between mothers and sons are avoided. Adult males mount each other or engage in rump-rump touching. Females use genito-genital or “G-G” rubbing during periods of tension, such as reconciliation or excitement during greeting. For example, young females entering a community for the first time seek sexual contact with the dominant females. G-G rubbing is frequent during feeding and after aggressive incidents. Low-ranking females initiate contact with higher-ranking females. This behavior is thought to relieve social tension between females and help them to cooperate without aggression. It thus plays a role in maintaining social cohesion.

Relationship with Humans Humans have hunted great apes for centuries. Before firearms were widely available, hunting was sustainable. All modern hunting of great apes is illegal, but it remains one of the main causes of their decline. This persecution is mainly for food, although there is some capture of live animals for international trade, which is also illegal. In Asia, orangutans in some regions are protected by strong cultural reluctance to eat them, but the “modernization” of attitudes has put them at risk. The modernization of hunting methods combined with unprecedented habitat loss and rapid expansion of human populations has caused orangutan populations to plummet.

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The young Bornean Orangutan becomes increasingly independent of its mother at 6–8 years old, especially following the birth of a younger sibling. But it may still seek her protection, and until displaced by the new infant, it also shares her nest. Males were thought to disperse from their natal territory and females to remain close by. Female orangutans grow more slowly than males, and continue growing until around 18 years old, which is longer than for any other hominid except humans. Males continue to grow throughout their lives.

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FAMILY HOMINIDAE Great Apes

In Africa, hunting of great apes as bushmeat is widespread, especially where they are not considered culturally “off the menu.” In many localities, religion and taboos against eating great apes prevent people from consuming their meat; for example, the Iyaelima people in DR Congo do not eat Bonobos, and the Vili people of coastal Gabon are forbidden from eating Chimpanzees. Nevertheless, the majority of people eat ape meat if given the chance. In 1994, T. Kano and R. Asato reported that everyone they interviewed in northern Republic of the Congo had eaten gorillas or Chimpanzees. Commercial and subsistence hunting grade into each other. Commercial hunting implies that meat is sent away from the hunter’s village to a nearby town, or to distant cities, as is increasingly common with improving transport networks in the region, to be sold at much higher prices as a luxury item for urban dwellers. In Central Africa, poaching is the main cause of great ape decline. Grauer’s Gorillas in eastern DR Congo have been particularly affected, targeted to feed illegal mining camps. The numbers of great apes captured live for international trade are dwarfed by the numbers killed for their meat. Nevertheless, live capture remains a serious threat, particularly in South-east Asia and West Africa. To obtain one infant, several adults will be killed—the mother and any individuals who try to defend her. Habitat loss is an overwhelming direct threat to great apes. Recent research suggests that forest clearance by humans in the rainforests of Central Africa started 3000 years ago, and apart from the huge block remaining in the Congo Basin, much of Africa’s forests have been lost. In the 1990s, 17 countries already had less than 10% of their original forest cover, and only six countries still had more than 20%. In West Africa, 80% of original forest cover is gone, mainly due to subsistence agriculture and unsustainable land-use, and yet forest loss continues. In Ivory Coast, for example, Marahoué National Park lost 93% of its forest cover in just six years (2002–2008), with the concomitant loss of most of the Chimpanzees living there. Deforestation is of particular concern in areas where there is existing or planned industrial agriculture, where there is a high demand for fuelwood or charcoal along roads penetrating the forest, and in areas of high human density where land is at a premium for slash-and-burn agriculture. In Asia, widespread logging (both legal and illegal), rapid expansion of oil palm

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and pulpwood plantations, extensive and poorly planned development of road infrastructure, and unrestrained use of fire to clear land are having catastrophic consequences for orangutans. It is estimated that Borneo and Sumatra will each have lost 98% of their original forest cover by 2022. The total area of natural habitat has been decreasing rapidly for over 50 years, and habitat loss has long been recognized as one of the main threats to the survival of the orangutan. Although orangutans can survive in lightly logged forests, they cannot live in oil palm plantations, where the habitat is irreversibly altered, without access to some natural forest. Recent analysis suggests that at least 10,000 km2 of natural forest—5% of total habitat of orangutans—was converted to oil palm between 2000 and 2010. Much of the remaining stronghold habitat of the Sumatran Orangutan (Tripa Peat Swamps within the Leuser Ecosystem) is currently under severe threat of conversion to plantations. Deforestation in the Congo Basin has been slower than in other regions where the great apes occur, but it has doubled since 1990 and will increase further in coming decades with the expansion of industrial agriculture. Although clearing of forest for mining is a worrying issue, it affects a far smaller surface area than clearing for industrial plantations or subsistence agriculture, and the most serious consequence of mining is usually massive poaching following the influx of people into lightly inhabited areas. Great ape populations outside the main forest block of the Congo Basin are greatly threatened by habitat fragmentation through the rapid removal of forest outside protected areas. In the drier regions of tropical Africa, regular fires also destroy great ape habitat. Crop depredation is a major source of conflict between people and wildlife globally. As human populations expand and natural habitats shrink, great apes increasingly come into contact and conflict with people over living space and food. The rapid clearance of forest for subsistence and commercial farming means loss of natural food species, which drives great apes to exploit human foods. Crop-raiding may threaten the economic security of rural peoples, and as a result, crop-raiding great apes risk harassment, injury, or even death during confrontations with people. Great apes are large, very strong, and pose a potential risk to human safety. This exacerbates conflict issues and sometimes provokes retaliatory killings by local people. The illegal hunting and capture of infants to sell into the pet trade are symptoms of habitat conversion when great apes are viewed as pests and killed for raiding crops. Disease is a major direct threat to great apes. According to T. Humle and R. Kormos, writing in 2011, infectious disease is the main cause of death in some populations of Eastern and Western Chimpanzees. Great apes in East and West Africa are generally most at risk from human-borne disease because human density is much higher than in the Congo Basin. Levels of hygiene in rural communities are poor, and the probability of great apes contacting humans or human waste is high. Local people and international tourists are potential carriers of diseases to which great ape populations have had no prior exposure and thus have no natural immunity. Indirect threats often act upon several direct threats at once. Increased access to forests is a good example. Penetration of formerly intact, remote forests by industrial logging and mining roads facilitates poaching, exacerbates habitat loss, and increases the probability of introducing human diseases into great ape populations. Roads allow journeys that would take weeks on foot to be covered in a matter of hours by a vehicle. Easy and rapid access deep into the forest and equally easy and rapid export of forest products, notably bushmeat, are the result. Meat can be transported swiftly for sale to surrounding villages and towns, and even to distant cities. Bushmeat destined for relatively wealthy city dwellers often travels hundreds of kilometers from the point of origin. The perception of bushmeat as a delicacy inflates prices at these destinations, and the trade is highly profitable to the middlemen and women along the commodity chain. A study distinguishing subsistence and commercial hunting in Gabon found that commercial hunting was the stronger driver of losses of great apes. In both Africa and Asia, especially in countries where there is pressure for land, newly created roads attract settlers who clear forest for subsistence agriculture, thus creating wide corridors of “farmbush” along road edges. Considerable areas of forest are removed and degraded as time goes on.

The time that the young Eastern Gorilla spends in contact with its mother decreases sharply at 18 months. By this age, most young gorillas have begun traveling independently, although they have been seen riding on their mothers’ backs as late as 44 months old. Following weaning at 3–4 years, close physical contact with the mother ceases altogether. Gorillas grow and mature faster than Chimpanzees (Pan troglodytes) or orangutans (Pongo). They have relatively smaller brains and may have fewer survival skills to learn than other apes, which are subjected to wider fluctuations in food availability and other environmental challenges. Gorilla beringei graueri Kahuzi-Biéga National Park, E DR Congo. Photo: Russell A. Mittermeier/ Conservation International

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FAMILY HOMINIDAE Great Apes

Young Bonobos play together, and older Bonobos often play with juveniles and infants. Unlike male Chimpanzees (Pan troglodytes), adult male Bonobos interact frequently with young ones and occasionally carry them. This contributes to the more harmonious nature of Bonobo societies, which show little of the aggression between individuals that is found among Chimpanzees. Studies of captive Bonobos have found that youngsters may also play an important role as facilitators of relationships between adults and between resident and new group members. In free-ranging animals, immigrant females join immature animals as the most frequent participants in play. An immigrant mother will carefully supervise the introduction of her daughter until she is accepted by the new group. Male Bonobos also remain close to their mothers long after they have reached maturity and continue to accompany them when traveling. The status of a young male Bonobo in a group is a direct reflection of his motherâ&#x20AC;&#x2122;s status. This continues well after males have reached maturity; a change in dominance between high-ranking males is sometimes preceded by a corresponding change in their mothersâ&#x20AC;&#x2122; relative status. This maternal influence may give sons greater access to females and thereby maximize the number of descendants of the mothers.

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Pan paniscus Photo: Konrad Wothe

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FAMILY HOMINIDAE Great Apes

Human population growth is an underlying indirect threat to great ape survival and is gravest where humans have already converted much of the habitat previously available to great apes. Average growth rates of human populations in East, West, and Central Africa are 2–3% per year, which results in a doubling of the population every 30–50 years. Indonesia and Malaysia have lower growth rates of 1% and 1·5%, respectively, but human densities are already extremely high at 86 and 132 people/km2, respectively, compared with about 36 people/km2 in sub-Saharan Africa. The degree of urbanization is highly variable; in some countries, most people live in towns and cities (for example, 86% in Gabon), and in others, a medium to large proportion live by subsistence farming in rural areas (for example, 55% in Indonesia and 87% in Uganda). All of this means that the area remaining for wildlife is being reduced at varying rates in different countries, and that some have very little land suitable for great apes outside the protected areas. Gabon and Republic of the Congo have by far the lowest human densities and among the highest urbanization rates of the forested zone (6–12 people/km2 and 62–86% of the population living in cities and towns), so it is not surprising that these two countries still have important great ape populations. A widespread, insidious, and extremely damaging indirect threat to wildlife and people alike is corruption. Corruption leads to most of the indirect threats that are associated with compliance with national and international laws. Most of the countries in which great apes are endemic are considered more corrupt than the global average (Ghana, Liberia, Malaysia, and Rwanda are exceptions), and twelve of them rank among the 25% most corrupt countries in the world. Two great ape taxa, Grauer’s Gorillas and Bonobos, occur only in DR Congo and three-quarters of the world’s Mountain Gorillas are found in this country, which ranks 15th on the global corruption scale. Corruption fuels many of the other indirect threats, especially the lack of law enforcement and judiciary follow-up, which in turn perpetuates illegal logging, illegal mining, illegal hunting, and illegal trafficking of wildlife, including great apes. Companies can and do profit from poor governance in some of the countries with great apes because they are able to exploit natural resources even in areas where such activities are prohibited (for example, inside national parks) and to ignore national and even international environmental regulations and quota systems. For example, illegal logging is rife in Indonesia and Sierra Leone, illegal clearance of land for oil palm plantations threatens Sumatra’s swamp forests, and oil exploration is

underway in Virunga National Park in DR Congo—a United Nations Educational, Scientific and Cultural Organization (UNESCO) World Heritage Site. Political instability, insecurity, and war are the final group of closely related indirect threats to the great apes. Many of the 23 countries that are home to the great apes have suffered protracted periods of civil war in recent years: the Aceh Province of Sumatra, eastern DR Congo, Liberia, and Sierra Leone, to name a few. The Eastern Afromontane Biodiversity Hotspot harbors both subspecies of the Eastern Gorilla and has been under intense pressure from armed militia and insecurity since the early 1990s. A recent analysis by S. Benz and J. BenzSchwarzburg showed that all countries where great apes live have experienced some kind of war since 1946. Even within the last 25 years (since the end of the Cold War), ten of these countries have experienced conventional internal war (between government and rebels), and several others have experienced so-called “new wars,” defined as conflicts between two or more non-governmental groups. The consequences of these conflicts include proliferation of firearms and other efficient weapons, poaching by soldiers or combatants for food, complete breakdown of law and order that in turn leads to illegal poaching and logging, felling of forests as fuelwood for refugees, and illegal mining to raise money to sustain the conflicts. The scramble for natural resources to fund conflicts and combatants often exceeds the quantities exploited in peacetime, because there is a low risk of these activities being controlled or punished by law enforcement officers and a high incentive to maximize profits. Thus, the rate and geographical extent of both poaching and habitat degradation tend to be much greater during times of conflict than when security returns, to the detriment of great apes and their habitats.

Status and Conservation Organisms that cannot rapidly replace losses in their numbers are intrinsically more vulnerable than those that can. The great apes reproduce very slowly, age of sexual maturity is late, their young require a long time to develop, and the interbirth interval is long (four to nine years depending on the species). After a great ape population has been severely reduced by hunting or disease, it takes several generations to recover, and generation time is 20–25 years, depending on the species. Orangutans are the slowest reproducers and most vulnerable of all, and a loss

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From infancy to the age of 4–5 years, young gorillas spend more time near or interacting with their fathers than with their mothers. The silverback may monitor play and stop it becoming too rough, just as the mothers do. The young female Eastern Gorilla (beringei subspecies “Mountain Gorilla,” shown here) usually emigrates on reaching sexual maturity to join another group or a solitary male. A young male with a particularly close relationship with his father may stay within the natal group. Others become solitary or leave the group accompanied by one or more females. Males that remain within a group and therefore are in a good position to replace the dominant male have a much higher likelihood of reproducing than those that leave.

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Gorilla beringei beringei Virunga National Park, NE DR Congo. Photo: Russell A. Mittermeier/ Conservation International

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FAMILY HOMINIDAE Great Apes

The most recent population estimate for the Bornean Orangutan was 45,000–69,000 individuals, living in around 86,000 km2 of habitat. This is around 14% of the historic population size, qualifying the species as Endangered on The IUCN Red List. But those figures were for 2000–2003, and both ape numbers and habitat extent are likely to have fallen steeply since then. Although fully protected by law, orangutans are hunted for meat and the pet trade; many are killed as pests. Pressures are exacerbated by the accelerating conversion of forests to industrial plantations. Young orangutans enter the pet trade after their parents are killed. Rehabilitation centers like this one attempt to return orphans to the wild by equipping them with the skills their mothers would have taught them. Pongo pygmaeus Sepilok Orang Utan Rehabilitation Centre, Sabah, NE Borneo. Photo: Colin Marshall/FLPA

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by at least 50% between the 1970s and the 1990s. Surveys in the mid-1990s suggested a population totaling about 17,800 (8700–25,500) in discrete areas of their range, but at least two subpopulations have been extirpated in the last few years. The current status of this subspecies is poorly known because there have been few recent surveys, and only in small areas where it was safe for field staff to operate; there are perhaps 2000– 10,000 Grauer’s Gorillas remaining. Mountain Gorillas are the only great ape whose numbers are stable or increasing, but fewer than 800 individuals remain in a tiny area of DR Congo, Rwanda, and Uganda. Western Chimpanzees are patchily distributed, and R. Kormos and colleagues estimated their numbers at 21,300–55,600 individuals in 2003. Numbers are certainly considerably lower now. Even at that time, some countries were thought to have only a few hundred individuals remaining (Guinea-Bissau and Senegal), and they are possibly extinct in Benin, Burkina Faso, and Togo. About two-thirds of the remaining representatives of this subspecies are thought to exist in Guinea and Sierra Leone. In 2010, a national survey of Western Chimpanzees in Sierra Leone by T. Brncic and colleagues found a population larger than anticipated, estimated at about 5500 (3100– 10,400). Recent work by G. Campbell and colleagues in Ivory Coast revealed that 90% of Western Chimpanzees vanished between 1990 and 2007; this author warned that other countries of the region could have lost Western Chimpanzees at a comparable rate. The subspecies stronghold, Guinea, has not been surveyed since 1998. Eastern Chimpanzees could number 200,000–250,000, occurring over a wide area of DR Congo, Tanzania, and Uganda, plus smaller areas of Burundi and Rwanda. This estimate was the result of a modeling exercise based on reliable surveys during the preceding decade. The vast majority live in DR Congo. In 2003, T. Butynski estimated that Central Chimpanzees could number 70,000–116,500 individuals, with the majority in three countries: Gabon, Cameroon, and Republic of the Congo. Declines have likely occurred throughout the region, especially in north-eastern Gabon and western Republic of the Congo due to poaching and Ebola. These declines are as yet unquantified; nonetheless, recent work suggests that there may be 20,000 Central Chimpanzees remaining in Gabon and 25,000 in Republic of the Congo. In 2012, it was confirmed that there are several thousand Central Chimpanzees in Equatorial Guinea. There are only 3500–9000 Nigeria-Cameroon Chimpanzees. As numbers have declined, large areas of suitable Chimpanzee habitat have become “empty forest”—a

841

of just 1% of females in a population can lead to local extinction. These factors—slow reproductive rate and long development time, plus the need for large home ranges—make great apes far more vulnerable to threats than smaller, faster breeders (even monkeys) living in the same habitat. In the past, great ape densities were much higher than they are today in most of the habitats remaining to them. This is evidenced by the fact that within the remaining patches of intact habitat where there is no hunting or habitat clearance, great ape density can be as high as five or more individuals per square kilometer, but it is more commonly one to two individuals. In most of the areas that are not effectively protected from poaching, great ape densities are now very low. In Indonesia, mean orangutan densities are 0·5–1 ind/km2. Forest patches in South-east Asia are much smaller than the extensive forested landscapes in Central Africa, and the rate at which orangutans are encountered in the forest has declined to about a sixth of what it was 150 years ago. At many sites in West Africa there have fewer than 0·5 ind/km2, and in Central Africa gorillas and Chimpanzees occur at low densities. Bonobo densities are also at the low end of the scale. Orangutan numbers have dropped alarmingly in the last century. A decade ago it was thought that only 8% of their original numbers remained. The most recent estimates put Sumatran Orangutans at about 6600 individuals (3500–12,000) and Bornean Orangutans at about 54,000 individuals (45,000– 69,000). Numbers continue to drop rapidly over the orangutans’ entire range, and in the next two to three decades, there may be few, if any, orangutans left in the wild. In the 20 years between 1980 and 2000, Western Lowland Gorilla populations in Gabon were halved by the combined impacts of poaching and a deadly strain of the Ebola hemorrhagic fever virus. An Ebola epidemic then swept across the border into Republic of the Congo claiming at least another 5000 gorillas in just a few months. It is believed that Ebola still poses a high risk to gorillas and Chimpanzees in northern Republic of the Congo, south-western Central African Republic, and south-eastern Cameroon. Western Lowland Gorillas now number about 140,000–160,000, most of which are in northern Republic of the Congo. Important populations also remain in Gabon and south-eastern Cameroon. The Cross River Gorilla numbers only 200–300 individuals. This is perhaps less than 2% of the original population, and their density has dropped to about 15% of what it was thought to be in the 1950s. As such, large areas of the former geographical range of the Cross River Gorilla are now empty. Grauer’s Gorilla numbers were reduced

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FAMILY HOMINIDAE Great Apes

842

phenomenon witnessed in much of the habitat of the great apes in Africa and Asia. Total population size of Bonobos is uncertain because only one-third of their historical distribution has been surveyed. Estimates from four known strongholds of Bonobos suggest a minimum population of 15,000–20,000 individuals. Nevertheless, numbers of Bonobos are still dropping; one-third of the population was lost in a small area of Salonga National Park, DR Congo, between 2006 and 2010, and most of the closed-canopy forest in the “Salonga corridor” no longer had Bonobos in 2007. The main direct threats to great apes are hunting, habitat loss and fragmentation, and disease. The relative importance of each threat depends on location and sociopolitical factors. Direct threats are exacerbated by several important indirect threats, which include human population growth, the bushmeat trade, industrial exploitation of great ape habitat, increased access to previously remote areas, political and economic instability (including proliferation of weapons and munitions), lack of political will, and ignorance and lack of enforcement of laws. Corruption underlies many of these indirect threats. Generally, in countries with little remaining natural habitat and high human densities, great apes survive essentially only in protected areas. In more lightly populated countries with large and intact habitat blocks, great apes are found both inside and outside protected areas. This implies that long-term and effective conservation strategies must be established in areas where currently the main policy focus is on agriculture, mining, or timber, rather than wildlife. Conservation strategies have been undertaken to protect great apes at different levels: site, national, and international. The lowest level is focused in and around specific sites and landscapes and includes maintaining the personnel, infrastructure, and funding for existing protected areas, managing logging concessions to ensure that no hunting of great apes or other protected species occurs, and environmental education of communities surrounding great ape populations. A recent continent-wide study in Africa showed that anti-poaching is one of the most important ways to maintain great ape populations over the long term. Broader policy-based approaches can help protect great apes at a country-wide scale by ensuring that national legislation for protection of great apes and their habitats is as strong as possible and enforced. These approaches will ensure that lawbreakers do not escape justice through corrup-

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tion, adjustments will be made to national spatial plans for logging, mining, and agriculture to minimize disturbance to great ape populations and habitats, and great ape–friendly information will be included in school curricula. International action includes ensuring maximum legal protection for all great ape species, through bodies such as the International Union for Conservation of Nature (IUCN), the United Nations Environment Programme (UNEP), and the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). Also essential is the brokering of agreements between neighboring countries that harbor great apes for the creation, protection, and maintenance of transboundary protected areas and corridors linking important habitats across borders. The IUCN guidelines for minimizing the effects of logging on great apes have been developed to provide information that can be followed by logging companies wanting to obtain (or to keep) Forest Stewardship Council certification. Research into preventing infection and proliferation of human-transmitted diseases has borne some fruit: there is now a greater understanding of how respiratory and other diseases have affected great ape communities in the past. Implementation of the IUCN guidelines for great ape tourism would go a long way in reducing the risks that tourism poses to great apes, but more proactive measures, specifically vaccination, may be necessary as the density of humans surrounding protected areas continues to rise and more great apes come into contact with tourists or park staff. Payments under the Reducing Emissions from Deforestation and Forest Degradation (REDD) scheme could be of use in securing great ape habitat. Nevertheless, bushmeat hunting in tropical forests is likely to reduce carbon stocks by shifting tree species composition away from the larger, carbon-storing trees whose seeds are typically dispersed by large frugivores, such as great apes. Control of hunting is likely to become an essential component of REDD+ programs in the future. All the great apes are listed as Endangered (Bornean Orangutans, Eastern Gorillas, Chimpanzees, and Bonobos) or Critically Endangered (Western Gorillas and Sumatran Orangutans) on The IUCN Red List. All the African great apes are on the Class A list (completely protected) of the African Convention on the Conservation of Nature and Natural Resources. Each country lists their great ape species as officially Both subspecies of Western Gorilla are listed as Critically Endangered on The IUCN Red List. Hunting for bushmeat and disease, especially the Ebola virus, have reduced numbers by more than 60% in the last 20–25 years and by 90–100% in some areas. Although illegal, bushmeat hunting has emptied some protected forests that would otherwise be prime gorilla habitat. The “Cross River Gorilla” (Gorilla gorilla diehli) is the most threatened of all gorilla subspecies, with just 200–300 individuals left in eleven subpopulations with little or no reproductive contact between them. Both subspecies of the Eastern Gorilla (G. beringei) are endangered, and the “Mountain Gorilla” (G. b. beringei) is also listed as Critically Endangered. It may be stable and recovering, but from very low numbers. Political unrest in eastern DR Congo exacerbates poaching of “Grauer’s Gorillas” (G. b. graueri). Gorilla gorilla gorilla Batéké Plateau National Park, SE Gabon. Photo: Cyril Ruoso

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FAMILY HOMINIDAE Great Apes

Until the mid-19th century, the now Critically Endangered Sumatran Orangutan was widespread, but it is now restricted to northern Sumatra, with its stronghold in Aceh Province. A proposed road network in Aceh threatens to fragment the main population, and expose it to hunting and habitat conversion. The renewal of logging permits is a further threat. The 26,000 km2 Leuser Ecosystem Conservation Area, which includes Gunung Leuser National Park, supports 75% of surviving Sumatran Orangutans. Efforts are underway to gain protection for the Batang Toru forests, where around 600 orangutans survive, but much of the area is allocated to logging concessions. Other populations are not thought to be viable in the long term.

protected by national legislation. Great apes also are protected by international laws, but law enforcement is generally weak (see Relationship with Humans). International recognition of the vulnerability of the great apes has been demonstrated by the creation of the United Nations (UN) Great Apes Survival Partnership (GRASP) and the Gorilla Agreement of the UN Convention on Migratory Species of Wild Animals (CMS). The latter lists pragmatic conservation actions to be taken by governments of the countries where great apes reside, such as prevention of poaching, ensuring the creation and maintenance of protected areas, and facilitating the fight against disease. The Kinshasa Declaration on great apes, signed in 2005, provided an international signal of political will to maintain great apes in all of their native countries. General Bibliography African Union (1968), Alvarez (2000), Amsini et al. (2008), Ancrenaz, Ambu et al. (2010), Ancrenaz, Dabek & O’Neil (2007), Ancrenaz, Goossens et al. (2004), Anderson et al. (2006), Andrews (1978), Andrews & Cronin (1982), Bayon et al. (2012), Benz & Benz-Schwarzburg (2010), Bergl et al. (2008), Bermejo & Omedes (1999), Bermejo et al. (2006), Bingham (1932), Blake & Fay (1997), Boesch & Boesch-Achermann (2000), Bradley et al. (2005), Brncic et al. (2010), Brodie & Gibbs (2009), Butynski (2001), Caldecott (2005a, 2005b), Caldecott & Ferriss (2005), Caldecott & McConkey (2005), Campbell-Smith, Campbell-Smith et al. (2011), Campbell-Smith, Simanjorang et al. (2010), Campbell, Kuehl et al. (2008), Cant (1987), CIA (2012), Cipolletta et al. (2007), Clark & Wrangham (1993), Clark et al. (2009), CMS (2007), Coolidge (1933, 1936), Corp & Byrne (2002), Corruption Perceptions Index (2011), Cousins (1990), Crockford & Boesch (2005), Delgado (2010), Delgado & van Schaik (2000), Doran (1996), Doran-Sheehy et al. (2004), Dudley et al. (2002), Elkan et al. (2006), Ellison et al. (2005), Emery Thompson & Wrangham (2008, 2013), Ernst et al. (2012), Ferriss (2005), Ferriss et al. (2005), Fischer et al. (2006), Fossey (1972), Fox et al. (2004), Fruth & Hohmann (1996), Furuichi et al. (1998), Galdikas (1988), Georgiev et al. (2011), Goldsmith et al. (2006), Gonder, Locatelli et al. (2011), Gonder, Oates et al. (1997), Goodall & Athumani (1980), Goodman (1963), Goossens, Chikhi, Ancrenaz et al. (2006), Goossens, Chikhi, Jalil et al. (2009), Goossens, Kapar et al. (2011), Gray, McNeilage et al. (2010), GRASP (2006), Gray, Roy et al. (2013), Gross-Camp et al. (2009), Grossmann et al. (2008), Groves (1986, 1988b, 1989, 1992, 2001, 2005a, 2013), Grueter et al. (2012), Guschanski et al. (2009), Hall et al. (1998), Hansen et al. (2011), Hanson et al. (2009), Hardus, Lameira, Singleton et al. (2009), Hardus, Lameira, Zulfa et al. (2012), Harrison & Chivers (2007), Head et al. (2011), Hicks et al. (2010), Hill, C.M. (2004), Hill, K. et al. (2001), Hockings & Humle (2009), Hockings & McLennan (2012), Hohmann & Fruth (1994, 2003, 2008), Humle (2003), Humle &

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Kormos (2011), Hunt & McGrew (2002), Ingmanson (1996), Inogwabini et al. (2007), Inskipp (2005), IUCN & ICCN (2012), Jansen et al. (2010), Kano & Asato (1994), Kingsley, M.H. (1897), Kingsley, S. (1981), Knott (1998a, 1998b, 2005a, 2005b), Knott, Emery Thompson et al. (2010), Knott, Emery Thompson & Wich (2009), von Koenigswald (1952), Koh et al. (2011), Koops et al. (2012), Kormos & Boesch (2003), Kormos et al. (2003), Kuehl et al. (2009), Lacambra et al. (2005), Lameira & Wich (2008), Laurance et al. (2006), Lingomo & Kimura (2009), Macdonald et al. (2011), Macfie & Williamson (2010), MacKinnon (1971), Marshall, Ancrenaz et al. (2009), Marshall, Lacy et al. (2009), Marshall & Wrangham (2007), Masi et al. (2009), McConkey (2005c, 2005d), McGrew (2004, 2010), Meijaard & Sheil (2008), Meijaard & Wich (2007), Meijaard, Albar et al. (2010), Meijaard, Welsh et al. (2010), Meijaard, Wich et al. (2012), de Merode et al. (2007), Miles et al. (2005), Morgan, B.J. & Abwe (2006), Morgan, B.J., Adeleke et al. (2011), Morgan, B.J., Wild & Ekobo (2003), Morgan, D. & Sanz (2006, 2007), Morrogh-Bernard et al. (2009), Myatt & Thorpe (2011), Myers Thompson (2002), Nijman (2009), Nishida et al. (2003), Nixon et al. (2010), Nixon et al. (2012), van Noordwijk & van Schaik (2005), Normand & Boesch (2009), Oates (2011), Oates, Groves & Jenkins (2009), Oates, Sunderland-Groves et al. (2007), Oken (1816), Paoli et al. (2006), Parnell (2002), Patterson et al. (2006), Plumptre, Amsini et al. (2009), Plumptre, Rose et al. (2010), Pradhan et al. (2012), Prasetyo et al. (2009), Pruetz & Bertolani (2007, 2009), Rainey et al. (2010), Rayadin & Saitoh (2009), Reinartz et al. (2013), Rijksen (1978), Robbins, A.M., Robbins et al. (2006), Robbins, A.M., Stoinski et al. (2011), Robbins, M.M. & Robbins (2004), Robbins, M.M. et al. (2004), Rogers (1993), Rogers, Abernethy et al. (2004), Rogers, Voysey et al. (1998), Rothman et al. (2008), Ruffler & Murai (2012), Ryan & Walsh (2011), Sarmiento & Oates (2000), Sawyer & Robbins (2009), Sayer et al. (1992), van Schaik (2001), van Schaik et al. (2009), Schöning et al. (2006), Schwarz (1929, 1932), Stanford (2006), Stewart (1988), Stokes et al. (2010), Stumpf & Boesch (2010), Sugiyama & Fujita (2011), Sunderland-Groves et al. (2009), Surbeck & Hohmann (2008), Surbeck, Deschner et al. (2012), Surbeck, Fowler et al. (2009), Thalmann et al. (2011), Thompson et al. (2008), Thorpe & Crompton (2009), Tranquilli et al. (2012), Tutin & Fernandez (1994), Tutin, Fernandez et al. (1991), Tutin, Stokes et al. (2005), Uehara (1990), UNDP (2011), Utami Atmoko & van Schaik (2010), Venter et al. (2009), Videan & McGrew (2002), van Vliet & Mbazza (2011), de Waal (1988), Waller (2011), Walsh, Abernethy et al. (2003), Walsh, Biek & Real (2005), Watts (1984, 1988, 1998, 2006, 2007, 2008), Whiten et al. (1999), Wich, Fredriksson et al. (2012), Wich, Meijaard et al. (2008), Wich, Riswan et al. (2011), Wich, Singleton et al. (2003), Wich, Utami-Atmoko et al. (2004), Wich, Vogel et al. (2011), Wich, de Vries et al. (2009), Wilkie, Shaw et al. (2000), Wilkie, Starkey et al. (2005), Williamson (1988), Williamson & Butynski (2013a, 2013b), Williamson & Fawcett (2008), Wilson et al. (2007), World Bank (2012), Wrangham (1986), Wrangham, Chapman et al. (1996), Wrangham, Conklin-Brittain & Hunt (1998).

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Pongo abelii Gunung Leuser National Park, N Sumatra. Photo: Art Wolfe

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species acco

blanca.indd 2

15/05/2013 11:15:52

ounts sample

blanca.indd 3

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ssp oerstedii

1 ssp citrinellus

ssp cassiquiarensis

2 ssp albigena

ssp sciureus

5 ssp collinsi

ssp boliviensis

ssp peruviensis

PLATE 24

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inches

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Plate 24 Species Accounts

Subfamily SAIMIRIINAE Genus SAIMIRI Voigt, 1831

1. Central American Squirrel Monkey Saimiri oerstedii French: Saimiri à dos roux / German: Mittelamerika-Totenkopfaffe / Spanish: Mono ardilla de América Central Other common names: Red-backed Squirrel Monkey; Black-crowned Central American Squirrel Monkey (oerstedii), Gray-crowned Central American Squirrel Monkey (citrinellus)

Taxonomy. Chrysothrix oerstedti Reinhardt, 1872, vicinity of David, Chiriquí, Panama. S. oerstedii has five pairs of acrocentric chromosomes. Two subspecies recognized. Subspecies and Distribution. S. o. oerstedii Reinhardt, 1872 – Pacific coast of SE Costa Rica (Puntarenas Province) and SW Panama (Chiriquí Province), from the S bank of the Río Grande de Térraba to the mouth of the Río Fonseca and the Archipelago of the Golfo de Chiriquí; in Panama elevations from sea level to 500 m. S. o. citrinellus Thomas, 1904 – historically along the Pacific coast of W Costa Rica in Puntarenas Province (elevations up to 500 m), the NE limit marked by the Río Tulín in the N Herradura Mts (9° 40’ N, 84° 35’ W) and Dota Mts (9° 37’ N, 84° 35’ W), and the S limit by the N bank of the Río Grande de Térraba (8° 25’ N, 84° 25’ W); its populations are entirely fragmented. Descriptive notes. Head–body 28–33 cm, tail 33–43 cm; weight 750–950 g (males) and 600–800 g (females). Female Central American Squirrel Monkeys tend to be c.16% smaller than males. The crown is dark, with tufted ears. White arches above the eyes are of the “Gothic” type. The back and sides of the trunk are largely bright orange or reddish orange. In the “Black-crowned Central American Squirrel Monkey” (S. o. oerstedii), crowns of males and females are black, and outer sides of legs are orange like arms. In the “Gray-crowned Central American Squirrel Monkey” (S. o. citrinellus), crowns of males are agouti and are black in females. Males have no sideburns, and their preauricular patch is agouti or buffy, like their cheeks. Females have dark sideburns separating the white face patch from the white fur of the ear. Outer sides of legs are buffy or grayish-agouti. Habitat. Lowland evergreen forest, with a preference for middle and lower canopies of secondary forest. Central American Squirrel Monkeys enter tall mature forest and late successional forest at times of food scarcity (late wet season). In Corcovado National Park, Costa Rica, where the Central American Squirrel Monkey has been studied by S. Boinski and her students and colleagues, it prefers forest with a heavy herbaceous ground cover of Musa sapientum (Musaceae), Heliconia (Heliconiaceae), and Piper (Piperaceae); a shrubby understory; and early pioneer trees that sometimes form dense stands, such as Cecropia obtusifolia (Urticaceae), Posoqueria latifolia (Rubiaceae), Vitex cooperi (Verbenaceae), and Psidium guajava (Myrtaceae). In more advanced stages of succession, abundant trees include Ficus (Moraceae), Inga (Fabaceae), Apeiba membranacea (Tiliaceae), Spondias mombin (Anacardiaceae), and Quararibea asterolepis (Malvaceae). Forests of the Pacific coasts of Costa Rica and Panama receive heavy annual rainfall, averaging 4970 mm. Some years are very wet, others drier, and there are marked seasons—late wet season, dry season, early wet season, and mid-wet season— when food availability clearly differs. Fewer insects are available during the mid- and late periods of the wet season (torrential rains and little fresh foliage) compared with the dry season and early wet season. Fruits and flowers are least abundant in the late wet season and most abundant in dry and early wet seasons. Food and Feeding. Diet of the Central American Squirrel Monkey includes fruits, nectar, and animal prey, including larval, pupal, and adult insects, bird eggs and nestlings, anole lizards, tree frogs, and bats. Squirrel monkeys are foliage gleaners, animal prey dominates their diets. Most prey is found in dead or living furled leaves (spiders and grasshoppers) or is effectively sessile (caterpillars, pupae, and bird eggs). The most important families providing fruits include Melastomataceae, Rubiaceae, Musaceae, Vitaceae, and Piperaceae. Fruits are generally small and are available piecemeal, ripening gradually over prolonged periods. Most food items are small, dispersed, and unpredictable in their location. In Boinski’s study, less than 3% of all feeding was dedicated to eating fruits or flowers in synchronized bouts in large tree crowns. In times of food scarcity, Central American Squirrel Monkeys increase their foraging time, so the amount of time that they spend feeding on arthropods varies little during the year. Fruit and nectar tend to be eaten more than expected based on availability and when insect abundance is low. Tent-making bats are an unusual food item of the Central American Squirrel Monkey. They recognize the “tents” made by certain phyllostomid bats up to 20 m away. These bats bite bases of lateral nerves of large leaves of species of Marantaceae, Araceae, Musaceae, Cyclanthaceae, and Heliconiaceae, causing leaves to collapse and form a tent around the mid rib. One to 50 bats may be found in these refuges, depending on the species. Three tent-making bats occur in Corcovado Na-

tional Park: Thomas’s Fruit-eating Bat (Artibeus watsoni), the Common Tent-making Bat (Uroderma bilobatum), and the Southern Little Yellow-eared Bat (Vampyressa pusilla). These bats are sensitive to vibrations of the foliage around them and cannot be stalked, so squirrel monkeys leap at the tents. Often tents are empty because these bats make and variably use a series of tents scattered through the forest. When a 4-year-old male Central American Squirrel Monkey captured a juvenile fruit-eating bat, it knocked the bat to the ground and then seized and killed it with seven bites to the head. The male took it up to a branch and ate it rapidly (1 minute and 40 seconds). Sometimes squirrel monkeys find spherical nests of paper wasps (Polybia) in the bat tents. They leap repeatedly at the tents to knock the wasp nest to the ground. After each leap, they fall to the ground and roll away several meters to avoid being stung. When the wasp nest falls and breaks, the squirrel monkeys grab a piece of it and eat the larvae. Female Central American Squirrel Monkeys are rapid and avid eaters and rest less frequently than males. Males spend less time feeding and more time in sexual interactions and investigations and vigilance for predators. Breeding. In Corcovado National Park, the mating season of the Central American Squirrel Monkey occurs in the mid-wet season from August to early October. Males are sexually mature at 2·5–3·5 years old. In June, about two months prior to the mating season, males begin to increase in body size, associated with high levels of thyroid hormones, steroids, and testosterone. Males may increase their weight by as much as 20%, and testicular volume and spermatogenic activity also increase. Older males become larger than younger males. During the mating season, up to 16 males (including some that are sexually immature) chase and mob females to smell their genitalia to assess their sexual receptivity. If not receptive, a female rejects males’ advances. Receptive females engage in mutual genital sniffing and follow and solicit copulations from the largest resident male. Evidence indicates that a female restricts her mating to just one male through an ovulatory cycle, which suggests that sperm competition does not occur. Sperm forms a copulatory plug that lasts several hours. Sometimes the largest male apparently hides (after having mated several times already that day) or is involved with another female, and another receptive female ends up mating with another resident male. The largest male copulates most and achieves an almost total monopoly of fully adult females. His supremacy as the largest male of the group only lasts one or two mating seasons. Sometimes a band of males from a neighboring group briefly infiltrates the group, and some of them copulate with females during the melee. Based on swelling of vaginal labia and the switch from rejection to solicitation, the period of sexual receptivity (periovulatory) is c.6–8 days. After gestation of 152–168 days, a female gives birth to a single young in the dry season (February–April) when food availability is increasing. Births are tightly synchronized, with the large majority occurring in the same week within each group (groups may synchronize in different weeks). Births of Central American Squirrel Monkeys are believed to be timed so that infants are weaned during the wet season when fruit is most abundant. Tight synchrony of births is also associated with cooperative vigilance for aerial predators by all females. Vigilance increases significantly when groups have neonates and numbers of raptors accompanying monkeys increase at this time. Chestnut-mandibled toucans (Ramphastos ambiguus swainsonii), ornate hawk-eagle (Spizaetus ornatus), and collared forest-falcons (Micrastur semitorquatus) have been seen to take neonates and infants. Allocare (females other than the mother carrying the young) is uncommon, Interbirth intervals are one year. Individuals have lived more than twelve years in captivity. Activity patterns. In her studies in Corcovado National Park, Boinski found that travel time of Central American Squirrel Monkeys was small and tended to occur in early morning between 05:00 h and 06:30 h. Their day is dominated entirely by foraging. Groups move gradually through the lower canopy and understory, foraging almost constantly for animal prey and occasionally eating fruits. Foraging tends to decrease as the morning progresses (09:00–12:30 h), with an increasing proportion of the group resting from 11:00 h to 14:30 h. Stationary resting peaks at around midday. Their foraging is almost constant through mid- to late afternoon until c.18:00 h when they settle down to sleep. For two years, Boinski found that the study group used only two sleeping locations, and during more than one of those years, they used just three trees. Sleeping sites are trees with crowns nearly isolated from the surrounding canopy, evidently limiting access by predators to one or very few routes. It is possible that the few appropriate sleeping trees may be a limiting factor in home range size and even group size. In all seasons, little time is spent purely in travel (less than 3%), but Boinski found that time spent foraging changed according to food availability. In the late wet season, a time of food scarcity, an individual (aged 18 months or older) spent an average of 64% of its time searching for or eating food. At other times when food was more abundant, time spent foraging dropped to 43–47%. Boinski distinguished group activity categories as “travel forage,” “stationary forage,” “stationary, rest, and forage,” and “stationary rest.” At times of extreme food scarcity, Central American Squirrel Monkeys may spend up to 95% their day looking for food, as was found by Boinski in Costa Rica and J. D. Baldwin and J. Baldwin in their late wet season study in Panama. Foraging at this time consists almost entirely of travel forage (c.56%) and stationary forage (c.37%). Travel foraging counted for only a little less of their time in the dry season and early and middle wet seasons, but stationary foraging dropped considerably (c.16% or less). When food was more abundant, stationary, rest, and foraging took up 22–28% of the day, and stationary resting up to 10%. Time spent in activities other than foraging varied enormously: lowest during the late wet season (1·8%) and highest during the early wet season (40·5%).

391

FAMILY CEBIDAE Squirrel Monkeys and Capuchins

On following pages: 2. Humboldt’s Squirrel Monkey (Saimiri cassiquiarensis); 3. Ecuadorian Squirrel Monkey (Saimiri macrodon); 4. Golden-backed Squirrel Monkey (Saimiri ustus); 5. Guianan Squirrel Monkey (Saimiri sciureus); 6. Black-capped Squirrel Monkey (Saimiri boliviensis); 7. Black-headed Squirrel Monkey (Saimiri vanzolinii).

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Plate 24 Species Accounts

Movements, Home range and Social organization. Central American Squirrel Monkeys live in multimale–multifemale groups of 35–65 individuals. The size of the main study group of Boinski was 38–45 individuals, including ten adult males and 16 adult females. In Panama, mean group size is 18·5 individuals (range of 4–40). Males are philopatric, but females disperse before their first mating season and transfer between groups. Males do not form all-male groups as they do in Black-capped Squirrel Monkeys (S. boliviensis). Interactions between individuals in the group are marked by an almost total lack of aggression. Exceptions are in sexual contexts, during weaning, and in some cases warding off over-curious individuals trying to investigate newborn infants. Females interact very little and do not form coalitions or hierarchies as they do in the Guianan Squirrel Monkey (S. sciureus) and the Black-capped Squirrel Monkey. Direct competition for food among Central American Squirrel Monkeys is very rare; competition is avoided indirectly by maintaining distance among group members when foraging. Some degree of aggression occurs when groups of males mob a female, trying to smell her genitalia and mate with her. There is no hierarchy among males that can be perceived during such aggression, avoidance, or competition over food. Males cooperate when mobbing or chasing females. There is, however, a ranking evident during the mating season with regard to size, female choice, and successful copulations. The largest adult males show a consistently high investment in vigilance for predators and in direct interventions of possible or real threats to neonates and other group members. Depending on the season, aerial vigilance by the largest adult males takes up 3–5% of their day, two to four times more than adult females. Most reproductively successful males retrieve neonates and infants and also show aggressive defense against would be predators. The home range size of Boinski’s main study group of 38–45 Central American Squirrel Monkeys was 176 ha. Home ranges of adjacent groups overlapped, but neighboring groups very rarely met. When approaching each other, within 100–150 m, groups tended to veer off in different directions. They used some parts of the home range more than others in different seasons, and there was no evidence of a core area of use. They tended to travel further and quicker when food was scarce (350–400 m/h) and less when it was abundant (100–250 m/h). In the late wet season when food is scarce, the group was more dispersed when traveling and foraging (over 1·6 ha) than it was in the early wet season when food was more abundant (0·9 ha). This probably reflected a greater need to avoid indirect competition when food is harder to come by. The large size of the groups and the small size of squirrel monkeys make them prey to numerous raptors, mammals, and snakes, including Virginia Opposums (Didelphis virginiana), Central American Spider Monkeys (Ateles geoffroyi), Panamanian White-faced Capuchins (Cebus imitator), White-nosed Coatis (Nasua narica), Tayras (Eira barbara), collared forest falcons (Micrastur semitorquatus), Guiana crested eagles (Morphnus guianensis), and snakes such as boa constrictors (Boa constrictor) and fer-de-lance (Bothrops asper). Other predators in Costa Rica and Panama include toucans, ornate hawk-eagles (Spizaetus ornatus), gray hawks (Buteo nitidus), roadside hawks (B. magnirostris), white hawks (Leucopternis albicollis), and red-throated caracaras (Daptrius americanus). Squirrel monkeys act as “beaters” by flushing prey for double-toothed kites (Harpagus bidentatus), tawny-winged woodcreepers (Dendrocincla anabatina), and gray-headed tanagers (Eucometis pencillata). These species regularly accompany groups of squirrel monkeys throughout the year and especially during the late wet season when animal prey is most scarce. Numerous other species occasionally follow groups of squirrel monkeys for this reason. Double-toothed kites catch tentmaking bats when they are flushed by squirrel monkeys. Status and Conservation. CITES Appendix I. Classified as Vulnerable on The IUCN Red List, with both subspecies oerstedii and citrinellus classified as Endangered. The main reason for the considerable decline in numbers of the Central American Squirrel Monkey has been loss of habitat due to deforestation and tourist development; their natural shyness makes them easily stressed by tourists. Individuals rarely descend to the ground: therefore, any break in the forest (such as for roads or telephone and electric power lines) can severely fragment a group’s habitat. It is also threatened by widespread spraying of insecticides. Only a few fragmented populations remain. In 1997–1998, Boinski estimated less than 4000 Central American Squirrel Monkeys in Costa Rica, including c.1000 individuals of the Gray-crowned Central American Squirrel Monkey. Boinski indicated that they were probably extinct in Panama, but recent surveys found a fragmented population of c.4775 Black-crowned Central American Squirrel Monkeys in Chiriquí Province, spread over 2613 km2 in far western Panama. Although Corcovado National Park is 41,788 ha, it is believed to have no more than c.400 squirrel monkeys because they are restricted to areas that contain disturbed and secondary forest, which only cover c.20 km2 of the park. The Black-crowned Central American Squirrel Monkey also occurs in Golfito Wildlife Refuge (2830 ha). The Gray-crowned Central American Squirrel Monkey occurs in Manuel Antonio National Park (682 ha). Bibliography. Arauz (1993), Baldwin (1971), Baldwin & Baldwin (1972, 1976a, 1981), Boinski (1987a, 1987b, 1987c, 1987d, 1988, 1994, 1999a, 1999b), Boinski & Cropp (1999), Boinski & Mitchell (1994), Boinski & Scott (1988), Boinski & Sirot (1997), Boinski & Timm (1985), Boinski et al. (1998), Janzen (1983), Matamoros & Seal (2001), Matamoros et al. (1996), Mitchell, C.L. et al. (1991), Rodríguez-Vargas (2003), Sierra et al. (2003), Wong (1990).

2. Humboldt’s Squirrel Monkey Saimiri cassiquiarensis French: Saimiri de Humboldt / German: Humboldt-Totenkopfaffe / Spanish: Mono ardilla de Humboldt

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Other common names: Colombian Squirrel Monkey (albigena)

Taxonomy. Simia sciurea cassiquiarensis Lesson, 1840, Río (Caño) Cassiquiare, Amazonas, Venezuela. Previously considered a subspecies of S. sciureus. Following a molecular genetic study published in 2009, X. Carretero-Pinzón concluded that S. cassiquiarensis albigena

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should be considered a distinct species. Two subspecies recognized here. Subspecies and Distribution. S. c. cassiquiarensis Lesson, 1840 – Colombian Amazon (between ríos Vichada and Apaporis W to the upper ríos Guaviare and Apaporis in the Andes), S Venezuela (upper Orinoco-Cassiquiare), and the Brazilian Amazon N of the Rio Solimões (W of the Rio Negro and Rio Demini and N of the Rio Japurá). S. c. albigena von Pusch, 1942 – C Colombia, in a small area between the E slopes of the Cordillera Oriental and the Eastern Llanos, from Boyacá and Arauca departments S to the upper Río Guaviare in Meta, and the upper Río Magdalena in Huila departments to elevations of 1500 m; the E limits of the distribution in the departments of Arauca and Casanare are unknown. Descriptive notes. Head–body 25–37 cm (males) and 28–34 cm (females), tail 38– 45 cm (males) and 36–43 cm (females); weight 650–1125 g (males) and 550–1200 g (females). The nominate subspecies of Humboldt’s Squirrel Monkey is very similar in its coloration and size to the Guianan Squirrel Monkey (S. sciureus) but has a more intense tawny (golden-yellow) basal section to hairs on the crown (the Guianan Squirrel Monkey is more gray-crowned). Nominate female Humboldt’s Squirrel Monkeys have two black lines above their ears (temporal band) that extend back to the nape and forward in front of the ears (preauricular patch or sideburns). Males lack temporal bands and do not have a tuft of black hairs in front of their ears. There is a brighter reddishtan coloring on the back, and a weakly contrasting, light nuchal collar. Forearms are more orangey in the nominate subspecies of Humboldt’s Squirrel Monkey (gray in the Guianan Squirrel Monkey). The “Colombian Squirrel Monkey” (S. c. albigena) is also similar to the nominate subspecies of the Guianan Squirrel Monkey, but with mainly grayish-agouti (grizzled gray) forearms and hands, and its back is more orange-toned. The crown and nape are grayish or buffy-agouti. The white facemask of the male Colombian Squirrel Monkey extends to the ears (no sideburns), but sometimes there is a pale agouti patch in front of the ears, which are tufted. Female Colombian Squirrel Monkeys have thin dark sideburns. Habitat. The nominate subspecies of Humboldt’s Squirrel Monkey occurs in the tall humid forests of the Guiana Shield in the basins of the Rio Negro, north of the Rio Japurá in Brazil to the north in the Federal Territory of Amazonas in Venezuela and west into Colombia, north of the Apaporis (including part of Colombia’s Orinoco Region, just north of the lower and middle Río Guayabero) to the Chiribiquete Plateau. In these areas, forest canopies reach 25–30 m and are on poor soils (oligotrophic, hydromorphic laterite, and podzols, and quartz sands). Tall terra firma forests are intermixed with islands of white sand scrub and savanna (“campina”) and small-leaved and sclerophytic white sand forest (“campinarana” or caatinga forest), along with swamp forests (“chavascal”), Mauritia palm swamps, and seasonally inundated black-water forests (igapó). The Chiribiquete Plateau is characterized by sclerophytic dwarf scrub. The Colombian Squirrel Monkey occurs in the eastern Andean region of Colombia in low-canopy gallery forests of the Eastern Llanos, sclerophyllous hillside forest of the foothills of the Cordillera Oriental of the Andes, and Mauritia palm swamp forest. Food and Feeding. Colombian Squirrel Monkeys eat principally fruits and insects. They have been reported catching large caterpillars, orthopterans, and cicadas. Near San Martín in the Llanos where they have been studied, there are distinct seasons: a dry season in December–March and a wet season in April–November. Fruits are abundant only in the late dry season and early wet season (January–June), and insects are scarcer in the mid-dry season (February–March). Breeding. In the group of Humboldt’s Squirrel Monkeys studied by R. Thorington, Jr. four infants were born during 31 days in February–early March, and a fifth female gave birth in the beginning of April at the end of the dry season and early wet season. When pregnant and nursing, females were less active and spent more time in association with a group of Large-headed Capuchins (Sapajus macrocephalus). They foraged more slowly and rested more than other group members. Thorington did not observe allocare by other females, but juveniles were notably interested in infants and traveled with pregnant females. At Sierra de la Macarena National Natural Park, Colombia, births occurred in April–June. Activity patterns. Colombian Squirrel Monkeys are most active in the early to midmorning and the middle to late afternoon. At midday, they rest for 1–2 hours. In the cool early morning, they stop and rest in a huddled position, but toward the hotter middle of the day, they stretch out and sprawl. Movements, Home range and Social organization. Group sizes of Colombian Squirrel Monkeys in Sierra de la Macarena National Natural Park were 25–35 individuals. Thorington carried out a short study of the Colombian Squirrel Monkey in 1965 in a gallery forest in the Eastern Llanos, east of San Martín in the Meta Department. He observed a group of 18–22 individuals that included three adult males, five adult females, and ten 1–3-year-old juveniles. During the day, the group split into subgroups, sometimes adult males separated from females and juveniles. Subgroups reunited at midday and also at the end of the day to sleep together. Male Colombian Squirrel Monkeys disperse from their natal groups and form all-male groups. Lone males have been observed following spider monkeys (Ateles) in Sierra de la Macarena. At San Martín, Colombian Squirrel Monkeys occasionally associate with Large-headed Capuchins, and more often in August–January when insect abundance is higher than at other times. There was no effect of fruit abundance on these associations, but they were most frequent when both fruit and prey were most abundant. It is believed that associations between the two species

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are relatively infrequent compared with other species of squirrel monkeys because of the overall scarcity of, and competition for, fruit. For the nominate subspecies, average group sizes were ten (n = 3) at the clear-water creek, Caño Pintadillo, and 18 (n = 10) at Caparú on the northern margin of Lago Taraira—both sites just north of the lower black-water Río Apaporis in Colombia. Densities of squirrel monkeys at these two sites, reported by E. Palacios and C. Peres in 2005, were very low, a finding attributed to the very heavy rainfall and nutrient poor soils of the area: 0·5 groups/km2 or 5·4 ind/km2 at Caño Pintadillo and 0·2 groups/km2 or 3·1 ind/km2 at Caparú. Long-term primate studies have been conducted at Caparú, and censuses in 1984–1986 also confirmed low densities of squirrel monkeys at 8·8 ind/km2 in terra firma and 7·1 ind/km2 in igapó, with group sizes of c.15 individuals. Somewhat higher densities of 12·7 ind/km2 were recorded for Colombian Squirrel Monkeys in Tinigua National Natural Park, Colombia. T. Defler recorded Humboldt’s Squirrel Monkeys infrequently, and they were usually associated with Large-headed Capuchins and Humboldt’s Woolly Monkeys (Lagothrix lagothricha), with both in the terra firma forest but just with the woolly monkeys in the igapó. Status and Conservation. CITES Appendix II. The nominate subspecies is classified as Least Concern (as S. sciureus cassiquiarensis) and the Colombian Squirrel Monkey as Near Threatened (as S. s. albigena) on The IUCN Red List. The geographic distribution of the Colombian Squirrel Monkey is c.100,000 km2, but it has been reduced to c.60,000 km2 by the spread of oil palm plantations. Fragmentation of the gallery forests and forest patches where they occur in the Llanos has caused local extinctions, particularly over large areas in the vicinity of large towns, such as Gigante and Garzón in the northern part of their distribution. Besides oil palm plantations, major causes of forest loss and fragmentation are cattle ranching, subsistence farming, petroleum extraction and exploration, and illegal crops such as coca. Squirrel monkeys have large home ranges, and they are lost from even quite large forest fragments when they are completely isolated. Fence rows (live and wire fences, hedgerows, and trees) play a very important role as corridors between forest fragments, particularly at times of food scarcity. Populations of Colombian Squirrel Monkeys in the upper Magdalena Valley of the Huila Department are particularly threatened by habitat loss. In the 1960s and early 1970s, the Colombian Squirrel Monkey suffered from capture for sale as pets and export for biomedical research. In Colombia, a small population has been found in Cueva de los Guácharos National Natural Park, and they also occur in Tinigua and Sierra de la Macarena national natural parks in their south-western distribution. It is believed that their numbers and geographic distribution are diminishing to the extent that they should be reclassified as Vulnerable or even Endangered. The nominate subspecies occurs in Pico da Neblina and Jaú national parks, Juami-Japurá Ecological Reserve, and Amanã State Sustainable Development Reserve in Brazil; Yaigojé Apaporis and Serranía de Chiribiquete national natural parks and Nukak and Puinawai national natural reserves in Colombia; and Parima Tapirapecó, Yapacana, Duida-Marahuaca, and Serrania de la Neblina national parks in Venezuela. Bibliography. Baldwin & Baldwin (1971), Carretero-Pinzón, Defler & Ruiz-García (2008, 2010), CarreteroPinzón, Ruiz-García & Defler (2009), Defler (2003b, 2004), Hernández-Camacho & Cooper (1976), Hershkovitz (1949, 1984), Klein & Klein (1976), Lavergne et al. (2009), Palacios & Peres (2005), Thorington (1968b, 1985).

3. Ecuadorian Squirrel Monkey Saimiri macrodon French: Saimiri d’Équateur / German: Ecuador-Totenkopfaffe / Spanish: Mono ardilla ecuatoriano

Taxonomy. Saimiri macrodon Elliot, 1907, Río Copataza, upper Río Pastaza, Pastaza, Ecuador. R. Thorington, Jr. considered S. macrodon a junior synonym of S. sciureus. In a paper published in 1976, J. Hernández-Camacho and R. Cooper recognized S. sciureus caquetensis, named by J. A. Allen in 1916, from the Rio Caquetá. It was considered to be a junior synonym of S. sciureus macrodon by P. Hershkovitz and C. P. Groves. S. macrodon is chromosomally distinct, with six pairs of acrocentric chromosomes. S. macrodon intergrades with S. boliviensis peruviensis in the basins of the ríos Tapiche and Blanco, and natural hybrids of S. macrodon × S. b. peruviensis have been recorded from Pucallpa, Peru, and the Río Ucayali, in the Tapiche Basin. Monotypic. Distribution. W Brazilian Amazon (W from the rios Japurá and Juruá), extending W in S Colombia (up to the Río Apaporis), to E Ecuador (W to the Andes), and to N & E Peru, S to the Río Abujao, (N of the Río Marañón as far as the mouth of the Río Huallaga where it also extends S of the Marañón along the left (W) bank of the Rio Huallaga to about 9° S, and E of the Río Ucayali). Descriptive notes. Head–body 25–32 cm, tail 34–44 cm; weight 835–1380 g (males) and 590–1150 g (females). The Ecuadorian Squirrel Monkey is very similar to the Guianan Squirrel Monkey (S. sciureus), but the back is darker. The general color including the crown and dorsal surface of the tail is a grayish olivaceous, washed with orange. Flanks and inside of the legs and arms and ventral surface of the tail are paler. Feet and hands are deep yellowy orange. Ventral surfaces are pale yellowish white. The muzzle is black with white around the eyes and on the cheeks and throat extending to the upper chest. Ears are white, slightly furred (not tufted), and pointed. The tail pencil is black on the dorsal surface. White arches above the eyes are of the “Gothic arch” type. Habitat. Humid tropical and subtropical forest at 200–1200 m above sea level. At least in Ecuador, they are more common at elevations of 500 m or less. Ecuadorian Squirrel

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Monkeys prefer dense vegetation and lianas of seasonally inundated forests, and they are able to adapt to secondary and disturbed forest. They are reported to be scarce or absent from terra firma lowland and hillside forest far from rivers of lakes. Food and Feeding. There is no specific information available for this species, but its diet is likely composed of small animals and fruits, including infructescences of Cecropia (Urticaceae), figs (Ficus, Moraceae), Euterpe palms (Arecaceae), and Campomanesia (Myrtaceae). Breeding. There is no information available for this species. Activity patterns. There is no information available for this species. Movements, Home range and Social organization. One group of Ecuadorian Squirrel Monkeys counted at the Quebradón Ayo, a small clear-water tributary of the Río Caquetá in Colombia, had 18 individuals. The area has nutrient poor soils, low productivity, and low primate densities. Surveys of Ecuadorian Squirrel Monkeys there indicated densities of 0·6 groups/km2 and 11·3 ind/km2. They have been recorded in groups of 40–50 individuals and, like other squirrel monkeys, associate with groups of capuchins (Sapajus and Cebus). Status and Conservation. CITES Appendix II. Classified as Least Concern on The IUCN Red List (as S. sciureus macrodon). The Ecuadorian Squirrel Monkey is widespread and generally common throughout its distribution where there is suitable habitat. In some areas in Peru, it raids cornfields and banana plantations and is considered a pest. It occurs in Amacayacu, Cahuinarí, and La Paya national natural parks in Colombia; Yasuní National Park, Cayambe-Coca, and Cofán-Bermejo ecological reserves, and Cuyabeno Wildlife Reserve in Ecuador; and ACR Comunal Tamshiyacu Tahuayo in Peru. Bibliography. Aquino & Encarnación (1994b), Allen (1916), Carretero-Pinzón et al. (2009), Defler (2003b), Hernández-Camacho & Cooper (1976), Hershkovitz (1984), Lavergne et al. (2009), Schneider, Harada et al. (1993), Silva et al. (1992), Tirira (2007).

4. Golden-backed Squirrel Monkey Saimiri ustus French: Saimiri à dos brûlé / German: Nacktohr-Totenkopfaffe / Spanish: Mono ardilla orejudo Other common names: Bare-eared Squirrel Monkey, Geoffroy’s Squirrel Monkey, Short-tailed Squirrel Monkey

Taxonomy. Saimiris ustus I. Geoffroy Saint-Hilaire, 1843, Brazil, restricted by A. Cabrera in 1958 to the Rio Madeira and restricted further by P. Hershkovitz in 1984 to Humaitá, right bank of the Rio Madeira. Marginally sympatric with S. sciureus in the lower Rio Madeira Basin. S. ustus hybridizes with S. sciureus, and possibly with S. boliviensis. S. ustus has five pairs of acrocentric chromosomes and although Hershkovitz aligned this species with the “Gothic arch” squirrel monkeys (S. sciureus), cytogenetically it is very similar to the “Roman arch” S. boliviensis. Monotypic. Distribution. Brazilian Amazon S of the Rio Solimões-Amazonas in the states of Amazonas, Pará, Mato Grosso, and Rondônia, from the Rio Tefé E to the Rio Xingu-Iriri, and S to the upper Rio Guaporé and the headwaters of the Rio Juruena. Descriptive notes. Head–body 25–35 cm (males) and 23–42 cm (females), tail 40– 45 cm (males) and 31–42 cm (females); weight 710–1200 g (males) and 620–880 g (females). The Golden-backed Squirrel Monkey is similar to the Guianan Squirrel Monkey (S. sciureus), but it is generally larger, with a shorter tail. The back is gold colored, the crown is agouti (intermixed or bordered with black in females), outer sides of thighs are grayish-agouti, and forearms, hands, and feet are orange or yellowish. The face is naked, the ears are only moderately hairy, without tufts, and arches above the eyes are of the Gothic arch type. There is some slight geographic variation in appearance; southerly Golden-backed Squirrel Monkeys have bright orange forearms, whereas over most of their distribution, this color does not extend above the wrists. Those from the lower Rio Tapajós have a yellowish crown and forearms. Habitat. Lowland evergreen rainforest, including terra firma forest, seasonally inundated forest, and swamp forest. Surveys at Urucu, in the Purus Basin, by C. Peres mainly recorded Golden-backed Squirrel Monkeys in the 100–200-m wide, black-water inundated forest (igapó) along river and creek-side forests. When fruit is scarce in the dry season, they become widely vagrant in the terra firma forest. Food and Feeding. There is no specific information available for this species, but as is typical of all squirrel monkeys, the diet is undoubtedly composed of fruit and small animal prey, particularly orthopterans and lepidopteran caterpillars and pupae. Breeding. There is no information available for this species. Activity patterns. The Golden-backed Squirrel Monkey is diurnal and arboreal. Although it has not been studied in the wild, a large part of its day likely involves moving and foraging in the lower canopy and understory of the forest, searching foliage for small animal prey. Movements, Home range and Social organization. There is little specific information available for this species, but at Urucu, Peres counted two groups, one of 38 individuals and the other of 76 individuals. Densities were estimated at 0·2 groups/km2 and 10·2 ind/km2. Status and Conservation. CITES Appendix II. Classified as Near Threatened on The IUCN Red List. Very little is known about the Golden-backed Squirrel Monkey in the wild, but its distribution coincides with the so-called arc of deforestation along the agricultural frontier in the south of the states of Pará, Mato Grosso and Rondônia, where forests have been clear-cut during the last 20 years for colonization, timber,

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cattle ranching, and industrial agriculture (notably soy beans). In Brazil, it probably occurs in Amazônia, Juruena, and Pacaás Novos national parks; Abufari, Guaporé and Jarú biological reserves; and Cuniã, Iquê, and Samuel ecological stations. Bibliography. Ayres (1985), Cabrera (1957), Carretero-Pinzón et al. (2009), Groves (2001), Hershkovitz (1984), Peres (1993a, 1994b).

5. Guianan Squirrel Monkey Saimiri sciureus French: Saimiri écureuil / German: Guayana-Totenkopfaffe / Spanish: Mono ardilla común

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Other common names: Common Squirrel Monkey; Collins’s Squirrel Monkey (collinsi)

Taxonomy. Simia sciurea Linnaeus, 1758, “India.” Restricted by Tate in 1939 to Guyana, Kartabo. S. sciureus has seven pairs of acrocentric chromosomes. S. s. collinsi was recognized by A. Cabrera in his catalogue of primates in 1958 and W. C. O. Hill in his review of the Cebidae in 1960. Modern revisions of squirrel monkey taxonomy by P. Hershkovitz, R. Thorington, Jr. in 1985, and C. P. Groves in 2001, however, listed it as a junior synonym of the nominate subspecies sciureus. Independent molecular genetic studies by A. Lavergne and coworkers and X. Carretero-Pinzón and coworkers (both in 2009) found collinsi to be distinct. There is some hybridization with S. ustus in the maze of channels and flooded forests between the rios Madeira and Purus, just south of the Amazon River. Two subspecies recognized. Subspecies and Distribution. S. s. sciureus Linnaeus, 1758 – Guianas and N Brazil, N of the Amazon River from the rios Negro and Demini (Amazonas State), E to the river mouth, and S of the Amazon River between the Rio Xingu-Iriri (Pará State) E to the Rio Pindaré (Maranhão State), extending S to c.6° S along the upper reaches of the Rio Xingu. S. s. collinsi Osgood, 1916 – N Brazil, Marajó I in the estuary of the Amazon River (Pará State), but further studies are needed to identify the extent of its occurrence, which may well be much larger; the identity of the squirrel monkeys on other islands in the Amazon estuary (Gurupá, Caviana, and Mexiana) has yet to be ascertained. Descriptive notes. Head–body 25–37 cm (males) and 25–34 cm (females), tail 36– 40 cm (males) and 36–47 cm (females); weight 550–1400 g (males) and 550–1200 g (females). The adult male type specimen of “Collins’s Squirrel Monkey” (S. s. collinsi): head–body 24·9 cm and tail 41·1 cm. The Guianan Squirrel Monkey is generally grayish or greenish to reddish-agouti, with an agouti-colored crown. White arches over the eyes are high and pointed in the “Gothic arch” style, and there are white ear tufts. The face is pink, with black around the muzzle. The nominate subspecies sciureus is buffy-agouti with yellowish-orange forearms, hands, and feet, and a white underside. The crown is gray-agouti in the male and intermixed or bordered with black in the female. Individuals south of the Amazon River are slightly yellower on the back and have a more yellowish suffusion on the crown. There is no defined nuchal band. Collins’s Squirrel Monkey is similar to the nominate subspecies, but its hands and feet are a dark rich tawny compared with the golden yellow or orange of the nominate subspecies. White around the ears is not (or only narrowly) continuous with white around the eyes. The back is paler than in the nominate subspecies, and the head, shoulders, and forepart of the back are grayish. Habitat. Mature forest and early and late successional stages of secondary lowland rainforest, seasonally inundated forest, river edge and gallery forest, and mangrove and swamp forest. Food and Feeding. A. Stone studied the feeding ecology of two groups of Guianan Squirrel Monkeys at Ananim, east of Belém, in the Pará State, Brazil. Their diets were principally insects, fruit, flowers, nectar, seeds, gums, spiders, lizards, and bird eggs. Insects accounted for 79–82% of their feeding and foraging times during the year. Insects contributed more to the diet in the dry season: 72–74% of the time spent feeding and foraging in the dry season compared to 50–51% in the wet season. In one year, squirrel monkeys ate fruits from 68 species and 37 families. The fleshy, yellow mesocarp of fruits of the palm Maximiliana (= Attalea) maripa (Arecaceae) was preferred, comprising an average of 28% of their feeding time and ranking first or second in the diet for nine months of the year. These palms grow in clusters, each having one to four bunches of several hundred to over one thousand fruits, which allows an entire group to feed simultaneously. In the wet season, flowers contributed only 1·7% of the plant diet, but they rose to 28·5% of the diet in the dry season when fruits were scarce. The two most important species providing flowers were the liana Memora magnifica (Bignoniaceae) and the vine Passiflora glandulosa (Passifloraceae). Nectar was eaten in the dry season, and they also ate gum and small (less than 4 mm) seeds of Stryphnodendron pulcherrimum (Fabaceae), which in one month comprised 39% of the plant feeding records. Of the insect prey recorded, 51% were orthopterans, but caterpillars and Hymenoptera were important in the wet season. In the dry season, Guianan Squirrel Monkeys frequently foraged in leaf litter (32% of insect foraging records) for large orthopterans and hemipterans, but only rarely in the wet season (2% of records). Another study of their diet was carried out by E. Lima and S. Ferrari in Gunma Ecological Park, also in the south of Pará. The study monitored the diet of a group of Guianan Squirrel Monkeys in lowland terra firma forest through the dry season (August–November) to the onset of the wet season (December–January). In contrast to the findings of Stone, the diet changed markedly during the study. Animal prey (mostly orthopterans and

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lepidopterans) accounted for 80% of the feeding records in August, while plant material (mostly fruit) accounted for 20%. These proportions gradually changed as the dry season progressed, with less animal prey and more fruit until January, in the early wet season, when animal prey comprised 20% of the diet and fruit 80%. Foraging success for animal prey declined progressively through the study, while numbers of trees in fruit gradually increased. Overall, they ate fruit from 21 species, nectar from Symphonia globulifera (Clusiaceae), and inflorescences of Cecropia (Urticaceae). Almost one-half of fruits eaten came from species of Fabaceae and Sapotacae. The Guianan Squirrel Monkey has been seen eating a bat only once, so it evidently does not hunt for them systematically as does the Central American Squirrel Monkey (S. oerstedii). Breeding. Breeding of the Guianan Squirrel Monkey is seasonal and normally synchronous in the group. Prior to the mating season, adult males become considerably fatter on the upper parts of their bodies, and they are much more vocal and aggressive. The mating season lasts about nine weeks in the early dry season. Unlike the Central American Squirrel Monkey, female Guianan Squirrel Monkeys apparently do not present sexually to males, nor do they follow or call to them. After a gestation of five months, births are highly synchronized among group members (all in less than one week) over two months (January–February) in the early wet season. The single large offspring is cared for by the mother and other adult females (allocare or alloparenting) that carry infants for short periods. The father shows no paternal care. The infant’s tail is slightly prehensile. Infants are weaned by about six months. Females are sexually mature at c.2·5 years and have their first infants about one year later. Males go through a subadult phase before entering true adulthood at 4–5 years old. Interbirth intervals are 1–2 years. Guianan Squirrel Monkeys can live 20 years or more. Activity patterns. A study of two groups of Guianan Squirrel Monkeys in eastern Brazil found that, on average, 51–53% of their days is spent foraging for, processing, and eating food during the year. In another study, activity budgets were slightly different between seasons. In the dry season, individuals foraged more for insects (c.31% vs. c.25%), spent more time eating (c.23% vs. c.15%), and less time resting (c.17·5% vs. c.27%) and occupied in social behavior (c.5% vs. c.8%) than in the wet season. Time spent traveling (c.22% of the day) was similar between seasons. Movements, Home range and Social organization. The two groups of Guianan Squirrel Monkeys studied by Stone at Ananim had 44 and 50 individuals. During one year, their home ranges were 110 ha and 123 ha, with little seasonal differences in home range use. Daily movements were more than 2 km, averaging 2347 m during 57 days for one group and 2290 m during 20 days for the other. Groups are multimale–multifemale, with each sex forming dominance hierarchies; males are typically larger and most or all are dominant over females. Male Guianan Squirrel Monkeys form coalitions. Groups studied in Suriname have frequent agonistic interactions, and commonly over fruits (1·5 interactions/hour). Males in the groups studied in Brazil were much less aggressive. Aggression between females is infrequent, and they do not form coalitions. Females disperse and males are philopatric. Groups of Collins’s Squirrel Monkey in gallery forest along the Rio Jutuba in the savanna of the eastern part of the island of Marajó were smaller (average 10 ind/group) than in extensive forest lowland terra firma forest. This is similar to the “Colombian Squirrel Monkey” (S. cassiquiarensis albigena) in gallery forest of the Eastern Llanos in Colombia, which also has smaller groups, perhaps an adaptation to the occupation of restricted linear habitats. Densities of Collins’s Squirrel Monkey have been estimated at 5·2 groups/km2 and 54·2 ind/km2. Status and Conservation. CITES Appendix II. Classified as Least Concern on The IUCN Red List. Collins’s Squirrel Monkey is not evaluated separately. The Guianan Squirrel Monkey is widespread and common, although it was extensively exploited in the past by the laboratory-animal and pet trades. It is rarely hunted. It occurs in numerous and many large protected areas within its distribution. Bibliography. Boinski (1999a, 1999b), Boinski & Cropp (1999), Carretero-Pinzón et al. (2009), Fernandes et al. (1995), Groves (2001), Hershkovitz (1984), Hill (1960), Jones et al. (1973), Lavergne et al. (2009), Lima & Ferrari (2003), Peres (1989c), Podolsky (1990), de Souza et al. (1997), Stone (2007), Tate (1939), Thorington (1968b, 1985).

6. Black-capped Squirrel Monkey Saimiri boliviensis French: Saimiri de Bolivie / German: Schwarzkappen-Totenkopfaffe / Spanish: Mono ardilla boliviano Other common names: Bolivian Squirrel Monkey (boliviensis), Peruvian Squirrel Monkey (peruviensis)

Taxonomy. Callithrix boliviensis I. Geoffroy Saint-Hilaire & de Blainville, 1834, Guarayos Mission, Río San Miguel, Santa Cruz, Bolivia. In a review of the taxonomy of the uacaris published in 1987, P. Hershkovitz recognized S. b. jaburuensis and S. b. pluvialis as valid subspecies. They were listed by C. P. Groves in 2001 as synonyms of the nominate subspecies boliviensis. This species may hybridize with S. ustus where the two are sympatric. S. boliviensis is chromosomally distinct, with five pairs of acrocentric chromosomes. Natural hybrids of S. b. peruviensis × S. macrodon have been recorded from Pucallpa, Peru, and the Río Ucayali (Tapiche Basin). Two subspecies recognized. Subspecies and Distribution. S. b. boliviensis I. Geoffroy Saint-Hilaire & de Blainville, 1834 – upper Brazilian Amazon S of the Rio Solimões, from between the rios Juruá and Tefé extending S into SE Peru

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Plate 24 Species Accounts

(S of Río Abujao, Ucayali Department) and N Bolivia W of the Río Guaporé (Beni, Cochabamba, Pando, and Santa Cruz departments, including the upper Madeira Basin), at elevations of 50–500 m. S. b. peruviensis Hershkovitz, 1984 – N & C Peru, S of the Río Marañón-Amazonas, from the W bank of the Río Tapiche W to the Río Huallaga, and S through the departments of San Martín and of Huánuco (to c.10° S), and Ucayali (between the ríos Pachitea and Tambo, at least as far as the Río Abujao); also possibly in Brazil (Amazonas State), at elevations of 90–800 m. Descriptive notes. Head–body 28–31·5 cm (males) and 26·5–28·5 cm (females), tail 38–43 cm (males) and 39·5–41 cm (females); weight c.1 kg (males, varies by season) and 700–900 g (females) for the “Bolivian Squirrel Monkey” (S. b. boliviensis). Head–body 27·3–32 cm (males) and 26·5–27·7 cm (females), tail 37·4–43·5 cm (males) and 37·7–40·4 cm (females) for the “Peruvian Squirrel Monkey” (S. b. peruviensis). The Black-capped Squirrel Monkey is sexually dichromatic. Males tend to be gray and females blackish, although normally both have a blackish crown and golden-yellow forearms, hands, and feet. There are narrow white lines of fur on each brow of the “Roman arch” type. The tail pencil is black and thin. The principal distinguishing character of the Bolivian Squirrel Monkey is the entirely agouti pelage of the forehead. The crown and preauricular patch are blackish in both sexes. The tail is grayish or buffy-agouti to blackish above, with a black tip. In the Peruvian Squirrel Monkey, the crown and preauricular patch are agouti in males and mainly black or blackish-agouti in females. The tail is grayish to blackish-agouti above, with a black tip. Habitat. All types of humid forest in the western Amazon, from river edge and seasonally flooded forests to terra firma forest. Black-capped Squirrel Monkeys tend to use terra firma forest only seasonally, depending on fruit abundance and dispersion. Their preference is for river edge, lacustrine succession, and flooded forests. Although Black-capped Squirrel Monkeys often feed on fruits in large-canopied, tall trees (especially Ficus and Brosimum, both Moraceae) in the upper canopy and even emergent vegetation, they travel mainly in the middle canopy and understory, 10–15 m above the ground. Food and Feeding. Diet of the Black-capped Squirrel Monkey is largely small animal prey and fruit. Its feeding ecology was studied by J. Terborgh and colleagues at Cocha Cashu in Manu National Park and Biosphere Reserve, Peru. Fruits they eat are generally small (mostly 1 cm or less in diameter or the short axis), succulent, and sweet, including berries and drupes that are often yellow or orange when ripe. The diet includes fruits from more than 150 species in 42 families. In the wet season, various fruits comprise 100% of the plant part of their diet. In the dry season, when fruit production in the forest is generally low, Black-capped Squirrel Monkeys are able to maintain a high a percentage of fruit (91%) in their diet by concentrating on figs; there are 16 species of Ficus (Moraceae) at Cocha Cashu, 13 of them providing fruits for squirrel monkeys. The three most important species are F. perforata, F. killipii, and F. erythrosticta. In May during the early dry season, for example, Blackcapped Squirrel Monkeys spent 90% of their fruit feeding time on figs, which equaled 77% of their time spent feeding overall. In the dry season, they also lick nectar from flowers of Combretum assimile (Combretaceae) and Quararibea cordata (Bombacaceae). Large-canopied figs produce enormous quantities of small fruits, attracting a wide range of birds and mammals for periods of c.10 days. Tall trees (up to 30–40 m) are sparsely distributed through the forest, and Black-capped Squirrel Monkeys, like the sympatric Shock-headed Capuchins (Cebus cuscinus) that also depend on figs in the dry season, range widely (450 ha). Because of their heavy use of figs, in which the entire group can feed simultaneously, Black-capped Squirrel Monkeys spend c.50% of their feeding time in the canopy or emergent vegetation at heights of 30 m or more. Black-capped Squirrel Monkeys at Manu and Central American Squirrel Monkeys (S. oerstedii) differ in their use of the small-canopied trees they exploit for fruits. Central American Squirrel Monkeys exploit species that produce fruits in small quantities over long periods. Black-capped Squirrel Monkeys at Manu eat a much larger diversity of fruits, which typically produce large crops that ripen over a short period or even simultaneously, in both large- and small-canopied trees. As a result, sizes of feeding parties differ: typically, 3–4 Central American Squirrel Monkeys and 17–18 Black-capped Squirrel Monkeys. As for all squirrel monkeys, Black-capped Squirrel Monkeys are efficient, rapid foliage gleaners; 83% of their foraging time is spent scanning and manipulating leaves of trees and vines for exposed rather than hidden prey. About one-half of all prey they take is immobile or sluggish that they grab from leaves, and c.30% are mobile insects that they snatch, even in mid-air, or pounce on. Orthopterans comprise c.33% of their prey, and c.50% are lepidopteran larvae, pupae, and adults. They also eat hymenopteran larva, galls, beetles, snails, frogs, lizards, nestlings, and numerous other small items that are impossible to identify. Black-capped Squirrel Monkeys are the most intense and rapid foragers, catching prey at a faster rate than any of the primates at Cocha Cashu. They capture prey at twice the rate of sympatric capuchin species, nearly one item per minute. When insects are scarce, particularly toward the end of the dry season, they increase their search rate and are thus able to maintain capture rates of 53–64 captures/hour during the year. Most of their foraging for animal prey is done while moving slowly through the understory and lower canopy at heights of 5–10 m. Breeding. As many as 23 breeding females can occur in a single group of Black-capped Squirrel Monkeys. Females give birth for the first time at c.2·5 years of age. Males reach reproductive maturity at about six years. As in other species of Saimiri, male Black-capped Squirrel Monkeys become “fatted” prior to the mating season, which lasts about two months. Births occur also during a two-month period, in contrast to the tight synchrony of two weeks in the Central American Squirrel Monkey and less

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than one week in the Guianan Squirrel Monkey (S. sciureus). Females other than the mother care for infants and may suckle them. Interbirth interval is 24 months, double those of Guianan and Central American squirrel monkeys. Activity patterns. Black-capped Squirrel Monkeys spend most of their day traveling through the understory searching for animal prey, finding occasional fruits from relatively small-canopied understory trees (5 m or less in diameter), and making short but frantic excursions up into the canopy to raid the large fruits of fig trees. At these times, the entire group may feed on fruits together. About 11% of the day is spent feeding on fruit or nectar, and another 11% resting. About 43% of their fruit feeding time is spent in large trees with canopies of 20 m or more. Movements, Home range and Social organization. Group sizes of Black-capped Squirrel Monkey at Manu National Park and Biosphere Reserve are 35–65 individuals, and home ranges are 250–500 ha. Home ranges of different groups overlap, and there is no evident territorial behavior. Groups have been seen feeding on fruits in a large fig tree one after the other or even at the same time in neighboring Brosimum trees. There is, however, competition for food within groups. Food-based disputes are 70 times more frequent in groups of Black-capped Squirrel Monkeys (although still not very frequent) than they are in egalitarian and peaceful groups of the Central American Squirrel Monkeys where such aggressive interactions occur 0·3 times/hour. Only twelve aggressive interactions (all disputes over animal prey) were recorded in more than 3000 observations of Central American Squirrel Monkeys. In c.23% of encounters (95% disputing fruit in fruiting trees), Black-capped Squirrel Monkey females interacted in coalitions; female Central American Squirrel Monkeys do not form coalitions. Female Black-capped Squirrel Monkeys stay in their natal group and, as adults, establish dominance hierarchies and develop alliances in kin-based coalitions. Male–male aggression is also common, and males also form coalitions. Males play no particular role in group vigilance and do not defend group members from predators. They disperse from their natal groups at 4–5 years of age and form allmale groups before attempting to join a mixed-sex group. Male coalitions are known to transfer between groups every 2–3 years. Females are dominant to males and keep them on the periphery of the group except during the mating season. Black-capped Squirrel Monkeys regularly travel with Large-headed Capuchins (Sapajus macrocephalus). The capuchin monkeys are usually the leaders, and it is believed that they help squirrel monkeys locate large crops of fruits such as figs. In a two-month study at Cocha Cashu, a group of 40–50 Black-capped Squirrel Monkeys associated with capuchin groups for c.63% of their time, with distances of 50 m or less between groups. Capuchin groups are smaller (8–12 individuals) and have smaller home ranges (c.80 ha), so squirrel monkeys with larger home ranges associate with up to five different capuchin groups. Association with any particular capuchin group generally lasts about five days, but sometimes they travel together for up to twelve days. When in association with capuchins, squirrel monkeys eat more fruit and nectar and spend less time foraging for animal prey. Capuchins are larger but are outnumbered by the squirrel monkeys. Squirrel monkeys benefit from being led to large fruit crops, which capuchin monkeys are unable to monopolize, but there is a cost. Capuchins are able to monopolize medium-sized and smaller crops, which they locate with the help of the squirrel monkeys. Capuchins travel higher in the forest using more vines and palms where they forage for insects. Foliage gleaning squirrel monkeys, on the other hand, travel and forage more through small and medium-sized trees where they are more likely to discover small to middle-sized fruit crops, which can then be taken over by capuchins. Competition means that both capuchins and squirrel monkeys eat faster when they are traveling together. Capuchins can also dominate insect infestations, such as caterpillar swarms, to the detriment of squirrel monkeys. On the plus side, squirrel monkeys occasionally benefit by gaining access to otherwise inaccessible mesocarp of discarded and dropped Scheelea palm fruits during and following feeding bouts by capuchins. The ornate hawk-eagle (Spizaetus ornatus) and the Ocelot (Leopardus pardalis) are confirmed predators of Black-capped Squirrel Monkeys, and the harpy eagle (Harpia harpyja) and the black-and-white hawk-eagle (Spizaetus melanoleucus) have also been seen to attack them. C. Peres compared densities in terra firma and seasonally flooded (várzea) forests along the Rio Juruá. At two várzea sites in the Brazilian Amazon, he obtained densities of 70·7 ind/km2 (Sacado do Condor) and 149·2 ind/km2 (Boa Esperança), and at six terra firma forest sites, also in the Brazilian Amazon, densities were considerably lower: 11·3 ind/km2 (Porongaba), 36·4 ind/km2 (Kaxinawá reserve), 25·4 ind/km2 (Penedo), 28·7 ind/km2 (Altamira), 7·7 ind/km2 (Igarapé do Jaraqui), and 13·5 ind/km2 (Vai Quem Quer). Density in Manu National Park and Biosphere Reserve, Peru was 50 ind/km2 in a forest of lacustrine succession (around Cocha Cashu). Status and Conservation. CITES Appendix II. Classified as Least Concern on The IUCN Red List, including both subspecies. The Bolivian Squirrel Monkey occurs in Amboró, Isiboro Securé, Carrasco, and Madidi national parks, Manuripi-Heath and Ríos Blanco y Negro national reserves, and Beni and Pilón Lajas biosphere reserves in Bolivia; and Serra do Divisor National Park, Rio Acre Ecological Station, and possibly Abufari Biological Reserve in Brazil. In Peru, it occurs in Manu National Park and Biosphere Reserve, Yanachaga-Chemillén National Park, and possibly Bahuaja-Sonene National Park and Tambopata National Reserve. The Peruvian Squirrel Monkey occurs in Pacaya-Samiria National Reserve in Peru. Bibliography. Aquino & Encarnación (1994b), Boinski (1999a, 1999b), Groves (2001), Hershkovitz (1984, 1987c), Jones et al. (1973), Martinez et al. (2010), Mendoza, Lowe & Levine (1978), Mitchell, C.L. (1991, 1994), Mitchell , C.L. et al. (1991), Schneider, Harada et al. (1993), Silva, Sampaio, Schneider, Schneider, Montoya, Encarnación, Callegari-Jacques & Salzano (1993), Silva, Sampaio, Schneider, Schneider, Montoya,

395

FAMILY CEBIDAE Squirrel Monkeys and Capuchins

Encarnación & Salzano (1992), Terborgh (1983, 1985), Williams, Gibson et al. (1994), Williams, Vitulli et al. (1986).

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FAMILY CEBIDAE Squirrel Monkeys and Capuchins

Plate 24 Species Accounts

7. Black-headed Squirrel Monkey Saimiri vanzolinii French: Saimiri noir / German: Dunkler Totenkopfaffe / Spanish: Mono ardilla de Vanzolini Other common names: Black Squirrel Monkey, Vanzolini’s Squirrel Monkey

Bibliography. Ayres (1985, 1993), Groves (2001), Paim (2008), Paim & Queiroz (2007, 2009).

396

Taxonomy. Saimiri vanzolinii Ayres, 1985, left (north) bank of Lago Mamirauá, at the mouth of the Rio Japurá, Amazonas, Brazil (2° 59’ S, 64° 55’ W). Of the S. boliviensis group, P. Hershkovitz placed S. vanzolinii as a subspecies of S. boliviensis. S. c. cassiquiarensis, otherwise restricted to the left bank of the Rio Japurá, occurs on the right bank in two localities. One is to the north of the Paraná do Jarauá, and the other is in the vicinity of the Paraná do Apara and Paraná do Mamirauá where in a small locality, it is syntopic with S. vanzolinii, forming seven known mixed groups. Monotypic. Distribution. Brazilian Amazon N of the Rio Solimões, only known from a small triangle of land in the Mamirauá Sustainable Development Reserve, between the Paraná do Jarauá and the Paraná do Aiucá in the W (the Ecuadorian Squirrel Monkey, S. macrodon, occurs W of the Paraná do Aiucá) and the Rio Japurá to the E, and also the Capucho (= Uanacá) and Tarará (= Pananim) Is downstream from the Mamirauá Sustainable Development Reserve; it does not occur on the island formed by the Paraná do Cauaçu and the Rio Solimões in the WC part of its distribution. Descriptive notes. Head–body 26–30 cm (males) and 22–26 cm (females), tail 35– 40 cm (males) and 37–41 cm (females); weight c.950 g (males) and c.650 g (females). Male and female Black-headed Squirrel Monkeys are similar in appearance, both being somewhat small with short dense pelage and a black crown. The dorsum is quite dark, forming a broad continuous black band from the crown to tail tip. Hands, forearms, and feet are light “burnt yellow,” and shoulders are grayish. Arches over the eyes are of the “Roman arch” type, as in the Black-capped Squirrel Monkey (S. boliviensis). Habitat. Young and low white-water flooded forest (várzea) inundated to heights of 11–12 m for about six months each year. There are two types of vegetation that the Black-headed Squirrel Monkey uses: várzeas on the higher ground (levees) and “chavascal” on the swamps behind the levees. Chavascal is gradually being silted over in the lower ground between the levees. The ground is swampy, muddy, and poorly aerated, and vegetation is low and shrubby and inundated for 6–8 months of the year at depths of 6–7 m. Characteristic trees include Cecropia (Urticaceae), Bambusa (Poaceae), Ficus (Moraceae), Bombax munguba (Bombacaceae), Piranhea trifoliata (Euphorbiaceae), Myrcia (Myrtaceae), and dense stands of palms Astrocaryum jauari (Arecaceae). Várzeas have soils that are coarser and better aerated. They are subdivided into high várzea (flooded 2–4 months at depths of 1–2·5 m) with larger trunked and taller trees and low várzea (flooded 4–6 months at depths of up to 5 m) transitioning to chavascal. Characteristic trees include Brosimum lactescens (Moraceae), Franchetella (Sapotaceae), Eschweilera turbinata (Lecythidaceae), Euterpe (Arecaceae), Ceiba pentandra (Bombacaceae), and Hevea spruceana (Euphorbiaceae). Black-headed Squirrel Monkeys spend most of their time in chavascal in both dry and wet seasons, but they enter várzeas when certain trees are in fruit. Curiously, neighboring species, the Ecuadorian Squirrel Monkey (S. macrodon) and the nominate subspecies of Humboldt’s Squirrel

Monkey (S. c. cassiquiarensis) occupy similar flooded forests in the region but prefer low várzea on higher ground, indicating divergence of habitat preferences from the Black-headed Squirrel Monkey. Food and Feeding. Diets of the Black-headed Squirrel Monkey are generally composed of insects supplemented with fruits. Species with small soft fruits typically eaten include Ficus pertusa (Moraceae), Xylopia frutescens (Annonaceae), Brosimum lactescens (Moraceae), Inga (Fabaceae), Franchetella and Chrysophyllum auratum (both Sapotaceae), Gustavia hexapetala (Lecythidaceae), and the liana Paullinia pinnata (Sapindaceae). Fruits are most abundant in várzea in the wet season (January–April). They also lick nectar from flowers of Eschweilera turbinata (Lecythidaceae) in the middle of the dry season (October). Breeding. “Fatted” male Black-headed Squirrel Monkeys are seen in groups in July in the early dry season, and infants are born in February–March in the middle of the wet season when fruits are most abundant. Activity patterns. The Black-headed Squirrel Monkey is diurnal and arboreal. In the morning, groups split into three or more subgroups (feeding parties) to feed on fruits. At midday, they regroup and spend more time foraging for insects and other small animal prey in the afternoon. Várzeas of the lower Japurá have a lower diversity of trees than is found in the terra firma forest, but they are widely dispersed and found in small patches that are insufficient for simultaneous feeding by the entire group. Black-headed Squirrel Monkeys forage for animal prey largely in the lower canopy and understory, but they venture onto the forest floor in the dry season. Movements, Home range and Social organization. The Black-headed Squirrel Monkey lives in large multimale–multifemale groups of 20–50 individuals. Surveys carried out in 2005–2007 indicated average group sizes of c.26 individuals in the dry season and 21 individuals in the wet season. Densities are 57·8–109·4 ind/km2. Home ranges are 50– 100 ha. Black-headed Squirrel Monkeys form mixed-species groups with Large-headed Capuchins (Sapajus macrocephalus). They are also frequently seen with Colombian Red Howlers (Alouatta seniculus) and sometimes feed alongside the Bald Uacari (Cacajao calvus) in fruiting Ficus and Brosimum. In July–August, they travel with the large flocks of 150 or more greater ani (Crotophaga major), presumably benefitting from prey that is flushed by the birds. A comparative study of their alarm calls (cackles) showed that there was a significant difference in the maximum frequency of the call notes compared with those of its neighbors. The nominate subspecies of Humboldt’s Squirrel Monkey has the lowest median maximum frequency, followed by the Ecuadorian Squirrel Monkey, and the Black-headed Squirrel Monkey produces alarm calls with the highest maximum frequency. Status and Conservation. CITES Appendix II. Classified as Vulnerable on The IUCN Red List. At about 870 km2, the geographic distribution of the Black-headed Squirrel Monkey is the smallest of all squirrel monkeys, which is the chief conservation concern. Current estimates indicate a minimum population of 5500–10,900 individuals. There is some logging in the area but not apparently for trees that are important food sources for the Black-headed Squirrel Monkey. There has been some consternation regarding the possibility of hybrids and a progressive invasion of its natural distribution, particularly by the nominate subspecies of Humboldt’s Squirrel Monkey, but the situation regarding this is still unclear. Besides the two small islands of Capucho and Tarará, the entire distribution of the Black-headed Squirrel Monkey is within Mamirauá Sustainable Development Reserve.

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Plate 25

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typical form

southern form

PLATE 25 inches

13 14

ssp apella

ssp margaritae

Colombian morph

Peruvian morph

Bolivian morph

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Brazilian morph

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Plate 25 Species Accounts

Subfamily CEBINAE Genus SAPAJUS Kerr, 1792

8. Black-horned Capuchin Sapajus nigritus French: Sapajou noir / German: Schwarzer Kapuzineraffe / Spanish: Capuchino negro Other common names: Black Capuchin, Crested Black Capuchin, Horned Capuchin

Taxonomy. Cercopithecus nigritus Goldfuss, 1809, Serra dos Orgãos, Rio de Janeiro, Brazil. C. P. Groves in 2001 recognized the southernmost (darkest) populations of S. nigritus as a separate subspecies, Cebus nigritus cucullatus, named by Spix in 1823. Its geographic distribution is poorly known, but it is probably a distinct taxon. Monotypic. Distribution. NE Argentina (Misiones Province) and SE Brazil, S of the Rio Doce and the Rio Grande (E bank affluent of the Rio Paraná) in the states of Minas Gerais and Espírito Santo, extending S through the Atlantic Forest, E of the Rio Paraná into the N part of Rio Grande do Sul State, to c.29° 50’ S. The most S occurring of all capuchins. Descriptive notes. Head–body 42–56 cm (males) and 42–48 cm (females), tail 43– 56 cm (males); weight 2·6–4·8 kg. The Black-horned Capuchin is a large species, characterized by horn-like tufts of fur on either side of the head at the temples. It is a very dark brown or grayish to black in the most southerly populations, often with reddish or yellow-fawn underparts. A dark crown contrasts greatly with the light colored face, and crown tufts are well developed in adults. The tail is black. Habitat. Lowland, submontane, montane tropical, subtropical forest, gallery, and secondary forest. The Black-horned Capuchin was studied by M. Di Bitetti and colleagues in the humid subtropical forest of Iguazú National Park, Argentina, where annual rainfall is 1900–2100 mm but with no marked seasonality. Abundances of fruits and insects are seasonal, however, following day length and temperature—lowest in the winter months of June–August and highest in October–January. In Iguazú, Blackhorned Capuchins are found in secondary forests and tall forest with abundant rosewood (Aspidosperma polyneuron, Apocynaceae) and palms (Euterpe edulis, Arecaceae). P. Izar and colleagues studied two groups in submontane and montane semi-deciduous forests of Carlos Botelho State Park in São Paulo State, Brazil, and studies of their ecology, demography, and reproduction were conducted by J. W. Lynch and J. Rímoli in a seasonal, semi-deciduous forest patch of c.1000 ha at Caratinga Biological Station in Minas Gerais State, Brazil. Food and Feeding. Diet of the Black-horned Capuchin contains fruits, seeds, leaves, roots, and animal prey (including insects and small vertebrates). In Iguazú National Park, fruits and arthropods are scarce in winter (May–August), and key food sources at this time include palm fruits Syagrus (= Arecastrum) romanzoffiana, important when other fruits are scarce in February–June, figs (Ficus, Moraceae), fruits of the vine Pereskia aculeata (Cactaceae), shoots of the bamboo Chusquea ramosissima (Poaceae), meristems and leaf bases of epiphytes such as orchids, bromeliads, and Philodendron (Araceae), and cultivated trees including Citrus and the oriental raisin tree Hovenia dulcis (Rhamnaceae). They pick tangerines and put their heads up and back, squeezing the fruit to drink the juice. At Carlos Botelho State Park, principal items in the diet are fruit (average 35%), invertebrate prey (22%), and leaves, especially leaf bases of bromeliads and pith of palm leaf stems (rachis) (36%). Leaves dominate diets in the dry season in the northern part of its distribution. Breeding. Although mating of the Black-horned Capuchin occurs throughout the year (even when they are pregnant and lactating), births occur only in the early and mid-wet season (October–February) when fruit and insect availabilities are at their highest. Females have fertile ovulatory cycles only during a short period in the early dry season when there is an increase in the number of adult females showing proceptive sexual behavior. Females begin cycling in February–March, and few females are still cycling by August. Conception usually occurs after 2–5 ovarian cycles in late autumn or winter when food availability is lowest and day length shortest. At this time, testosterone levels of alpha and subordinate males increase, although there is generally no overt competition among them for the females’ attentions. Adult males are not aggressive toward females as they are in species of Cebus. Female Black-horned Capuchins solicit mating, usually from the alpha male, with an elaborate courtship. The female’s proceptive phase lasts c.4–6 days at intervals of 14–21 days, probably reflecting the ovarian cycle. Her consortship with an alpha male lasts c.3–4 days. Adult females show a preference for the alpha male; they follow him constantly and consort with subordinate males only when he is engaged with another female. Female Black-horned Capuchins never solicit subadult males. During this consortship, the alpha male is slow to respond and delays copulating for hours or even days. He delays more in the dry season when females are fertile than in the wet season when they are not. After he mates, there is a post-copulatory phase, which is believed to be

a form of mate-guarding on the part of the male; he follows the female rather than vice versa. The female ovulates on the sixth or last day of her proceptive phase, and she also mates with subordinate males at this time. When females solicit subordinate males, the courtship is less complex, the response by the male is more immediate, the male and female separate immediately, and there is no post-copulatory consortship. These are referred to as “unimount” copulations. Alpha males are never interrupted by subordinate males, and subordinates are only occasionally interrupted by alpha males. Males evidently do not mate twice in the same day. The reason behind the reluctance of the alpha male to mate is believed to be because they are unable to ejaculate more than once a day, and for this reason, a premium is placed on making sure that each mating counts. Although the alpha male is apparently reticent and choosy, he eventually copulates with all, or nearly all, females in the group in any one mating season, and genetic studies have shown that the alpha male generally sires all offspring in the group. Gestation is c.153 days (range 149–158 days). Interbirth intervals at Caratinga Biological Station average 25·6 months (range 21–35 months), which is shortened to eleven months (range 9–14 months) when an infant dies. At Iguazú National Park, the estimated birth rate is 0·6 infants/female/year, with a mean interbirth interval of c.19 months, although some females breed successfully in successive years. When infants die before they are six months old, the interbirth interval is shortened to 11–12 months. The interbirth interval recorded at Carlos Botelho State Park is longer, averaging 30 months (n = ten females). Infants are weaned at 12–18 months. Females reach puberty (begin ovarian cycling) at about four years old, but they first conceive only when they are more than 4·5 years old, giving birth when they are generally 6–7 years old. Females begin cycling in February–March, and few females are still cycling by August. Conception usually occurs after 2–5 ovarian cycles in late autumn or winter when food availability is lowest and day length shortest. Activity patterns. Activity budgets of Black-horned Capuchins differ somewhat according to season and whether groups travel together or divide into subgroups. When traveling together in the wet season (food abundant), the day is divided into eating c.22% of the time, handling food c.14%, searching (stationary) for food c.8%, traveling c.39%, resting c.6%, social activities c.6%, and miscellaneous c.5%. In the wet season, individuals in subgroups spend more time eating, less time handling and more time searching for food, less time traveling and resting, and more time in social activities. The same comparison of subgroups in the dry season also found them eating, handling, and searching for food more, while traveling, resting, and socializing less. Overall, foraging (eating, handling, and searching for food) takes up c.38–44% of their day. In Carlos Botelho State Park, foraging consumed more time, averaging c.58% of their day, with traveling averaging 36%; very little time was spent resting and socializing (average 6%). In Iguazú National Park, one group used 34 sleeping sites during 203 nights, five of which were used more than 20 times each. All sites were tall (average height 31 m), large-crowned (average diameter 14 m) trees with numerous horizontal branches and forks. Movements, Home range and Social organization. Groups of 8–35 Black-horned Capuchins have been recorded at Iguazú National Park (averaging 12–17 individuals depending on the year), occupying home ranges of 81–293 ha (average 161 ha). Home ranges of two groups of eight individuals and 19 individuals in the Carlos Botelho State Park averaged 484 ha. Groups at other locations in the state of São Paulo had 8–15 individuals with 1–2 adult males. A group studied at Caratinga Biological Station was relatively large, with 24–28 individuals including four adult males, two subadult males, six adult females, six subadult females, and juveniles and infants. This group tended to divide into subgroups, which, when comparing activity budgets with single cohesive groups, evidently provides a slight but probably significant advantage when looking for food. At Carlos Botelho, groups divide into subgroups when food patches are smaller. At Iguazú, male Black-horned Capuchins disperse from their natal groups at 5–9 years old, but females are philopatric. Females may also transfer groups especially when groups divide or there is a change of the alpha male. Males and females form hierarchies, and although there is often more than one adult male in the social group, females interact and associate more with the alpha male than with subordinate males and other females. The alpha male sires most or all infants born in the group. His tenure can exceed eight years, but young adult females in the group avoid soliciting their father. Infanticide has been recorded when a new male takes over the alpha position in the group. On these occasions, pregnant females mate with the incoming male—probably a strategy to avoid infanticide. Status and Conservation. CITES Appendix II. Classified as Near Threatened on The IUCN Red List (as Cebus nigritus). The Black-horned Capuchin is adaptable and widespread, but the large majority of its original forests have been destroyed and fragmented. It is hunted for food. It occurs in a number of protected areas, including Iguazú National Park in Argentina, and Caparaó and Iguaçú national parks, Carlos Botelho, Intervales, Alto Ribeira, Morro do Diabo, Rio Doce and Serra do Brigadeiro state parks, and Xitué State Ecological Station in Brazil. Bibliography. Carosi et al. (1999), Di Bitetti (2001, 2003a), Di Bitetti & Janson (2000, 2001), Di Bitetti et al. (2000), Fragaszy, Fedigan & Visalberghi (2004), Fragaszy, Visalberghi et al. (2004), Freese & Oppenheimer (1981), Groves (2001), Izar, Verderane et al. (2012), Izar, Ramos-da-Silva et al. (2007), Lynch Alfaro (2005, 2007), Lynch & Rimoli (2000), Ramírez-Llorens et al. (2008), Rylands, da Fonseca et al. (1996), Rylands, Kierulff & Mittermeier (2005), Torres (1988), Wright & Bush (1977).

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On following pages: 9. Hooded Capuchin (Sapajus cay); 10. Crested Capuchin (Sapajus robustus); 11. Bearded Capuchin (Sapajus libidinosus); 12. Yellow-breasted Capuchin (Sapajus xanthosternos); 13. Blond Capuchin (Sapajus flavius); 14. Guianan Brown Capuchin (Sapajus apella); 15. Large-headed Capuchin (Sapajus macrocephalus).

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Plate 25 Species Accounts

9. Hooded Capuchin Sapajus cay French: Sapajou du Paraguay / German: Azara-Kapuzineraffe / Spanish: Capuchino de Azara Other common names: Azara’s Capuchin

Taxonomy. Cebus apella cay Illiger, 1815, left bank of the Río Paraguai, Paraguay. This species is monotypic. Distribution. SE Bolivia (departments of Tarija and Santa Cruz), N Argentina (provinces of Jujuy, Salta, Formosa, and Chaco), Brazil (W of the Rio Paraná— through the N of Mato Grosso State into SW Goiás , and Mato Grosso do Sul states), and Paraguay (E of the Río Paraguay as far as the mouth of the Río Paraná). Its range to the west in Bolivia is poorly known; it would seem that it is absent from the Bolivian Chaco as it is from the adjacent Paraguayan Chaco west of the Río Paraguay. There is no evidence to date that the Yungas populations in SE Bolivia and NW Argentina are continuous with the population in Brazil and Paraguay to the E. Descriptive notes. Head–body 40–45 cm, tail 41–47 cm; weight 3–3·5 kg. The Hooded Capuchin is a small, short-limbed species without sexual dimorphism, typified mainly by its prominent dark dorsal stripe. It is very variable in color but generally quite pale. Its crown is pale to blackish brown with two small tufts like horns. The Hooded Capuchin differs from other robust/tufted capuchins in that hair on the back of the neck and dorsal proximal two-thirds of the tail is slightly burnt brown and dorsal parts of the body (shoulders, front of the upper arms, saddle, rump, and thighs) are grayish-brown. Forearms, hands, wrists, lower legs, and feet are blackish. Eyes, nose, and mouth are variably surrounded by white hairs. There is a small white beard, and a dark line extends down from the ears to the jowls and under the chin. Habitat. Subtropical humid and semi-deciduous forests. In southern Bolivia and north-western Argentina in the Yungas Biogeographic Province, Hooded Capuchins are found in seasonal subtropical submontane (laurel) and montane forests up to elevations of c.1500 m. In eastern Paraguay, they occur in dense humid semi-deciduous forest and gallery forests in areas of thorn scrub and savanna, but not in the Chaco west of the Río Paraguay except possibly a small region of the southern wet chaco of the country. In the Pantanal of Mato Grosso, they occur in seasonal semi-deciduous forests and gallery forest. Food and Feeding. Diet of Hooded Capuchins is composed largely of fruits, leaves and animal prey. Studies in El Rey National Park, Argentina, in the north-western part of its distribution found seeds and fruits in diets during the wet season (November–March) and a significant preponderance (70%) of succulent leaf bases, peduncles of inflorescences, and infructescenses of epiphytic Bromeliacae (notably Aechmea distichantha but also the larger Tillandsia maxima and Vriesea tucumanensis) throughout the year. In the Pantanal, Hooded Capuchins visit flowers and lick nectar of the vine Combretum lanceolatum (Combretacae). When feeding in vegetation along riverbanks in the Pantanal, shoals of fish, notably the fruit-eating characid Brycon microlepis, follow capuchins to pick up debris they drop. Fruit of Guarea cf. guidonia (Meliaceae) and Zanthoxylum riedelianum (Rutaceae) particularly attract capuchins and fish. Breeding. There is no information available for this species. Activity patterns. There is no information available for this species. Movements, Home range and Social organization. There is no information available for this species. Status and Conservation. CITES Appendix II. Classified as Least Concern on The IUCN Red List (as Cebus cay). The Hooded Capuchin is widespread but poorly known. It occurs in Baritú, Calilegua, and El Rey national parks in Argentina, Noel Kempff Mercado National Park in Bolivia, Pantanal Matogrossense and Serra da Bodoquena national parks in Brazil, and Caaguazú, Cerro Cora, and Ybycui national parks in Paraguay. Bibliography. Anderson (1997), Brown (1989), Brown & Colillas (1984), Brown & Zunino (1990), Brown, Chalukian & Malmierca (1984), Brown, Chalukian, Malmierca & Colillas (1986), Fragaszy, Fedigan & Visalberghi (2004), Fragaszy, Visalberghi et al. (2004), Freese & Oppenheimer (1981), Hill (1960), Prance (1980), Rylands et al. (2005), Sabino & Sazima (1999), Stallings (1985), Torres (1988).

10. Crested Capuchin Sapajus robustus French: Sapajou robuste / German: Schopfkapuzineraffe / Spanish: Capuchino crestado

400

Other common names: Robust Tufted Capuchin

Taxonomy. Cebus robustus Kuhl, 1820, Morro da Arara, north of the Rio Mucuri, Minas Gerais, Brazil. C. P. Groves in 2001 considered this form to be a subspecies of Cebus nigritus. Monotypic. Distribution. SE Brazil, from the Rio Jequitinhonha in the S of Bahia State S to the rios Doce and Suaçuí Grande in Espírito Santo State and the E part of Minas Gerais State, E of the Serra do Espinhaço. Descriptive notes. Head–body 42–56 cm (males) and 33–44 cm (females), tail 43– 56 cm; weight 1·3–4·8 kg. The Crested Capuchin is very dark wood-brown or blackish above and on the limbs, with a trace of a dorsal stripe. Underparts are deep maroon-

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red or yellowish, and forearms, hands, lower legs, and feet are very dark brown to black. The face is dark grayish, with some white hairs on the forehead and temples. Crown tufts are tall and conical. Habitat. Tropical lowland and submontane forest, and dry semi-deciduous forest in the caatinga xeric scrub region of the middle Rio Jequitinhona and, farther inland, in forest patches in the cerrado (bush savanna), east of the Serra do Espinhaço. Food and Feeding. There is no specific information available for this species, but the diet presumably includes fruits, seeds, buds, flowers, invertebrates, and small vertebrates. Breeding. There is no information available for this species. Activity patterns. There is no information available for this species. Movements, Home range and Social organization. Crested Capuchins live in groups of 8–10 individuals, with 1–3 adult males. Small groups of about four individuals are believed to be a result of hunting. Densities are always low at c.0·2 groups/km2. Population surveys in the Espírito Santo State protected areas indicate densities and total populations of 0·6 ind/km2 and c.4766 individuals in Linhares Forest Reserve, 1·5 ind/km2 and c.2987 individuals in Sooretama Biological Reserve, 1 ind/km2 and c.150 individuals in Córrego do Veado Biological Reserve, and 0·6 ind/km2 and c.62 individuals in Córrego Grande Biological Reserve. Status and Conservation. CITES Appendix II. Classified as Endangered on The IUCN Red List (as Cebus robustus). Hunting of Crested Capuchins for food and pets and widespread destruction and fragmentation of their forests for agriculture, cattle ranching and eucalyptus plantations are the reasons for its endangered status. Less than 9% of the forest in the Espírito Santo State remains and the large majority of remnants are small patches of less than 1000 ha. The future of the Crested Capuchin lies in the permanence of the protected areas in its distribution: Linhares Forest Reserve of the Vale do Rio Doce mining company and Sooretama, Córrego do Veado, and Córrego Grande federal biological reserves in Espírito Santo State and Acauá State Ecological Station in Minas Gerais State. Bibliography. Chiarello (1995b), Chiarello & de Melo (2001), Fragaszy, Fedigan & Visalberghi (2004), Fragaszy, Visalberghi et al. (2004), Freese & Oppenheimer (1981), Groves (2001), Hill (1960), Martins (2005, 2008), Oliver & Santos (1991), Pinto (1941), Rylands, da Fonseca et al. (1996), Rylands, Kierulff & Mittermeier (2005), Torres (1988).

11. Bearded Capuchin Sapajus libidinosus French: Sapajou barbu / German: Rückenstreifen-Kapuzineraffe / Spanish: Capuchino barbudo Other common names: Black-striped Capuchin

Taxonomy. Cebus libidinosus Spix, 1823, Brazil, Rio Carinhanha, north of Minas Gerais, Brazil. Replaced by S. apella to the west, by S. flavius to the east, and by S. xanthosternos to the south of the Rio São Francisco; S. nigritus occurs just south of the Rio Grande and hybridization between it and S. libidinosus is evident in the western part of Minas Gerais State (in the area known as the Triângulo Mineiro). Monotypic. Distribution. C & NE Brazil, W and N of the Rio São Francisco to Maranhão State and the W of Piauí State and E to C Rio Grande do Norte (W of Jucurutu), NW Paraíba, W Pernambuco, and W Alagoas states, to the W it extends to the Rio Araguaia and the S limit is the N bank of Rio Grande in Minas Gerais State. Descriptive notes. Head–body 34–44 cm, tail 38–49 cm; weight 1·3–4·8 kg. The Bearded Capuchin is small without sexual dimorphism. It differs from all other species of Sapajus by the rusty red hair on the back of the neck, the dark brown preauricular stripe running down the side of the face in front of the ears, sometimes extending to the beard, and the orangey-yellow throat and dorsal parts of the body, flanks, outer parts of arms, and proximal two-thirds of the tail. Forearms are dark, and the lower back and outer surface of thighs are grayish brown, with some reddish hairs. The crown is black, with rounded, sometimes bushy, black tufts. Habitat. Two distinct vegetation types in Brazil: dry xerophytic caatinga forest and scrub in the north-east and the cerrado (bush savanna) of central Brazil. In the caatinga, annual rainfall is often below 200 m and rarely above 1000 mm. Bearded capuchins are found in the arboreal caatinga, a dense, tall, closed-canopy, deciduous forest, once widespread but now largely destroyed and degraded. They are also found in shrubby caatinga, low xerophytic, spiny scrub of profusely branched bushy vegetation mixed with prickly succulent cacti, and spiny, rigid-leaved bromeliads, reaching 8–10 m in height. Elevations are 300–600 m above sea level. Bearded Capuchins are generally associated with rocky escarpments and hillsides in mountainous regions. Legumes (Fabaceae) and Euphorbiaceae dominate the flora. The cerrado is a mosaic of savanna and savanna forest (“cerradão”) of twisted and gnarled low trees, often with thick, waxy, xeromorphic leaves, 5–15 m tall, forming a discontinuous canopy, and dry, dense semi-deciduous forest patches. The so-called “campo cerrado” is more open grassland with frequent but isolated trees. Elevations are generally above 500 m, and annual rainfall is 1500–2000 mm. Bearded Capuchins also occupy gallery forest and tall humid forest (“brejos”) in the caatinga, with a mixture of Amazonian and Atlantic Forest plant species benefitting from orogenic rainfall along the plateaus and windward slopes of mountain ranges. Food and Feeding. Bearded Capuchins eat mainly fruits and small animal prey, particularly insects. In the caatinga of Fazenda Boa Vista in Piaui State, the diet comprised

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Plate 25 Species Accounts

c.47% fruits, c.31% invertebrate prey, c.4% flowers, 4% leaves, and c.12% miscellaneous items. Palm fruits are available throughout the year and provide a vital and abundant food source during the dry season. Palms include Astrocaryum campestre, Attalea barreirensis, a second species of Attalea and a species of Orbignya. In Rio Grande do Norte, they also eat fruits of Syagrus. Palms are acaulous (a much shortened trunk) and their bunches of fruits are at ground level. Bearded Capuchins pull and twist out fruits and eat mesocarp from all except Astrocaryum. They use hard stones and a sandstone anvil to break open fruits to eat the endocarp. Stones are used to dig out tubers of Manihot (Euphorpbiacaeae) and Thiloa (Combretaceae) and break them into pieces. They are also used to open hollow branches to get at ant nests and vertebrate prey such as lizards and to get at the soft inner pith of cactuses (Pilosocereus piauhyensis). Twigs are used to probe tree holes and rock crevices for insects, honey, or water. It would appear that tool use, principally using rocks to break open palm fruits, is widespread in the caatinga region where Bearded Capuchins occur. They raid maize and sugar cane plantations. Breeding. Aspects of reproduction and breeding of Bearded Capuchins are undoubtedly similar to, or the same as, other species of Sapajus, but studies are lacking. As in other Sapajus capuchins, females show proceptive sexual solicitation of the group’s dominant male, who is not aggressive toward females and does not coerce them into mating. Interbirth intervals recorded for four females at the Fazenda Boa Vista averaged 22 months. Activity patterns. The activity budget of a group of Bearded Capuchins at Fazenda Boa Vista was foraging (searching for, handling, and eating food) c.49%, traveling c.37%, resting c.10%, and other behaviors such as grooming, play, and soliciting the sexual attentions of dominant males c.4%. More time is spent foraging in the dry season when palm fruits, which take some time to process, assume a larger proportion of the diet. The caatinga group of Bearded Capuchins at the Fazenda Boa Vista spends much of its time on the ground, or very near to it, in vegetation that is very open compared with tall forest, and they are correspondingly more skittish. In a direct comparison with Black-horned Capuchins (S. nigritus) living in tall forest, rate of alarm calling was higher: 0·2 alarms/hour for Bearded Capuchins compared to 0·1 alarms/hour for Black-horned Capuchins. Movements, Home range and Social organization. Group sizes of Bearded Capuchins in the caatinga of Serra da Capivara National Park in Piauí State average nine individuals with a maximum of 16. One group of ten had two males, five females, and three juveniles. Two groups in Fazenda Boa Vista had eight individuals and the other had 19 individuals, with home ranges of c.300 ha. A very large group of 53 individuals was found in the arboreal caatinga in the western part of Rio Grande do Norte. Groups of Bearded Capuchins are cohesive and do not split into subgroups. Groups of Black-horned Capuchins spread out while foraging, but Bearded Capuchins in these caatinga groups feed from concentrated small clumps of palm fruits, and rates of foodrelated aggression are correspondingly higher. Unlike Black-horned Capuchins, female Bearded Capuchins establish a clear dominance hierarchy. Status and Conservation. CITES Appendix II. Classified as Least Concern on The IUCN Red List (as Cebus libidinosus). As is true for all species of capuchins, the Bearded Capuchin is hunted wherever it occurs. It has undoubtedly declined in numbers in a diminishing and increasingly fragmented range over the last 40 years, with the enormous expansion of the agricultural frontier in central Brazil. It is, however, widespread and adaptable.

Food and Feeding. Yellow-breasted Capuchins eat fruits, flowers, leaves of bromeliads, palm hearts, and small animal prey, including insects, birds (and bird eggs), lizards, and small mammals. They are the largest arboreal mammals in the forests where they live and are important seed dispersers—perhaps the only seed disperser of many of the plants in their habitat. They eat fruits from 96 plant species and swallow seeds of 88 of them. They feed also on cultivated exotic species such as oil palm (Elaeis guineensis, Arecaceae), jackfruit (Artocarpus heterophyllus, Moraceae), and cacao (Theobroma cacao, Malvaceae). Breeding. A primiparous female Yellow-breasted Capuchin was recorded having twins in the Rio de Janeiro Primate Center in 1997. Her two infants were carried ventrally for the first month, and then increasingly on her back. In the fifth month, the infants occasionally left their mother and sometimes were carried by other females. Weaning began at one year of age. They weighed 1·5 kg and 1·6 kg at twelve months and 1·7 kg and 1·8 kg at 20 months, and still briefly rode on the mother’s back when they felt threatened. The male did not carry the young. Activity patterns. There is no specific information available for this species, but sleeping sites are in large emergent trees. Movements, Home range and Social organization. Group sizes of Yellow-breasted Capuchins are 9–27 individuals, but it is not known to what extent small groups result from hunting. A large group of 27 individuals used a large home range of more than 1000 ha, traveling c.3000 m during the day, whereas a smaller group of nine individuals used 418 ha. Females are philopatric and show little aggression. Surveys in 2003– 2004 provided a density estimate in three forests in southern Bahia of 3·7 ind/km2. Status and Conservation. CITES Appendix II. Classified as Critically Endangered on The IUCN Red List (as Cebus xanthosternos). Although there are no reliable estimates of remaining populations of the Yellow-breasted Capuchin, it is believed to be among the rarest of the Neotropical primates. Its forests were largely obliterated during colonization of the region from the early to mid-1500s. Historical records show that in 1757 the region of the Reconcavo da Bahia and the main part of the states of Bahia and Sergipe, where the Yellow-headed Capuchin once thrived, produced more than 300,000 cattle/ year, all bred in pastures that were once tall tropical forests. By 1938, only 0·1% of Sergipe State was forested. There are no localities remaining where the Yellow-breasted Capuchin is found in anything but very low densities. Moreover, they are hunted for their meat and occasionally trapped for the pet trade. The Yellow-breasted Capuchin is known to occur in Una and Mata Escura biological reserves, Serra do Conduru State Park, and Serra das Lontras National Park created in 2010. In 2005, the population in Una Biological Reserve was estimated at 340 individuals (4·4 inds/km2). A breeding program was initiated at the Rio de Janeiro Primate Center in Brazil in 1984, and the Brazilian government established an international committee for the management and conservation of the Yellow-breasted Capuchin in the wild and in captivity in 1992. Between 1990 and 2000, 21 Yellow-breasted Capuchins were sent to seven zoos in Europe. In 2000, as a result of the efforts of the Mulhouse Zoo in France, the Yellow-breasted Capuchin was managed through the European Endangered Species Programme, with no further imports. By 2010, the number of captive individuals had risen to 140 maintained in 21 zoos. Surveys of the wild Yellow-breasted Capuchins resulted in estimates of c.3000 individuals remaining in widely scattered localities, but none of the populations are considered viable in the long term.

Bibliography. Ferreira, Emidio & Jerusalinsky (2010), Ferreira, Jerusalinsky et al. (2009), Fragaszy, Fedigan & Vis-

Visalberghi (2004), Fragaszy, Visalberghi et al. (2004), Freese & Oppenheimer (1981), Kierulff et al. (2008), Ler-

alberghi (2004), Fragaszy, Izar et al. (2004), Fragaszy, Visalberghi et al. (2004), Freese & Oppenheimer (1981), Hill

nould et al. (2012), Oliver & Santos (1991), Pissinatti et al. (1999), Rylands, da Fonseca et al. (1996), Rylands,

(1960), Izar, Stone et al. (2008), Izar, Verderane et al. (2012), Moura (2007), Moura & Lee (2004), Moura & McConkey

Kierulff & Mittermeier (2005), Seuánez et al. (1986), Sick & Teixeira (1979), Torres (1988).

Bibliography. Baker & Kierulff (2002), Canale et al. (2009), Cassano et al. (2005), Coimbra-Filho (1986d), Coimbra-Filho, da Rocha e Silva & Pissinatti (1992), Coimbra-Filho, Rylands et al. (1991/1992), Fragaszy, Fedigan &

(2007), Freese & Oppenheimer (1981), Rylands et al. (2005), Silva (2001), Torres (1988), Visalberghi et al. (2007).

12. Yellow-breasted Capuchin Sapajus xanthosternos French: Sapajou à poitrine jaune / German: Gelbbrust-Kapuzineraffe / Spanish: Capuchino de pecho amarillo

13. Blond Capuchin Sapajus flavius French: Sapajou blond / German: Gelber Kapuzineraffe / Spanish: Capuchino rubio Other common names: Blonde Capuchin, Marcgrave’s Capuchin

Other common names: Buff-headed Capuchin, Golden-bellied Capuchin, Smooth-headed Capuchin

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Taxonomy. Simia flavia Schreber, 1774, Côrrego do Inferno, Usina Maravilha, municipality of Goiana, Pernambuco, Brazil, 7° 28’ 35·95” S, 34° 59’ 4·85” W. The provenance and identity of S. flavius, known only from an early illustration, was a mystery until a specimen was collected in 2005. It was described and designated as a neotype by M. Oliveira and A. Langguth in 2006. It was also described as a new species, Cebus queirozi by A. R. M. Pontes and colleagues in 2006. Monotypic. Distribution. Coastal NE Brazil from the S of Rio Grande do Norte State (as far W as Jucurutu, 6° 12’ S, 37° 02’ W, in the caatinga dry forest scrub of the Serra do Estreito), through Paraíba State to NE Pernambuco State; it is possible that it extends to the left bank of the Rio São Francisco in Alagoas State. Descriptive notes. Head–body 36·8–40 cm (two males) and 35·1–36·1 cm (two females), tail 37·8 cm (one male) and 42 cm (one female); weight 2·9–3 kg (two males) and 1·8–2·5 kg (two females). The Blond Capuchin is small, distinctive, and untufted. It has a uniformly golden-yellow body and limbs, and lower parts of the body are slightly darker. Hands and feet are black, and the tail is uniformly golden-blond (darker than the rest of the body on the dorsal side). It has a rectangular, snow-white cap on the front of the head, extending to just above the ears, and a furless, pendulous throat

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Taxonomy. Cebus xanthosternos Wied-Neuwied, 1826, Rio Belmonte, Bahia, Brazil. This species is monotypic. Distribution. EC Brazil, S and E of the Rio São Francisco, S to the Rio Jequitinhonha in the S of Bahia State. Descriptive notes. Head–body 39–42 cm (males) and 36–39 cm (females), tail 38–45 cm; weight 2–4·8 kg (males) and 1·3–3·4 kg (females). The Yellow-breasted Capuchin is generally brindled reddish above with a sharply marked, golden-red underside. The tail and limbs are black. The crown does not contrast with the body, the cap is black, and the face and temples are fawn. It is sometimes considered to be an exception among the robust/tufted capuchins because it lacks tufts, but it does in fact have small backward pointing tufts when inspected more carefully. In the northern part of its distribution, Yellow-breasted Capuchins tend be pale, and in the south-west in the north of Minas Gerais State, they are considerably darker in overall color. Habitat. Humid tropical lowland and submontane forest and, in the western part of its distribution, dry, semi-deciduous and deciduous forest. In the caatinga, the Yellowbreasted Capuchin is restricted to hills and mountain ranges where more humid forests can be found in valleys and slopes that receive orogenic rainfall.

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Plate 25 Species Accounts

flap. The face and forehead are pinkish, and eyes are brown. Sizes of tracks of adults on the ground are, on average, 72·4 mm for the hand (n = 20) and 95 mm for the foot (n = 22). Habitat. First found in degraded patches of coastal Atlantic Forest and Montrichardia linifera (Araceae) swamp in Pernambuco. In the west of Rio Grande do Norte, the Blond Capuchin has been recorded in shrubby caatinga, a low xerophytic, spiny scrub of profusely branched bushy vegetation up 8–10 m in height, mixed with prickly succulent cacti, and spiny, rigid-leaved bromeliads. It has also been observed using sand dunes, mangroves, sugar cane, and corn plantations, all of which bordered the forest fragments. It uses all layers of the forest, including ground. Food and Feeding. The Blond Capuchin eats fruits, leaves, insects, spiders, and small vertebrates. More than 32 items were recorded in the diet of a population in Paraíba State. Another population in a forest patch north of Mamanguape in north-eastern Paraíba used tools to obtain termites (Nasutitermes) in arboreal nests. Individuals first slapped the nest with both hands and then broke off a small twig, c.20–30 cm long, and stuck it into the nest by pushing and rotating the twig, holding it at its tip near the nest. Sometimes they broke the twig to shorten it, evidently needing it to be more rigid or fine. After perforating the nest, they pulled out the twig and ate any termites attached to it. They repeated the procedure three or four times in a bout, and before reinserting the twig, they slapped the nest again with the left hand. Each bout of “termite-fishing” lasted 40–60 seconds before the twig was discarded. Researchers imitated the capuchins and found that rotating the twig helped to perforate the nest (just trying to push the twig in was ineffective—it would break) and slapping the nest increased numbers of termites biting the twig. This termite-fishing behavior has not yet been observed in any other population of Blond Capuchins. Breeding. There is no specific information for this species, but infant Blond Capuchins have been seen throughout the year. Activity patterns. Blond Capuchins spend most of their time searching for, handling, and eating food and traveling. In the caatinga scrub, they are very terrestrial. Movements, Home range and Social organization. There are four research teams studying the Blond Capuchin in the wild and in captivity. Group size varies depending on location: 18–52 individuals in Pernambuco, 45 individuals in caatinga in the Serra do Estreito in south-central Rio Grande do Norte, and 7–72 individuals in forest fragments north of Mamanguape, Paraíba. Camera-trapping showed group sizes of 2–32 individuals, but single individuals were also recorded. Blond Capuchins have a rich vocal repertoire, with at least ten different call types. Call frequencies are 0·5–10 kHz. Some calls seem to carry information about individual age and have a behavioral context. Blond Capuchins apparently have a complex fusion-fission society. Only females carry infants. Status and Conservation. CITES Appendix I. Classified as Critically Endangered on The IUCN Red List (as Cebus flavius). The Blond Capuchin may have been one of the first of the South American primates to be taken to Europe, evidenced by a fresco by Andrea del Sarto in the Villa Medici of Poggio a Caiano, near Florence, called “Tributo a Cesare” dating from 1519–1521, which clearly depicts the Blond Capuchin. This underlines the long history of region’s colonization, accompanied by widespread and extremely rapid destruction of natural vegetation in the early 1500s. Enormous quantities of timber were exported, and forests were replaced with cattle pasture, sugar cane plantations, and, in many areas, desert scrub. Today, the Blond Capuchin lives close to highly populated areas in north-eastern of Brazil, north of the Rio São Francisco where only 5% of the original forest remains. Although small populations of the Blond Capuchin occurring through a relatively large area, they are restricted to isolated forest patches surrounded by sugar cane plantations. These small populations are extremely vulnerable, susceptible to selective cutting of forest, fires, hunting, and disturbance by tourists and domestic animals. In 2008, the total population was estimated at only 180 individuals, scattered over some two dozen subpopulations. Including the caatinga populations of Blond Capuchins discovered more recently, it is probable the total population is 1000–2000 individuals. Blond Capuchins have been reported in 26 fragments of Atlantic Forest in north-eastern Brazil and 15 fragments in the Paraíba State. Bibliography. Bastos et al. (2012), Bezerra et al. (2012), Brazil, ICMBio-MMA (2012), Coimbra-Filho & Câmara (1996), Ferreira et al. (2009), Masseti & Veracini (2010), de Oliveira & Langguth (2006), Pontes et al. (2006), Souto et al. (2011).

14. Guianan Brown Capuchin Sapajus apella French: Sapajou brun / German: Haubenkapuzineraffe / Spanish: Capuchino pardo

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Other common names: Black-capped Capuchin, Brown Capuchin; Margarita Island Capuchin (margaritae)

Taxonomy. Simia apella Linnaeus, 1758, “America.” Restricted by É. Geoffroy Saint-Hilaire in 1812 to “Cayenne, French Guiana.” Taxonomy of Amazonian robust/tufted capuchins is still not well understood. Eight Amazonian subspecies of Cebus apella were listed by W. C. O. Hill in 1960. These were largely ignored because of their uncertain distributions and difficulties of understanding regional variation or patterns, with so much variation in tufts and color patterns. C. P. Groves in 2001 listed five of Hill’s subspecies as valid species or subspecies. J. S. Silva, Jr. in 2001 argued

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for the existence of just two Amazonian robust capuchin species: S. apella in the eastern and central Amazon Basin and S. macrocephalus (recognized as a subspecies of apella by Hill) in the western Amazon Basin. Following Silva, S. apella includes, as a junior synonym, C. fatuellus tocantinus, named by Lönnberg in 1939—a dark capuchin from Cametá, Rio Tocantins, Brazil (recognized by Hill and Groves). Preliminary genetic studies by J. W. Lynch Alfaro and her coworkers indicated that apella and macrocephalus may not be distinct taxa, but further studies are needed. Two subspecies recognized. Subspecies and Distribution. S. a. apella Linnaeus, 1758 – forests of the Amazon Basin in EC Colombia, S Venezuela, and Brazil, extending N to the S part of the Orinoco Delta in Venezuela and the Guianas; limits in the S, SE, and E are defined by the extent of the Amazon forest, in the E extending into the Zona dos Cocais (babassu palm, Orbignya phalerata, forest) in the S and E of Maranhão State that marks the transition zone to xeric deciduous forest and scrub of the caatinga; in the W, the distributional limits are poorly known, but defined roughly by the interfluvium of the rios Negro and Solimões and the Rio Madeira Basin. S. a. margaritae Hollister, 1914 – highlands of E Margarita I, Venezuela (Serrania de El Copey and the Cerros El Tamoco, Tragaplata, La Yalla, and Matasiete). Descriptive notes. Head–body 38–46 cm, tail 38–49 cm; weight 2·3–4·8 kg (males) and 1·3–3·4 kg (females). The Guianan Brown Capuchin is large and somewhat heavily built, with a broad head, flat face, and short limbs. The coat is long and coarse, with extremities noticeably darker than the rest of the body. It is generally gray-fawn to dark brown above, with a yellowish or red underside. Lower limbs and tail are black, and there is a variably well-developed dorsal stripe. The face is light gray-brown, and the characteristic crown tuft consists of a thick mat of erect black hairs, forming short tufts above the ears. This gives the top of the head a flat, squared-off or “eared” frontal outline or, alternately, elongated at each frontal side to form “horns.” The black crown of the Guianan Brown Capuchin forms a slight vertex on the forehead (not extending to the nose), and there is whitish line framing the face, forming a slight arch above the eyes. The face and temples are light gray-brown. The darker area above the eyes gives the appearance of eyebrows. The crown cap extends down the cheeks as a distinct, thick black bar in front of each ear; these “sideburns” often meet below the chin. Sexes are similar, but males are a bit heavier and often considerably darker. The “Margarita Island Capuchin” (S. a. margaritae) is darker than forms from the upper Orinoco in Venezuela. Dark sideburns in front of the ears are longer (extending from crown to throat) and more defined than in the nominate subspecies of the Guianan Brown Capuchin. When tufts are present, they are longer in the nominate form than in the Margarita Island Capuchin. In the Margarita Island Capuchin, outsides of upper arms and shoulders are a pale-yellow straw color. Wrists, ankles, and inner forearms are black, thighs and rump are brindled (pale yellow) brown, and flanks, lower back, and upper chest are pale brown, becoming paler on the upper back to the neck. There is a dark midline stripe down the back. The face is grayish, tinged pink on the cheeks and chin, with sparse whitish hairs on the temples and around the mouth. The face is framed by a black line extending from the black cap to sideburns to the throat. The black cap extends in a “V” to between the eyes, with small round tufts above each eye. The form from the Rio Tocantins Basin is dark gray-fawn to dark chestnut-brown, with reddish undersides and flanks. There is a trace of a dorsal stripe. Forearms, thighs, shanks, feet, and tail are black. The head is also black with little trace of white, and crown tufts are well developed. Habitat. A wide range of forest types: lowland, submontane (700–1000 m above sea level), and montane forests of the Guiana and Brazilian shields of the central and eastern Amazon Basin, including seasonally inundated forests, tidal flooded forest (tidal várzea) in the delta region of the Amazon River, mangrove forest and palm swamp forest, liana forest (“mata de cipó”), gallery forest and forest patches in the Roraima and Amapá states savannas, and open-canopied babassu palm (Orbignya) forest on the south-eastern border of the Amazon River in the states of Maranhão, Goias, and Pará. Although the geographic distribution of the Guianan Brown Capuchin includes sclerophytic, small-leaved, white-sand forests (“caatinga alta” or “campinarana,” also Wallaba forest in the Guianas) and scrub (“caatinga baixa” or “campina”) typical of the Rio Negro Basin and also Serra do Cachimbo on the Pará State/Mato Grosso State border, it is not known to what extent they occupy them. The Margarita Island Capuchin is confined to isolated montane forest patches in the eastern part of the island, including pre-montane dry forest, humid montane and pre-montane forest, and disturbed (broken canopy) palm forest (“cocal”). Food and Feeding. Diet of Guianan Brown Capuchins consist of fruits and seeds (68%), small animal prey (19·7%), and other items such as palm heart, the rachis of palm leaves, and the succulent bases of bromeliad leaves (12·3%). In a study by W. Spironello near Manaus in the Central Amazon, six species of palms (Arecaceae) figured prominently in the diet of a group of 9–14 Guianan Brown Capuchins, particularly two species: Jessenia (= Oenocarpus) bataua and Maximiliana (= Attalea) maripa. They ate the albumen (endocarp) of immature fruits and the mesocarp of mature fruits of these two species and Oenocarpus bacaba, Astrocaryum munbaca, Mauritia flexuosa, and Syagrus inajai. In the early dry season, 42% of all records of fruit feeding were of palms fruits, peaking at c.52% in July. Throughout the year, the group ate fruits, seeds, nectar, gum, inflorescences, pith, and petioles from more than 200 plant species. Besides palms, the other plant families most commonly found in the diet included Sapotaceae (Micropholis, Chrysophyllum, Pouteria), Moraceae (Brosimum, Ficus), Urticaceae (Pourouma), Fabaceae (Inga), Euphorbiaceae (Micrandropsis), Goupiaceae (Goupia glabra), and Lecythidaceae. This group of Guianan Brown Capuchins had a very large home range of c.850 ha, probably because of the low density of palms in the area. Further north in Suriname and Guiana, where rains are also very seasonal, palms Socratea exorrhiza and Maximiliana maripa are important to Guianan Brown Capuchin

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in the dry season. In Suriname, the Guianan Brown Capuchin’s propensity to pound hard fruits is particularly applied to the thick-husked woody fruits of the Brazil nut family, Lecythidaceae. When immature, the fruit is relatively soft, and the reward of seeds rich in lipids, proteins, and carbohydrates easily compensates for difficulties of getting at them. In a study at the Nouragues Field Station, French Guiana, S. Zhang found that Guianan Brown Capuchins ate mostly fruits during the wet season (December– June), peaking in March–June when 80–99% of the diet was fruit. In the dry season (October), fruits comprised as little as 30% of the diet, which was supplemented by flowers, pith, stems, petioles, and leaves and an increase in the time spent foraging for animal prey. Guianan Brown Capuchins eat freshwater crabs (Pseudothelphusidae) along river banks. They eat oysters (Crassostrea rhizophorae) from mangrove swamps, banging them with oyster shells until they weaken and open. Vertebrate prey includes frogs, lizards, birds, and small mammals such as mouse opossums (Marmosa). The diet of the Margarita Island Capuchin, studied by L. Marques and V. Sanz in 1989–1990, was 50·9% fruits, 24·6% insects, 14% pith, 3·5% petioles, 3·5% seeds, and 3·5% flowers. Animal prey include Hymenoptera (ants: adults, larvae and pupae), Orthoptera, and Coleoptera. Guianan Brown Capuchins use similar methods to forage for animal prey and exploit palm fruits as do Large-headed Capuchins (S. macrocephalus). Breeding. The menstrual cycle of the Guianan Brown Capuchin is 20·8 days; menstruation lasts three days, sometimes evidenced by a minimal menstrual bleeding. Births peak in October–January. Normally only one offspring is born at a time. Mean interbirth interval in captivity is 20·6 months (n = 23 successive births). Males are directly involved with the young or are at least tolerant of them. Females are fully adult at c.4–5 years, but males take longer to mature (up to eight years in some cases). As in other species of Sapajus, females show proceptive behavior during the periovulatory period, ending on the sixth day when ovulation occurs. The female stays with the alpha male, showing courtship behavior: grimacing, eyebrow raising, circling the male, presenting and touching him, and making mating calls. The male is slow to respond but eventually may mount several times. This courting can continue for up to four days; on the fifth day, the alpha male follows the female and interferes with subordinate males attempting to mate with her. On the sixth day, the alpha male leaves the female. She may then mate with subordinate males, but without prolonged courtship, and the partners separate immediately after mating. Gestation is c.155 days. Neonates weigh c.210 g (range 170–260 g), or c.9% of the mother’s weight. Neonatal growth is rapid for eight weeks after birth but then slows. Female Guianan Brown Capuchins stop growing at about five years old, but males continue to gain weight for another couple of years. In captivity, males are fertile when they are a little more than four years old, but in the wild, they probably do not breed for another few years when they can secure a position as an alpha male. Females are fertile and able to reproduce at five years old. Activity patterns. In a study in the Nouragues Field Station, activity patterns varied during the year, influenced largely by food availability and dispersion. In the wet season when fruits were abundant and widespread, Guianan Brown Capuchins tended to travel more widely. Throughout the year, feeding on fruits took up 20–30% of the day, foraging for animal prey 20–35%, travel 20–30% (more time was spent in travel in December–January in the early wet season), 5–10% resting, and 4–15% in other activities (e.g. grooming and play). When traveling and foraging, they generally used middle and lower canopies and understory, 10–20 m above the ground. Sleeping sites in the Manaus and Nouragues studies were typically in crowns of tall (20–25 m) Jessenia palms, where individuals could lie flat on the leaf bases and where access to the tree was limited to fronds, providing some protection from mammalian predators. Movements, Home range and Social organization. The Guianan Brown Capuchin lives in single-male or age-graded (with a single dominant male) groups of generally 10–20 individuals, including up to five adult females. The Margarita Island Capuchin lives in small single-male groups of 4–6 individuals, including 1–2 adult females, subadults, and juveniles. The geographic distribution of the Guiana Brown Capuchin largely coincides with the Guiana and Brazilian shields, very ancient rock formations with nutrient poor soils compared with alluvial plains of the western Amazon Basin, occupied by the Large-headed Capuchin. Forest productivity of the shields is low, and home ranges tend to be large, from 355 ha at the Nouragues Field Station in French Guiana to 850 ha north of Manaus. At Manaus, daily home ranges were 34–70 ha and daily movements were 2236–4560 m. In this terra firma forest, Guianan Brown Capuchins spent 39% of their time in areas of poorly drained soils along streams where their favored palm, Jessenia bataua, was found. They typically slept in these palms (92% of the recorded sleeping sites). Daily movements were longer in the wet season when fruit sources were more widespread. A similar pattern was found in Nouragues where daily movements were 1746–3469 m (average 2268 m) and were longer in December–January when fruiting trees were neither scarce nor abundant but widespread. Small groups of Margarita Island Capuchins occupy home ranges of c.30 ha. Predators include forest cats and the large raptors. Status and Conservation. CITES Appendix II. Classified as Least Concern on The IUCN Red List (as Cebus apella), with the Margarita Island Capuchin classified as Critically Endangered (as C. a. margaritae). The Guianan Brown Capuchin is intensively hunted for meat, particularly where the larger atelines have already been hunted out. It is adaptable, however, and wide ranging in the remotest and most untouched areas of the Amazon Basin to the north of the Amazon River. To the south of the river, enormous areas of forest are being destroyed in northern Mato Grosso and southern Pará states in the Madeira and Tapajos basins. The Guianan Brown Capuchin occurs in numerous and large protected areas. The Margarita Island Capuchin is well separated from other robust/tufted capuchin monkeys—the nearest population is in the southern extreme of the Orinoco Delta, c.1200 km away—and suffers from a tiny distribution, habitat degradation, illegal hunting, and commerce. Capuchins raid crops and are

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considered to be pests and persecuted, even though they are also favored as pets. Possibly a further threat to the Margarita Island Capuchin is the recent introduction of the Guianan Weeper Capuchin (Cebus olivaceus) to Margarita Island, where they may compete for diminishing habitat. The Margarita Island Capuchin occurs in Cerro El Copey National Park (7130 ha), but parts of the Park are being encroached upon and there is illegal logging. It is also found in Cerro Matasiete y Guayamuri Natural Monument (1672 ha), which affords it some protection. Bibliography. Boher-Bentti & Cordero-Rodriguez (2000), Boinski et al. (2001), Fernandes (1991), Fernandes et al. (1995), Fragaszy, Fedigan & Visalberghi (2004), Fragaszy, Visalberghi et al. (2004), Freese & Oppenheimer (1981), Guillotin et al. (1994), Groves (2001), Husson (1957), Linares (1998), Lönnberg (1939), Lynch Alfaro, Boubli et al. (2012), Márquez & Sanz (1991), Martinez et al. (2000), Mittermeier & van Roosmalen (1981), Nagle & Denari (1982), Phillips et al. (1994), Port-Carvalho et al. (2004), Rettig (1978), Rylands et al. (2005), Sanz & Márquez (1994), Simmen & Sabatier (1996), Spironello (1991, 2001), Torres (1988), Zhang Shuyi (1995a, 1995b), Zhang Shuyi & Wang Lixin (1995).

15. Large-headed Capuchin Sapajus macrocephalus French: Sapajou à grosse tête / German: Großkopf-Kapuzineraffe / Spanish: Capuchino de cabeza grande

Taxonomy. Cebus macrocephalus Spix, 1823, forests of Lago Cactua, near Rio Solimões, Amazonas, Brazil. In 2001, J. S. Silva, Jr. argued for just two species of Amazonian robust/tufted capuchins: S. apella in the eastern and central Amazon Basin and S. macrocephalus (recognized as a subspecies of apella by W. C. O. Hill in 1960 and C. P. Groves in 2001) in the western Amazon (distributional limits poorly defined). Following Silva, S. macrocephalus includes, as junior synonyms, Simia fatuellus from the upper Magdalena Valley, Colombia (recognized by Hill and Groves), Cebus fatuellus peruanus from Huaynapata, Marcapata, 760 m, Cuzco, Peru (recognized by Hill, Groves, and R. Aquino and F. Encarnación in 1994), Cebus apella maranonis from Hamburgo, Peru (recognized by Hill and Aquino and Encarnación), Cebus pallidus from the Río Beni (recognized by Hill, Groves, and S. Anderson in 1997), Cebus libidinosus juruanus from opposite João Pessoa, Rio Juruá, Brazil (recognized by Hill and Groves), and Cebus apella magnus from the Río Putumayo, 1° N, 76° W (recognized by Hill). The form in central and northern Bolivia (south of the Río Madre de Dios) has also been referred to as S. libidinosus pallidus and S. apella pallidus in recent publications. Preliminary genetic studies in 2012 by J. W. Lynch Alfaro and her coworkers failed to indicate that apella and macrocephalus were distinct taxa, but further research is needed. Monotypic. Distribution. Upper Amazon Basin in E Colombia (N as far as the Río Arauca on the Venezuelan border; an isolated population in the upper Río Magdalena in the Huila Department), E Ecuador, E Peru, W Brazil, and C & N Bolivia (S at least to the upper Río Beni); the exact limits of its distribution have not been delineated, and particularly where they meet those of the Guianan Brown Capuchin (S. apella) in the Rio Madeira Basin, in the N along the Orinoco, and in the interfluvium of the Rio Solimões and upper Rio Negro. Descriptive notes. Head–body 37·5–45·5 cm (males) and 39·5–40·9 cm (females), tail 42·5–49 cm (males) and 41·6–42 cm (females); weight 2·9–4·6 kg (males) and 1·3–3·4 kg (females). The overall color of the Large-headed Capuchin is gray-brown or gray-ochery to dark brown above, with a dark dorsal stripe, and yellow-fawn or red-gold (occasionally blackish) below. Sides of the neck are lighter, upper arms are pale yellowish, and legs are black with yellow-fawn or red-gold below. In the darkest individuals, the crown contrasts very little with the body, and shape of the crown cap in front (i.e. angular or broad) and presence of white margins are variable. Adults have very welldeveloped, high, pointed crown tufts that resemble horns, which become reduced or flattened with age. There is often a gray-white stripe running from eye to ear. Three forms of the Large-headed Capuchin have been noted. The Colombian form is bright brown above and red below and has a prominent dorsal stripe. Its face is almost naked and a dark purplish flesh color. The Peruvian form is uniformly dark chestnut-brown above, becoming more reddish toward the flanks, and is deep yellow-brown below. A dark brown band runs down the midline of the back. Its legs, tail, and (occasionally) forearms are black. Its cap is black and distinct, and temples and sides of the crown are often white. There is a crescent-shaped whitish patch above each eye. Crown tufts are absent or minimal. The third form from Brazil is reddish-brown above with a very pronounced blackish dorsal stripe. The throat and upper chest are blackish or pale reddish-buff, and limbs and tail are dark brown or black. Habitat. Evergreen humid tropical lowland forests, including seasonally inundated forests, bamboo forest, palm swamps, and subtropical montane (cloud) forests of the upper Amazon Basin, up to elevations of 1800 m in Peru and 1300 m in Colombia. In Ecuador, the Large-headed Capuchin is mostly found below 600 m, but there is an isolated population in the Río Magdalena, Colombia, at 2700 m. It extends north through the deciduous gallery forests of the Eastern Llanos of the eastern tributaries of the Orinoco in Colombia as far north as Río Arauca, but apparently not extending into Venezuela (Maracaibo Basin). Food and Feeding. Diet of the Large-headed Capuchin largely consists of fruit and insects but also seeds, pith, leaves, stems, flowers, nectar, millipedes, spiders, snails, frogs, lizards, nestlings, and bird eggs. Fruits include succulent drupes and berries, especially of Moraceae, and palm (Arecaceae) fruits, which are a particularly important

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her ovulatory cycle, she persistently follows the alpha male, approaching, touching, running away, grimacing, eyebrow-raising, making distinctive calls, and adopting submissive postures. On the penultimate day of her ovulatory cycle, the female begins to solicit other males, and the alpha male follows her and prevents them from approaching, although aggression between males is infrequent. Active solicitation by the female is believed to be related to the alpha male’s ability to control the other group members’ access to food sources, particularly palm fruits, during periods of food scarcity. The alpha male tolerates females with whom he has mated. He may also intervene on a female’s behalf in disputes over food with other group members, particularly subordinate males. Food shortage at Cocha Cashu in Manu National Park and Biosphere Reserve during the early dry season is considered to be critical enough to affect the females’ health and fecundity. It is unclear why females solicit and copulate with other males at the end of their ovulatory cycle, but it may ensure pregnancy if the alpha male is infertile and confer future benefits considering that an alpha male’s tenure may be limited. Gestation is c.153 days. At Sierra de la Macarena National Natural Park, Colombia, most births occur in the early wet season (February–June). Females first give birth at 7–8 years old. Interbirth intervals average 25·6 months when the infant survives but 15·5 months when the infant is lost. At Cocha Cashu, births occur in the early and middle part of the wet season (October–December) when fruit abundance is increasing. Infants begin to leave their mothers at about three months old, and juveniles carry infants. Six- month-old infants eat tidbits of food, and weaning begins at 8–12 months and is completed by c.20 months. Males, but not adult females, play with the infant. Activity patterns. Large-headed Capuchins in Manu National Park and Biosphere Reserve spent 50% of their time foraging for small animal prey, 22% traveling, 16% feeding on plant material, 12% resting, and the remainder in social activities (e.g. grooming, courting, and playing). Eating fruit peaks in the early morning and again in the middle of the afternoon, but the predominant activity during the day is foraging for animal prey. Resting peaks for 30–60 minutes at c.12:00 h. Movements, Home range and Social organization. At Manu National Park and Biosphere Reserve, groups of Large-headed Capuchins are generally 8–14 individuals, with one alpha male, one or more subordinate males, and 1–4 adult females. At Sierra de la Macarena National Natural Park, five groups monitored during five years ranged in size as follows: 13–16, 14–19, 8–10, 12–13, and 17–23. The last group had 7–8 adult males and 4–5 adult females. At one point when there were seven adult males in this group, five of them fought, causing serious wounding and the death of one of them. The group split into two groups, based on two dominant female lineages: one with six individuals and the other with eight individuals. The larger of the new groups grew over the following two years to 15 individuals, with three adult males and five adult females. Home ranges of groups at Manu are c.80 ha, with daily movements of 1630–2620 m. Male and female Large-headed Capuchins form hierarchies. Dominant individuals are rarely challenged by subordinates. There is a single alpha male, and the most dominant female is immediately below him in rank. Disputes are typically over food sources, particularly palm fruits, figs, Strychnos (Loganiceae) fruits, and Combretum (Combretaceae) nectar. Dominant individuals feed more at these food sources than subordinates, and the alpha male is able to commandeer feeding sites and allow females that mate with him to feed, while disallowing others. He favors his presumed offspring the same way. Individuals that he is intolerant of spend more time foraging for animal prey to compensate their otherwise reduced food intake. This is believed to be related to the evolution of their unusual mating system of prolonged proceptive behavior by females toward the alpha male during the periovulatory periods. Cebus males, by contrast, monitor females reproductive status, are aggressive to them, and pursue them to mate with them rather than vice versa. Males are more vigilant for predators (especially raptors) than females, and they confront and mob terrestrial predators and intervene when individuals in the group are threatened. Status and Conservation. CITES Appendix II. Classified as Least Concern on The IUCN Red List (as Cebus macrocephalus). Large-headed Capuchins are hunted, and they can become a principal target when larger spider and woolly monkeys are locally extirpated. There are areas where they have been extirpated in Ecuador and Peru. They are now classified as Near Threatened in Ecuador, but they are adaptable and wide ranging and occur in large, remote protected areas in the western Amazon Basin. Bibliography. Aquino & Encarnación (1994b), Defler (1982, 2003b, 2004), Escobar-Páramo (1989), Fragaszy, Fedigan & Visalberghi (2004), Fragaszy, Visalberghi et al. (2004), Freese & Oppenheimer (1981), Groves (2001), Hernández-Camacho & Cooper (1976), Hill (1960), Izawa (1978b, 1979a, 1992, 1994a, 1994b), Izawa & Mizuno (1977), Janson (1984, 1985, 1986), Lynch Alfaro, Boubli et al. (2012), Peres (1991c), Phillips, Bernstein et al. (1994), Phillips, Grafton & Haas (2003), Podolsky (1990), Rylands et al. (2005), Silva (2001), Struhsaker & Leland (1977), Terborgh (1983), Torres (1988), Wright & Bush (1977).

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part of their diet. A study by K. Izawa and colleagues in a site near the Río Duda on the western border of Sierra de la Macarena National Natural Park in Colombia recorded six species of palms in their diet, four of which—Astrocaryum chambira, Jessenia polycarpa, Socratea elegans, and Oenocarpus mapora—were systematically exploited for their fruits, particularly the albumen. Large-headed Capuchins also eat flowers and mesocarp of ripe fruits from Astrocaryum and Jessenia. They put young Astrocaryum fruit up to their mouth, raise their head up, and with one bite, open it and drink the albumen. With older Astrocaryum fruit, they bite off the exocarp and puncture the already woody husk through the germ-pore with their canine teeth, and then bash it against nodes of giant bamboo (Bambusa, Poaceae) and lick up the yogurt-like albumen that comes out. When older still, with the germ-pore closed, they eat the lipid-rich mesocarp and then open the fruit by bashing it against bamboo nodes until it cracks, and they then eat the hardened albumen. Studies by J. Terborgh and C. Janson in Manu National Park and Biosphere Reserve, Peru, showed that palms are also important to Large-headed Capuchins, including, to varying degrees, Astrocaryum, Bactris, Iriartea, Mauritia, and Scheelea. They eat immature inflorescences and pith of frond petioles (rachis) of Astrocaryum and Scheelea, fleshy lipid-rich mesocarp of fruits of all palm species, apical meristem (palm heart) of Bactris, and endosperm (albumen) of seeds of Astrocaryum. Astrocaryum and Scheelea plams are abundant in Manu, and with densities estimated at 39 trees/ha and 25 trees/ha, respectively, a group of Large-headed Capuchins with a home range of c.50 ha has access to more than 1000 trees of each species. Fruits comprise 99% of the plant part of the diet in the wet season, but only 66% in the dry season. Fruits and seeds (also pith and meristems) of these palm species are the mainstay (64% of feeding time) of the diet through the early dry season (May–July) when fruit is scarce. Figs are also important in the early dry season (27% of the diet) and even more so in the second one-half of the dry season (49% of the diet). In the wet season, fruits of palms or fig trees comprise 82% (October–December) to 90% (January–April) of the diet. C. Peres made a particular study of seed predation by Large-headed Capuchins at Urucu in the Purus Basin, south-western Amazonian Brazil. Seeds of palms such as Jessenia (= Oenocarpus) bataua are important in their diet throughout the year. Their asynchronous fruiting and relative abundance (22·7 trees/ha) meant that the impact of Large-headed Capuchins was not significant—many trees were never visited while fruiting. Seeds and arthropods were important foods in the middle of the dry season when fleshy fruits were rare, and at this time, Large-headed Capuchins had a devastating effect on seed crops of twelve Cariniana micrantha (Lecythidacae) that fruited during a 3–5 week period. The fruit of C. micrantha is a woody pyxidia containing numerous winged seeds that are dispersed by the wind when an operculum opens and releases them. Large-headed Capuchins pick off the fruits and bash them, at first with force and then more gently when they perceive that the operculum seal has cracked. If the operculum seal does not crack, they drop the fruit and try another. If it cracks, they pull it out and pick off and eat the highly nutritious seeds. Almost all of the fruits were either successfully cracked open and their seeds eaten (69·5%) or rotted on the forest floor (30·1%). In Colombia, Izawa also noted Large-headed Capuchins eating young bamboo leaves and occasionally leaf stems from Monstera pertusa (Araceae), Calathea (Marantaceae), and Heliconia (Heliconiaceae). Izawa observed an adult female catching and eating a Proboscis Bat (Rhynchonycteris naso). The insects eaten by Largeheaded Capuchins include ants (adults, larvae, pupae, and eggs) that they look for in bamboo internodes and Crematogaster and Azteca ants that they find in hollow twigs and small rotten branches. When foraging in bamboo, they scan culms, probably looking for signs of attack or small holes, and then run their hands up the internodes, tapping lightly and listening for frogs or insects (including orthtopterans) inside. If they hear movement, they bite and rip open the culm to take the prey. They also break open ant nests in the joints of the leaves of Phenakospermum guyanense (Strelitziaceae) and among the moribund leaves of Jessenia. Large-headed Capuchins bite open termite nests to eat adults, nymphs, and eggs; they hunt for grasshoppers among leaf litter and debris piles caught in the palm trees; and they eat beetle larvae, wasp larvae, and honeycombs whenever they find them. Terborgh noted that foraging for animal prey by Large-headed Capuchins is essentially manipulative and destructive, biting open and breaking bamboo canes, dead branches, and palm rachides; stripping bark; and generally rummaging in leaf litter and forest debris, particularly in palm crowns and liana tangles. Large-headed Capuchins spend more time searching in palms (32% of animal prey foraging time) than sympatric species of Cebus (21%), which are less destructive in their foraging and spend more time looking for insects hidden in more easily manipulated substrates (e.g. leaf curls and litter). Breeding. The ovarian cycle of the Large-headed Capuchin is c.22 days. A female is proceptive, constantly soliciting the attention of and mating (once a day at most) with the alpha male during her ovulatory cycle of c.5–6 days. During the first 3–4 days of

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Plate 26

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subadult adult

subadult

ssp olivaceus

adult

subadult adult

20 21 ssp castaneus

adult

adult subadult

22 24

adult

subadult

23 subadult

adult

ssp curtus

28 27 subadult

ssp capucinus adult

PLATE 26

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inches

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Plate 26 Species Accounts

Genus CEBUS Erxleben, 1777

16. Marañón White-fronted Capuchin Cebus yuracus French: Sapajou du Maranon / German: Marañon-Kapuzineraffe / Spanish: Capuchino del Marañón Other common names: Peruvian White-fronted Capuchin

Taxonomy. Cebus albifrons yuracus Hershkovitz, 1949, Montalvo, a site on the left bank of Río Bobanaza, c.45 km above its junction with the Río Pastaza, an affluent of the Marañón, eastern Ecuador, elevation c.500 m. C. P. Groves in 2001 considered this form to be a junior synonym of C. cuscinus. Monotypic. Distribution. S Colombia, E Ecuador, NE Peru (N of the Río Amazonas to the Río Putumayo, and W of the Río Ucayali, S as far the Río Pachitea), and presumably E Brazil (between the rios Içá and Amazonas). Descriptive notes. Head–body 43 cm (males) and 37 cm (females), tail 47 cm (males) and 45 cm (females); weight 2–4·7 kg. The Marañón White-fronted Capuchin is grayfronted on the forehead, sides of the face, chest, and outer sides of the arms. It is similar to Spix’s White-fronted Capuchin (C. unicolor), but its general color is ocherous brown, sharply contrasting with grayish or buffy on the outer side of forelimbs; flanks are paler. Underparts are pale silvery to pale ocherous orange. The cap is dark to very dark brown (bistre), and the tail is brown like the back, paler toward the tip. Habitat. Wet lowland terra firma and seasonally inundated forests in the upper Amazon Basin, extending to montane forests on western slopes of the Andes at elevations up to 2000 m. At Tiputini Biodiversity Station, Ecuador, where Marañón White-fronted Capuchins have been studied, annual rainfall is as high as 3274 mm, with an average of 273 mm/month. Seasonality is not marked, and no month has less than 100 mm of rain. Nevertheless, there is a relatively dry season in July–November, and fruit abundance is lowest in May–December and highest in January–April. Marañón White-fronted Capuchins usually occupy middle to upper canopies but sometimes forage on the ground. Food and Feeding. Diet of Marañón White-fronted Capuchins includes fruits, flowers, seeds, insects and other arthropods, bird eggs, and small vertebrates. In a study at Tiputini by L. Matthews a group spent c.10% of their day feeding on fruits and 54% foraging for animal prey. Breeding. Births of Marañón White-fronted Capuchins have been recorded in September–March in Peru and in November–January at Tiputini. Activity patterns. During a one-year study of a group of Marañón White-fronted Capuchins at Tiputini, the daily activity budget was foraging for animal prey 54%, traveling 25%, feeding on fruit 10%, resting 5%, and social and other activities 6%. They slept in the upper canopy along branches covered by lianas or between fronds of Scheelea or Mauritia palms (Arecaceae). Movements, Home range and Social organization. In Ecuador, groups of Marañón White-fronted Capuchins contain 5–35 individuals, with several adult males and females. A group studied on the north bank of the Río Tiputini had one adult male, two adult females, one subadult female, two juveniles, and two infants. The group’s home range was 240 ha, and it overlapped extensively with other groups. When groups encounter each other (on average one encounter about every four days), females and juveniles flee. Males give loud, high-pitched “yah” calls, also referred to as screams, and encounters are always aggressive, on occasion involving fights among males of the different groups. Individuals also utter loud “yah” calls when they are separated from their group. Marañón White-fronted Capuchins form mixed-species groups with Ecuadorian Squirrel Monkeys (Saimiri macrodon). Status and Conservation. CITES Appendix II. The Marañón White-fronted Capuchin has not been assessed on The IUCN Red List, but it is considered near threatened in Ecuador and vulnerable in Peru. In both countries, it is heavily hunted and is extirpated rapidly around human settlements. It can otherwise be found in high numbers in, for example, Pacaya-Samiria National Reserve in Peru. It is also protected in Sangay, Sumaco Napo-Galeras, and Yasuní national parks, Cayambe-Coca and Cofán-Bermejo ecological reserves, and Cuyabeno Wildlife Reserve in Ecuador. Bibliography. Aquino & Encarnación (1994b), Freese & Oppenheimer (1981), Hershkovitz (1949), Matthews (2009), Tirira (2007).

17. Shock-headed Capuchin Cebus cuscinus French: Sapajou ébouriffé / German: Peru-Kapuzineraffe / Spanish: Capuchino pálido

Taxonomy. Cebus flavescens cuscinus Thomas, 1901, Callanga, Río Pinipini, upper Río Madre de Dios, Cuzco, Peru. This species is monotypic.

Distribution. Poorly known, but it is believed to extend from the S (right) bank of the upper reaches of the Rio Purus in SE Peru, W into the Río Urubamba Valley in the Cuzco Department, including the upper Río Madre de Dios, S and E as far the Tambopata Basin, and extending into NW Bolivia. Descriptive notes. Head–body 40 cm (males) and 39–46 cm (females), tail 44 cm (males) and 39–47·5 cm (females); weight 2·8–3 kg. The Shock-headed Capuchin is similar to Spix’s White-fronted Capuchin (C. unicolor), but it has longer, silkier fur and is less brightly colored. Limbs are browner and contrast less with the back. The cap is large, distinct, and dark brown, and upper surface of the body is tawny-ocherous in the anterior parts and tawny toward the lower back. Lateral fringe and outer sides of upper arms are brown. The forearms are orangey-rufous on the outside, with wrists and hands darker. Outer thighs are like the rump, and shanks laterally are mixed orange-rufous. Surfaces of feet are brown to auburn. Underparts are ocherous-orange and silvery, becoming warm buff on the chest. There are whitish areas on the fronts of the shoulders and inner sides of the upper arms. The tail is cinnamon brown above, and brown below (a little paler toward the tip). The male has a broad pale frontal region sharply defining the dark brown cap, whereas the female has a dark brown frontal diadem continuous with the cap. Habitat. Lowland terra firma and seasonally inundated forests in the upper Amazon Basin, to the western slopes of the Andes in montane forest at elevations up to 1800 m. Shock-headed Capuchins usually occupy the middle to upper canopy but sometimes forage on the ground. Food and Feeding. Shock-headed Capuchins in the Manu National Park and Biosphere Reserve, Peru, have feeding habits and diet similar to the Large-headed Capuchin (Sapajus macrocephalus), but with some subtle and important differences in feeding strategies that allow sympatry, particularly during fruit shortages. Fruit and insects are the principal components the diet of Shock-headed Capuchins. Fruit comprises 99% of the plant part of the diet in the wet season (supplemented with pith and meristems) and 53% in the dry season. Seeds, particularly from palms, are also an important component of the diet in the dry season, and small quantities of pith, meristems, and petioles are eaten. Unlike Large-headed Capuchins, Shock-headed Capuchins can not break open Astrocaryum palm nuts to eat the endosperm—useful in the dry season when fruit is scarce. In the dry season, Shock-headed Capuchins spend hours searching through fallen bunches of palm fruits looking for those that have been attacked by bruchid beetles (subsequent to falling to the ground) but that still contain some endosperm. They smell and shake the nuts to gauge whether they still contain sufficient endosperm to make opening them worthwhile. Those they deem worthy are taken into a tree to bang them against a branch, or two nuts against each other, to open them and scrape out the hardened albumen with their teeth and fingernails. This is a prolonged process, and they spend longer time (sometimes more than two hours in a day), for less reward, than Large-headed Capuchins that spend c.45 minutes a day breaking open intact fruits from trees. To complement their dry-season diet, groups of Shock-headed Capuchins travel through much larger home ranges (more than 150 ha) than Largeheaded Capuchins to find other and large fruits crops, particularly those from widely scattered fig trees (Ficus, Moraceae). In the early dry season, Shock-headed Capuchins spend 56% of their feeding time on palm fruits and 41% of their feeding time on figs. Sympatric Large-headed Capuchins, in contrast, spend 64% their feeding time on palms and only 9% on figs. Shock-headed Capuchins are less destructive while foraging for animal prey and spend more time searching in litter, leaves, and tangles of lianas and much less time in palms than is typical of Large-headed Capuchins. The composition of the animal part of the diet is otherwise very similar between the two capuchins; both concentrate heavily on Hymenoptera, Orthoptera, and Lepidoptera. Breeding. Female Shock-headed Capuchins solicit males intermittently when they are receptive, and although there is a distinct hierarchy, mating is not restricted to the most dominant male. Males take an active interest in the sexual condition of females, often sniffing their urine, evidently to see if they are in a periovulatory stage and receptive. They try to mount females even when they are not receptive. Activity patterns. The annual activity budget of Shock-headed Capuchins in Manu National Park and Biosphere Reserve is foraging and feeding on insects 39%, feeding on plant material 22%, traveling 21%, resting 12%, and 6% in miscellaneous activities (e.g. grooming, play, and territorial behavior), with little seasonal change. In the early dry season, time spent eating fruits tends to be longer because of the long time they spend working on Astrocaryum nuts. They spend more time eating fruit in the morning, and foraging for animal prey increases gradually during the day and especially after resting at c.11:00 h. They also tend to eat fruit late in the afternoon before retiring. Movements, Home range and Social organization. Groups of Shock-headed Capuchins are multimale–multifemale and average c.15 individuals. The sex ratio is about even (1:1). They use large home ranges of more than 150 ha, spending time in any areas with fruit trees until their fruits are depleted. They may travel 1500–2200 m/day. Their ranging is nomadic, and there is no evidence of the use of a core area. Although home rang-

On following pages: 18. Spix’s White-fronted Capuchin (Cebus unicolor); 19. Humboldt’s White-fronted Capuchin (Cebus albifrons); 20. Guianan Weeper Capuchin (Cebus olivaceus); 21. Ka’apor Capuchin (Cebus kaapori); 22. Venezuelan Brown Capuchin (Cebus brunneus); 23. Sierra de Perijá White-fronted Capuchin (Cebus leucocephalus); 24. Río Cesar White-fronted Capuchin (Cebus cesarae); 25. Varied White-fronted Capuchin (Cebus

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FAMILY CEBIDAE Squirrel Monkeys and Capuchins

versicolor); 26. Santa Marta White-fronted Capuchin (Cebus malitiosus); 27. Ecuadorian White-fronted Capuchin (Cebus aequatorialis); 28. Colombian White-faced Capuchin (Cebus capucinus); 29. Panamanian White-faced Capuchin (Cebus imitator).

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FAMILY CEBIDAE Squirrel Monkeys and Capuchins

Plate 26 Species Accounts

es of different groups overlap, Shock-headed Capuchins are quite territorial. Usually they move away in different directions when they perceive another group’s presence up to 100 m away. When encounters do happen, there is considerable cooperation among group members. They vocalize loudly, and dominant males come together and all group members confront the opposing group with aggressive displays and sometimes chases. This is not typical of Sapajus or Saimiri, which are considerably more tolerant of other groups. Because of relatively large home ranges of Shock-headed Capuchins, groups have access to many more fruiting trees of any particular species over a wider area of forest than is the case for sympatric Sapajus that has home ranges about one-third the size (c.80 ha). Therefore, the diversity of the diets of Shock-headed Capuchins is lower, but an important aspect of their wider ranging is that they are able to exploit larger fruit crops in large-canopied trees (e.g. figs) more than Large-headed Capuchins, which use smaller-canopied trees (e.g. palms). About 40% of fruit feeding by Shock-headed Capuchins is in trees with crown diameters of 20–50 m compared to 12% by the Largeheaded Capuchins. The Shock-headed Capuchin lives in larger groups than Sapajus, multimale rather than single-male, and the males are philopatric and form coalitions to defend their groups. Aggressive interactions between males are less frequent than in Sapajus and males associate together more than do the females or any other age class. Males are more aggressive to females, and females are more aggressive to each other. Although an adult Sapajus male is more robust and stronger than a male Cebus, two Cebus males are able to challenge and displace a tufted capuchin male from a food source. Cebus groups are dominant as such to Sapajus groups by outnumbering them. Shockheaded capuchins often travel with squirrel monkeys (Saimiri boliviensis) and the groups often intermingle. Individuals can feed close together and only occasional antagonistic interactions and displacements occur (mostly in smaller-crowned fruiting trees). In the late afternoon, the two groups separate to different sleeping sites but rejoin in the morning. Squirrel monkeys generally travel in front of the Cebus groups. Predators of Shock-headed Capuchins include the larger raptors (Harpia, Morphnus, Spizaetus, and Spizastur), felids, the Tayra (Eira barbara), and snakes. Whereas a dominant male Sapajus is vigilant for aerial predators on behalf of his group (barking a warning), the dominant male Cebus hides like any other group member. Adult males, however, do mob ground predators, giving silent threat displays. Status and Conservation. CITES Appendix II. Classified as Near Threatened on The IUCN Red List (as C. albifrons cuscinus). Distribution of the Shock-headed Capuchin is not really known, and recent phylogenetic studies of the genus Cebus have highlighted the dearth of information regarding distributions of what may prove to be a number of distinct species in the southern Amazon Basin. The supposed distribution of the Shock-headed Capuchin in northern Bolivia, south-eastern Peru, and possibly the far south-western Brazilian Amazon Basin (Acre State) is relatively small, and development and colonization in some areas have resulted in considerable forest loss and hunting. Its hypothetical distribution includes some major protected areas such as Manu National Park and Biosphere Reserve in Peru and Madidi National Park and Manuripi-Heath National Reserve in Bolivia. Bibliography. Aquino & Encarnación (1994b), Freese & Oppenheimer (1981), Hill (1960), Janson (1986), Peres (1991c), Terborgh (1983).

18. Spix’s White-fronted Capuchin Cebus unicolor

408

French: Sapajou unicolore / German: Spix-Kapuzineraffe / Spanish: Capuchino de Spix

Taxonomy. Cebus unicolor Spix, 1823, Forests of the Rio Tefé, near its confluence with the Rio Solimões, Amazonas, Brazil. Although T. Defler and J. Hernández-Camacho in 2002 argued that C. unicolor was a junior synonym of C. albifrons, independent genetic studies by M. Ruiz-García and J. Boubli and their coworkers showed that white-fronted capuchins south of Rio Amazonas-Solimões are distinct. Morphological and genetic diversity of white fronted capuchins in the south-central Amazon Basin is yet to be investigated. Monotypic. Distribution. Wide ranging in the upper Brazilian Amazon Basin, S of the Rio SolimõesAmazonas, W from the Rio Tapajós, through the N of the states of Mato Grosso and Rondônia (at least to 10° S), and the Madeira, Purus, Juruá, and Javarí basins to the Río Ucayali in E Peru. White-fronted capuchins occur in northern Bolivia, S at least to the middle reaches of the Beni and Mamoré in the departments of Pando, Beni, and La Paz, and they are presumed to be Spix’s White-fronted Capuchin. Nevertheless, where distributions of Spix’s White-fronted Capuchin and the Shock-headed Capuchin (C. cuscinus) of the upper Purus and SE Peru meet is not known. Descriptive notes. Head–body 36·5–37·5 cm, tail 42–46 cm. No specific data are available for body weight. Spix’s White-fronted Capuchin is uniformly bright ocher or grayish-brown (flanks grayer and mid-back darker brown), with a yellowish or creamy-fawn front and reddish-yellow or reddish limbs and tail. The crown is nearly black and ends just behind the brows. There is no white on the front of the shoulders. Habitat. Lowland terra firma and seasonally inundated forest (várzea) and forest patches in Amazonian savannas. Food and Feeding. Diet of Spix’s White-fronted Capuchins undoubtedly contains fruits and invertebrate prey. They are particularly partial to mesocarp of fruits from Astrocaryum vulgare and Maximiliana (= Attalea) maripa (Arecaceae). Breeding. There is no information available for this species.

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Activity patterns. There is no information available for this species. Movements, Home range and Social organization. Groups of 12–16 Spix’s White-fronted Capuchins have been seen near the Rio Aripuanã in the northern Mato Grosso State, Brazil. Population surveys at various sites in the Rio Juruá Basin by C. A. Peres suggested high densities of Spix’s White-fronted Capuchin in four várzea forests: 12·2 ind/km2, 40·1 ind/km2, 44·7 ind/km2, and 48·6 ind/km2. Densities were 4·1– 16·8 ind/km2 in eleven terra firma forest sites. On Barro Vermelho Island, densities were 33·1 ind/km2 in terra firma forest and 44·7 ind/km2 in neighboring várzea forest. Status and Conservation. CITES Appendix II. Classified as Least Concern on The IUCN Red List (as a junior synonym of C. a. albifrons). Although Spix’s White-fronted Capuchin is hunted for food, it has a large range in the western Amazon Basin, south of the Rio Amazonas-Soliomões, and there is no reason to believe that it is threatened. Bibliography. Boubli et al. (2012), Freese & Oppenheimer (1981), Hershkovitz (1949), Peres (1997a), RuizGarcía, Castillo et al. (2010).

19. Humboldt’s White-fronted Capuchin Cebus albifrons French: Sapajou à front blanc / German: Weißstirn-Kapuzineraffe / Spanish: Capuchino de frente blanca Other common names: White-fronted Capuchin

Taxonomy. Simia albifrons Humboldt, 1812, Venezuela, forests near Santa Barbara and the cataracts of the Río Orinoco, Amazonas. C. albifrons as used here is a poorly defined species. It is known for sure only from a small region around the type locality, but P. Hershkovitz’s review in 1949 indicated that all white-fronted capuchins should be classified as its subspecies, including the form unicolor believed by him to occupy the majority of the Amazonian distribution of C. albifrons, both north and south of the Amazon River. There is no holotype specimen; the original description is believed to have been based on a pet seen in a hut. A review by T. Defler and J. HernándezCamacho in 2002 designated a neotype and argued that unicolor was a junior synonym. The molecular genetic study by J. Boubli and colleagues in 2012, however, showed that white-fronted capuchins south of the Amazon were quite distinct from those to the north. The form unicolor was accordingly resurrected for the gracile/untufted capuchins to the south of the river, and those to the north, by default, continue to be called albifrons. Nevertheless, the strong possibility remains that there are more taxa of gracile capuchins north of the Amazon (and to the south), which have yet to be identified. Intermediates between C. albifrons and C. capucinus occur in the middle San Jorge Valley, lower Río Cauca, Colombia. Monotypic. Distribution. Wide ranging in the upper Amazon Basin of S Venezuela (Federal Terrritory of Amazonas), S & E Colombia (Colombian Amazon region, N of the ríos Amazonas and Içá-Putumayo, and patchily occurring in the E lowlands W of the Orinoco, N as far as the lower Río Meta), and NW Brazil (N of the Solimões, W from the rios Negro and Branco, as far N as the Rio Uraricoera); it would seem that it is absent in the Colombian Amazon Basin from the middle and upper ríos Meta and Vichada and from the N bank of the upper Río Guaviare. Descriptive notes. Head–body 37·5 cm (males) and 36·5–37·5 cm (females), tail 42·5 cm (males) and 41–46 cm (females) for specimens from the rios Negro and Cassiquiare. Measurements of two young males, designated and described as the neotype and topotype by T. Defler and J. Hernández-Camacho in 1992 were: neotype head– body 38·5 cm, tail 43 cm, weight 2·6 kg, and topotype head–body 36·5 cm, tail 42·5 cm, weight 2·1 kg. An adult female topotype: head–body 33·8 cm, tail 41·2 cm; and weight 2·3 kg. The body of Humboldt’s White-fronted Capuchin is overall a pale grayishbrown, darker on limbs. Hands and feet are a yellowish brown. The tail is ashy above, whitish below, and brownish black toward the tip. The front is creamy, and there is a cap of short dark fur on the crown that is rounded in the front and well demarcated from the light forehead. The face is naked and pink. Habitat. Primary and some secondary deciduous, gallery, mangrove, and flooded forest, as well as high-elevation forest to 2000 m. Humboldt’s White-fronted Capuchin seems to prefer less disturbed, moister forest than other capuchins. It occupies semideciduous forest patches, seasonally inundated forests, and gallery forest in the Eastern Llanos of Colombia in the northern part of its distribution. The Guianan Brown Capuchin (Sapajus apella) is also found in this region, but the two are generally parapatric. Much of the distribution of Humboldt’s White-fronted Capuchin covers the sclerophytic, small-leaved, white-sand forests (“caatinga alta” or “campinarana”) and scrub (“caatinga baixa” or “campina”) typical of the Rio Negro Basin, but it is not known to what extent they occupy them. T. Defler studied a population in El Tuparro National Natural Park, south of the Río Tomo (tributary of the Río Orinoco) in the Eastern Llanos of Colombia. There were distinct seasons: a wet season in May–October when low-lying savannas and gallery forest were extensively flooded and a dry season in November–April. Semi-deciduous forests, 20–25 m high, on granitic hills with shallow and gravelly soils did not flood. Annual rainfall was c.2100 mm. Food and Feeding. At El Tuparro National Natural Park, Humboldt’s White-fronted Capuchins spent 80% of their feeding time eating fruits, nuts, seeds, leaves, stems, and flowers and 20% eating animal prey, including insects (adults, larva, and pupae), spiders and other invertebrates, tree frogs, lizards, and honey of melipone bees. Crowns are favored sites for foraging for animal prey. Palms (Arecaceae) are an abundant

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important food source for Humboldt’s White-fronted Capuchins. They eat mesocarp and endosperm of fruits of six species including Attalea regia, Jessenia polycarpa, Mauritia flexuosa, Syagrus orinocensis, and Bactris. Other species supplying fruits include Oxandra espintana (Annonaceae), Goupia glabra (Goupiaceae), Ficus (Moracae), Passiflora (Passifloraceae), Inga and Dipteryx (Fabaceae). The group at El Tuparro often traveled and foraged on the ground, picking up fallen fruits, eating fruits of terrestrial bromeliads (Ananas comosus, Bromelia), and foraging for insects in leaf litter. They used well worn trails on the ground to travel between forest patches. Humboldt’s White-fronted Capuchins drink water from tree holes, reservoirs in the tightly packed foliage of Phenakospermum (Strelitziaceae), and pools on the ground. Breeding. Female Humboldt’s White-fronted Capuchins have a 16–20-day reproductive cycle. Breeding occurs throughout the year, but in the highly seasonal Llanos, there is a birth peak in the late dry and early wet season. A female gives birth to a single young after gestation of 162–180 days. Males share in the care of offspring. Individuals have been known to live for up to 44 years. Activity patterns. Humboldt’s White-fronted Capuchins become active a little after 05:00 h. They feed and forage until midday when they rest for 1–3 hours. When foraging for animal prey, a group can be spread over an area 250 m wide. In the afternoon, they resume foraging until 16:00–16:30 h when they return to a sleeping site and rest, play, and groom until they enter sleeping trees a little before dusk. They sleep in crowns of Attalea regia palms, 25–30 m above the ground. Movements, Home range and Social organization. The group of Humboldt’s Whitefronted Capuchins studied by Defler numbered 35 individuals, with four adult males, ten adult females, along with subadults and juveniles. Its home range was 110–120 ha, and it traveled 4–5 km each day. About 20% of the home range overlapped with that of another group. Group interactions are tense and aggressive. The males give “yah” vocalizations and chase the males in the opposing group. Males form a dominance hierarchy, and the alpha male is the most vigilant and active in defending the group against predators and other groups. Males are very tolerant of infants and juveniles, often carrying them and rescuing them in situations of alarm. Predators include the black-and-white hawk eagle (Spizastur melanoleucus), the ornate hawk-eagle (Spizaetus ornatus), and the Tayra (Eira barbara). A harpy eagle (Harpia harpyja) was seen taking a Humboldt’s White-fronted Capuchin in Jaú National Park, Brazil. Population surveys in three terra firma forests of south-eastern Colombia in the basins of the rios Apaporis and Caquetá, where hunting is minimal or entirely lacking, suggested naturally low densities of 0·02–0·4 groups/km2 and 1·8–3·6 ind/km2. Status and Conservation. CITES Appendix II. Classified as Least Concern on The IUCN Red List. Humboldt’s White-fronted Capuchin is hunted, but it is widespread and occurs in numerous large protected areas in the Venezuelan, Colombian, and Brazilian Amazon Basin. Much of its distribution is in the western part of the Guiana Shield, with typically nutrient poor soils and forest, including large expanses of white-sand forests and scrub in the Rio Negro Basin. It occurs in numerous protected areas including Jaú and Pico da Neblina national parks in Brazil; Amacayacu, Cahuinarí, El Tuparro, La Paya, Serranía de Chiribiquete, and Sierra de la Macarena national natural parks and Nukak and Puinawai national natural reserves in Colombia; and Jaua-Sarisarinama, Parima Tapirapecó, Serrania de la Neblina, and Yapacana national parks in Venezuela. Bibliography. Barnett et al. (2011), Defler (1979a, 1979b, 1980, 1982, 1985, 2003b, 2004), Defler & Hernández-Camacho (2002), Freese & Oppenheimer (1981), Hernández-Camacho & Cooper (1976), Hershkovitz (1949), Palacios & Peres (2005).

20. Guianan Weeper Capuchin Cebus olivaceus French: Sapajou pleureur / German: Brauner Kapuzineraffe / Spanish: Capuchino oliva Other common names: Wedge-capped Capuchin; Chestnut Weeper Capuchin (castaneus), Weeper Capuchin (olivaceus)

Taxonomy. Cebus olivaceus Schomburgk, 1848, Venezuela, southern foot of Mount Roraima, Bolívar State, (c.4° 57’ N, 61° 01’ W), Venezuela, elevations 3100 feet (945 m). P. Hershkovitz in 1949 listed five forms that he “provisionally recognized” as subspecies of a monotypic weeper capuchin, C. nigrivittatus, named by Wagner in 1848. Although the name nigrivittatus was used for the Guianan Weeper Capuchin through the 1970s, J. G. Robinson pointed out that in 1941 B. von Pusch combined Saimiri and Cebus, resulting in nigrivittatus being a secondary homonym due to the prior description of the squirrel monkey Chrysothrix nigrivittatta by Wagner in 1848 (a junior synonym of Saimiri sciureus). The name for the Guianan Weeper Capuchin thus became C. olivaceus. C. P. Groves in 2001 did not consider any of the subspecies valid and concluded that C. olivaceus was monotypic. A phylogenetic analysis of C. olivaceus by J. Boubli and co-workers in 2012 largely confirmed the conclusion of Groves, except for one specimen from Guyana that could be distinguished as a distinct taxon; it diverged from the C. olivaceus c.700,000 years ago. This was ascribed to castaneus as listed by Hershkovitz in 1949. Its type locality is Cayenne, French Guiana, and it was considered to be the weeper capuchin of Guyana by G. Tate in 1939. Only one specimen was included in the analysis, but with further samples, castaneus may prove to be a distinct species. Two subspecies recognized. Subspecies and Distribution. C. o. olivaceus Schomburgk, 1848 – might be restricted to the Venezuelan Amazon Basin from the upper Río Orinoco, and throughout the Orinoco savanna above the mouth of

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the Río Meta, as far N and W as the Sierra de Perijá and the Venezuelan Cordillera de la Costa (Coastal Range), to the left bank of the Rio Essequibo in W Guyana, in forests of the Guiana Shield; distributional limits separating the two subspecies are not well known. C. o. castaneus I. Geoffroy Saint-Hilaire, 1851 – Guianas (possibly from the Rio Essequibo in Guyana E through Suriname and French Guiana) and N Brazil, where its distributional limits are not well known but are possibly marked by the rios Negro and Branco and Catrimani (right bank affluent of the Rio Branco) in the W, the Rio Amazonas in the S, and the Atlantic coast in the E, and it also occurs on Caviana and Mexiana Is in the estuary of the Rio Amazonas. Small numbers introduced as pets are now feral on Margarita I off the Venezuelan coast. Descriptive notes. Head–body 37–46 cm, tail 45–55 cm; weight 3–4·2 kg (males) and 2·3–3 kg (females). Male Guianan Weeper Capuchins are c.19·5% larger than females. It is a large, heavy-set, gracile/untufted species with long limbs and relatively coarse, shaggy fur. Pelage is brown with black-agouti banding on flanks, limbs, and tail. Hands, feet, and tail tip tend to be darkened. Underside tends to be dark. Lighter areas are light gray-brown, restricted to face and forehead and setting off a dark brown, sharp, V-shaped crown cap; the point of the “V” is connected to a thin umber stripe that runs down the center of the face to the nose. The face is naked and normally pink. The “Weeper Capuchin” (C. o. olivaceus) is mainly dark brown or reddish with black on the extremities and buffy-white cheeks. In the “Chestnut Weeper Capuchin” (C. o. castaneus), the black triangle on the crown is narrow, and the rest of the head is yellowish-white but more reddish- chestnut above the ear and nape. Upperparts of the body and limbs are reddish chestnut, and shoulders and fronts of arms above the elbows are pale yellow. Hands and feet are blackish. The tail is blackish brown with gray tipped hairs on the dorsal surface. Habitat. Primary rainforest, evergreen, and gallery forest from sea level to 2000 m; rarely in dry deciduous forest and shrub woodland. All levels of the forest are used by the Guianan Weeper Capuchin, although the middle and understory are preferred. Groups occasionally forage and play on the ground. In Suriname, the Chestnut Weeper Capuchin is almost entirely restricted to the interior, and like bearded sakis (Chiropotes) and spider monkeys (Ateles), it just enters the old coastal plain in a small part of western Suriname. Whereas the Guianan Brown Capuchin (Sapajus apella) is more of a habitat generalist in the Guianas, the Chestnut Weeper Capuchin is mostly restricted to high terra firma rainforest and is rarely or never seen in liana forest, pina (Euterpe) forest, and mountain savanna forest. An important study site for the Weeper Capuchin is Hato Masaguaral, a cattle ranch in the Llanos (savanna plains) of central Venezuela, a mosaic of grassland, palm savanna, shrub woodland, and gallery forest. The forest there is seasonal semi-deciduous dry forest, with annual rainfall of c.1450 mm, most of which falls during the wet season (May–October). Weeper Capuchins have also been studied at Hato Piñero 60 km south of Hato Masaguaral. Although physiognomically similar, the floristic composition of forests at each site is very different. Only 34 of 116 tree species occur at both sites, and those that are shared occur in very different densities. Of 79 tree species in the diet of Weeper Capuchins, only 15 (19%) are eaten at both Masaguaral and Piñero. Food and Feeding. In a detailed study of the diet of Weeper Capuchins at Hato Masaguaral by Robinson in the late 1970s, plant material accounted for 55% of all feeding records and animal prey 33% (in 12% of the records the food item was not identified). Fruit, largely fleshy and mostly ripe, was the main item of plant origin (46%) from more than 50 species in 30 families, the most important Rubiaceae and Moraceae. Fig trees (Ficus pertusa and F. trigonata, Moraceae) produce fruit asynchronously and were a staple in most months of the year. Large seeds were not ingested, but most small ones were, and were defecated intact. Seeds of Coccoloba (Polygonaceae) and Zanthoxylum (Rutaceae) were chewed and crushed. Weeper Capuchins sometimes ate grass seeds. In the middle of the dry season (March–April), palm fruits (Copernicia, Arecaceae) were picked unripe and eaten while the seed was still soft. Hard fruits such as those of Sterculia apetala (Sterculiaceae) and Hymenaea courbaril (Fabaceae) were pounded to open them. They also ate buds, leaves, and shoots but mostly just chewed them and then spat out the fibrous material, perhaps mainly to get water. This was common in the dry season and included rachis (central stem) of Copernicia fronds. When rachis of young fronds first appeared in the crown, Weeper Capuchins would ingest them, but older fronds were chewed and spat out. Flowers were rarely eaten, but those of the epiphytic cactus Hylocereus polyrhizus were favored. Large male Weeper Capuchins, in particular, sometimes pulled up sapling Cochlospermum vitifolium (Bixaceae) and ate the roots. Weeper Capuchins eat freshwater snails (Pomacea), arthropods (spiders, cockroaches, mantids, stick insects, termites, grasshoppers, cicadas, scale insects, caterpillars, beetle grubs, ants, especially Cephalotes, and millipedes), frogs, frog eggs, iguanas, birds (including nestlings and eggs), and Red-tailed Squirrels (Sciurus granatensis) when they can catch them. They search for prey in litter, palm crowns, green and dried palm fronds, along branches, dead wood, and green and dead leaves. They also prey on wasp nests and eat larvae, pupae, and adults. Bird eggs eaten included those of rufous-vented chachalaca (Ortalis ruficauda), green ibis (Mesembrinibis cayennensis), red-legged tinamou (Crypturellus erythropus), white-tipped dove (Leptotila verreauxi), greater ani (Crotophaga major), and hoatzin (Opisthocomus hoazin). They eat nestling doves and, at least, adult ruddy ground-doves (Columbina talpacoti). Fruits are most abundant in the wet season. In the dry season, they eat fewer fruits and more invertebrates, along with alternatives such as roots. In the dry season, hard fruits of Guazuma tomentosa (Sterculiaceae) are important, and they forage more on the ground, taking Pomacea freshwater snails and tettigoniid grasshoppers in the leaf litter. A leaf flush occurs with the first heavy rains of the wet season, and phytophagous caterpillars become abundant prey at that time. Breeding. Female Guianan Weeper Capuchins have a 16–20-day reproductive cycle. Births occur throughout the year but peak in May–June. Eyebrow raising is absent from the proceptive female’s repertoire, but partners grin and gaze at each other and tilt their heads. There is also the dance of the female running around the male, touch-

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ing him, and running away. A female produces a single offspring about every two years, after a gestation of 149–158 days. Infanticide has been reported, although males are generally tolerant of young and will often play with them. Female Guianan Weeper Capuchins are sexually mature at 4–7 years old, and males mature about a year after that (although full adult size is not reached until c.15 years old). Births are most common at the end of the dry season and early wet season. Infants are entirely dependent on adults until they are about four months old. At 4–12 months old, they gradually become more independent. They are considered juveniles at twelve months, although they continue nursing sporadically for another six months. Activity patterns. Overall, Guianan Weeper Capuchins spend almost 70% of their day foraging (c.22% catching and eating animals, 17% eating plant material, the rest searching for, extracting, and processing food items). Traveling takes up c.22% of their day, and resting and social behavior take up the remaining 8%. Males tend to rest more, and females tend to engage more in social activities. In the last month of the dry season, they spend c.58% of their day foraging and 19% traveling, but in the first months of the rainy season, they spend 43% of the day foraging and 17% traveling. They play and socialize much less in the dry season (6%) than in the wet season (20%). In the Llanos, groups of Guianan Weeper Capuchins leave their sleeping sites often in the dark and always before sunrise, and move rapidly to feeding sites, especially fruiting trees. They forage throughout the day, but less around midday, particularly in the hot dry season. In the dry season, foraging declines after c.10:30 h and increases again after c.14:30 h and particularly in the late afternoon before retiring to their sleeping sites. Much of their foraging is done on the ground. Males spend more time lower in trees and foraging on the ground than females. Adult and subadult males spend as much as 34% of their day on the ground, whereas adult and subadult females limit their time on the ground to c.10%, spending more time in the trees at heights of 5–10 m. Movements, Home range and Social organization. Group sizes of Guianan Weeper Capuchins average c.20 individuals but can be as large as 36 individuals, with the most skewed sex ratios of any of the capuchins (c.1 male:2 females). A group of c.20 Weeper Capuchins studied in the Llanos at Hato Masguaral in the late 1970s was composed of a single adult male, two subadult males, and 6–8 adult females, along with juveniles and infants. As a ripe-fruit specialist, their annual home range was large, up to 275 ha, and the group traveled 1046–3580 m/day, averaging 2141 m/day. When foraging for animal prey, a group is considerably spread out, over as much 150 m. Males disperse, sometimes as early as two years old but generally between three and six years old. Solitary males are rarely seen and only for a short period. Males may transfer between groups more than once. Low-ranking and old females may disperse, but they most often stay in their natal groups. Males and females have separate dominance hierarchies, with the alpha female ranking immediately below the alpha male. Home ranges of neighboring groups overlap, but groups generally avoid each other when their paths cross, except when in a fruiting tree. Larger groups displace smaller groups at fruiting trees, and this is seen as a crucial advantage at times of food shortage (dry season) and a reason why reproductive success of the females is higher in large groups than small groups. Females in large groups have a quite constant food intake during the year, but those in smaller groups have a high food intake in the wet season but very low intake when food is scarce in the dry season. Males also have better reproductive success in large groups because they have longer tenure and access to more females. With more subordinate and subadult males in a group, they are less likely to suffer aggressive takeovers by males from other groups, which not only ends (at least temporarily) the resident alpha male’s breeding career but also results in episodes of infanticide by incoming males, damaging the reproductive success of the females and the past-resident breeding male. Males remaining as subordinates in large groups have the advantage of a potentially rewarding tenure as dominant male, although his time as dominant will probably be shorter than it would be in a smaller group. An effect of group size on female fecundity has been shown at Hato Masaguaral and Hato Piñero. L. E. Miller, who studied Guianan Weeper Capuchins at Hato Piñero, argued that females in larger groups benefit from the group’s ability to commandeer the major fruiting trees in the dry season, and they also spend more time on the ground because of the higher overall vigilance, which is beneficial for their foraging rate when food is scarce. Females in smaller groups have less competition for food within the group but suffer more from a higher predation risk. They spend more time higher in the forest and much less time on the ground than females in larger groups, which is evidently detrimental to their feeding rate. Status and Conservation. CITES Appendix II. Classified as Least Concern on The IUCN Red List. The Chestnut Weeper Capuchin has not been assessed independently. The Guianan Weeper Capuchin is hunted for meat in some areas and is generally less common than the sympatric Guianan Brown Capuchin. The Guianan Weeper Capuchin occurs in numerous large protected areas in the northern Amazon Basin. Bibliography. Bodini (1989), Bodini & Pérez-Hernández (1987), Boubli et al. (2012), De Ruiter (1986), Fernandes et al. (1995), Fragaszy (1986, 1990), Fragaszy, Fedigan & Visalberghi (2004), Fragaszy, Visalberghi et al. (2004), Freese & Oppenheimer (1981), Groves (2001), Hershkovitz (1949, 1955), Miller (1991, 1998a, 1998b, 2002a), Freese & Oppenheimer (1981), Mittermeier & van Roosmalen (1981), Oppenheimer & Oppenheimer (1973), von Pusch (1941), Robinson (1981, 1984a, 1986, 1988a, 1988b), Tate (1939), Valderrama et al. (1990).

21. Ka’apor Capuchin Cebus kaapori 410

French: Sapajou de Ka’apor / German: Ka’apor-Kapuzineraffe / Spanish: Capuchino de Ka’apor Other common names: Kaapori Capuchin

Taxonomy. Cebus kaapori Queiroz, 1992, Quadrant 7·1 km south-west of the ChagaTudo Prospection, Carutapera, near right bank of Rio Gurupí, Maranhão, Brazil (0° 30’ S, 47° 30’ W).

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This species is monotypic. Distribution. NE Brazil (NE Pará and NW Maranhão states); the precise distribution is unknown but is suspected to include an area of at least 15,000 km2 from the Rio Tocantins in Pará to the right bank of the Rio Grajaú in Maranhão. Descriptive notes. Head–body 37–46 cm, tail 40–55 cm; weight 3 kg (males) and 2·4 kg (females). The Ka’apor Capuchin is a gracile/untufted species with a long body compared with other species of Cebus. It is a grayish agouti brown, lighter on flanks. The face, shoulders, mantle, and tip of the tail are silvery-gray, limbs are agouti, and hands and feet are dark brown or black. The crown has a triangular black cap that extends to a dark stripe down the nose. Habitat. Tall lowland terra firma forest below 200 m above sea level. The Ka’apor Capuchin has not been recorded in seasonally inundated forest or secondary forest. In Maranhão, its supposed distribution along the Rio Grajaú indicates that it occurs in babassu palm (Orbignya) forest transitioning to the cerrado (bush savanna) of central Brazil. Food and Feeding. There is so specific information available for this species, but the diet undoubtedly includes fruits, seeds, and insects. Breeding. There is no information available for this species. Activity patterns. There is no information available for this species. Movements, Home range and Social organization. The Ka’apor Capuchin is generally seen in small groups of 1–7 individuals and sometimes with groups of Black Bearded Sakis (Chiropotes satanas). No studies of its behavior and ecology have been published. Status and Conservation. CITES Appendix II. Classified as Critically Endangered on The IUCN Red List. The Ka’apor Capuchin is threatened by habitat loss and hunting. It is restricted to an area believed to be no more than 15,000 km2 in the most densely populated region in the Brazilian Amazon Basin where more than 50% of the forest has been logged, clear-cut, and converted to farmland and pasture. Deforestation continues, and most of the remaining forests now comprise isolated, usually hunted and degraded patches on farmland. There are three indigenous areas in its distribution: Awá Indigenous Area (65,000 ha) and the Indian reservations of Alto Turiaçu (530·5 ha) and Caru (175,000 ha). It is known to occur in two protected areas: Gurupi Biological Reserve and Lago de Tucuruí Environmental Protection Area. A large part of the forest in Gurupi Biological Reserve has been logged and destroyed since its creation in 1988. A study by S. Ferrari and A. Lopes in 1996 found a density of 1 ind/km2 in the Reserve. It would seem that the Ka’apor Capuchin is naturally rare; it is hunted and is susceptible to any, even light, disturbance, or degradation of its habitat. Its rarity may be related to competition with sympatric Guianan Brown Capuchins, and naturally low densities may come from the need for large home ranges. Bibliography. Carvalho (2003), Carvalho et al. (1999), Cunha et al. (2007), Ferrari & Lopes (1996), Ferrari & Queiroz (1994), Groves (2001), Kierulff & de Oliveira (2008), Lopes & Ferrari (1996), Queiroz (1992), Silva (2001), Silva & Cerqueira (1998).

22. Venezuelan Brown Capuchin Cebus brunneus French: Sapajou d’Allen / German: Venezuela-Kapuzineraffe / Spanish: Capuchino de Venezuela Other common names: Brown Weeper Capuchin

Taxonomy. Cebus apella brunneus Allen, 1914, Aroa (Pueblo Nuevo), station on the Bolívar Railway, Yaracuy, north-western Venezuela, elevation 730 feet (222 m). P. Hershkovitz in 1949 considered this form to be a subspecies of C. nigrivittatus (= olivaceus). C. P. Groves placed it as a junior synonym of C. olivaceus. The phylogenetic analysis carried out by J. Boubli and coworkers in 2012, however, found it to be a distinct species most closely related to C. leucocephalus just to the west in extreme western Venezuela and north-eastern Colombia. The form C. albifrons trinitatis named by von Pusch in 1941 from the island of Trinidad is genetically indistinguishable from C. brunneus. Monotypic. Distribution. N Venezuela, E of the Sierra de Perijá and along the Venezuelan Cordillera de la Costa (Coastal Range), also on E & SE of Trinidad I, where possibly introduced (lowland moist forests of the Nariva Swamp, lowland forest E of the Central Range Mountains, and the Trinity Hills Mts). Descriptive notes. Head–body 42 cm, tail 44 cm, from type specimen. No specific data are available for body weight. Pelage of the Venezuelan Brown Capuchin is very thick and long. General color of upperparts of the type specimen is darker along the middle of the back than on the sides; hairs are dusky at their bases, passing gradually through a broad zone of chestnut into blackish with long hazel tips. The face and sides of the head are pale yellowish gray. The crown has a broad V-shaped patch of longish hairs, narrowing to a point in front, from which a narrow black line runs forward to the nose. The chin and lower part of the cheeks are whitish (clear grayish white or fulvous white in different specimens). Underparts are thinly haired, blackish brown, and tips

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Plate 26 Species Accounts

of the hairs are hazel. The throat is lighter than the chest and belly. Upper arms from shoulders to elbows are pale yellowish (maize yellow) to the base of the hairs. Outer forearms have hairs that are blackish for most of their length, with long yellowish tips; inside forearms they are much darker. Hands are blackish. Hindlimbs are nearly like the upperparts but lighter on the outside of thighs. Hindfeet are nearly black. The tail is colored similarly to the back. Habitat. Lowland moist, montane, and submontane forests along the central and eastern Cordillera de la Costa of northern Venezuela and dry semi-deciduous forest and gallery forests in the western Venezuelan Llanos. Food and Feeding. There is no specific information available for this species, but Venezuelan Brown Capuchins on Trinidad have been seen to use leaves as cups to retrieve water from tree cavities. Breeding. There is no information available for this species. Activity patterns. There is no information available for this species. Movements, Home range and Social organization. There is no information available for this species. Status and Conservation. CITES Appendix II. Classified as Least Concern on The IUCN Red List (as C. olivaceus brunneus). The Venezuelan Brown Capuchin is reported to be common. Protected areas within its distribution include Henri Pittier, El Avila, and Peninsula de Paria national parks in Venezuela, and if it is indeed the capuchin on Trinidad, very small populations are found in Bush Bush and Trinity Hills wildlife sanctuaries. Three groups totaling 31 individuals were recorded in Bush Bush and one group of twelve individuals was recorded in Trinity Hills in 1997 surveys. The population on Trinidad is classified as Critically Endangered on The IUCN Red List. Bibliography. Agoramoorthy & Hsu (1995), Allen (1914), Hill (1960), Bodini (1989), Bodini & Pérez-Hernández (1987), Freese & Oppenheimer (1981), Hershkovitz (1949), Linares (1998), Phillips (1998), Phillips & Abercrombie (2003).

23. Sierra de Perijá White-fronted Capuchin Cebus leucocephalus

French: Sapajou à tête blanche / German: Weißkopf-Kapuzineraffe / Spanish: Capuchino de Perijá

Taxonomy. Cebus leucocephalus Gray, 1866, Colombia, restricted by P. Hershkovitz in 1949 to El Tambor, Río Labrija, 25 km north-west of Bucaramanga, Santander, Colombia. The form from the eastern base of the Sierra de Perijá (adustus) is paler, and the limbs are redder, more sharply contrasted with the trunk. Its taxonomic status and distribution are uncertain, however; it may be a variant of the Sierra de Perijá White-fronted Capuchin or may be distinct. Monotypic. Distribution. N Colombia (from the W slope of the Cordillera Oriental in the Santander Department, E through low passes to the Río Zulia and Río Catatumbo basins, Norte de Santander Department) and NW Venezuela (Zulia State). Descriptive notes. Head–body 37–40·7 cm (males), tail 39·2– 49·9 cm (males). No specific measurements are available for females or body weight. The Sierra de Perijá White-fronted Capuchin is the darkest of the white-fronted capuchins. The cap is cinnamon brown to bistre. The back is cinnamon-brown mixed with tawny on the upper back and more russet on the lower back. Flanks are paler (snuff-brown). Upper sides of shoulders and lateral surfaces of upper arms are cinnamon brown. Outer sides of forearms are burnt sienna, grading into auburn. Lateral surfaces of thighs are cinnamon brown, and forelegs and fronts of thighs are burnt sienna. Wrists, ankles, and upper surfaces of hands and feet are auburn. Hairs on the belly and lower part of the chest are burnt sienna, changing to orange-rufous on the upper chest and inner sides of upper arms. The tail is cinnamon brown above, becoming paler toward the tip, and is a paler buffy underneath. Habitat. Lowland moist forest, semi-deciduous dry forest, and mangroves. Food and Feeding. There is no information available for this species. Breeding. There is no information available for this species. Activity patterns. There is no information available for this species. Movements, Home range and Social organization. There is no information available for this species. Status and Conservation. CITES Appendix II. The Sierra de Perijá White-fronted Capuchin has not been assessed on The IUCN Red List. Ciénagas del Catatumbo and Sierra de Perijá national parks in Venezuela and Tamá National Natural Park in Colombia are within its distribution. Bibliography. Defler (2003b, 2004), Freese & Oppenheimer (1981), Hernández-Camacho & Cooper (1976), Hershkovitz (1949), Hill (1960).

Mompós, Bolívar Department, Colombia, elevation c.50 m. Phylogenetic analysis of the white-fronted capuchins carried out by M. Ruiz-García and coworkers in 2010 found pleei and cesarae to be closely related. C. P. Groves placed the forms cesarae and pleei as junior synonyms of C. albifrons versicolor. Monotypic. Distribution. N Colombia, in the Río César Valley, W into S & E slopes of the Sierra Nevada de Santa Marta in the E part of the Magdalena Department, up to 500 m above sea level. Descriptive notes. Head–body 34·8–40·7 cm (males) and 35·3–38·5 cm (females), tail 41·9–49·5 cm (males) and 46·1–50 cm (females). No specific data are available for body weight. The Río Cesar White-fronted Capuchin is the palest of the northern Colombian and Venezuelan white-fronted capuchins. Hairs on sides of the face, superciliary band, chin, throat, sides of neck, and around the ears are cartridge buff. The cap is cinnamon or snuff brown-orangey. Middle of the back, forearms, and forelegs are orangey and contrasted with sides of back and trunk. Hairs of belly and chest are ocherous-orange to pale ocherous-buff and silvery, contrasting with the pale area on the front extending over variable amounts of upper surfaces of shoulders and the inner sides of upper arms. Upper surface of the tail is frosted cinnamon-brown. Habitat. Dry semi-deciduous forest patches and gallery forest and mangroves in a region that is largely deforested. Food and Feeding. There is no information available for this species. Breeding. There is no information available for this species. Activity patterns. There is no information available for this species. Movements, Home range and Social organization. There is no information available for this species. Status and Conservation. CITES Appendix II. Classified as Data Deficient on The IUCN Red List (as C. albifrons cesarae). The Río Cesar White-fronted Capuchin occurs in Ciénaga Grande de Santa Marta and Los Flamencos fauna and flora sanctuaries, and probably also in Macuira National Natural Park. Bibliography. Defler (2003b, 2004), Hernández-Camacho & Cooper (1976), Hershkovitz (1949). Hill (1960), Freese & Oppenheimer (1981).

25. Varied White-fronted Capuchin Cebus versicolor French: Sapajou varié / German: Kolumbien-Kapuzineraffe / Spanish: Capuchino versicolor Other common names: Bogotá Monkey, Varied Capuchin

Taxonomy. Cebus versicolor Pucheran, 1845 Santa Fé de Bogota, Colombia. C. P. Groves in 2001 placed C. albifrons adustus, C. a. cesarae, C. a. malitiosus, C. a. leucocephalus, and C. a. pleei as junior synonyms of C. albifrons versicolor. Monotypic. Distribution. N Colombia in the middle Río Magdalena except for the W slope of the Cordillera Oriental, from the S portion of the Magdalena Department S to the departments of Cundinamarca and Tolima. Descriptive notes. Head–body 45–50·5 cm, tail 42–45·5 cm. No specific data are available for body weight. The Varied White-fronted Capuchin is darker than the Río Cesar White-fronted Capuchin (C. cesarae). It is a rather pale form (extensions of the pale areas being fairly variable), with red tones on the mid-dorsal region and foreparts of limbs, generally contrasting with the rest of the body. Habitat. Lowland moist forest and palm swamps in the middle Río Magdalena Valley. Food and Feeding. There is no information available for this species. Breeding. There is no information available for this species. Activity patterns. There is no information available for this species. Movements, Home range and Social organization. There is no information available for this species. Status and Conservation. CITES Appendix II. Classified as Endangered on The IUCN Red List (as C. albifrons versicolor). The Varied White-fronted Capuchin probably occurs in Catatumbo Barí National Natural Park. Bibliography. Defler (2003b, 2004), Hershkovitz (1949), Hill (1960), Freese & Oppenheimer (1981), Hershkovitz (1949), Hill (1960).

26. Santa Marta White-fronted Capuchin Cebus malitiosus

24. Río Cesar White-fronted Capuchin Cebus cesarae French: Sapajou du Cesar / German: Río-Cesar-Kapuzineraffe / Spanish: Capuchino del César

Taxonomy. Cebus cesarae Hershkovitz, 1949, Río Guaimaral, a channel of the Río César Department of Magdalena, Colombia, elevation 140 m. Includes as a junior synonym the form C. albifrons pleei named by Hershkovitz in 1949, which was described from swamplands of the western bank of the Río Magdalena near the village of Norosi at the base of the northern extremity of the Cordillera Central,

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Taxonomy. Cebus malitiosus Elliot, 1909, vicinity of Bonda, north-west corner of base of Sierra Nevada de Santa Marta, Magdalena, Colombia. This species is monotypic. Distribution. N Colombia, known only from the NW base of Sierra de Santa Marta, but it may range throughout the lower W and N slopes of the Sierra Nevada. Descriptive notes. Head–Body 45·7 cm, tail 43·3 cm. No specific data are available for body weight. The cap of the Santa Marta White-fronted Capuchin is pale brown, and the back is cinnamon brown. Forearms and forelegs are not markedly contrast-

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French: Sapajou des Santa Marta / German: Santa-Marta-Kapuzineraffe / Spanish: Capuchino de Santa Marta

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Plate 26 Species Accounts

ing in color with the back and sides of the body. Hairs on the belly and chest are ocherous tawny to cinnamon brown and silvery. There is a contrasting pale area of the front extending well over upper surfaces of the shoulders and inner sides of upper arms. Habitat. Lowland, submontane, and montane forest. Food and Feeding. There is no information available for this species. Breeding. There is no information available for this species. Activity patterns. There is no information available for this species. Movements, Home range and Social organization. There is no information available for this species. Status and Conservation. CITES Appendix II. Classified as Endangered on The IUCN Red List (as C. albifrons malitiosus). The Santa Marta White-fronted Capuchin occurs in Sierra Nevada de Santa Marta and Tayrona national natural parks. Bibliography. Defler (2003b, 2004), Hernández-Camacho & Cooper (1976), Hershkovitz (1949).

27. Ecuadorian White-fronted Capuchin Cebus aequatorialis French: Sapajou d’Équateur / German: Ecuador-Kapuzineraffe / Spanish: Capuchino ecuatoriano

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Other common names: Ecuadorian Capuchin, Equatorial Capuchin

Taxonomy. Cebus aequatorialis J. A. Allen, 1914, Río del Oro, Manaví Province, near sea level, Ecuador. This species is monotypic. Distribution. Ecuador lowlands W of the Andes (from the Río Esmeraldas-Guayllabamba to the S) and NW Peru (Tumbes Department, the southernmost locality is the Cerros de Amotape National Park). Descriptive notes. Head–body 35–51 cm, tail 40–50 cm; weight 1·7–3·6 kg (males) and 1·2–2·2 kg (females). The upperparts of the Ecuadorian White-fronted Capuchin, from the nape over the back, are pale cinnamon rufous, darker along the midline of the back. Front and sides of the head are a pale yellowish white, with a narrow black transverse line on the forehead forming the cap, from which a narrow median black line descends to the nose. An indistinct blackish line runs from the posterior border of the eye to the mouth. Outsides of limbs are similar in color to the body. Hands and feet are a little darker (more brownish) than the arms and legs, and the ventral surface is a little paler than flanks. The chest is lighter than the belly. Dorsal surface of the tail is dull wood-brown above, darker than the body, and undersurface of tail is much paler. Habitat. Dry forest in lowlands and including coastal areas to wet submontane Andean forest to elevations of 1100–2040 m. The Ecuadorian White-fronted Capuchin evidently prefers tall, mature terra firma forest but also uses disturbed and degraded mixed secondary forest and cultivated areas. Food and Feeding. Ecuadorian White-fronted Capuchins eat fruits, insects, and other small animals. They eat tender bases of bromeliad leaves and fruits of Vitex gigantea (Lamiaceae), Spondias (Anacardiaceae), Eugenia (Myrtaceae), Ficus (Moraceae), and Cecropia (Urticaceae). Breeding. There is no information available for this species. Activity patterns. There is no information available for this species. Movements, Home range and Social organization. Surveys of the Ecuadorian Whitefronted Capuchin in 2002–2005 in western Ecuador, located eleven groups in five of eleven sites visited. three in the Cerro Blanco Forest Reserve, four in the Hacienda El Paraíso, two in Jauneche Biological Reserve Station, one in La Hesperia Biological Reserve and one in Lalo Loor Dry Forest Reserve. The groups ranged in size from five to 20 individuals (mean 13·9). There were generally more females in the group than males; the sex ratio was 0·8 male:1 female. The composition of six of the groups was: 1–6 adult males, 3–5 adult females, 2–4 subadult males, 2–6 juveniles, and 1–2 infants. Densities were 2–22 ind/km2, with a median of 2·4 ind/km2. Two groups in the Cerro Blanco Protected Forest had home ranges of 561 ha and 507 ha. Status and Conservation. CITES Appendix I. Classified as Critically Endangered on The IUCN Red List (as C. albifrons aequatorialis). Forests in the western lowlands of Ecuador have been devastated over the last century, and the Ecuadorian White-fronted Capuchin is hunted and, in some areas, persecuted for crop-raiding (banana, corn, plantains, and cacao). It is known from 20 forests in Ecuador and Peru. It occurs in Bilsa Biological Station in Mache-Chindul National Park, Manglares Churute National Park, Cerro Blanco Forest Reserve, La Hesperia Biological Reserve, and Lalo Loor Dry Forest Reserve in Ecuador; and Cerros de Amotape National Park and Tumbes National Reserve in Peru. Hunting and deforestation continue, however, even in protected areas. Reports that it occurred in Cotacachi-Cayapas Ecological Reserve, north of the Río Esmeraldas-Guayllabamba in Ecuador, are, it seems, unfounded, and it is believed that it disappeared from a 4000-ha forest at Cabo Pasado, also in Ecuador, in 1998. Bibliography. Albuja & Arcos (2007), Allen (1914), Encarnación & Cook (1998), Freese & Oppenheimer (1981), Hershkovitz (1949), Hill (1960), Jack & Campos (2012), Parker & Carr (1992), Tirira (2007).

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28. Colombian White-faced Capuchin Cebus capucinus French: Sapajou capucin / German: Weißschulter-Kapuzineraffe / Spanish: Capuchino de cara blanca de Colombia Other common names: White-headed Capuchin, White-throated Capuchin; Colombian White-faced Capuchin (capucinus), Gorgona White-faced/White-throated Capuchin (curtus)

Taxonomy. Simia capucina Linnaeus, 1758, Colombia. Restricted by E. A. Goldman in 1914 to northern Colombia. Intermediates between C. capucinus and C. albifrons occur in the middle San Jorge Valley, lower Río Cauca, Colombia. Two subspecies recognized. Subspecies and Distribution. C. c. capucinus Linnaeus, 1758 – E Panama, W Colombia (Pacific coastal region), and NW Ecuador (S as far as the Río Esmeraldas-Guayllabamba). C. c. curtus Bangs, 1905 – Gorgona I, Colombia. Descriptive notes. Head–body 33–45 cm, tail 35–55 cm; weight 3–4 kg (males) and 1·5–3 kg (females). Male Colombian White-faced Capuchins are c.27% larger than females. They are relatively slender in build. The body, crown, limbs, and tail are black. The chest is white, extending forward to the face and front of the crown and upward to the shoulders and upper arms. The hairs on the cap form a distinctive black “V” shape. Longer forehead and crown hairs on older individuals may form a ruff, and the white area on the forehead tends to become thinly haired or even somewhat bald with age. The “Colombian White-faced Capuchin” (C. c. capucinus) is black with white or yellowish-white on the face, front of the crown, throat, and shoulders. The “Gorgona Whitefaced Capuchin” (C. c. curtus) is a small and relatively short-tailed insular subspecies. Habitat. Variety of habitats, preferring terra firma primary forest or older secondary forest, but also occurs in seasonally inundated forests, remnant degraded forest patches with Scheelea magdalenica palms (food and sleeping sites), mangroves, and deciduous dry forest in both lowland and montane areas. On the western slopes of the Andes, Colombian White-faced Capuchins occur up to elevations of 1800–2100 m. They prefer the canopy but use all levels of the forest, and go to the ground. Food and Feeding. The Colombian White-faced Capuchin eats mainly ripe fruits and insects, but also leaves, flowers, and bird eggs. The Gorgona White-faced Capuchin eats oysters, which they open by banging them with stones. They catch and eat crabs at low tide and raid corn crops. Breeding. Female Colombian White-faced Capuchins give birth to a single young every two years. Gestation is 157–167 days. Births may occur at any time of the year but reach a peak in December–April. They have been known to live over 40 years. Activity patterns. There is no information available for this species. Movements, Home range and Social organization. Group sizes of Colombian Whitefaced Capuchins are 6–24 individuals. There have been no studies in the wild, and the large majority of what is known about white-headed capuchins comes from studies of populations in Central America. Until recently, these were considered to be synonymous with the Colombian White-faced Capuchin, but they are now classified as the Panamanian White-faced Capuchin (C. imitator). There is no doubt, however, that ecological and behavioral aspects of the Colombian White-faced Capuchin will be broadly similar to, or the same as, those of the well-known Panamanian White-faced Capuchin. Status and Conservation. CITES Appendix II. Classified as Least Concern on The IUCN Red List, with the Gorgona White-faced Capuchin classified as Vulnerable. The Colombian White-faced Capuchin is hunted and trapped in some areas as a crop pest. Many populations are threatened by deforestation. The nominate subspecies, the Colombian White-headed Capuchin, occurs in Chagres, Darién, and Portobelo national parks in Panama, Cotacachi-Cayapas Ecological Reserve and Los Cedros Protected Forest in Ecuador, and Ensenada de Utría, Farallones de Cali, and Los Katios national natural parks in Colombia. The Gorgona White-faced Capuchin occurs in Gorgona National Natural Park. Bibliography. Boubli et al. (2012), Defler (2003b, 2004), Freese & Oppenheimer (1981), Hernández-Camacho & Cooper (1976), Hill (1960), Jack (2011), Ruiz-García, Castillo et al. (2010), Rylands et al. (2006), Tirira (2007).

29. Panamanian White-faced Capuchin Cebus imitator French: Sapajou du Panama / German: Panama-Kapuzineraffe / Spanish: Capuchino de cara blanca de Panamá Other common names: White-headed Capuchin, White-throated Capuchin

Taxonomy. Cebus imitator Thomas, 1903, Chiriquí, Boquete, Panamá, elevation 1350 m. Abundant scientific literature on this species refers to it as C. capucinus. In his 1949 review of the Colombian capuchins, P. Hershkovitz listed the form limitaneus from the eastern border between Honduras and Nicaragua. It was also recognized by W. C. O. Hill in 1960 and E. R. Hall in 1981. It was believed to be a smaller race than imitator with a smaller skull. Hershkovitz was not convinced that it was a separate taxon, and J. Boubli and M. Ruiz-García and their coworkers independently concluded that it was genetically indistinguishable from C. imitator and, having been described

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Plate 26 Species Accounts

ing, playing, and engaging in other activities. In dry forest at Santa Rosa National Park, Costa Rica, foraging takes up more time (41%), traveling less (37%), and resting more (21%), with very little time in social activities. In the wet season, Panamanian Whitefaced Capuchins spend about the same amount of time foraging for plant foods (21%) as they do for animal prey (22%), but in the dry season, foraging for plant food takes up 26% of the day and animal prey 10·5%. They often go to the ground to forage, drink water, or move between patches of trees. They sleep at the ends of the branches in large tall trees. Groups generally do not sleep in the same site on consecutive nights. Movements, Home range and Social organization. Group sizes of Panamanian Whitefaced Capuchins average c.16, and adult sex ratios of c.0·7 male:1 female. During five years, a group studied by J. Oppenheimer on Barro Colorado Island had 1–3 adult males and 5–7 adult females. Their home range was 164 ha, with a core area of 87·8 ha where most of their time was spent. Home ranges, but not core areas, overlap, and when groups (infrequently) meet, there are aggressive displays, particularly by males. Females typically remain in their natal group and males disperse. Females and males form independent dominance hierarchies, and the alpha female is subordinate only to the alpha male. She dominates subordinate males. Females form coalitions and together they can displace the alpha male at disputed food sources. Females tend to threaten males more than females, and they receive fewer threats than they give. Males do not form all-male groups, and when males move into another group and displace resident males, it is quite rapid and generally violent, sometimes involving fatalities. Males may transfer between groups several times in their lifetimes, either singly or in coalitions of as many as two other males that are sometimes siblings. Overall, 67–80% of all emigrations involve parallel dispersal (two or more males transferring groups together). Dispersals of these coalitions are robust, and a coalition can last for several transfers; residency of coalitions in any one group is longer than individually dispersing males. Sometimes males transfer to a new group peacefully and unobtrusively, without contesting the existing male hierarchy, but when they are aggressive and involve the replacement of the alpha male, they are associated with the wounding, death, and disappearance of infants. Most male takeovers of groups occur during the dry season, and c.82% of the infants that are less than one year old die (average age of death is 4·4 months) after the takeover. In years when there is no male takeover, c.2% of infants die. Males spend more time scanning the environment than females, but they are less concerned with predators than they are with detecting takeover threats from outside males and with monitoring males in their own group. Unlike other capuchins, Panamanian White-faced Capuchins rarely associate with squirrel monkeys (Saimiri) where they are sympatric (e.g. Corcovado National Park, Costa Rica). This is probably because squirrel monkeys would gain little from increased predator detection by the capuchins, and the particularly predaceous capuchins would interfere with the squirrel monkeys’ foraging. Predators include snakes (Boa constrictor), large cats (Panthera onca, Puma concolor), small cats (Puma yaguaroundi and possibly Leopardus pardalis and L. wiedii), Tayra (Eira barbara), Coyotes (Canis latrans), spectacled caimans (Caiman crocodilus), and raptors, including the great black hawk (Buteogallus urubitinga). Panamanian White-faced Capuchins give alarm calls that are specific to aerial and terrestrial predators. When detected close, terrestrial predators are mobbed and chased. Status and Conservation. CITES Appendix II. Classified as Least Concern on The IUCN Red List (as C. capucinus imitator). The Panamanian White-faced Capuchin occurs in numerous protected areas: La Amistad International Park (Panama/Costa Rica), Braulio Carillo, Chirripó, Corcovado, Guanacaste, Palo Verde, Piedras Blancas, Rincón de la Vieja, Santa Rosa, Tortuguero, and Volcán Poas national parks, Lomas Barbudal Biological Reserve, and Cabo Blanco Strict Nature Reserve in Costa Rica; Cerro Hoya, Coiba Island, Soberanía, Altos de Campaña, Soberanía, Omar Torrijos Herrera-El Copé, and Volcán Barú national parks and Barro Colorado National Monument in Panama; and Pico Bonito, Jeanette Kawas, Cusuco, Montaña de Yoro, Sierra de Agalta, and Punta Izopo national parks in Honduras. Bibliography. Boubli et al. (2012), Defler (2003b, 2004), Fedigan (2003), Fedigan & Jack (2004), Fedigan & Rose (1995), Fragaszy, Fedigan & Visalberghi (2004), Fragaszy, Visalberghi et al. (2004), Freese (1977), Freese & Oppenheimer (1981), Gros-Louis (2002), Gros-Louis et al. (2003), Hall (1981), Hershkovitz (1949), Hill (1960), Jack (2011), Jack & Fedigan (2004a, 2004b), Manson et al. (1999), Matamoros & Seal (2001), Milton & Mittermeier (1977), Newcomer & de Farcy (1985), Oppenheimer (1968, 1973, 1982), Panger et al. (2002), Perry, (1996), Perry & Rose (1994), Rose & Fedigan (1995), Rose et al. (2003), Ruiz-García et al. (2012), Rylands et al. (2006), Silva-López et al. (1995), Thomas (1903).

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in 1914, is a junior synonym. Individuals from Honduras have frosted yellow on their inner thighs. Monotypic. Distribution. N Honduras, C & W Nicaragua, Costa Rica, and W Panama (including Coiba and Jicarón Is); reports of capuchins in the Mayan Mountains of W Belize (Chiquebul forest and in the region of the Trio and Bladen branches of the Monkey River), Sarstoon National Park on the S border, and in the Sierra del Espíritu Santo near the Honduras border have not been confirmed. Descriptive notes. Head–body 34·3–42 cm (males) and 38·5–40·5 cm (females), tail 44–46 cm (males) and 43–45 cm (females); weight 3·7–3·9 kg (males) and 2·6–2·7 kg (females). Male Panamanian White-faced Capuchins are c.27% larger than females. The Panamanian White-faced Capuchin resembles the typical Colombian White-faced Capuchin (C. c. capucinus), but females have elongated frontal tufts with hairs c.40 mm long, with a brownish tinge contrasting with the white of the cheeks and throat, entirely altering the facial appearance. Habitat. Lowland, submontane, and montane moist forests from sea level to 1500 m and mosaics of tropical dry forest patches and gallery forest in different stages of regeneration, with severe dry seasons and annual rainfall less than 1700 mm. On the Caribbean coast, annual rainfall can exceed 5000 mm. Panamanian White-faced Capuchin enter mangrove swamps. Food and Feeding. Diet of the Panamanian White-faced Capuchin includes fruits, insects, snails, crabs, clams, slugs, frogs, lizards (Anolis and Ctenosaura), nestling and adult birds, nestling and adult Variegated Squirrels (Sciurus variegatoides), White-nosed Coati pups (Nasua narica), and tree rats. Predation on coati pups occurs in April–May when coatis are breeding. When coati nests are defended, Panamanian White-faced Capuchins cooperate, with some individuals baiting and distracting adult coatis and others grabbing pups. They also eat eggs of various birds, including curassows, guans, magpie jays, nightjars, tinamous, woodpeckers, wrens, herons, and wood ducks. Flowers, leaves, flower and leaf buds, stems and roots, and nectar are also eaten. When foraging for animal prey, Panamanian White-faced Capuchins extensively search leaf litter, the underside of leaves, curled leaves, rotten wood, dead leaves, fallen branches, and open hollow vines and thorns. On Barro Colorado Island, Panama, fruits are least abundant in November–February, and they eat more apical meristems and succulent bases of new shoots. Panamanian White-faced Capuchins especially like to eat larvae and nymphs of beetles, butterflies, moths and spittlebugs, and they attack ant and wasp nests. They rub larvae against branches to remove spines or poisonous hairs, and sometimes they also wrap them in a leaf before rubbing them. Individuals that capture larger prey are only minimally harassed for a share by other group members that are content with bits dropped or abandoned. Panamanian White-faced Capuchins drink water, often from tree holes. Water sources in the dry season can be rare, and daily access to them restricts their movements. Sometimes more than one group uses the same pool to drink, causing tense meetings between groups. Breeding. When courting, female Panamanian White-faced Capuchins do not raise their eyebrows and grimace as do female Sapajus. Instead, they make a so-called “duckface” with lips protruded while looking at their prospective partner. They also have a courtship dance. Pairs pirouette and face away, and then look at each other (mutual gazing) over their shoulders or through their legs. There is a specific call given at this time. Females court and mate throughout the year and in all reproductive states, even when pregnant. Males frequently sniff females’ urine and are more likely to respond when a female is close to ovulating. Females mate with the alpha males more than with subordinates and do so more when fertile. They mate with subordinate males more when they are infertile. Births of Panamanian White-faced Capuchins occur throughout the year but are more common in the dry season. All group males mate but most infants are sired by the alpha male (63–84%). Average interbirth interval for females that have successfully raised their offspring is 27·5 months. If an infant dies (not in the context of a male takeover), interbirth interval drops to 12·3 months. When an infant dies during or after a male takeover, interbirth interval is a little longer at c.15·7 months. Females first give birth at about seven years old and males reach reproductive maturity at about ten years. In captivity, they have been known to live for nearly 55 years. Activity patterns. Panamanian White-faced Capuchins are active most of the day, starting at or a little before dawn, and rest for a while at midday. Groups in humid (but seasonal) forests of Barro Colorado Island have a general daily pattern of 28% foraging (looking for, handling, and eating food), 47% traveling, 14% resting, and 11% groom-

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