Mammals of Africa Volume II: Primates 9781408122525, 9781472926920, 9781408189917

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mammals of africa volume II primates

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Series Editors Jonathan Kingdon Department of Zoology, University of Oxford David C. D. Happold Research School of Biology, Australian National University Thomas M. Butynski Zoological Society of London/King Khalid Wildlife Research Centre, Saudi Wildlife Authority Michael Hoffmann International Union for Conservation of Nature – Species Survival Commission Meredith Happold Research School of Biology, Australian National University Jan Kalina Soita Nyiro Conservancy, Kenya

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mammals of africa volume II primates edited by thomas m. butynski, jonathan kingdon and jan kalina

Illustrated by Jonathan Kingdon

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Dedication This volume is dedicated to Carly and Jake Butynski, the children of Jan Kalina and Tom Butynski.

First published in 2013 Copyright © 2013 by Bloomsbury Publishing Copyright © 2013 illustrations by Jonathan Kingdon All rights reserved. No part of this publication may be reproduced or used in any form or by any means – photographic, electronic or mechanical, including photocopying, recording, taping or information storage or retrieval systems – without permission of the publishers. Bloomsbury Publishing Plc, 50 Bedford Square, London WC1B 3DP Bloomsbury USA, 175 Fifth Avenue, New York, NY 10010 www.bloomsbury.com www.bloomsburyusa.com Bloomsbury Publishing, London, New Delhi, New York and Sydney A CIP catalogue record for this book is available from the British Library. Library of Congress Cataloging-in-Publication Data has been applied for. Commissioning editor: Nigel Redman Design and project management: D & N Publishing, Baydon, Wiltshire ISBN (print) 978-1-4081-2252-5 ISBN (epdf) 978-1-4081-8991-7 Printed in China by C&C Offset Printing Co., Ltd This book is produced using paper that is made from wood grown in managed sustainable forests. It is natural, renewable and recyclable. The logging and manufacturing processes conform to the environmental regulation of the country of origin. 10 9 8 7 6 5 4 3 2 1

Recommended citations: Series: Kingdon, J., Happold, D., Butynski, T., Hoffmann, M., Happold, M. & Kalina, J. (eds) 2013. Mammals of Africa (6 vols). Bloomsbury Publishing, London. Volume: Butynski, T. M., Kingdon, J. & Kalina, J. (eds) 2013. Mammals of Africa.Volume II: Primates. Bloomsbury Publishing, London. Chapter/species profile: e.g. Williamson, E. A. & Butynski, T. M. 2013. Gorilla gorilla Western Gorilla; pp 39–45 in Butynski, T., Kingdon, J. & Kalina, J. (eds) 2013. Mammals of Africa:Volume II: Primates. Bloomsbury Publishing, London.

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Donors and Patrons T. R. B. Davenport, D. De Luca and the Wildlife Conservation Society, Tanzania R. Dawkins R. Farrand & L. Snook R. Heyworth, S. Pullen and the Cotswold Wildlife Park G. Ohrstrom Viscount Ridley & M. Ridley L. Scott and the Smithsonian UK Charitable Trust M. & L. Ward R. & M. Ward

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Contents Series Acknowledgements10 Acknowledgements for Volume II11

Pan paniscus Gracile Chimpanzee (Bonobo, Pygmy Chimpanzee) – G. E. Reinartz, E. J. Ingmanson & H. Vervaecke

64

TRIBE HOMININI Hominins – J. Kingdon & C. P. Groves

70

Mammals of Africa: An Introduction and Guide – David Happold, Michael Hoffmann, Thomas Butynski & Jonathan Kingdon

13

Genus Homo Humans – J. Kingdon Homo sapiens Modern Human – J. Kingdon

74 76

SUPERCOHORT SUPRAPRIMATES (EUARCHONTOGLIRES) – J. Kingdon

21

SUPERFAMILY CERCOPITHECOIDEA Cercopithecoids: Old World Monkeys – J. Kingdon & C. P. Groves

90

COHORT EUARCHONTA – J. Kingdon

22

SUPERORDER PRIMATOMORPHA – J. Kingdon

23

FAMILY CERCOPITHECIDAE Cercopithecids: Old World Monkeys – C. P. Groves & J. Kingdon

92

ORDER PRIMATES Primates – J. Kingdon & C. P. Groves

24

SUBFAMILY COLOBINAE Colobines: Colobus Monkeys – J. Kingdon & C. P. Groves

93

SUBORDER HAPLORRHINI Haplorrhines: Tarsiers, Monkeys, Apes, Humans – J. Kingdon & C. P. Groves

29

HYPORDER ANTHROPOIDEA (INFRAORDER SIMIIFORMES) Anthropoids: Monkeys, Apes, Humans – J. Kingdon & C. P. Groves

30

PARVORDER CATARRHINI Catarrhines: Old World Monkeys, Apes, Humans – C. P. Groves

31

SUPERFAMILY HOMINOIDEA Anthropoids: Apes, Humans – C. P. Groves & J. Kingdon

31

FAMILY HOMINIDAE Hominids: Great Apes, Humans – C. P. Groves & J. Kingdon

32

Genus Colobus Black-and-white Colobus Monkeys – J. Kingdon & C. P. Groves 95 Colobus satanas Black Colobus – M.-C. Fleury & D. Brugière  97 Colobus polykomos King Colobus (Western Pied Colobus, Western Black-and-white Colobus) – A. H. Korstjens & A. Galat-Luong 100 Colobus angolensis Angola Colobus (Angola Black-andwhite Colobus, Angola Pied Colobus) – C. M. Bocian & J. Anderson 103 Colobus vellerosus White-thighed Colobus (Geoffroy’s Pied Colobus, Ursine Colobus) – T. L. Saj & P. Sicotte 109 Colobus guereza Guereza Colobus (Black-and-white Colobus, Abyssinian Colobus) – P. J. Fashing & J. F. Oates 111

SUBFAMILY HOMININAE Hominins: African Great Apes, Humans – C. P. Groves & J. Kingdon

33

Genus Procolobus Olive Colobus Monkey, Red Colobus Monkeys – P. Grubb, T. T. Struhsaker & K. S. Siex

TRIBE GORILLINI Gorillas – C. P. Groves

35

Genus Gorilla Gorillas – C. P. Groves Gorilla gorilla Western Gorilla – E. A. Williamson & T. M. Butynski Gorilla beringei Eastern Gorilla – E. A. Williamson & T. M. Butynski

35

TRIBE PANINI Chimpanzees – C. P. Groves

53

Genus Pan Chimpanzees – C. P. Groves & J. Kingdon Pan troglodytes Robust Chimpanzee (Common Chimpanzee) – M. E. Thompson & R. W. Wrangham

53

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SUBGENUS Procolobus Olive Colobus Monkey – P. Grubb & C. P. Groves Procolobus verus Olive Colobus (Van Beneden’s Colobus) – J. F. Oates & A. H. Korstjens

120 121 121

39 45

55

SUBGENUS Piliocolobus Red Colobus Monkeys – P. Grubb, T. T. Struhsaker & K. S. Siex Procolobus badius Western Red Colobus (Bay Colobus) – T. M. Butynski, P. Grubb & J. Kingdon Procolobus preussi Preuss’s Red Colobus – T. M. Butynski & J. Kingdon Procolobus pennantii Pennant’s Red Colobus (Bioko Red Colobus) – T. M. Butynski, P. Grubb & J. Kingdon Procolobus rufomitratus Eastern Red Colobus – T. T. Struhsaker & P. Grubb

125 128 134 137 142

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Contents

Procolobus gordonorum Udzungwa Red Colobus (Iringa / Uhehe / Gordon’s Red Colobus) – T. T. Struhsaker, P. Grubb & K. S. Siex Procolobus kirkii Zanzibar Red Colobus (Kirk’s Red Colobus) – K. S. Siex & T. T. Struhsaker

Papio anubis Olive Baboon (Anubis Baboon) – R. A. Palombit 151

SUBFAMILY CERCOPITHECINAE Cercopithecines: Cheek-pouched Monkeys – J. Kingdon & C. P. Groves

155

TRIBE PAPIONINI Papionins: Macaques, Drill-mangabeys, Mandrills, Baboon-mangabeys, Kipunji, Baboons, Gelada – C. J. Jolly

157

Genus Macaca Macaques – C. P. Groves & J. Kingdon Macaca sylvanus Barbary Macaque (Barbary Ape) – J. E. Fa

159 159

Genus Cercocebus Drill-mangabeys (White-eyelid Mangabeys) – J. Kingdon & C. P. Groves Cercocebus galeritus Tana River Mangabey – J. A. Wieczkowski & T. M. Butynski Cercocebus agilis Agile Mangabey – N. F. Shah Cercocebus chrysogaster Golden-bellied Mangabey – C. L. Ehardt & T. M. Butynski Cercocebus sanjei Sanje Mangabey – C. L. Ehardt & T. M. Butynski Cercocebus atys Sooty Mangabey (Smoky Mangabey) – W. S. McGraw Cercocebus lunulatus White-naped Mangabey (Whitecrowned Mangabey) – T. M. Butynski Cercocebus torquatus Red-capped Mangabey (Whitecollared Mangabey) – C. L. Ehardt Genus Mandrillus Mandrills – J. Kingdon & C. P. Groves Mandrillus sphinx Mandrill – K. Abernethy & L. J. T. White Mandrillus leucophaeus Drill – C. D. Schaaf, E. L. Gadsby & T. M. Butynski Genus Lophocebus Baboon-mangabeys (Grey-cheeked Mangabeys, Black Mangabeys) – C. P. Groves & T. M. Butynski Lophocebus albigena (also L. osmani, L. johnstoni, L. ugandae) Grey-cheeked Mangabey – W. Olupot & P. M. Waser Lophocebus aterrimus (also L. opdenboschi) Black Mangabey – A. Gautier-Hion

233

148

165 167 170 174 177 180

Genus Theropithecus Gelada – C. J. Jolly Theropithecus gelada Gelada (Gelada Baboon) – T. J. Bergman & J. C. Beehner TRIBE CERCOPITHECINI Cercopithecins: Guenons (Allen’s Swamp Monkey, Talapoin Monkeys, Patas Monkey, Savanna Monkeys, Mountain Monkeys, Arboreal Guenons) – J. Kingdon & C. P. Groves Genus Allenopithecus Allen’s Swamp Monkey – C. P. Groves & J. Kingdon Allenopithecus nigroviridis Allen’s Swamp Monkey – A. Gautier-Hion Genus Miopithecus Talapoin Monkeys – J. Kingdon & C. P. Groves Miopithecus talapoin Southern Talapoin Monkey (Angolan Talapoin Monkey) – A. Gautier-Hion Miopithecus ogouensis Northern Talapoin Monkey (Gabon Talapoin Monkey) – A. Gautier-Hion Genus Erythrocebus Patas Monkey – C. P. Groves & J. Kingdon Erythrocebus patas Patas Monkey (Hussar Monkey, Nisnas) – L. A. Isbell

239 240

245 248 248 251 252 253 256 257

182 186 190 192 197

204

Genus Chlorocebus Savanna Monkeys – C. P. Groves & J. Kingdon Chlorocebus aethiops Grivet Monkey – T. M. Butynski & J. Kingdon Chlorocebus tantalus Tantalus Monkey – N. Nakagawa Chlorocebus sabaeus Green Monkey (Callithrix) – G. Galat & A. Galat-Luong Chlorocebus pygerythrus Vervet Monkey – L. A. Isbell & K. L. Enstam Jaffe Chlorocebus cynosuros Malbrouck Monkey – E. E. Sarmiento Chlorocebus djamdjamensis Djam-djam Monkey (Bale Monkey) – T. M. Butynski, A. Atickem & Y. A. de Jong

264 267 271 274 277 284 287

206 210

Genus Rungwecebus Kipunji – T. R. B. Davenport Rungwecebus kipunji Kipunji – T. R. B. Davenport & T. M. Butynski

211

Genus Papio Baboons – C. J. Jolly Papio papio Guinea Baboon – A. Galat-Luong & G. Galat Papio hamadryas Hamadryas Baboon (Sacred Baboon) – L. Swedell Papio ursinus Chacma Baboon – G. Cowlishaw Papio cynocephalus Yellow Baboon – J. Altmann, S. L. Combes & S. C. Alberts

217 218

213

221 225 228

Genus Allochrocebus Mountain Monkeys – J. Kingdon & C. P. Groves Allochrocebus preussi Preuss’s Monkey – T. M. Butynski Allochrocebus lhoesti L’Hoest’s Monkey – E. E. Sarmiento Allochrocebus solatus Sun-tailed Monkey – J.-P. Gautier & D. Brugière  Genus Cercopithecus Arboreal Guenons – J. Kingdon & C. P. Groves Cercopithecus dryas Dryad Monkey (Salongo Monkey) – T. M. Butynski Cercopithecus (diana) Group, Diana Monkeys Group – C. P. Groves & J. Kingdon

290 292 296 300 303 306 309 7

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Contents

Cercopithecus diana Diana Monkey – C. M. Hill & J. F. Oates 310 Cercopithecus roloway Roloway Monkey – S. H. Curtin 313

SUBFAMILY PERODICTICINAE African Lorisids: Potto, Angwantibos (Golden Pottos) – T. M. Butynski

392

Cercopithecus neglectus De Brazza’s Monkey – A. Gautier-Hion 315

Genus Perodicticus Potto – T. M. Butynski Perodicticus potto Potto – E. R. Pimley & S. K. Bearder

393 393

Cercopithecus (mona) Group, Mona Monkeys Group – J. Kingdon & C. P. Groves Cercopithecus mona Mona Monkey – M. E. Glenn, K. J. Bensen & R. M. Goodwin Cercopithecus lowei Lowe’s Monkey – A. Galat-Luong, G. Galat, M. E. Glenn & W. S. McGraw Cercopithecus campbelli Campbell’s Monkey – G. Galat, A. Galat-Luong, M. E. Glenn & W. S. McGraw Cercopithecus denti Dent’s Monkey – E. E. Sarmiento & J. Kingdon Cercopithecus wolfi Wolf’s Monkey – A. Gautier-Hion Cercopithecus pogonias Crowned Monkey – A. Gautier-Hion Cercopithecus hamlyni Owl-faced Monkey (Hamlyn’s Monkey) – J. A. Hart, T. M. Butynski, E. E. Sarmiento & Y. A. de Jong Cercopithecus (nictitans) Group, Nictitans Monkeys Group – J. Kingdon Cercopithecus nictitans Putty-nosed Monkey (Greater Spotnosed Monkey) – A. Gautier-Hion Cercopithecus mitis Gentle Monkey (Diademed Monkey, Blue Monkey, Sykes’s Monkey) – M. J. Lawes, M. Cords & C. Lehn Cercopithecus (cephus) Group, Cephus Monkeys Group – J. Kingdon Cercopithecus cephus Moustached Monkey – A. Gautier-Hion Cercopithecus sclateri Sclater’s Monkey – J. F. Oates & L. R. Baker Cercopithecus erythrotis Red-eared Monkey (Red-nosed Monkey) – T. M. Butynski & J. Kingdon Cercopithecus ascanius Red-tailed Monkey – M. Cords & E. E. Sarmiento Cercopithecus petaurista Lesser Spot-nosed Monkey – W. S. McGraw, A. Galat-Luong & G. Galat Cercopithecus erythrogaster White-throated Monkey (Redbellied Monkey) – J. F. Oates SUBORDER STREPSIRRHINI Strepsirrhines: Lemurs, Lorises, Pottos, Galagos – J. Kingdon & C. P. Groves

319 322 325

Genus Arctocebus Angwantibos (Golden Pottos) – C. P. Groves & J. Kingdon Arctocebus calabarensis Calabar Angwantibo (Northern Golden Potto) – J. F. Oates & L. Ambrose Arctocebus aureus Golden Angwantibo (Southern Golden Potto) – L. Ambrose

399 400 402

328 330 333 335

339 344 350 354

FAMILY GALAGIDAE Galagids: Galagos (Bushbabies) – S. K. Bearder & J. Masters Genus Otolemur Greater Galagos – S. K. Bearder Otolemur crassicaudatus Large-eared Greater Galago (Thick-tailed Greater Galago / Bushbaby) – S. K. Bearder & N. S. Svoboda Otolemur garnettii Small-eared Greater Galago (Garnett’s Galago / Bushbaby) – C. S. Harcourt & A. W. Perkin Genus Sciurocheirus Squirrel Galagos – C. P. Groves & J. Kingdon Sciurocheirus alleni Allen’s Squirrel Galago – L. Ambrose & E. R. Pimley Sciurocheirus makandensis sp. nov. Makandé Squirrel Galago – L. Ambrose Sciurocheirus gabonensis Gabon Squirrel Galago – L. Ambrose

404 407 409 413 417 418 421 422

363 366 369 371 375 381

Genus Galago Lesser Galagos – J. Kingdon Galago senegalensis Northern Lesser Galago (Senegal Lesser Galago, Senegal Lesser Bushbaby) – L. T. Nash, E. Zimmermann & T. M. Butynski Galago moholi Southern Lesser Galago (South African Lesser Galago) – S. Pullen & S. K. Bearder Galago gallarum Somali Lesser Galago (Somali Bushbaby) – T. M. Butynski & Y. A. de Jong Galago matschiei Spectacled Lesser Galago (Eastern Needle-clawed Galago) – T. M. Butynski & Y. A. de Jong

424 425 430 434 437

384 387

INFRAORDER LORISIFORMES Lorisiforms: Lorises, Pottos, Galagos – C. P. Groves & J. Kingdon

390

SUPERFAMILY LORISOIDEA Lorisoids: Lorises, Pottos, Galagos – C. P. Groves

390

FAMILY LORISIDAE Lorisids: Lorises, Potto, Angwantibos – C. P. Groves & T. M. Butynski

391

Genus Euoticus Needle-clawed Galagos – J. Kingdon & C. P. Groves Euoticus elegantulus Southern Needle-clawed Galago (Elegant Galago) – L. Ambrose Euoticus pallidus Northern Needle-clawed Galago (Pallid Galago) – L. Ambrose & J. F. Oates Genus Galagoides Dwarf Galagos – P. E. Honess & S. K. Bearder Galagoides zanzibaricus Zanzibar Dwarf Galago – P. E. Honess, A. W. Perkin & T. M. Butynski Galagoides rondoensis Rondo Dwarf Galago – A. W. Perkin & P. E. Honess

441 442 444 446 447 450

8

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Contents

Galagoides orinus Mountain Dwarf Galago – A. W. Perkin, P. E. Honess & T. M. Butynski Galagoides granti Mozambique Dwarf Galago (Grant’s Dwarf Galago) – P. E. Honess, S. K. Bearder & T. M. Butynski Galagoides cocos Kenya Coast Dwarf Galago (Diani Dwarf Galago) – C. S. Harcourt & A. W. Perkin Galagoides demidovii Demidoff’s Dwarf Galago – L. Ambrose & T. M. Butynski Galagoides thomasi Thomas’s Dwarf Galago – L. Ambrose & T. M. Butynski

Glossary467 452 Bibliography475 454

Authors of Volume II550

457

Indexes French names German names English names Scientific names

459 462

554 554 555 555

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Series Acknowledgements Jonathan Kingdon, David Happold, Thomas Butynski, Michael Hoffmann, Meredith Happold and Jan Kalina

The editors wish to record their thanks to all the authors who have contributed to Mammals of Africa for their expert work and for their patience over the very protracted period that these volumes have taken to materialize. We also thank the numerous reviewers who have read and commented on earlier drafts of this work. We are also grateful for the generosity of our sponsoring patrons, whose names are recorded on our title pages, who have made the publication of these volumes possible. Special thanks are due to Andy Richford, the Publishing Editor at Academic Press, who initiated and supported our work on Mammals of Africa, from its inception up to the point where Bloomsbury Publishing assumed responsibility, and to Nigel Redman (Head of Natural History at Bloomsbury), David and Namrita PriceGoodfellow at D & N Publishing, and the whole production team who have brought this work to fruition. We also acknowledge, with thanks, Elaine Leek who copy-edited every volume. We are grateful to Chuck Crumly, formerly of Academic Press and now the University of California Press, for being our active advocate during difficult times.

above left:

We have benefited from the knowledge and assistance of scholars and staff at numerous museums, universities and other institutions all over the world. More detailed and personal acknowledgements follow from the editors of each volume. The editors are also grateful to the coordinating team of the Global Mammal Assessment, an initiative of the International Union for Conservation of Nature (IUCN), which organized a series of workshops to review the taxonomy and current distribution maps for many species of African mammals. These workshops were hosted by the Zoological Society of London, Disney’s Animal Kingdom, the Owston’s Palm Civet Conservation Programme, and the Wildlife Conservation Research Unit at the University of Oxford; additionally, IUCN conducted a review of the maps for the large mammals by the Specialist Groups of the Species Survival Commission. We owe a particular word of thanks to all the staff and personnel who made these workshops possible, and to the participants who attended and provided their time and expertise to this important initiative. We also thank IUCN for permission to use data from the IUCN Red List of Threatened Species.

photograph by Jan Kalina

Jan Kalina. above: From left to right: Jonathan Kingdon, Thomas Butynski, Meredith Happold, David Happold and Andrew Richford. left: Jonathan Kingdon (left) and Michael Hoffmann.

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Acknowledgements for Volume II Tom Butynski

It was a long time ago (1998) that Jonathan Kingdon* invited me to serve as an editor for the ‘Mammals of Africa Project’. At that time we imagined that the Project would be handily completed in seven years. That was not to be! Mammals of Africa would take twice that long to bring to press. I hope that you will agree with me that the six volumes arising from this project were well worth the long wait. As the Senior Editor of Volume II (Primates) of Mammals of Africa, I have the privilege of acknowledging those people who contributed most to this volume. I also have the privilege (and feat) of acknowledging, albeit all too briefly, those many people who most influenced my professional life and led me along the path to and through Mammals of Africa. A good number of these friends, mentors and colleagues are the authors of these pages. Most of my work on this volume was conducted in Nairobi in offices generously provided by the Institute of Primate Research, the National Museums of Kenya, and the IUCN Eastern Africa Regional Program, and later, on the Laikipia Plateau at the Sweetwaters Wildlife Sanctuary and Soita Nyiro Conservancy. Some of this volume was prepared at the Moka Wildlife Center, Bioko Island, Equatorial Guinea. During my years of work on Mammals of Africa, I was employed by Zoo Atlanta, Conservation International, the Bioko Biodiversity Protection Program (a program of Arcadia University and, later, Drexel University) and the Zoological Society of London. The taxonomy and distribution maps adopted for the volume derive largely (but not entirely) from a workshop (‘Primate Taxonomy for the New Millennium’) held in Orlando, Florida, in February 2000 (Grubb et al. 2003). This workshop was organized by the IUCN/SSC Primate Specialist Group, the IUCN Global Mammal Assessment, and Conservation International, supported by the Disney Wildlife Conservation Fund and hosted by the Disney Institute. The ‘African Section’ of this workshop comprised Peter Grubb,* John Oates,* Simon Bearder,* Todd Disotell, Colin Groves,* Tom Struhsaker,* Carolyn Ehardt* and myself. It is not possible to identify all of the people and institutions that contributed to Mammals of Africa. I acknowledge the hundreds of people who have studied Africa’s primates and worked towards their conservation, as well as those institutions that supported their projects. I owe a great debt of gratitude to the excellent work of my coeditors on this volume, Jonathan Kingdon* and Jan Kalina, and to the 73 authors who wrote the 146 profiles. They gave generously of their precious time and extensive knowledge in order to fill these

pages with their expertise and unpublished data. Furthermore, they all stood by Mammals of Africa for more than a decade. All of the authors are named at the end of this volume and at the end of their respective profiles. Three authors, Annie Gautier-Hion,* Peter Grubb* and Dietrich Schaaf,* all now deceased, require particular mention. Annie contributed greatly to our understanding of the ecology and behaviour of the primates of central Africa (Gautier et al. 1999), Peter did much to lay the foundation for the taxonomy on which this volume is based (Grubb et al. 2003) and Dietrich gave unbridled support to this project – from beginning to end! The profiles in this volume benefited greatly from excellent, authoritative reviews by the following people (acknowledged here in alphabetical order): Gwendolin Altherr, Matt Anderson, Christos Astaras, Simon Bearder,* Keith Bensen,* David Brugiere,* Geneviève Campbell, Colin Chapman, Dorothy Cheny, Marc Colyn, Marina Cords,* Yvonne de Jong,* Marc De Meyer, Bertrand Deputte, Isabelle Faucher, Peter Fashing,* Leslie Field, John Fleagle, Barbara Fruth, Takeshi Furuichi, Anh Galat-Luong,* Gérard Galat,* Jean-Pierre Gautier,* Annie Gautier-Hion,* Ian Gilby, Spartico Gippoliti, Mary Glenn,* Linda Gordon, Colin Groves,* Peter Grubb,* Rob Hammond, John Hart,* Ed Heller, Gottfried Hohmann, Paul Honess,* Michael Huffman, Chadden Hunter, Clifford Jolly,* Trevor Jones, Bright Kankam, Takayoshi Kano, Margaret Kinnaird, Hans Kummer, Suehisa Kuroda, Joanna Lambert, Jean-Marc Lernould, Josh Linder, Michel Louette, Mairi Macleod, Fiona Maisels, Andrew Marshall, Judith Masters,* Scott McGraw,* Angela Meder, Addisu Mekonnen, Bethan Morgan, Iregi Mwenja, Leanne Nash,* Peter Neuenschwander, Ronald Noe, John Oates,* Andrew Perkin,* Jane Phillips-Conroy, Francesco Rovero, Thelma Rowell, Esteban Sarmiento,* Helga Schulze, Makoto Shimada, Pascale Sicotte,* Brice Sinsin, Tammy Smart, Bill Stanley, Dawn Starin, Tom Struhsaker,* Larissa Swedell,* Julie Teichroeb, Jo Thompson, Nelson Ting, Caroline Tutin, Peter Waser,* Sian Waters, Patricia Whitten, Julie Wieczkowski,* Kathy Wood, Dietmar Zinner and Klaus Zuberbühler. The authors of the profiles in this volume owe much to those museums that hold the largest collections of Africa’s primates. My own profiles were helped by examination of specimens at The National Museums of Kenya (Nairobi), Natural History Museum (London), American Museum of Natural History (New York) and United States National Museum (Washington, DC). The excellent libraries of the Zoological Society of London, American Museum 11

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Acknowledgements for Volume II

of Natural History and Smithsonian Institution somehow always managed to provide even the oldest and most obscure of references. Most prominent among those who worked to bring Mammals of Africa to press is Andy Richford, the Publishing Editor at Academic Press, who commissioned this project in 1999 and who has stood by the project through thick and thin. It is no exaggeration to state that Mammals of Africa would not exist except for Andy’s vision, dedication, diplomacy and unselfish hard work. Elaine Leek did a superb job of copy editing all the profiles in this volume. The efficient and hard-working production team at Bloomsbury Publishing must be acknowledged, particularly Nigel Redman (Head of Natural History), and David and Namrita Price-Goodfellow of D & N Publishing. Special thanks are due to Lorna Depew for checking the proof pages, Anh Galat-Luong and Gérard Galat for advising on the French vernacular names, and Dietmar Zinner and Torsten Wronski for advising on the German vernacular names. I also acknowledge the following people (in alphabetical order) who are not mentioned above but who, in one way or another, long ago, or recently, enabled Mammals of Africa: ‘Kutse’Aaron, Bernard Agwanda, Karl & Katherine Ammann, Sam Andanje, Tony Archer, Conrad Aveling, Ros Aveling, Rollin Baker, Richard Bagine, ‘Bandusya’, Jonathan Baranga, Vincent Bashekura, Isabirye Basuta, Ben Beck, Leon Bennun, Leo Beonowabo, Richard Bergl, Lindsay Birch, Cassie Boggs, Richard Bonham, Trish Bonham, Brendan Bowles, Gordon Boy, Chrysee & Esmond Bradley-Martin, Bill Brown, Demitrio Bucuma, Eriya Bunengo, Neil Burgess, John Bushara, Michael & Rita Butynski, Paul & Jane Butynski, Benny Bytebier, Alex Campbell, Janis Carter, Graham Child, Rob Clausin, Steve Collins, Chris Conrad, William Conway, John Cooper, Ian Craig, Jared Crawford, Andeliene Croce, James Culverwell, Peter Cunningham, Ted Dardani, Glyn Davies, Richard Dawkins, Jeff Dawson, Jean-Pierre, Noah & Lois Dekker, Lorna Depew, JeanPierre d’Huart, Maria Dodds, Nike Doggart, Iain Douglas-Hamilton, Bob Dowsett, Francois Dowsett-Lemaire, Bob Drewes, Holly Dublin, Jeff Dubois, Helen Dufresne, Jef Dupain, Jeffrey Dutki, Tony & Rose Dyer, Eric Edroma, Jim Else, Dick Estes, Leigh Evans, Idle Farah, Brian Finch, Petra Fitzgerald, Tony Fitzjohn, Debra Forthman, Kerry Fugett, James Fuller, Steve Gartlan, Michael Ghiglieri, Ian Gordon, Jefferson Hall, Alan Hamilton, Nancy Handler, John Hanks, Sandy Harcourt, Gail Hearn, Daphne Hill, Chris Hillman, Geoffrey Howard, Peter Howard, Kim Howell, Jimmy Hyatt, Skinner Hyatt, Mohamed Isahakia, Junichiro Itani, Colin Jackson, Paula Jenkins, Natalie Johnson, Trevor Jones, Paula Kahumbu, Celeste & Joe Kalina, Erustus Kanga, Peter Karani, Ursula Karlowski, John Kasenene, Fred Kayanja, Stuart Keith, Maria Kelly, Julian Kerbis,

Billy Keresh, Anthony & Juliet King, John King, Joseph Kirathe, Agi Kiss, Hans Klingel, Jules & Richard Knocker, Willy Knocker, Richard Kock, Bill Konstant, Rebecca Kormos, Adrian Kortlandt, Heidi Koster, Stan Koster, Ken Kuhle, Sally Lahm, Hugh Lamprey, Olivier Langrand, Annette Lanjouw, Linda Larange, Richard Leakey, Lysa Leland, Claire Lewis, Dennis & Anita Longenecker, Quentin Luke, Susan Murdock Lutz, Jerry Lwanga, Richard Malenky, Rob Malpas, Greg Mann, Terry Maple, James Maranga, Peter Marler, Nina Marshall, Paul Matiku, Roseanna Mattingly, David Mbora, Liz Mcfie, Shirley McGreal, Pat McLaughlin, Susan McMahon, Rita Mcmanamon, Dennis Milewa, John Miskell, Russ Mittermeier, Nancy Moinde, Wayne Morra, Cynthia Moss, David Moyer, Arthur Mugisha, Alex Muhweezi, Peter Muller, Ursula & Willem Muller, Susan Murray, Githua Mwangi, Stephen Nash, Anna Nekaris, Fleur N’gweno, Debbie Nightingale,Toshisada Nishida, Kate Nowak, Matti Nummelin, James Okua, Annie Olivecrona, Naima & Rob Olivier, Ilambu Omari, James Omoding, Alfred Otim, Wilber Ottichilo, Jake Owens, Ian Parker, George Petrides, Barnaby Phillips, Andy Plumptre, Derek Pomeroy, Tony Potterton, Galen Rathbun, Fiona & Graham Reid, Clare Richardson, Alan Rodgers, Alan Root, Joan Root, Tony Rose, Linda & Oskar Rothen, Noel Rowe, John Rwagara, Anthony Rylands, Jorge Sabator-Pi , Jim Sanderson, George Schaller, Jennifer & Jim Seale, Robert Seyfarth, Joe Skorupa, Kes & Fraser Smith, Raey Smithers, Jorge Soares, Bill Stanley, Mark Stanley-Price, Terry Stephenson, Beth Stevens, Tara Stoinski, Shirley Strum, Simon Stuart, Klaus-Jurgen Sucker, Simon Thomsett, Louise Tomsett, Sharon & Joe Torres, Eldad Tukahirwa, Duane Ullrey, Leonard Usongo, Amy Vedder, Sally Vickland, Richard Vigne, Wolfgang von Richter, Dan Warton, Sam Wasser, John Watkin, Bill Weber, Jessica Weinberg, Samson Werikhe, David Western, Rick Weyerhauser, Ed Wilson, Roger Wilson, Vivian Wilson, Philip Winter, Roland Wirth, Carol Fisher Wong, Mike Woodford, Torsten Wronski, Derek Yalden, Hagos Yohannes, Steven Yongili and Truman Young. I acknowledge my parents, Anna and Michael Butynski, for ‘setting the right course’, and for a boyhood and a profession that engulfed me in nature. Finally, Carly and Michael ‘Jake’ Butynski need to be acknowledged for their patience, understanding and support while suffering two parents embarked on the long and time-consuming journey that became known simply as ‘MoA’. I extend my deepest appreciation and thanks to all of the abovementioned people and institutions for their many and varied contributions to Volume II of Mammals of Africa. *Author in Volume II

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Mammals of Africa: An Introduction and Guide David Happold, Michael Hoffmann, Thomas Butynski and Jonathan Kingdon

Mammals of Africa is a series of six volumes that describes, in detail, every extant species of African land mammal that was recognized at the time the profiles were written (Table 1). This is the first time that such an extensive coverage has been attempted; all previous books and field guides have either been regional in coverage, or have described a selection of mammal species – usually the larger species.These volumes demonstrate the diversity of Africa’s mammals, summarize what is known about the distribution, ecology, behaviour and conservation status of each species, and serve as a guide to identification. Africa has changed greatly in recent decades because of increases in human populations and the related exploitation of natural resources, agricultural development and urban expansion. Throughout the continent, extensive areas of forest, woodland and savanna have been destroyed and much of what remains is degraded and fragmented. Many of the drier areas are threatened with desertification. As a result, the abundance and geographic ranges of many species of mammals have declined – some marginally, some catastrophically, some to extinction. Hence, it is appropriate that our knowledge of each species is recorded now, on a pan-African

Table 1.  The mammals of Africa. Order Hyracoidea Proboscidea Sirenia Afrosoricida Macroscelidea Tubulidentata Primates Rodentia Lagomorpha Erinaceomorpha Soricomorpha Chiroptera Carnivora Pholidota Perissodactyla Cetartiodactyla 16 a

Number of families

Number of genera

Number of species

1 1 2 2 1 1 4 15 1 1 1 9 9 1 2 6 57

3 1 2 11 4 1 25 98 5 3 9 49 38 3 3 41 296

5 2 2 24 15 1 93 395a 13 6 150 224 83 4 6 93 1116b

Including five introduced species. b Species profiles in Mammals of Africa.

basis, because the next few decades will see even more humaninduced changes. How such changes will affect each mammalian species is uncertain, but this series of volumes will act as a baseline for assessing future change. The study of African mammals has taken several stages. During the era of European exploration and colonization, the scientific study of African mammals was largely descriptive. Specimens that were sent to museums were described and named. As more specimens became available, and from different parts of the continent, there was increasing interest in distribution and abundance, and in the ecological and behavioural attributes of species and communities. At first, it was the largest and most easily observed species that were the focus of most studies, but as new methodologies and equipment became available, the smaller and more cryptic and secretive species became better known. Many species were studied because of their suspected role in diseases of humans and livestock, and because they were proven or potential ‘pests’ in agricultural systems. During the past decade or so, there has been greater emphasis on the genetic and molecular characteristics of species. These studies have produced a wealth of information, especially during the past 40 years or so. These volumes are not only a distillation of the huge literature on African mammals, but also of much previously unpublished information. There is a huge discrepancy among species in the amount of information available. Some species have been studied extensively for many years, especially the so-called ‘game species’, some species of primates and a few species that are widespread and/or easily observed. In contrast, other species are known only by one or a few specimens, and little has been written about them. Likewise, some areas and countries have been well studied, while other areas and countries have been neglected. During the preparation of these volumes, the editors have often been surprised by the wealth of information about some species when little was anticipated, and by the paucity of information about others, some of which were assumed to be ‘well known’. In addition to presenting information that is based on sound scientific evidence, the aims of these volumes are to point out where there are gaps in knowledge and to correct inaccurate information that has become embedded in the literature. For most taxa (including all primates), the detail provided in the species profiles allows accurate identification. Mammals of Africa comprises six volumes (Table 2). The volumes consist mainly of species profiles – each profile being a detailed 13

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An Introduction and Guide

Table 2.  The six volumes of Mammals of Africa. Volume

Contents

Number of species

Editors

I

Introductory chapters. Afrotheria (Hyraxes, Elephants, Dugong, Manatee, Otter-shrews, Golden-moles, Sengis and Aardvark)

49

II

Primates

93

III

Rodents, Hares and Rabbits Hedgehogs, Shrews and Bats

408

V

Carnivores, Pangolins, Equids and Rhinoceroses

93

VI

Pigs, Hippopotamuses, Chevrotain, Giraffes, Deer and Bovids

93

Jonathan Kingdon, David C. D. Happold, Michael Hoffmann, Thomas M. Butynski, Meredith Happold and Jan Kalina Thomas M. Butynski, Jonathan Kingdon and Jan Kalina David C. D. Happold Meredith Happold and David C. D. Happold Jonathan Kingdon and Michael Hoffmann Jonathan Kingdon and Michael Hoffmann

IV

380

account of the species. They have been edited by six editors who distributed their work according to the orders with which they are most familiar. Each editor chose authors who had extensive knowledge of the species (or higher taxon) and, preferably, had experience with the species in the field. Each volume follows the same general format with respect to arrangement, subheadings and contents. Because Mammals of Africa has contributions from 356 authors (each with a different background and speciality), and because each volume was edited by one or more editors (each with a different perspective), it has not been possible or even desirable to ensure exact consistency throughout. Species profiles are not intended to be exhaustive literature reviews, partly for reasons of space. None the less, they are written and edited to be as comprehensive as possible, and to lead the reader to the most important literature for each species. Inevitably, not all information available could be accommodated for the better-known species, and so, such profiles are a précis of available knowledge. Extensive references in the text alert and guide the reader to more detailed information. In addition to the species profiles, there are profiles for the higher taxa (genera, families, orders, etc.). Thus, there is a profile for each order, for each family within the order, for each genus within the family, and for each species within the genus. For some orders there are additional taxonomic levels, for example, tribes (e.g. in Bovidae), subgenera (e.g. in Procolobus), and species-groups, or ’superspecies’ (e.g. in Cercopithecus).The taxonomy used in Volume II mostly follows that presented in Grubb et al. (2003), although, in a few cases, the editors adopted an alternative taxonomy when there were good reasons for doing so. Volume I differs from the other volumes in that it contains a number of introductory chapters about Africa and its environment, and about African mammals in general.

The continent of Africa For the purposes of this work, ‘Africa’ is defined as the continent of Africa (bounded by the Mediterranean Sea, the Atlantic Ocean, the Indian Ocean, the Red Sea and the Suez Canal) and the islands on the continental shelf. The largest of the ‘continental islands’ are Zanzibar (Unguja), Mafia and Bioko (Fernando Po). All ‘oceanic islands’, e.g. São Tomé, Principe, Annobón (Pagulu), Madagascar, Comoros, Seychelles, Mauritius, Socotra, Canaries, Madeira and Cape Verde, are excluded with the exception of Pemba, which is included because of its close proximity (ca. 50 km) to the mainland. The names of the countries of Africa are taken from the Times Atlas (2005). The Republic of Congo is referred to as ‘Congo’, and the Democratic Republic of Congo (former Zaire) as ‘DR Congo’. Smaller geographical or administrative areas within countries are rarely referred to except for Provinces in South Africa, which are used extensively in the literature. Maps showing the political boundaries of Africa (Figure 1a), the Provinces of South Africa (Figure 1b), and the major physical features of Africa (Figure 1c) are provided, as is a list of the 47 countries together with their previous names as used in the older literature on African mammals (Table 3). Africa is the second largest continent in the world (after Asia), but it differs from other continents (except Australia and Antarctica) in being essentially an island. At various times in the past, Africa has been joined to other continents – a situation that has had a strong influence on the fauna and flora of the continent. Africa is a vast continent (29,000,000 km², 11,200,000 mi²) that straddles the Equator, with about two-thirds of its area in the northern hemisphere and one-third in the southern hemisphere. As a result, Africa has many varied climates (with seasons in each hemisphere being six months out of phase), many habitats (including deserts, savannas, woodlands, swamps, rivers, lakes, moist forests, monsoon forests, mountains and glaciers), and altitudes ranging from 155 m (509 ft) below sea level at L. Assal, Djibouti, in the Danakil (Afar) Depression, to 5895 m (19,341 ft) on Mt Kilimanjaro, Tanzania. Africa is comprised of 47 countries, some of which are very large (e.g. Sudan, 2,506,000 km², 967,000 mi²; Algeria, 2,382,000 km², 920,000 mi² and Democratic Republic of Congo, 2,345,000 km², 905,000 mi²) and others that are relatively small (e.g. Djibouti, 23,200 km², 9,000 mi²; Swaziland, 17,400 km², 6,700 mi²; and The Gambia, 11,300 km², 4,400 mi²). The human population of each country also varies greatly, from about 346/km² in Rwanda to only about 2.5/km² in Namibia. With its great size and varied habitats, Africa supports a high biodiversity, including a large number of species of mammals. Likewise, most countries have a high diversity of mammals (especially when compared with temperate countries). Africa can be divided into ‘biotic zones’ (Figure 2). A biotic zone is defined as an area within which there is a similar environment (primarily rainfall and temperature) and vegetation, and which differs in these respects from other biotic zones. Thirteen biotic zones are recognized, two of which may be divided into smaller categories. The biotic zones where each species of mammal has been recorded are listed in each profile for several reasons. They indicate the environmental conditions in which the species lives and they provide data with which the geographic distribution can be explained and predicted. Furthermore, the number of biotic zones exploited by a species indicates its level of habitat tolerance and

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The continent of Africa

0°

10°

a

30°

M

c oro

10°

co

20°

Tunisia

30°

30°

Western Sahara

le Ni

Algeria Libya

20°

Egypt 40°

Mauritania

Niger

r Nige

Chad

Burkina Faso

Somaliland Ethiopia

ia

South Sudan

al

a

Cameroon Togo Benin Bioko (Equatorial 0° Guinea) Gabon 0° Rio Muni (Equatorial Guinea) 1000 miles Cabinda (Angola)

Uganda

Congo

Kenya

Co

ng

o

10°

Central African Republic

So

Liberia

10°

an

Côte d’Ivoire

Djibouti

Nigeria

Gh

GuineaGuinea Bissau Sierra Leone

500 1000 km

0°

Pemba Zanzibar

Tanzania

Mafia

10°

10°

Angola

10°

Malawi

Zambia

qu

e

i bez am

bi

Z

Figure 1. (a) Political map of Africa; (b) provinces of South Africa; (c) altitudes and major rivers of Africa. South Sudan and Somaliland are not identified as separate countries in the text.

Zimbabwe

20°

Namibia

am

500

Rwanda Burundi

50°

oz

0

Democratic Republic of Congo

M

0

50°

Eritrea

Sudan

m

Senegal The Gambia 10°

20°

Mali

Botswana

20° 40°

Swaziland

c

30°

30°

South Africa

Lesotho 30°

20°

le Ni Awa sh

W hite Nile

Tana

Za

Shire

e en un

e

Limpopo

Gauteng

North West

a um Ruv Lake Malawi

opo mp Li

Or

b

Free State Northern Cape

Eastern Cape Western Cape 0

ang e

KwaZulu– Natal

zi be m

Lake Kariba Okavango Delta

C

Mpumalanga

Rufiji

Lake Mweru Lake Bangweulu

o ng ba Cu

altitude (metres) 0 1–200 201–500 501–1000 1001–2000 2001–4000 above 4000

Lualaba

ili Kw o ang Kw

1000 miles

1000 km

i Lomam Sankuru Kasai

é

oou

500 500

a

a Og

0 0

o She bel Om u l Mbomo Lake Uele Albert Lake Turkana Congo Aruwimi-Ituri Mt Elgon Rwenzori Mtns Mt Kenya Lake Lake Tshuap a Edward Victoria Lukenie Mt Kilimanjaro Galana Lake Tanganyika Jub

Sangh

Cross

e nu Be Mt Cameroon aga San Ivindo

Lu an gw a

Lake Volta

Lake Tana

Ouban gui

Black Volta

olta ite V Wh

Lake Chad

ile eN Blu

gal

e Sen r Nige

0

300 miles 300 km

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An Introduction and Guide

Table 3.  The countries of Africa: names, areas and human population density. Country name Algeria Angola (includes Cabinda) Bénin * [Dahomey] Botswana [Bechuanaland] Burkina Faso * [Upper Volta; Burkina] Burundi [part of Ruanda-Urundi (= part of Belgian Congo)] Cameroon [includes former French Cameroon, German Cameroon and part of Eastern Nigeria] Central African Republic # Chad [Tchad] Congo [Republic of Congo] Côte d’Ivoire * [Ivory Coast] Democratic Republic of Congo [Belgian Congo; Congo (Kinshasha); Zaire] Djibouti [French Somaliland] Egypt Equatorial Guinea # (includes Rio Muni [Spanish Guinea] and Bioko I. [Fernando Po]) Eritrea (formerly part of Ethiopia) Ethiopia [Abyssinia] Gabon # The Gambia Ghana [Gold Coast] Guinea * Guinea-Bissau [Portuguese Guinea] Kenya Lesotho [Basutoland] Liberia Libya Malawi [Nyasaland] Mali * Mauritania * Morocco [includes former Spanish Morocco and French Morocco]; (now also includes Western Sahara = former Spanish Sahara) Mozambique [Portuguese East Africa] Namibia [South-west Africa] Niger * Nigeria Rwanda [part of Ruanda-Urundi (= part of Belgian Congo)] Senegal * Sierra Leone Somalia ¥ [British Somaliland and Italian Somaliland; Somali Republic] South Africa Sudan § [Anglo-Egyptian Sudan] Swaziland Tanzania [German East Africa; Tanganyika] (now includes Zanzibar I., Mafia I. and Pemba I.) Togo [Togoland] Tunisia Uganda Zambia [Northern Rhodesia] Zimbabwe [Southern Rhodesia] Totals/mean density

Area (km2) ’000

Area (miles2) ’000

Human population ’000 (2006)

People per km2

2,382 1,247 113 582 274 27.8 475

920.0 481.0 43.0 225.0 106.0 10.7 184.0

33,500 15,800 8,700 1,800 13,600 7,800 17,300

14.1 12.7 77.0 3.1 49.6 280.5 36.2

623 1,284 342 322 2,345

241.0 496.0 132.0 125.0 905.0

4,300 10,000 3,700 19,700 62,700

6.9 5.8 10.8 61.2 26.7

23.2 1,001 28.1

9.0 387.0 10.8

800 75,400 500

34.5 75.3 17.8

94 1,128 268 11.3 239 246 36 580 30.4 111 1,760 118 1,240 1,030 447

36.0 436.0 103.0 4.4 92.0 95.0 13.9 224.0 11.7 43.0 679.0 46.0 479.0 412.0 172.0

4,600 74,800 1,400 1,500 22,600 9,800 1,400 34,700 1,800 3,400 5,900 12,800 13,900 3,200 32,100

48.9 66.3 5.2 132.7 94.6 39.8 38.9 59.8 59.2 30.6 3.6 108.5 11.2 3.1 71.8

802 825 1,267 924 26.3 197 71.7 638 1,220 2,506 17.4 945

309.0 318.0 489.0 357.0 10.2 76.0 27.7 246.0 471.0 967.0 6.7 365.0

19,900 2,100 14,400 134,500 9,100 11,900 5,700 8,900 47,300 41,200 1,100 37,900

24.8 2.5 11.3 145.6 346.0 60.4 79.5 13.9 38.7 16.4 63.2 40.1

56.8 164 236 753 391 29,448

21.9 63.0 91.0 291.0 151.0 11,383

6,300 10,100 27,700 11,900 13,100 902,600

110.9 61.6 117.4 15.8 33.5 56.8

Former names are listed in chronological order in square brackets, with the oldest name listed first. Obsolete names are listed because much of the older literature refers to past colonial entities. * = formerly part of French West Africa. # = formerly part of French Equatorial Africa. § At the time of going to press, the country of Sudan had been divided into two: the Republic of Sudan in the north, and the Republic of South Sudan in the south. ¥ The former British Somaliland is now a self-declared state under the name of the Republic of Somaliland, but remains internationally unrecognized.

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Species profiles

The primates of Africa

1

This volume, Volume II, is devoted to the order Primates. The order Primates, using the taxonomy adopted for this volume, contains four families, 25 genera and 93 species. About 8% of Africa’s species of mammal are primates. Since the texts for this volume were prepared, one new species of primate has been described:

2

3 6a

4

5

7

5

6

6a

1 = Mediterranean Coastal Biotic Zone 2 = Sahara Arid Biotic Zone 3 = Sahel Savanna Biotic Zone 4 = Sudan Savanna Biotic Zone 5 = Guinea Savanna Biotic Zone 6 = Rainforest Biotic Zone    6a = Northern Rainforest–Savanna Mosaic    6b = Eastern Rainforest–Savanna Mosaic    6c = Southern Rainforest–Savanna Mosaic 7 = Afromontane–Afroalpine Biotic Zone (discontinuous, shaded brown) 8 = Somalia–Masai Bushland Biotic Zone 9 = Zambezian Woodland Biotic Zone 10 = Coastal Forest Mosaic Biotic Zone 11 = South-West Arid Biotic Zone    11a Kalahari Desert    11b Namib Desert    11c Karoo 12 = Highveld Biotic Zone 13 = South-West Cape Biotic Zone

Lesula Cercopithecus lomamiensis J. Hart, Detwiler, Gilbert, Burrell, Fuller, Emetshu, T. Hart, Vosper, Sargis & Tosi, 2012. PLOS ONE 7(9): e44271, p. 4. Type locality: Near Lohumonoko (01°01´S, 24°25´E; 470 m asl), west bank, Lomami R., Central Basin, Democratic Republic of Congo. Taxonomy: Member of the Owl-faced Monkeys Group Cercopithecus (hamlyni). Distribution: Between Lomami R. and Tshuapa R., C DRC (01°01´–01°26´S, 24°25´–25°02´E; 440– 715 m asl). Area of occurrence: ca. 17,000 km². See map on p. 341. Habitat: Mature terra firma evergreen forest. Description: Slender, medium-sized, long-limbed monkey. Recalls Owl-faced Monkey C. hamlyni but facial skin pinkish-grey to tan-brown; vertical nose stripe cream or indistinct; chin, throat and chest yellowish-buff; posterior 30–50% of dorsum with prominent, amber, median stripe (brightest at base of tail); tail tuft absent. Further information on C. lomamiensis is presented in Hart et al. (2012). See illustration on p. 344.

8 6

6b

6c 10 9

11a 11b

12 11c 13

Figure 2. The biotic zones of Africa.

the extent to which it is vulnerable to loss of a particular habitat. The Rainforest Biotic Zone and the South-West Arid Biotic Zone are divided into regions and sub-regions that reflect the different biogeographical distributions of species, each region/sub-region having a community of mammals and other animals that is different to any other. Details of the biotic zones of Africa, and the regions and sub-regions of the Rainforest Biotic Zone and South-West Arid Biotic Zone, are given in Chapter 5 of Volume I of Mammals of Africa.

crown nape

forehead

Species profiles Information about each species is given under a series of subheadings, the amount of information under each of which varies greatly among species; where no information is available, this is recorded as ‘No information available’ or similarly. The sequence of subheadings is: Scientific Name (genus and species)  The currently accepted name of the species. Common Names  English, French and German names are given, as available. The first given English name is the preferred common

withers

rump

muzzle back

neck

tail base

nostrils lips

cheek chin

shoulder

throat

buttock

flanks hindquarter

belly

dewlap elbow

upper hindleg

upper foreleg hock knee lower hindleg

Figure 3. External features of a mammal: Common Eland Tragelaphus oryx.

pastern

lower foreleg fetlock

fetlock

pastern

hoof

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An Introduction and Guide

Figure 4. External features of a mammal: Genet Genetta sp. (side-view and face frontal).

head

neck

body mid-dorsal line

tail

DORSAL

back (dorsal pelage)

external ear (pinna) crown

rump

forehead

face

flank buttock

neck

eye muzzle

cheek throat

nostrils lips

forehead

ventral surface ventral pelage

crown

basal end of tail thigh

VENTRAL

chin

tuft

chest shoulder

tail

POSTERIOR

distal end

tip of ear forelimb (or foreleg) (upper and lower) base of ear

temple

ear, pinna digits (1, 2, 3, 4, 5)

digit(s)

muzzle

hindlimb (or hindleg) (upper and lower)

forefoot

eye nostrils (nose) lips

pelage (= fur) hair (= single hair(s))

(vernacular) name for the species; alternative names are given in parentheses for some species. Most of the English common names used in this volume are taken from Grubb et al. (2003). The French and German common names derive from various sources or are direct translations of the English vernacular. Scientific Citation  This provides the full scientific name of the species, i.e. genus name, species name, authority name and date of authority. Parentheses around the authority’s name and date indicate that the species was originally named in a different genus to its present generic allocation. The scientific name is followed by the publication where the species was described and the type locality (i.e. where the type specimen [or type series] was obtained). Most of this information is taken from Wilson & Reeder (2005). Taxonomy  This section contains information about previous scientific names of the species, taxonomic problems, and the relationship with other species in the genus. For some species, there is considerable information about these topics; for others, there may be nothing. Synonyms are listed in alphabetical order (without the taxonomic authority for each unless essential for clarity) and the number of subspecies (if any) is presented, mostly taken from Grubb et al. (2003) and Wilson & Reeder (2005). The chromosome number is given if available and, in some cases, this is followed by other information relevant to the chromosomes. In late 2006, a revised edition of the Atlas of Mammalian Chromosomes was published (O’Brien et al. 2006), but it was not possible to incorporate the findings of that important work here. Description  This section, together with the illustrations, provides the reader with adequate information to identify the species. The section begins with a brief overall description of the

species, including an indication of size. This is followed by a detailed description of the external features of the species’ head (and parts of the head), dorsal pelage, legs, feet, ventral pelage and tail (in this order), as well as any special characteristics unique to the species. For some species, diagnostic characteristics of the skull are given. The mammary formula (i.e. the number and arrangement of nipples) is noted wherever this feature varies among the taxa being discussed. The characters described in this section are common to all subspecies of this species (see also Geographic Variation). Characters that are diagnostic to the genus are not usually repeated in a species profile; hence, higher taxa profiles should also be consulted. Geographic Variation  Variation within the species may be of two sorts: (a) clinal variation without subspecies, or (b) subspecific variation. If (a), then there is a description of the character(s) that alter clinally across the geographic range of the species. If (b), each of the subspecies is listed with its geographic range and the characters that distinguish it from all other subspecies of the species. Similar Species  Species that are sympatric or parapatric with the species under consideration, and with which it may be confused, are listed along with diagnostic characteristics and geographic ranges (additionally, readers may refer to profiles of the similar species in question). In some instances, similar species that are allopatric are also included. Distribution  The first sentence is often ‘Endemic to Africa’, indicating that the species is found (in the wild) only in Africa. If a species also occurs outside Africa (and, hence, is not endemic), this is noted at the end of this section. The next sentence usually gives the Biotic Zone(s) where the species has been recorded; this provides the reader with a general impression of where the species occurs in Africa and the sort of habitats where the species lives. Finally, the countries (or parts of countries) where the species has been recorded are listed. As a general rule, descriptions of the range for species with very restricted

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Species profiles

distributions are more precise in terms of information given (including, for example, geographic coordinates) than for more widespread species, where a more generalized range statement is adequate. A distribution map (see below) augments the information given here. Habitat  This section provides a description of the habitat, or range of habitats, where the species lives. Details of plant communities, plant species, vegetation structure, water availability, etc. (if available) are also presented. Other information may include average annual rainfall, average annual rainfall limits, altitudinal limits, temperature limits and seasonal variation in habitat characteristics. Abundance  A general indication of abundance of the species in its habitat(s). This may be unquantified, such as ‘abundant’, ‘common’, ‘uncommon’, ‘rare’, or phrases such as ‘rarely seen but frequently heard’. For better-known or rare species, abundance may be expressed as estimates of density (e.g. number/ha or number/km2), or relative abundance (e.g. ‘the second most numerous species’). Adaptations  This section describes morphological, physiological, and behavioural characteristics that show how the species uniquely interacts with its environment, with conspecifics and with other animals. This section may also describe species-specific adaptations for feeding, locomotion, production of sound, sensory mechanisms and activity patterns. In some instances, comparison with related or convergent species allows the unique adaptations of the species under discussion to be detailed or emphasized. Foraging and Food  The first sentence briefly describes the food habits of the species (e.g. insectivorous, folivorous, granivorous, omnivorous). This may be followed by the method of collecting food (foraging), size of home-range and daily distance moved. The diet is then described either by a list of the taxa of animals or plants consumed,

and/or as a quantitative measure based on direct observations, or of examination of the contents of the stomach or the faeces. Social and Reproductive Behaviour  Topics in this section may include social organizations (e.g. solitary, social, or colonial), group size, group composition, agonistic and amicable behaviour, comfort behaviour, territoriality, courtship and mating, parental behaviour, parent–young interactions, presence of helpers, vocalizations, and interactions with other species (mammals, birds, etc.). Reproduction and Population Structure  This section begins with an assessment of the reproductive strategy (if known) and the times/seasons of the year when there is reproductive activity (mating, pregnancy, birth, lactation). Other information may include length of gestation, litter-size, birth-weight and size, birth intervals, birth rates, time to weaning, time to maturity, longevity, mortality rates, sex ratios and adult/immature ratios. Predators, Parasites and Diseases  Predators, parasites and diseases are listed. Additional information is given if the species is a host to diseases that affect humans and domestic stock, and if the species is hunted by humans (‘bushmeat’). Remarks  This subheading subsumes the last five of the above sub­ headings in those cases where there is little or no information available. Conservation  The conservation status of the species in 2012 is stated, as given by the IUCN Red List of Threatened Species.The IUCN Red List ‘degree of threat categories’ follow the definitions and criteria given in the IUCN Red List Categories and CriteriaVersion 3.1 (www.iucnredlist. org). The categories are listed in Table 4. For those species classified as ‘threatened’ (i.e. ‘Vulnerable’, ‘Endangered’, ‘Critically Endangered’), readers can obtain detailed reasons for the classification by going to

Table 4.  Definitions for the IUCN Red List categories (from IUCN – Red List Categories, Version 3.1). Category

Description

Extinct (EX)

A taxon is Extinct when there is no reasonable doubt that the last individual has died. A taxon is presumed Extinct when exhaustive surveys in known and/or expected habitat, at appropriate times (diurnal, seasonal, annual), throughout its historic range have failed to record an individual. Surveys should be over a time frame appropriate to the taxon’s life-cycles and life-form. A taxon is Extinct in the Wild when it is known only to survive in cultivation, in captivity or as a naturalized population (or populations) well outside the past range. A taxon is presumed Extinct in the Wild when exhaustive surveys in known and/ or expected habitat, at appropriate times (diurnal, seasonal, annual), throughout its historic range have failed to record an individual. Surveys should be over a time frame appropriate to the taxon’s life-cycle and life-form. A taxon is Critically Endangered when the best available evidence indicates that it meets any of the criteria A to E for Critically Endangered, and it is therefore considered to be facing an extremely high risk of extinction in the wild. A taxon is Endangered when the best available evidence indicates that it meets any of the criteria A to E for Endangered, and it is therefore considered to be facing a very high risk of extinction in the wild. A taxon is Vulnerable when the best available evidence indicates that it meets any of the criteria A to E for Vulnerable, and it is therefore considered to be facing a high risk of extinction in the wild. A taxon is Near Threatened when it has been evaluated against the criteria but does not qualify for Critically Endangered, Endangered or Vulnerable now, but is close to qualifying for (or is likely to qualify for) a threatened category in the near future. A taxon is Least Concern when it has been evaluated against the criteria and does not qualify for the Critically Endangered, Endangered, Vulnerable or Near Threatened categories. Widespread and abundant taxa are included in this category. A taxon is Data Deficient when there is inadequate information to make a direct, or indirect, assessment of its risk of extinction based on its distribution and/or population status. Data Deficient is not a category of threat. Listing of taxa in this category indicates that more information is required and acknowledges the possibility that future research will show that a threatened classification is appropriate. A taxon is Not Evaluated when it has not yet been evaluated against the criteria.

Extinct in the Wild (EW)

Critically Endangered (CR) Endangered (EN) Vulnerable (VU) Near Threatened (NT) Least Concern (LC) Data Deficient (DD)

Not Evaluated (NE)

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An Introduction and Guide

the IUCN Red List website. Some species have changed status due to improved knowledge, taxonomic revision, or the impact of threatening processes or conservation actions. Readers can obtain detailed reasons for the past and present status of a species by going to the IUCN Red List website. If, in 2012, a species was listed on Appendix I or Appendix II under CITES (Convention on International Trade in Endangered Species; www.cites.org), this is also indicated. For some species, additional information is provided, such as presence in protected areas, major threats, and current or recommended conservation measures. Measurements  A series of morphological measurements is provided. For each species there is a standard set of measurements provided for adult males and adult females. The abbreviation and definition for each measurement is given in the Glossary. A measurement is cited as the mean value, range (given in parentheses) and sample size. For some, the standard deviation (mean ± 1 S.D.) is given instead of the range.Where possible, information is given on the location(s) where the specimens were obtained and the source of the data. Sources are either cited publications, specimens in museums, or unpublished information from authors or others. Acronyms for museums referred to in this volume are given in Table 5.

Table 5.  Museum acronyms. Acronym

Museum name

AM

Amatole Museum, King William’s Town, South Africa (formerly Kaffrarian Museum) American Museum of Natural History, New York, USA Natural History Museum, London, UK [formerly British Museum (Natural History)] Carnegie Museum of Natural History, Pittsburgh, USA Cornell University Museum of Vertebrates, Ithaca, NewYork, USA Field Museum of Natural History, Chicago, USA Los Angeles County Museum, Los Angeles, USA Museum of Comparative Zoology, Harvard University, Cambridge, USA Museum National d’Histoire Naturelle, Paris, France National Museums of Kenya, Nairobi, Kenya Natural History Museum of Zimbabwe, Bulawayo, Zimbabwe Powell-Cotton Museum, Birchington, UK Royal Museum for Central Africa, Tervuren, Belgium Transvaal Museum, Pretoria, South Africa United States National Museum of Natural History, Smithsonian Institution, Washington DC, USA Zoologisches Forschungsmuseum, Alexander Koenig, Bonn, Germany

AMNH BMNH CM CUMV FMNH LACM MCZ MNHN NMK NMZB PCM RMCA TM USNM ZFMK

Key References  This is a list of the more important references for the species. Each reference is given in full in the Bibliography. Author  The name of the author, or authors, is given at the end of each profile. All profiles should be cited using the author name(s).

Higher taxon profiles The profiles for orders, families and genera are less structured than for species. Each profile usually begins with a listing of the taxa in the next lower taxon; for example, each family profile lists the genera in that family. An exception to this arrangement is where a taxon has only one lower taxon. Higher taxa profiles provide the characteristics common to all members of that taxon; these characteristics are usually not repeated in the lower taxa profiles (unless essential for identification).

Distribution maps Each species profile contains a pan-African map showing the geographic range of the species. Most maps were provided by the author(s) of the profile and were compiled from literature records, museum specimens, and unpublished sources; some maps were provided by the editors. Maps in this volume were checked (and modified if necessary) by the members of the Africa Section of the ‘Primate Taxonomy for the New Millennium’ workshop held in Orlando, Florida, in February 2000 (Grubb et al. 2003). This workshop was organized by the IUCN/SSC Primate Specialist Group, The IUCN Global Mammal Assessment, and Conservation International. Each map shows the boundaries of the 47 countries of Africa, some of the major rivers (Nile, Niger–Benue, Congo [with the tributaries Ubangi, Lualaba and Lomani], Zambezi and Orange), and Lakes Chad, Tana, Turkana (formerly Rudolf), Albert, Edward, Victoria, Kyoga, Kivu, Tanganyika, Malawi, Mweru, Bangwuela

and Kariba. The map projection is Transverse Mercator, with the following parameters: False Easting: 0; False Northing: 0; Central Meridian: 20; Linear Unit: metre; Datum: Clarke 1866. The geographic distribution of a species is indicated as: • red shading = current range(s). When presented, different colour shading denotes subspecies. • × = isolated locations considered to be separate from the main geographic range(s). Some locations indicated by × may include two or more closely spaced locations. • ? = locality of uncertain validity; relevant information usually in text. • coloured arrow = presence on the island indicated by the arrow.

Editors of Mammals of Africa Jonathan Kingdon, Department of Zoology, University of Oxford, WildCRU, Tubney House, Abingdon Road, Tubney OX13 5QL, UK. (Vols I, II, V & VI) David Happold, Research School of Biology, Australian National University, Canberra, ACT 0200, Australia (Vols I, III & IV) Thomas Butynski, Eastern Africa Primate Diversity and Conservation Program, PO Box 149, Nanyuki 10400, Kenya, and Zoological Society of London, King Khalid Wildlife Research Centre, Saudi Wildlife Authority, PO Box 61681, Riyadh 11575, Kingdom of Saudi Arabia (Vols I & II) Michael Hoffmann, International Union for Conservation of Nature – Species Survival Commission, 219c Huntingdon Road, Cambridge CB3 0DL, UK. (Vols I, V & VI) Meredith Happold, Research School of Biology, Australian National University, Canberra, ACT 0200, Australia (Vols I & IV) Jan Kalina, Soita Nyiro Conservancy, PO Box 149, Nanyuki 10400, Kenya (Vols I & II)

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Supercohort SUPRAPRIMATES

Supercohort SUPRAPRIMATES (EUARCHONTOGLIRES) Supraprimates Waddell, Kishino & Ota, 2001. Genome Informatics 12: 141–154. Euarchonta

Primates and allies

p. 22

Glires

Rodents, Hares

See Mammals of Africa, Volume III

Efforts to understand the relationship of primates to other mammals have exercised biologists for more than 100 years. Based primarily on comparative anatomy, the deepest levels of affinity eluded success until the advent of molecular phylogeny. The latest genetic studies reveal some unexpected affinities, refute others and, in at least one case, broadly confirm a supposed taxonomic relationship that is of long standing. Thus, Gregory (1913) clustered primates with treeshrews (Scandentia), colugos or flying lemurs (Dermoptera) and bats (Chiroptera). The bat connection is firmly rejected by all molecular studies while the long-suspected, but hotly disputed, link between primates and tree-shrews receives some support (Waddell et al. 2001). The colugos, however, turn out to have the closest genetic affinities with primates, followed by Scandentia (Murphy et al. 2001, Bininda-Emonds et al. 2007, Perelman et al. 2011). More distant than either tree-shrews or colugos, rodents and lagomorphs are the next closest relatives of primates (Eizirik et al. 2001, Murphy et al. 2001). These previously hidden subtleties of relationship elicit a need for taxonomic expression at various supraordinal levels. As such, Waddell et al. (2001) propose a supercohort named ‘Supraprimates’ to group primates, flying lemurs, tree-shrews, rodents and lagomorphs. Other authors apply the name ‘Euarchontoglires’ to the same grouping (Madsen et al. 2001, Murphy et al. 2001, Van Dijk et al. 2001). A still higher level of grouping is mooted by Hedges et al. (1996) and Eizirik et al. (2001), who link ‘Euarchontoglires’ and ‘Laurasiatheria’ in ‘Boreoeutheria’ to stress their putative common origin in the northern continents. A continental dimension for taxonomy has long had obvious meaning for endemic groups such as kangaroos in Australia, golden-moles in Africa and armadillos in South America, but formal expression through archaeocontinental names for mammal groupings is essentially new and reflects a heightened awareness that geographic separation is a fundamental part of evolution (Hedges et al. 1996). This innovation has come about because there is now general recognition that the splitting of Pangaea into Laurasia and Gondwana, and subsequent fragmentation of the latter into the southern continents, had consequences for the evolution of placental

90

85

80

75 mya Haplorrhini Strepsirrhini Dermoptera Scandentia Lagomorpha Rodentia

Tentative phylogenetic tree for the Supraprimates (after Springer et al. 2003).

mammals (Scally et al. 2001). While controversy still surrounds allocation of these supraordinal groupings to specific land masses, they are founded upon the most plausible interpretation of the evidence currently available: Supraprimates (Euarchontoglires) embraces Primates, Dermoptera, Scandentia, Rodentia and Lagomorpha. Molecular clocks suggest that the primary divergence between Supraprimates and their closest other supercohort, the Laurasiatheria, was during the mid-Cretaceous, between 102 mya (Bininda-Emonds et al. 2007) and 92 mya (Kumar & Hedges 1998). Within Supraprimates, the Euarchonta/Glires split is estimated at about 98 mya by Bininda-Emonds et al. (2007) but later by others. While the timing of such divergences remains open to question, the relationships among major groupings have found closer agreement. The phylogenetic tree that is presented here follows BinindaEmonds et al. (2007); hopefully, the broad pattern of its branching will not undergo further major changes even if the putative times of divergence eventually need revision. In the absence of fossils, any reconstruction of what a 100-millionyear-old common ancestor of all supraprimates might have looked like must be extremely tentative. This ancestor was probably small, nocturnal and semi-arboreal: superficially it may have resembled a small opossum or dormouse (but without the specializations of contemporary marsupials or rodents). Jonathan Kingdon

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Cohort EUARCHONTA

Cohort EUARCHONTA Euarchonta Murphy, Elzirik, O’Brien, Madsen, Scally, Douady, Teeling, Ryder, Stanhope, de Jong & Springer, 2001. Science 294: 2348–2351.

This newly erected category associates the primates, on the basis of genetic similarities, with two non-African taxa: the Oriental treeshrews (Scandentia) and the South-East Asian colugos (flying lemurs) (Dermoptera). Discussion of possible affinities with tree-shrews has a long and interesting history, beginning with observations by Parker (1885) in which he first noted resemblances. Gregory (1910, 1913) went on to erect the taxon ‘Archonta’, which grouped primates with tree-shrews, colugos and bats. Following detailed surveys of treeshrew morphology by Carlsson (1922) and Le Gros Clark (1924, 1934), Simpson (1945) went so far as to include tree-shrews within Primates, remarking that the former were ‘either the most primatelike insectivores or the most insectivore-like primates’, and ‘the use of [tree-shrews] to represent the earliest primate or latest preprimate stage of evolution is as valid and useful and subject to as much caution as is any use of living animals to represent earlier phylogenetic stages’. Subsequent taxonomists disagreed and removed tree-shrews from Primates (Roux 1947, Van Valen 1965, Szalay & Delson 1979).

tree-shrew (Scandentia)

early adapid primate

Skull outlines of a tree-shrew (Scandentia) and an early adapid primate (after Martin 1990).

Controversies over classification are less interesting than understanding degrees and levels of relationship, so the new molecular techniques have had the special virtue of making the construction of phylogenetic trees more objective and plausible. As Martin (1990) remarked, an objective assessment of the phylogenetic relationship between tree-shrews and primates is actually a valuable test case in understanding primate origins. The fact that tree-shrews and colugos are both exclusively Asian taxa and have never been found, even as fossils, outside Asia, provides some confirmation that tree-shrews and colugos, as well as primates, diverged from common ancestors in Asia during the mid-Cretaceous, some 100–93 mya. Tree-shrews fall on the more primitive side of the Euarchonta/ Rodentia divide, so it is interesting that several Oriental squirrels have extraordinary resemblances with sympatric tree-shrews, a convergence that was first noted by Shelford (1916). New recognition that rodents have an ancient relationship with primates and tree-shrews does not make such resemblances any less expressive of convergent evolution in separate lineages, but it does imply substantial continuity in the niche structure of tropical forests – as does the continuous presence of tarsiers since the mid-Eocene, 40 mya (Gebo et al. 2000). Opportunities for small, nest-making omnivores (tree-shrews eat mainly arthropods and small fruits) with a weight range of 45–350 g, occur at all levels of the forest, including the floor, where one genus, Urogale, spends most of its life. Attempts to envisage primate, rodent, placental or marsupial ancestors by referring to mammals that look like ‘primitive insectivores’ have long been a part of grappling with evolution. Romer (1966) wrote, ‘it may well be that in tree-shrews we see the most primitive of living placentals – forms not too distant from the common base of all eutherian stocks’. Martin (1990) was more specific, noting that tree-shrews conform to the expectation of an intermediate between primitive insectivore and advanced primate. In spite of recognizing a genetic affinity, the new molecular trees and their associated clocks are a reminder that primates and treeshrews have pursued separate evolutionary paths for more than 90 million years. Jonathan Kingdon

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Superorder PRIMATOMORPHA

Superorder PRIMATOMORPHA Primatomorpha Waddell, Kishino & Ota, 2001. Genome Informatics 12: 141–154.

This taxon has been erected in recognition that the closest and most exclusive genetic affinity between primates and any other living mammal is with the South-East Asian colugos (Cynocephalidae, Dermoptera). Cronin & Sarich 1980 were the first to report monophyly between these two groups (and tree-shrews). In naming ‘Primatomorpha’, Waddell et al. (2001) gave formal expression to this relationship within the Euarchonta. Colugos, of which there are two species, weigh 1–1.7 kg and have developed skin webbing between their limbs and tail as a gliding membrane or patagium. They are vegetarian, eating leaves, shoots, flowers and sap, and have very long, lightly built limbs, large clawed feet and hands, and a wide, flat head that resembles that of a lemur, hence their alternative name, ‘flying lemur’. It would seem that modification of skin to provide a ‘vol-plane’ is a relatively simple development and has evolved independently in many animals, including amphibians, reptiles and mammals. Among Australian possums the gliding membrane has evolved several times. The closest living relative of one form, the Greater Glider Petauroides volans, is the non-gliding Lemuroid Possum Hemibelideus lemuroides, not one of several other gliding possums. The habitat that favours gliding is open, broken-canopy woodlands where the branches of trees are not in contact. Here, arboreal animals that need to range widely must either become semi-terrestrial or evolve the capacity to glide from tree to tree. This the ancestors of colugos did, but when gliding developed and at what stage of evolution in the colugo lineage is not known. It is possible, however, that among the diverse forms of proto-primates a gliding form emerged and that the colugo derives directly from that very early radiation. The pre-existence of efficient gliding mammals (anomalures in Africa, squirrels and colugos in Asia) has probably deterred primates from evolving gliding forms. Indeed, there is no evidence for there ever having been any kind of gliding primate.

Skeleton of colugo (Dermoptera, Cynocephalidae, Cynocephalus).

Resemblances, such as there are, between lemurs (Lemuriformes) and colugos suggest that the common ancestor of dermopterans and primates was not strikingly different from either in their facial morphology and slender limbs. Jonathan Kingdon

Profile and portrait views of colugo Cynocephalus sp. to compare with extant lemur Lemur sp. (bottom).

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Order PRIMATES

Order PRIMATES – Primates Primates Linnaeus, 1758. Systema Naturae, 10th edn, vol. 1. Hominidae (3 genera, 5 species) Cercopithecidae (15 genera, 68 species) Lorisidae (2 genera, 3 species) Galagidae (5 genera, 18 species)

Great Apes, Humans Old World Monkeys (Cercopithecids) Lorises, Potto, Angwantibos Galagos (Bushbabies)

p. 32 p. 92 p. 391 p. 404

Because every reader of these pages is a primate, the origins, diversity and radiation of our ancient mother-order have a peculiarly personal significance. Our historical search for self-knowledge now includes reaching back to chart our particular place within a family tree that we share with many other primate species, all related but to very varying degrees. Thus, describing primates and primate fossils accurately, and analysing their affinities and biology are particularly challenging and important tasks. Comparisons between one species and another, one group and another group, are an essential part of the scientific process, but such comparisons need extensive information on as many and as diverse species (both living and extinct) as possible. This volume has been designed to assist that process but it should be emphasized, from the start, that our knowledge is still extraordinarily, almost shamefully, incomplete for such an important group of mammals. The scale of our ignorance (but also the pace of recent discovery) can be gauged by the fact that a popular inventory of African primates published 28 years ago listed 43 species in 13 genera (Haltenorth & Diller 1980), while the most recent and most exhaustive review listed 95 species in 22 genera (Groves 2001). The taxonomy followed in this volume is a close (but not exact) match with the latter work and with Grubb et al. (2003). There are several reasons for this more than two-fold increase in recognized species, aside from the idiosyncrasies of authors. Molecular scientists have been a major influence in elevating the taxonomic status of already-described forms, and greater sensitivity to the significance of differences among populations has been another factor, but the actual scientific discovery of new forms of primates in the wild has also swelled the numbers since 1980. As a consequence, while this inventory of primates represents the most up-to-date review of all the known primates of Africa, it should still be regarded as provisional. In addition to increasing numbers, there are changes in how relationships are understood, sometimes precipitated by the discovery of new fossil primates. In general, ideas about primate origins have developed faster since 1980 than at any previous time. What explains the extraordinary abundance of primate species in Africa? Primates are essentially tropical and mainly arboreal animals. Africa is, at the grossest level of generalization, the largest area of equatorial land on earth and this fact could be taken as sufficient to explain primate abundance. However, it is the particular dispersal of humid-to-arid habitats and, as climates have fluctuated, the changing boundaries of major habitat blocks that helps explain the extraordinary diversity of primates. This evolutionary mechanism has been explored in some of the introductory chapters in Volume I of Mammals of Africa, as well as in some of the family and genus profiles in this volume. How many primate species are there in Africa, and how are they related to one another? The table above enumerates the families,

Stereoscopic vision in primates. Top: Whole field of vision registered separately on left and right sides of retinas. Some optic fibres from right half of both retinas transmit to right brain hemisphere. Likewise, retinal impulses from left half of both retinas travel to left side of brain’s visual cortex. Cross-over takes place in chiasma (at base of midbrain). Processing takes place in the lateral geniculate bodies of the thalamus at the back of the brain (in part after Ankel-Simons 2000). Bottom left: Visual orientation in tilted head of a strepsirrhine, the Potto Perodicticus potto. Bottom right: Less tilted head of a haplorrhine, the red colobus monkey Procolobus. Stereoscopy is likely facilitated by reduction of the olfactory apparatus.

genera and species that we recognize. The diagnostic attributes of primates are seldom clear-cut, largely because they retain many basal mammalian features. Even so, all, or nearly all primates share certain traits or trends. These are as follows: 1 A tendency for the brain, from foetus to adult, to be proportionally large. 2 Forward rotation and convergence of the eyes, and stereoscopic vision. 3 Loss of one pair of incisors and one pair of premolars. Thus, the dental formula for the majority of African primates is 2123/2123. 4 Nails rather than claws on most digits (a few non-African primates have claws on most digits). 5 Spreadable fingers on grasping hand, with a divergent and opposable thumb in most species. 6 Spreadable toes on grasping foot, with divergent big toe (hallux). 7 Compared to most other mammals (and allowing for size), slower foetal growth, longer gestation times and longer lives.

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Order PRIMATES

Some of these trends have been taken to their furthest degree in humans and great apes, implying that they are among the most ‘primate-ish’ of all primates! Among the diagnostic characteristics common to all primates are highly versatile hands with soft finger pads, long digits, relatively short palms, and very flexible wrists attached to long, relatively slender arms. It is of interest that primates possess an elaborated type of nerve ending, Meissner’s corpuscles, in the digital pads. These are, otherwise, found only in arboreal marsupials. This detail is of particular relevance for human evolution because these corpuscles give a special sensitivity to the hands and fingers. Although primates have ‘hands’ on all limbs (and were once called ‘quadrumanes’), the feet are a lot less versatile than the hands. The feet, however, have flexible ankles attached to powerfully muscled legs that, for a majority of species, propel the animal by running, leaping or bounding, mainly on branches and stems. In combination, the limbs provided a firm base for movement in all directions and through highly obstructed environments. Primates represent one of the basal or near-basal orders of placental mammals; the first primates presumably shared many traits with the earliest placental mammals. Matthew (1904), Martin (1990), Sussman (1991) and Cartmill (1992) consider it likely that all the earliest placentals were to some extent arboreal, and Lewis (1983) discusses the evidence for the hands and feet of early placental mammals being adapted to a combination of arboreal and terrestrial habits. Primates are an old group, originating at least as early as the Cretaceous, and, according to molecular analyses, share a common early ancestry with the Asian tree shrews and flying lemurs ( BinindaEmonds et al. 2007). These authors date the emergence of Primates as an order at ca. 94 mya (mid-Cretaceous) and calculate that the supercohort Supraprimates (or Euarchontoglires) separated from its sister supercohort (Laurasiatheria) ca. 102 mya. Murphy et al. (2001) place the latter divergence at 88–79 mya, while Wible et al. (2007) place it after 65.5 mya (late Cretaceous). While the earliest mammals may have emerged in cooler environments (see Mammalia, Volume I), primates are, today, overwhelmingly tropical, so the initial divergence between primates and other mammals (or, possibly, between Supraprimates and the rest) may have been partly geographic or latitudinal: probably within the Asiatic land mass. In terms of habitat, the extremities of tropical trees and shrubs represent, by volume, a high proportion of the plants’ biomass and occupation of space, a space almost continuously loaded with leaves, fruit and invertebrates (the latter being the likely food of the earliest primates). The differentiation of primates from other mammals probably involved a decisive adaptation to living in trees. Life within a dense lattice of fine branches, twigs and twiglets demanded flexible leverage, an efficient grasp and speedy reaction times. To this end, all primates have realigned their limb joints and articulations, evolving ingenious swivel points in the limbs and neck, a firm pelvic girdle, exceptionally dexterous, clasping hands and feet, and a relatively energetic life-style. There is some agreement among scientists that primates arose as arboreal, and perhaps nocturnal, placental mammals taking the form of very small, visually oriented invertebrate-eaters, possibly foraging quite systematically through the fine foliage. Cartmill (1974) supposed that ‘the last common ancestor of the extant

Old World anthropoids (Colobus, living)

Strepsirrhine (slow loris, living)

Tarsier (living)

diurnal lemur (Hadropithecus, recent) Omomyid (Necrolemur, 33 mya)

Adapid (Notharctus, 45 mya)

ancestral lemur (80 mya)

New World monkey (Cebupithecia, 15 mya)

ancestral anthropoid (Aegyptopithecus, 33 mya)

ancestral Haplorrhine (70 mya) basal primate (‘of modern aspect’, Teilhardina)

Outline of primate phylogeny showing skulls of five extant and six extinct lineages and likely phyletic relationships (after Martin 1990, Ross 1996).

primates, like many extant prosimians, subsisted to an important extent on insects and other prey, which were visually located and manually captured in the insect-rich canopy and undergrowth of tropical forests’. There has been some controversy, which has yet to be resolved, as to which early mammals can legitimately be termed primates. Thus ‘euprimates’ and ‘plesiadapoids’ occupy uncertain positions close to the evolutionary roots of primates. These controversies affect arguments about the timing of primate origins and diversification, as well as the diagnostic features of the order. Apart from offering some broad generalities about primate affinities and characteristics, our discussion by-passes such controversies here by beginning with an outline of the known history of primates in Africa. Widespread confusion has surrounded the crucial issue of how the order Primates should be broken down into its very diverse component parts. The most thorough early classification of primates (‘quadrumanes’) was by É. Geoffroy (1812a, b). He divided primates into two informal ‘families’, apes and monkeys (‘singes’ and ‘lemuriens’). The first ‘family’ he divided into Catarrhini and Platyrrhini; all of the second ‘family’ he included in a third group, Strepsirrhini. Haeckel (1874) originated the distinction between ‘half-monkeys’ (or ‘Prosimiae’) and ‘monkeys’ (or ‘Simiae’), based loosely on the schemes devised earlier by Illiger (1811) and É. Geoffroy (1812a, b). He lumped, under Prosimiae, tarsiers, a variety of living lemurs, and fossil forms. One of the earliest authors to align the tarsiers with monkeys and apes, rather than with lemurs, was Pocock (1918), who divided the primates into two grades, one comprising the lemurs, for which he revived É. Geoffroy’s (1812b) name‘Strepsirrhini’ (but spelling it with a single ‘r’), the other including tarsiers and anthropoids, for which 25

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he coined the name ‘Haplorhini’ [sic]. Initially, much more influential was Simpson’s (1945) revival of the Prosimii/Anthropoidea division, which was followed by Le Gros Clark (1959). Among mid-twentieth century authors, only Hill (1953) adopted Pocock’s insight. Groves (1989) revived Pocock’s scheme, abandoning Prosimii as a scientific category and dividing Primates into two extant suborders, Strepsirrhini and Haplorrhini. This arrangement, in which major taxa correspond to groups (clades) defined by exclusive common ancestry (Hennig 1950) has found wide acceptance and is followed in this volume. Strepsirrhini and Haplorrhini are generally agreed terms, but there is some disagreement about the best term to label the monkey and ape clade within the Haplorrhini. The name Simiiformes, proposed by Hofstetter (1982), has not found wide acceptance – nearly all biological anthropologists use Anthropoidea instead of Simiiformes. While we find Hofstetter’s (1982) arguments for using Simiiformes cogent, we go with the flow and, in this work, use Anthropoidea in its place. Central to the division of primates into Strepsirrhini and Haplorrhini are differences in the structure of their skulls and eyes, which relate to ancestral adaptations to night or day vision. However, the South-East Asian tarsiers, which are certainly Haplorrhini, are believed to be secondarily nocturnal (i.e. they derived from diurnal ancestors) (Cartmill 1970, Groves 1989, Ross 1996).This hypothesis has, however, yet to find unequivocal support from the fossil record. Dentally, tarsiers are extremely conservative but in the skull (notably the enormous orbits) and in the limbs (in particular the elongation of the calcaneus and navicular, and the extensive fusion of the tibia and fibula) they are extraordinarily specialized. Some measure of the age of Primates can also be gauged from recovery of fossils ascribed to the extant tarsier genus as Tarsius eocaenus from 45 mya (mid-Eocene) deposits in China (Beard et al. 1994). On present fossil evidence, strepsirrhines appear in Africa later than anthropoids, but the great diversity of lemurs in Madagascar must derive from an African source. This suggests that the earliest African lemuroids have escaped being found as fossils (Seiffert et al. 2004). The ultimate common roots between the Asiatic lorisids (subfamily Lorisinae) and African lorisids (subfamily Perodicticinae) can hardly be in question but Asian lorises form a monophyletic clade separate from that formed by African pottos Perodicticus and angwantibos Arctocebus. The Lorisidae split probably occurred during the early Miocene (23 mya; Goodman et al. 1998). The Asian and African lorisid clades show a large measure of convergence; for example, each has a larger, plumper representative (Nycticebus in Asia, Perodicticus in Africa) and a smaller, more slender representative (Loris in Asia, Arctocebus in Africa). This has sometimes led primatologists into misunderstanding the true phylogeny and its biogeographic significance. Only Africa, however, has the active, long-legged forms known as galagos or bushbabies (family Galagidae). The degree to which primates differ in terms of night vision (in nocturnal species) and colour vision (in diurnal species) remains an area of active research. This topic is discussed further in the profiles of Strepsirrhini and Haplorrhini. While many anatomical features of living primates are advanced, some strepsirrhine species retain very unspecialized teeth. The anterior dentition (‘toothcomb’) is, however, a dramatic modification of the ancestral primate pattern (selection for the comb derives in most, if not all, species from the need to keep specialized, scent-

dispensing fur in prime condition). In adapting to a frugivorous/ folivorous diet, from an originally insectivorous one, most African anthropoids developed blunter, more robust teeth set in more compact toothrows with the two mandibular components fused at the chin (only a few very large, non-African strepsirrhines have fusion of the symphysis). For more than half a century the earliest fossils of monkeys that were plausible ancestors for both OldWorld and NewWorld monkeys all came from 36–30 million-year-old (late Eocene–early Oligocene) deposits in Egypt (Andrews 1906, Simons 1963). The oldest likely primate fossil from Africa is the rather fragmentary Altiatlasius from Morocco (Sigé et al. 1990), at 57 million years old (late Paleocene), but its relationships remain uncertain. Altiatlasius was assigned by its describers to the extinct haplorrhine family Omomyidae. Gunnell & Rose (2002) suggest, however, that Altiatlasius might belong to an, as yet, poorly known separate radiation of early primates. Unfortunately, few primate-containing fossil deposits occur in Africa until the late Eocene. In 1992, a tiny, apparently anthropoid primate, Algeripithecus minutes, was discovered in Algeria and dated to 45–40 mya (midEocene) (Godinot & Mahboubi 1992).This, and later Egyptian fossils, show that a radiation of higher primates was already under way by the mid-Eocene. Seiffert et al. (2005a) describe the most complete early Anthropoidea from 37-million-year-old deposits in the Fayum, including two species of marmoset-sized Biretia, both with dentition that was consistent with their being within the ancestral lineage of later anthropoids. Noting that one of these, Biretia megalopsis, had enlarged orbits (implying nocturnal habits), E. Seiffert (pers. com.) considers this diversification of niches another indication that Anthropoidea were already long-established in Africa by the late Eocene (37 mya). Early occurrence, a diversity of species, their absence from the much more numerous and widely representative Eurasian deposits, plus the sheer abundance of diverse primates in the African Miocene (24–5 mya), has long supported the idea that most of the anthropoid primates, as we know them today, developed exclusively in Africa. This proposition remains true for the more derived forms but now needs significant qualification when it comes to ultimate origins. It is now theoretically admissible that one of the earliest of all placental mammals after the afrotheres to arrive from Asia was an ancestor for the higher primates. The recent discovery in eastern Asia of fragments of very small primates, Eosimias, makes it more likely that the earliest haplorrhines were not African (Ni et al. 2004). Combining tarsier-like and non-tarsier haplorrhine traits, the Eosimiidae are known from the mid-Eocene (ca. 45 mya) deposits in Burma and China (Beard et al. 1994). This supports the proposal that Asia was their place of origin and undermines the assumption of African roots for all the higher primates (Gebo et al. 2000, Beard & Klinger 2005, Ciochon & Gunnell 2006). Eosimias is unlikely to be the descendant of an immigrant out of Africa (partly because of the continent’s extreme isolation in the Eocene). If, as its discoverers claim, Eosimias is a very primitive anthropoid ‘monkey’, the earliest origins of anthropoids must lie in Asia, which is also where tarsiers, the closest relatives of anthropoids live (as well as the tree shrews and flying lemurs, the primates’ closest relatives). Fossil tarsiers of similar age to Eosimias have also been found in Asia. Even the fact that living tarsiers survive only in tropical Asia implies support for the idea

26

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Tentative composite phylogenetic tree for African primates (assembled from Steiper & Young 2006, Bininda-Emonds et al. 2007, Janec˘ka et al. 2007).

100

90

80

70

KT 60

50

40

30

20

10

0 mya

Papionini Macaca Cercopithecini Colobini Platyrrhini Lemuroidea Lorisidae KT Cretaceous

that, at the very least, a proto-anthropoid ancestor entered Africa from Eurasia. The supposed divergence between Asian eosimiids and African anthropoids has now been narrowed to some time during the Paleocene (65.5–55.8) (Ciochon & Gunnell 2006). Just how tarsier-like that ancestor was remains debatable, but the ultimate immigrant status of anthropoid primates in Africa has become much more plausible than it was a few years ago. North African fossil primates are few. Unless we include Altiatlasius as a precursor, early fossil strepsirrhines have yet to be found. The fossil primates documented so far in Africa are localized and far from the supposed equatorial heartland. None the less, it can be inferred that primates flourished in Africa throughout the Oligocene (33.9–23.0 mya). The catarrhine–platyrrhine split almost certainly occurred in Africa before founders of the platyrrhine branch (now exclusively American) drifted across a much narrower Atlantic Ocean in the Eocene, some 43 mya (Steiper & Young 2006). Primates with anatomy comparable to that of some of the Egyptian fossils are thought to have founded the platyrrhine or New World primate fauna (Dagosto 2002). Some time in the mid-to-late Oligocene (28–25 mya), the early catarrhines gave rise to two lineages; one ancestral to cercopithecid monkeys, the other to apes. The descendants of both branches were so successful that they eventually colonized other continents. Although the primate fossils from Egypt are relatively diverse, whatever richness there may have been throughout the rest of Africa is unknown until the latest Oligocene. This 10-million-year break, from which there are effectively no fossils, must have been a critical time for primate evolution. A series of important Miocene sites in Kenya and Uganda document the separation of Cercopithecoidea and Hominoidea, and also an astonishing abundance and diversity of catarrhine lineages that have since gone extinct. Of these, the most notable is the diverse and abundant family of ‘ancestral apes’ or ‘proto-apes’, the Proconsulidae. An important diagnostic detail, manifesting an advance in forelimb versatility, is the hinging of the humerus on the ulna. It is this detail that allows the Proconsulidae to be classed in Hominoidea, although they differed both from apes and monkeys in many other respects (Walker & Shipman 2005).

Palaeocene

Eocene

Oligocene

Miocene

A few Miocene catarrhines are known by nearly complete skeletons, showing that some were arboreal but slow and quadrupedal (Afropithecus), others were arm-swingers (Nacholapithecus) and yet others were mainly terrestrial (Equatorius) (Walker & Shipman 2005). Griphopithecus, a very close relative of Equatorius, may represent, and certainly exemplifies, the sort of early modern ape that spread out of Africa and flourished in Eurasia, where its remains have been recorded from deposits dated 17.0–16.5 mya (mid-Miocene) in Turkey and Germany (Begun 2000, Heizmann & Begun 2001). Molecular data suggest that the hominoid ape lineage split from the cercopithecoid monkey lineage some time during the mid- to late Oligocene (31–23 mya). Interestingly, hominoids are abundant in north-east African Miocene fossil sites, cercopithecoids are rare. Why the discrepancy? Were cercopithecoid monkeys more abundant anywhere else? Africa is a vast continent with comparatively few fossil sites, so it is not altogether surprising that fossils of early Cercopithecoidea have so far escaped discovery. This is especially so if southern or south-eastern Africa was the region for their differentiation (the rationale for which is discussed in Volume I, p. 80 and in subsequent profiles, pp. 90 & 155). The pre-eminence of apes was eventually overtaken by cercopithecoids. So far as we can deduce from fossils, the pioneers of this lineage were the now extinct Victoriapithecinae. Prior to 10 mya (mid-Miocene), this lineage split into the Colobinae and the Cercopithecinae. Colobinae fossils are common until the Pleistocene (1.8 mya) but virtually all fossil species of colobine eventually went extinct. Still later, the cheekpouch monkeys, the Cercopithecinae (another lineage with likely south-eastern Africa origins that are hidden from the fossil record) came to dominate the scene, as they do today. These developments are discussed in the profiles that follow. African forests of today contain five main primate groups: anthropoid apes, colobines, cercopithecines, lorises and galagos. Their distinctness at the generic level from Asian primate communities has been influenced by a biogeographic peculiarity. This is the existence of a ‘filter’, a semi-arid belt lying between Africa and Asia, that has blocked exchanges between forest-adapted faunas since the Oligocene (25 mya) and possibly even earlier. In particular, no forest-dependent primate has entered or left Africa since at least the Oligocene. 27

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Africa–Eurasia diffusion routes. Primates probably followed the ‘tropical’ route.

1. The cold northern or gazelle-horse route 2. The tropical Indian or monkey-porcupine route 3. The marine shoreline or dugong-flying fox route

Eurasian temperate biota Oriental/Asiatic tropical biota

The semblance of such an exchange might be suggested by treeliving mammals, such as squirrels that exist on both sides of the barrier, but all such immigrants can be shown, or inferred, to have derived from ancestors that were not wholly forest-adapted. These founding stocks were sufficiently versatile to cross by way of the narrow corridors that have periodically connected Asia and Africa. The filter has operated both ways, with less forest-limited primates leaving Africa to found Asian radiations. This, undoubtedly, explains the presence of apes, colobines and macaques in Asia, and may also apply to the lorisids. A significant complication of this pattern is that once an immigrant from Eurasia had dispersed as far south as the tropics, it was faced by an established community of true rainforest mammals. A combination of competition, disease and pre-adaptation to nonforest environments probably inhibited or slowed down successful invasion of the forest. On the other hand, for populations living in non-forest corridors, fluctuating climates must have periodically engulfed non-forest populations living in drier ‘corridors’ as forests expanded from both sides of the corridor. Such enforced exposure of Eurasian immigrants to African forest conditions would have exerted strong selective pressure and probably assisted the process of adapting (or‘re-adapting’!) to forest life. From the perspective of human evolution, the most significant of all these exchanges was the emigration of African apes to Eurasia during the early Miocene (19–17 mya, when the ‘filter’ was less arid) and the eventual ‘return’ of a versatile Eurasian ape about 10.5 mya ago, or earlier. This ‘out-of-Africa-and-back’ exchange best explains the evolution of modern apes and hominins in Africa (Stewart & Disotell 1998, Begun et al. 1997, Kingdon 2003). The immigrant

might have resembled Anoiapithecus brevirostris, a Eurasian tree-ape that shared its ancestry with the orang-utans (Pongo), or, perhaps, a descendant of the same lineage as Pierolapithecus catalaunicus. This medium-sized ape was recently described from a fossil in Spain from 13.0–12.5 mya (mid-Miocene) and is distinguished by having short, straight digits and mobile, typically ape-like, shoulders. Whatever its precise origins, the immigrant ape was ancestral to at least three distinctive lineages. One led to the gorilla (Gorilla) clade, while the other two led to the closely related chimpanzee (Pan) and human (Homo) clades. The success of this ape might have been helped by a well-developed strategic intelligence. Such an interpretation is hotly contested by some authors (Wrangham & Pilbeam 2001, Bernor et al. 2004), who believe that modern African apes derive from a resident African lineage. This is discussed elsewhere in this volume (see p. 35). The separation of primate lineages into arboreal equatorial populations living, for the most part, in the forests of Central andWest Africa (an area unseparated by natural barriers from drier habitats to the north), and terrestrial or semi-terrestrial ones (baboons, savanna monkeys and some galagos) in southern and south-eastern Africa, has many historical, evolutionary and ecological dimensions that have yet to be addressed. The nature of this forest/non-forest, centre-west/ south-east dichotomy has many implications for our understanding of the dynamics of primate evolution even though contemporary species are distributed over much wider areas. We hope that the profiles in this volume help stimulate the further research that is needed. Jonathan Kingdon & Colin P. Groves

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Suborder HAPLORRHINI

Suborder HAPLORRHINI – Haplorrhines: Tarsiers, Monkeys, Apes, Humans Haplorrhini Pocock, 1918. Proc. Zool. Soc. Lond. 3: 719–741.

In Africa, the Haplorrhini embraces all the Catarrhini or Old World monkeys, great apes and humans. The other (extralimital) members of this group are the Platyrrhini (or New World monkeys) and the Tarsidae, or Oriental tarsiers. In Africa there are two families, 18 genera and some 73 species of haplorrhines. Today the majority of species are confined to forests in the tropics but a few species, notably the baboons and savanna monkeys, occupy the temperate south and relatively dry areas south of the Sahara, sometimes with striking success. Of others, only humans have escaped the ecological constraints that limit the ranges of most contemporary African haplorrhines. Haplorrhines have all the traits enumerated in the profile of Primates but have larger brains than Strepsirrhini and, in general, are of larger size, with more species having partial or wholly terrestrial habits. All African species are diurnal. In general, diurnal and frugivorous species have greater acuity in daylight vision (having differentiated the structures of the inner eye to become more sensitive to colour and to particular wavebands). Most platyrrhines (except for howler monkeys Alouatta) have only a single medium/long-wave-sensitive locus, which is on the X chromosome, but there are two or (in some species) more alleles at this locus, so that whereas all males are dichromats, some (or even most) females are trichromats. In catarrhines (and independently in Alouatta) the medium/long-wave-determining locus has split into two, so that potentially all individuals are trichromats, males as well as females. Many interesting contributions on this topic are found in Anthropoid Origins: NewVisions (Ross & Kay 2004). One genus of South American monkeys, the owl monkeys Aotus, has become nocturnal (filling the galago niche in Amazonian forests). Interestingly, Aotus eyes and orbits have greatly enlarged and reverted to becoming close to monochromatic, so the animals have greatly reduced colour vision. This reversion and the differences between Old World and New World monkey vision raises many interesting questions about the selective forces operating on primate visual apparatus (Jacobs 1993, Wright 1996). The South American monkeys also include a dwarf marmoset that illustrates a very significant evolutionary process, heterochrony or, in this case, paedomorphosis by progenesis (Groves 1989), that could also be operating, but not so obviously, among some African primates, notably talapoin monkeys (Miopithecus spp.), and possibly Dryad Monkey Cercopithecus dryas. Most marmosets have a cryptic agouti-patterned coat and ‘babyish’ paedomorphic appearance while they are juveniles and the Pygmy Marmoset Callithrix pygmaea is no exception, being dull khaki and growing at the same rate as its larger congeneric, the Common Marmoset C. jacchus. At about 12 months old, Pygmy Marmosets suddenly stop growing and abruptly become sexually mature. They stay this way for the rest of their lives, resembling dwarfed, immature versions of their closest relative. Natural selection can, therefore, alter the setting of biological clocks over a large number of features, as in this case, or can operate on

Infant Patas Monkey Erythrocebus patas. Typical signs of paedomorphism are a diminished face and an enlarged brain.

a very few features, or perhaps a single feature, in others. Thus, selection for particular features, in this case ones that already exist in the ontogeny of the animal (e.g. small size, cryptic coat colour and squeaky vocalizations) can serve to open new niches within an established primate community. A similar mechanism may well have operated among the ancestors of Miopithecus, where the adults most resemble juvenile Patas Monkeys Erythrocebus patas (see illustration p. 251). While both Miopithecus and Erythrocebus have, today, greatly diverged both morphologically and ecologically, it appears that they derive from a common ancestor (Dutrillaux et al. 1980). Paedomorphism in talapoins may, therefore, have its roots in a similar selective process as that which gave rise to the Pygmy Marmoset. Similar processes are also likely to have operated in the evolution of another haplorrhine lineage, that of the Homininae. Modern Humans have many paedomorphic traits that are most easily illustrated with comparisons between adult human faces and those of juvenile apes. In this instance, juvenile appearance may be but one aspect of traits that have been favoured by selection, the others being less easily characterized aspects of juvenilia, such as psychological interdependency, curiosity, playfulness, susceptibility to social learning, and attraction to other group members. In any event, there is sufficient evidence to suggest that heterochrony and selection for paedomorphic traits is common in the Haplorrhini, with substantial implications for understanding the evolution of morphology and behaviour in this major group of mammals. Jonathan Kingdon & Colin P. Groves 29

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Hyporder ANTHROPOIDEA

Hyporder ANTHROPOIDEA (Infraorder: SIMIIFORMES) – Anthropoids: Monkeys, Apes, Humans Anthropoidea Mivart, 1864. Medical Times 1: 672.

Within the suborder Haplorrhini, the hyporder Anthropoidea (or infraorder Simiiformes) serves to distinguish the Old World monkeys, the New World monkeys (extralimital) and the hominoids from the infraorder Tarsiiformes and a third, extinct, infraorder, the Omomyiformes, which embraces a large group of fossil primates.This distinction reflects the biogeographic history behind the radiation of Primates. Although a fragmentary tarsier fossil, Afrotarsius, has been described from the Oligocene (33.9–23.0 mya) of Egypt, and another fragment from Ethiopia, their identification is challenged by Beard & Klinger (2005), who consider that the Tarsiiformes are an exclusively Eurasian group, a region in which the living and diverse genus Tarsius has been supposed to occur continuously since at least 45 mya (mid-Eocene). By comparison with Strepsirrhini, Anthropoidea can be diagnosed by less reliance on scent and more on vision. They lack a reflecting tapetum and have a greater degree of colour vision. The lachrymal bone lies within the orbit rather than outside it. The two halves of the mandible fuse together early in life (probably associated with a more vertical action of the incisors, which number two in each quadrant). Canine teeth tend to be larger and have deeper rooting. The three molars of each quadrant tend to have a squarer form. Most anthropoids are larger than most extant strepsirrhines. From an African perspective, the presence of Anthropoidea goes back to some uncertain and hotly contested dates when a small ancestor to all the living members of this group found its way to a peculiarly isolated African land mass. E. Seiffert (pers. comm.) thinks it possible that fossil fragments of Altiatlasius from 56-million-yearold late Paleocene deposits in North Africa (Ouarzazate Basin) could be stem anthropoids (also see Godinot & Mahboubi 1992, Beard & Klinger 2005, Seiffert et al. 2005a). This implies that anthropoid origins could be as early as the late upper Cretaceous. Steiper & Young (2006) calculate a molecular divergence date of 77.5 mya within a range of 97.7–67.1 mya (mid- to late Cretaceous), while Pennisi (2007) provides an estimate of 71 mya. These dates are much older than those proposed by Ciochon & Gunnell (2006), who put the divergence between Asian Eosimiids and Anthropoidea in the Paleocene (65.5–55.8 mya), and Gillman (2007), who estimates a 57-million-year-old origin for the Anthropoidea. Miller et al. (2005) think the fossil evidence showing a late Eocene presence in North Africa accords with an African origin for anthropoids. Tabuce & Marivaux (2005), instead, propose a mid-Eocene migration of an anthropoid ancestor to Africa.

Otolemur crassicaudatus

Lophocebus albigena

Skulls of strepsirrhine Otolemur crassicaudatus and anthropoid Lophocebus albigena. Simple rings surround strepsirrhine eyes whereas Lophocebus eye sockets are typical of all anthropoids in enclosing the eyes in bony cups.

After radiating within Africa, a single rafting established the ancestor of all New World primates in South America. The date of this event (in which the most plausible agency would have been a floating ‘island’ of forest trees) has been dated to 42.9 (52.4–37.3) mya (mid- to late Eocene) by Steiper & Young (2006). At 44 mya, Pennisi (2007) offers an estimate that is well within this range and a time when the Atlantic was very much narrower than it is today, particularly between today’s Guinea coast and north-eastern Brazil. Gillman (2007) has, instead, estimated 32 mya (early Oligocene), when the Atlantic had become quite wide. Among the Catarrhini, the two superfamilies, the Cercopithecoidea and the Hominoidea, diverged within Africa during the Oligocene, a radiation that is discussed in following profiles. Much later, and in succession, apes, colobines, macaques and hominins emigrated to Asia, as is detailed in the following profiles.This poses numerous challenging puzzles, which are only beginning to be addressed by scientists today. Jonathan Kingdon & Colin P. Groves

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Superfamily HOMINOIDEA

Parvorder CATARRHINI – Catarrhines: Old World Monkeys, Apes, Humans Catarrhini Pocock, 1918. Proc. Zool. Soc. Lond. 3: 719–741.

Catarrhini embraces the descendants of some primates that remained and flourished in Africa after the ancestors of Neotropical monkeys had left. Later, during the Oligocene (33.9–23.0 mya), this lineage gave rise to the two superfamilies Cercopithecoidea and Hominoidea. As the name implies, the catarrhines share simple down-pointing (Greek kata) nostrils, which have only a narrow septum between them, a feature that distinguishes them from the New World

platyrrhine, or ‘flat-nosed’ monkeys. Other features shared by all catarrhines are the reduction of the premolars to just two in each half of each jaw, and the development of true opposability of the thumb, such that the thumb can be rotated until its pulp faces that of the index finger. Colin P. Groves

Superfamily HOMINOIDEA – Anthropoids: Apes, Humans Hominoidea Gray, 1825. Annals of Philosophy 10: 338.

The superfamily Hominoidea embraces all the surviving apes, including gibbons and humans, as well as some fossil groups that have left no descendants (Afropithecidae, Oreopithecidae, Proconsulidae). In this, as in other aspects of primate higher taxonomy, we follow Groves (1989, 2001). Of living primates, we include the extralimital orang-utans (Pongo), together with the African great apes (Gorilla and Pan) and humans (Homo), in the family Hominidae, but we exclude gibbons (Hylobatidae). We place the African biogeographic entity (African apes and humans) in the subfamily Homininae and reserve the tribe Hominini for the many taxa of bipedal apes and proto-humans that flourished in Africa until quite recent times. For Africa, the Hominoidea comprises three extant genera and five extant species. Conservative and homocentric taxonomists argue that these rankings give far too little taxonomic weight to the peculiarity of humans. Until relatively recently, humans had been placed in their own family, leaving the great apes in a paraphyletic family Pongidae; such an arrangement sacrifices the (phylogenetic) information content of taxonomy for mere convenience, with an anthropocentric flavour. A school of taxonomists who argue for a strict time-ranked classification (Schneider et al. 1997, Goodman et al. 1998) would rank Hominoidea as no higher than a family because this grouping probably diverged from the Cercopithecoidea later than the Oligocene/Miocene boundary (23 mya; see temporal/phylogenetic tree of hominoid relationships on p. 27). Strict adherence to such a system might well, as Goodman et al. (1998) argued, put humans and chimpanzees in the same genus and would lump many very distinctive primates in a small number of genera. While this may, in the end, prove to be justified, in the interim we feel it best to remain conservative. We have, therefore, retained most well-established genera and subgenera, and even recognized some controversial new ones. The divergence between hominoids and cercopithecoids is of special interest because, on present evidence, it occurred within

Africa at a time when the continent was particularly isolated from other land masses. From fossil anatomy we can correlate differences in body form and gait with several ecological, climatic and behavioural differences. The late Oligocene (23 mya) was a period of global cooling, preceded by the first formation of an Antarctic ice-sheet and a substantial retraction of tropical forest in Africa (see ‘Africa’s Environmental and Climatic Past’, Chapter 4, Volume I). The proto-cercopithecoids seem to have adapted to these changes in climate by becoming longer-backed, more terrestrial, faster, and better able to forage and escape predators in more open habitats.

Body proportions as displayed in schematic skeletons of (left) Robust Chimpanzee Pan troglodytes and (right) Australopithecus (Praeanthropus) afarensis.

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The biogeographic dimension to this divergence can be related to the outline discussed in the introductory chapter on mammalian evolution (Chapter 6, Volume I). Because a large proportion of dry, more temperate Africa was south of the Equator during the Oligocene (more so than today because the continent has meanwhile drifted northwards), there are good grounds for supposing that the cercopithecoids had mainly south-eastern origins. In this divergence, the hominoid lineage can be seen as the more conservative in the sense that they remained the most committed arborealists, with very mobile joint articulations and compact, shortbacked trunks. Certainly some forms became adapted to less than wholly forested habitats, but, in general, the early apes seem not to have readily accommodated to habitats where travelling and foraging on the ground was required. Because closed forests, with yearlong supplies of plant and animal foods, are ultimately dependent on tropical temperatures and rainfall, apes, then as now, probably preferred equatorial forests and/or dense woodlands along a centre-

west axis. It is, therefore, possible that a catarrhine ancestral stock split along latitudinal lines and that hominoids dominated northern and equatorial Africa (remembering that there was no Sahara desert at that time!), while the earliest cercopithecoids were of south-eastern provenance. That it was hominoids, not cercopithecoids, that first got out of Africa (ca. 19 mya) lends increased weight to this hypothesis. The Hominoidea are easily distinguished from their closest relatives, the Cercopithecoidea, by such characters as the lack of a tail, the broad rib cage with the scapula at the back, and the greatly enhanced rotatory ability of the shoulder joint. The Hominoidea lack the outstanding dental specialization of the Cercopithecoidea – the bilophodont molars (and premolars, the sectorial anterior lower premolar, of course, excepted); the morphology of the postcanine dentition in the Hominoidea retains an overall plesiomorphic condition. Colin P. Groves & Jonathan Kingdon

Family HOMINIDAE HOMINIDS: GREAT APES, HUMANS Hominidae Gray, 1825. Annals of Philosophy 10: 344.

Homininae Gorilla (2 species) Pan (2 species) Homo (1 species)

Gorillas Chimpanzees Humans

p. 35 p. 53 p. 74

The Hominidae, in the sense that we use it in this volume, follows the taxonomic arrangements of Groves (2001).This taxon essentially clumps all the larger apes, Asiatic and African, and humans. Linnaeus (1758) placed humans in the order Primates, but most of his successors demurred, preferring to set apart ‘man’ in a separate order, Bimana. The most conspicuous exception was Gray (1825), who first recognized and named the family Hominidae, which he divided into two sections, as follows: † Tail none. 1. Hominina: Homo. 2. Simiina: Troglodytes, Geoff. Simia, Lin. Hylobates, Illiger. †† Tail long or short (section containing Old World monkeys).

Troglodytes was the generic name at that time used for the chimpanzee, and Simia for the orang-utans, while Hylobates is the generic name still in use for one of the genera of gibbons. Gray was thus well ahead of his time, not only in including humans in the Primates, and in the group we would now call catarrhines, but in the same family as the great and lesser apes. Today, it is almost universal to place the great apes in the Hominidae, and has been so since the 1980s, but it was not until the last years of the twentieth century that the gibbons were also included in the Hominidae (Goodman et al. 1998), although they are still more usually placed in a separate family, Hylobatidae, though within the super family Hominoidea along with the Hominidae and some fossil families. The origins of this group are deeply controversial, with some scientists believing that the ‘great apes’ arose and differentiated

within Africa and only later entered Asia. Stewart & Disotell (1998), however, showed that, according to the fossil evidence, although the Hominidae probably arose within Africa, an initial diversification in Asia is much more parsimonious. Certainly the evidence for gibbons (Hylobatidae) being of wholly Asian origin is generally accepted (there has never been any evidence for African gibbons or protogibbons). Furthermore, Eurasian fossils (notably Oreopithecus and Lufengpithecus) imply that the Ponginae (to which the orang-utan belongs) and gibbons share common Eurasian roots. It seems more probable, therefore, that the African apes arose from a Eurasian ‘returnee’ than that they arose from an unknown lineage within Africa. The family Hominidae contains not only Gorilla, Pan, Homo and Pongo, but also many fossil forms, notably Sivapithecus, Dryopithecus and Graecopithecus in Asia and a variety of later African fossil taxa (see profiles for Homininae and Hominini). Today, Asian and African apes range through quite restricted localities within the total rainforest and neighbouring areas of their respective continents. This restriction is undoubtedly partly due to competition with other primates, including humans. Ranges are also likely to have been pruned by climatic fluctuations, even tectonic events. In addition, the heavyweights, orang-utans and gorillas, seem to be poor dispersers, a limitation that earlier, lighter and more versatile apes, such as Dryopithecus spp., seem to have escaped. For example, Dryopithecus fossils are extremely widespread and numerous in Europe between 13 and perhaps as little as 9 mya (mid-Miocene). The possible significance of such differences is discussed in the Homininae profile. It suffices here to point out that a newly discovered great ape, the nearly 10-million-year-old Nakalipithecus nakayamai (Kunimatzu et al. 2007), from a late Miocene deposit in Kenya, most resembles the Eurasian Ouranopithecus and is consistent with the ‘returnee hypothesis’ (Disotell & Tosi 2007).

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The most obvious features shared by all members of the family Hominidae include the relatively shortened, more robust canine teeth of the males, the presence of at least the rudiments of a metaconid (second cusp) on the anterior lower premolar, the reduced hair density on the body, the reduction in the number of thoracolumbar vertebrae and the short and stout vertebral bodies, the deep mandible (especially its symphysis), and the separation of the wrist bones from the ulna by a meniscus (giving the wrist greater flexibility). Colin P. Groves & Jonathan Kingdon

Pronation and supination of the human hand is made possible by rotation of the ulna and radius.

Subfamily HOMININAE – Hominins: African Great Apes, Humans Homininae Gray, 1825 Annals of Philosophy 10: 338.

This subfamily is primarily made up of a large number of fossil genera (extinct hominins, australopithecines and others), with only Modern Humans and African apes surviving. Groves (2001) and Grubb et al. (2003) list two species of Gorilla, two species of Pan and one species of Homo. We follow the same arrangement here. These five species are the sole survivors of a much larger intra-African radiation of large apes and hominins. The detailed anatomy of this African radiation shows the following differences from their close Asiatic relatives, the orang-utans (Pongo). The premolar row is shortened compared to the molars. The forearm is shortened, the brachial index being below 100. In the wrist, os centrale is fused to the scaphoid; the talus (astragalus) is nearly as broad as it is long; the calcaneus has a long, broad ‘heel’. The axillary organ, a coalescence of apocrine glands in the armpit, is large and elaborated. The scalp is more densely haired than the body. The intestine is long, more than nine times the head and body length. These features appear to be related to a more semiterrestrial life compared with a basic rainforest arboreal niche, and some de-emphasis (notably among some gorilla populations and among humans and their ancestral lineage) of frugivory. The broad talus and the developed ‘heel’ indicate efficient locomotion on the ground, and the shortened forearm and more compact wrist strongly suggest a weight-bearing role for the forelimbs. Tolerance of nonforest environments is suggested by the thickly haired scalp, and the importance of a complex, compact social organization is indicated by the development of the axillary scent organ. The ability to subsist on terrestrial herbaceous vegetation (THV), during periods of scarcity of more preferred foods, is implied by the reversal of molar/ premolar emphasis and by the lengthened gut.

In gorillas and chimpanzees, the ‘weight-bearing role of the forelimbs’ involves knuckle-walking, a unique form of locomotion seen in no other mammal. The weight of the foreparts is borne on the medial phalanges of the hand: not only is the proximal/medial joint held at a right-angle, but the entire wrist region must be held rigid, resisting the compressive forces that would tend to hyperextend the joints. There are both a specialization of the mid-carpal articulation (known as conjoint rotation) and a prominent dorsal ridge on the distal end of the radius, helping to stabilize the wrist and hand in knuckle-walking position. Given that gorilla and chimpanzee are not sister-groups, but rather chimpanzee and humans together form a sister-group to gorilla, it may be that the ancestor of the gorilla and the ancestor of the chimpanzee independently developed knucklewalking specializations. The alternative hypothesis, that the common ancestor of the Homininae developed these specializations and that they were lost somewhere along the human lineage, is, however, more parsimonious.This prediction was verified by the Richmond & Strait’s (2000) analysis of the distal radius of Australopithecus anamensis and A. afarensis, mid-Pliocene (3.6 mya) members of the human lineage, in which they demonstrated the persistence of knuckle-walking traits. Based on molecular data, the Ponginae and Homininae lineages separated 16.5–12.5 mya (mid-Miocene), gorilla and human– chimpanzee diverged 12.0–7.1 mya (late Miocene), and the human–chimpanzee split occurred 7.0–5.5 mya (Raaum et al. 2005, Perelman et al. 2011, Roos et al. 2011, Scally 2012). There is claim (Suwa et al. 2007) of a possible gorilla ancestor, Chororapithecus, from Ethiopia, dating at 10.5–10.0 mya (the claimed dental similarities to the gorilla are real enough, although more evidence is needed to show whether they are genuine synapomorphies or convergence). 33

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The differences between surviving African apes and Modern Humans formerly seemed much greater than could easily be explained. None the less, when ape and human anatomy was examined in detail virtually all the physical differences were long ago shown to be ones of changed proportion or differing linear dimensions. In almost every case these changes have come to be

plausibly correlated with environmental or behavioural changes during the evolution of both African apes and humans. Meanwhile, an ever-richer treasure-trove of fossils has revealed a diverse number of Homininae, illustrating many intermediate forms between apes and humans, as well as some surprising offshoots (see Hominini and illustrations on p. 71).

Hands and ‘small object precision handling’, as the interface with their environment, drove hominin evolution. Left: Top to bottom, ten drawings of ape hands. Right: Top to bottom, six drawings of human hands.

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Reconstruction of ‘Toumai’ Sahelanthropus tchadensis. Top: Supposed appearance. Bottom: Skull (as reconstructed in Kingdon 2003).

Prominent among these fossil members of the Homininae are some European genera, notably Anoiapithecus, and also Dryopithecus and Ouranopithecus, which are robust with heavily built facial skeletons, including supraorbital tori. The second of these (the correct name may in fact be Graecopithecus), known from approximately 9 mya deposits in Greece, may be a very primitive member of the gorilla lineage, but, as Begun (2002) has pointed out, the similarities – mainly related to robusticity – may be symplesiomorphic. This makes sense in the light of the extreme robusticity shown by the controversial Sahelanthropus, which has been represented as the earliest evidence for separation of the human lineage (Brunet et al. 2002). It has also been argued, however, that Sahelanthropus is not clearly a member of any of the separate hominine lineages but rather represents a ‘presplit’ population close to the common stock of African apes and humans (Kingdon 2003, Wolpoff et al. 2006). Colin P. Groves & Jonathan Kingdon

Tribe GORILLINI Gorillas Gorillini Frechkop, 1943. Exploration du Parc National Albert, Mission S. Frechkop (1937–1938). 1. Mammifères, p. 11.

Because there has been a generally felt need to differentiate humans and bipedal apes from quadrupedal ones, the former have tended to be placed in the tribe Hominini. This has left the affinities of quadrupedal apes unanswered. Groves (1986) has pointed out that cladistic rules absolutely prohibit the clustering of gorillas Gorilla spp. and chimpanzees Pan spp. into a single group that does not include Modern Humans Homo (as was proposed by Andrews 1987). Any cladistically acceptable arrangement, therefore, requires there to be two tribes: Gorillini and Panini. As far as the living fauna is

concerned, both tribes are synonymous with the genera Gorilla and Pan, and for most intents and purposes are effectively redundant. The diagnosis that follows is, therefore, appropriately brief. The tribe Gorillini has a single extant genus. A second genus, Chororapithecus, provisionally allocated to this tribe, is known from the late Miocene (10.5–10.0 mya) (Suwa et al. 2007) and is mentioned in the profile for Gorilla. Colin P. Groves

GENUS Gorilla Gorillas Gorilla I. Geoffroy,1852. Comptes Rendus de l’Académie des Sciences, Paris 34: 84.

Polytypic genus. In the latter half of the nineteenth century and early twentieth century, a large number of species and subspecies of the genus Gorilla were described. Coolidge (1929) united all of them into a single species, Gorilla gorilla, with two subspecies, namely G. g. gorilla and G. g. beringei, regarding all the other named taxa as synonyms of one or the other. Subsequent authors have mostly maintained the single-species arrangement; the main exception being Schultz (1934), who regarded Coolidge’s two subspecies as distinct species, although it seems that he may have inadvertently allocated a few specimens to the wrong species. It was not until over half a century later that Groves (2000b), once again arguing for the adoption of a Phylogenetic Species Concept, separated G. gorilla and

G. beringei at the full species level. Diagnoses of these two species, and their subspecies, are given in Groves (2001). A brief history of gorilla taxonomy, with something of the rationale behind the original description of the different species in the early phase of gorilla taxonomy, is presented in Meder & Groves (2005). Gorilla gorilla (Western Gorilla) is found mostly in lowland forest from the Congo–Oubangui R., DR Congo, westwards to the coast. The Sanaga R., Cameroon, is the northern border of the continuous area of distribution. There are outlying populations to the north-west in the Ebo Forest to the north of the Sanaga R. and in the montane forests of Cross River District on the Cameroon–Nigeria border. Gorilla beringei (Eastern Gorilla, including, but not limited to, the 35

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famous Mountain Gorilla) is confined to the forests, both lowland and montane, of Kivu District (CE DR Congo), the montane forests of the Virunga Mts (where DR Congo/Rwanda/Uganda meet), Bwindi Impenetrable Forest (SW Uganda) and, from here, westward across the Uganda/DR Congo border into the Sarambwe Forest. The genus Gorilla is characterized by extreme sexual dimorphism, mature !! weighing at least two-and-a-half times as much as mature "", with much larger sagittal crests (very rarely absent in adult !!, and present in only about 20% of adult "") and larger nuchal crests. Both sexes are dark in colour, the naked skin of the face, ears, chest, palms and soles being jet black (with occasional deep pigmented spots on the palms and soles); the pelage is jet black in G. beringei, and a deep blackish-brown, often with a red crown, in G. gorilla. In both species the mature ! has a grey to white ‘saddle’ on the dorsum; between the shoulders and the rump in G. beringei, but spreading back to the thighs in G. gorilla. Infants have a narrow white tuft of hair above the anus. The ears are remarkably small, but lobed. The nostrils are large, slightly raised above the level of the nose and upper lip, and often ‘padded’. The skull is not unlike that of Pan spp., but can be distinguished by the more anteriorly prominent, rounded supraorbital torus, continued from side to side across the glabella with almost no break. The lateral orbital pillars are likewise prominent and rounded. The interorbital pillar has a median ridge, which runs down the internasal suture. The incisors are narrow and unspecialized, both upper and lower. The canines are elongated in adult !!, more than in Pan. The molars are characterized by high crystalline cusps, with prominent crests running between them; the enamel is somewhat wrinkled, and thin, so that the dentine ‘horns’ penetrate considerably into the cusps. The cusps are peripherally situated on the occlusal surfaces, so that the central basin is wide; the upper molars have wide but short proximal and distal foveae, separated by the crests from the central basin. These features indicate an enhanced shearing function, related to their dependence on terrestrial herbaceous vegetation in the diet. The thorax is very broad, widening very considerably from first to last rib. All vertebrae, but particularly the lumbars, are short and broad. The iliac crests are extremely broad, second only to Homo. The intermembral index (ratio of arm bones to leg bones) is about 112–120, higher than in Pan. The knuckle-walking characters are well developed, the hands are short and wide. The toes are short; the length of the heel, the length of the sole and the relative lack of divergence of the great toe are second only to Homo among the Hominoidea. These, and other terrestrial adaptations, have been described in detail, illustrated and tabulated by Sarmiento (1994). Compared to other hominids, growth and development in gorillas is surprisingly rapid. Though the gestation averages 257 days compared to 228 days for Robust Chimpanzees Pan troglodytes (and 240 days for orangutans Pongo spp.), all the other parameters are shorter than for other hominids: interbirth interval (between surviving infants) around 4.2 years in G. beringei and 5.2 years in G. gorilla, compared to 5.4 years or more in P. troglodytes; age at weaning 4 years or less in G. beringei, 5–6 years in G. gorilla, cf. 4–5 years in P. troglodytes; menarche at 7.0–7.5 years in G. beringei and 6.5–8.5 years in captive G. gorilla, cf. 10–11 years in P. troglodytes; menstrual cycle 28 days in G. beringei and 32–33 days in captive G. gorilla, cf. 36 days in P. troglodytes (Groves & Meder 2001). Male gorillas reach the ‘blackback’ stage, when they are sexually but not physically (or

socially) mature, at age ten years in G. gorilla, perhaps even earlier in G. beringei, and reach the ‘silverback’ stage of full physical maturity at 18 years in G. gorilla (Breuer et al. 2009) and perhaps only 15 years in G. beringei (Watts & Pusey 1993). Groves & Meder (2001) calculated mean ages at death for G. b. beringei reaching maturity as follows: "": Virunga Mts, 24 years (but 32 years according to Harcourt & Stewart 2007a); !!: Virunga Mts, 20–27 years (25 years according to Harcourt & Stewart 2007a). This compares with P. troglodytes at Gombe (W Tanzania) and Kibale (SW Uganda), where a " who reaches maturity can be expected to survive into her early or mid30s, and a ! to 29 years (Gombe) and 41 years (Kibale). These are, of course, mean figures, but maximum achieved ages also seem low for G. beringei, the mid-40s, compared with the 50s in P. troglodytes. About ten years may have to be added to these maxima for captive individuals, although Harcourt & Stewart (2007a) note that gorillas run through their life history stages at much the same rate in captivity as in the wild, whereas chimpanzees grow and reproduce at much faster rates in captivity. These life history parameters are surprising because one would predict late weaning and age at maturity, long interbirth intervals and long life in large-bodied primates (Harvey et al. 1987). Groves & Meder (2001) argue that gorillas may be considered in the traditional sense to be r-selected. One would also, according to this scheme, predict large brain size, but in gorillas the encephalization index is actually less than for other hominids. Until the twenty-first century, the gorilla lacked a fossil record. This recently changed: Pickford & Senut (2005) described a few, mostly fragmentary, teeth from Kapsomin and Cheboit in the Lukeino Formation of the Tugen Hills, Kenya, the same sites (dating to 5.9 mya) where the earliest known hominin, Orrorin tugenensis, occurs. More recently still, Suwa et al. (2007) described a new genus and species, Chororapithecus abyssinicus, from Chorora, Ethiopia, dated at somewhat over 10 mya; this has the characteristic crest formation, peripheral cusps and short mesial fovea of modern gorillas, but thicker enamel and lower cusps, and less developed crista obliqua, suggesting a primitive, presumably ancestral, morphology. The distribution of gorillas today is strikingly disjunct: that of G. gorilla extends east as far as the Oubangui R., whereas that of G. beringei does not begin until east of the Lualaba R., DR Congo. Even within their distributional areas, both species show patchy distributions. Gorilla g. gorilla populations are quasi-continuous from the Congo R. estuary to the Sanaga R., then there is a considerable gap to the range of G. g. diehli to the north-west. Gorilla beringei populations are also quasi-continuous in the Kivu lowland and mountain regions of E DR Congo, while those of the Virunga Mts (i.e. G. b. beringei) and the Bwindi–Sarambwe Forest represent further isolates. What caused the enormous gap between the distributional areas of the two species, and how long has it existed? Thalmann et al. (2005), using mtDNA, calculate that the two species separated 1.3 mya, and later (Thalmann et al. 2007), using 16 noncoding autosomal sequences, give a range of 1.6–0.9 mya. A more recent study puts the divergence time at 1.75 mya (Scally et al. 2012). This presumably marks the time of some geographic disjunction, and Thalmann et al. (2007) point to geological changes during that period. Yet the fact that some of these mtDNA lineages are shared between the two species indicates that there has been more recent gene flow between them, i.e. that the ranges have been in contact again at one or more times since their

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Individuality in the faces of gorillas Gorilla. Facial differences vary with region, age, sex and emotion (from Kingdon 1990).

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Western Lowland Gorilla Gorilla gorilla gorilla (from Kingdon 1971).

initial separation. Thalmann et al. (2007) argue that this more recent gene flow was male-mediated and asymmetrical (predominantly from beringei to gorilla), and ceased about 77,700 years ago. It is possible that the ranges of the two species may have approached each other again very recently. First, some (the exact number, whether three or four, is unclear) gorillas were said to have been shot near Bondo, on the Uele R., DR Congo, in 1898. As discussed by Hofreiter et al. (2003), these specimens, now housed in the Museum for Central Africa in Tervuren (Belgium), are indistinguishable morphologically from G. gorilla (despite having been referred to a distinct subspecies), and a mtDNA sequence obtained from one of them is nested within sequences of that species. There are uncertainties connected with the provenance of at least some of the specimens, and Hofreiter et al. (2003) doubt whether the locality is accurate, although this would not necessarily follow from their findings. It is certainly plausible that G. gorilla followed the expansion of the western central African rainforests north of the Grand Cuvette of the Congo R. during climatic amelioration at the end of the Pleistocene (10,000 years B.P.), and that one or more population isolates might have remained in northern DR Congo until very recently. The question of what might limit the distribution of gorillas has been raised by Groves (1971), who noted that gorillas seem to largely avoid both marshy forest and monodominant Gilbertiodendron forest. The latter forest type has little ground vegetation, and permanent residence in that type of forest by most terrestrial herbivores, such as gorillas, is difficult or impossible. Hart et al. (1989) argue that

monodominant forests of this type are those that have remained undisturbed over relatively long periods. Strikingly, charcoal samples from what are now Gilbertiodendron dominated formations in the Ituri Forest indicate that these areas were mixed forest less than 1000 years ago (Hart, T. B. et al. 1996). The implication is that, over the course of long periods of climatic stability and minimal environmental (including human) disturbance, shade-tolerant species of poor dispersal ability, such as Gilbertiodendron dewevrei, would very gradually spread and take over from the mixed forest, limiting, if not excluding, herbivores such as gorillas. When looking at distribution maps, it is striking that, with very few exceptions, red colobus monkeys Procolobus spp. occur only where gorillas do not. The gorilla heartlands of the western central African region and the Kivu/Central African Rift region are almost without red colobus, which on the contrary are abundant in the closed-canopy monodominant forests where gorillas are unable to exist. They appear to coexist only in a few regions: Kahuzi-Biega and Itombwe (E DR Congo), Ebo Forest, Ngotto (SW Central African Republic) and east of Motaba (NE Congo). It would be of great interest to know whether their apparent coexistence in these regions is broad-scale only, and the two taxa maintain separate micro-habitats, or whether there are indeed places where a silverback gorilla may look up and see a red colobus looking down at him. Colin P. Groves

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Gorilla gorilla WESTERN GORILLA Fr. Gorille de l’Ouest; Ger. Westlicher Gorilla Gorilla gorilla (Savage in Savage & Wyman, 1847). Boston Journal of Natural History 5: 417. Gabon Estuary, Mpongwe country, Gabon.

Taxonomy Polytypic species. The history of gorilla taxonomy is a long and complicated one, and is covered in detail by Groves (1966, 2003) and Sarmiento & Oates (2000). An overview of the taxonomy of the Gorilla spp. is presented in the Mountain Gorilla Gorilla beringei profile. Two subspecies of G. gorilla are recognized: Western Lowland Gorilla G. g. gorilla and Cross River Gorilla G. g. diehli. Formally referred to as G. g. gorilla, recent morphological and molecular studies indicate that the Cross River Gorilla is as different from G. g. gorilla as is G. b. beringei from some populations of Grauer’s Gorilla G. b. graueri (Oates 1998, Sarmiento & Oates 2000, Oates et al. 2003). Time of divergence ca. 17,800 years ago (Thalmann et al. 2011). As such, G. g. diehli was revived by Sarmiento & Oates (2000) and widely supported (Groves 2001, 2005c, Grubb et al. 2003, Oates et al. 2007, Sunderland-Groves et al. 2007, Nicholas et al. 2009, Oates 2011). Taxonomic status of gorilla populations in Ebo/Ndokbou, SW Cameroon, awaits clarification (Groves 2005a). Synonyms: adrotes, africanus, castaneiceps, diehli, ellioti, gigas, gina, halli, hansmeyeri, jacobi, matschiei, mayêma, savagei, schwarzi, uellensis, zenkeri. Chromosome number: 2n = 48 (Romagno 2001). Description Very large (adult !! ca. 170 kg, adult "" ca. 60 kg), small-eared, tailless, brown-grey or brownish-black, mostly terrestrial primate. Well-developed supraorbital ridges. Nose large, flattened. Nostrils large. Nasal septum with projection (‘lip’) above. Nasal openings nearer to mouth than to orbits. Eyes small, dark brown. Ears small, flat, black or brown. Pelage brownish-grey or brownish-black except crown, which is often brownish to reddishbrown. Bare skin of face, hands and feet black. Length, colour and distribution of hair variable. Adult !! have well-developed sagittal crest and completely greyish-silver ‘saddle’ on the back (i.e. ‘silverback’) and often on the thighs. Adult "" ca. 35% the weight of adult !! and lack a well-developed sagittal crest.

Western Lowland Gorilla Gorilla gorilla gorilla adult female and young.

Geographic Variation G. g. gorilla Western Lowland Gorilla. Occupies all of the range of G. gorilla except that portion in the Cross R. area on the Nigeria– Cameroon border. Longer/larger skull measurements. Adult !! from the ‘coastal sample’ (n = 71), which represent the smallest of the G. g. gorilla subpopulations: mean greatest length of skull = 296 mm (S.D. = 16.6); mean cranial length = 196 mm (S.D. = 13.7); face height = 146 mm (S.D. = 10.1); but relatively narrow mean biorbital breadth = 136 mm; and mean bizygomatic breadth = 174 mm (Groves 2001). Cheektooth surface area for adult !! from various sites: mean = 1098 mm² (S.D. = 103, range 954–1369, n = 58). Cheektooth surface area for adult "" from various sites: mean = 915 mm² (S.D. = 66, range 775–1042, n = 28) (Sarmiento & Oates 2000, Sarmiento 2003). G. g. diehli Cross River Gorilla. Confined to the upper Cross R. forest on the Nigeria–Cameroon border. Shorter/smaller skull measurements (Sarmiento & Oates 2000, Groves 2001). Adult !! (n = 25): mean greatest length of skull = 183 mm (S.D. = 13.7); mean cranial length = 183 mm (S.D. = 13.7), face height 140 mm (S.D. = 7.4); but relatively broader mean biorbital breadth = 136 mm; and mean bizygomatic breadth = 176 mm (Groves 2001). Cheektooth surface area for adult !!: mean = 957 mm² (S.D. = 84, 807–1159, n = 32). Cheektooth surface area for adult "": mean = 839 mm² (S.D. = 72, range 707–960, n = 17) (Sarmiento & Oates 2000, Sarmiento 2003). Similar Species Pan troglodytes. Sympatric below ca. 2300 m. Smaller (adult !! 3000 G. g. gorilla in 2011 (H. Ruffler & M. Murai pers. comm.). In 2009, total number of G. g. gorilla estimated at >150,000 (F. Maisels pers. comm. in Pain 2009). This is considerably more than earlier estimates by Harcourt (1996), Kemf & Wilson (1997), Butynski (2001) and Plumptre et al. (2003a) of 111,500, 111,000, 95,000 and 110,000, respectively. The current number of G. g. gorilla is not known because (1) much of the range has never been surveyed, (2) much of the survey data are now out-dated, and (3) commercial hunting and the Ebola virus have dramatically reduced numbers during the past two decades (Ferriss 2005, Tutin et al. 2005).

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There are ca. 200–300 G. g. diehli (Oates et al. 2003, 2007, Sunderland-Groves et al. 2007, Nicholas et al. 2009, Bergl et al. 2011). Only ca. 0.2% of G. gorilla are G. g. diehli, making this the rarest subspecies of gorilla. Typical density of G. g. gorilla is 0.25 weaned ind/km², although they occur at higher densities in Marantaceae and swamp forests. At some sites there are 3–25 gorillas/km², while poor habitat may host as few as 0.1/km² (Poulsen & Clark 2004, Rainey et al. 2009). Half of breeding group members are immatures (Lokoué 48%, Maya 56%; Gatti et al. 2004). At two sites in Congo, 5% of the population is solitary !! (Magliocca et al. 1999, Parnell 2002a).

Finding enough good quality food, especially patchily distributed fruit, is a challenge for G. gorilla. Dozens of types of fruit are produced in lowland forest but individual trees bear fruit for only a few days or a few weeks of the year. Thus, greater intelligence is needed to efficiently exploit food sources in lowland tropical forests than in G. b. beringei’s more heterogeneous and less complex montane environment. Gorilla gorilla is likely to have similar capacity to Pan troglodytes for mental mapping, to remember locations, and to exploit ephemeral fruit sources by anticipating ripening (Williamson 1988). P. troglodytes has an acute memory of location and perception of relative distances (Menzel 1973), and uses spatial memory and mental mapping (Boesch & Boesch 1984). Gorilla g. gorilla possesses Adaptations Diurnal and semi-terrestrial. Gorilla g. gorilla forages extensive knowledge of food resources and animals travel long intensively early in the day in the vicinity of nest-sites (Williamson et distances to find rare foods (e.g. travelled 4 km in two days to feed on al. 1990), alternating periods of feeding and travel throughout the Treculia obvoidea, Tutin 1997a). An indication of species differences day. Gorilla gorilla has less time available for resting and socializing in brain function is asymmetry of cerebral hemispheres (Groves & than G. beringei due to its frugivorous diet (Doran-Sheehy et al. 2004). Humphrey 1973). Feeding is the primary impetus for climbing (Remis 1998). Gorillas Adult !! have laryngeal air sacs in the chest cavity that produce are modified brachiators (Napier 1963), and G. g. gorilla exhibits more resonance when the chest is beaten with open palms of the hands suspensory features than G. beringei with broad scapulae, and relatively (Schaller 1963, Dixson 1981). short phalanges and metacarpals (Doran 1997b). Gorilla g. gorilla is an Gorilla g. gorilla builds a nest to sleep in every night; animals pull, agile climber, more arboreal and more gracile than G. b. beringei, with bend and break the stems of vegetation and arrange them around and longer, more slender limbs. Immatures and adults both brachiate and under their bodies. Materials used for construction depend on local walk quadrupedally along branches (Williamson 1988). Solitary adult plant availability. The majority of ground nests are constructed from !! climb more than adult !! in groups (Remis 1998). Adult "" Aframomum spp. and species of Marantaceae. In the Likouala Swamps climb more than adult !! (Doran & McNeilage 1998). Will wade of Congo, most nests are made of the fronds of Raphia sp. (Blake across streams and in swamps bipedally using outstretched arms for et al. 1995). Tree nests are built by folding branches to form a bed balance (Parnell 2002b). of leaves at the centre, and built by all age–sex classes. Adult !! Gorilla g. gorilla is similar to the Robust Chimpanzee Pan troglodytes likely build fewer tree nests than smaller individuals (Remis 1998). in craniodental (Shea 1983) and gut morphology (Chivers & Hladik Nesting on or above ground is determined by availability of raw 1980). Adaptations to frugivory include relatively narrow mandibular materials, likelihood of rain, or disturbance by elephants Loxodonta corpus and symphysis, and smaller area for masseter attachment than spp. (Tutin et al. 1995). Proportion of tree nests varies among sites G. b. beringei (Uchida 1998, Taylor 2002). Shearing crests on molars (Lac Télé, Congo terra firma forest, 3%, n = 719 [Poulsen & Clark are reduced and incisors broad compared to more folivorous G. b. 2004]; Bai Hokou, Central African Republic, 17%, n = 1123 [Remis beringei (Doran & McNeilage 1998). 1993]; Odzala, Congo, 18%, n = 630 [Bermejo 1999]; Lopé, Gabon, The simple stomach does not have the capacity for fermentation, 35%, n = 2435 (Tutin et al. 1995)]. Tree nests are more prevalent in but G. gorilla is anatomically equipped to digest fibre and consume habitats where herbs are scarce (Ngotto, Central African Republic, foods containing digestion inhibitors through a combination of 61%, n = 145 [Brugière & Sakom 2001]; Lac Télé, swamp forests, large body size and surface area of the gut, and retention of digesta 66%, n = 719 [Poulsen & Clark 2004]; Petit Loango, Gabon, 73% in the gut to maximize absorption of nutrients (Chivers & Hladik on ground, n = 110 [Furuichi et al. 1997]). Day nests are resting 1980, Rogers et al. 1990, Remis 2000). The caecum is small with places moulded between bouts of feeding. These are simpler and less a vermiform appendix; the colon is large and morphologically flattened than night nests, since they are used for shorter periods. complex (Chivers & Hladik 1980, Caton 1999), and contains many cellulose-digesting entodiniomorph ciliates (Landsoud-Soukate et Foraging and Food Herbivorous, folivore–frugivore. Tutin al. 1995). Gorilla gorilla tolerates high levels of fibre, total phenols (2003: 299) described G. gorilla as ‘folivores who like fruit’. All and condensed tannins in its food (Calvert 1985, Rogers et al. age classes feed in trees, up to 30 m above ground. Animals adopt 1990). In captivity mean gut retention time is 50 h (range 16–136; both sitting and standing positions for feeding. They bend terminal Remis 2000). Gorilla gorilla does not have the gut specializations branches within reach, often without breaking them. Fruits and required to digest seeds (Chivers & Hladik 1980, Andrews & Aiello leaves are plucked with the lips, or pulled off by hand and transferred 1984). to the mouth. When fruit abundance is low adult !! remain on Gorilla gorilla relies on physical strength to break open termite the ground rather than expending energy to climb (Remis 1999). mounds and other food sources, and does not use tools to access Adult !! also bend and break saplings to access foliage, fruit or foods. Tremendous strength allows these animals to snap off fruit- vines (Williamson et al. 1990). When feeding on the ground, group laden terminal branches to carry to safer feeding spots. It also members spread out at distances of up to 500 m. Animals will wade enables access to resources that are not available to other frugivores, in swamps to forage on aquatic herbs, and sit in water chest-deep for for example, they bite into the hard protective shell of Detarium up to 2 h. They wash sediment from aquatic plants before ingestion macrocarpum to eat the seeds (Williamson et al. 1990). by waving handfuls of plants back and forth in the water (Parnell 41

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2002b). In Gabon, they occasionally cross open savanna to eat fruits of shrubs (Williamson et al. 1990). Gorilla gorilla eats fruit, seeds, leaves, stems, bark, shoots, roots, petioles, bracts, vine tendrils, invertebrates and earth, with striking similarities across sites. The diverse diet of G. g. gorilla with an important fruit component is closer to the diet of P. troglodytes than to G. b. beringei (Tutin et al.1991a). Average dietary diversity is 148 food species (range 100–180; Rogers et al. 2004). The feeding strategy of G. g. gorilla requires it to consume leaves to meet protein needs, even when fruit is abundant (Tutin & Fernandez 1994). Staple foods are pith of Aframomum spp. and leaves and shoots of Marantaceae (primarily Haumania spp.), which are abundant, accessible, and available year-round. Gorilla gorilla is highly selective; for example, animals eat the easily digestible stem- and leaf-bases of Megaphrynium macrostachyum and Haumania liebrechtsiana but discard the remainder of the plant. They consume leaves high in protein, ripe succulent fruit high in soluble sugars and low in tannins (Rogers et al. 1990, Remis et al. 2001), and freshwater herbs high in protein and minerals such as sodium and potassium (Magliocca & Gautier-Hion 2002, Doran-Sheehy et al. 2004). Unripe fruit and leaves high in digestion inhibitors are avoided. Fruit is widely available in lowland habitats, thus G. g. gorilla is more frugivorous than G. beringei (Williamson et al. 1990, Doran & McNeilage 2001). Gorilla gorilla eats fruits from up to 100 species (Tutin et al. 1997a). Fruit is the most diverse food category at all sites studied (range 44–70% of food species; Rogers et al. 2004). When abundant, fruit forms the bulk of the diet, although quantitative data are not available and consumption is measured by faecal analysis (fruit remains recorded in 90–100% of faecal samples, Rogers et al. 2004). However, the first study of G. g. gorilla by direct observation indicates that degree of frugivory may be lower than previous estimates (Doran-Sheehy et al. 2006). Seeds of ripe fruits are ingested with pulp, but rarely digested, thus G. g. gorilla is an important seed disperser (Tutin et al. 1991b). An exception is in Likouala, where G. g. gorilla feeds heavily on Gilbertiodendron dewevrei seeds during mast fruiting (Blake & Fay 1997), but processing of seeds is time-consuming and individuals have difficulty picking up small seeds on the ground (Tutin et al. 1997a). In Gabon, immature seeds of Dialium lopense are reingested through coprophagy (Rogers et al. 1998). In Gabon, G. gorilla feeds sporadically in streams and marshes on semi-aquatic Marantaceae, Marantochloa cordifolia, M. purpurea and Halopegia azurea (Williamson et al. 1988). In Congo, animals make extensive use of waterlogged or permanently flooded swamp forest where preferred foods are aquatic Hydrocharis chevalieri and sodium-rich sedges Rhynchospora corymbosa and Cyperus sp. (Magliocca & Gautier-Hion 2002, Parnell 2002b). In Likouala and Lac Télé swamps, staple foods are Raphia sp. palm fronds and Pandanus candelabrum, respectively (Blake et al. 1995, Poulsen & Clark 2004). Fallback foods are always available but tend to be lower quality (pith, leaves, barks and fibrous fruits) and are ignored when ripe succulent fruits are available (Rogers et al. 1994, 2004). For example, Duboscia macrocarpa and Klainedoxa gabonensis are tough, dry fruits eaten in large quantities only when other fruits are lacking (Williamson et al. 1990). Gorilla g. gorilla consumes >20 species of invertebrate, mostly social ants and Cubitermes termites. Weaver ants Oecophylla longinoda

are ingested in convenient nests, containing eggs, larvae, pupae and adults. Remains of ants have been recorded in 31% of faeces (Williamson et al. 1990). The gorillas are more insectivorous in areas dominated by secondary forest, where Crematogaster (ants) and Thoracotermes (termites) are also eaten (Deblauwe et al. 2003). Insectivory seems to occur at about the same rate at four sites: Lopé, Belinga, Ndoki and Dzanga-Sangha (Tutin & Fernandez 1992, Deblauwe et al. 2003). Termites are the most commonly observed food item and eaten on 91% of days (Cipolletta et al. 2007). Geophagy has been observed at natural salt-licks with a high concentration of sodium (e.g. Williamson et al. 1990). The diet of G. g. gorilla varies seasonally. The amount of fruit eaten is positively correlated with rainfall and the availability of ripe fruit trees (Goldsmith 1996, Remis 1997b). When fruit is abundant, it constitutes most of the diet (68%), but only 30% in the dry season (Tutin et al. 1991a). In the dry season more fibrous vegetative matter is eaten, including shoots, young leaves and bark. Milicia excelsa bark is eaten only during the dry season (Williamson et al. 1990, Tutin et al. 1997a). Little is known about the diet of G. g. diehli. Diet includes fruit, leaves, stems, piths, invertebrates and soil, but fruit is preferred when available (Oates et al. 2003). The habitat of G. g. diehli is notable for strong seasonality, with a prolonged (4–5 month) dry season during which fruit becomes scarce and diet shifts to bark, leaves and pith of terrestrial herbs (Oates et al. 2003). Landolphia leaves are the staple food at Afi, Nigeria (Rogers et al. 2004). Ranging patterns are shaped by the availability of particular foods, and G. g. gorilla travels widely between patchily distributed fruit trees (Tutin 1996, Remis 1997b, Goldsmith 1999). Mean distance travelled each day by G. g. gorilla was 1.1–2.6 km (Lopé 1105 m, range 220–2790, n = 80 [Tutin 1996]; Bai Hokou 2588 m, range 342–5237, n = 85 [Goldsmith 1999]; Bai Hokou 1527 m, median = 1450, range 250–3300, n = 431 [Cipolletta 2004]; Mondika 1904 m, range 1485–2651, n = 94 [Doran & McNeilage 2001]; Mondika 2014 m, range 400–4860, n = 334 [Doran-Sheehy et al. 2004]). Mean daily travel distance for one group of G. g. diehli was 1270 m, 600–3700, n = 75 (McFarland 2007). Gorilla gorilla adopts a low-cost energy strategy during periods of fruit scarcity by decreasing day range and shifting diet towards abundant but lower quality leaves and woody vegetation. For example, at Bai Hokou, shorter distances are travelled by G. g. gorilla during dry season months: dry 1326 m (S.D. = 432, n = 149) vs. wet 1595 m (S.D. = 642, n = 177) (Cipolletta 2004). Gorilla g. gorilla home-ranges are large (Lopé 7–14 km² annual, n = 3 groups, total 21.7 km² for ten years, n = 1 group [Tutin 1996]; Bai Hokou 10.6 km² annual, range 7.5–13.3, n = 3 groups [Cipolletta 2004]; Mondika 15.4 km², one group, one year [DoranSheehy et al. 2004]). Annual home-range of one group of G. g. diehli at least 13.1 km², but probably closer to 20 km². Total home-range roughly 30 km² (McFarland 2007). Social and Reproductive Behaviour Gorilla gorilla is social, living in stable, cohesive groups with one adult !, several "" and their offspring. One-male breeding groups are the norm in G. g. gorilla (Levréro et al. 2006). The ! : " ratio in groups is 1 : 3 (Parnell 2002a, Douadi et al. 2007) with, on average, four immatures per group (Gatti et al. 2004). Basic group structure is

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similar across sites and between gorilla species, one main difference being that multimale groups are rare in G. g. gorilla, although known at Lopé and Lossi (Tutin et al. 1992, Bermejo 1999). Average G. g. gorilla group size is similar to G. b. beringei (Maya: 11.2, range 2–22, n = 31 [Magliocca et al. 1999]; Mbeli: 8.4, range 2–16, n = 14 [Parnell 2002a]; Lokoué: 8.2, range 3–15, n = 37 [Gatti et al. 2004]). Groups with >20 individuals known only at two sites in Congo (maximum = 32 [Bermejo 1999, Magliocca et al. 1999]). Gorilla g. diehli group size is smaller (4 years of age. Crown becomes brown at ca. 1.5–2.5 months and then black again by 8–9 months (Schaller 1963). Geographic Variation G. b. beringei Mountain Gorilla. Virunga Mts. Hair longer, tending towards jet black or bluish-black, rarely with brownish or reddish tones. Pelage on crown longer, shaggier. Face wider. Nostrils more ovate and angular, strongly outlined above and well defined. Upper lip (alae) weakly padded. Cranial height longer. Facial height and palate breadth of ! shorter. Hallux longer. Humerus

Mountain Gorilla Gorilla beringei beringei adult male skull.

shorter. Clavicle longer. Scapula with vertebral border pulled outward at root of scapular spine, sinuous (Groves 1966, 2001, Jenkins 1990). Although it is often stated that G. b. beringei is larger than G. b. graueri, the available data on body size do not support this. G. b. graueri Grauer’s Gorilla. West of the Western Rift Valley. Hair, shorter, black, often with brownish or reddish tones. Pelage on crown shorter, less shaggy. Face narrower. Nostrils rounded, not strongly outlined above. Upper lip (alae) strongly padded. Cranial height shorter. Facial height and palate breadth of ! longer. Hallux shorter. Humerus longer. Clavicle shorter. Scapula with vertebral border relatively straight, not sinuous (Groves 1966, 2001, Jenkins 1990). G. b. ssp.? Bwindi Gorilla: known only from Bwindi Impenetrable N. P. with a few individuals entering Sarambwe Forest across the border in DR Congo (see below). See Sarmiento et al. (1996) for details of morphology. Similar Species Pan troglodytes. Sympatric below ca. 2300 m. Smaller (adult !! 37 m) tree species are P. latifolius, Prunus africana, Parinari excelsa, Newtonia buchananii, Entandrophragma excelsum, Chrysophyllum gorungosanum and Symphonia globulifera. The more common middle stratum (9–21 m) tree species include C. macrostachyus, N. macrocalyx, Albizia gummifera, Carapa procera, Faurea saligna, Harungana madagascariensis, Macaranga capensis kilimandscharica, Olea capensis ssp. macrocarpa, Polyscias fulva, Strombosia scheffleri and Syzygium guineense. The following are among the more common understorey (75% of diet is comprised of three species: G. 1996). The caecum is small with a vermiform appendix and the ruwenzoriense, P. linderi and C. nyassanus (Watts 1984). Bamboo shoots, colon is complex with specialized fermentation chambers. Together, a highland food (above ca. 2300 m), are a seasonal, highly preferred, the caecum and colon provide a large surface area for absorption of food that is eaten when available, sometimes comprising as much as nutrients (Chivers & Hladik 1980). Large body size and long gut 90% of the diet (Casimir & Butenandt 1973,Vedder 1984). Highland retention times also facilitate digestion of fibre (Remis 2000). Gorilla populations of G. b. graueri also eat large quantities of the basal parts beringei tolerates high levels of fibre, total phenols and condensed of the sedge Cyperus latifolius (Casimir 1975). tannins in food (Waterman et al. 1983). Diversity of the plant diet increases with decreasing altitude Gorilla beringei does not use tools, relying on physical strength as the plant diversity of the habitat increases. Lowest number of to tear apart food items. These gorillas do, however, learn complex species consumed was recorded for G. b. beringei in Rwanda (62 techniques for gathering food with bimanual coordination of the species; Watts 1996), and highest for Bwindi Gorillas at Buhoma hands. Many foods with stings (e.g. nettles) or spines are processed (140 species; Ganas et al. 2004). Gorilla b. graueri is intermediate, in a sequence of precision movements (Byrne & Byrne 1993). with many more species eaten in the lowlands than in the highlands Adult !! have laryngeal air sacs in the chest cavity that produce of Kahuzi-Biega N. P. (121 species vs. 79 species; Yamagiwa et al. resonance when the chest is beaten with open palms of the hands 2003). Fruit availability is also inversely correlated with altitude and (Schaller 1963, Dixson 1981). reflected in gorillas’ degree of frugivory (Goldsmith 2003, Ganas Like all great apes, G. beringei builds a nest in which to sleep at et al. 2004). Fruit consumption by G. b. beringei is negligible due to night by bending or breaking vegetation (twigs and branches of lack of suitable fruit in the environment (Vedder 1984, Watts 1984,

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McNeilage 2001). Gorilla b. graueri feeds on more species of fruit than sympatric P. troglodytes (Yamagiwa et al. 2003). Fruit remains are present in 89–96% of faecal samples. Fruit accounts for 25% of food species in highlands, 40% in lowlands (Yamagiwa 2004). Diet of Bwindi Gorillas is more similar to G. b. graueri than to G. b. beringei, due to greater overlap in food availability (Robbins et al. 2006). Fruit remains are found in 66–82% of faecal samples, forming ca. 26% of species in the diet (Ganas et al. 2004). By volume, fruit accounts for ca. 25% of diet; the most important species is M. holstii (seeds found in 20% of faecal samples; Stanford & Nkurunungi 2003). Fruit is eaten on 60–80% of days (Robbins & McNeilage 2003, Ganas et al. 2004). Gorilla b. beringei diet changes little during the year (Watts 1998c). Only bamboo shoots are limited by season (Casimir & Butenandt 1973, Vedder 1984). Seasonality of diet increases as altitude declines (Yamagiwa et al. 1994, Nkurunungi et al. 2004, Robbins & McNeilage 2003). Fruit intake correlates with availability (Stanford & Nkurunungi 2003), and varies interannually (Robbins et al. 2006). Gorilla b. graueri and Bwindi Gorillas rely on fibrous items as fallback foods, which are always available, but eaten only when is fruit scarce (Ganas et al. 2004). All subspecies of G. beringei consume insects. Gorilla b. beringei does so rarely as ant availability decreases with increasing altitude (Watts 1989a). Gorilla b. graueri in the lowlands consumes ants and termites frequently (ants in 37% of faecal samples, n = 171; Yamagiwa et al. 1991). There are few sex or age differences in the diets of G. beringei, but in Bwindi Gorillas smaller individuals are more insectivorous (2% of faecal samples from adult !! contain ants, compared to 13% adult "", 11% juveniles, Ganas & Robbins 2004). Individuals in some groups ingest earth a few times a year (Mahaney et al. 1990). Geophagy coincides with feeding on plants containing high levels of toxins (Mahaney et al. 1995). Gorilla b. beringei also eats dung (Harcourt & Stewart 1978). The functions of coprophagy are unclear, but adult "" and juveniles sometimes compete for the dung of adult !! (E. A. Williamson pers. obs.). Gorilla beringei subspecies move ca. 1 km each day, but differences are known. Daily travel distances are greater in lowland than in highland areas. Gorilla b. beringei is surrounded by food, so travels ca. 570 m/day (range 190–3000 m, n = 116; Watts 1991b). Mean day range for G. b. graueri in the highlands is ca. 851 m (range 239– 3570 m, n = 225) but these gorillas travel farther in the lowlands in search of fruit (mean = 1531 m, range 142–3439 m, n = 8; Yamagiwa et al. 2003). Bwindi Gorilla groups travel ca. 716 m/day (range 242–2055 m, n = 109; Stanford & Nkurunungi 2003). Gorilla beringei home-range size varies widely. Gorilla b. beringei range is smallest as herbaceous food densities are exceptionally high (annual home-range 3.1–33.8 km2, n = 11 groups; McNeilage 1995, Watts 1998b, IGCP/M. Gray pers.comm.). Gorilla b. graueri in the lowlands requires a larger area than in the highland sector but size of home-range is unknown (Yamagiwa et al. 2003). Estimates for the highlands vary widely: 23–31 km2 (n = 1 group; Casimir & Goodall cited in Yamagiwa 1999) to 13–17 km2 (n = 1 group; mean = 14.1 km2; Yamagiwa et al. 2003). Total area used over eight years was 42.2 km2. Bwindi Gorilla home-ranges are comparable to G. b. graueri and G. g. gorilla: annual home-range 16–28 km2 (mean = 22 km2, 45.5 km2 for 6 years, n = 1 group; Robbins et al. 2006). Gorilla b. beringei group home-ranges overlap 24–72% (n = 6 groups;

Watts 1998b). Overlap is similarly ‘extensive’ for G. b. graueri and Bwindi Gorilla (Yamagiwa et al. 2003, Ganas & Robbins 2005). Availability of particular foods influences ranging even where food is abundant (Casimir & Butenandt 1973, Vedder 1984, Watts 1998b). Gorilla b. beringei shows no seasonal patterns of range use except for increased time spent in the bamboo zone when shoots are present (Vedder 1984, Watts 1998c). Gorilla b. graueri increases travel to access preferred fruits, and increases range during the dry season (Yamagiwa et al. 1996). The limited distribution of bamboo causes seasonal shifts in ranging (Casimir & Butenandt 1973). Ranging patterns are also influenced by social factors such as inter-group encounters, mate-searching and acquisition of group members. Mate competition has a strong short-term effect (Watts 1998c), at times concealing the influence of ecological factors. Home-ranges of solitary !! are larger than would be necessary to meet nutritional requirements as they follow groups in attempts to acquire "" (Yamagiwa 1986, Watts 1994). Groups also range farther after interactions with other social units, and aggressive encounters can cause abrupt shifts in range (Watts 1998c). Social and Reproductive Behaviour Gorilla beringei is social and lives in stable, cohesive, polygynous groups composed of several "", their offspring and at least one adult ! (i.e. ‘silverback’). Groups are one-male, multimale or non-reproductive (containing no adult ""). Multimale groups in the Virunga Mts, exceptionally, have up to eight adult !!. Some adult !!, but no "", become solitary. Gorilla beringei group sizes range from 2 to >50 individuals with a mean of roughly 10 (G. b. beringei: mean 12.5, median 10.5, 2–47, n = 36 [Gray et al. 2011]; G. b. graueri highlands: mean 9.7, 2–36, n = 25 [Inogwabini et al. 2000]; G. b. graueri lowlands: mean 6.8, 2–31, n = 41 [calculated from Hall et al. 1998b]. See also Amsini et al. (2008) and Hart et al. (2007). Bwindi Gorilla: mean 11.3, 3–25, n = 27 [McNeilage et al. 2006]). In the Virungas, habituated groups are larger than unhabituated groups (14.5 vs. 8.4, Gray et al. 2011). One G. b. graueri group with >40 individuals (Yamagiwa 1983), one G. b. beringei group with >50 individuals (Gray et al. 2010) and one Bwindi Gorilla group with >32 individuals (T. Butynski pers. obs.). Polygynous G. b. graueri groups sometimes fission temporarily into subgroups and nest apart, each subgroup with at least one adult ! (Yamagiwa 2001). Subgrouping is most frequent during fruiting seasons (Yamagiwa et al. 2003). Typical G. b. beringei group composition is one adult !, five adult "", and their offspring (Harcourt & Stewart 2007b). Multimale groups form when maturing !! remain in their natal group. Both G. b. beringei and Bwindi Gorillas have a significant proportion of multimale groups (G.b.beringei 36% [Gray et al. 2010]; Bwindi Gorillas 44% in 2002 [McNeilage et al. 2006] compared to G. b. graueri ca. 10% [Yamagiwa et al. 2003, 2009, 2012]). One adult ! dominates the ! hierarchy. Adult "" are ‘dispersal-egalitarian’, forming neither hierarchies nor coalitions (Sterck et al. 1997). Affiliative behaviour between adult !! is rare. Competition among adult !! is intense and aggression between !! is likely when "" are in oestrus (Harcourt et al. 1980). Most intra-group aggression is between adult "", and is usually limited to aggressive vocalizations. Rarely does aggression between adult "" escalate beyond screaming as adult !! intervene to end disputes. Interactions between adult !! and 49

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Bwindi Gorillas Gorilla beringei ssp. resting.

adult "" are limited to interventions, exchanges of vocalizations, aggressive displays by !! towards "", and appeasement behaviour by subordinates. Most affiliative behaviour is between related "", who maintain close proximity and groom each other. Grooming is a common intra-group behaviour in Mountain Gorillas. Most grooming is between mothers and offspring, but is also extended, in reducing frequency, to maternal relatives, paternal relatives and unrelated individuals. Juveniles groom each other and also groom the dominant !; adult "" are known to groom dominant !!, and adolescent !! sometimes groom adult "" (Schaller 1963, Harcourt 1979a, b, Fossey 1983,Watts & Pusey 1993, Fletcher 1994). Grooming almost certainly serves a social purpose in terms of reinforcing such bonds as exist between individuals, but is ultimately related to the removal of ectoparasites, dry skin flakes and vegetation. Gorilla beringei !! and "" are both philopatric, but most emigrate from their natal group (Robbins 1995, Watts 2000a). Some "" are known to reproduce within their natal group (31%, n = 29) and many reproduce in more than one group (56%, n = 27; Watts 1996). Half of G. b. beringei and most G. b. graueri !! emigrate from their natal group by age 15 years (range 9.6–14.4, n = 6; Robbins 1995, Yamagiwa & Kahekwa 2001). Maturing !! who emigrate either spend time in an all-male group, or remain solitary and attempt to attract "". Solitaries, however, are rarely successful at establishing groups (Robbins 1995, Watts 2000a, E. A. Williamson pers. obs.). Adult !! in multimale groups are often related, and subordinate !! in these groups sire a small proportion of offspring (Bradley et al. 2005,Yamagiwa et al. 2012). Adult social bonds are strongest between "" and !!. Most "" are unrelated and do not associate regularly with each other (Watts 1996). Adult "" associate with adult !! as a means to avoid infanticide by extra-group !! (Watts 1989b, Yamagiwa et al. 2009, 2012). Most infanticides occur when a mother is not

accompanied by an adult ! (Watts 1989b). Infanticide shortens the time for mothers to become fertile again and accounts for 26% of infant deaths (n = 19; Robbins & Robbins 2004). Multimale groups are more stable; if the dominant ! in a multimale group dies, a subordinate takes over and the group remains intact (Robbins 1995). Habituated groups of G. b. beringei are almost all multimale (Kalpers et al. 2003). Copulation is initiated by both sexes. Females initiate 63% by approaching, staring and reaching towards the !. Males initiate through approach, display and ‘train-grunt’ vocalization (Watts 1991a). Copulations are brief (median = 80 sec, range 30–310 sec, n = 251; Watts 1991a). Dominant !! perform most copulations. Subordinate !! also mate but are often harassed by a dominant adult !. Newborns cling to the mother’s hair, suckle and are carried ventrally. Infants are highly dependent on their mothers at birth and unlikely to survive if orphaned before three years of age. During the first few months, infants have a white tail tuft and travel in a ventro-ventral position. Travel on the mother’s back (dorsal ride) starts at 1–2 months and climbing at 6–12 months (Fossey 1979). From ca. six months infants spend increasing amounts of time away from the mother (Fletcher 2001). Play begins when the infant is ca. nine months old, peaks during juvenility and decreases during adolescence (Fletcher 1994). Infants manipulate vegetation at eight months, build clumsy nests by 18 months, but sleep in the mother’s nest until age three years (Fossey 1979). They become independent at 3.5–4 years, eating solid food and building their own nests. By four years their locomotion is roughly adult (Tuttle & Watts 1985). The dominant ! has a protective role, defending "" and offspring from other adult !! and predators with intimidating displays (Schaller 1963). Immatures are attracted to the dominant ! as the group’s focal point during both feeding and resting periods (Stewart 2001). As time spent near the mother decreases in late infancy, time spent in proximity to the dominant ! increases. Adult ! frequently intervenes during aggressive conflicts between immatures, which serves to protect immatures from high levels of aggression (Watts 1997, Stewart 2001). More than 16 G. b. beringei vocalizations have been identified. The vocal repertoire and sound production within groups is dominated by adult !! (92% of all vocalizations; Marler & Tenaza 1977).When encountering another group, adult !! convey alarm or threat by barks, roars and screams, usually accompanied by displays (Schaller 1963, Fossey 1972). Over half of within-group vocalizations are exchanges with neighbours (Harcourt & Stewart 2001). When G. b. beringei feeds, individuals disperse and often cannot see each other in the dense vegetation. At such times they emit belch vocalizations to maintain contact within the group, and ‘close calls’ are thought to be important for spacing. Close calls seem to coordinate group movement by signalling intent (Harcourt & Stewart 1996). Other vocalizations include threat barks during aggressive displays, question barks, a mildly aggressive cough-grunt, infant whimpers, breathy chuckles during play, staccato whimpers during copulation, ‘humming’, ‘singing’ and hoots (Schaller 1963, Fossey 1972, Harcourt & Stewart 1996, Sicotte 2001). Chest-beats are provoked by excitement and used in many contexts from play to intimidation within groups, to communication between groups (Schaller 1963, Dixson 1981). All age classes charge, but only adult !! produce the full displays incorporating charges,

50

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chest-beats, strutting, screams or barks, hoot-series (vocalizations), ground-thumping and vegetation throwing. The ‘stiff-legged strut’ is described as ‘showing off’ (Schaller 1963). Adult !! emit a musky odour from axillary glands in the armpit in situations of excitement or fear (Schaller 1963), and all age classes produce diarrhoeic dung when stressed or afraid. Inter-group encounters, where adult !! exchange chest-beats and vocalizations, are aggressive contests for adult "", not for food (Sicotte 1993). Groups usually try to avoid each other, but when inter-group encounters occur over two-thirds of them induce aggressive interactions between adult !! (Harcourt 1981, Sicotte 1993). When these escalate to physical contact, the fights are intense (Harcourt 1981, Watts 1989b) and sometimes fatal (E. A. Williamson pers. obs.). Adult !! in multimale groups cooperate by herding to prevent "" from emigrating (Sicotte 1993). Gorilla beringei is sympatric with P. troglodytes over all but the highest altitudes of their geographic range.The diets of G. beringei and P. troglodytes overlap but they show different foraging strategies when fruit is scarce, and there is little evidence of inter-specific feeding competition (Yamagiwa et al. 1996, Stanford & Nkurunungi 2003). Gorilla b. beringei shows curiosity and is gentle on the rare occasions that they interact with other animals (E. A. Williamson pers. obs.), unless they encounter potential dangers (e.g. poachers, Cape Buffalo Syncerus caffer), at which times adult !! actively defend other group members. Reproduction and Population Structure The median length of the menstrual cycle in G. b. beringei "" is 28 days (mean = 28.8, range 20–39, n = 25; Watts 1991a). Females are proceptive for 1–4 days (Watts 1991a). Ovulation is at the mid-cycle, and mating occurs near peak oestrogen concentrations (Czekala & Sicotte 2000). Gorilla b. graueri " menstrual cycles are slightly longer at 33.2 days (Yamagiwa & Kahekwa 2001). Nulliparous "" have small sexual swellings but parous "" show no external signs of oestrus (Czekala & Sicotte 2000). Gestation lasts ca. 255 days (Watts 1991a, Czekala & Sicotte 2000, Yamagiwa & Kahekwa 2001). There is no evidence of seasonality in births for G. b. beringei (n = 206; Gerald 1995, Watts 1998c), but there appears to be a May–Jul birth peak for G. b. graueri (n = 47; Yamagiwa et al. 2012). Gorilla beringei typically give birth to a single infant.Twins are rare, but have been born into the Virunga and Kahuzi-Biega populations; however, there is only one known case of both twins surviving (Meder 2004). Birth weight ca. 2 kg. Sex ratio at birth is 1 : 1 (n = 214; Robbins et al. 2007). Birth rate is 0.22–0.28 births per adult " per year, or about one birth per adult " every 4.4 years (n = 101; Gerald 1995, Steklis & Gerald-Steklis 2001). Females surviving to adulthood (60%) have an average reproductive lifespan of 14 years and produce a mean of 4.6 offspring that survive to beyond infancy (Gerald 1995). Females are not fertile whilst suckling young and lactational anoestrus lasts ca. three years. Gorilla b. beringei mean inter-birth interval is close to four years when the previous sibling survives (median 3.9 years, S.D. = 0.7 years, n = 62). If an infant dies before weaning, another is born two years later (S.D. = 1.1 years, n = 39; Gerald 1995). Gorilla b. graueri has a slightly longer interval of 4.6 years (range 3.4–6.6, n = 9) between surviving offspring, or 2.2 years when an infant dies (range 1.4–2.7, n = 3; Yamagiwa

& Kahekwa 2001). Infants are weaned at 3–4 years (median = 43 months, range 22–62 months, n = 5; Stewart 1988, Fletcher 2001). Gorilla b. beringei grows faster than G. g. gorilla (Taylor 1997). Age at fertility in !! is unknown, but !! do not copulate until age 9–10 years (Watts 1991a). Gorilla b. beringei !! show a growth spurt and develop secondary sexual characteristics from ten years of age, but are not fully grown until 15 years (Watts 1991b, Watts & Pusey 1993). Gorilla b. beringei "" reach sexual maturity and first copulate at 7.0–7.5 years (Groves & Meder 2001), but experience ca. two years of adolescent sterility before first conception (Watts 1991a). Gorilla b. graueri has a similar sterile subadult period (Yamagiwa & Kahekwa 2001, Yamagiwa et al. 2003). Mean age at first parturition is 10.2 years in G. b. beringei (range 8–13, n = 42; Gerald 1995),and 10.6 years in G. b. graueri (range 9.1–12.1, n = 6; Yamagiwa & Kahekwa 2001). In G. b. beringei the ! : " ratio is 1 : 1.7 and of immatures : adults is 1 : 1.2 in a population of 255 individuals (based on Kalpers et al. 2003). Mortality rates are highest for infants and older adults (Gerald 1995). Gorilla b. beringei infant mortality is greatest in the first six months (18%, n = 151; Gerald 1995) and 34% in first three years (n = 65, Watts 1991a). Rates are similar in G. b. graueri (20% in first year, 26% in first three years, n = 46;Yamagiwa & Kahekwa 2001). Mortality is highest in the wet season due to increase of respiratory infections (200% higher than predicted; Watts 1998c). About 60% of G. b. beringei survive to age eight years (Gerald 1995). Survivorship is constant from the young adult age-class (8–12 years) through the mature adult age class (12–20 years) and drops thereafter. Adult !! die relatively young, perhaps because of competition among them (Groves & Meder 2001). About 32% of !! die at 24–30 years, compared to only 8% for "" (Gerald 1995). The oldest known G. b. beringei individual died at 45 years of age (Robbins & Robbins 2004). Predators, Parasites and Diseases Due to its large size, G. beringei probably has only two predators of any significance. Humans are, by far, the primary predator of G. beringei, killing them for their meat, body parts and in retaliation for damage to crops (Plumptre et al. 2003a). Several cases of G. beringei predation by Leopards Panthera pardus are described by Schaller (1963). Gorilla beringei is susceptible to numerous diseases and parasites, including: common cold, pneumonia, whooping cough, influenza, hepatitis A and B, Epstein–Barr virus, chicken pox, smallpox, bacterial meningitis, tuberculosis, diphtheria, measles, rubella, mumps, yellow fever, yaws, paralytic poliomyelitis, encephalomyocarditis, schistosomiasis,giardiasis,filariasis,strongyloidiasis,cryptosporidiosis, shigellosis, salmonellosis, Capillaria hepatica, Entamoeba coli, E. histolytica, Endolimax nana, Ancylostoma sp., Oesophagostomum sp., Acanthocephala sp., Cyclospora sp., Chilomastix sp., Iodamoeba buetschlii and Sarcoptes scabiei (Ashford et al. 1990, 1996, Durrette-Desset et al. 1992, Butynski & Kalina 1998, Homsy 1999, Butynski 2001, Woodford et al. 2002, Ryan & Walsh 2011). See also Conservation. Conservation IUCN Category (2012): G. beringei Endangered; G. b. beringei Critically Endangered; G. b. graueri Endangered. CITES (2012): Appendix I as G. gorilla. Listed as an ‘Endangered Species’ under the US Endangered Species Act of 1973. 51

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Threats to G. beringei all relate to the high human population density within the geographic range and human requirements for natural resources, especially land for agriculture, timber and bushmeat. Populations of G. beringei are being increasingly fragmented, isolated and destroyed directly through unsustainable hunting (i.e. poaching), and indirectly through habitat degradation, loss and fragmentation (Lee et al. 1988, Kemf & Wilson 1997, Bowen-Jones 1998, Hall et al. 1998a, Butynski 2001, Plumptre et al. 2003a, Rose et al. 2003, Ferriss et al. 2005, Yamagiwa et al. 2012). Such fragmented populations are susceptible to extinction not only from further habitat loss and over-exploitation, but also from random (stochastic) genetic and demographic changes, and from environmental catastrophes such as disease. While much has been written about the impact of habitat loss and hunting on populations of G. beringei, less has been said about the known and potential impacts of disease on this species. Disease, including parasites, is another major concern as transmission from humans to G. beringei occurs and has the potential to be catastrophic. Because G. beringei is phylogenetically close to humans, this species is highly susceptible to numerous human diseases (see Predators, Parasites and Diseases, and Homsy 1999, Butynski 2001,Woodford et al. 2002, Ferriss et al. 2005, Palacios et al. 2011). Many of the diseases to which G. beringei is susceptible are fatal or cause morbidity, with severe consequences for normal behaviour and reproduction. Of particular concern at this time is the fact that, each year, thousands of tourists from hundreds of localities around the world, step out of crowded, poorly ventilated airplanes and airports and within 1–2 days are close to, and sometimes touching, habituated G. beringei (Butynski & Kalina 1998, Sandbrook & Semple 2006, Macfie & Williamson 2010, Ryan & Walsh 2011). These visitors can carry exotic strains of pathogens while not yet showing clinical signs of disease. The risk is that humans will transfer a disease to an immunologically naïve population of G. beringei, triggering an epidemic. Both of the G. beringei populations that are now the focus of intensive tourist viewing are already small and highly threatened: the Virunga Mts populations with ca. 480 individuals, and the Bwindi Impenetrable N. P. population with ca. 300 individuals. Each day, ca. 75% of the individuals in the Virunga population are visited by people (tourists, researchers, guides, porters, rangers and military escorts). The risks and consequences of disease transmission between humans and G. beringei are predicted to become increasingly serious if once-stable ecosystems and large (genetically diverse) populations of G. beringei are fragmented, reduced and stressed by humans. Small populations are likely to have diminished genetic variation, one result of which is increased vulnerability to infectious diseases. In the case of G. beringei the stress involved with the habituation process and frequent visits by people may further challenge their wellbeing, compromising their ability to respond normally to disease. The introduction of a human-borne infection into small, stressed, genetically depressed populations of G. beringei could lead not only to the extinction of the population but also (where the subspecies is represented by but one population) to the extinction of the subspecies (Butynski & Kalina 1998, Butynski 2001). Identifying and implementing actions to minimize and reduce the major threats to G. beringei have been the focus of many workshops, articles and books (e.g. Schaller 1963, Dixson 1981, Lee et al. 1988, Butynski 2001, Caldecott & Miles 2005, Ferriss et al. 2005, Pain

2009) and will not be reviewed here. The major protected areas whose effective management is critical to the long-term survival of G. beringei are Kahuzi-Biega N. P., Maiko N. P., Itombwe Nature Reserve and Virunga N. P. in DR Congo, Bwindi Impenetrable N. P. and Mgahinga Gorilla N. P. in Uganda, and Volcanoes N. P. in Rwanda. Research priorities for G. beringei at this time are: (1) new surveys to determine the present distribution and numbers of G. b. graueri; (2) more research on the impacts of tourism on the ecology and behaviour of G. b. beringei and the Bwindi Gorilla; and (3) a detailed assessment of the taxonomic status of the gorillas of Mt Tshiaberimu and Bwindi Impenetrable N. P. Measurements Gorilla beringei WT (!!): 165 (?–?) kg, n = 5 WT (""): 90 (?–?) kg, n = 3 G. b. beringei and G. b graueri from various sites combined (Sarmiento et al. 1996) G. b. beringei Standing ht (!!): 1700 (1610–1710) mm, n = 5 Girth (!!): 1490 (1380–1630) mm, n = 8 Arm span (!!): 2310 (2000–2760) mm, n = 8 Arm length (!!): 1050 (970–1110) mm, n = 5 Leg length (!!): 660 (610–710) mm, n = 2 HB (!!): 1105 (1010–1200) mm, n = 2 T (both sexes): 0 mm HF (!!): 305 (286–320) mm, n = 10 E (!!): 58 (50–65) mm, n = 6 WT (!!): 152 (120–191) kg, n = 7 WT (""): 84 (70–98) kg, n = 2 GLS (!!): 311 (287–342) mm, n = 19 GLS (""): 247 (237–260) mm, n = 11 GWS (!!): 183 (179–197) mm, n = 19 GWS (""): 148 (140–154) mm, n = 10 Virunga Mts. Compiled primarily by C. P. Groves (1966, pers. comm.) from numerous sources. Includes one adult ! collected by E. Heller in 1925. Details taken from E. Heller’s notes, which are on deposit at FMNH (J. Kerbis pers. comm.). One " WT from C. A. Whittier (pers. comm.). G. b. graueri Standing ht (!!): 1820 (1690–1960) mm, n = 6 Girth (!!): 1540 (1420–1600) mm, n = 4 Arm span (!!): 2510 (2340–2700) mm, n = 3 Arm length (!!): 990 (860–1100) mm, n = 3 Leg length (!!): 795 (790–800) mm, n = 2 HB (!!): 1090 (1040–1140) mm, n = 4 T (both sexes): 0 mm HF (!!): 297 (287–312) mm, n = 4 E (!!): 52 (50–54) mm, n = 4 WT (!!): 159 (150–209) kg, n = 4 WT (""): 76 (73–80) kg, n = 2 GLS (!!): 302 (276–334) mm, n = 43 GLS (""): 243 (219–258) mm, n = 31 GWS (!!): 182 (167–200) mm, n = 40 GWS (""): 149 (135–164) mm, n = 29

52

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Various sites in E DR Congo. Compiled by C. P. Groves (1966, pers. comm.) from numerous sources. Includes one adult ! collected by E. Heller in 1924. Details taken from E. Heller’s notes, which are on deposit at FMNH (J. Kerbis pers. comm.). See Sarmiento & Oates (2000) and Sarmiento (2003) for cheektooth surface area data for six G. beringei populations. See Sarmiento et al. (1996) for various long bone, hand bone, foot bone, vertebral, cranial, facial, and dental measurements and indices for G. b. beringei and Bwindi Gorilla.

Key References Butynski 2001; Dixson 1981; Ferriss et al. 2005; Fossey 1983; Homsy 1999; Kalpers et al. 2003; Robbins et al. 2001; Sarmiento et al. 1996; Schaller 1963; Taylor & Goldsmith 2003;Yamagiwa et al. 2009, 2012. E. A. Williamson & Thomas M. Butynski

Tribe PANINI Chimpanzees Panini Delson, 1977. Journal of Human Evolution 6: 450.

As outlined in the tribal designation of Gorillini, the need for a tribe that is effectively synonymous with the genus is dictated by a generally accepted need to separate bipedal and quadrupedal apes

(Groves 1986). The tribe Panini consists of a single genus; hence its definition and characterization is the same as that for Pan (below). Colin P. Groves

GENUS Pan Chimpanzees Pan Oken, 1816. Lehrbuch der Naturgeschichte, ser. 3 (2): 11.

a

c

b

d

(a) Western Chimpanzee Pan troglodytes verus. (b) Eastern Chimpanzee Pan troglodytes schweinfurthii. (c) Central Chimpanzee Pan troglodytes troglodytes. (d) Gracile Chimpanzee (Bonobo) Pan paniscus.

Polytypic genus endemic to the forests of tropical Africa. There are two species in this genus: the Robust or Common Chimpanzee Pan troglodytes and the Gracile Chimpanzee, also known as the Bonobo or Pygmy Chimpanzee, Pan paniscus. The latter was described as a subspecies of chimpanzee by Schwarz (1929), and elevated to the

rank of species by Coolidge (1933). The last shared ancestor was ca. 1.8 mya (Gondet et al. 2011). A suggestion that the West African P. troglodytes verus might also be ranked as a distinct species (Morin et al. 1994) has not been widely adopted. The differences between the two species of chimpanzees relate primarily to body build: P. paniscus is much more slender (i.e. ‘gracile’), with an especially small round head and heavy, pillar-like legs. As such, the intermembral index (ratio of arm length to leg length) for P. paniscus is about equal to 100, whereas the intermembral index is >100 in P. troglodytes. Infant P. troglodytes have pink faces that gradually darken with age, often developing conspicuous freckles and large tan spots, becoming black at or after maturity; infant P. paniscus already have black faces, except around the mouth, and this does not essentially change with age. Both species go bald on the scalp with age, "" earlier and usually more extensively than !!. Compared to Gorilla, Pan differs as follows. Size is much smaller (large chimpanzee !! weigh about as much as small gorilla ""), and sexual dimorphism is not so marked, chimpanzee !! being (in most populations) little larger than "". The ears are conspicuously larger, and in adults generally remain bronze rather than black. The nose is both shorter and narrower, though an approach to the ‘squashed tomato’ nostrils of many gorillas may be made. The arms are relatively shorter (intermembral index, even in P. troglodytes, is lower), the hand is much longer and narrower, the thorax is narrower, the vertebral border of the scapula is much shorter, the iliac crests lack the expansion, the calcaneum is shorter, the feet are narrower, the toes are longer, and the hallux (great toe) is more slender and more divergent. The pelage is almost invariably jet black; adult !! lack a ‘silverback’ saddle, although with extreme age both sexes become grey, first on the lower back and thighs, the greyness later 53

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spreading to other parts of the body. Like gorillas, infant chimpanzees have a whitish tuft above the anus. The skull can be distinguished from that of gorillas, first, by the smaller size (the greatest length of the skull is rarely above 220 mm, whereas even in " gorillas it is rarely below 250 mm), and, secondly, by the flattening of the upper face.The supraorbital tori, though often dorsoventrally expanded, are more or less flattened on their anterior surface (as well as being separated in the midline by a depression at glabella), and the lateral orbital pillars are also wide and flat; in particular, the interorbital space is very wide and flat, and there is no median nasal ridge. In the dentition, the enamel is thin. The maxillary incisors are distinctive: broad, thick at the base and with a strong lingual tubercle, deeply incised around the base. Lateral incisors are similar to the central ones. The canines of !! are not as elongated as in ! gorillas, and canine dimorphism is less. Cheekteeth are bunodont, with the cusps low but fairly well defined, without the sharp crests of Gorilla, so that, for example, the central basins of the maxillary molars are not strongly interrupted by the crista obliqua. It is safe to suppose that the ancestral Pan ranged over a larger geographic area and was less restricted in its choice of habitats than the two species are today. Furthermore, on the basis of recent historical evidence, Kortlandt & Van Zon (1969) concluded that P. troglodytes also occupied a broader spectrum of habitats, and they envisaged earlier populations occupying semi-open habitats. These authors emphasized the part played by humans and proto-humans in constraining and progressively diminishing the chimpanzee’s ecological niche. If this is correct, the geographic and ecological range of Pan evidently contracted greatly as the apes relinquished more open habitats to hominins, and such a history has important implications for understanding the behaviour and even the morphology of contemporary populations. For example, their ability to climb tall rainforest trees with apparent ease may be a skill that has been superimposed during the last 5 million years or so over an older, less specialized semi-arborealism. Recent discovery of a half-millionyear-old fossil chimpanzee in Kenya (McBrearty & Jablonski 2005), in the Kapthurin Formation, where early human fossils are also found, may take the prediction of such evolutionary changes out of the realm of speculation and into scientific documentation. The exploitation by Pan of fruit or seeds in tall emergent trees within the forest has provoked debate on how making use of this particularly demanding resource might have had a precedent in earlier Pan habitats, such as open woodlands. For a majority of primates, the canopy of the rainforest is the main resource: a second ‘floor’ above the relatively barren, deeply shaded ground below. Competition for all types of food is intense here but the spaced-out emergents above this crowded floor are less accessible to smaller primates for two reasons. One is the physical challenge of climbing thick trunks, the other, more decisive inhibitor, is exposure to predators. Even if, as Kortlandt & Kooij (1963) and others have suggested, Pan was originally less of a true forest animal, its exploitation of spaced out large woodland trees (something that still occurs) would have ‘pre-adapted’ these large-bodied, powerfully muscled apes to make use of forest emergents (Kingdon 2003). Such an interpretation is consistent with the exceptional development of the forelimbs and strength of the chimpanzee’s long, curved fingers. In relation to their putative hominin competitors, these traits would have closed off

Central Chimpanzee Pan troglodytes troglodytes adult male.

Gracile Chimpanzee (Bonobo) Pan paniscus adult male.

any possibility of chimpanzees becoming bipedal. For that outcome an opposite trend – reduction, not amplification – of the forelimb would have been necessary. All P. troglodytes populations so far studied have turned out to be partially carnivorous, hunting monkeys (predominantly red colobus Procolobus spp.) in particular, also occasionally small ungulates such as duikers Cephalophus spp. and Philantomba spp., Bushbucks Tragelaphus scriptus and young Bushpigs Potamochoerus larvatus. Hunting is often a cooperative affair and, like many other aspects of chimpanzee behaviour, differs in its cultural norms from place to place.This, as well as the fission–fusion community social organization, patterns of tooluse and tool-making, and so on, speaks of a behavioural heritage that in many respects parallels that of humans – or were these features already characteristic of the common ancestor, as parsimony would suggest? The first identified chimpanzee fossil (consisting of teeth only) was, as described above, found in the Baringo region of Kenya, in deposits only slightly less than 545,000 years old (McBrearty & Jablonski 2005). Schwartz & Tattersall (2003) suggested that some isolated teeth from the Plio-Pleistocene (ca. 1.8 mya) of Koobi Fora, east of L. Turkana, Kenya, a well-known site of early hominins, may also actually be proto-chimpanzee, including one of the teeth (1590F) usually ascribed to a specimen of Homo rudolfensis. If this is so, it implies that we should also look for other representatives of the Panini in early hominin deposits. Colin P. Groves & Jonathan Kingdon

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Pan troglodytes ROBUST CHIMPANZEE (COMMON CHIMPANZEE) Fr. Chimpanzé commun; Ger. Gemeiner Schimpanse Pan troglodytes (Blumenbach, 1775). De generis humani varietate nativa, p. 37. Mayoumba, Gabon.

consistent, though genetic similarities prompted some researchers to suggest that Pan could be regarded as a subgenus of Homo (Wildman et al. 2003). Genetic studies put the divergence of the Homo–Pan clade in the late Miocene (ca. 8–6 mya) (Caccone & Powell 1989, Ruvolo 1997, Perelman et al. 2011, Roos et al. 2011). No confirmed cases of hybridization between P. troglodytes and any other ape taxon. Synonyms: adolfi-friederici, africanus, angustimanus, aubryi, calvescens, calvus, castanomale, chimpanse, cottoni, ellioti, fuliginosus, fuscus, graueri, heckii, ituricus, ituriensis, jocko, koolookamba, lagaros, leucoprymnus, livingstonii, mafuca, marungensis, nahani, niger, ochroleucus, oertzeni, pan, papio, pfeifferi, pongo, purschei, pusillus, raripilosus, reuteri, satyrus, schneideri, schubotzi, schweinfurthii, steindachneri, tschego, vellerosus, verus, yambuyae. The complete genome has been sequenced (Chimpanzee Sequencing and Analysis Consortium 2005). Chromosome number: 2n = 48 (Young et al. 1960).

Brachiating adult male Central Chimpanzee Pan troglodytes troglodytes.

Taxonomy Polytypic species. There is a complicated history of generic, specific and subspecific classification, resulting from both broad anatomical similarities among African and Asiatic ape taxa, and from considerable inter-individual variation in colouring and facial features within Pan. Most common former classifications substituted the generic names Anthropopithecus, Troglodytes or Simia and/or the species name satyrus (Hill 1969, Jenkins 1990, Groves 2001).The type specimen, no longer in existence and given the name Simia troglodytes, was likely P. t. troglodytes (Hill 1969). Current designation as a single species can be traced to Schwarz (1934, using the species name satyrus) and Allen (1939), who both included the Gracile Chimpanzee (or Bonobo) Pan paniscus within Pan troglodytes. Coolidge’s (1933) classification of the Gracile Chimpanzee into a separate species is widely accepted today. One genetic study suggests that the Western Chimpanzee has diverged sufficiently to be designated as a full species, Pan verus (Morin et al. 1994). Modern taxonomic usage is fairly

Description Moderately large, robustly built, knuckle-walking ape. Sexes alike in colour but adult "" have smaller canines, narrower shoulders, and are about 80% as heavy as adult !!. Face, ears, hands and feet of infants pink, generally darkening to brown or black in adults; often with a dark ‘mask’ in juveniles. Head prognathic with pronounced brow ridges. Face and centre of forehead primarily bare and framed by hair. Iris orange-brown to dark brown. Sclera brown (rarely, white). Ears completely or partially bare, humanlike in general shape but relatively large, and can face forward or lay flat against the side of the head. Upper and lower lips highly flexible and strong. Hands long and slender with short, opposable thumb. Metacarpals and phalanges curved. Fingers and palms hairless. Grasping feet with broad soles and short toes. Sole and toes hairless. Forelimbs slightly longer than hindlimbs. Tail absent. Pelage long, coarse, dark brown to black. Many older adults with light brown or grey hair on the lower back, legs and/or chin. Immatures with tuft of white hair above the anus. Geographic Variation Three subspecies widely recognized (Groves 2001, Becquet et al. 2007). Genetic (Gonder et al. 1997, 2006, 2011, Stone et al. 2010, Bowden et al. 2012) and molar morphometric (Pilbrow 2006) data strongly support the designation of a fourth subspecies, P. t. ellioti (formerly vellerosus; Oates et al. 2009, Morgan et al. 2011, Oates 2011), and point to weak divergence between P. t. troglodytes and P. t. schweinfurthii (Gonder et al. 2011). Hill (1969) described a fifth subspecies, P. t. koolokamba, the Gorilla-like Chimpanzee; this designation has no current credence, as both historical (Schwarz 1939) and modern (Groves 2001) experts define these specimens within P. t. troglodytes. Based on a recent craniometric study, Groves (2005b) argues for two subspecies within what is presently P. t. schweinfurthii; a north-eastern subspecies (P. t. schweinfurthii) and a south-eastern subspecies (P. t. marungensis). This is, however, not supported by the genetic evidence (Gonder et al. 2011). Others argue that subspecies designations are not warranted (Fischer et al. 2006). Resolution of these issues awaits 55

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Pan troglodytes

greater understanding of gene flow among populations and studies at the known and probable geographic limits or contact zones for each taxon (Jolly et al. 1995, Won & Hey 2005). Here, four subspecies are recognized, following the current IUCN classification (Grubb et al. 2003). All subspecies are best diagnosed based on the locality of collection or sighting; we provide some general phenotypic characteristics of each subspecies, though individual phenotypic variation is extensive enough to preclude diagnostic field criteria to distinguish the taxa. P. t. verus Western Chimpanzee or Upper Guinea Chimpanzee. Southeastern Senegal and S Mali south-east to either the Dahomey Gap (Bénin) or Niger R. Tend towards profuse white ‘beards’. Darkly pigmented circumocular and/or nasal ‘mask’ develops rapidly. Face often maintains some pink colouration into adulthood. Face typically broad across forehead with ears large, prominent and pale. Hair of scalp parting along midline. Palms and soles pale with irregular patches of darker pigment on digits. P. t. ellioti Elliot’s or Gulf of Guinea or Nigerian-Cameroon Chimpanzee. Southern Nigeria and W Cameroon, probably from the Dahomey Gap (Bénin) or Niger R. south to the lower Sanaga R. (Morgan et al. 2011, Oates 2011). Recognized based on mtDNA (Gonder et al. 1997, 2011) and molar morphometric (Pilbrow 2006) evidence. Relative to P. t. verus, ears small and lie close to head; top of head rounder; brow ridge straighter, more gracile build; face, hands and feet uniform black in adults (Oates 2011). P. t. troglodytes Central Chimpanzee or Lower Guinea Chimpanzee. Sanaga R. south-east to Ubangi R. and south to Congo R. Skin, including face, ears, palms and soles, tends to be uniformly dark brown or black in adulthood. Ears small to medium. Tends to quickly develop prominent bald patches on the forehead. P. t. schweinfurthii Eastern Chimpanzee or Long-haired Chimpanzee. Ubangi R. east across DR Congo, north of Congo R. and east of

Eastern Chimpanzee Pan troglodytes schweinfurthii juvenile.

Lualaba R. to SW Tanzania. Slightly smaller in body size than other subspecies. Hair long, particularly around the face and shoulders. Facial pigmentation ranges from pale brownish-pink to brown or greyish-black in adulthood, with traces of pink evident primarily near the lips in some individuals. Face typically longer than P. t. verus. Palms and soles usually brick red to bronze. Similar Species Pan paniscus. Parapatric. Limited to central Congo Basin, DR Congo, south of the Congo R. More gracile, ca. 15% lighter. Head small and round. Mouth region contrastingly pink. Face black at birth. Upper molar rows not parallel. Gorilla gorilla and Gorilla beringei. Sympatric. Larger (adult !! >130 kg). Ears relatively small and black. Sagittal crest well developed in adult !!. Nasal openings nearer to mouth than to orbits. Distribution Historical Distribution The historical geographic range of P. troglodytes is roughly 2.3 million km2 (Butynski 2003), comprising 25 countries. Probably extirpated from Bénin, Burkina Faso and Togo, but confirmation needed. On the verge of extirpation from Senegal and Ghana. Extirpated from large areas within most countries. Current Distribution Endemic to equatorial Africa. Rainforest BZ. Occurs in 22 or 23 countries from Senegal east to SW Tanzania, from ca. 13° N to 7° S (Butynski 2001, 2003). Habitat Most habitats are mosaics, particularly of moist evergreen or semi-deciduous forest, swamp forest, gallery forest, woodlands, colonizing forest and grassland. Preferred habitats are mature forests, though colonizing forests are frequently used. Altitudes range from sea level to at least 2949 m (Nyungwe Forest, Rwanda; Gross-Camp et al. 2009). Mean annual rainfall is typically

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over 1400 mm (summarized in: Kortlandt 1983, Butynski 2001). A few populations, including those at Fongoli and Mt Assirik, Senegal (P. t. verus), and Ugalla (Tongwe), Tanzania (P. t. schweinfurthii), utilize drier, open grassland and woodland habitats (Itani 1979, McGrew et al. 1981, Pruetz 2007). Associated and important plant species cannot be generalized across sites, though the density of Robust Chimpanzees seems to vary positively with the density of large trees bearing fleshy fruit (Balcomb et al. 2000). Abundance Estimates of abundance are rough given that only a small portion of the species’ range has ever been surveyed, and that most of the survey data were collected well over a decade ago. Abundance data for many areas may now be overestimates due to recent catastrophic disease outbreaks, heavy hunting and habitat loss (see Conservation). These figures may also be misleading due to highly fragmented habitats; e.g. Uganda contains 4000–5700 Robust Chimpanzees, but many of these are in small populations (20 dimorphism in the Eastern Chimpanzee P. t. schweinfurthii and humans years old.Today P. paniscus has a patchy, highly fragmented distribution (Parrish 1996). Despite its common name ‘Pygmy Chimpanzee’, P. (Butynski 2001). Rare or absent where human population density paniscus is not a diminutive form of chimpanzee; the range in body is high (Kano 1984, 1992, Reinartz et al. 2006). Surveys in the size and weight overlaps (up to 85%) that of P. t. schweinfurthii. Head central portion of the range confirm presence at: North and South rounded with small brow. Face black, even in infants. Lips light to Sectors of Salonga N. P. (Reinartz 2003, Blake 2005, Reinartz et pink, contrasting with face. Ears small, close to sides of the head. Head al. 2006, 2008, Grossman et al. 2008), Lui Kotal on the western hair flattened with long horizontal tufts of hair surrounding the face. edge of Salonga N. P. (Hohmann & Fruth 2003c, Mohneke & Fruth Body covered by long silky black hair (except for face, hands, feet and 2008),Wamba (Furuichi & Mwanza 2003, Idani et al. 2008), Lomako genitalia). Anal tuft white. Upper molar rows curved. Features such (Dupain et al. 2003), Lukuru (Thompson & Tshina-tshina 2003), as smaller head, less prominent canine teeth, white tail tuft and low Kokolopori north-east of Wamba (Thompson et al. 2003), and south degree of sexual dimorphism are considered by some primatologists to of Lokoro (J. Eriksson pers. comm.). In the eastern extent of the be juvenile characteristics indicating paedomorphic evolution (Gijzen range, P. Paniscus occurs between the Lomami R. and Congo-Lualaba 1974, Kuroda 1979, 1980, Kano 1992). R. (Hohmann & Eriksson 2000, Vosper et al. 2007). Five remnant populations have been confirmed at the extreme western end of the Geographic Variation None recorded. range: three between Lac Tumba and Lac Mai Ndombe (Mwanza et al. 2003, Inogwabini et al. 2007, 2008), and two between the Congo Similar Species None within the known geographic range of R. and Kwa-Kasai R. (Inogwabini et al. 2007). P. paniscus. Pan troglodytes. Parapatric with P. paniscus. More robust, ca.15% Habitat Mosaic of low, dry, semi-deciduous forest punctuated heavier. Head large, vault flattened, face prognathic, brow ridge by monotypic stands of primary evergreen forest, swamp forest and well developed. Skull length greater (!!: mean = 198 mm, secondary forest (Evrard 1968, Boubli et al. 2004). In the drier and range = 182–213 mm, n = 23; "": mean = 186 mm, range higher elevations of the southern portion of the range, the forest is 65

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increasingly interposed by grasslands. Optimal habitat is dense, humid, mixed mature, semi-deciduous lowland forest on terra firma soils with herbaceous understorey (Marantaceae, Zingiberaceae) (Kano 1983, Kano & Mulavwa 1984, Kortlandt 1995, Reinartz et al. 2006). Pan paniscus can, however, utilize a wide variety of habitat types, including young and old secondary forest, grassland, marsh grasslands, seasonally inundated and swamp forests, and agriculture (Sabater Pi & Vea 1990, Thompson-Handler et al. 1995, Hashimoto et al. 1997). Altitudinal range: 300–565 m. Annual temperature range: 19–30° C. Annual rainfall range: 1670–2210 mm (Kano 1992, Thompson 1997).

1996). Pan paniscus rarely use tools for food acquisition. However, they do incorporate tools into social communication, such as branchdragging by adults (see Social and Reproductive Behaviour), or by infants during social play (Ingmanson 1988, 1996). In addition, P. paniscus occasionally makes and uses napkins, fly swatters, tooth picks and other items, and drapes vegetation over the head and shoulders to provide protection during heavy rains (Kano 1982, Fruth & Hohmann 1993, Ingmanson 1996).

Foraging and Food Omnivorous. Pan paniscus spend up to 40% of their time foraging/feeding. Most foraging occurs within groups while Abundance The majority of the survey data for P. paniscus are in trees (White 1989). At Lomako and Wamba, group size is positively two decades old and vast areas of the potential range, estimated correlated with food patch size and food abundance (White 1989, at 343,000 km2 (Butynski 2001), have never been surveyed Kano 1992, Mulavwa et al. 2008, Furuichi et al. 2008), but studies in (Thompson-Handler et al. 1995, Dupain & Van Elsacker 2001b). Salonga do not reveal any correlation (Hohmann et al. 2006). Population estimates are based on density estimates ranging from Fruits, located most often in the canopy, constitute 54–83% of the 0.25 ind/km2 (Thompson 1997) to 0.40 ind/km2 (Kano 1984) and diet. Fruits of Apocynaceae vines, Pancovia, Dialium, Polyalthia and extrapolated to the probable occupied area. Because of widespread Annonidium, are particularly common in the diet. Leaves comprise hunting by humans and loss of habitat, the area occupied by P. paniscus 15–21% (Caesalpiniaceae, Papilionaceae) of the diet, and seeds, piths, at present is believed to be far less than the potential historical range. shoots and animals constitute the remainder (Badrian & Malenky The most recent estimates are that there are between 20,000 and 1984, Kano & Mulavwa 1984, White 1992, Idani et al. 1994). Diet 50,000 individuals (Butynski 2001, Dupain & Van Elsacker 2001b). is high in protein, low in tannins and, compared to P. troglodytes, is relatively low in sugar and crude fat (Hohmann et al. 2006). Adaptations Semi-terrestrial and diurnal. Pan paniscus is Terrestrial herbaceous vegetation (predominantly Marantaceae) considered more of a true forest ape than P. troglodytes and, as such, is an important source of protein (Malenky & Stiles 1991). When many of the morphological characters that separate P. paniscus from P. foraging on herbs, P. paniscus quietly splinter off into subgroups in troglodytes are described as adaptations to differences in the habitats search of shoots and petioles of Haumania liebrechtsiana, Megaphrynium they occupy (Susman 1984a). Compared to P. troglodytes, P. paniscus macrostachyum and Aframomum spp. Fruit consumption (and species has narrower shoulders, chest and hips, longer legs, nearly equal leg consumed) varies according to availability (Kano & Mulavwa 1984), and arm lengths, a greater proportion of leg to body mass resulting whereas Marantaceae herbs are utilized at approximately the same in a lower centre of gravity, and a higher propensity to walk bipedally levels throughout the year (Malenky & Stiles 1991). Pan paniscus (Zihlman 1980, 1996, Susman 1984a, Thompson 2002). However, occasionally eat marshland herbs and grasses (Uehara 1990), and recent studies that extend the range of P. paniscus into drier forest/ sub-aquatic algae and vegetation (Thompson 2002). Coprophagy is savanna mosaic habitats challenge this assumption (Thompson 2002). practiced but is rare (Sakamaki 2010). When arboreal, P. paniscus engages in more leaping and diving types Although ‘cooperative hunting’ has never been observed, duikers of movements than does P. troglodytes (Doran 1996). Whether or not (Cephalophus spp. and Philantomba monticola), anomalures Anomalurus P. paniscus is more arboreal than P. troglodytes, as once believed, is open spp., shrews, snakes and many invertebrate species are eaten (Ihobe to question. Pan paniscus is said to engage in bipedal behaviour more 1992, Kano 1992, Hohmann & Fruth 1993). Patterns of meat eating, often than P. troglodytes, especially when carrying objects, entering meat sharing and prey search image appear to vary among populations water, to peer over tall grasses and during friendly social behaviour (Hohmann & Fruth 2003a). Pan paniscus travel 0.4–6.0 km per day (whereas P. troglodytes is more likely to engage in bipedalism during while foraging in forest habitat (Kano 1992). Once a food patch is aggressive interactions). Webbing that sometimes occurs between located, group feeding is often preceded by vocalizations and animated the toes of P. paniscus may be related to their willingness to enter movements as food is collected and consumed (Kuroda 1980, Kano water to forage. Molars of P. paniscus are more flattened than those 1992). Food begging and sharing are frequent (Fruth & Hohmann of P. troglodytes, providing a greater grinding surface area. This may 2002). Adults may reach out a hand slowly toward the possessor’s food, allow higher consumption rates of terrestrial herbaceous vegetation and may touch and grin. The possessor responds either by ignoring by P. paniscus, which may be associated with decreased individual or by giving the beggar a portion of the food. Copulations between feeding competition and larger social groups (Malenky & Stiles !! and "", as well as homosexual encounters, are frequent during 1991). However, measurements of mandibular traits do not indicate feeding times (e.g. "" engage in intensive genito-genital rubbing). that P. paniscus is necessarily adapted to a coarser and more fibrous diet than P. troglodytes (Taylor 2002). Social and Reproductive Behaviour Social. As for P. Tool-using behaviour of P. paniscus differs from that of P. troglodytes troglodytes, the community or unit-group is the largest mixed(Hohmann & Fruth 2003a). The ability of P. paniscus to make and sex social unit, whose members maintain a closed social network. use tools is clear from observations of the extensive use of tools Community’s members share a discrete, large home-range (22– by captive individuals (Takeshita & Walraven 1996), as well as the 60 km²), but extensive overlap between communities (40–66%) may complexity of their manipulation of objects in the wild during nest- exist and there may be seasonal and yearly variations in home-ranges building and arboreal bridging (Fruth & Hohmann 1993, Ingmanson (Van Elsacker et al. 1995). Communities contain 10–22 individuals 66

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Distinctive proportions of Gracile Chimpanzee (Bonobo) Pan paniscus; longer limbs and more slender than Robust Chimpanzee Pan troglodytes (gouache from photographs).

in Lomako and 30–120 individuals in Wamba (Kano & Mulavwa 1984). There are almost equal numbers of adult !! and adult "" in Wamba (Kano 1992), whereas in at least one Lomako community, the adult sex ratio is strongly female-biased (Fruth 1995, Hohmann et al. 1999). Entire communities come together less often at Lomako than at Wamba (Kano 1992, F. J. White 1992, Fruth 1995). Through fission and fusion, membership of parties changes in varying degrees within days, hours or even minutes. By contrast, membership of communities changes only with the birth or death of members, or permanent inter-group transfer. Smallest functional unit of P. paniscus daily life is the party, defined as individuals remaining in sustained proximity to one another, or

within earshot of each other (Hashimoto et al. 2003), or travelling and foraging together (Van Elsacker et al. 1995). Larger, more stable parties are seen in Wamba, with on average 13 individuals (Kano 1992), than in Lomako, with about five individuals on average (1–16) (Hohmann & Fruth 2002). Parties usually contain mature individuals of both sexes, with more "" than !! (Kano 1982, F. J. White 1988, Fruth 1995, Hohmann & Fruth 2002). Pan paniscus lives in fission–fusion communities or unit-groups (Kano 1992). Unit-groups have recognizable members, with " transfer out of, and ! residency in, the natal group. A possible case of fusion of unit-groups was observed at Wamba following population disruption related to human activities (Hashimoto et al. 67

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2008). In comparison to P. troglodytes in East Africa, P. paniscus unit groups tend to be more cohesive and larger. Strong social bonds exist among "" and !!, and among "" (Furuichi 1997, Furuichi et al. 1998, Hohmann et al. 1999, Hohmann & Fruth 2002, Stevens et al. 2006). Relative to P. troglodytes, P. paniscus has low levels of aggression, both between and within unit groups. However, violent acts do sometimes occur during encounters of different unit groups (Hohmann & Fruth 2002). Males and "" both form dominance hierarchies within the group (Furuichi 1997, Vervaecke et al. 2000a, Stevens et al. 2007). Unrelated "" form social bonds with each other and support each other against aggression by !! (Kano 1992, Parrish 1996, Vervaecke et al. 2000b). The bond between mothers and their adult sons is very strong, long lasting and may play a role in the dominance hierarchy. In one unit-group at Wamba, !! rarely became alpha-male until their mother achieved alpha status (Kano 1992, Furuichi 1997). Sexual behaviour occurs in almost all age–sex categories, including infants (Hashimoto 1997), and plays an important role in the non-reproductive social cohesion of a group, i.e. maintaining male–female coexistence (Kano 1992). Compared with P. troglodytes, P. paniscus "" exhibit sexual swellings that extend beyond the ovulatory period (Thompson-Handler 1990, Heistermann et al. 1996, Vervaecke 1999, Furuichi & Hashimoto 2002). Adult copulations are not limited to time of ovulation, but the majority of copulations occur at maximum swelling, a period that is loosely linked to the fertile phase (Furuichi 1987, Kano 1989, Vervaecke 1999, Reichert et al. 2002). Takahata et al. (1996) showed that adult P. paniscus !! at Wamba do not copulate more than adult P. troglodytes !! at Mahale (P. paniscus: 0.10–0.21/h; P. troglodytes: 0.20–0.29/h), that adolescent P. paniscus !! copulate less frequent than adolescent P. troglodytes !!, and that adult P. paniscus "" copulate at an equal rate to adult P. troglodytes "". Only adolescent P. paniscus "" copulate more frequently than adolescent P. troglodytes "". Copulations also occur between adult "" and juvenile !!, though rarely between mothers and sons (Kano 1992). Adult !! mount and thrust, and occasionally penetrate juvenile "", but the frequency of penetration increases as "" reach adolescence and begin exhibiting sexual swellings. Adult !! also use genital stimulation toward infants as an apparent means of soothing them (Hashimoto 1997). Sexual contact between adult !! takes the form of mounting, often reciprocally, rump–rump touching and, on rare occasions, penile fencing. Sexual activities between adult "" have been much studied (Hohmann & Fruth 2002, 2003b, Fruth & Hohmann 2006). Genitogenital (G-G) rubbing occurs when two "" embrace ventrally and move their hips laterally, rubbing the labia and clitoris together (Kano 1992). Females engage in G-G rubbing during periods of excitement, such as greeting and feeding. This behaviour may serve as a mechanism for social bonding between the "", allowing them to cooperate and share feeding spaces without aggression. Young "" who first enter a group quickly seek out the dominant "" and engage in G-G rubbing (Idani 1991). Kuroda (1984) describes the use of a rocking gesture by freeliving P. paniscus to request closer proximity to one another. Ingmanson (1996) describes the use of branch-dragging to convey complex information related to coordinating group movement, such as direction and timing of movement.

Reproduction and Population Structure Most of the demographic data for P. paniscus come from Wamba, where freeliving P. paniscus have been food provisioned and studied for 20 years (Kano 1992, Furuichi et al. 1998). In both species of Pan, mature "" have continuous cyclic ovarian activity accompanied by overt swelling of the anus and labia, reaching maximal volume and turgidity in the period around ovulation. In wild P. paniscus, swelling cycles and menarche first occur at 9–12 years of age (Kano 1992); in captivity, they occur, on average, at 8.2 years (range = 6.0–11.2 years, n = 9; Thompson-Handler 1990). Onset of menarche is generally followed by 2–3 years of adolescent sterility (Van Elsacker et al. 1997). In P. paniscus, the period of swelling is longer than the window of fertility, and the end of the period of maximal swelling and the timing of ovulation are weakly associated (Heistermann et al. 1996, Reichert et al. 2002). Wild adult "" at Wamba showed maximal swelling during 48% of the cycle (Kano 1992), while wild adolescent "" showed maximal swelling most of the time (Kano 1984). Swelling in P. paniscus may conceal rather than signal ovulation (Kano 1992, Reichert et al. 2002) leading to longer periods of " sexual receptivity in P. paniscus than in P. troglodytes (ThompsonHandler et al. 1984, Furuichi & Hashimoto 2002). In wild "", the mean interval between two successive maximal swellings is 42 days (range = 37–49, n = 3; Furuichi 1987). In captivity, the mean length of the menstrual cycle is 34 days (range = 31–51 days, n = 6; Heistermann et al. 1996). If conception does not occur, there are 1–3 days with slight vaginal bleeding (Vervaecke 1999, Vervaecke et al. 1999). In contrast to P. troglodytes, where the labia are entirely flat during non-fertile phases of a normal cycle, the labia are flat only in some captive adults during the latter half of pregnancy and/or early lactation (Vervaecke 1999). Captive !! reach sexual maturity at an average age of ca. seven years (ThompsonHandler 1990). However, DNA analyses confirm the paternity of captive !! as young as five years of age (Leus et al. 2003, Reinartz et al. 2003). In captivity, gestation averages 234 days (range = 229– 238, n = 3) from hormonally detected ovulation, or 246 days (range = 227–277, n = 11) from last menses (Harvey 1997). Single young are most frequent; twins are exceptional. Newborns weigh ca.1.5 kg (range = 1.2–1.8, n = 13; Mills et al. 1997). Age of "" at first birth ca. 12–13 years in the wild (Kano 1992), and 14.2 years (n = 6) (Kuroda 1989) and 10.5 years in captivity (8–15 years, n = 20; De Lathouwers & Van Elsacker 2003, 2005, Reinartz et al. 2003). At Wamba, mean birth interval is 4.8 years (n = 28; Furuichi et al. 1998). At Lomako, however, the median birth interval may be as long as nine years (B. Fruth pers. comm. in Knott 2001). Mean birth interval in captivity is 4.93 years (range = 1.88–7.60, n = 34; De Lathouwers & Van Elsacker 2003, 2005). The infant is generally weaned at the birth of the next sibling. In the wild, births occur throughout the year with a peak (57%) in Mar– May (n = 15) and a low period (43%) from Oct–Feb (Furuichi et al.1998). Furuichi et al. (1998) reported a 4.5% first-year mortality for infants at Wamba (n = 22 infants); however, this rate is the lowest reported for any great ape and may be a sampling artefact. In captivity, 16% of P. paniscus infants are stillborn (De Lathouwers & Van Elsacker 2003). Of live born infants, 21% die during the first year (n = 155 infants) (Reinartz et al. 2003) and 84% of live-born offspring survive until five years of age (n = 51) (De Lathouwers & Van Elsacker 2003, 2005, Reinartz et al. 2003).

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Pan paniscus

Sex ratios: ! : " ratio: 1 : 1.1 (n = 70; Kitamura 1983). 1 : 1.3 (n = 69; Kuroda 1979). 1 : 2.1 (n = 22) for Group 1; 1 : 1.6 (n = 23) for Group 2; 1 : 1:1 (n = 9) for Group 3 (White 1988). Adult ! : adult " ratio: 1 : 1.1 (n = 31; Kano 1982). 1.1 : 1 (n = 32) for Group 1; 1 : 0.9 (n = 39) for Group 2 (Kano 1987). Adolescent ! : adolescent " ratio: 1 : 1.6 (n = 13; Kano 1982). 1 : 1.6 (n = 18) for Group 2 (Kano 1987). In captivity, no sex ratio bias at birth (64 : 73 : 4 = ! : " : unknown; n = 141; De Lathouwers 2004). Females in the wild typically emigrate from their natal group at ca. 7–8 years. Males remain in their natal group and retain a lifelong bond with their mother (Kano 1992). Maximal life-span is unknown for wild P. paniscus, and is >50 years in captivity (Leus et al. 2003, Reinartz et al. 2003). Predators, Parasites and Diseases Except where local taboos against hunting still exist, humans are the main predator of P. paniscus throughout the range, and present rates of off-take are unsustainable (Thompson-Handler et al. 1995, Butynski 2001, Dupain & Van Eslacker 2001a, Reinartz et al. 2006, Hart et al. 2008, Idani et al. 2008). Natural predators probably include Leopards, African Crowned Eagles Stephanoaetus coronatus (Horn 1980, Kano 1983), Nile Crocodiles Crocodylus niloticus and Central African Rock Pythons Python sebae. Because of its close genetic relationship to humans and frequent close contact with humans, P.paniscus is highly susceptible to numerous human diseases, including the following (reviewed Butynski 2001, Woodford et al. 2002): colds, pneumonia, influenza, tuberculosis, measles, mumps, hepatitis A and B, bacterial meningitis, diphtheria, yellow fever, whooping cough, poliomyelitis, encephalomyocarditis, and haemorrhagic fevers such as Ebola. Thus, the species is vulnerable to the diseases/epidemics manifested in surrounding human populations. Near Wamba P. paniscus has displayed leprosyand herpes-like lesions, and a high incidence of limb abnormalities (Kano 1992). Internal parasites in wild P. paniscus include Troglodytella sp., Capillaria sp., Trichuris sp., Strongyloides sp., dicrocoeliid eggs and strongylid eggs resembling hookworm eggs (Hasegawa et al. 1983). Illnesses in newly orphaned P. paniscus commonly include severe diarrhoea (attributed to or exacerbated by parasites), infections (gram-negative bacteria), gum disease, severe psychological stress, immune suppression and life-threatening malnutrition (Messinger & Bi-Shamamba 1997, D. Messinger pers. comm.). Their parasites include Ancylostoma spp., Trichomonas intestinalis, Strongyloides spp., Entamoeba histolytica, whipworms, tapeworms, mites and lice (Messinger & Bi-Shamamba 1997, Butynski 2001). Captives are sensitive to respiratory infections and laryngeal air sacculitis (Rietschel & Kleeschulte 1989). Conservation IUCN Category (2012): Endangered. CITES (2012): Appendix I. Population decline is primarily the result of unsustainable hunting due to the combination of several key factors, including a growing

bushmeat trade (Butynski 2001, Dupain & Van Elsacker 2001a, Rose et al. 2003), the disappearance of traditional taboos against eating P. paniscus (Furuichi & Mwanza 2003), the uncontrolled infusion of firearms into the region combined with the occupation of onceremote areas by soldiers and displaced people during civil wars (Draulans & Van Krunkelsven 2002, Amman et al. 2003) and the lack of law enforcement. Formerly dense populations of P. paniscus (e.g. Lomako) may have suffered a decline of up to 75% as a consequence of the civil war and concomitant increases in hunting (Amman et al. 2003, Dupain et al. 2003). Trade in orphans for pets is a continuing problem (C. Andrè pers. comm.) Massive habitat destruction stems from logging and agriculture. While logging in DR Congo has not yet reached the levels of other central African countries (Wolfire et al. 1998), where logging occurs it has caused habitat destruction, population fragmentation and a dramatic increase in bushmeat hunting (Butynski 2001, Dupain & Van Elsacker 2001a, Rose et al. 2003). There is only one national park designated for P. paniscus protection, the Salonga N. P. It is not yet clear whether this Park harbours a viable population (Reinartz et al. 2006). Conservation priorities are: (1) to assess the distribution/abundance of P. paniscus in order to identify major populations; (2) to determine the degree of population fragmentation and the ecological factors affecting distribution; and (3) to direct resources toward law enforcement, support for protected areas and creation of additional protected areas. In captivity, P. paniscus has the smallest population of all the great ape species: 168 individuals worldwide (excluding African sanctuaries). With intensive genetic and demographic management, the captive population can be self-sustaining for up to five generations (Reinartz et al. 2003). Measurements Pan paniscus HB (!!): 780 (730–830) mm, n = 4 HB (""): 740 (700–760) mm, n = 4 T (both sexes): 0 mm HF (!!): 22 (21–22) mm, n = 4 HF (""): 22 (20–22) mm, n = 4 E (both sexes): 63 (55–72) mm, n = 7 WT (!!): 45 (37–61) kg, n = 7 WT (""): 33 (27–38) kg, n = 6 GLS (!!): 163 (150–171) mm, n = 28 GLS (""): 163 (142–172) mm, n = 31 Data from museum specimens from various localities in DR Congo (HB, WT: Jungers & Susman 1984; HF, E: Coolidge & Shea 1982; GLS: Jenkins 1990) Key References Butynski 2001; Furuichi & Thompson 2008; IUCN & ICCN 2012; Kano 1992; Susman 1984b; ThompsonHandler et al. 1995. Gay E. Reinartz, Ellen J. Ingmanson & Hilde Vervaecke

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Tribe HOMININI Hominins Hominini Gray, 1825. Annals of Philosophy 10: 338.

An international scramble to find human and proto-human fossils, especially in Africa, has begun to flesh out the concrete, physical evidence for human evolution. Tracing the past fortunes of the Hominini, therefore, promises to become one of the best documented, and certainly the single most arresting, example of the process that has given rise not only to us but to all the astonishing diversity of life on Earth. It is this that makes the Hominini one of the most fascinating taxa among African mammals. By the same token, this is a fast-moving field of enquiry and the wide scatter and fragmentary nature of most fossil hominins creates difficulties when it comes to listing and describing the substantial number of fossil forms belonging to this tribe. The following genera are commonly recognized in the Hominini: Sahelanthropus Brunet et al., 2002 (‘Toumai’). Late Miocene (7–6 mya). Resemblances with gorillas Gorilla spp., chimpanzees Pan spp. and hominins suggest it might predate hominin emergence. While

possibly not Hominini, Sahelanthropus is listed here because it is a highly significant fossil for our understanding of hominin emergence. Orrorin Senut et al., 2001 (Millennium Human Ancestor). Late Miocene (ca. 6 mya). Ardipithecus White et al., 1995 (Ground Apes). Late Miocene to early Pliocene (5.8–4.4 mya). Also see White et al. (1994, 2009). Praeanthropus Weinert, 1950 (‘Lucies’). Early to mid-Pliocene (4.2– 3.0 mya). Australopithecus Dart, 1925 (Southern Ape and South Africa Manape). Mid- to late Pliocene (4.2–2.0 mya). Kenyanthropus Leakey et al., 1995 (Kenya Flat-face Man). MidPliocene (ca. 3.5 mya). Paranthropus Broom, 1938 (‘Nutcracker Man’). Mid-Pliocene to early Pleistocene (2.6–1.4 mya). Homo Linnaeus, 1758 (Early to Modern Humans). Mid-Pliocene (2.4 mya) to present day.

The certainty of ancestors – the uncertainty of ancestry (from Kingdon 2003). Top row: Australopithecus (Praeanthropus) anamensis, A. (P.) afarensis, A. (P.) bahrelghazali, A. (P.) aethiopicus, A. (P.) garhi, A. (P.) robustus, A. (P.) boisei. Middle row, left: Orrorin tugenensis, Kenyanthropus platyops, Homo rudolfensis. Middle row, right: Homo ergaster, H. heidelbergensis, H. sapiens. Bottom row, left: Australopithecus africanus, Homo habilis.

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Homo sapiens

H. sapiens neanderthals H. erectus

Homo ergaster ‘A.’ robustus ‘H.’ ‘A.’ boisei ‘H.’ habilis rudolfensis ‘A.’ aethiopicus A. africanus ‘A.’ afarensis

Australopithecus Pan

Ramapithecus

Gorilla

Changing perceptions of Human ancestry. Left: Loring Brace (1971). Centre: Olson (1981)/Falk (1988). Right: Hominin genealogy according to the ‘Evolution by Basin Model’ (modified after Kingdon 2003).

This classification includes at least three paraphyletic genera, that are presumed to incorporate successive lineal ancestors of Homo. There has, however, been much reshuffling of species from one genus to another, especially as some authorities do not recognize Paranthropus as separate from Australopithecus, and yet others think that a further genus, Praeanthropus, may be distinct from Australopithecus (Strait et al. 1997, Kingdon 2003). Recently, it has been proposed that all the described species in the Hominini should be incorporated into a single genus, Homo, which of course would lead to the tribe itself being redundant except that it does serve to separate bipedal humans from quadrupedal apes. One must avoid the mistake of assuming that human evolution was unilineal, one species succeeding another in unbroken advance. This assumption, in as far as it still survives, is a legacy of the historical origins of the subject itself – among (mainly medically trained) anatomists, not among evolutionary biologists. It is only since the 1970s that it has become clearer that, just like most other mammals whose fossil record is at all well-known, multiple species of hominins arose, coexisted for a while and mostly became extinct without issue: a bush not a ladder. The characteristics of the Hominini include highly manipulative hands, specializations for habitual upright posture, bipedal locomotion, and extreme reduction of the canine teeth (involving a particular shortening of the pointed tip, but also raising of the mesial and distal ‘shoulders’, to render the canine almost incisiform in both jaws). An intermediate stage of the development of the postural/locomotor specializations appears to be illustrated by Orrorin; in which canine reduction (including reduction of sexual dimorphism) can be seen in the stepwise sequence Ardipithecus kadabba – Ardipithecus ramidus – Australopithecus (Praeanthropus) anamensis – Australopithecus (Praeanthropus) afarensis (using ‘traditional’ generic designations). While intense interest in the origins of our own species has led to extraordinary squabbles, taxonomic instability, and disagreements on phylogeny based on anatomical salami-slicing, there is no doubt that it has led to the

human fossil record being one of the best represented (and, despite all the controversies, best understood) of any mammal lineage. Dated phylogenetic trees serve to illustrate both the growth in the number of taxa thought to be distinct, and significant conceptual progress from the ‘ladder’ model of evolution (Loring Brace 1971) to the much more complex and bushy trees of contemporary thinking. Given that the fossil record is always incomplete, all trees are essentially provisional and tentative, and can be seen as steps in a series of successive approximations. Beyond the number of genera, note the geographical range of fossils and presumed habitats of this family. Prior to some 2.5–2.0 mya (after the emergence of the genus Homo), all representatives of the Hominini appear to have been African. With few exceptions, these Pliocene hominins are known from just two regions: the Rift Valley of eastern and north-eastern Africa, and the caves of the Transvaal highveldt. Throughout their evolutionary history, Hominini have been typical of south-eastern Africa. Partly the reflection of a paucity of fossil sites, this bias shows up in numerous other organisms and supports the supposition that the primary split between protohominins and quadrupedal apes had a geographic and ecological base (Kingdon 1993, 2003). What caused only one of the lineages of hominins listed above (i.e. Homo) to persist and survive? Part of the answer must extend back to an exploration of how the earliest ancestors of humans might have responded to some of the challenges posed by the environment of their region/ecology of origin. Among the influential modifications made in response to specific local ecologies and climates, we can infer adjustments in behaviours such as social organization and modes of communication. Eventually, certain acquired characteristics allowed Homo to spread and out-compete other hominins. Tracing the regional specifics of adaptation, therefore, remains a central strand in the study of hominin and human prehistory. As such, discovering exactly where the human lineage emerged within the vastness of Africa is a quest 71

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of the greatest importance and gives a special value to conserving the full spectrum of African habitats and species. Implied habitats favoured by early hominins are generally wooded and close to water, although some sites represent more closed forest, later ones were adjacent to more open plains. Diets (known as far as the early stages are concerned from stable isotope analysis) were, perhaps, largely vegetarian, including both fruits and underground parts. The latter is clearly consistent with the terrestriality of hominins but also implies the means to excavate. The unearthing or capture of small but numerous food items is implied by hominins having highly manipulative hands (possibly assisted on occasion by crude digging tools). Termite feeding has been convincingly proposed and it can be argued that sustained use of the hands for collecting terrestrial and sub-terrestrial mini-foods was the initial driving factor in the emergence of hominins (Kingdon 2003). Because apes, as well as other primates, prefer a seated position while foraging over prolonged periods for small items on or under the ground, it is reasonable to suppose that this ‘squat-foraging’ posture (as in Geladas Theropithecus gelada) became the norm for the earliest (probably south-eastern African) ground apes. The habitual adoption of such a foraging posture has substantial long term implications inasmuch as natural selection is likely to favour a number of anatomical changes. A stable squatting position on the ground favours flatter, broader feet that can provide a firmer platform for long-armed, mobile forequarters. The latter would have been inhibited because the rib cage of a typical, top-heavy, ape is closely tied to the broad, high blades of the pelvis and the lumbar region is exceptionally weak and inflexible. The fossil record confirms that the development of a functional articulation between the thorax and the pelvis was one of the earliest innovations of hominins. The rib cage became narrower, shorter and flatter (from front to back) while the iliac blades of the pelvis retracted to form a more compact structure that was no longer integrated into a single body mass. Elongation right:

and strengthening of the lumbar region (including an increase in the number and robustness of lumbar vertebrae) allowed a ‘waist’ to develop. The most plausible rationale for this change is that a seated ape needs to twist and flex its body during squat-foraging. Another implication for this behaviour becoming habitual is that selection would favour the head becoming more vertically positioned above, rather than oblique to the spinal column. All these changes in early hominins are commonly correlated with bipedalism but can be even more strongly argued as evolutionary adaptations to squat-foraging. If an intensification of terrestrial foraging with the hands was the motor of Hominin evolution then a seated position for this activity is demonstrably necessary. Previous difficulties for a quadruped attempting to rear up on two legs became negligible once the entire body had become rebalanced (more or less vertically) above a groundbased pelvic basin. Corroboration for a squat-foraging phase in hominin evolution can be inferred from the pelvis, spinal column, skull and feet of the earliest known and best-documented hominin, Ardipithecus ramidus. This species retained long ape-like arms but had a basin-like pelvis, a strong lumbar column with an increased number of larger vertebrae, a typically hominin foramen magnum and, surprisingly, the long legs of a slow but habitual walker (Lovejoy et al. 2009). Emerging from the inner aspect of their broad, splayed feet were rigid, strut-like ‘big toes’. While such feet were crudely functional for both tree-climbing and walking their obviously platform-like structure was somewhat anomalous for both activities. Such a structure not only suggested a squatting ancestry but implied that squatting (on both flat ground and on branches) was still a functional activity for this long-armed, big handed terrestrial biped. It can now be argued that the combination of

Proportions in three hominids while in a squatting posture.

Reconstruction of a Ground Ape Ardipithecus ramidus adult female.

Modern Human Homo sapiens showing contracted pelvis, robust legs and gracile arms.

Gorilla Gorilla showing robust arms, short legs and tall, plate-like pelvis.

Ground Ape Ardipithecus ramidus showing long arms and splayed feet (pelvis uncertain) (derived from J. Matternes in White et al. 2009).

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Anoiapithecus

Sahelanthropus tchadensis

Pan troglodytes

above: Rear views of hominid skulls. Left: Robust Chimpanzee Pan troglodytes. Top centre: Southern Ape Australopithecus (Praeanthropus) afarensis. Top right: Nutcracker Man Paranthropus. Bottom centre: South Africa Man-ape Australopithecus africanus. Bottom right: Handy Man Homo habilis.

Australopithecus africanus

Australopithecus sediba

Homo habilis

Hominin skulls. Top left: Generic Anoiapithecus. Top centre: ‘Toumai’ Sahelanthropus tchadensis (in part after Zollikofer et al. 2005). Top right: Robust Chimpanzee Pan troglodytes. Bottom left: South Africa Man-ape Australopithecus africanus. Bottom centre: Australopithecus sediba. Bottom right: Handy Man Homo habilis.

features displayed by A. ramidus renders previous models involving any sort of direct leap from quadrupedalism to bipedalism obsolete. Among later hominins, legs became longer still (and, eventually, arms shortened) and some species moved out into more open habitats. Large mammals began to be hunted by some hominins, having first, perhaps, been scavenged. As early hominins adapted to various and wider ranges of habitat, necessary changes in behaviour induced strong selection for appropriate incremental changes in physiology and morphology. At least three major lineages can be identified and as many as six or more hominin species might have existed in and out of Africa at any one time (though not in the same locality). One branch (including the famous ‘Lucy’ Australopithecus [or Praeanthropus] afarensis) culminated in the Paranthropus or ‘nutcracker humans’. This

Three grades of hominid feet. Left: Robust Chimpanzee Pan troglodytes climbing foot with curved digits. Centre: Ground Ape Ardipithecus walk-climb foot retains phylogenetically earlier ‘platform’ structure from a squatting phase of evolution. Right: Modern Human Homo sapiens walking/running foot with re-aligned large toe.

lineage dominated the scene 4–2 mya but was eventually replaced by the Homo lineage that were relative late-comers. It now seems likely that, among a diverse scatter of hominins, the southern-most, more temperate-adapted species, Australopithecus (Praeanthropus) africanus and Australopithecus sediba, gave rise to the Homo lineage. It has been argued that strong seasonality in the hilly or mountainous habitats of A. africanus demanded exceptionally versatile social and strategic responses (Kingdon 2003). Global fluctuations in climate eventually permitted the descendants of these hominins (originally exclusive to South Africa) to spread northwards and eventually to enter Eurasia, where they proliferated still further. Because such studies are hostage to the availability of rare fossils, reconstructing progressive changes in a wide scatter of hominins through space and time, especially those of the Homo lineage, poses one of the most difficult but fascinating challenges in contemporary science. Jonathan Kingdon & Colin P. Groves right:

Reconstruction of face of Ground Ape Ardipithecus.

Reconstruction of the original Nutcracker Man Zinjanthropus (now Australopithecus [Paranthropus] boisei).

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Genus Homo Humans Homo Linnaeus, 1758. Systema Naturae, 10th edn, 1: 20.

Homo sapiens Modern Human Homo floresiensis ‘Hobbit’ Homo heidelbergensis ‘Heidelberg’ Homo habilis ‘Handy Man’ Homo neanderthalensis Homo rudolfensis ‘Rudolf Man’ Neanderthal Homo ergaster ‘Work Man’ Homo erectus Erect Man (might include the un-named ‘Denisova DNA species’) There are scientists who, citing how recently our evolution has taken place and seeking uniform time-criteria for taxonomy, have proposed including chimpanzees Pan spp., even gorillas Gorilla spp., in Homo. This has not found, and remains unlikely to find, general acceptance. The genus Homo, by current definition, embraces a single living species – ourselves. All of us are, in a very basic sense, African mammals because the emergence and tenancy in Africa of our ancestors was probably about twice as long as Modern Human presence anywhere else (200,000–300,000 years in Africa versus 30 published names for proposed species or subspecies of living or extinct Homo. Most are of merely historical interest but some of the fossil forms provide rich and incontrovertible evidence for the reality of human evolution in Africa.

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Homo sapiens

Of the other species of Homo that exist as fossils, the earliest, Homo habilis ‘Handy Man’, is known from about 2.5 mya and Homo erectus ‘Erect Man’ at 2 mya. There is good fossil and molecular evidence to suggest that our own species, Homo sapiens ‘Modern Human’, emerged only ca. 250,000–300,000 years ago. The placement of Homo sapiens within current mammalian systematics is as follows: Class Mammalia   Subclass Eutheria   Order Primates    Suborder Haplorrhini     Parvorder Catarrhini      Superfamily Hominoidea       Family Hominidae        Subfamily Homininae         Tribe Hominini          Genus Homo           Species Homo sapiens Lists of synonyms for H. sapiens are available in Groves (2001, 2005a). Modern Humans have 46 chromosomes, two less than chimpanzees Pan spp. and gorillas Gorilla spp., which have 48. However, this anomaly is due to the human chromosome 2 being an end-to-end fusion of two ape chromosomes, a fact revealed by the banding patterns on human chromosome 2 (Yunis & Prakash 1982).

Description  A uniquely bipedal, large, primate with a peculiar distribution of hairy patches on the head and limb axia, but otherwise a general tendency to greatly reduced hairiness. Surface features, such as hair type, skin/eye/hair colour and nose shape, vary both individually and regionally. Sexual dimorphism is moderate; adult // being, on average, smaller than adult ??. Modern Humans resemble the great apes closely in much of their anatomy and physiology (a fact that has led to the use of chimpanzees as human proxy experimental subjects in medical, pharmaceutical and cosmetic laboratories). The fossil record now offers evidence for many of the steps leading from our common ancestry with chimpanzees and gorillas. It is in the proportions of limbs and head that chimpanzees, gorillas and humans differ most; humans having elongated legs, shortened arms and face, and enlarged cranium. The hands of African great apes also differ substantially from those of humans and have probably become progressively more specialized for weight-bearing and climbing. The functional significance of some human peculiarities is discussed in ‘Adaptations’. Geographic Variation  Modern Humans vary greatly in external appearance and this variation has both individual and regional roots. The majority of Modern Humans have skins that are various shades of light brown, with dark brown eyes and straight, black hair. Two

North-east Africans. Top from left: Maasai adult male and juvenile male; El Molo male youth; Oromo middle-aged female; Samburu elderly female. Bottom from left: Maasai elderly male and middle-aged male; Rendille elderly male; two Maasai adult males.

Lateral, palatal and dorsal views of skull of adult Modern Human Homo sapiens.

Eurasians. Top from left: West European middle-aged male (profile and frontal); German Jewish youth; West European middle-aged female (frontal and profile). Bottom from left: North European elderly male; Central European middleaged male; Western European adult male; Middle Eastern adult female (Kurd); Pakistani adult male.

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Melanesians. Top from left: New Guinea (Gogdala) adult male; New Guinea (Huli) adult male; New Guinea (Highlander) middle-aged male; New Guinea (Telefol) adult female. Bottom from left: Solomon Islander adult female; Vanuatuan middle-aged male; New Guinea (Kewa) adult male; New Guinea (Duna) adult female.

major departures from this primary type involve opposite trends towards ‘super-pigmentation’ or ‘depigmentation’. A gene that plays a major role in depigmentation is the theomine gene SLC24A5, which Lamason et al. (2005) estimated to have arisen a mere 6000– 12,000 years ago. The roots of this trait can be confidently located in the Baltic region of northern Europe and is typified by blonde hair and skin, and blue eyes. The opposite trend, with dark brown or black skin and eyes, spiralling hair and distinctive physiognomic features, is now most widespread in Africa but this genetic package of characteristics might have arrived there in prehistoric times after originating in Melanesia (Haddon 1919, Kingdon 1993, 2003). Eyes are also subject to significant differences in shape, some being the product of subcutaneous deposits of fat that probably serve to protect the eye-balls, insulating them from extremes of cold and shielding them from bright reflectance off snow. Such traits can sometimes be traced to selection for useful traits under extreme conditions, as in the higher reaches of the Andes and Tibet, where the thin air poses problems for pregnant women. Still other manifestations of regional

Australians. Top from left: Queensland middle-aged female; Tasmanian middle-aged female; Queensland youth; Arnhemland female; West Australian elderly female. Bottom from left: Queensland adult male; South Australian elderly male; Central Australian elderly male; Arnhemland adult and middle-aged males.

South-East Asians (Negrito). Top from left: Philippine (Aeta) middle-aged male; Malayan (Batek) young adult female; Malayan (Semang) adult male. Bottom from left: Malayan (Semang) adult male; Malayan (Batek) adult male; Philippine (Aeta) middle-aged female.

above: East Asians. Top from left: Siberian adult female; Yunnan adult female; Nepalese male youth; Vietnamese adult male; Siberian middle-aged female. Bottom from left: Alaskan (Inuit) middle-aged male; Central Asian (Kazahk) adult male; South Chinese middle-aged male; North Chinese middle-aged male; Japanese elderly male. right:

Andamanese. Top from left: Young adult females. Bottom from left: Young adult female; young adult male; adult female.

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Homo sapiens

difference can be traced to founder-effects, as when a very small number of immigrants has colonized an island or spread widely over a continent. Similar Species  Humans are broadly sympatric with all six species of great apes. Resemblances with orang-utans, chimpanzees and gorillas offer many evolutionary insights but the erect posture, hairlessness and large cranium of modern humans prohibit any confusion in identification.

Palaeolithic sequences and artefact types from African archaeological sites (diagram modified after Gowlett 1992).

Distribution  Modern Humans occur in all African biotic zones and inhabit every continent. A primary reason to include humans in a continental mammal inventory is that Homo sapiens evolved, exclusively, over millions of years, within African mammal communities. We can be sure that prehistoric distributions of primates represented complex patterns of ecological partitioning, exclusion, competition, constraints (and, possibly, facilitation) for almost every species of primate. At various stages of their evolution, proto-humans and extinct humans were integral to these patterns of interaction. Few surviving species, either primate or non-primate, have escaped the legacy of human competition/exploitation of commonly used resources. Furthermore, this human onslaught has been strung out, step-by-step, habitat-by-habitat and region-byregion. It is, therefore, interesting to find some African Middle Stone Age industries (dated 250,000–45,000 years BP, and once commonly referred to as ‘Stillbay’) that were mainly confined to upland, temperate and semi-arid zones. Here, tool types were remarkably similar from the Cape to the Horn of Africa, suggesting a welldispersed, mainly savanna-dwelling population that used relatively uniform techniques. Then, about 42,000 years ago, living sites became much more numerous and began to extend into low-lying and humid parts of central and West Africa (Anciaux de Faveaux 1955, Clark 1967, 1982, Isaac 1982). At this time, tool-kits became

more varied and numerous, representing many regional variants. The implications are of expanding, less habitat-specific populations (perhaps even ‘tribes’) devising a variety of new techniques to exploit an expanding range of environments. In spite of 42,000 years being deep in prehistory, that expansion of numbers and range could be seen as one of several starting points for the modern era. It suggests a substantial enlargement of our ancestors’ capacity to exploit resources that were previously not used. Because equatorial lowlands are hotbeds of primate diseases, it is possible that diseaseresistance in a particular human population was a decisive factor in this ecological expansion (Kingdon 1993). This expansion of range also seems to mark a significant leap in an invasive, ‘niche-thieving’ dynamic that has continued to typify human interactions with the rest of nature. The present era undoubtedly marks another, much more comprehensive and sudden, technological and demographic leap. If such archaeological discoveries could be plotted through time, and investigated in terms of staged expansions into once unpopulated regions and into previously unexploited ecosystems, there would likely be important insights to our understanding of the biology of many mammal species. It may eventually be possible to reconstruct long-term patterns of ecological change and extinction induced by human activities. When such reconstructions are attained, it is 79

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predicted that a deeper understanding of mammalian biology in Africa will emerge. The archaeological record provides reminders that the impact of human numbers, and of the ever-expanding technological inventiveness of humans, has deep roots, and that we are witnesses to but one moment in a very protracted human assault on the natural environment – and on all species that live in these environments. Habitat  Human habitats are essentially self-made and the invention of clothing, harnessing of fire, ability to make tools and to construct shelters and transport systems, etc., means that modern humans have come to occupy the entire range of contemporary terrestrial habitats. This ecological annexation has proceeded stepby-step, incrementally. It has long been recognized that when humans lack appropriate technologies, their ecological niches and impacts are narrower, even though prehistoric modern humans were no different in physique or intellect to contemporary people. Thus, the invasion of rainforests, deep swamps, high mountains and polar regions is probably relatively recent, whereas savannas, especially African savannas, represent an archetypal habitat for Homo sapiens. When such insights are referred to actual species it can be appreciated that bovids, such as the Hartebeest Alcelaphus buselaphus, Wildebeest Connochaetes taurinus and Common Eland Tragelaphus oryx, evolved within savanna habitats where humans were already a factor in natural selection. Thus, human activities, such as grass-burning or intensive hunting around waterholes in dry seasons or during arid climatic phases, could have favoured one antelope versus another, and shaped some details of their behaviour and evolution (and may have caused the extinction of especially vulnerable species). By contrast, a forest bovine, such as the Bongo Tragelaphus eurycerus, or a desert antelope, such as the Addax Addax nasomaculatus, evolved in effectively human-free environments. In all instances, there are implications for our understanding of the species’ biology and conservation status today. Our historic and prehistoric interactions with predators also raise numerous questions. Many species of large predator have gone extinct in Africa as elsewhere. We can only guess at some of the reasons for these extinctions but once humans became effective predators in their own right it is certain that they became a significant factor shaping predator communities. From detailed studies of predator guilds in several parts of Africa (e.g. Serengeti N. P. in Tanzania, Kruger N. P. in South Africa, Bale Mountains N. P. in Ethiopia) we know there are highly structured specializations in prey type and killing technique, as well as systematic appropriation of prey. These may be the evolutionary outcomes of ancient interactions or ‘arms races’ between different predators, but the exact spectrum or balance of carnivores in any one place at any one time is the direct product of locality-specific competition. The constraints on early humans, and the two-way dynamics of human interaction with Lions Panthera leo, Leopards Panthera pardus, Cheetahs Acinonyx jubatus,Wild Dogs Lycaon pictus, Spotted Hyaenas Crocuta crocuta, Black-backed Jackals Canis mesomelas and other large, savanna-living, predators, have scarcely begun to be examined in this context. It is even more important to understand the dynamics of our evolutionary interactions with close relatives, especially chimpanzees and gorillas. Assuming ancient periods of physical separation (because our common ancestor could not have speciated without that), there are likely to have been other times when expanding and contracting ranges (probably correlated with climatic changes as well

as technological innovation) brought formerly separate lineages into contact again. Of special interest are those ancient times when the burgeoning lineages of early Hominini and early Pan were a lot more alike than they are today. At such early times we can assume that ancestral chimpanzees and ancestral hominins retained some residual overlap in their ecological preferences. What happened during these early interactions is crucial for understanding the nature of our biological differences. Extrapolating from what we know about ecological partitioning in general, it is likely that direct competition within these early zones of overlap served to define ecological boundaries among the species. Thus, chimpanzees may well have been forced to become more decisively forest-dwellers and more specifically ‘big tree climbers’ as a direct consequence of ancestral exclusions by our own lineage (and, perhaps, other primates) in the distant past. In Africa, understanding the differing susceptibilities of antelopes, carnivores, or the great apes, whether prey, predator, or competitor, needs to be informed by the history or pre-history of their interaction with humans and proto-humans. Abundance  At about 7 billion (US Census Bureau 2007), humans are today, by far, the most abundant primate on earth. Humans are currently in an unprecedented phase of demographic expansion, especially in Africa. The UN estimated projections of future global population range from 7.6 and 9.8 billion for 2050, while projections for 2150 are as high as 30 billion. Increasing densities, unbalanced age distributions and newly urban societies have transformed, or destroyed, traditional economies and modes of behaviour. Nomadic foragers and hunters used to live in small, mobile, family-sized functional groups. Pastoralists also had to be mobile but tended to operate more expansive clan systems with the young men in warrior groups. Settled farming societies varied greatly but generally had enlarged family groups because their labour-intensive crops could support more children and plants needed more hands to be cultivated and harvested (Butzer 1971, Flannery 1973). City living, on the other hand, tends to favour nuclear families operating within large social aggregations that are controlled by clan-like kings, religious figures, or other leaders (Harris 1978). Some of the biological underpinnings of human societies are explored under ‘Social and Reproductive Behaviour’. Rapid increase in numbers and huge expansions in the geographic range of humans has involved the extirpation of many subspecies and several species of large mammals in Africa, notably the Blue Buck Hippotragus leucophaeus in South Africa and the Red Gazelle Gazella rufina in North Africa. A currently fashionable myopia promotes the idea that most human enterprises need not have adverse effects on the survival of mammals, large and small. On the contrary, an exponential increase in human numbers can only lead to further extirpation of species, most particularly those species that occupy small areas in localities with large (and/or lawless) human populations. Current trends suggest that burgeoning human populations will soon cause the extermination of some, or all, of the following species of mammals in their natural habitats: Pennant’s Red Colobus Procolobus pennantii, Preuss’s Red Colobus Procolobus preussi, Tana River Mangabey Cercocebus galeritus, Sclater’s Monkey Cercopithecus (cephus) sclateri, Red-bellied Monkey Cercopithecus erythrogaster, Preuss’s Monkey Allochrocebus preussi, Drill Mandrillus leucophaeus, Rondo Dwarf Galago Galagoides rondoensis, Golden-rumped Sengi Rhynchocyon chrysopygus, Ethiopian Wolf Canis simensis,Wild Ass Equus africanus, Grevy’s Zebra Equus grevyi,

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Aders’s Duiker Cephalophus adersi, Hirola Antelope Beatragus hunteri, Dama Gazelle Nanger dama, Slender-horned Gazelle Gazella leptoceros, Scimitar-horned Oryx Oryx dammah and Addax Addax nasomaculatus, to name but a few. The activities of humans are, of course, also having a severe negative impact on the world’s birds, amphibians, reptiles, fishes, plants, and species in other taxonomic groups. Adaptations  Primarily diurnal and terrestrial. Some of the adaptations that most distinguish Modern Humans are best appreciated by comparing characteristics (some obvious, others more cryptic) with equivalent features of modern apes and fossil hominins. Homo sapiens is the last survivor of a great diversity of extinct hominins that are becoming ever more richly documented by the fossil record. These fossils demonstrate the tangible reality of human evolution and often offer hints as to how some of our uniquely human adaptations were acquired. The earliest of these fossils, ‘Toumai’ Sahelanthropus tchadensis, is a well-preserved 6–7 million-year-old hominid skull. This skull combines characteristics of Modern Humans, chimpanzees and gorillas, confirming Darwin’s 1871 prediction that Africa was the most likely home of the Homo sapiens lineage, and that chimpanzees and gorillas are our closest living relatives. The somewhat younger ‘Millennium Human Ancestor’, Orrorin tugenensis (6 mya), has a much more fragmentary skull, but is probably closer to the human line of descent. The next oldest hominin fossils belong to the ‘Ground Apes’, Ardipithecus kadabba and Ardipithecus ramidus, of Ethiopia. The earliest specimens of kadabba are ca. 5.8 mya, the youngest specimens of ramidus are ca. 4.4 mya. These eastern apes lived in riverine forests and woodlands in a relatively dry region of eastern Africa. Extrapolating from equivalent contemporary East African riverine forests and woodlands, the ground was likely to have been a richer source of forage than the treetops. As is summarized below, this detail hints at the driving force that initiated hominin divergence and the emergence of Modern Humans. Since genetic isolation is an essential part of speciation, eastern provenances for these and subsequent fossil hominins suggest that an arid corridor allowed the earliest hominins to diverge in isolation from the much larger populations of apes occupying central and West Africa. In apparent concert with our upright stance, humans have developed strong, flexible ‘waists’ that separate and balance a slabshaped thorax above a basin-like pelvis; chimpanzee and gorilla rib cages are splayed and conical, their lower margins bound closely to broad pelvic plates in a single, oblique and top-heavy body mass. These anatomical differences are now associated with bipedalism in humans and quadrupedalism in chimpanzees and gorillas. However, the initial divergence in body proportions, especially the slimming down of shoulders and chest, was likely to have begun with the adoption, by our earliest ground ape ancestors, of a ‘squat-foraging’ mode. This was a posture in which the upper body became less topheavy and the vertebral column became more upright. The detailed adaptations of the Ardipithecus ground apes remains to be elucidated but it is clear that any ‘squat-foraging’ primate gleaning for small food items, both plant and animal, on the forest floor, must have employed increasingly dextrous fingers (Kingdon 2003). The actual size of our hands is, proportionally, somewhat smaller than in chimpanzees and gorillas, but we should not equate

‘Penfield homunculus’ (adapted from brain maps in Penfield & Rasmussen 1950 and from a figure in Dawkins 2004).

anatomical size with functional significance. This has been illustrated in an original and interesting way. In 1950, Penfield & Rasmussen published a paper on the human cerebral cortex that offered a graphic demonstration of how important hands are for H. sapiens. These authors mapped two aspects of brain function: one represented the ratios of the brain devoted to controlling muscles, the other mapped equivalent ratios for the sense of touch. In each instance, the hands occupied hugely disproportionate parts of the brain. The ‘homunculus’ that emerged from this exercise was grotesquely ‘hand-heavy’, as were the parts of the face given over to vocalization: tongue, lips and jaws (see illustration above). A significant conclusion emerging from the evidence that hands were of paramount importance in human evolution is that skills in manipulation help explain the emergence of bipedalism. Once deft, food-gathering hands became the prime adaptive specialization of ground apes, and once the vertebral column began to be rebalanced, it was inevitable that bipedalism would develop. To gather and handle a wide variety of mainly small food items is not entirely without precedent (some African and South American monkeys are highly manipulative).What was new was the combination of direct finger-gathering with indirect tool-use (we can infer the latter from numerous instances of its existence, in rudimentary form, in chimpanzees). More important, this specialization in tool-assisted foraging represented an entirely novel way of interacting with the external world. Bipedality allowed the descendants of ground apes to become more mobile, but this was far from being an instant conversion. There is telling evidence from fossils to suggest that two-legged walking and running took a long time to improve, let alone perfect. Long, forager’s arms had to shorten while apish squatter’s legs took several million years to become long, powerfully muscled legs.Throughout this period, trees 81

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and cliffs are likely to have continued to be important as sources of refuge and shelter, especially at night. T. Butynski (pers. comm.) points out that the distributions of dry country monkeys (i.e. Patas Monkey Erythrocebus patas, savanna monkeys Chlorocebus spp., baboons Papio spp.), as well as some populations of Robust Chimpanzee Pan troglodytes, are dependent on surface water and on safe sleeping sites. Noting that (1) habitats away from drainage lines tend to produce much the same foods over large areas, and (2) that no monkey or ape exploits this vast supply of food, he envisages significant opportunity for, and selective pressures on, early hominins to exploit these foods, including meat. The expansion of the geographic range of early hominins into this enormous ‘empty niche’ was likely dependent on (1) the ability to carry resources (e.g. food, water, building poles and tools) that bipedalism allows for, (2) the ability to make water containers, build shelters, hunt large prey and avoid and/or defend against predators that tool-use and complex vocal communication enable, and (3) the ability to use fire for cooking, warmth, hunting and defence. In short, development of bipedalism, tool-use, complex language and control of fire among early hominins allowed for the much greater exploitation of the natural resources (especially food) of the vast, waterless, African savannas and bushlands. The swollen braincase of Modern Humans is one of the last obvious innovations to emerge. We are fortunate to have a rich fossil record demonstrating progressive enlargement of human brains, most of which took place over the last 2 million years. People are often struck by how ‘human’ young primates are. This is to invert the situation: humans resemble big-headed baby primates because selection has to operate upon pre-existent traits and processes. So humans are ‘neotenous’ or ‘paedomorphic’ primates in their bulging foreheads, reduced teeth, chewing muscles and, above all, in many aspects of their behaviour. Neoteny is essentially a consistent alteration in the timing of various developmental processes. For example, if brains are to enlarge, the bony plates that surround and protect them need to remain loose long enough to accommodate this enlargement. The mechanism allowing this to happen is retention and extension of the juvenile phase of development and suppression of some adult features, such as massive ? brow-ridges. Neoteny and the extension of childhood have a central role to play in the development of human social systems. These are further explored under ‘Social and Reproductive Behaviour’. Other adaptive peculiarities of H. sapiens do not fossilize, among them important physiological properties of the skin and hair. Most notable of these is the superabundance of eccrine glands in H. sapiens, a characteristic that is as diagnostic of Modern Humans as speech or bipedalism (Sokolov 1982). Eccrine glands are found in many mammal species with a soft skin interface between themselves and the ground or branches on which they walk or climb.The fine watery eccrine secretions that exude from the palms of primates, carnivores etc., are seldom found anywhere else but on finger-pads and paws. Their primary role seems to be to condition, protect and cleanse these sensitive, exposed, wound- and infection-prone surfaces from contamination or harm. Human eccrine secretions even possess antibiotic properties (Randerson 2001). Another important property is to increase the sensitivity and micro-traction of fingers and palms. This is a significant virtue for contemporary humans (a sensitivity greatly enhanced by dense mosaics of Meissner’s corpuscles

embedded in the skin surfaces of primate fingers). Human hands, especially the fingertips, are so sensitive that skills such as reading Braille, sewing, servicing watches or computers, or playing small, complex musical instruments, can quickly be learned. (Incidentally, most of these talents would have had prehistoric equivalents in terms of finely tuned manual skill.) Finally, evaporation of the water in eccrine secretions also produces a pronounced cooling effect. Today, this last property of eccrine secretions seems the most obvious advantage. ‘Sweating’and cooling must have been a major evolutionary benefit when our ancestors moved into more exposed habitats and undertook high-exertion activities such as walking long distances while carrying food and water. However, it was probably the cleansing functions of eccrine glands that first favoured their initial spread and multiplication in apes and their near total replacement of other glands in Modern Humans. In terms of hair and skin hygiene, humans have effectively abandoned the relatively dry, oil-based system employed by many other mammals. Instead they have enlisted the water-greedy eccrine glands to cleanse and cool a relatively naked skin. A possible connection between nakedness and eccrine glands is discussed further under ‘Social and Reproductive Behaviour’. The adaptive property, which is most frequently thought to distinguish humans from other animals, is the development of a mind capable of articulating and sharing knowledge and feelings with others. In 1837, Charles Darwin made a jotting in his notebook: ‘man is a species like any other. The mind is a function of body. He who understands baboons would do more towards metaphysics than Locke’ (Browne 1995). Ever since, scientists have been exploring the many ways in which mind is a function of body – and baboons, like other African primates, continue to offer us insights into one of the most difficult of all evolutionary puzzles. Foraging and Food  Omnivorous. In their wild forms, most foods eaten by humans were or are shared with other species: fruits with fruit-bats, palm dates with palm civets, roots with root-rats, honey with Honey Badgers, and meat with Lions, Leopards and Spotted Hyaenas. In many instances, plants that are now cultivated and eaten by humans co-evolved with non-human consumer species that served the plant as disperser or pollinator. Where such animals have been entirely displaced by humans the latter could, in an evolutionary sense, be said to be ‘thieves’, but that could probably be said of many other instances of evolutionary displacement. Human perspectives invert this, so wild animals that attempt to share resources with us are dubbed ‘pests’. Humans have developed a battery of devices that effectively withhold potential foods from other animals.We have typically mammalian instincts about attacking or excluding competition. Conflicts between H. sapiens and other mammals pose fundamental problems for the long-term survival of many mammal species. As the texts of these volumes exemplify, food resources are often partitioned to some degree among the animals that consume them, and the consumers have prescribed tastes and genetically determined food-getting techniques that are unique to the species. Humans, instead, have emancipated themselves from a limited range of species-specific foods and have, with the help of various toolassisted techniques, devised numerous ways of protecting, obtaining, preserving, processing and altering otherwise unavailable or inedible foods. These characteristics are part of our evolved repertoire. Thus,

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skills in cultivating, breeding, processing, and protecting edible plants and animals are not new, nor is the capacity to consume a wide range of species (Ucko & Dimbleby 1969). So, is this merely a vastly enlarged expansion in tool-assisted omnivory? If it is argued that the consumption of a continuously expanding harvest has long been characteristic of our evolutionary career, can we project its momentum on into the future? Will we reach a point where there will be no plants or animals that are not, in some sense, consumable? Is such a state desirable? Perhaps unease with that question lurks in ideological arguments as to how ‘naturally vegetarian’ or ‘naturally carnivorous’ humans are? In many languages the word for meat is also used for animal (i.e. ‘nyama’ in Kiswahili) and ‘going the way of all flesh’ (dying) also includes humans in the same animal commodity. Lee (1968) documented contemporary, subsistence-based, human hunter-gatherer societies eating far more, and larger, vertebrate prey than any other primate. In an effort to arrive at some (implicitly retrospective) averages, Lee (1968) sampled 58 such societies from many latitudes and in many parts of the world. With one exception, he found that all these societies derived at least 20% of their diet from hunting mammals (mean ca. 35%). He, therefore, postulated that, on average, prehistoric humans derived 30–40% of their diet from the meat of mammals. In spite of many prehistoric societies having scant, or only seasonal, access to fish, Lee added a mean of 26% of fish into postulated prehistoric diets. He concluded that mammals and fish comprised 61% of the diet of prehistoric humans. Given that other vertebrates and invertebrates were not considered, Lee’s estimate of 61% of animal matter was a conservative value. Butynski (1982c), reviewing vertebrate predation by contem­ porary primates, including humans, showed that while animal matter is a major component of the diets of many species of primates (sometimes 30–70% of the diet), almost all of this derives from invertebrates. Animal matter comprises only 1–4% of the diet of baboons and chimpanzees (far less than this in gorillas). The hunting of vertebrates by non-human primates is an uncommon, albeit widespread, behaviour. Butynski (1982c) points out that chimpanzees and humans are the only primates known to occasionally kill their prey by flailing it against a hard surface and to carry meat for distances of >1 km. No primate other than humans is known to prey upon animals larger than itself. Chimpanzees and baboons seldom kill prey weighing more than 6 kg, and 10 kg appears to be close to the upper limit. In contrast, humans often kill prey many times their weight. The frequent hunting and utilization of large mammals by humans appears to have been enabled by the addition of complex vocal communication, bipedalism, fire-use and weapon-use to a basic primate hunting pattern. One probable outcome of this ‘hominin hunting pattern’ was the hunting of vertebrates (especially mammals) as a major activity and ‘way of life’. This appears to have resulted in a dramatic (perhaps 30–35-fold) increase in the consumption of meat from vertebrates, an increase perhaps already evident >2.5 mya. The hominin hunting pattern comprises adaptations not shared with any extant nonhuman primate nor, presumably, with any pre-hominid ancestor. The hominin hunting pattern allowed for the exploitation of a new, very different, and vast food-niche (see above) in which there was little or no competition with other primates – although there was probably important competition with several large African predators (Butynski 1982c).

There is no consensus concerning the diet of early hominins. As such, anthropologists argue passionately about just how frugivorous, omnivorous or carnivorous prehistoric hominins were, notably for more recent periods, when diets reflected the local availability of plant and animal foods. The issues are certainly relevant to understanding hominin divergence from our common ancestor with the other apes but are still far from being resolved. Knowing that hands were used for food-gathering and that early hominin hands differed from those of other apes, we can safely infer that diet was involved. The most likely difference was that the ground apes were omnivorous and foraged for small items on the ground whereas ape ancestors were predominantly arboreal eaters of relatively large fruits. It may be too much to hope that an appreciation for the initial divergence between the human and ape lineages being founded on small dietary differences could translate into greater sympathy for African apes and for their present plight. Even so, insisting that apes be recognized as fellow primates, our closest living relatives, has to be preferable to treating them as an exotic food, as they are in the restaurants of several West African and European cities (Peterson & Ammann 2003, Rose et al. 2003). Human appetites, not just gastronomic ones, threaten a great many of the mammals described in this work. If some recognition emerges that Modern Humans are an integral part of Africa’s mammalian fauna, and that chimpanzees and gorillas are our cousins, then consumption of chimpanzees and gorillas may eventually come to be seen as closer to a form of genocidal cannibalism than to gourmet dining. The ability of contemporary societies to ship ape and other carcasses to far away markets is an essentially modern and new challenge but it is part of a much larger trend. As all types of human impact on the environment grow, agriculture (for the most part primitive, but increasingly machine- and chemical-dependent) demands more and more land and excludes more and more species. In rich countries, trade, research and transport have spread access and knowledge of foods to an ever-expanding market. In poor countries, population growth and hunger drives continuous agricultural expansion and unsustainable exploitation of many local foods that were previously ignored or only eaten in extremis. As wild foods decline, the ultimate loss is of local ecological integrity and diversity, and an increasing and permanent impoverishment of the natural world. The great Australian writer and scientist, Tim Flannery, has dubbed us the ‘Future Eaters’ (Flannery 1994). There are three major forces, which, if they continue to follow present trajectories, will extirpate many species of the larger mammals in Africa. One is the increasing numbers of humans with the need and, increasingly, the means, to inhabit virtually the entire land surface of Africa. Concurrently, the single most direct force exterminating large mammals is the widespread and unregulated commercial bushmeat trade. The third major force is the use of everincreasing areas of land for commercial crops such as beef, sugar, oil-palm, cereals, coffee, tea, fruits and vegetables, timber, even flowers, and concomitant appropriations of water sources. Were we to articulate the interests of other mammals as though they were comparable with our own interests, or were we to entitle natural ecosystems the ‘right’ to survive, the progressive turn-over of all lands to the purposes and interests of a single species could only be called theft. The ultimate effect of additive theft by one species is denial of the ‘right’ of other species and natural communities to 83

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exist. Of course, few humans can acknowledge such an extreme characterization of their actions but, in ecological terms, humans are actively stealing the niches of other animals. As such, we should at least consider what can be done to mitigate our destructive ecological role and evolutionary status as ‘niche-thieves’. At the international level, land-use policies are seldom ecologically based. Both national and international bodies concerned with feeding human populations continue to value the soils and climates of remaining non-agricultural land only in terms of their potential for crops or livestock. The ambassador of a major Western nation, on visiting a small African national park of almost unprecedented ecological diversity and of a natural biological richness that dwarfed that of his own country, enthused publicly about the area’s potential for conversion to vineyards. (Although his advocacy of viticulture was not taken up, the size of the park was subsequently drastically diminished and the excised areas were, indeed, given over to agriculture, much of it for the production of alcohol.) For the ambassador nothing could conceivably transcend the value of wine. His mental imposition of a Western wish-landscape over a real, but unfamiliar, African one illustrated the imprinting power of culture. He also exemplified the almost total, worldwide, absence of ecological insight or training in contemporary public leadership. Political leadership is still oblivious to some of the most policyrelevant findings of modern science. Studies of Africa’s indigenous flora and fauna have demonstrated that no agronomic or pastoral system devised by humans has ever, or will ever, begin to compare with natural ecosystems for inherent productive efficiency and for the progressive diversification of ecological niches. Accelerating degradation of African landscapes by so-called ‘modern’ agriculture, and drastic over-grazing by livestock, must eventually persuade thoughtful people to seek knowledge of the natural structure of African ecosystems and induce respect for the rich landscapes that preceded today’s spreading ecological deserts. All aspects of human welfare and all domesticated plants ultimately depend upon our need to understand their evolutionary history. The realization is growing that all plants and animals, including ourselves and our domesticates, have spent significant periods of evolutionary time subject to precise ecological parameters and confinement to quite precise geographic regions.There are innumerable potentialities for human exploitation in the adaptations of highly specialized biota. There are also many foods and condiments that were once part of human resource use in Africa that are being displaced by imported plants (Maguire 1980, Peters et al. 1992, O’Brien & Peters 1998). The workings of the evolutionary process tie our time and place to past and future, and tie our survival to all the animals and plants on which we depend, fruit, oil-palm, rice, wheat, maize, livestock, fish and many more, every one of which owes its existence to the same over-arching process. Many out-moded and, originally, nonAfrican agricultural and pastoral practices will eventually have to be scaled down or even abandoned. In the meantime, maintaining viable mammal communities is integral to the long-term objective of ensuring that Africa develops locally relevant, not primitive or exotic, systems of resource use. Social and Reproductive Behaviour  Social. In the past, human societies differed from those of other primates in the prolonged dependence and extreme vulnerability of their young, and in the

Reconstruction of the ‘Idaltu Human’, one of the earliest and most complete fossil skulls of a Modern Human Homo sapiens.

high level of dependence of mothers on a social system that enhanced security for all. Early human societies would also have differed from those of most apes in that both sexes and all ages were more similar in physique. If human ?? show less difference from human // (and all ages and sexes are neotenous compared to, say, ? gorillas or ? chimpanzees), what significance does this have for society? For a start, as a result of exceptionally helpless babies, every member of a human social group was more vulnerable than its ape equivalent; even adult ??, always a minority, shared an interest in finding security within a group of relatively helpless // and children. If all classes were in some sense juvenilized, a group-wide, shared, sense of vulnerability would have selected for behaviour that put the whole group at an advantage. Many animal societies find security in numbers and coordinated activities, but human group activities have more than a simple defensive role. At an early stage, ancestral human groups probably modified originally defensive behaviour into a more deliberate, systematic and proactive engagement with any aspect of the environment that might provide food or other resources. Thus, human societies became oriented to the systematic ‘removal of obstacles’ (including overcoming the evolved defences of plants and animals) in order to gain group-access to resources. The development of scrapers, cutters, crushers and diggers by early humans are all evidence for skills that serve this central feature of the human ecological niche (Renfrew 1973, Gowlett 1992; see p. 79). One manifestation of neoteny in recent human societies is the extension of childhood psychology and assumptions into adulthood. Perhaps the most fundamental social purpose served by the dependence of infants on parents is social subordination. Juveniles generally follow parental example and practice, and societies of all sorts benefit from any traits that subordinate individual behaviour to the immediate needs of the group. In small family-like groups, subordination to biological parents may last as long as the parent lives. Ancestor cults in many societies bear witness to the fact that even after the death of a parent their memory is a source of psychological authority that has been integrated into specific social structures. In larger groups, that subordination tends only to continue if the offspring benefits from the status of its parent, parents or long-dead ancestor. This does not mean that psychological dependence on protective adult authority disappears.Within an enlarged group, any leader can assume a pseudoparental role and it is in the varied ways in which ‘pseudo-parents’

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Ritualized intimidation displays. Left: Adult male gorilla Gorilla (accompanied by a bout of chest-beating). Centre: Robust Chimpanzee Pan troglodytes (short noisy charge, sometimes waving branch). Right: Adult male Modern Human Homo sapiens (‘Haka’).

manipulate infantile psychological dependency that neoteny finds social expression (Chagnon 1975). The ways in which leaders bolster their power by assuming parent-like authority varies greatly but some general patterns are shared across all cultures. At the ontogenetic and psychological level, a sense of continued defence by parents comforts individuals and helps smooth the transition from safe juvenile to much more vulnerable young adult. At broader historical and social levels, the transfer of each child’s individual dependence upon one or two mortal, ageing parents, to generic, socially sanctioned, parent-like leaders, was a relatively small step among groups with small family-like structures. In larger, more highly organized societies, this fundamental carry-over of childhood dependence provided opportunities for the emergence of chiefs or monarchs (Bloch 1966). Once such powers were consolidated, and social structures became multi-generational, veneration for a symbolic parent lost its association with single individuals. Typically, monarchs, intent on defending or extending their own and their descendants’ power, have tended to install agents charged with disseminating acceptance of their leadership by whatever means (Carneiro 1970). The most effective way of achieving this objective was to stress the parental properties of the monarch or, if the monarch was old or dead, to deify their memory. In this way, symbolic parenthood became ‘eternal’ and metaphysical. Most societies devise elaborate coming-of-age rituals that are designed to appropriate the allegiances and energies of their youth. The transition into adulthood is emphasized, but the neotenous psychology of dependency on the groups’ ‘pseudo-parents’ continues and is, if anything, intensified. Allied with coercive force of arms, a dynasty’s warriors, ‘guards’ and agents could impose veneration for their own pseudo-parent over a much wider area. With the development of media (initially books), the power of a local dynasty could be augmented and spread exponentially. Furthermore, it served the interests of dynastic agents

to extend the veneration of a pseudo-parent, both to themselves and to the books that had become the instrument of their success and power: thus even books, obviously human artefacts, became ‘sacred’ in some ‘Cultures of the Book’! Among contemporary societies, the North Korean dynasty and its apparatus is an instructive cartoon of this process. Elsewhere, one-time agents of dynastic power and privilege long ago became priesthoods of various denominations. All depend on some degree of entrenched veneration for a symbolic parent, and their priesthoods provide obvious opportunities for ambitious leaders, who, wittingly or unwittingly, exploit a neotenous mammalian trait for their own social ends. There are few social institutions that are untouched by this dynamic. Physiological mechanisms mediate all animal life, and biochemical agents trigger or suppress most of the behaviours that dominate social relations among mammals. In terms of social structures, the primary function of aggression is to optimize the spacing of individuals or groups. As such, aggression is centrifugal in nature (Marler 1965, Freid et al. 1968). Aggression is controlled by hormones, particularly testosterone among ??, which drive individuals to confront competing or intruding conspecifics (usually other ??). Centripetal tendencies, instead, are mediated by hormones that induce conciliatory, even submissive behaviour. In their relationship to social behaviour in humans, hormones have not been significantly modified – in spite of their social utility being no longer obvious. Specific and local manifestations of these chemically driven behaviours have acquired abstract, culture-specific names, such as ‘hate’, ‘anger’, ‘obsequiousness’, ‘capitulation’ and, at the broader, social level, find expression in phrases such as ‘the enemy’, ‘war-mongering’, or ‘religious intolerance’. The most reductionist explanation for much animal behaviour, including human behaviour, is that it is ‘territorial’, but territorialism has many expressions. Humans, like other mammals, need access 85

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to adequate water and food, and space secure and ample enough for reproduction, play, sleep, waste disposal, etc. Like any other mammal, humans require space – territory – and they, like any other mammal, will fight for it, at national, tribal, family or individual levels, against any entity that would deny them. A single mammalian species now regards Africa as its ‘own’ territory and has plans to use and ‘develop’ every hectare of Africa’s surface for its own purposes. Thus all large mammals in Africa (and most small ones too), as well as the entire ecosystems on which they depend, exist on borrowed time. They exist on borrowed time because they are powerless to defend their lives and livelihoods against all these human needs. They are helpless to defend their space from a species that is now equipped to take away their entire livelihood, even its physical substrate, shipping it away on flatbed logging trucks. The fact is, that over the greater part of the continent, wild mammals and wild places are not just memories, they are forgotten, and with that forgetfulness, 99.9% of human history has disappeared beyond recall. Humans emerged as a singular component of the natural communities that are now being destroyed. At the present time, our knowledge of that immensely long and influential phase of our history and prehistory is minuscule because current political, social and intellectual cultures put no value on such knowledge. Most humans, today, are much more ignorant of nature than their precursors were. In the future, ‘neoknowledge’ of ecological processes will have to become an important strand of scientific education. Such scientifically informed education systems will also need to reappraise fundamental assumptions about culture, race, history and identity. It is in understanding the ecological underpinnings of human societies that we can begin to explain many expressions of variation among human cultures, societies and religions. In every instance there had to be a resource base to support whatever permutations of human society evolved. In every instance, food, technology and demography have all been linked and in a constant state of flux and change (Renfrew 1974). In every part of the world that Modern Humans inhabit, external ecological constraints, as well as internal social ones, have shaped cultural evolution. In adapting to naturally complex ecosystems and to increasingly complex social environments, humans devised ever-greater complexity (Freid 1967, Sahlins 1972). Thus, as human numbers increased and as humans spread ever more widely, the organic evolution of biodiversity and biocomplexity has been paralleled, or mimicked, by the cultural evolution of increasing complexity in human societies. In the context of this work, it is useful to remember that other mammals have had a huge historical influence on African peoples. For millions of years before any animal or plant was domesticated, mammals were a primary food resource for hunter-gatherer populations. Indeed, it appears that a major difference between humans and all other primates is the amount of meat in the diet, especially mammals, and the hunting patterns by which they acquired these prey (Lee 1968, Butynski 1982c; see ‘Foraging and Food’). Modern Humans have spent, by far, the greatest part of their existence as hunter-gatherers; a time in which human knowledge of plants and animals was much greater than it is for the majority of contemporary humans. When cattle were first domesticated, some 10,000 years ago, peoples’ relationship with the land, particularly grassland, changed (Zeuner 1963). New pastoral societies with new land-management techniques, such as firing the savannas, emerged in Africa and their demographic fortunes changed radically because domestic stock

can generally support a higher density of people than hunting (Epstein1971). In southern Africa, some Khoi-San peoples retained a foraging economy while others adopted pastoralism. The subsequent fortunes of the foraging San and the pastoral Khoi (near annihilation for the former, semi-integration into modern economies for the latter) are reminders of how vulnerable foragers become when non-foragers want the land they inhabit. The Khoi’s adoption of an economy that

People in the Sudd, S Sudan. Impressions from a sketch-book.

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was perceived as intrinsically ‘inferior’ by the San ensured the Khoi’s survival and an increase in their numbers while the San succumbed to more powerful economies. Within our lifetime, external forces have systematically dismantled the last vestiges of a way of life that sustained our ancestors for hundreds of thousands of years (Lee 1972). As a San hunter once put it, ‘the string has been broken’. Mammals of all sorts had hundreds of thousands of years to accommodate to sustained hunting by humans and this may help to explain why so many species have managed to survive in Africa. Elsewhere, notably in Australia and the Americas, many so-called ‘naïve’ mammal species became extinct soon after humans invaded their realms (Flannery 1994, 2001). For the indigenous African herbivores, the arrival of exotic livestock brought new elements of competition. For the larger carnivores, pastoral humans represented a shield denying them access to a source of meat that has continued to expand at the expense of their original prey base. If carnivores have lost out to pastoralism, herbivores have lost even more to agriculture as their own attempts to consume cultivars have turned them into ‘pests’. Even more significant, the expansion of agricultural peoples has progressively eaten into all sorts of natural ecosystems, in many instances obliterating the natural vegetation and faunas of entire regions. Both the numbers of humans and the complexity of their societies have continued to enlarge. Recently created ‘sovereign states’ are already being drawn into a web of global institutions that are in the process of transforming the scale of basic human enterprises. Among these enterprises is the ancient practice of studying and enumerating resources. Within the bounds of their territories, foragers knew the whereabouts, habits, sometimes the numbers, of the animals and plants on which they depended (Roth 1897). Pastoralists kept a tally of all their animals and knew intimately their physical needs. Farmers monitored and recorded many details of their crops and livestock. Today, international bodies, such as United Nations Food and Agriculture Organization (FAO), have globalized these practices. The editors and authors of this work, together with organizations such as The Wildlife Conservation Society (WCS), IUCN, WWF, Fauna and Flora International (FFI) and the Zoological Society of London (ZSL), are engaged in the vast and endlessly incremental task of studying and conserving the mammalian communities of the world, communities of which H. sapiens is an organic and integral part. This volume is a contemporary expression of human concern and interest in the mammals of Africa. Many of these mammals helped sustain our ancestors: hopefully they will continue to sustain our descendants. Reproduction and Population Structure  Human gestation lasts about nine months. It is theoretically possible for human numbers to double in 200) cm HB (both sexes): est. (73–83) cm T (both sexes): 0 cm HF (both sexes): est. 22 (15–33) cm E (both sexes): est. 63 (22–55) mm WT (??): 80 (35–>100) kg (max. 419 kg) WT (//): 66 (30–>100) kg (max. 730 kg) Marked regional and temporal variation, from small, light-weight Twa and San to tall Nuer and Dinka people. Upper weights distorted by dietary habits and hormonal condition. Maximum weights cited are from exceptionally obese, effectively immobile individuals. Figures given here averaged from diverse sources. For detailed figures see Ruff (2002). Key References  Darwin 1859; Jones et al. 1992; Kingdon 1993, 2003; Stringer & Andrews 2005. Jonathan Kingdon 89

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Superfamily Cercopithecoidea

Superfamily Cercopithecoidea –

cercopithecoids: Old World Monkeys Cercopithecoidea Gray, 1821. London Medical Repository 15: 297.

Colobinae. Colobus monkeys (red colobus Procolobus).

Myology of Olive Baboon Papio anubis sub-adult male.

The superfamily Cercopithecoidea includes a single living family, Cercopithecidae, which embraces the subfamilies Colobinae (‘leaf monkeys’) and Cercopithecinae (‘cheek-pouched monkeys’). Cercopithecoidea also includes at least one extinct family, Victoriapithecidae. While the split between cercopithecoids and hominoids (apes) poses questions, the split clearly took place within Africa. There are two sources of information for dating the divergence between the cercopithecoid and hominoid lineages. The first, inferred from fossils, produces an estimate of 23.3 mya (late Oligocene) (Walker & Shipman 2005). The second method, using molecular clocks, gives a substantially earlier (late Eocene–early Oligocene) estimate of 30.5 (36.4–26.9) mya (Steiper & Young 2006) and 31.6 mya (Perelman et al. 2011), although Roos et al. (2011) provide an estimate of 26.5– 21.9 mya, which is similar to the estimate based on fossils. It may be significant that the end of the Eocene (33.9 mya) saw a marked change in climate, and that much of the Oligocene was drier and cooler, with forest retreating to the equatorial region (see Chapter 4 in Volume I). Among the Cercopithecoidea there are indications that their common ancestor was less than wholly arboreal, and that their emergence was probably linked to substantial and extensive aridity. In both fossil and living cercopithecoids, the primary indications of a less arboreal ancestral phase are an elongation of the back combined with more fore–aft movement in the limbs. Both of these alterations are correlated with fast movement on the ground. A terrestrial ancestry is unambiguous both for Cercopithecinae (many of which are still strongly terrestrial) and for Colobinae (in spite of being almost entirely arboreal today). Apart from a relatively rich fossil record, which confirms their early terrestrial bias, colobines share many

Cercopithecinae. Cheek-pouched monkeys (baboon Papio).

anatomical features with cercopithecines (quadrupedal adaptations of the postcranial skeleton and, in particular, the striking bilophodonty of the molar teeth). In spite of the great dietary specialization of most contemporary species of Colobinae, a few extant species retain enough ecological flexibility to betray their common origins with Cercopithecinae (particularly evident in the semi-terrestrial Semnopithecus spp. langurs of South Asia). As for an intra-African separation between proto-cercopithecoids and proto-hominoids, the latter were the first to leave Africa and this has phylogenetic as well as biogeographic implications. Thus, at the time of their emigration during the early Miocene (ca. 20 mya), Hominoidea seem to have had a more northerly and equatorial range in Africa while the earliest Cercopithecoidea were, putatively, differentiating in the drier, more temperate south-east (which, at that time, was farther south and more extensive than today). The features that colobids and cercopithecids have in common are dietary: not only the bilophodont cheekteeth, but also, apparently, an ability to detoxify plant secondary compounds in the gut. This is an ability that hominoids lack and which gave the Old World monkeys a marked ecological advantage.

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Anatomical reflections of ‘branchrunning’ and brachiating. In quadrupedal branch-running, the monkey long serratus muscle and scapula are appoximately vertical (a, d and f). In brachiating, the ape serratus muscle and scapula wrap around the trunk (b, c and e).

a

b

e

c

d

f

In addition, there are cranial and dental features indicative of a dietary shift in which a frugivorous diet had to accommodate to more seeds/nuts. This would have been consistent with greater seasonality in the south. Cercopithecoid bilophodonty has been analysed in terms not only of increasing the surface for grinding harder foods but also the construction of reinforced, wedge-like cusps that could crack and open nut shells and break-up hard seeds (Kay 1975, Maier 1977, Benefit & Pickford 1986). The entire skull had to withstand occlusal forces and provide the anchorage for more powerful mandibular muscles (Benefit 1999). This led to loss of the maxillary sinus and more heavily reinforced buttressing of the

mandibles. Thus, all Cercopithecoidea share locomotory, digestive, dental and cranial specializations. It is possible that these traits evolved in response to a diminished choice of foods, especially fruit, in south-east Africa. These traits may have begun to evolve before colobines and cercopithecines diverged, and before any movement out of their south-eastern enclave. However, the first cercopithecoid lineage to move back into the equatorial belt would have had to face competition from their abundant and diverse tropical precursors, the apes. This competitive challenge may have given the proto-colobines a selective advantage, which led to further accentuation of the dietary trait. Just such a break-out of south-eastern isolation could 91

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have generated the phylogenetic split within the Cercopithecoidea and initiated a distinctive colobine lineage. Meanwhile, the parent population, still isolated in the south-east, would have been free of competition from apes but subject to its own selective forces (mostly in relation to predation and socially driven pressures in habitats that were harsher and more seasonal). Such a staged history would be consistent with colobines getting out of Africa later than the apes, yet several million years earlier than the cercopithecines. Thus, south-eastern origins for the Cercopithecoidea would not only account for the primary split

in a common anthropoid ancestor, it also helps explain why apes were the first to leave Africa and why colobine ancestors were next (because they were the first to move north-east). Eventually, colobines and cercopithecines both had Eurasian diasporas, which then radiated extensively, especially in tropical South-east Asia. More detailed accounts of the features that distinguish colobines from cercopithecines are given in their respective profiles and in the species profiles. Jonathan Kingdon & Colin P. Groves

Family Cercopithecidae cercopithecids: Old World Monkeys Cercopithecidae Gray, 1821. London Medical Repository 15: 297.

Colobinae (2 genera with 2 subgenera, or 3 genera; about 12 species) Cercopithecinae (13 genera, 56 species)

Colobus Monkeys (Colobine Monkeys)

p. 93

Cheek-pouched Monkeys (Cercopithecine Monkeys)

p. 155

Until recently, cercopithecine monkeys and colobine monkeys were generally distinguished at the familial level (i.e. Cercopithecidae and Colobidae). Thus, most references before 2000 use Cercopithecidae in this sense.With the rise of molecular phylogenetics and a gradually improving fossil record, the objective dating of evolutionary divergences at various higher taxonomic levels has become, for the first time, possible. This offers taxonomists a temporal criterion to determine the taxonomic rank to which any one group can be allocated. In the provisional temporal ranking of taxa suggested by Goodman et al. (1998), the emergence of a family should take place in the late Oligocene (28–25 mya), while subfamilies should emerge in the early Miocene (23–22 mya). Fossil and molecular data combine in suggesting that the cercopithecine monkeys and colobine monkeys diverged from a common ancestor in the early to mid-Miocene (14–18 mya; Perelman et al. 2011, Roos et al. 2011), which, on the new criteria, precludes the two taxa from being ranked any longer as families. We, therefore, adopt Cercopithecidae as the sole extant family within the Cercopithecoidea, the other potential taxa being extinct fossil lineages (notably the lineage or ‘plesion’ to which Prohylobates belonged and another to which Victoriapithecine monkeys might have belonged). The family Cercopithecidae embraces some 23 genera within a very diverse group of African and Eurasian monkeys. These include the colobine monkeys or ‘leaf-monkeys’, subfamily Colobinae, and the cercopithecine monkeys or ‘cheek-pouched monkeys’, subfamily Cercopithecinae. The Cercopithecinae includes two tribes: the longtailed African guenons and their allies, Cercopithecini, and the largemuzzled African baboons, drills and other baboon-like monkeys, Papionini. The Papionini also includes the predominantly Asian genus Macaca, which is thought to be of African origin and to have emigrated

Frontal and lateral view of skull of Miocene Victoriapithecus macinnesi (Maboko Island, Kenya).

to Asia before 5 mya (late Miocene) (Stewart & Disotell 1998). Features distinguishing Cercopithecidae from Hominidae are quadrupedal locomotor apparatus, with arms not much shorter than the legs, somewhat elongated lumbar spine, and bilophodont cheekteeth, which initially operate as a series of transverse ridges along the toothrow and, with wear, leave a series of enamel loops that prolong the life of the teeth. Among living groupings, Cercopithecidae effectively share all their characteristics with Cercopithecoidea. Therefore, consult the Cercopithecoidea profile for the characteristics that distinguish Cercopithecidae in its new, post-2000, sense. The features of subfamilies and genera are presented under the appropriate taxonomic headings. Colin P. Groves & Jonathan Kingdon

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Subfamily Colobinae – Colobines: Colobus Monkeys Colobinae Jerdon, 1867. Mammals of India, p. 3. Colobus (5 species)

Procolobus (The 2 subgenera are often ranked as full genera)  (Procolobus) (1 species)  (Piliocolobus) (6 or more species)

Black Colobus Monkey, Black-and-white Colobus Monkeys Olive Colobus Monkey, Red Colobus Monkeys Olive Colobus Monkey Red Colobus Monkeys

p. 95

p. 120 p. 121 p. 125

Colobus monkeys are medium-sized, variously coloured monkeys with big bodies and small heads. One species is all black, some blackand-white, some have red and orange tints, and one species is dull olive. At close quarters their most distinctive peculiarity is a lack of thumbs. Amputation of digits is a mutilation for humans, hence the monkeys’ anthropocentric name, from the Greek, kolobos, meaning ‘mutilated’. Thumblessness and dietary specialization represent the two adaptations that most clearly separate the extant African colobines from other cercopithecoid monkeys. The progressive development of these peculiarities over time poses questions of the greatest biological interest (Hartwig 2002). There are a dozen recognized species in the African branch of Colobinae and these belong to three genera or subgenera, the Blackand-white Colobus-Group Colobus, the Olive Colobus Procolobus (subgenus Procolobus) and the Red Colobus-Group Procolobus (subgenus Piliocolobus). There are seven Asian genera, all of which derive from an African source following an emigration at about 12–11 mya (mid-Miocene; Perelman et al. 2011, Roos et al. 2011). Molecular phylogenetic evidence indicates that the African colobine radiation started by the late Miocene with the Black-and-white Colobus-Group splitting from the Olive Colobus/Red ColobusGroup by 9.9–6.8 mya (Ting 2008a, b, Perelman et al. 2011, Roos et al. 2011). The last common ancestor for Olive Colobus and Red Colobus is estimated at 6.4 mya (Ting 2008a, b) and 6.9 mya (Perelman et al. 2011, Roos et al. 2011). The chromosome count for all African colobines that have been examined thus far is 2n = 44 (Romagno 2001). Today, African colobus monkeys are almost exclusively equatorial and wholly arboreal, but the fossil record and their emigration to Asia demonstrate that, in the past, their ecology was more diverse, their geographic distribution much greater and their diversity more rich. Fossil colobines from the late Miocene and Pliocene show that they were then semi-terrestrial, and some are thought to have been wholly terrestrial, while at least one fossil species, Mesopithecus from the late Miocene of Eurasia, had a sizeable thumb. Jablonski (2002) and Leakey & Harris (2003) provide an exhaustive review of current knowledge of the fossil colobines and summarized the evidence available for African colobines. The earliest fossils date from the late Miocene (Benefit 1999) and several fossil genera have been described, notably Microcolobus (according to Elton 2007 the earliest fossil colobine at about 9 mya), Kuseracolobus, Rhinocolobus, Dolichopithecus and Cercopithecoides. An exceptionally large Pliocene form, Paracolobus chemeroni, was likely predominantly terrestrial, as was Dolichopithecus (Delson 1994, Benefit & Pickford 1986). To date, no fossil colobines have been

reliably allocated to the living genera or subgenera, and most fossil forms did not give rise to extant species. The divergence between Cercopithecinae and Colobinae has been variously estimated at ca.14 mya (Stewart & Disotell 1998) and 16.2 mya (17.9–14.4) (Raaum et al. 2005); the latter range seems more likely when it is remembered that by 11 mya well-developed colobines were probably present in Asia (Stewart & Disotell 1998, Tosi et al. 2005). The beginning of the mid-Miocene coincided with a period of warming just before a more general period of global cooling. Such an amelioration of climate might have allowed the colobine ancestor to detach itself from its parental population, putatively in south-eastern Africa, and move into the equatorial belt. This may help explain why colobines had such a substantial head-start over cercopithecines, not only in colonizing Asia but also in reaching outlying areas north of the equator. The first fossil cercopithecid in North Africa was a late Miocene colobine, Libypithecus. The colobine emigration to Asia took place about 11 mya, whereas the eastward spread of Macaca was 4 million years later. It seems plausible, therefore, that when the colobine ancestor moved north-west to share evergreen equatorial forests with a variety of mostly larger (and possibly more strategic-minded) protoapes, their advantage lay in being ‘digestion specialists’ that could cope with food types that were too difficult for the proto-apes, such as plants that protected their seeds and leaves with distasteful or toxic secondary compounds (Montgomery 1978). Later, when colobines and cercopithecines came into direct competition, the colobines’ dietary specializations became even more pronounced. This development gains some credence when it is remembered that at least one Asian genus, the partly terrestrial Semnopithecus, retains a less specialized digestive physiology. Further evidence for this progressive, staged, digestive specialization is registered in changes in the dentition of colobine fossils during the Pliocene (Benefit 1999). Judging from the relative abundance of their fossils, Colobinae were only overtaken by Cercopithecinae (in Ethiopia, which must have been very much of a peripheral outpost for them, even then) as late as 4.0–3.5 mya. At the early Pliocene site at Aramis, Ethiopia, White et al. (1994) calculated that colobines were 12 times as abundant as cercopithecines, but they had become much rarer by 3.3 mya (Benefit 1999). The mainly Pliocene radiation of Cercopithecini, particularly of guenons, which embrace a range of body sizes similar to colobines, seems to have progressively narrowed the niche for colobines. This is most obvious in Africa, where colobines originated and have the longest history of interaction with other monkeys. Thumblessness and dietary specialization represent the two adaptations that today separate the African colobines from other cercopithecoid monkeys. Only in monkeys wholly committed to living in dense forest would the hands become modified into flexible hooks. Many fossil colobines were not only more terrestrial, living in less than true forest, but they had thumbs. The evolution of hands, such as those possessed by modern African colobines, involved the alignment of the long fingers into a single, narrow, curved arc (where a thumb would actually obstruct its branch-gripping function). 93

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Peters’s Angola Colobus Colobus angolensis palliatus.

Because their hands have lost the ability to manipulate isolated, droppable objects or living prey, colobus prefer to take material off a plant directly into the mouth. Thus thumblessness implies that colobines became almost wholly arboreal and vegetarian at much the same time; but when? It is likely that these were relatively late developments, probably strongly influenced by competition from cercopithecines (but see Ting 2008a, b). The rise of cercopithecines eventually excluded colobines from all their earlier, more terrestrial niches, at the same time leading to still stronger selection for specialized digestion of chemically protected plant parts. The complex, sacculated stomach of colobus monkeys holds up to one-third of their total body-weight in food. They are ‘foregutfermenters’ and digestion requires long rests to allow bacterial fermentation of a sort that is similar to that of ruminants and other purely herbivorous animals (except that colobines do not regurgitate and chew cud). The bacteria are short-lived and protein from their dead bodies provides a large proportion of easily absorbable nutrients for the monkey (R. Hofmann pers. comm.). There is clearly a history of co-evolution between African colobines and the trees in their disparate habitats. A prominent part of most colobine diets consists of leguminous plants, the leaves and fruits of which are exceptionally well protected by chemicals. Because of this peculiar chemistry, and because legumes have dominated African forests, the processing of legume toxins must have been an important factor in the evolution of African colobine digestion (Oates et al. 1977, Montgomery 1978, Moreno-Black & Bent 1982). Although long referred to as ‘leaf-monkeys’, colobines are better described as ‘processors of difficult plant material’ and their diet includes fruits, seeds, petioles and flowers, as well as leaves, but most species actively avoid ripe,

soft, colourful fruit, preferring unripe fruits, seeds and seed-pods (Oates et al. 1977).There are significant differences among colobines species in the proportions of fruits and seeds that they eat, as is well exemplified in the profiles that follow. While colobines share the primary feature of a toxin-processing and leaf-digesting chambered stomach, the members of the Blackand-white Colobus-Group have the most advanced digestive capacity and a correspondingly extensive distribution through moist evergreen forests. The Olive Colobus Procolobus verus with, apparently, a less advanced ability to cope with fibrous old leaves and plant secondary compounds, is much more restricted in its small West African range. Monkeys belonging to the widely scattered, but patchily distributed, Red Colobus-Group appear to be intermediate. Colobine teeth are only moderately modified for a leafy diet, being essentially higher-cusped and higher-crowned specializations on the general cercopithecoid pattern (Strasser & Delson 1987). Generic modifications do occur. For example, the cheekteeth of Piliocolobus and Procolobus tend to be relatively narrower than those of Colobus. In Procolobus, the third lower molar is usually six-cusped, whereas in the other genera it is, as in most other cercopithecoids, five-cusped. The central incisors in both jaws are short and broad in Procolobus and Piliocolobus, but long and comparatively narrow in Colobus.The unworn lateral incisors are caniniform; in Procolobus and Piliocolobus their points are acute and are directed laterally, but in Colobus they are more obtuse and are directed medially. In Procolobus the incisors have a prominent lingual cingulum with a distinct lingual tubercle. The unusually robust teeth of Black Colobus Colobus satanas may be seen as adaptations to considerably more hard seeds in the diet (Oates & Trocco 1983). Apart from the dental characters mentioned above, there are well-marked differences among the three African colobine groups in the skull. Procolobus develop sagittal crests in adult ??, whereas Colobus never do. In Piliocolobus the orbits are angular, with thick supraorbital ridges interrupted by a notch or channel; there are wellmarked suborbital fossae; and the choanae and interpterygoid fossa are deep and narrow. In Colobus the orbits are more rounded, with supraorbital ridges that are usually less marked and generally run uninterrupted above each orbit without marked notches; the facial skeleton is relatively flat on either side of the nasal aperture, without suborbital fossae; and the choanae and interpterygoid fossa are low and wide. In most respects, Procolobus resembles Colobus cranially, except that, like Piliocolobus, there are marked suborbital fossae. Differences among the three groups were first described in detail by Verheyen (1962), although some of the characters he ascribed to Piliocolobus apply only to central African species. There are also characteristic differences among species both within Colobus and Piliocolobus. In particular, the skulls of C. satanas and Guereza Colobus guereza are very distinctive (see illustrations pp. 98 & 113 ). Lumping all colobus monkeys under a single genus, Colobus, was common practice until recently. Indeed, all our principal authors have, over time, shifted positions on colobine taxonomy. In their earlier works Groves (1970), Kingdon (1971) and Struhsaker (1975) all followed the authorities of that time (Booth 1954, 1958a, b,Verheyen 1962, Napier & Napier 1967) in referring to various regional forms of red colobus as subspecies of the Western Red Colobus Colobus badius. Initially, the arrival of molecular taxonomy scarcely changed this: Cronin & Sarich (1975) divided colobines into three equal genetic lineages, the African Colobus, and the Asian Pygathrix and Presbytis.

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Tentative phylogenetic tree of extant colobines (after Ting et al. 2008a).

Groves (1989) subdivided African colobines into two genera, Colobus and Procolobus, and he further subdivided the latter into the subgenera Procolobus and Piliocolobus. Since 1989, the generic or subgeneric name, and further subdivisions, of red colobus monkeys have been at variance (Grubb et al. 2003, Groves 2007b, Ting 2008a, b, Roos et al. 2011). Readers should be aware that opinions on the taxonomic status of red colobus and the number of species contained within this entity are still contentious, even among the editors and authors of this work. In adopting the subgenera Procolobus (Procolobus) and Procolobus (Piliocolobus) the editors and authors of this work have arrived at a provisional compromise. In this volume, T. Struhsaker, P. Grubb and K. Siex treat Piliocolobus as a subgenus of Procolobus; they have written profiles of the three taxa designated as P. rufomitratus, P. gordonorum and P. kirkii. Further profiles, designated as P. badius, P. pennantii and P. preussi, are presented by other authors. Of the forms described herein as subspecies of P. rufomitratus, C. P. Groves, J. Kingdon and T. Butynski recognize that complex, and the not easily explained interactions (perhaps hybrid zones) that exist between the bestdefined regional populations. They suspect, however, that some of the forms within P. rufomitratus merit full species status (notably tholloni, foai, tephrosceles, oustaleti). Readers will appreciate that little is known about red colobus biology in general, especially at the

molecular level, and that, as such, colobine taxonomy remains in a state of flux (Grubb et al. 2003, Groves 2007, Ting 2008a, b, Roos et al. 2011). Regardless of current controversies, the red colobus diaspora embraces a complex of 18 or more identifiable populations that have long posed major puzzles for scientists. Red colobus are recognizable by their distinctive colouring, with red caps or red patches on the crown being the norm in almost all species. Crown hair forms complex crests and crisp whorls in some species (notably badius, pennantii, tephrosceles, rufomitratus), but can be lank and unstructured in other species. A black band between orbits and ears is obvious in most populations and spreads up onto the brows or down onto the cheek in some eastern and central Congo Basin populations (notably rufomitratus, tephrosceles, tholloni) and in the Niger Delta population epieni.The distribution of red or black patches on the body and limbs is highly variable; some populations are quite drab, such as P. rufomitratus and P. pennantii, while others (notably P. kirkii, P. gordonorum, P. tholloni) are brightly coloured. Procolobus gordonorum has two main morphs, one rather drab and blackish, the other more colourful and contrasty in pattern, but both typically have red crown hair forming a ‘toupee’. The relevance of this polymorphism, which occurs within groups throughout their range, would be worth study, especially in relation to the selective effects of differing levels of predation and population densities. Procolobus foai is also highly variable; it may be that what are now classified as the four or five subgroups of this taxon are actually hybrid swarms occupying zones in between the distributions of formerly more distinct taxa (Colyn 1991). Other features of the Colobinae are presented in the genus and species profiles. Jonathan Kingdon & Colin P. Groves

Genus Colobus Black-and-white Colobus Monkeys Colobus Illiger, 1811. Prodroinus Systematis Mammalium et Avium, p. 69.

Western Guereza Colobus guereza occidentalis.

Polytypic genus endemic to the forests of tropical Africa. Until recently it was common to find the name Colobus applied to all extant African colobines, including some fossil species (see Subfamily Colobinae). The Black-and-white, or Pied, Colobus-Group of the genus Colobus consists of five species: Black Colobus Colobus satanas; Angola Colobus C. angolensis; King Colobus C. polykomos; Whitethighed Colobus C. vellerosus; and Guereza Colobus C. guereza. Apart from the bold black-and-white colouring, this genus is distinguishable from Piliocolobus and Procolobus by its conjoined ischial callosities, by the absence of sexual swellings in // and by the absence of perineal organs in ??. All species have very loud calls (‘roars’) that emanate from an enlarged larynx and subhyoid sac that are unique to Colobus. The stomach has three chambers that offer, within the colobines, the most advanced mode of digestion of difficult vegetation types. The skulls are different from species to species and, to a lesser extent, from population to population (Hull 1979). For detailed discussion and diagnosis of the significance of features unique to Colobus, see Oates et al. (1994). With the exception of C. satanas, the infants of all species are white at birth. 95

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Tentative phylogenetic tree for extant Colobus spp. (after Ting 2008a).

Colobus species include much mature green leaf in their diet. This enlargement of the dietary range has allowed two species, C. guereza and C. angolensis, to range well outside the main forest block into forest mosaics, galleries and degraded evergreen vegetation in eastern, north-eastern and south-central Africa. Both of these species have been particularly successful in colonizing montane forest habitats, where they grow thicker, longer pelage. Earlier expansions, presumably during wetter, warmer periods, have left isolated populations on mountain massifs in eastern Africa and some of these are distinct subspecies. Colobus satanas and C. polykomos, specialized seed-eaters, are much more restricted to high forest, though their preferred diets enable them to subsist in swamp forest and other forests with extremely poor soils. Taking the ability to digest chemically protected plant material as the primary adaptation in Colobinae, Colobus is clearly the most advanced genus. As such, the other African genera must derive from earlier branches of the colobine tree. Awaiting further study are differences among populations of the same Colobus species within and outside the main forest block. Other monkey species, including other colobine genera and guenons, are relatively few outside the main forests, whereas competition from the large guilds of primates within equatorial forests is intense. Comparing C. angolensis in the

Western Guereza Colobus guereza occidentalis neonate.

Top: Skeleton of Guereza Colobus Colobus guereza. Above: Myology of Western Guereza Colobus guereza occidentalis.

southern Congo Basin with C. angolensis in NW Tanzania could be revealing, as could comparisons between C. guereza east and west of the Eastern (Gregory) Rift. In the Semliki and north Rwenzori forests, SW Uganda, C. angolensis lives in montane forest and C. guereza lives in lowland forest. Colobus guereza has possibly played a role in the recent disappearance of Procolobus in this area (the main influences being hunting, forest clearance and degradation). In the coastal littoral and ‘Eastern Arc’ montane and forested areas of East Africa there is a north–south partition between C. guereza and C. angolensis, the latter occupies all the coastal and gallery forests of S Kenya and Tanzania, while C. guereza occupies forests north and west of the Pare Mts up to 2900 m (notably Mt Kilimanjaro, Mt Meru, Mt Kenya and the Aberdares) (T. Butynski pers. comm.). This suggests a dynamic in which a possibly more physiologically advanced C. guereza expanded from the west (and only north of the Congo R.), possibly displacing C. angolensis in some localities but not in others, although there are areas of overlap between the two Colobus species in E DR Congo (e.g. Ituri Forest). Such localities could be rewarding for the study of niche formation in competitive primate communities. Colobus, therefore, offers numerous opportunities for study of dynamics in African ecosystems (Struhsaker 1975). Recent molecular evidence indicates that the five extant Colobus spp. diverged between 3.5 mya (mid-Pliocene) and 0.2 mya (end of the Pleistocene) with C. satanas being the first extant species to diverge and C. polykomos and C. vellerosus being the last to diverge (Ting 2008a, b). Jonathan Kingdon & Colin P. Groves

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Colobus satanas

Colobus satanas  Black Colobus Fr. Colobe noir; Ger. Schwarzer Stummelaffe Colobus satanas Waterhouse, 1838. Proc. Zool. Soc. Lond. 1837: 57 [1838]. Fernando Po (=Bioko I.), Equatorial Guinea.

Black Colobus Colobus satanas adult female.

Taxonomy  Polytypic. Two subspecies (Grubb et al. 2003). Formerly considered a subspecies of King Colobus Colobus polykomos (e.g. Haltenorth & Diller 1977), but the distinctive phenotypic, cranial, dental and vocal features warrant species status (Dandelot 1974, Hull 1979, Oates & Trocco 1983). The full species status of C. satanas is now widely accepted (Groves 2001, 2005c, 2007b, Grubb et al. 2003). Grubb (1978) suggested that C. satanas represents an ancestral form of Colobus spp. This is supported by recent molecular evidence that indicates that within the Black-and-white ColobusGroup, C. satanas was the first to diverge (Ting 2008a, b). Synonyms: anthracinus, limbarenicus, metternichi, municus, zenkeri. Chromosome number: 2n = 44 (Gregory 2008). Description  Large, black, arboreal monkey with heavy body and long limbs and tail. Entirely black (including bare skin areas). Sexes identical in colour. Adult / C. s. satanas about 80% as heavy as adult ? (Butynski et al. 2009). Head with crest of hairs. Ears with extremely irregular outline. Tail with tuft of hairs at base but not at tip. Dorsal outline of braincase in lateral view is saddle-shaped. Skull less prognathous than for other Colobus spp. (Groves 2001). Individual with aberrant coat colour (white and black areas irregularly mixed) described from Bioko I., Equatorial Guinea (González-Kirchner 1997a). Infants brown. Geographic Variation C. s. satanas Bioko Black Colobus. Bioko I. endemic. Pelage long and thick. Smaller; tail ca. 16% shorter; hindfoot ca. 10% shorter, body weight about 10% less (see below).

Colobus satanas

C. s. anthracinus Gabon Black Colobus. Mainland Africa. Pelage short and thin. Larger. Similar Species  None within geographic range. Distribution  Endemic to western central Africa. Rainforest BZ. Restricted to rainforests of Bioko I., Equatorial Guinea, Cameroon south of Sanaga R., south through coastal Rio Muni (Equatorial Guinea) to SW Gabon, and east to W Congo. Eastern and southern limits poorly known (Groves 2001). Early in the 20th century one specimen collected east of 14° E and two specimens collected north of 03.5° N (Napier 1985). There are no data to suggest that the Black Colobus is still present this far east or north. On Bioko I. now apparently occurs in two populations: one centred on the Pico Basilé (central part of the island) and one in southern onethird of the island (Butynski & Koster 1994). Three populations in Rio Muni: one on left bank of Uoro-Mbini R. between Niefang and Macizo de los Montes Mitra, one in the mountains near Cabo San Juan (ca. 01° 15´ N, 09° 30´ E) and one in the Nsoc-Nzomo area (ca. 01° 55´ N, 11° 00´ E) (González-Kirchner 1994). Distribution patchy in Gabon; in Monts de Cristal and in Minkébé area. Not known whether present between these two areas. In south present in the Massif du Chaillu. In west present between Monts Doudou and Atlantic coast. Distribution limits to east uncertain. Not known between left bank of Ivindo R. and right bank of Ogooué R. Present in Lopé N. P. and adjacent Forêts des Abeilles (Malbrant & Maclatchy 1949, Blom et al. 1992, Lahm 1993, White 1994, Brugière et al. 2002). In Congo possibly restricted to area between 97

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eastern boundary of Odzala N. P. and Gabon border (Carpaneto 1995, M. Fay pers. comm.). Habitat  Primary and old secondary moist forest. Coastal forests to montane forest to heathland on Bioko I., from sea level to 3000 m (Butynski & Koster 1994). On the mainland, observed from sea level to 800 m (in Waka N. P., C Gabon; Abitsi 2006, F. Maisels pers. comm.). Absent in degraded and young secondary forests but in gallery forests. Presence of tall trees essential as the species preferentially uses the upper canopy: 36% and 40% of time is spent higher than 30 m at Makandé, central Gabon (Fleury 1999), and on Bioko I., respectively (González-Kirchner 1997b). Mean annual rainfall for sites at which C. satanas occurs ranges from ca. 1500 mm (Lopé, Gabon; White 1994) to >10,000 mm (south Bioko; Butynski & Koster 1994). Abundance  Colobus s. anthracinus common in non-hunted areas but abundance can vary markedly within a given area. For example, in the Lopé N. P., densities vary from 11 ind/km2 in primary forest (Brugière 1998) to 30 ind/km2 in gallery forest (Harrison 1986). Over the species’ geographic range, densities vary from 7 ind/km2 in Forêt des Abeilles, Makandé (Brugière et al. 2002) to 30 ind/km2 in Douala Edea F. R., Cameroon (McKey 1978). On Bioko I., C. s. satanas encountered at the rate of 0.02 groups/ km along 373 km of transect during an island-wide survey in 1986 (Butynski & Koster 1994). Other encounter rates on Bioko are as follows: 0.18 groups/km in 2008 along 44 km of transect in Gran Caldera de Luba; 0.14 groups/km in 2008 along 49 km of transect on south slope of Pico Basilé; and 0.39 groups/km in 2009 along 48 km of transect and 0.32 groups/km in 2010 along 50 km of transect at Badja North, SW Bioko (T. Butynski, G. Hearn, M. Kelly & J. Owens pers. obs.). These last-mentioned three sites are remote and receive relatively low levels of hunting. Also, there has been little to no anthropogenic impact on the habitats at these sites. As such, these encounter rates are likely close to what can be expected for undisturbed populations of C. s. satanas. Adaptations  Diurnal and arboreal. The Black Colobus is the most granivorous of all Colobus spp. Seed eating is an adaptative strategy as seeds are high in nutrients and more palatable than leaves. Polyspecific associations of Black Colobus with Cercopithecidae monkeys permit a higher consumption of seeds (Gautier-Hion et al. 1997). Geophagy occurs when the consumption of leaves is high. Chemical analysis shows that the soils eaten have sodium and magnesium contents significantly higher than non-eaten forest soils (Fleury 1999). When the tree species composition of the forest induces both seasonal food shortage and episodic intra-annual severe bottlenecks in food supplies (as in forest dominated by the irregular mass fruiting Caesalpiniceae tree species), Black Colobus shift to a semi-nomadic ranging behaviour over a large home-range (Fleury & Gautier-Hion 1999). This is the least costly strategy to cope with the low carrying capacity of the habitat. Black Colobus spent 37–60% of the daylight hours in inactivity, 22–27% handling and ingesting food, 4–32% moving and 4–10% in social interactions (McKey & Waterman 1982, Fleury 1999). Grooming is the predominant social interaction (38%), while

Lateral and palatal views of skull of Black Colobus Colobus satanas adult male.

agonistic interactions account for only 7%. Typical daily activity pattern includes the following sequence (from sun rise to sun set): moving (short distance), feeding, resting, moving (long distance), feeding and resting (Fleury 1999). Foraging and Food  Granivorous-folivorous. At Makandé (Gabon, 00° 40´ S, 11° 54´ N) foraging activities peak between 07:00h and 08:00h, and 15:00h and 17:00h. This corresponds to the most active period of the day. Black Colobus often remained within small areas for several days while intensively exploiting a few individual trees. This is followed by days when they move farther, to other food patches in which they linger (Fleury & Gautier-Hion 1999). Mean distance travelled/day is 852 m (range 20–1980, n = 24) at Makandé, 510 m (range 40–1100) at Lopé (Gabon, 00° 30´ S, 11° 40´ E) and 459 m (range 100–800) at Douala-Edéa (Cameroon, 03° 20´ N, 10° 00´ E). Daily travel distance increases with increasing seed intake and decreases with increasing leaf intake at Makandé and Lopé (Fleury & Gautier-Hion 1999). In contrast, at Douala-Edéa, daily travel distance increased with increasing mature leaf intake because mature leaves were rare and patchily distributed plant species (McKey 1979). Home-range size at Makandé (573 ha) was three times that of a group at Lopé (184 ha) and eight times that of a group at Douala-Edéa (69 ha) (McKey 1979, Harrison & Hladik 1986, Fleury 1999). Seeds and leaves (young and mature) account, respectively, for 56% and 38% of the diet at Makandé, 64% and 26% at Lopé and 53% and 38% at Douala-Edea (McKey 1978, Harrison 1986, Gautier-Hion et al. 1997). Consumption of leaves increases when availability of seeds decreases. Mature leaves are eaten when young leaves are scarce. Foods rich in minerals and nitrogen, but low in lignin and secondary compounds, are preferred (McKey et al. 1981). Seed consumption increases when Black Colobus feed in mixedspecies groups with (frugivorous) Putty-nosed Monkeys Cercopithecus

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(n.) nictitans, Crowned Monkeys Cercopithecus (m.) pogonias and Greycheeked Mangabeys Lophocebus albigena (Gautier-Hion et al. 1997). At Makandé, the three most often eaten plant food species are Petrocarpus soyauxii (Fabaceae), Dialium pachyphyllum (Caesalpinaceae) and Aucoumea klaineana (Burseraceae), but their use varies among years (Fleury 1999). Opportunistic observations on Bioko I. suggest that Black Colobus there eat few, if any, seeds. Here, the flower buds of Tabernaemontana brachyantha (Apocynaceae) and the leaves of Schefflera mannii (Araliaceae) appear to be particularly important foods. On Bioko I., Black Colobus sometimes come to the ground to feed (T. Butynski pers. comm.). Social and Reproductive Behaviour  Social. Groups have 2–6 adult ?? and 2–7 adult //. Mean group size 13 (range 5–30, n = 13; Sabater Pi 1973a, McKey, Eisentraut in Oates 1994, Fleury 1999). Adults always more numerous than immatures (at Makandé, mean percentage of immatures/group is 30% (n = 3). Allomothering observed several times at Makandé. Group home-ranges overlap. At Makandé up to seven groups shared the same space. Overlap of a group’s home-range by other groups reaches 65% (Fleury & Gautier-Hion 1999). At Makandé encounters between Black Colobus groups occurred more often than expected by chance. Encounters mainly occur at food patches and are peaceful. Short chases and counter-chases occur, are rare, and involve from one to five adult ?? in each group (Fleury & Gautier-Hion 1999). Males transfer between groups more often than do //. Integration into the new group is instantaneous (Fleury 1999). At Makandé, Black Colobus were in association with one or more other species of primate (C. nictitans, C. pogonias, Moustached Monkey Cercopithecus (c.) cephus and L. albigena) 14% of the time (n = 3 groups). At this site a single C. pogonias (?) was integrated into a group of Black Colobus and interspecific grooming with that individual occurred (Fleury & Gautier-Hion 1999). The Black Colobus is less vocal than are other Colobus spp. and the vocal repertoire is less extensive. A high volume, low frequency (0.5–1.5 kHZ) loud-call (the ‘roar’) is produced by both sexes. The roar is given mainly in response to potential or identified danger. Other vocalizations include ‘squeals’ that are often produced before roars, and ‘caws’ that are given during agonistic encounters (Fleury 1999).The roar is not used as a territorial loud-call as in other Colobus spp. (Fleury 1999). Oates & Trocco (1983) found that among Colobus spp., C. satanas has the most distinct roar. On Bioko I., roars often heard at night, especially during the hour before dawn. Once the male(s) of one group begins to roar, the ?? of 1–3 distant groups often begin to roar. A ‘soft honk’ is frequently given as an intragroup contact call that can be heard to ca. 50 m. A ‘loud, sharp honk’ is given as an alarm/warning call that can be heard to >150 m.The loud, sharp honk often elicits a bout of roaring and ‘aint’ alarm/warning calls from other members of the group (T. Butynski pers. comm.). Reproduction and Population Structure  Black Colobus // have a slight raising of the bare black area adjacent to the perineum during the mating and birth periods (Oates & Trocco 1983, Fleury 1999). Females solicit copulations using a

Adult Black Colobus Colobus satanas.

presentation posture. Length of gestation unknown. At Makandé (Fleury 1999) and Douala-Edea (McKey 1979), most births occur during the second half of the year, but the sample is low (n = 12). Only one infant born at a time. At Makandé the inter-birth interval is longer than two years (n = 7 //). Suckling occurs for at least eight months. Age of maturity not know, but estimated at >4 years (Fleury 1999). The overall ? : / ratio for one group at Makandé over two years varied from 1 : 1.3 to 1 : 1.8. When adults only are considered, the ? : / ratio varied from 1 : 1.2 to 1 : 1.4 at Makandé (Fleury 1999), 1 : 2.0 to 1 : 5.0 at Douala-Edéa (McKey 1979), and 1 : 2.5 to 1 : 5.0 at Lopé (M. Harrison pers. comm.). The adult/immature ratio for one group at Makandé over two years varied from1 : 0.2 to 1 : 0.5. Birth rate in this group was 0.29 births/year/adult /. No deaths occurred in this group during the 2-year study (Fleury 1999). Birth-weight not known; a 2–3-weekold infant weighed 770 g (Fleury 1999). Longevity not known. Predators, Parasites and Diseases  Leopards Panthera pardus are known predators (Henschel et al. 2005, 2011). Robust Chimpanzees Pan troglodytes and African Crowned Eagles Stephanoaetus coronatus are probable predators. Predation rates probably low as no case of predation observed during the monitoring of groups at Makandé, Lopé or Douala-Edéa. Diseases and parasites unknown. Conservation  IUCN Category (2012): Vulnerable as C. satanas and as C. s. anthracinus. Endangered as C. s. satanas. CITES (2012): Appendix II. Main threats are logging, forest clearance for agriculture and hunting by humans. Populations persist in logged forests as long as logging does not significantly alter the structure and composition of the forest (Brugière 1998). The Black Colobus is unable to thrive in degraded secondary forest but persists in a mosaic of secondary and primary forest. It is highly vulnerable to hunting because of its large body size, its relative inactivity and the relative lack of fear of humans. From 1998 to 2005, between 170 and 380 Black Colobus were sold each year at the Malabo Market, Bioko I. (Hearn et al. 2006). See also Fa et al. (2000), Fa & Garcia Yuste (2001), Kumpel et al. (2008) and Mora et al. (2009). The Black Colobus occurs in protected areas in Cameroon: Douala-Edea Faunal Reserve (1283 km²) (not present in Dja Faunal Reserve; probably extirpated from Campo-Maan N. P.); in Gabon: Lopé N. P. (4910 km²), Monts de Cristal N. P. (1200 km²), Minkébé N. P. (7567 km²); in Equatorial Guinea, Bioko I: Pico Basile N. P. 99

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(330 km2), Gran Caldera & Southern Highlands Scientific Reserve (510 km2); in Rio Muni: Monte Alén N. P. (2000 km²). There are no Black Colobus in the world’s zoos.

GWS (/): 74 mm, n = 1 Bioko I., Equatorial Guinea (Butynski et al. 2009). Skull measurements by T. Butynski (pers. obs.)

Measurements Colobus satanas C. s. satanas HB (??): 595 (510–675) mm, n = 37 HB (//): 576 (500–680) mm, n = 48 T (??): 759 (690–840) mm, n = 37 T (//): 742 (600–825) mm, n = 47 HF (??): 174 (160–188) mm, n = 38 HF (//): 170 (154–190) mm, n = 46 E (??): 32 (28–40) mm, n = 38 E (//): 30 (26–36) mm, n = 47 WT (??): 10.3 (7.3–13.1) kg, n = 12 WT (//): 8.2 (6.6–10.0) kg, n = 7 Upper Canine (??): 15 (10–18) mm, n = 28 Upper Canine (//): 6 (4–10) mm, n = 43 Lower Canine (??): 11 (6–14) mm, n = 28 Lower Canine (//): 5 (3–8) mm, n = 43 GLS (?): 108 mm, n = 1 GWS (?): 80 mm, n = 1 GLS (/): 105 mm, n = 1

C. s. anthracinus HB (??): 654 (580–710) mm, n = 8 HB (//): 607 (465–690) mm, n = 5 T (??): 902 (830–1000) mm, n = 9 T (//): 892 (820–970) mm, n = 6 HF (??): 196 (180–210) mm, n = 9 HF (//): 184 (170–195) mm, n = 5 E (??): 28 (20–46) mm, n = 5 E (//): 44, 50 mm, n = 2 WT (??): 11.1 (9.0–13.2) kg, n = 10 WT (//): 9.4 (6.0–10.9) kg, n = 5 Data from various locations; HB, T, HF, E and / WT (Malbrant & Maclatchy 1949, Fleury 1999, O’Leary 2003); ? WT (Malbrant & Maclatchy 1949, Harrison 1986, Fleury 1999, Delson et al. 2000) Key References  Fleury 1999; Fleury & Gautier-Hion 1999; Harrison & Hladik 1986; McKey 1978; McKey et al. 1981; Oates 2011. Marie-Claire Fleury & David Brugière

Colobus polykomos  King Colobus (Western Pied Colobus, Western Black-and-white Colobus) Fr. Colobe magistrat; Ger. Weißbart-Stummelaffe Colobus polykomos (Zimmermann, 1780). Geogr. Gesch. Mensch. Vierf. Thiere 2: 202. Sierra Leone.

Taxonomy  Monotypic species. Between 1927 and 1983, polykomos and White-thighed Colobus vellerosus were considered subspecies of C. polykomos (Rahm 1970, Hull 1979), because W. P. Lowe had collected specimens of an intermediate subspecies, C. polykomos dollmani in 1927 in Côte d’Ivoire (Oates & McGraw 2009). Oates & Trocco (1983) conclude that vellerosus and polykomos are separate species and that dollmani represents a hybrid swarm. Groves et al. (1993) argue that dollmani is more closely related to C. vellerosus than to C. polykomos. Groves (2001, 2005c, 2007b) and Grubb et al. (2003) list dollmani as a synonym of C. vellerosus. Groves (2007b) lists ursinus as a synonym of C. polykomos. Synonyms: comosa, polycomos, regalis, tetradactyla, ursinus. Chromosome number: 2n = 44 (Gregory 2008). Description  Large, long tailed, thumbless, black-and-white, arboreal monkey. Sexes alike in colour but ?? have slightly longer canines (Plavcan 1999). Adult / about 84% as heavy as adult ?. Face furless and black. Nose slightly bent, long. Top of head, sides of face and throat greyish-white. Front of shoulders and forearms with straggly, long greyish-white hair. Body and limbs black. Tail long ca. 170% of HB, not tufted. Males have small testes compared to Procolobus spp. (Oates 1994). Callosities of ?? joined and fringed by one large white triangle, which sometimes continues to the genitalia, while // have two smaller triangles. Infants predominantly white for first 41–53 days. Full adult colouration attained at 97–120 days (Mearns & Pidgeon 1978).

Geographic Variation  None recognized but see Oates & McGraw (2009). Similar Species Colobus vellerosus. Perhaps parapatric in vicinity of Bandama R. Face encircled by thick ruff of white fur. Shoulders lack epaulettes or with a few white hairs.Thighs with broad white stripe on proximal two-thirds. Distribution  Endemic to coastal West Africa. Rainforest BZ. Historical Distribution The forest zone along the coast of Côte d’Ivoire, Liberia, Sierra Leone, Guinea, Guinea-Bissau and scattered forest patches in Senegal, up to 14° N (Booth 1954, 1958b, Rahm 1970, Oates & Trocco 1983). Reports of skins in Gambia are questionable (Oates & Trocco 1983). Eastern boundary: Sassandra R., Côte d’Ivoire (starting at 06° W). Current Distribution  Guinea (Barnett et al. 1994, Ziegler et al. 2002, Eriksson & Kpoghomov 2006), Sierra Leone (Harding 1984a), Liberia (Waitkuwait 2003), Côte d’Ivoire (Oates et al. 1990, Oates 1994), and a few remaining sites in Guinea-Bissau (C. Sousa pers. comm.). Extinct in Senegal. Colobus polykomos–vellerosus hybrid population between Sassandra R. and Bandama R. is likely restricted to one site (Gonedelé Bi et al. 2006, 2012), if it still exists (Oates & McGraw 2009).

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King Colobus Colobus polykomos adult male.

Habitat  Lowland forests: wet evergreen, moist evergreen, moist semi-deciduous and dry semi-deciduous forest. Also in riparian forests in savanna and patches of dry forest well outside the major moist forest blocks (Oates 1977b). Mean annual rainfall and mean annual temperature range from 3000 mm and 27 °C at Tiwai and Gola, Sierra Leone, to 1830 mm and 26.5 °C at Banco, Côte d’Ivoire, to 300 mm with 24.5 °C in Nimba Mts, Liberia and Guinea

Colobus polykomos

(Korstjens & Dunbar 2007). Range in altitude from near sea level to 800 m at Mt Nimba (Galat-Luong & Galat 1990). Abundance  Common where habitat available and hunting pressure low. About 5.6 groups/km2 (50 individuals/km2) in undisturbed forest at Tiwai, Sierra Leone (Dasilva 1989, Oates et al. 1990), and 2.8 groups/km2 (47 individuals/km2) in Taï, Côte d’Ivoire (Korstjens 2001, but see Galat & Galat-Luong 1985 who calculated 23.5 ind/km2, n = 2, in Taï based on their home-range estimates). Densities drop dramatically for areas where poaching is common, such as in Taï N. P. away from research areas (Refisch & Koné 2005, A. Korstjens pers. obs). Adaptations  Diurnal and arboreal. Colobus polykomos spends ca. 52% of time in closed canopy, ca. 33% in emergents and ca. 15% in lower strata both at Taï (Galat & Galat-Luong 1985, n = 2242; see also McGraw 1996, 1998a, McGraw & Sciulli 2011) and at Tiwai (Dasilva 1989). Comes to ground to forage on fallen seeds of Pentaclethra macrophylla, to cross forest clearings and for conspecific inter-individual chasing. Regularly found at forest fringes. Remains inactive for long periods and hides in thick tangles of lianas. Sits while feeding and often sprawls over a bough while resting (McGraw 1998c). In Taï spends ca. 40% of time on boughs, ca. 47% on medium-sized branches and only ca.13% on thin branches (Galat & Galat-Luong 1985, n = 2117; see also McGraw 1996, 1998b, c). Postures, such as hunching and sunbathing (spends 39% of time in the sun; A. Galag-Luong pers. obs.), and travel distances optimize energy intake and expenditure according to climatic conditions and food availability (Dasilva 1992, 1993). Annual activity budget in Taï and Tiwai, respectively: resting 54–55% and 61%, feeding 16–31% and 101

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28%, moving 13–23% and 9%, and socializing 6–8% and 1% (GalatLuong 1983, n = 2233; Dasilva 1989, Korstjens 2001). Rests 53% of time out of reach of leaves (A. Galat-Luong pers. obs., n = 522) and prefers tall bare trees for sleeping but does not regularly use the same sleeping-trees (Dasilva 1989, A. Korstjens pers. obs.). Foraging and Food  Folivorous–frugivorous. Forages primarily on leguminous trees and lianas. In Taï (Korstjens et al. 2007) and Tiwai (Davies et al. 1999) the annual diets were, respectively, 28% and 30% young leaves, 20% and 27% mature leaves, 48% and 36% fruits (33% hard seeds and 3% whole fruits in Tiwai) and 3% and 3% flowers. In Taï Galat & Galat-Luong (1985) found 53% leaves, 32% fruits, 4% flowers and 10% miscellaneous (e.g. lichen) (n = 209 food item intakes). In Taï and Tiwai the most frequently consumed food is Pentaclethra macrophylla seeds (Dasilva 1989, 1994, Korstjens 2001, Korstjens et al. 2007). The long canines are used to strip open the wooden pods of these and similar unripe fruits to reach the hard seeds inside (A. Korstjens pers. obs.). In Taï the number of food species is low compared to sympatric Western Red Colobus Procolobus badius badius and Olive Colobus Procolobus verus (Korstjens 2001, Korstjens et al. 2002). Mean daily travel distance is 677 m (range 200–1241 m, n = 54; Korstjens 2001, Korstjens et al. 2007) in Taï and 860 m (range 350–1410, n = 72; Dasilva 1989, 1992) in Tiwai. Daily travel distances increase during the months in which P. macrophylla seeds are the main food and decrease when high quality food is scarce at Taï and Tiwai. Detailed lists of plant food species are presented in Dasilva (1992, 1994) and Korstjens (2001). Despite similar mean group sizes (see below), mean annual homerange size is 77.4 ha (range 71.5–83.3, n = 4) in Taï (but see Galat & Galat-Luong 1985, who found mean home-range size of 37.5 ha [range 29–46 ha, n = 2] in Taï) and 22 ha (n = 1) in Tiwai (Dasilva 1989, Oates 1994). Home-ranges of conspecific groups overlap 20–22% in Taï. Due to similar percentage overlap with three to five groups, no group had an area of exclusive access in its home-range (Korstjens et al. 2005). Social and Reproductive Behaviour  Social. Lives in groups of 5–19 individuals, mean = 16.2 (n = 10) in Taï and 12.5 in Tiwai (n = 2), with 1–3 adult ?? (in Taï eight of ten groups had one ?, and 1–3 adult ?? in Tiwai where most groups had two adult ??) and 4–6 adult // (Galat & Galat-Luong 1985, Dasilva 1989, Korstjens 2001). A few solitary ?? have been seen in Taï but none in Tiwai (Galat & Galat-Luong 1985, Dasilva 1989, Korstjens 2001). Agonistic interactions among adult // are rare (Dasilva 1989, Korstjens et al. 2002) but, with 0.60 interactions/focal observation hour in Taï, more common than in C. vellerosus (P. Sicotte pers. comm.) or in Black-and-White Colobus C. guereza (Fashing 2001c). Aggression among adult // is most frequent during foraging, especially over items that require a long handling time such as seeds from wooden pods (Korstjens et al. 2002). Aggression between the sexes is rare, but adult ?? displace adult // (Dasilva 1989, Korstjens 2001). Clear dominance relationships exist among adult ?? (Dasilva 1989). Proximity between individuals: Taï, 35% of time is spent within 2 m of conspecifics; Tiwai, 48% within 2.5 m of conspecifics. Grooming is the main affiliative interaction (see ‘time budget’). Adult // groom up to ten times more and spend up to twice as much time with neighbours than adult ?? (Dasilva 1989,

Adult King Colobus Colobus polykomos.

Korstjens 2001). Males spend little time together and are often at the periphery of the group. Inter-group interactions occur once every 6.6 and 8.0 observation days in Taï and Tiwai, respectively. Inter-group encounters range from simple proximity (12% of 83 encounters in Taï and 33% of nine encounters in Tiwai), to displays (25% and 0%), or fights and chases (63% [Korstjens et al. 2005] and 67% [Dasilva 1989]). Female participation in inter-group conflicts, generally rare in colobus monkeys (Oates 1977c, Struhsaker & Leland 1979, Fashing 2001c), is common in Taï (52% of 83 encounters [Korstjens et al. 2005]) but was not observed in Tiwai (Dasilva 1992). In Taï, // are more often aggressive during the months when they eat P. macrophylla seeds. Adult ?? perform forays to other groups (average of once every 20 days in Taï) and chased members of the target group in 75% of 16 forays. One to six adult // joined the ? in 25% of the forays, but // never attacked the target group. Forays were especially frequent when the target group had young infants (see Sicotte & MacIntosh 2004 for similar observations on C. vellerosus). Males often threaten ?? from other groups with a ‘stiff-legged display’ and by bouncing through the trees. Vocalizations are rare and most are soft. The most conspicuous vocalization is the loud-call (‘roar’). The roar has similar general characteristics in the different Colobus species, but has a faster pulse rate and higher pitch in C. polykomos compared to C. vellerosus and C. guereza (Oates & Trocco 1983, Oates et al. 2000b). Roars occur throughout the day, and unlike in C. guereza (Marler 1969), morning choruses are relatively rare in C. polykomos (Dasilva 1989, A. Korstjens pers. obs.). Most roars are produced in response to a predator threat. Roar characteristics differ according to the type of predator (i.e. Leopard Panthera pardus or African Crowned Eagle Stephanoaetus coronatus) that is perceived (Schel et al. 2009). Roars are often contagious (i.e. other groups respond with a roar). Although most complete roars are performed by ??, // do sometimes roar in Taï in response to a threat (A. Korstjens & A. Galat-Luong pers. obs., E. C. Nijssen pers. comm.). Roars are rarely given during inter-group encounters (Dasilva 1989, A. Korstjens pers. obs.). Females and ?? jointly threaten, mob and alarm-call when threatened by humans or predators but ?? are the more aggressive (Korstjens et al. 2005). Females disperse at least occasionally and ?? disperse as a rule (Dasilva 1989, Nijssen 1999, Korstjens 2001). Sexual behaviour is rarely observed. Females in all reproductive states (cycling, pregnant, lactating) copulate. Females have no sexual swellings and

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solicit copulations by presenting. Copulatory vocalizations do not occur (Dasilva 1989). In Tiwai all three ?? in a three-male group mated with // (most mates were pregnant/lactating // [Dasilva 1989]); in Taï, only the dominant ? was observed to mate in a bimale group (A. Korstjens pers. obs.). Infant handling is common and is most often performed by juvenile and nulliparous //. Lactating // whose infants are being handled seem to be able to devote more time to feeding (Dasilva 1989, E. C. Nijssen pers. comm.). Colobus polykomos spent 28% of time in a polyspecific association (both in Taï and Tiwai), which is no more than expected by chance (Whitesides 1989, Höner et al. 1997). However, in Taï, encountered primate groups often contain C. polykomos (68% of encounters of groups, n = 37); associations with Diana Monkeys Cercopithecus (d.) diana and red colobus being the most frequent (Galat & Galat-Luong 1985). Red colobus solitary ?? and solitary // regularly associate for several days or weeks with C. polykomos groups (Korstjens et al. 2007). Inter-specific social interactions include grooming, playing and aggression (GalatLuong 1983, Deffernez 1999). Colobus polykomos sometimes handle Olive Colobus infants (A. Korstjens pers. obs.) and / red colobus sometimes handle C. polykomos infants (Fimbel 1992); in both cases, both parents try to get the infant back (A. Korstjens pers. obs.). Reproduction and Population Structure Inter-birth interval: mean ± S.D. = 25.5 ± 5.0 months; median = 25.0 months (Taï, n = 4; A. Korstjens pers. obs.); mean = 24 months (Tiwai, n = 4; Dasilva 1989). Births occur throughout the year (n =  6) in Taï (A. Korstjens pers. obs.), but only during Dec–Feb (i.e. dry season) in Tiwai (n  = 9) (Dasilva 1989). Gestation: ca. 165 days (147–178, n = 5) at Jersey Zoo (Mallinson 1973). Birth-weight is 597 g (Ross 1991). One infant is born; twins not reported. Infants feed from their mothers for at least five months and rarely suckle after one year (Dasilva 1989, Korstjens 2001). One of four // in Taï had their first infant at four years of age, but the other three did not reproduce for the first 6–7 years (after which they disappeared from their natal group). Females are receptive for 3–7 days and can have five consecutive receptive periods (A. Korstjens pers. obs.). Maximum recorded life-span in captivity is 30.5 years (Ross 1988). Predators, Parasites and Diseases  Main predators in Taï Forest are Robust Chimpanzees Pan troglodytes (Boesch & Boesch-

Achermann 2000), African Crowned Eagles (Shultz et al. 2004), Leopards (Hoppe-Dominik 1984, Zuberbühler & Jenny 2007) and humans (Refisch 2000). Robust Chimpanzees are estimated to catch 1.4% (Korstjens 2001), Leopards 7.0% and African Crowned Eagles 2.1% (Shultz et al. 2004) of the C. polykomos population each year in Taï. Although viraemia is longer in C. polykomos than in cercopithecines, the role of C. polykomos in Yellow Fever transmission should be less important because the proportion of immature individuals is lower (Galat & Galat-Luong 1997). Conservation  IUCN Category (2012): Vulnerable. CITES (2012): Appendix II. Local populations of C. polykomos are threatened throughout the range due to habitat loss and hunting by humans (McGraw 2007b). Human consumption of C. polykomos in the Taï region is 1.4 ind/ km2/year (11.7 kg/km2/year) while maximal sustainable harvest is estimated at 0.9 ind/km2/year (Refisch & Koné 2005). Colobus polykomos is the fourth primate species to disappear from the Taï region because of human activity (Galat & Galat-Luong 1997). In this region high population densities are only maintained near research stations (Refisch & Koné 2005). Taï N. P., Nimba MAB Reserve, National Park of Upper Niger (Guinea) and Tiwai are the main refuges. Survive also in ‘sacred woods’ in Côte d’Ivoire and Guinea (Galat & Galat-Luong 1997, Gonedelé Bi et al.2006, 2012). Measurements Colobus polykomos HB (??): 1530, 1590 mm, n = 2 T (??): 900, 940 mm, n = 2 HF (??): 190, 200 mm, n = 2 E (??): 20, 25 mm, n = 2 WT (??): 9.9 (8.0–11.7) kg, n = 5 WT (//): 8.3 (6.6–10.0) kg, n = 10 Body measurements: Côte d’Ivoire and Liberia (O’Leary 2003) WT: Tiwai, Sierra Leone (O’Leary 2003) Key References  Dasilva 1989; Galat & Galat-Luong 1985; Korstjens 2001; Korstjens et al. 2007; McGraw et al. 2007; Oates 1994, 2011. Amanda H. Korstjens & Anh Galat-Luong

Colobus angolensis  Angola Colobus (Angola Black-and-white Colobus, Angola Pied Colobus) Fr. Colobe noir et blanc d’Angola; Ger. Angola-Mantelaffe Colobus angolensis Sclater, 1860. Proc. Zool. Soc., Lond. 1860: 245. 483 km inland from Bembe, Angola.

Taxonomy  Polytypic species. Seven subspecies: Colyn (1991) described five subspecies in the Congo Basin. Dandelot (1974) and Hull (1979) recognized a subspecies from Kenya and Tanzania. There is an unnamed subspecies in W Tanzania (Nishida et al. 1981). Subspecies are distinguished by pelage, cranial measurements (Hull 1979), habitat type and geographical distribution (Groves 2007b). Molecular data support recognition of sharpie (McDonald & Hamilton 2010). Synonyms: adolfi-friederici, benamakimae, cordieri, cottoni, langheldi, maniemae, mawambicus, nahani, palliatus, prigoginei,

ruwenzorii, sandbergi, sharpei, weynsi. Chromosome number: 2n = 44 (Dutrillaux et al. 1981, Wienberg & Stanyon 1998). Description  An arboreal, black-and-white monkey with long white cheek-hairs and white ‘epaulettes’. Sexes alike in colour. Adult / about 80% as heavy as adult ?. Crown and neck black. Face black across the orbital region and nose. Narrow line of white hairs form a ‘brow-band’ above the eyes. Ears black. Pelage under chin grizzled. Long, flowing white hairs (‘whiskers’, 6–10 cm) 103

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Peters’s Angola Colobus Colobus angolensis palliatus adult male (Southern Highlands, Tanzania).

extending from temples and cheeks, and from shoulders and upper forelimbs (‘epaulettes’, 15–30 cm long). Thumb absent. Dorsum, ventrum and flanks black; forelimbs and hindlimbs black. Tail black in basal region and mid-section, gradually lightening onto the distal region with a terminal tuft of white hairs. Ischial callosities pink, fringed with white hairs; callosities fused into a central ridge in ??. Subspecies differ in the length and extent of epaulettes, and white hair coverage on the brows, cheeks, tail and callosities. Three subspecies (angolensis, ruwenzorii and palliatus) have a white ‘pubic band’ of hair between the legs. Pubic band absent in the other four subspecies. In newborn infants the face is pink and pelage completely white. Infants’ face and pelage change colour gradually; they acquire the black-and-white pattern characteristic of adults by the age of 3.5–4.0 months (Bocian 1997). Geographic Variation  The following seven subspecies are recognized by Groves (2001, 2007b) and Grubb et al. (2003). Descriptions presented here are based on Colyn (1991) and Groves (2001): C. a. angolensis Sclater’s Angola Colobus. Synonyms: benamakimae, maniemae, sandbergi, weynsi. DR Congo, Angola and perhaps NW Zambia; Congo Basin, south and west of the Congo/Lualaba R., extending south-west through the Kasai and Kwango Basins (Colyn 1991) to the Luando R., Angola (Machado 1969). May be present in north-western tip of Mwinilunga District, Zambia (Ansell 1974). Extreme south-east record is from the Lusiji R. area (SE Baluba Province, DR Congo; Colyn 1991). White ‘whiskers’ and broad white epaulettes, forming a continuous band on each side of the body and sometimes covered by long black hairs. Narrow medial stripe of white hairs in the pubic region. Distal 30–70% of tail white. The rest of the body is black. C. a. cottoni Powell-Cotton’s Angola Colobus. Synonyms: mawambicus, nahani. DR Congo; east bank of the Congo R., extending north to the Uele R. Range delimited in the west by the Itimbiri R. basin; in the south by the Lindi R.; in the east by the forest/savanna ecotone extending from L. Albert to L. Edward (Colyn 1991). White cheek-whiskers well-developed, more so than epaulettes, with which they form a continuous narrow band on either side; no white in pubic region; distal half or so of tail greyish to greyishwhite. Colobus a. cottoni × ruwenzorii hybrids occur near the southeast limit of cottoni distribution (Colyn 1991).

a

b

c

d

e

f

Subspecies of Angola Colobus Colobus angolensis: (a) Sclater’s Angola Colobus C. a. angolensis. (b) Powell-Cotton’s Angola Colobus C. a. cottoni. (c) Cordier’s Angola Colobus C. a. cordieri. (d) Prigogine’s Angola Colobus C. a. prigoginei. (e) Rwenzori Angola Colobus C. a. ruwenzorii. (f) Peters’s Angola Colobus C. a. palliatus.

C. a. cordieri Cordier’s Angola Colobus. DR Congo. South from the Ulindi R. to the Elila R., and from the Lualaba R. east to Shabunda, Bukavu and Mwenga. Cheek whiskers poorly developed, forming a continuous band with epaulettes; no white in pubic region; tail wholly greyish except for proximal 5–8 cm. Colobus a. cordieri × ruwenzorii hybrids occur along east limit of cordieri distribution (Colyn 1991). C. a. prigoginei Prigogine’s Angola Colobus. DR Congo. Holotype from Mt Kabobo (=Misotshi-Kabogo), ca. due west of Kigoma on the west side of L. Tanganyika. Unconfirmed, but may be present between L. Tanganyika and L. Mweru (Ansell 1974). Similar to C. a. cordieri but tail yellowish-white instead of greyish; pelage long and silky. C. a. ruwenzorii Rwenzori Angola Colobus. Synonym: adolfi-friederici): Western Rift, from DR Congo and Uganda south to Rwanda, Burundi and NW Tanzania. Cheek whiskers and epaulettes forming a broad, continuous white band, sometimes overlain with long black hairs; a 6–10 cm wide band of white or greyish hairs in pubic region; distal 5–10 cm of tail greyish. C. a. palliatus Peters’s Angola Colobus. Synonyms: langheldi, sharpei. SE Kenya and Tanzania. Not in Malawi (Ansell 1974, Ansell & Dowsett 1988). Epaulettes large; white pubic band broad in ??, narrow or absent in //. Distal 30% of tail white; white band on forehead broad and continuous with full cheek-whiskers; occipital hairs lengthened; coat long, thick and soft. C. a. ssp. nov. Mahale Mountains Angola Colobus. Mahale Mts, W Tanzania. Pelage similar to that of C. a. palliatus and C. a. ruwenzorii but lacks white pubic band. Tail greyish only at the tip (Nishida et al. 1981, Groves 2001, 2007b, Grubb et al. 2003).

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Similar Species Colobus guereza. Sympatric in the N Congo Basin.White hair coverage of tail is far greater; longer epaulettes form a continuous mantle (cape) across the shoulders, flanks and back. Muscle development on head of ?? is marked, giving ‘double-humped’ appearance. Distribution  Endemic to equatorial Africa. Rainforest, Afro­ montane–Afroalpine and Coastal Forest Mosaic BZs. Forested habitats from the central Congo Basin east to the Rwenzori Mts and L. Victoria, then south to W Rwanda, W Burundi, and north-west side of L. Tanganyika. An isolated population in Mahale Mts N. P. on the east side of L. Tanganyika. From Congo/Lualaba R. and Itimbiri R., south to NW Angola and, perhaps, NW Zambia. Colyn (1991) reports a hiatus in C. angolensis distribution east of the Congo/Lualaba R. in the area between the Lindi R. and Ulindi R. Hart & Sikubwabo (1994), however, saw C. angolensis in Maiko N. P. It is, therefore, possible that the northern boundary of the hiatus lies farther south at either Maiko R. or Lowa R. Also present in the coastal forests of S Kenya and E Tanzania, through the Eastern Arc Mts and Selous G. R. to the Southern Highlands, perhaps into NE Zambia. Ansell (1974) and Ansell & Dowsett (1988) unable to substantiate reports of presence in N Malawi (e.g. Misuku Hills). Habitat  Restricted to forests and forest fragments. Across the species’ geographical distribution, mean annual rainfall ranges from ca. 1100–1800 mm; average annual minimum and maximum temperatures are ca. 11 °C and ca. 26 °C; altitude ranges from sea level in East Africa to 2415 m in Nyungwe Forest, Rwanda (Bocian 1997, Anderson et al. 2007c, Fashing et al. 2007b). Lowland subspecies of the Congo Basin (angolensis, cottoni and cordieri) inhabit evergreen and semi-deciduous forest, including swamp and seasonally flooded areas. Distribution associated with forests dominated by leguminous trees, particularly the Caesalpinioideae. Most populations of C. a. ruwenzorii inhabit montane forest of the Western Rift, although also in gallery forest on the western edge of L.Victoria. Colobus a. prigoginei and C. a. ssp. nov. in montane forest. Colobus a. palliatus in montane forest, coastal forest, coastal scrubland and mangrove. In the Ituri Forest, DR Congo, a high density of mature, broad- and deep-crowned trees, including Cynometra alexandri, Julbernardia seretii, Gilbertiodendron dewevrei, Erythrophleum suaveolens and Cassia mannii results in a relatively closedcanopy forest. Canopy height reaches 30–40 m, with emergents >40 m. Caesalpinioideae accounts for ca. 47% of sampled trees (Bocian 1997). Colobus a. cottoni prefers mature mixed forest where its preferred food trees are common, particularly C. alexandri, Celtis mildbraedii, Alstonia boonei and E. suaveolens. Monodominant stands of G. dewevrei occur throughout Ituri (Hart et al. 1989), but C. a. cottoni is uncommon in this forest type (Bocian 1997). In forest inhabited by C. a. angolensis in Salonga N. P., DR Congo, Caesalpinioideae accounts for 39% of sampled trees. Soil here is very acidic (pH = 4.13), sandy (87%) and nutrient-poor (Maisels et al. 1994). In the Diani Forest, Kenya, C. a. palliatus is common in tall (>10 m), closed-canopy coastal forest; uncommon in coastal shrub; rare in mangrove and bush-farmland. Colobus occupancy of forest fragments is determined by fragment size and degree of canopy cover. In unprotected areas beyond the Shimba Hills National Reserve groups occupy fragments as small as 1–3 ha (Anderson

Colobus angolensis

2005). Primarily dependent on indigenous tree species for food, but can survive in heavily degraded forest patches if favoured tree and shrub species are still present. Colobus a. palliatus is adaptable; in modified habitats like Diani, it has incorporated exotic tree species into the diet (e.g. Azadrachta indica, Delonix regia), and will travel through bush-farmland to gain access to relict indigenous trees in degraded cultivated areas (Anderson 2005). Abundance  Surveys for C. a. palliatus conducted in Kenya during 2001 found 55 isolated populations in coastal forest fragments. Total Kenyan population is estimated at between 3100 and 5000 individuals. Density varies widely among sites and is significantly affected by forest area, forest loss over 12 years and the availability of 14 major food tree species. The Shimba Hills National Reserve protects both the largest forest and largest C. angolensis population in Kenya; density in the reserve is estimated to be 2.9 ± 0.52 groups/ km2 or 15.3 ± 2.88 ind/km2. Density in the Diani Forest estimated to be 31 ind/km2; in the Mwache F. R., six ind/km2; colobus are absent from some forest fragments (Anderson et al. 2007c). Surveys in Tanzania from 1971–76 found 42 isolated C. a. palliatus populations (Rodgers 1981). There are at least 10,000 individuals in Udzungwa Mts, SC Tanzania (Rovero et al. 2009). Estimates of C. angolensis abundance are not available for populations in the Congo Basin or Western Rift. In the Okapi Faunal Reserve (central Ituri Forest, DR Congo) density in mature mixed forest is estimated to be 1.2 ± 0.38 groups/km2 or 16.7 ± 5.28 ind/km2; density in Gilbertiodendrondominant forest is estimated to be 1.1 ± 0.45 groups/km2 or 7.0 ± 2.88 ind/km2 (Bocian 1997). Adaptations  Diurnal and arboreal. Like other colobines, C. angolensis shows morphological and physiological adaptations to a folivorous diet; i.e. a sacculated stomach in which leaves can be retained separately for fermentation, and molars with high shearing crests that are effective in tearing leaves. 105

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Lateral and palatal views of skull of Angola Colobus Colobus angolensis adult male.

Intensive feeding bouts begin at sunrise and continue until mid- to late morning, followed by a resting period. In Ituri, C. a. cottoni begins a second series of feeding progressions in mid-afternoon, continuing to travel and feed until 17:30–18:30h, then settling into sleeping trees for the night (Bocian 1997). At Diani C. a. palliatus rests and feeds alternately from 06:00–18:30h. Resting always occurs in the primary and secondary canopy layers in particular trees within easy access to food sources (Moreno-Black & Maples 1977). Similarly, individual sleeping trees are consistently used throughout the year. Intensive periods of ‘sun-basking’ behaviour occur, particularly following feeding bouts (and rainy periods), with a plethora of resting positions observed (J. Anderson pers. obs.). In the Nyungwe F. R. (Rwanda), C. a. ruwenzorii forms unusually large groups of >300 individuals; the abundance of high quality mature leaf forage is thought to facilitate such group formation (Fimbel et al. 2001). In response to aerial predators (e.g. African Crowned Eagle Stephanoaetus coronatus) C. angolensis conceals itself in dense tree crowns, remaining motionless and silent until the predator is gone (C. Bocian pers. obs.). Foraging and Food  Folivorous. Feeds primarily on leaves and seeds, although fruit pulp, flowers and lichens are also consumed. In the Ituri Forest C. a. cottoni consumes more leaves than seeds (leaves, 51% of feeding observations; seeds, 22%; flowers, 7%; fruit pulp, 5%; lichen, 0.4%; n = 2457 observations). Preferred food items include Amphimas pterocarpoides flowers, C. mildbraedii leaves, Celtis zenkeri leaves and Lecaniodiscus cupanioides seeds. Peak seed consumption occurs in Aug and Sept (58% and 70%, respectively, of feeding observations) coinciding with high availability of C. alexandri and E. suaveolens seeds. Peak leaf consumption occurs in Nov and Mar (82% and 73%, respectively; Bocian 1997). Daily travelling distance of C. a. cottoni increases when availability of primary food is low. In this habitat C. a. cottoni roams extensively in search of food (mean daily travel distance is 983 m, range 312–1914 m, n = 52 days); cumulative home-range of the study group was still increasing in size, beyond 371 ha, after one year (Bocian 1997).

In the Salonga N. P. C. a. angolensis consumes more seeds than leaves (seeds, 50% of feeding observations; leaves, 27%; fruit, 17%; flowers, 6%; n = 486; Maisels et al. 1994). Here the forest is a mosaic of swamp, seasonally flooded and well-drained ground. Leguminous species, dominant here and in the Ituri Forest, have protein-rich seeds but poor-quality mature leaves (Maisels et al. 1994, Bocian 1997). In the Congo Basin frequently consumed food plants include C. alexandri, E. suaveolens, A. pterocarpoides, Dialium sp., Guibourtia demeusei, Angylocalyx pinnaertii, Millettia sp., Piptadeniastrum africanum, Albizia sp. (all Leguminosae), C. mildbraedii, C. zenkeri, Ongokea gore, Strombosiopsis tetrandra, Strombosia sp., Alstonia boonei, Xylopia aethiopica and Pycnanthus angolensis (Maisels et al. 1994, Bocian 1997). In Kenya C. a. palliatus is predominantly folivorous (leaves, 57%; fruit, 21%; seeds, 11%; flowers, 11%; Moreno-Black & Maples 1977). Frequently consumed plants include Adansonia digitata, Lannea welwitschii, Cussonia zimmermannii, Combretum schumannii, Drypetes spp., Trichilia emetica, Milicia excelsa, Millettia usaramensis, Zanthoxylum sp., Lecaniodiscus fraxinifolius, Lepisanthes senegalensis, Sideroxylon inerme, Grewia sp. and Ficus sp. (Lowe & Sturrock 1998, Anderson et al. 2007a). In the Nyungwe Forest one group of C. a. ruwenzorii was primarily folivorous (leaves, 66%; fruit, 17%; petioles, 6%; flowers, 5%; lichen, 5%; n = 14,259; Fimbel et al. 2001). A nearby group, however, consumed a more varied diet in which leaves (38%), lichen (32%) and seeds (20%) were all major components; other items eaten included whole fruits, petioles, bark, flowers and soil (Vedder & Fashing 2002). This population, in which groups sometimes exceed 300 individuals, relies heavily on an abundant supply of high-quality mature leaves, particularly the common terrestrial scrambler Sericostachys scandens (Fimbel et al. 2001). Home-ranges are enormous at Nyungwe, with one group occupying 26.5 km2 over a 2-year period before suddenly moving 13 km south of their former range. This ranging behaviour is unprecedented among Colobus spp. and may be linked to the need to allow time for depleted food patches to regenerate after large groups have foraged in them (Fashing et al. 2007b). In Kenya, C. a. palliatus groups move through mangrove, perennial crops and wooded shrubland to forage on indigenous food trees. Leaf buds and young leaves of Rhizophora mucronata, Heritiera littoralis and Ceriops tagal are also consumed (Anderson et al. 2007b). With the exception of C. a. ruwenzorii at Nyungwe, C. angolensis feeds mainly in the mid canopy (21–30 m high) and, to a lesser extent, at lower levels (11–20 m high) in mature mixed forest; C. a. cottoni and C. a. palliatus rarely come to the ground, and only do so to eat soil (Bocian 1997, J. Anderson pers. obs.) or to move between forest fragments. Social and Reproductive Behaviour  Social. Colobus a. cottoni in the Ituri Forest lives in groups of 6–20 individuals. In mature mixed forest mean group size is 13.9 animals; groups typically consist of 2–5 adult ??, 2–8 adult //, 0–2 subadults and 0–5 immature animals (n = 8 groups; Bocian 1997). Groups of C. a. angolensis in Salonga N. P. range in size from 3–7 individuals (n = 5 groups; Maisels et al. 1994). Groups in the Udzungwa Mts comprise 2–14 individuals (Rovero et al. 2009). Colobus a. palliatus in Kenya live in groups of 2–13 individuals (mean = 6, n = 136). Groups are typically comprised of one adult ?, two adult // and an array of subadults, juveniles and infants. Single-male groups are far more common (88% incidence) than multimale groups (11% with two

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??, 1% with three ??; n = 190; Anderson et al. 2007c). This demographic pattern may be maintained by a high degree of adult ? dispersal (solitary ? to group ratio 1 : 7). At Nyungwe, at least two groups of >300 C. a. ruwenzorii individuals have been observed (Fimbel et al. 2001, Fashing et al. 2007b). Oates (1974) reported much smaller groups of C. a. ruwenzorii in the Sango Bay Forests (Uganda): one group of at least 30 and another of at least 51 individuals; this second group was judged to be an association of three smaller groups. Nishida et al. (1981) reported a group of about 30 C. angolensis (now named ssp. nov.) in the Mahale Mts. Social bonds are strong among adult // in the same group, who commonly groom each other and rest near each other in clusters with young animals. Grooming and resting in proximity is also common among adult ?? in the same group, who appear to maintain a dominance hierarchy (Bocian 1997). In Ituri Forest encounters between two groups are common, often leading to the formation of temporary aggregations or ‘super-groups’.These associations, during which groups rest, feed and/or travel in proximity (52, n =  29). All the ?? observed from infancy to adulthood (n = 10) dispersed from their natal group. Female transfer also occurs (Saj & Sicotte 2005, Teichroeb et al. 2009). Predators, Parasites and Diseases  Leopards Panthera pardus and Lions Panthera leo prey on C. vellerosus in Comoé N. P. (Bodendorfer et al. 2006). African Crowned Eagles Stephanoaetus coronatus and Robust Chimpanzees Pan troglodytes are predators of colobus at other sites and probably also prey on C. vellerosus. At BFMS C. vellerosus reacts by grunting and crouching when large birds fly close to the canopy. Human hunting is undoubtedly the primary source of predation.

See Abundance above. Colobus vellerosus is hunted for its coat and meat. In the 1890s an estimated 190,000 skins were exported from Ghana. In the early twentieth century the trade averaged 17,000 per year (Grubb et al. 1998). Since the 1970s C. vellerosus has been protected by law in Ghana and Bénin, and partially protected in Côte d’Ivoire, Togo and Nigeria (De Klemm & Lausche 1987). However, poaching occurs and specimens are sometimes found in local markets (Côte d’Ivoire: McGraw et al. 1998, Fisher et al. 2000, Gonedelé Bi et al. 2010, 2012; Ghana: Ntiamoa-Baidu 1998; Bénin: P. Neuenschwander pers. comm.; W Nigeria: Happold 1987). Loss of habitat is the other primary threat. Forested habitats are now rare in Togo, Bénin and SW Nigeria. Wolfheim (1983) suggests that C. vellerosus may be able to adapt to low levels of logging, but a comparison of the population densities in four Forest Reserves and in Bia N. P. in Ghana found that even low level timber exploitation was associated with a reduced population density (Martin & Asibey 1979 cited in Martin 1991). Better enforcement of hunting laws, better habitat protection and more protected areas are necessary. Where local taboos against hunting C. vellerosus are effective, populations can increase. Small-scale ecotourism programmes may encourage further conservation efforts (e.g. BFMS, Ghana; Kikélé, Bénin). Outside West Africa, C. vellerosus is not reported to occur in zoos (Reichler 2001). Measurements Colobus vellerosus HB (??): 663 (600–670) mm, n = 4 HB (//): 623 (600–670) mm, n = 4 T (??): 865 (830–930) mm, n = 4 T (//): 834 (730–904) mm, n = 4 HF (??): 196 (190–210) mm, n = 4 HF (//): 183 (175–190) mm, n = 4 E (??): 33 (31–38) mm, n = 4 E (//): 35 (31–38) mm, n = 4 WT (??): 8.5 (range unknown) kg (n = 3) WT (//): 6.9 (range unknown) kg (n = 5) Body measurements: W Ghana (Jeffrey 1975) Weight: Oates et al. (1994) from BMNH and MNHN Key References  Booth 1958a; Grubb et al. 1998; Oates 2011; Oates & Trocco 1983; Saj et al. 2005.

Conservation  IUCN Category (2012): Vulnerable. CITES (2012): Appendix II.

Tania L. Saj & Pascale Sicotte

Colobus guereza  Guereza Colobus (Black-and-white Colobus, Abyssinian Colobus) Fr. Colobe guéréza; Ger. Guereza Colobus guereza Rüppell, 1835. Neue Wirbelt. Fauna Abyssin. Gehörig. Säugeth., p. 1. Damot region, Gojjam, Ethiopia.

Taxonomy  Polytypic species. Nine subspecies recognized by Rahm (1970), six by Dandelot (1974) and eight by Napier (1985), Groves (2001, 2007b) and Grubb et al. (2003). Long referred to as Colobus abyssinicus, following Oken (1816), who named it Lemur abyssinicus. In 1956, however, the International Commission on Zoological Nomenclature ruled (Opinion 417) that Oken’s name was invalid (Napier 1985). Synonyms: abyssinicus, albocaudatus,

brachychaites, caudatus, dianae, dodingae, elgonis, escherichi, gallarum, ituricus, kikuyuensis, laticeps, managaschae, matschiei, occidentalis, percivali, poliurus, roosevelti, ruppelli, rutschuricus, terrestris, thikae, uellensis. Chromosome number: 2n = 44 (Bigoni et al. 1997). Description  Large, robustly-built, arboreal colobine monkey, with striking, glossy, black-and-white pelage and a ‘roar’ loud-call. 111

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Western Guereza Colobus guereza occidentalis adult male.

Distinguished from other Colobus species by mantle (or cape) of long white hairs that extend from shoulders to flanks and across the lower back. Adult / about 68–84% as heavy as adult ?, depending on the subspecies. Lower brow, cheeks, chin and throat white, forming a circumfacial ruff. Crown, upper back, limbs, hands, feet and ventrum jet black. Tail with white tuft on tip. Extent of white on tail, length and bushiness of terminal tuft and length of mantle vary with subspecies. Sexes similar in colour, except ring of white pelage circling the ischial callosities is complete in ?? and incomplete in //. Infants have an entirely white pelage and pink skin. Adult pelage and black skin appear by 14–17 weeks. In adults crown of head has double-humped appearance resulting from muscle development, especially marked in adult ??, whose crowns are up to 1.5 times as large as those of adult //. Photographs of C. guereza from sites in Kenya and Tanzania available at: www.wildsolutions.nl Geographic Variation  The following eight subspecies are recognized by Napier (1985), Groves (2001, 2007b) and Grubb et al. (2003). Data on percentage of the tail that is white were provided by P. Grubb (pers. comm.) based on the examination of 132 specimens at the BMNH. C. g. guereza Omo River Guereza. Ethiopian Highlands west of Rift Valley, south to lowlands in the Omo Valley. Mantle hair relatively long, covering ca. 20% of tail. Tail much longer than HB: proximal part of tail grey; distal ca. 53% silvery white (S.D.=6.4, range=38–62, n=13). C. g. gallarum Djaffa Mountains Guereza. Ethiopian Highlands east of Rift Valley. Proximal part of tail black with scattered grey hairs increasing distally; distal ca. 55% white and bushy (S.D.=6.7, range=45–61, n = 5). C. g. occidentalis Western Guereza. Donga River Valley, Nigeria, south through Cameroon to NE Gabon and Congo, and east through Central African Republic to N DR Congo, SW Sudan and W Uganda. Hair of mantle and tail tip creamy-white. Tail ca. 40% longer than HB: distal ca. 40% creamy-white (range=25–51, n = 64). C. g. dodingae Dodinga Hills Guereza. Imatong Mts, SE Sudan. Hair of mantle slightly creamy. Similar in pelage and craniometrics to C. g. occidentalis, with which it was grouped by Dandelot (1974).

Tail about same length as HB: distal ca. 46% creamy-white and not very bushy (S.D.=4.5, range=40–55, n = 10). C. g. percivali Mt Uarges Guereza. Mathews Range (=Waragess =Uarges), C Kenya. Mantle hair long, creamy-white, covering 20–25% of tail. Tail longer than HB: distal ca. 72% (n = 1) white and bushy. C. g. matschiei Mau Forest Guereza. Kenya, Uganda and Tanzania, from Mt Elgon east to Rift Valley (including Kakamega Forest, Mau Forest, and forests near L. Nakuru and L. Naivasha) and south-west to Grumeti R. of western Serengeti in NW Tanzania. Tail longer than HB: proximal part black; distal ca. 47% white (S.D.=55, range=36–58, n = 16). C. g. kikuyuensis Mt Kenya Guereza. Kenya, east of Rift Valley including Mt Kenya, Aberdares Range and Ngong Hills. Mantle long and luxuriant, covering ca. 25–30% of tail. Tail relatively short, length about equal to HB: proximal part grey or black with scattered grey hairs increasing distally; white tuft very bushy. Distal ca. 78% of tail white (S.D.=3.5, range=71–83, n = 19). C. g. caudatus Mt Kilimanjaro Guereza. N Tanzania, including Mt Kilimanjaro and Mt Meru. Mantle even longer than on C. g. kikuyuensis. Male loud-call (‘roar’) higher pitched than C. g. occidentalis (Oates et al. 2000b). Proximal part of tail black with scattered grey hairs; white tuft comprising ca. 80% of tail length. Tail longer than HB: distal ca. 82% of tail white (S.D.=7.7, range=71–88, n = 4). Similar Species Colobus angolensis. Angola, Congo Basin, SW Rwanda, SW Uganda, SE Kenya and Tanzania. Lacks white mantle (veil) and welldeveloped tail tuft (Oates 1994). Distribution  Endemic to equatorial Africa. Rainforest and Afromontane–Afroalpine BZs. The most widespread of the blackand-white colobus monkeys, the Guereza occupies woodlands and

Colobus guereza

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forests from E Nigeria (ca. 10° E) across the northern fringe of the Congo Basin to eastern Africa, as far east as ca. 42° E in Ethiopia. The northern limit is ca. 14° N in Ethiopia and the southern limit is ca. 03° S in Tanzania. In western Africa the southern limit is just south of the Equator in Gabon and Congo. Guerezas occur from ca. 200 m asl in Cameroon to at least 3300 m in Ethiopia (Oates 1977b). Present from 1900–2900 m on the Aberdares Range, C Kenya (Butynski 1999), and from 1800–2900 m on Mt Kilimanjaro, N Tanzania (T. Butynski pers. comm.). A ‘mummified’ individual found at 4700 m on Mt Kenya (Young & Evans 1993), and a carcass found at 4680 m in a cave on Mt Kilimanjaro (Guest & Leedal 1954), but both records are well above the typical range for this species at these two sites. Subspecies distributions given above under Geographic Variation. Habitat  Guerezas inhabit a wide array of forest types, including lowland and medium-altitude moist forest, montane forest, swamp forest, dry forest, gallery forest and disturbed forest (Oates 1994, 2011, Fashing 2007, Fashing et al. 2012). Mean annual rainfall varies considerably across this range of habitats, from 700 mm in N Central African Republic (Fay 1985), to 1100–1200 mm in gallery forest in East Africa and Ethiopia (Oates 1977a, R. Dunbar pers. comm.), to 2220 mm in Kakamega, Kenya (Cords 1987b). Abundance  Guerezas often attain higher densities than most of the primates with which they are sympatric. Densities tend to be particularly high in small patches of forest along lakes and rivers (315 animals/km2: Bole, Ethiopia [Dunbar 1987]; 347 animals/km2: Kyambura Gorge, SW Uganda [Krüger et al. 1998]; 396 animals/ km2: L. Naivasha, Kenya [Rose 1978, M.D.]; 800 animals/km2: Murchison Falls, Uganda [Leskes & Acheson 1970]), and particularly low in large areas of undisturbed moist forest (3 animals/km2: Ituri Forest, DR Congo [Bocian 1997]; 4.5 animals/km2: Kibale Forest (Ngogo), SW Uganda [Struhsaker 1997]). Guerezas attain intermediate densities in moist forest areas that have been subjected to low to moderate levels of human disturbance (100 animals/ km2: Kibale Forest (Kanyawara) [Oates 1974]; 150–168 animals/ km2: Kakamega Forest, W Kenya [Fashing & Cords 2000, Fashing et al. 2012]; four to >10 groups/km2 in the montane forest of the Aberdares Range [Butynski 1999]). Adaptations  Diurnal and arboreal. Because they reach such high densities in many gallery forests and forest fragments, Guerezas are believed to be specially adapted to life in these forests (Oates 1977a, 1994). They thrive on the colonizing deciduous tree species and lianas characteristic of these forests, possibly because these plant species invest their energy more in rapid growth than in secondary compounds and lignin for their leaves (Oates 1977a). Even in continuous moist forests, Guerezas prefer areas of secondary growth and forest edge (Butynski 1985, Thomas 1991, Bocian 1997). For example, in the moist montane forest at Bwindi, Uganda, Guerezas are confined to the edge of the forest and appear to be absent at distances >2.8 km into the forest (Butynski 1985). Like other colobines, Guerezas are characterized by an enlarged forestomach in which microbial fermentation of food occurs (Kay & Davies 1994). They may be especially good at digesting high-fibre food items; a study by Watkins et al. (1985) found that

Lateral, palatal and dorsal views of skull of Western Guereza Colobus guereza occidentalis adult male.

captive Guerezas fed on a high-fibre diet exceeded the digestive efficiency predicted for ruminant mammals of the same body size. Their capacity for subsisting on mature leaves during times of preferred food scarcity (Oates 1977a, Fashing 2004) may explain why Guerezas are sometimes able to achieve extraordinarily high densities (e.g. Leskes & Acheson 1970, Dunbar 1987, Krüger et al. 1998). As a result of their relatively leafy diet and digestive adaptations, Guerezas also have a particularly sedentary life-style; they spend at least half of the day resting at all three sites where their activity patterns have been studied extensively (Kibale Forest, Uganda [Oates 1977a]; Ituri Forest, DR Congo [Bocian 1997]; Kakamega Forest, Kenya [Fashing 2001a]). Their tendencies to lead inactive life-styles, sunbathe in the canopy during the cool early morning and hunch over during rainstorms (Oates 1977a, Fashing 2001a) suggest that Guerezas may be adopting a strategy of behavioural thermoregulation similar to that of their West African congener King Colobus Colobus polykomos (Dasilva 1993). In many habitats Guerezas sometimes travel and feed on the ground. This behaviour is particularly noticeable in forest galleries in savanna, where they move hundreds of metres on the ground between forest patches (Oates 1977a, c, Fay 1985), but it has also been observed in moist forest habitats, where they sometimes come to the ground to consume swamp plants or soil (Oates 1978; Fashing et al. 2007a). 113

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In a craniometric study Hull (1979) found Guerezas to differ markedly from other black-and-white colobus species in their teeth, palate and jaws. For instance, Guerezas have relatively smaller incisors and longer molars than the other species, dental features that may be correlates of a more leafy diet. Foraging and Food  Folivorous. Extensive studies of Guereza diets have been conducted at four field sites (Kibale, Uganda; Ituri, DR Congo; Kakamega, Kenya; Budongo, Uganda). The results of these studies suggest that Guerezas exhibit impressive dietary flexibility. Guerezas tend towards extreme folivory at Kibale (Oates 1977a,Wasserman & Chapman 2003, Chapman et al. 2004) and Ituri (Bocian 1997), while their diets are more evenly balanced between leaves and fruit at Kakamega (Fashing 2001b) and Budongo (Plumptre 2006). Few primates are as folivorous as Guerezas at Kibale where up to 89% of the annual diet consists of leaves (Chapman et al. 2004), while at Kakamega, fruit accounts for up to 44% of the annual diet, and up to 81% of the diet in months when fruit is abundant (Fashing 2001a, b). Unlike other Colobus species (McKey 1978, Harrison 1986, Dasilva 1994, Maisels et al. 1994), Guerezas consume primarily pulpy fruits rather than seeds (Dunbar & Dunbar 1974a, Fashing 2001b; A. Plumptre pers. comm.). In the case of both leaves and fruits Guerezas tend to focus on abundant species (Oates 1977a, Fashing 2001b). Furthermore, the total number of plant species consumed annually is generally low (Ituri 31 spp. [Bocian 1997]; Kakamega >37 spp. [Fashing 2001b]; Kibale 43 spp. [Oates 1977a]). Often a single species plays a major role in the diet of Guerezas: plant parts (mostly young leaves) of Celtis gomphophylla (syn. C. durandii) (Ulmaceae) comprised 50% of the annual diet for Guerezas at Kibale (Oates 1977a) and plant parts (mostly mature leaves) of Prunus africana (Rosaceae) made up 19% of the annual diet for Guerezas at Kakamega (Fashing 2001b, 2004). In addition to being the most frequently consumed items in the annual diet of Guerezas at Kakamega, P. africana mature leaves were also the primary fallback resource for Guerezas at this site, accounting for as much as 50% of the diet during months of fruit scarcity (Fashing 2004). The chemical basis of food choice has been unusually well studied in Guerezas. Guerezas typically select food items that are high in protein, low in fibre, or both (Bocian 1997, Chapman et al. 2004, Fashing et al. 2007a). Secondary compounds also sometimes play a role in Guereza food choice, with most items high in condensed tannins tending to be avoided at Kibale (Oates et al. 1977) and Kakamega (Fashing et al. 2007a), but not at Ituri (Bocian 1997). Most minerals do not appear to strongly influence food choice, though there are several exceptions (Rode et al. 2003, Fashing et al. 2007a). Guerezas at both Kibale and Kakamega select for food items high in zinc, and engage in long journeys to access rare resources such as herbaceous swamp plants or Eucalyptus (Myrtaceae) bark that are rich in sodium (Oates 1978, Rode et al. 2003, Fashing et al. 2007a, Harris & Chapman 2007). Guerezas typically engage in several prolonged feeding bouts spaced throughout the day with particularly sharp increases in time spent feeding occurring in the late afternoon at Kibale (Oates 1977a) and Chobe, Uganda (Oates 1977a), and in the mid- to late afternoon at Ituri (Bocian 1997). Feeding bouts are generally

followed immediately by long periods of rest, which are presumed to be necessary if Guerezas are to ferment and extract nutrients from their leafy diets (Oates 1977a). In forest habitats group daily travel distances are relatively low (Kibale: mean = 535 m, range 288–1004 m, n = 60 days on one group [Oates 1977a]; Kakamega: mean = 588 m, range 166– 1360 m, n = 185 days on five groups [Fashing 2001a]; Ituri: mean = 609 m, range 268–1112 m, n = 55 days on one group [Bocian 1997]). Unlike many other primates Guerezas do not appear to substantially alter their daily travel distance in response to temporal fluctuations in food availability (Oates 1977a, Bocian 1997, Fashing 2001a, b). Instead, Guereza ranging patterns may be influenced more by the distribution of the rare, sodium-rich resources, such as herbaceous swamp plants and Eucalyptus bark, that they periodically make long journeys to access (Oates 1977a, Fashing 2001a, Fashing et al. 2007a, Harris & Chapman 2007). They have also been seen out in freshly burned grassland, apparently eating ash or charcoal (Kingdon 1971). These journeys require some groups to cover much greater distances than others depending on how far a group’s usual ranging area is from the high-sodium resources (Harris & Chapman 2007). This disparity among groups in distance to sodium-rich resources may help explain why Guereza daily path lengths and home-range sizes are not typically correlated with group size (Fashing 2001a, Fashing et al. 2007a, Harris & Chapman 2007). It is also possible, however, that the lack of a correlation between group size and ranging variables reflects an absence of scramble competition over food within most Guereza groups (Fashing 2001a). Home-range areas of groups vary widely from 1.5 ha at Murchison Falls, Uganda (n  = 1, Leskes & Acheson 1971) to 100 ha at Ituri (n = 1, Bocian 1997). Mean home-range areas at other sites include: Limuru, Kenya: 2.0 ha, n = 1 (Schenkel & SchenkelHulliger 1967); Bole, Ethiopia: 2.0 ha, range 1.4–3.6 ha, n = 10 (Dunbar 1987); Kyambura Gorge, Uganda: 3.7 ha, range 1.7– 6.2 ha, n = 24 (Krüger et al. 1998); L. Naivasha, Kenya: 4.8 ha, n = 1 (Rose 1978); L. Shalla: Ethiopia, 5.6 ha, range not reported, n = 6 (Dunbar 1987); Entebbe, Uganda: 7.5 ha, range 6.4–9.3 ha, n = 3 (Grimes 2000); Kibale: 13.7 ha, range 8.8–18.8 ha, n = 6 (Harris 2005); Budongo, Uganda: 14 ha, range 7.3–21.3, n = 25 (Suzuki 1979); Kakamega: 18 ha, range 16–20 ha, n = 2 (Fashing 2001a); Kibale: 28 ha, n = 1 (Oates 1977a). Even at sites where home-ranges are relatively large (e.g. Kakamega, Kibale, Ituri), groups tend to concentrate their activities within a smaller ‘core area’ of their range (Oates 1977a, c, Bocian 1997, Fashing 2001a, Harris 2005). At Kibale, Harris (2006a, Harris et al. 2010) found that core areas featured a greater abundance of food per unit area than other portions of her groups’ home-ranges. Comparisons across Guereza study sites suggest that home-ranges become compressed into increasingly smaller areas as population density increases (Dunbar 1987, Fashing 2001a). Range overlap between groups is often high in moist forests where densities are intermediate (Kibale: 74% overlap [Oates 1977b], 83% overlap [Harris 2005]; Kakamega: >67% overlap [Fashing 2001a]), but tends to be much less extensive in moist forests where densities are low (Ituri: 22% overlap, Bocian [1997]; Budongo, Uganda: overlap not reported, but can be inferred from ranging and density data to have been minimal [Suzuki 1979]), and in gallery forests where densities are high (Chobe, Uganda: 10% overlap [Oates 1977a]; Bole, Ethiopia:

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‘relatively little’ overlap [Dunbar & Dunbar 1974a]). The extensive range overlap at Kibale and Kakamega may be due in part to the convergence by many groups on small patches of rare resources at these sites (swamp plants and soil at Kibale, and Eucalytpus bark and soil at Kakamega) (Oates 1977c, 1978, Fashing 2001a, Fashing et al. 2007a, Dierenfeld et al. 2007). Social and Reproductive Behaviour  Social. Guerezas live in groups that typically include 1–2 adult ??, 1–6 adult // and their dependent offspring (Oates 1994, Fashing 2007). Adult ?? not belonging to bisexual groups appear to travel most often alone or in pairs, though larger all-male groups of up to four animals occur (Oates 1974, P. Fashing pers. obs.). Bisexual groups range in size from two (Marler 1969, Suzuki 1979) to 23 individuals (Fashing 1999). Mean group size tends to be larger in large forest blocks than in small fragments and gallery forests (Dunbar 1987, Onderdonk & Chapman 2000, Fashing 2007). Groups in large forest blocks are more likely to include multiple ?? (Oates 1994, Fashing 2007). The extent to which multimale groups are stable has been debated. Dunbar & Dunbar (1976) and Oates (1994) contend that multimale groups are only the temporary results of immigration and maturation within the group, while von Hippel (1996) argues that multimale groups can be stable over long periods and are, in fact, the typical social unit for Guerezas inhabiting large moist forest blocks. Long-term, intermittent, longitudinal monitoring of Guereza populations in two large moist forests suggests that the extent to which multimale groups predominate and are long-lasting varies among forests. Over a recent 28-year period at Kakamega, five of six censuses of Guereza group composition indicated that 50% or more of the groups surveyed contained multiple ?? (1980: 50%, n = 6 [Cords in Mulhern 1991]; 1990: 100%, n = 2 [Mulhern 1991]; 1992: 89%, n = 18 [von Hippel 1996]; 1997–98: 40%, n = 5 [Fashing 2001a]; 2004: 80%, n = 5; 2008: 83%, n = 6 [P. Fashing pers. obs.]). Furthermore, P. Fashing (pers. obs.) found that one recognizable adult ? at Kakamega remained subordinate in a multimale group for at least seven years, suggesting that the composition of multimale groups sometimes remains stable over long periods. On the other hand, studies over the past three decades at Kibale indicate that multimale groups are consistently less common than uni-male groups (1971–72: 14–29%, n = 7 [Oates 1977c]; 1992–93: 43%, n = 40 [Teelen 1994]; 2002–03: 17%, n = 6 [Harris 2006a]) and do not appear to be stable in composition over time (Oates 1977c). Affiliative behaviour is common while agonism is rare within Guereza groups (Leskes & Acheson 1971, Dunbar & Dunbar 1976, Oates 1977b, Struhsaker & Leland 1979, Dunbar 1987, Fashing 1999, 2001a, Harris 2005). Grooming is the most frequent affiliative behaviour among Guerezas and they spend up to 15% of their time engaged in this behaviour (Kakamega: 6% [Fashing 2001a]; Kibale: 6% [Oates 1977b], 15% [Harris 2005]). Adult // are the primary groomers in most groups at Kibale and Kakamega (Oates 1977b, Fashing 2001a, Harris 2005), although in groups where they are present, juvenile // frequently groom others at Kakamega as well (P. Fashing 2001a, pers. obs.). Adult and juvenile ?? groom others only rarely both at Kibale and Kakamega (Oates 1977c, Fashing 2001a, Harris 2005). Adult // are typically the primary recipients of grooming (Oates 1977b,

Fashing 2001a), although Harris (2005) found that adult ?? in Kibale often received more grooming than most adult //. Amongst adult // within a group, there is considerable inter-individual variation in the extents to which they groom and are groomed by others (Oates 1977b, Harris 2005, P. Fashing pers. obs.). Oates (1974) noted that the smallest adult // in his study group at Kibale received far less grooming than other adult //. This pattern was also observed in the group for which social relationships were most carefully studied at Kakamega (P. Fashing pers. obs.). Agonism is typically uncommon within Guereza groups (Kibale: one incident every 8.7 h [Oates in Struhsaker & Leland 1979]; one incident every 9.1 h [Harris 2005]; Kakamega: no incidents during 16,710 scan samples and only occasional incidents outside scan samples [Fashing 2001a]). Still, Harris (2005) found that, at Kibale, displacements amongst adult // occurred more often than expected in the context of feeding, and that // displacing others fed more often than expected in the immediate aftermath of the displacement. Harris (2005) also noted that some adult // had consistently unidirectional dominance relationships with other // in their groups. These results suggest that, despite their reliance on a highly folivorous diet, contest competition over food occurs amongst // within Guereza groups at Kibale (Harris 2005), albeit at a low rate. Relationships between Guereza groups are typically antagonistic (Oates 1977a, c, Fashing 1999, 2001c, 2007, Harris 2005, 2006b, 2010). Patterns of home-range defence vary widely across habitat types, across forests of similar habitat type, and even within individual forests over time. Defence of the entire range appears typical of Guerezas in gallery forests where ranges are small (Dunbar 1987), while groups in large moist forests, where ranges are larger, tend to focus on defending only portions of their range (Oates 1977c, Fashing 1999, 2001c, Harris 2005). Guerezas in the large moist forest at Kakamega consistently engage in site-specific home-range defence, most staunchly and successfully defending those portions of their range they occupy most often (Fashing 1999). In the large moist forest at Kibale, Oates (1977c) found that the outcomes of most encounters were also location-specific, though some encounters appeared to be decided by inter-group dominance relationships instead. In another study at Kibale 30 years later, Harris (2006b) found that inter-group dominance relationships were the decisive factor influencing the outcomes of most encounters and that her six study groups could be ordered into a linear transitive dominance hierarchy based on competitive ability during encounters. Males are the most aggressive group members during intergroup encounters, with // only occasionally playing aggressive roles (Oates 1977b, Fashing 2001c, Harris 2010). Male intergroup aggression appears related primarily to the defence of food resources, although in some instances aggression may also be related to mate guarding (i.e. direct defence of mates [Fashing 2001c, Harris 2010]). The occasional / aggression that occurs during encounters is probably related to resource defence, although during most encounters // appear to rely on ?? to do the bulk of the resource defence (Fashing 2001c, Harris 2010). Fashing (2001c, 2007) suggests that Guereza ?? may engage in inter-group resource defence as a means of indirect mate defence; // may be more likely to mate with, and less likely to transfer away from, ?? who successfully defend food sources for their group. 115

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Western Guereza Colobus guereza occidentalis.

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One of the most distinctive sounds in the forests of equatorial Africa is the loud-call of the ? Guereza. This call, termed a ‘roar’ (Schenkel & Schenkel-Hulliger 1967), can be heard as far as 1.6 km away from its source (Marler 1969). Males uttering roars often simultaneously engage in a ritualized jumping display. Roars are most often given around dawn, when they are usually contagious, with ?? from across the forest joining in once one ? begins roaring (Schel & Zuberbühler 2012). Dawn roars have been postulated to serve as inter-group spacing calls (Marler 1969, Waser 1977b) and/or as a form of male–male competition (Oates & Trocco 1983, Oates et al. 2000a, Harris et al. 2006). Roars are also sometimes given during the day when they appear to function primarily as predator alarm calls (Marler 1972, Oates 1994, Schel et al. 2009, 2010, Schel & Zuberbühler 2009). Kingdon (1971) noted roaring in response to nocturnal earthquakes and found that some groups in western Uganda called at about 03:00h with some frequency. Occasionally given at night, the function of these nocturnal roars is unclear. In a study of captive ? Guerezas, Harris et al. (2006) found that the mean formant dispersion (i.e. difference, in Hz, between frequency bands) of the roars uttered by individual ?? was significantly inversely correlated with their body mass. Harris (2006b) also reported that the mean formant dispersion of roars by ?? in the wild at Kibale could be used to predict the outcome of encounters between groups. The lower the mean formant dispersion of a male’s roars, the more likely his group was to win encounters with other groups. Guereza roars thus appear to be honest signals of body size, which may reflect ? competitive ability (Harris 2006b, Harris et al. 2006). Allomaternal behaviour is common in Guerezas with juvenile // and nulliparous adult // particularly interested in carrying the infants of other //. This behaviour has been most thoroughly investigated in captive animals (Wooldridge 1969, Emerson 1973, Horwich & Manski 1975, Horwich & Wurman 1978). At Kibale, infants are handled most by non-mothers in their first 1–2 weeks of life, when they have all-white coats and are still completely dependent on others for all locomotion (Oates 1977c). Rate of infant transfers to allomothers during this stage is ca. 3–5 incidents/h at Kibale. Infants and, to a lesser extent, their mothers sometimes attempt to resist transfers to allomothers, and infants often squeal and flail about under the care of allomothers until their mothers come to retrieve them (Oates 1977c). Adult ?? rarely engage in infant care, with all observed instances resulting from infants approaching ?? and clinging to them (Oates 1977c, P. Fashing pers. obs.). However, individual juvenile ?? occasionally seek out young infants to hold and carry, though much less frequently than // (P. Fashing pers. obs.). Most of what is known about Guereza mating behaviour comes from a recent study at Kibale (Harris & Monfort 2006). During this study, 334 solicitations for copulation were observed, of which 85% were accepted. Females and ?? played the role of solicitor almost equally often. Twenty-three per cent of copulations were harassed by other group members, most commonly subadult ??, though adult // and juveniles occasionally harassed copulations as well. When a / is in oestrus, copulatory rate can be high; one / copulated with a particular ? 29 times in 64 min (Harris & Monfort 2006). Based on this report and a smaller sample of copulatory events observed

at Kakamega, Guerezas appear to be multiple mounters (Harris & Monfort 2006, Fashing 2007). The percentage of time Guerezas spend in close proximity with other primate species (i.e. in polyspecific associations) varies across forests, though rarely reaches the frequencies observed among cercopithecines (Waser 1987, Cords 1990, Enstam & Isbell 2007). At Kakamega and Kibale, where polyspecific associations were defined as occasions when members of two species were within 50 m of one another, Guerezas spent 24% (P. Fashing pers. obs) and 40% (Harris 2005) of their time in these associations, respectively. Guerezas most often formed these associations with Blue Monkeys Cercopithecus (n.) mitis stuhlmanni at Kakamega (P. Fashing pers. obs.) and with Uganda Red Colobus Procolobus rufomitratus tephrosceles at Kibale (Harris 2005). Polyspecific associations were defined differently at Bole where they were considered to occur only when the two closest members of different species are nearer to one another than are the two most widely separated group members of the same species. By this definition, Guerezas spent 11% of their time in polyspecific associations at Bole, most often with Grivets Chlorocebus aethiops (Dunbar & Dunbar 1974a). Reproduction and Population Structure  Unlike the Olive Colobus Procolobus verus, red colobus Procolobus spp., the Angola Colobus Colobus angolensis and the Black Colobus Colobus satanas, Guereza // lack sexual swellings (Oates 1994, Bocian 1997). Ovarian cycle length, based on hormonal monitoring of three // at Kibale, is ca. 24 days (range 15–27 days; Harris 2005). Most copulations at Kibale occurred from five days before to three days after the estimated date of ovulation. In some groups at Kibale multiple // are sometimes simultaneously in oestrus (Harris & Monfort 2006). Females in captivity first give birth at 4.5–5.0 years of age after a gestation period of ca. 170 days (Rowell & Richards 1979). Gestation in the wild is ca. 152 days (range 142–161 days) based on hormonal monitoring of three // at Kibale (Harris & Monfort 2006). Only singletons have been recorded. Birth-weight averages 445 g (Harvey et al. 1987). Inter-birth intervals are ca. 17 months at Kakamega (Fashing 2002), and 22–25 months at Kibale (Oates 1977c, Harris & Monfort 2006). No birth season observed at either Kibale or Kakamega, though there was some synchrony of births within study groups at Kakamega (Oates 1977b, Fashing 1999, 2002). Rowell & Richards (1979) suggest that Guerezas breed rapidly and aseasonally because their specialized digestive system releases them from the selective pressures imposed on other monkeys by seasonal food shortages. Few data are available on ? reproductive parameters. Groups nearly always contain more adult // than adult ?? (Oates 1994, Fashing 2007). Average adult / to adult ? ratios in groups were 3.4 : 1.4 at Kibale (n = 7 groups; Oates 1977c) and 3.8 : 2.4 at Kakamega (n = 5 groups; Fashing 2007). Immature to adult / ratios in groups were 6.5 : 3.4 at Kibale (n = 7 groups; Oates 1977c) and 6.8 : 3.8 at Kakamega (n = 5 groups; Fashing 2007). Ten of 11 adult // in three closely monitored groups gave birth during a 17-month study at Kakamega (Fashing 2002). Only one of these infants disappeared during the study period, suggesting that infant survivorship is high at this site (Fashing 2002). Infant mortality attributed to falls and infanticide (Oates 1977b), though the latter has been observed only at Kibale (Onderdonk 2000, Harris 117

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Mt Kilimanjaro Guereza Colobus guereza caudatus adult male.

& Monfort 2003, Chapman & Pavelka 2005). Chapman & Pavelka (2005) suggest that infanticide risk may act as the primary constraint on group size among Guerezas at Kibale. Longevity in the wild is unknown, though Guerezas live to at least 23 years and 9 months in captivity (Jones 1982). Male Guereza emigrate from their natal groups after adolescence and // may occasionally transfer between groups (Harris et al. 2009). Bachelor ?? and, to a lesser extent, all-male groups consisting of adult and/or subadult ?? occur at Kibale and Kakamega, indicating that ?? spend considerable periods living outside bisexual groups after dispersing (Oates 1977c, Fashing 1999). An all-male group with four members was regularly observed following one of P. Fashing’s (pers. obs.) study groups at Kakamega over several weeks before eventually joining it permanently. An adult / and her small juvenile who did not belong to any of the Kakamega study groups were also observed following and occasionally approaching one of Fashing’s groups on several consecutive days but then were not seen again. Two members of another Kakamega study group, an adult ? and a large juvenile /, became increasingly peripheral to their group over several weeks before disappearing permanently. They are assumed to have transferred.There is also evidence from Kakamega that adult // take an active role in expelling other adult // from their group (P. Fashing pers. obs.). On several occasions over a 2-day period adult // cooperated in holding down an adult / group-mate while biting and hitting her until she fell to the forest floor. After the last instance of aggression from her / group-mates, the victim fled through the undergrowth and was never observed in the group again. Predators, Parasites and Diseases  The primary predator on Guerezas appears to be the African Crowned Eagle Stephanoaetus coronatus, though the intensity of Crowned Eagle predation differs widely among sites. For example, Guerezas accounted for 39% of the prey of Crowned Eagles at Kanyawara study site in Kibale Forest (Skorupa 1989). However, just 12 km away at Ngogo, Guerezas comprised only 4% of the Crowned Eagle’s diet (Mitani et al. 2001). Mitani et al. (2001) suggest that this disparity may be the result both of Guereza densities being higher at Kanyawara and inter-individual variation in hunting behaviour between Crowned Eagle pairs at the two sites. Robust Chimpanzees Pan troglodytes prey on Guerezas at both Kibale (Mitani & Watts 1999, Watts & Mitani 2002) and Budongo

(Suzuki 1975). However, the rate of chimpanzee predation at Kibale is low with Guerezas accounting for only 4% of the chimpanzee’s mammalian prey items (Watts & Mitani 2002). Leopards Panthera pardus probably also prey on Guerezas at low rates: Hart, J.A. et al. (1996) found that Guerezas and Angola Colobus combined comprised only 1% of the prey items in Leopard scats at Ituri, DR Congo; such remains could arise from Leopards scavenging African Crowned Eagle kills. Guerezas appear to use several tactics to avoid predation. For example, adult ?? give loud-calls (‘roars’) when they detect a predator. These vocalizations may help intimidate the predator and alert group-mates (Marler 1972, Schel et al. 2009, 2010). In the case of African Crowned Eagles, ? Guerezas may also use physical threats to intimidate them. P. Fashing (pers. obs.) once witnessed a ? Guereza chase off an Crowned Eagle perched quietly in the same tree as the ? and his group; the ? Guereza repeatedly raced to within 1 m of the Crowned Eagle and lunged at it. Another tactic Guerezas may use to avoid predation is to cluster together on moonlit nights, presumedly to reduce their chances of being detected. Consistent with this assertion is von Hippel’s (1998) finding that the number of sleeping trees occupied on a given night by members of a Guereza group in Kakamega Forest is significantly inversely correlated with the fullness of the moon. Lastly, aside from their loud-calls, most Guereza vocalizations are relatively quiet, a characteristic that reduces their conspicuousness to predators. Ten species of gastrointestinal parasites were present in 476 faecal samples collected from Guerezas at Kibale: Trichuris sp., Entamoeba coli, Entamoeba histolytica, Oesophagostomum sp., Strongyloides fulleborni, Ascaris sp., Colobenterobius sp., Bertiella sp., an unidentified Stronglye, and a species in the Dicrocoeliidae. Prevalence (percentage of faecal samples in which a parasite was present) exceeded 10% only for Trichuris sp., which was found in 79% of the samples (Gillespie et al. 2005b). A preliminary study of 23 Guereza faecal samples from Kakamega revealed nine species of parasites: Trichuris sp., E. coli, E. histolytica, Heterophyes sp., Fasciola sp., Schistosoma sp., an unidentified Strongyle, an unidentified hookworm and an unidentified worm. Like at Kibale, Trichuris sp. was among the most prevalent parasites and was found in 87% of samples from Kakamega. Other parasites present in at least 10% of samples from Kakamega were E. coli, E. histolytica, Heterophyes sp., Fasciola sp., the unidentified Stronglyle and the unidentified hookworm (P. Fashing, C. Ashira & I. Farah pers. obs.). Many of the parasites found among Guerezas at Kibale also occur commonly among the human population in W Uganda. However, no differences were found in parasite prevalence between Guerezas living in anthropogenically disturbed (logged) forest and those inhabiting undisturbed forest (Gillespie et al. 2005b). Still, when Chapman et al. (2005) examined the effects of immigration of Guerezas from a fragment cleared by humans into a second fragment where Guereza parasite loads were already being monitored, they found that, over the next five years, Trichuris sp. infection prevalence and intensity increased while Guereza density declined. Conservation  IUCN Category (2012): Least Concern. C. g. percivali: Endangered. C. g. gallarum, C. g. dodingae and C. g. matschiei: Data Deficient. All other subspecies: Least Concern. CITES (2012): Appendix II.

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The Guereza is one of the few primate species that generally responds well to some habitat disturbance (Fashing et al. 2012), actually attaining higher densities in logged than in undisturbed areas at Kibale (Skorupa 1986, Struhsaker 1997, Chapman et al. 2000) and Budongo (Plumptre & Reynolds 1994). However, intensive logging and forest clearance for agriculture are as much a threat to Guerezas as they are to other forest-dependent primates (Chapman et al. 2003, 2007). Measurements Colobus guereza HB (??): 615 (543–699) mm, n = 20 HB (//): 576 (521–673) mm, n = 22 T (??): 667 (521–826) mm, n = 20 T (//): 687 (528–797) mm, n = 22 Specimens in BMNH; localities not listed (Napier 1985)

Western Guereza Colobus guereza occidentalis adult male.

Guerezas have traditionally been hunted for ceremonial purposes by many African peoples, including the Kuria, Chagga, Kikuyu, Samburu and Luhya. Guerezas were also hunted heavily for their skins to supply the European fur market in the nineteenth century, and in the twentieth century to make rugs for the tourist trade (Oates 1977b). The Guereza skin trade was outlawed in Kenya and Ethiopia in the 1970s (Dunbar & Dunbar 1975a, Oates 1977b), though Guereza pelts and rugs were still found on sale illegally in an Addis Ababa souvenir shop as recently as 2003 (P. Fashing pers. obs.). Although primates are not often hunted for their meat in the African savanna zone, or in much of East Africa, Guerezas are hunted as food in the forest zone; in western equatorial forests they are threatened, along with other large forest primates, by the bushmeat trade. For instance, Fay (1985) reported that Guerezas were still abundant in gallery forests in the Manovo–Gounda–St Floris N. P. in the savanna zone of Central African Republic, while they had been nearly extirpated in the southern, forested, portion of the country. Perhaps the most threatened subspecies is C. g. percivali, which is endemic to the Mathews Range F. R. (940 km2) where this subspecies remains widespread from 1400–2000 m. Incidence of loud calls indicates that some sites support at least three groups/ km². It appears that the habitat and the primates of the Mathews Range are better protected now than in the recent past (Mwenge 2008, De Jong & Butynski 2010a).

C. g. occidentalis HB (??): 593 (535–690) mm, n = 16 HB (//): 554 (485–640) mm, n = 13 T (??): 811 (670–885) mm, n = 16 T (//): 773 (715–825) mm, n = 13 HF (??): 191 (175–207) mm, n = 16 HF (//): 179 (165–190) mm, n = 13 E (??): 44 (37–50) mm, n = 16 E (//): 40 (35–43) mm, n = 13 WT (??): 9.3 (6.8–11.3) kg, n = 46 WT (//): 7.4 (5.4–10.9) kg, n = 46 Body measurements: various localitis in E DR Congo (Allen 1925) Weight: numerous localities (Delson et al. 2000) C. g. guereza WT (??): 13.5 (12.4–14.4) kg, n = 3 WT (//): 9.2 (8.2–10.1) kg, n = 3 Specimens from Ethiopia in MNHN (J. F. Oates pers. obs.). C. g. matschiei WT (??): 9.9 (8.2–11.8) kg, n = 15 WT (//): 8.3 (6.4–10.2) kg, n = 15 Several localities (Delson et al. 2000) Key References  Fashing 2001a, c; Harris 2006a, b, 2010; Oates 1977a, c, 2011. Peter J. Fashing & John F. Oates

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Family CERCOPITHECIDAE

Genus Procolobus Olive Colobus Monkey, Red Colobus Monkeys Procolobus de Rochebrune, 1887. Faune de Sénégambie. Suppl. Vert., Mamm. 1: 95.

5 Adult and subadult // have perineal swellings that vary in size over time. There is tremendous inter-taxa variation in the maximum size of these swellings, with the largest so far recorded being found in P. badius temminckii, P. badius badius, P. preussi, P. rufomitratus oustaleti and P. gordonorum, and the smallest in P. rufomitratus tephrosceles, P. r. rufomitratus and P. kirkii. 6 Males of all ages have a perineal organ that superficially resembles the very smallest swellings of adult //. 7 Ischial callosities are separate in both sexes.

Tshuapa Red Colobus Procolobus rufomitratus tholloni adult male.

Polytypic genus endemic to the forests of tropical Africa. Two subgenera provisionally recognized (Procolobus and Piliocolobus), one species of Olive Colobus and 18 taxa of red colobus monkeys. The number of species of red colobus monkeys is controversial but six are profiled in this volume. For further details, see profiles for the subgenera Procolobus and Piliocolobus, and Struhsaker (1981b, 2010), Colyn (1991), Grubb et al. (2003), Groves (2001, 2007b), Ting (2008a, b), Cardini & Elton (2009) and Oates (2011). Recent molecular data indicate that Procolobus and Piliocolobus diverged prior to the late Miocene (6.9–6.4 mya) (Ting 2008a, b, Roos et al. 2011). If the suggested divergent time standard for genera of 6–4 mya is adopted, Piliocolobus should be considered a genus based on its divergence from Procolobus at least 6 mya (Goodman et al. 1998, Groves 2001). All members of the genus Procolobus share the following characters: 1 Four-chambered stomach. This differs from the three-chambered stomach of Colobus. All Colobinae have cellulolytic bacteria that allow consumption and digestion of large quantities of leaves and seeds. 2 A sagittal crest in most adult ??, and a larger nuchal crest in ??. 3 Enlarged supraorbital ridges. 4 Larynx reduced in size (not enormously enlarged as in Colobus), subhyoid sac absent and pterygoid fossa deepened.

Pelage colour usually includes varying amounts of reddish-brown or orange, depending on the taxon. Coat colour is often highly variable, even amongst members of the same social group. Cranial differences are considerable, and the two putative subgenera are considered by many authors (Kingdon 1997, Jablonski 1998, Groves 2001, 2005c, 2007b) to be generically distinct. In his monograph on cranial morphology,Verheyen (1962) separated the Olive Colobus Procolobus verus as a distinct genus while uniting red colobus with black-andwhite colobus in the genus Colobus. Procolobus eat relatively little animal food and rarely drink water (e.g. from tree-holes), obtaining most water from food. They are largely diurnal although some activities, such as copulation, sometimes occur at night. Their forest habitats are highly variable in rainfall and tree species composition, ranging from the dry and seasonal forests (mean annual rainfall of ca.1050 mm for P. b. temminckii at Fathala, S Senegal; Gatinot 1976) to the extremely wet forests of S Bioko I., Equatorial Guinea (ca. 10,000 mm mean annual rainfall) in the case of P. p. pennantii. Found from sea level (e.g. P. p. pennantii on Bioko I. and P. kirkii on Zanzibar [Unguja] I.) to ca. 2200 m (P. gordonorum in the Udzungwa Mts, Tanzania). Peter Grubb, Thomas T. Struhsaker & Kirstin S. Siex

Ashy Red Colobus Procolobus rufomitratus tephrosceles perineal and anal region in adult female (left) and adult male (right).

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Procolobus verus

Subgenus Procolobus Olive Colobus Monkey Procolobus de Rochebrune, 1887. Faune de Sénégambie. Suppl. Vert., Mamm. 1: 95.

Monotypic subgenus endemic to the moist forests of West Africa. Subgenus Procolobus embraces a single species, the Olive Colobus P. verus. Procolobus verus is restricted mainly to high forest in West Africa, though occurring also in some gallery forests, for example along the Benue R., Nigeria (its easternmost distribution). This is the smallest of all extant African colobines. Pelage dull olive greyish-green or olive-brown comprised of agouti-banded hairs. Procolobus verus has a swept-up crest and distinctively cow-licked hair on the crown, hairy ears, and a glans penis covered in minute papillae. Differs from the subgenus for red colobus monkeys, Piliocolobus, in numerous cranial features (Verheyen 1962, Groves 2001, Cardini & Elton 2009). Some of these are: 1 Facial skeleton not so prognathous, premaxillae vertical; supraorbital ridges thin, curved; margins of pyriform aperture sharp; an incipient anterior nasal spine; posterior palatal canals deeply sunk in fossae; wide choanae and pterygoid fossa, with flat basisphenoid floor. 2 Symphyseal foramen present in mandible. This is a rare feature in ‘higher primates’. 3 Maxillary incisors have a lingual cingulum and tubercle; lateral incisors are rather caniniform. Lower M3 have a tuberculum sextum.

4 Second and fourth fingers are remarkably shortened, and the second finger has a peculiarly claw-like nail. Subgenus Procolobus shares the following features with Colobus: shallow, wide interpterygoid fossa and other features of the basicranium, and oval orbits with thin supraorbital arches. This subgenus, however, lacks the subhyoid sac and enlarged larynx that characterize the very vocal Colobus species. No other colobines, living or fossil, have been allocated to this subgenus. Of behavioural peculiarities, mothers carrying their young in the mouth or the young clinging to the mother’s neck. These are assumed to be primitive or conservative behaviours, although these habits could have been selected through infants being consistently weak or inefficient in their grasp of the mothers’ short, slippery hair. Characteristically, Procolobus are quiet and inconspicuous, and their groups form long-term associations with those of sympatric Cercopithecus spp., especially Diana Monkey Cercopithecus (d.) diana. Other features of this subgenus are given in the profile for P. verus. Peter Grubb & Colin P. Groves

Procolobus verus  Olive Colobus (Van Beneden’s Colobus) Fr. Colobe de van Beneden; Ger. Grüner Stummelaffe Procolobus verus (van Beneden, 1838). Bull. Acad. Sci. Belles-Lettres Belg.5: 347. ‘Africa’.

Taxonomy  Monotypic species. Sometimes treated as a monotypic genus (see below), but most authors currently recognize the Olive Colobus as a monotypic subgenus within Procolobus, a genus that also contains the subgenus Piliocolobus, the red colobus monkeys (Grubb et al. 2003). Van Beneden’s original description placed the Olive Colobus in the genus Colobus, but it was allocated to its own genus, Procolobus, by de Rochebrune (1887). Pocock (1935) recognized the close affinities of the red colobus monkeys and the Olive Colobus by ‘provisionally’

assigning the red colobus monkeys to Procolobus, with verus as the type species. This arrangement has been supported by several later authors, including Kuhn (1967), Grubb et al. (2003) and Oates (2011). Others, however, see Procolobus as a monotypic genus (Dandelot 1974, Corbet & Hill 1980, Kingdon 1997, Groves 2001, 2005c, 2007b). Synonyms: chrysurus, cristatus, olivaceus. Chromosome number: not known.

Olive Colobus Procolobus verus adult male.

Geographic Variation  None recorded.

Description  Small, olive-brown, arboreal monkey. Smallest colobine monkey. Adult // same colour as adult ??. Adult // average about 91% the weight of adult ??. Head small and rounded. Face naked, dark grey. Eyes surrounded by obvious ‘spectacles’ of bare, puckered, grey skin. Ears large. Crown with short sagittal crest, which is particularly noticeable in adult ??. Thumbs extremely reduced. Hands long. Feet especially long, exceeding in length both the thigh and the crus. Detailed anatomical description given by Hill (1952). Dorsal pelage varies from light reddish-brown to dark greyish-brown, sometimes with a slight olivaceous tinge. Ventrum dull grey to whitish. Testes large, contained in a pendulous scrotum. Glans of the penis unique among anthropoids in bearing small horny spicules. Adult // have large cyclical circumvulval swellings, which reach a length of >6 cm. Perineal swellings present in juvenile ??. Infants similar to adults in colour.

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Procolobus verus

Similar Species  None within geographic range. Distribution  Endemic to West Africa. Rainforest BZ. Restricted to coastal forests from Sierra Leone eastward to just east of the Niger R. in Nigeria. Although most records are south of 08° N (Oates 1981, Wolfheim 1983, Grubb et al. 1998), the Olive Colobus occurs as far north as 09° N in the Comoé N. P., Côte d’Ivoire (Fischer et al. 2000). Recent records for areas where this monkey had not been recorded previously (Dahomey Gap of S Bénin [Oates 1996b, Campbell et al. 2004, Nobíme et al. 2011]; Niger Delta [Anadu & Oates 1988, Powell 1995]) suggest that the Olive Colobus may be more widespread than has been suspected, and that its apparent rarity may be due in part to its crypticity. Current distribution probably similar to the historical distribution, but populations are today fragmented within this range as a result of deforestation by humans. The distribution of the Olive Colobus shows remarkable general correspondence to that of another endemic West African mammal, the Pygmy Hippopotamus Choeropsis liberiensis. Habitat  Lowland moist forest, swamp forest and forest galleries in the derived savanna/dry forest zone. Most abundant in riverine forest (Oates 1981). Presence in the Niger Delta confirmed only for the seasonally flooded forest of the upper Delta (Powell 1995). In Bénin the habitat in the Lama Forest is seasonally inundated. The sacred forest where the Olive Colobus occurs at Togbota is in the lagoon of the Ouémé R. Annual rainfall (and its distribution) within the species’ range is extremely variable, from over 3000 mm with a 4-month dry season at Tiwai I., Sierra Leone, to ca. 2000 mm with a 3–4 month dry season in Taï N. P., Côte d’Ivoire, to 300 mm per year since 1979 (Galat et al. 2009). The single wet season is from mid-Jun to mid-Oct, with Aug being the wettest month (Gunderson 1977, Starin 1994, 1999). Mean relative humidity ranges from 51% (Feb) to 87% (Aug) (Gunderson 1977). Procolobus b. temminckii also in the Kilimi area (240 km², ca. 200 m asl, 09° 43´ N, 12° 32´ W), NW Sierra Leone. Here, mean daily temperature is between 21 °C and 27 °C, and temperatures range from 18 to 38 °C. Mean annual rainfall is ca. 2160 mm (Harding 1984a, b). Most populations of P. b. temminckii are found 50% reduction in the area of forest and a followed by Pterocarpus erinaceus, Ficus glumosa and Detarium senegalense. >30% decline in woody species diversity, the size of this populations A second study in Fathala Forest found that leaves are most often dropped by only 12% between 1974–76 and 2002. They attributed eaten from E. guineense, Terminalia macroptera, Dichrostachys glomerata, this survival to five major adaptive shifts, namely: (1) increased P. erinaceus and Celtis integrifolia (Galat-Luong & Galat 2005). In frugivory; (2) greater terrestriality; (3) a higher tendency to form Abuko Nature Reserve, the diet is more diverse, with the top ten, polyspecific associations with Green Monkeys Chlorocebus sebaeus; (4) top five and top one food species accounting for 61.2%, 44.1% and increased use of more open habitat; and (5) adoption of mangrove 12.6%, respectively (n = 1 group). The most common food species forest as both a refuge and source of food. in Abuko Nature Reserve include Parinari excelsa, Ficus trichopoda, D. ‘Gloger’s Rule’ states that colour tones darken with increasingly senegalense, Parkia biglobosa and Pseudospondias microcarpa. Feeding on humid environments. Both P. b. badius and P. b. waldronae live in soil from termite mounds occurs at Abuko Nature Reserve (Starin relatively tall, dense, dark primary moist forest. The colouring 1991). of P. b. badius and P. b. waldronae represents an extreme among red In Fathala Forest, Gatinot (1975) found P. b. temminckii at a mean colobus, being made up of intensely black upperparts and strongly height of 9.4 m, while Diouck (1999) found the mean height to contrasting mahogany-red cheeks, lower limbs and ventrum. The be 5.1 m during the wet season and 5.8 m during the dry season geometry of these contrasts and the intensity of fully saturated (n = 7077 records). In Abuko Nature Reserve, 61% of observations black and red pigmentation suggest intra-specific selection for (n = 99) in canopy. In Pirang Forest Park, 80% of observations strong visual emphasis of gestures and of positioning of the limbs. (n = 298) in canopy. In Taï N. P., 92% of observations (n = 1903) in The evolution, in many taxa of animals, of bright species-specific canopy (Galat-Luong 1988). See also McGraw (1998, 2007). colouring is correlated with ritualized positional behaviours and Procolobus b. temminckii in Fathala Forest, Pirang Forest Park and displays. It appears that intra-specific selection for unambiguous Abuko Nature Reserve live in a much more open habitat (i.e. dry postures and gestures (in the relatively dense and dark primary moist forest, gallery forest and woodland). The amount of time spent on forest) has been stronger in P. b badius and P. b. waldronae than has the ground varied from 1 to 4% for Fathala Forest (Diouck 1999), selection for crypsis against predators. This cannot be said for P. b. 2.4% for Pirang Forest Park (n = 298) and 15% for Abuko Nature temmincki. This subspecies has a pale grey and ochre tinted pelage Reserve (n = 99; Galat-Luong 1988, Galat-Luong & Galat 2005). At and occupies much drier, more open, lower canopy forests on Fathala Forest, groups sometimes move >2 km across open ground the north-western margins of the species’ range. Here, far better to temporarily occupy small patches of isolated forest (Galat-Luong visibility and selective pressures imposed by visual predators (e.g. 1988). African Crowned Eagle Stephanoaetis coronatus and Leopard Panthera Size of group home-ranges for P. b. temminckii was 9.0–19.7 ha pardus) are likely explanations for the ‘faded’ tints that show much (n = 7) in Fathala Forest (Gatinot 1975, Diouck et al. 1996, Galatless colour or tonal contrast. Luong & Galat 2005) and 4.3–12.8 ha in Abuko Nature Reserve (n = 3; Gunderson 1977). A later, long-term (5.5 years) study in Foraging and Food  Folivorous. Procolobus b. temminckii spends Abuko Nature Reserve found group home-ranges of 11–34 ha ca. 21% of time feeding, although this varies on a monthly basis (mean=22 ha, n = 3). The main study group had a home-range of (range 13.8–34.7%) (Starin 1991). Fruits and seeds comprise the 34 ha, of which >60% was shared with two other groups. A second

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Procolobus badius

group, with a home-range of 11 ha, shared >62% of its home-range with other groups (Starin 1991, 1994). Home-range size for one group of P. b. badius in Taï Forest was 100 ha (Galat & Galat-Luong 1985). See also Korstjens et al. (2007).

group with at least one fellow natal group mate. In contrast, six of seven subadult ?? in the focal group were aggressively forced out of the group. All six spent time as ‘adolescent exiles’ and four, perhaps five, returned to their natal group once a resident adult ? died or disappeared. Males prefer to rejoin their natal group, probably Social and Reproductive Behaviour  Social. Live in because joining a ‘strange’ group can be fatal. Two ?? were killed, multimale-multifemale groups. Mean size of P. b. badius groups in and another two ?? were probably killed, while attempting to join Taï Forest was 36.8 (8–70, n=17); Galat & Galat-Luong 1985), an alien group. Both of the attacks that led to killings were initiated but groups of >90 animals occur (Korstjens et al. 2007). Groups and maintained by the resident adult //, and the killings were, in of 20–>60 present in Gola F. R., Sierra Leone (Davies 1987). each case, conducted by a single adult ? and multiple adult //. In Groups of >100 in Sierra Leone up to the 1950s (Grubb et al. addition, six solitary ‘alien’ ?? were chased from the focal group. 1998). Mean size of P. b. temminckii groups in Fathala Forest was In all instances the initial aggressive response was by immature // 29 (14–62, n = 22) in 1973 (Gatinot 1975), 18 (9–38, n = 14) and immature ?? screaming, or by adult // screaming and/or in 1990–94 and 16 in 1996–2002 (Galat-Luong & Galat 2005). In chasing the alien ?. Exiled ?? lived alone, with an older ?, with Abuko Nature Reserve, mean group size was 34 (24–40, n = 3) a /, or with a natal group ? for >1–26 months before joining a in one study (Gunderson 1977). A later study found mean group group (n = 7). size at Abuko Nature Reserve to be 23 (14–32, n  = 5; Starin 1991, The great majority of copulations with fully swollen // are 1994). Mean size of three groups in the Pirang Forest Park was 18 performed by one ?. These ‘chief copulators’, however, usually (17–20). All eight groups observed in Cantanhez Forest comprised change from breeding season to breeding season (Starin 1994). >25 individuals (Gippoliti & Dell’Omo 1996). Mean size of five Group composition varies over the short term with the formation, groups in Kilimi area was 7.5, with the largest group comprising by adult //, of subunites, indicating a fission-fusion sociality 20 individuals (Harding 1984a, b). Solitary individuals reported (Gunderson 1977, Starin 1991, 1994, Diouck et al. 1996, Galatin Abuko Nature Reserve, Fathala Forest, Cantanhez Forest and Luong & Galat 2005). Territorial behaviour not observed although Kilimi area (Harding 1984, Starin 1994, Gippoliti & Dell’Omo aggressive encounters between groups occur. Adult ?? and adult 1996, Galat-Luong & Galat 2005). // both participate in these aggressive inter-group encounters In Abuko Nature Reserve, groups of P. b. temminckii contain 1–5 (Starin 1991, 1994, Galat-Luong & Galat 2005). For further detail adult ?? and 9–14 adult // plus young (Starin 1991, 1994). on social and reproductive behaviour see Gatinot (1977), Starin Group adult sex ratio varies from 2.0 to 7.0 / : ? (n = 16; Gatinot (1991, 1994, 2001) and Galat-Luong & Galat (2005). 1977, Starin 1991). No apparent bias in infant sex ratio (n = 28 From 1990–2002, Galat-Luong & Galat (2005) found P. b. temminckii infants; Starin 1991). In Taï Forest, one group of 32 P. b. badius had groups in Fathala Forest to be in polyspecific associations during three adult ?? and 13 adult //, while a group of 37 had about 35.7% of 171 encounters; 10.5% of these associations were with Patas nine adult ?? and ten adult //. Mean number of adult // per Monkeys Erythrocebus patas and 89.5% were with C. sabaeus. All three adult ? was 3.3 (n = 6 groups). Mean number of immatures per species were in association on one occasion. Pourrut et al. (1996), adult was 0.7 (n = 10; Galat-Luong & Galat 2005). during 114 encounters with groups of P. b. temminckii in Fathala Forest, Procolobus b. temminckii spend ca. 52% of the time resting, 21% found P. b. temminckii + C. sabaeus 39% of the time, and P. b. temminckii + feeding, 13% moving, 7% playing and 6% grooming (n = 1 group; C. sabaeus + E. patas 6% of the time. No observations were made of P. b. Starin 1991). Time spent in resting and feeding varies more temminckii + C. patas only. Diouck (1999) encountered 64 polyspecific among individuals than among age-sex classes. Adult // are the associations at Fathala Forest. Of these, 95% were of P. b. temminckii predominant groomers and adult ?? are the main recipients of + C. sabaeus, 3% were of P. b. temminckii + E. patas and 2% were of grooming. Play is conducted mainly by infants and juveniles, mostly all three species. In Kilimi area, P. b. temminckii were consistently in the trees (only ca. 1% of play occurs on the ground). Infant associated with King Colobus Colobus polykomos (Harding 1984a). In ?? play more than do infant //; conversely juvenile, subadult Taï Forest, P. b. badius groups in polyspecific associations during 87% and adult // play more than do ?? of the same age categories of 67 encounters; most frequently with Diana Monkey Cercopithecus (Starin 1991). See McGraw (1996, 2007a) and McGraw & Sciulli (d.) diana (55% of encounters), followed by Lesser Spot-nosed (2011) for activity budget and positional behaviour of P. b. badius in Monkey Cercopithecus (c.) petauristia (43%) and Campbell’s Monkey Taï Forest. Cercopithecus (m.) campbelli (31%) (Galat & Galat-Luong 1985). See Procolobus b. temminckii subadult ?? and (surprisingly) subadult also McGraw et al. (2007). // both move between groups. During one long-term (5.5 years) Procolobus badius has a distinctive vocal repertoire (Struhsaker study at Abuko Nature Reserve, 12 subadult // permanently 1975, 1981b, 2010). Procolobus b. temminckii give the following calls: emigrated from their natal group, ten subadult // permanently ‘chirp’, ‘nyow (bark)’, ‘yelp’, ‘squeal (scream)’, ‘sneeze (cough)’, immigrated, and six subadult // temporarily moved into or ‘sqwack’, ‘rraugh’, ‘whine’, ‘quaver’, ‘wa-ah!’, ‘wa!’, ‘woo’, ‘ack’, out of the focal group (Starin 1991, 1994). Movement of // ‘eh!’ and ‘copulation quavers’, most of which are shared with P. b. appears to be voluntary and not the result of overt competition and badius. The vocal repertoires of P. b. temminckii and P. b. badius do, aggression. Their transfer is immediate and with little aggression. however, differ somewhat. For example, the ‘wa-ah’ and ‘whine’ of Of the 11 subadult // who left the focal group, eight travelled in P. b. temminckii are not known to be given by P. b. badius (Struhsaker the immediate company of age mates; not spending time as solitary 1975, 2010, Starin 1991, Galat-Luong & Galat 2005). The ‘chist’ and or extra-group //. Ten of these 11 // eventually ended up in a ‘wheet’ are notably absent from the vocal repertoire of P. badius. See 131

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Predators, Parasites and Diseases  Four percent of 215 Leopard scats in Taï N. P. held P. b. badius (Hoppe-Dominik 1984). In another study, 10% of 215 scats held P. b. badius (Zuberbühler & Jenny 2007). Here, 80% of the prey of Robust Chimpanzees Pan troglodytes were P. b. badius (Boesch & Boesch-Achermann 2000; see also Bshary 2007). P. troglodytes kill ca. 3–4% of this population each year (Shultz et al. 2004). Predation by African Crowned Eagles on P. b. badius is well documented for Taï N. P. (Shultz 2001, McGraw et al. 2006a, Shultz & Thomsett 2007). Shultz et al. (2004) estimate that 8% of the P. b. badius in Taï N. P. are killed each year by the above-mentioned three predators. Humans are, however, the primary predator (Koné Temminck’s Red Colobus Procolobus badius temminckii adult female (left) and Bay Colobus Procolobus badius badius adult male (right). & Refisch 2007, McGraw et al. 2007; see Conservation section). In Abuko Nature Reserve, from 1978–1983, Nile Crocodile Crocodylus Struhsaker (1975, 1981b, 2010) and Starin (1991) for information niloticus and Central African Rock Python Python sebae account for on the circumstances and functions of some of these vocalizations. 40% of known deaths of P. b. temminckii; two young adult ?? killed by C. niloticus and two adult // killed by Python sebae. In addition, Reproduction and Population Structure  Male P. b. two adult // appeared to have died of snakebite. Python sebae is temminckii in Abuko Nature Reserve begin reproducing at ca. 28 thought to be the most important predator for P. b. temminckii at this months (range 26–30, n = 4). Females begin reproducing at ca. 34 site (Starin, 1989, 1991, 1992). months (range 30.8–38.8, n = 4), with the first infant born at ca. The following parasites were found in 57 P. b. temminckii faecal 50 months (range 24–60, n = 4). Mean inter-birth interval is 29.4 samples at Fathala Forest: strongyles (present in 38.1% of faecal months (range 27.8–32.0, n = 4). Adult // exhibit large sexual samples), strongyloides (5.0%) and amoeba (1.4%). There was no (perineal) swellings during which mating and conception occur. Full evidence for ascaris or trichurus. Procolobus b. temminckii living in core swelling lasts 4–8 days (mean = 5.4 days, median = 5 days, n = 23). gallery forests (where they do not need to move on the ground and Mean length of gestation is about 173 days (n = 2). Pregnant // where human presence is less frequent) had a much lower incidence do not appear to avoid strenuous exercise or stressful situations. Up of infection (i.e. at least one of the above-listed parasites was present until the time of birth they take part in intense inter-group chases, in 4.3% of 24 faecal samples) than those living in more open habitats attacks, and fights with alien (intruder) ??. Eight of nine infants at and where human presence is frequent (e.g. forest boundaries Abuko Nature Reserve were born during the night or early morning and near camps where at least one of the above-listed parasites (19:00–07:00h), while only one was born during the daylight hours was present in 37.5% of 33 faecal samples). Whitish individuals, (sometime between 07:45 and 13:00h). Six of seven nulliparous // and individuals with areas lacking hair, observed near the largest left the group for a period of 1–9 days after giving birth. In contrast, neighbouring village. This may be the result of severe parasitism or none of the seven multiparous // left the group just before or after of inadequate intake of at least one nutrient (A. Galat-Luong & G. giving birth. Neonates are licked clean and the placenta is probably Galat pers. comm.). eaten by the mother immediately after being expelled (Starin 1988, In Abuko Nature Reserve, ulcers on the penis, scrotum and groin 1991). observed on all P. b. temminckii breeding ?? (and on some subadult The majority of conceptions in Abuko Nature Reserve take place ??), and external mouth ulcers seen on at least five juvenile // during times of high precipitation and humidity, rising temperatures, (Starin 2004). Mouth ulcers also reported for P. b. temminckii in increasing day length, and when diets are rich in fruit and flowers. Fathala Forest (A. Galat-Luong & G. Galat pers. comm., E. Starin Births are seasonal, occurring primarily during the dry season. pers. comm). Mouth ulcers on // and genital ulcers on ?? There is considerable intra-group synchrony in the time of births. present at Bijilo Forest Park, Kiang West N. P. and River Gambia N. Infant mortality is high (ca. 21%) during the first five months of life P., Gambia (E. Starin pers. comm.) (n = 28). After the first five months, mortality for ?? was 0% up until their third or fourth year, and mortality for // was 0% well into Conservation  IUCN Category(2012): Endangered as P. badius, adulthood. These data agree with data collected elsewhere in Abuko P. b. badius and P. b. temminckii. Critically Endangered as P. b. waldronae. Nature Reserve; of the 13 non-focal group deaths, the majority were CITES (2012): Appendix II. young ??.There is strong indirect evidence for infanticide (dead Numbers of all three subspecies have declined thoughout the infants with canine puncture wounds). In one group, of six infants range in recent decades, but details on population size and extent of below the age of six months that died or disappeared, two (perhaps decline are lacking for most sites (Wolfheim 1983, Lee et al. 1988). three) were the victims of infanticide. Live to at least 16 years in the Details on the distribution of P. b. temminckii at the north end of the wild (Starin 1991, 1994). range provided by Galat et al. (2009), along with the reasons for the Male P. b. temminckii are multiple mounters. Although the decline of this species in this region. Surviving populations are widely majority of // mate with many ??, including ?? from other scattered and isolated. Procolobus b. badius and P. b. waldronae appear to groups, they prefer the dominant ? (who receives the most sexual be particularly sensitive to habitat degradation and fragmentation. advances and the least rejections). Masturbation uncommon but Like all Procolobus spp., P. badius is extremely vulnerable to hunting observed both among ?? and // at Abuko Nature Reserve (Davies 1987, Lee et al. 1988, Starin 1989, Grubb et al. 1998, (Starin 2004). Struhsaker 1999, 2005, 2010, Oates et al. 2000a, McGraw & Oates 132

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2002, 2007, N’Goran et al. 2012). This is because Procolobus spp. are (1) large and, therefore, provide much meat for the cost of a shotgun shell, (2) conspicuous as they are brightly coloured, noisy and live in large groups, and (3) they are often slow to detect danger or to flee from dangers (Davies 1987). Survival of the westernmost population of P. b. temminckii in the Fathala Forest and Abuko Nature Reserve illustrates that some populations have the capacity to adapt their behaviour to limited levels of habitat change (see Galat-Luong & Galat 2005, Galat et al. 2009, and Adaptations section). The extinction, or near extinction, of P. b. waldronae illustrates how vulnerable all red colobus species are in countries that exert little or no control over bushmeat hunting and the destruction of forest (Oates et al. 1997, McGraw 1998d, 2005, McGraw et al. 1998b). The known range of P. b. waldronae in Ghana has been searched since 1993, but no living animals have been found. Although the search continues, the last material evidence for the existence of P. b. waldronae in Ghana was obtained in 1972 in the form of a skin (Struhsaker & Oates 1995, Oates et al. 1997, Oates 2006). In early 2002, another hunter’s skin raised hopes that a population of P. b. waldronae might still survive in or near the Ehy (=Tanoé) Forest (300 km2), extreme SE Côte d’Ivoire (McGraw & Oates 2002, 2007). Subsequent surveys, however, failed to find any evidence that P. b. waldronae is not extinct (Koné 2004, Koné & Akpatou 2005, McGraw 2005, Koné et al. 2007a, b, Oates 2011, Gonedelé Bi et al. 2012). The Ehy Forest seems to be the only place where a small population of P. b. waldronae might survive, but this forest is being logged, cleared for oil palm plantations, and heavily hunted by Ivorian and Ghanaian hunters. An urgent survey of the Ehy Forest has been called for. If extinct, P. b. waldronae is ‘the first recorded extinction of a widely recognized primate taxon in the twentieth century, and human hunting rather than habitat loss has almost certainly been the primary cause of the monkey’s extinction’ (Oates et al. 2000a, p. 1530). At least seven species of threatened primates occur in the same forests as P. badius. These include White-thighed Colobus Colobus vellerosus (Vulnerable), Roloway Monkey Cercopithecus (d.) roloway (Critically Endangered), White-naped Mangabey Cercocebus lunulatus (Critically Endangered) and Robust Chimpanzee Pan troglodytes (Endangered) (Gonedelé Bi et al. 2012). All of these species would benefit from actions taken to ensure the survival of P. badius, especially the protection of habitat and the strict enforcement of hunting laws. Development and effective implementation of a ‘Red Colobus Action Plan’ should have a high conservation priority (Oates 1996a, Oates et al. 2000a, McGraw & Oates 2002, 2007). Some of the most important sites for the survival of P. badius are: P. b. temminckii: Niokolo Koba N. P. (8175 km²), Fathala Forest (76 km²) in Saloum Delta N. P., Forêt Classée de Patako (55.8 km²), Forêt Classée de Sangako (21.4 km²) and Basse Casamance N. P. (5.0 km²), Senegal; Kiang West N. P. (110 km²), Bama Kuno Forest Park (9.3 km²), River Gambia N. P. (= Baboon I.) (5.8 km²), Katilenge (= Kahlenge) Forest Park (3.2 km²), Abuko Nature Reserve (1.1 km²), Pirang Forest Park (0.6 km²) and Bijilo Forest Park (0.5 km²), Gambia; Basin of the Tombali, Cumbija and Cacine Rivers, including the Cantanhez Forest (650 km²), Guinea Bissau. Details on the distribution and conservation status of P. b. temminckii in Senegal and Gambia are given in Galat et al. (2009), along with the reasons for the decline of the populations of P. b. temminckii in this region.

P. b. badius: Taï N. P. (3400 km²) Côte d’Ivoire; Grebo National Forest (2603 km²), Sapo N. P. (1308 km²), North Lorma National Forest (712 km²), Liberia; Gola Forest (748 km²), Loma Mountains Non-hunting Forest Reserve (332 km²; now under consideration for national park status) and Tiwai I. (12 km²), Sierra Leone; Réserve Naturelle Intégrale des Monts Nimba (= Nimba UNESCO Man and Biosphere Reserve) (218 km²), Guinea. P. b. waldronae: Tanoé Swamps Forest (= ‘Ehy Forest and vicinity’; ca. 300 km²), Côte d’Ivoire. This is thought to be the only site in which this subspecies might still exist. The conservation of this site is of particular concern at this time as there are plans to cut this forest in order to establish an oil palm plantation. Important populations of C. lunulatus and C. (d) roloway also here. See: http://www.manifestefmt.org/ Measurements Procolobus badius P. b. badius HB (??): 611 (584–627) mm, n = 3 HB (//): 562 (500–635) mm, n = 6 T (??): 676 (635–706) mm, n = 3 T (//): 715 (630–800) mm, n = 6 HF (??): 159 (152–173) mm, n = 3 HF (//): 175 (165–185) mm, n = 6 E (??): 29 (25–33) mm, n = 3 E (//): 31 (27–34) mm, n = 6 WT: (??): 8.4 (6.4–9.6) kg, n = 17 WT: (//): 7.8 (5.0–10.0) kg, n = 37 GLS (??): 105.0 (100–106) mm, n = 5 GLS (//): 98.0 (93–105) mm, n = 10 GWS (??): 78.3 (74–82) mm, n = 4 GWS (//): 72.7 (70–75) mm, n = 9 Linear measurements from Verheyen (1962), Allen (1925) and BMNH WT from Delson et al. (2000) P. b. temminckii HB (/): 522 mm, n = 1 T (/): 730 mm, n = 1 HF (/): 166 mm, n = 1 E (/): 35 mm, n = 1 WT: n. d. GLS (??): 99, 101 mm, n = 2 GLS (//): 93.4 (88–103) mm, n = 5 GWS (?): 77 mm, n = 1 GWS (//): 68.5 (66–71) mm, n = 5 Verheyen (1962), Allen (1925) and BMNH P. b. waldronae HB (??): 499 (435–570) mm, n = 8 HB (//): 496 (415–565) mm, n = 8 T (??): 603 (500–686) mm, n = 8 T (//): 555 (515–750) mm, n = 8 HF (??): 162 (150–174) mm, n = 8 HF (//): 164 (146–175) mm, n = 8 E (??): 29 (20–38) mm, n = 8 E (//): 30 (27–34) mm, n = 8 133

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WT: (??): 6.4 (6.3–6.5) kg, n = 2 WT: (//): 5.8 (5.5–6.0) kg, n = 2 GLS (??): 101 (92–109) mm, n = 8 GLS (//): 95.3 (92–101) mm, n = 15 GWS (??): 79.5 (72–86) mm, n = 8 GWS (//): 71.2 (67–73) mm, n = 15 Linear measurements from Verheyen (1962), Allen (1925) and BMNH WT from Delson et al. (2000)

Key References  Galat & Galat-Luong 1985; Galat et al. 2009; Galat-Luong & Galat 2005; Gatinot 1977; McGraw et al. 2007; McGraw & Sciulli 2011; Oates 2011; Starin 1991, 1994; Struhsaker 2010. Thomas M. Butynski, Peter Grubb & Jonathan Kingdon

Procolobus preussi  Preuss’s Red Colobus Fr. Colobe bai de Preuss; Ger. Preuss-Stummelaffe Procolobus preussi (Matschie, 1900). Sitzb. Ges. Naturf. Fr. Berlin, p. 183. Barombi, Elephant L., N Cameroon.

recognized geographic barriers to primate distribution (e.g. major rivers). Moreover, the geographic range of preussi lies relatively close to, and between, the ranges of the Bioko Red Colobus P. p. pennantii and the Niger Delta Red Colobus P. p. epieni. As such, Grubb et al. (2003) provisionally include preussi as a subspecies of P. pennantii. This is referred to as the ‘Western Assemblage of Red Colobus’ or ‘Procolobus pennantii-Subgroup’. This close relationship is supported by molecular data, which place P. preussi closest to P. p. pennantii with a divergence time of 0.3 mya (Ting 2008a, b). A close relationship between P. preussi and P. pennantii is, however, not supported by the data on vocalizations. The vocal repertoire of preussi is distinct but with closest affinity with P. badius (Struhsaker 1981b). Vocal repertoire of P. preussi overlaps the vocal repertoires of P. b. badius and P. b. temminckii by 58%, and that of P. p. pennantii by only 32% (Struhsaker 2010). Dandelot (1974) viewed the differences among preussi, badius and pennantii as species-level differences and concluded that preussi is a full species. This was followed by Groves (1993, 2001, 2005c, 2007b), Kingdon (1997), Cardini & Elton (2009), Struhsaker (2010) and Oates (2011), and is the taxonomy used here. This very localized form might represent a stabilized hybrid that arose in the contact zone between more westerly and easterly parent populations. Chromosome number: not known.

Preuss’s Red Colobus Procolobus preussi adult female.

Taxonomy  Monotypic species. Taxonomic history of P. preussi summarized by Grubb et al. (2003) and Ting (2008b). Cranium distinct (Groves 2001, Cardini & Elton 2009). Based on morphological and phenotypic characters, Schwarz (1928a), Allen (1939), Rahm (1970), Napier (1985) and Grubb (1990) treat preussi as a subspecies of P. badius. There are, however, some phenotypic characters (e.g. pale inner limbs and ventrum, agouti-speckled dorsum) that suggest affinity to Pennant’s Red Colobus Procolobus pennantii. In addition, the geographic range of preussi is >1000 km from the nearest population of P. badius and the region in between holds several well-

Description  Medium-sized arboreal monkey with orangerufous cheeks, limbs and tail. As far as is known, colouration of adult ? like adult /. The few body measurement data available suggest that there is little, if any, sexual dimorphism, except that the adult ? appears to be slightly more robust than the adult /. Face quite flat, dark grey with pink margins around mouth and nose. Nostrils ‘swollen’ at base like P. badius. Fur dense, more frizzy than other red colobus species. Cheeks and sides of neck orange-rufous. Brow to ears and upper cheeks black. A whorl above brows, but no whorls above ears. Crown and temples with longish pelage that is swept back to cover ears. Crown, nape, shoulders, back, rump and base of tail blackish, blackish-grey, or greyish-brown with fawn or deep red bands or tips to hairs (i.e. agouti-speckled). Dorsum may become greyer posteriorly. Flanks and limbs orange-rufous or sandy, becoming dark brown-black on hands with tendency for digits to be black. Limbs white on inner surface. Ventrum pinkishbuff or pale red-gold, this colour going narrowly up throat to chin. Tail all rusty; sometimes sandy or reddish with brown-black, light grey, or blond over distal ca. 25%. Perineal organ of adult ? not

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conspicuous. Adult / has prominent clitoris and very large, pink, sexual swelling (Struhsaker 1975). Neonate black above, light grey below. Vocally distinct (Struhsaker 1981b). Geographic Variation  None, but individual variation exists in the intensity and extent of orange and red. Similar Species  Sympatric monkeys are unlikely to be confused with this colobine species. Cercopithecus (c.) erythrotis. Sympatric. Reddish nose and ears. No red, rufous or orange on limbs. Distribution  Endemic to a small region between Cross R. in extreme SE Nigeria south-eastward to Sanaga R. in SW Cameroon (Eisentraut 1973, Napier 1985, Lee et al. 1988, Oates 1996a, Grubb et al. 2000, Dowsett-Lemaire & Dowsett 2001, Oates et al. 2004). Rainforest BZ. In 1988 and 1999 observed north-east of Ekonganaku (05° 04´ N, 08° 39´ E) in the Ikpan Block of the Oban Division (2800 km²) of Cross River N. P., Nigeria (Oates 1996a, Grubb & Powell 1999, Grubb et al. 2000). In 1977 thought to be confined in Cameroon to the region along the border with Nigeria; south of the Ikon-Mamfe Road (04° 24´ to 05° 36´ N, 08° 48´ to 09° 20´ E) in an area of ca. 7200 km² (S. Gartlan pers. comm. to Lee et al. 1988). Within this area, confirmed only for Korup N. P. (04° 53´ to 05° 28´ N, 08° 42´ to 09° 16´ E; 1260 km²) at this time but in 1977 present in Ejagham Council F. R. (749 km²) off the north boundary of Korup N. P. (S. Gartlan pers. comm. to Lee et al. 1988). Procolobus preussi last reported in this forest in 1996 (Usongo 1996). About 80 specimens collected in Yabassi District and Ndokfass District, S Cameroon, by P. C. M. Merfield in 1939 (Napier 1985). In 2001 observed in the Ndokbou Forest (>1000 km²) and Ebo Forest (1400 km²; 04° 30´ N, 10° 30´ E),Yabassi region, just to the north of the Sanaga R. South-east limit probably near Ebo (04° 10´ N, 10° 16´ E. Also near Toumbassala, south-east of Mt Nlonako (Dowsett-Lemaire & Dowsett 2001, F. Dowsett-Lemaire pers. comm.). Reported to be in the Bakossi Mts and in Banyang Mbo during the 1990s (I. Faucher pers. comm. to F. Dowsett-Lemaire). This species probably widespread from the Cross R. to Ebo in the recent past. It is somewhat surprising that P. preussi does not occur on the foothills of Mt Cameroon, especially given the proximity of C. pennantii on Bioko I. to the west. Habitat  Coastal lowland forest and mid-altitude forest (Lee et al. 1988, Dowsett-Lemaire & Dowsett 2001, Oates et al. 2004). Appears to prefer primary forest and old secondary forest (Usongo & Amubode 2001, Linder 2008). Lowest known altitude is roughly 50 m (J. Linder pers. comm.). Maximum altitude reported for P. preussi is ca. 1000 m (Ebo Forest at southern end of range; F. Dowsett-Lemaire pers. comm.). Although Korup N. P. ranges from near sea level to 1079 m (Mt Yuhan), P. preussi not known to occur below 50 m or above 300 m (in north-east Korup N. P.; J. Linder pers. comm.). Dominant plant family at Korup N. P. is Leguminosae (especially the subfamily Caesalpiniaceae). Other major families are Annonaceae, Euphorbiaceae, Rubiaceae, Scytopetalaceae, Myristicaceae, Olacaceae, Verbenaceae and Sterculiaceae (Gartlan et al. 1986, Linder 2008). One major refuge for P. preussi is Korup N. P. where 1700 plant species have been recorded. Nearly 500 tree

Procolobus preussi

species have been recorded for south Korup N. P. The structure of the tree community at some sites in Korup N. P. that are occupied by P. preussi is described in detail by Linder (2008). Procolobus preussi lives in one of the wettest areas of Africa; rainfall >500 mm during most months at some sites (Gartlan & Struhsaker 1972, Struhsaker 1975, Sarmiento & Oates 2000). Mean annual rainfall at south end of Korup N. P. is ca. 5460 mm and mean annual rainfall at north end of Korup N. P. is ca. 2700 mm, about one-third of which falls in Jul and Aug (Gartlan et al. 1986, Linder 2008). Over the historic range of P. preussi there is a short dry season during Dec–Feb. In this region humidity is usually above 90% and temperatures range from 15 to 33 °C. In south Korup N. P., monthly temperature ranges from a mean minimum of 23.7 °C to a mean maximum of 30.2 °C (Gartlan et al. 1986). August is the coolest month and Feb is the hottest month. Abundance  Gartlan & Agland (1980) estimated that fewer than 8000 P. preussi survived in 1980. Oates (1996a) estimated that 10,000–15,000 were present in Korup N. P. in 1996. No estimates exist for theYabassi region, but it is said to be ‘widespread’ (DowsettLemaire & Dowsett 2001: 5). British museums hold at least 80 P. preussi specimens collected from the Yabassi region in 1939 alone. This strongly suggests that P. preussi was once common in this region (Napier 1985). In 1970, T. Struhsaker (pers. comm. in Linder 2008) encountered 0.15 groups of P. preussi/h in south Korup N. P., making this one of the most frequently recorded species of primate in this region. In Korup N. P., in 2004–05, Linder (2008) encountered 0.04 groups/km during 352 km of census. In south Korup N. P., Dunn & Okon (2003) encountered 0.06 groups/km in 2001–03 during 420 km of census, while Linder (2008) encountered 0.05 groups/ km during 243 km of census here in 2004–05. In north Korup N. P., Edwards (1992) encountered 0.07 groups/km in 1990 during 74 km of census. She estimated 0.52 groups/km2 (quadrat method) and 0.56 groups/km2 (line transect method), or 26–28 individuals/ 135

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km2. In this same region, Linder (2008) encountered 0.05 groups/ km during 74 km of census in 2004–05 and estimated 0.46 groups/ km² and 23 individuals/km² (line transect method). Adaptations  Diurnal and arboreal. The colouring of P. b. badius, which has some resemblances with that of P. preussi, is discussed in the profile of that species and the point is made that strong colour contrasts can serve intra-specific communication. Red, especially, acts as a strong contrast with green vegetation (Sumner & Mollon 2003). It is interesting, therefore, that the most conspicuous feature of P. preussi is its bright orange-rufous tail. Procolobus preussi is not the only cercopithecoid monkey to evolve such a brightly coloured tail; members of the Cercopithecus (cephus) group, including the sympatric C. erythrotis, also have bright orange-rufous tails. In the latter there are behaviour patterns to suggest that tail postures and movements provide information about dominance ranking. Whether this is also the case for P. preussi is not known. Orange-rufous limbs presumably help enhance the visibility of limb postures and gestures. Of 13 groups of P. preussi encountered during surveys in Korup N. P., 92% were in association with groups of at least one other species of monkey (Struhsaker 2000a). These large associations are believed to enhance predator detection and avoidance, and to provide foraging advantages (Gartlan & Struhsaker 1972, Struhsaker 2000a). Foraging and Food  Folivorous, dependent on emergent trees for food (S. Gartlan pers. comm. to Lee et al. 1988). Prefers the upper strata (Linder 2008). Seventeen species of plants belonging to nine families observed eaten by P. preussi in Korup N. P. (Usongo & Amubode 2001). Species and plant part most eaten were young leaves of Lecomtedoxa klaineana (27%) and Xylopia aethiopica (22%). Families Sapotaceae and Annonaceae constituted about 50% of total food items. Information on the nutritive values (e.g. crude protein, crude fibre, ether extract, nitrogen-free-extractive and total ash) of some of the food items is presented in Usongo & Amubode (2001). Social and Reproductive Behaviour  Social. Little-studied. Struhsaker (1975, 2000a) reports mean group size in Korup N. P. >47 (range >24–>80). All of his 36 encounters with P. preussi in Korup N. P. were with groups (i.e. no solitary individuals were encountered). More recently (2001–03) Dunn & Okon (2003) observed groups of >100 individuals in south Korup N. P. and found a mean group size of 35 (range = 10–130, n = 23). Has the most complex vocal repertoire of all Procolobus spp., including several calls not found amongst other red colobus taxa. The calls given by P. preussi include the ‘nyow’, ‘yowl’ and ‘copulation quaver’ (Struhsaker 1975, 1981b, 2010). Reproduction and Population Structure  Few data. Females probably have largest sexual swelling of any species of Procolobus, reaching an estimated 25–33% of the female’s body volume (Struhsaker 1975) and measuring at least 33 cm lengthwise and 45 cm in circumference (F. G. Merfield pers. comm. in Napier 1985). Sexual swelling of / pink. Females give a quavering copulation call before, during and after mating (Struhsaker 1981b, Oates 1994). Predators, Parasites and Diseases  No information, but likely predators include Leopards Panthera pardus, African Golden Cats

Profelis aurata, Robust Chimpanzees Pan troglodytes, Central African Rock Pythons Python sebae and Nile Crocodiles Crocodylus niloticus. The African Crowned Eagle Stephanoaetus conronatus is probably the most significant natural predator of Procolobus spp. (Struhsaker 2000a, 2010), but any such predation has long been dwarfed by heavy hunting by humans. Conservation  IUCN Category (2012): Critically Endangered. CITES (2012): Appendix II. Procolobus preussi still present in one protected area in Nigeria, the Oban Division of Cross River N. P., which is contiguous with Korup N. P. (J. Oates pers. comm.). The largest known population occurs in Korup N. P. A second population (of unknown distribution and size) is present in Ndokbou Forest and Ebo Forest but this population is not protected. The bushmeat trade, logging and habitat loss have reduced and extirpated populations over the past 40 years (Lee et al. 1988, Oates 1996a, Linder 2008, Linder & Oates 2011). Hunting of critical populations of P. preussi continues at a high level in Oban Division of Cross River N. P. (J. Oates pers. comm.), in Korup N. P. (Oates 1996a, Linder 2008) and in the Yabassi region (DowsettLemaire & Dowsett 2001). Procolobus preussi is one of the most common monkeys for sale in the bushmeat markets in the vicinity of Korup N. P. (Linder 2008). As a result of hunting, P. preussi is now extirpated from many areas, including most, if not all of the Korup Support Zone, of which the Ejagham Council F. R. is a part (Waltert et al. 2002, Steiner et al. 2003). Although there remains considerable habitat for P. preussi, national and international conservation bodies have proved helpless to protect P. preussi from the pressures of the bushmeat trade (Bowen-Jones & Pendry 1999, Oates 1999, Linder 2008). The main recommendations for the long-term conservation of P. preussi are (1) to stop hunting at all sites and to successfully implement the current human resettlement projects for Korup N. P., (2) to conduct surveys to better determine the distribution and abundance of P. preussi, especially in Cross River N. P., Ejagham Council F. R. andYabassi region, and (3) to up-grade the conservation status of Ebo Forest, Ndokbou Forest and Nlonako Forest and provide them with high levels of protection against hunters. Measurements Procolobus preussi HB (??): 560, 630 mm, n = 2 HB (/): 620 mm, n = 1 T (??): 750, 760 mm, n = 2 T (/): 750 mm, n = 1 WT (?): n. d. WT (/): 7.3 kg, n = 1 GLS (??): 111 (107–121) mm, n = 9 GLS (//): 108 (102–115) mm, n = 21 GWS (??): 84 (81–87) mm, n = 9 GWS (//): 80 (75–83) mm, n = 21 Powell-Cotton Museum (C. P. Groves pers. comm.) except GLS and GWS for two ?? and two // at BMNH (P. Grubb pers. comm.) Key References  Lee et al. 1988; Linder 2008; Oates 2011; Struhsaker 2010; Usongo & Amubode 2001. Thomas M. Butynski & Jonathan Kingdon

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Procolobus pennantii

Procolobus pennantii  Pennant’s Red Colobus (Bioko Red Colobus) Fr. Colobe bai de Pennant; Ger. Pennant-Stummelaffe Colobus pennantii (Waterhouse, 1838). Proc. Zool. Soc. Lond. 1838: 57. Fernando Po (= Bioko I.), Equatorial Guinea.

Taxonomy  Polytypic species, here taken to include three subspecies, pennantii, bouvieri, epieni. See taxonomic reviews in Grubb et al. (2003) and Ting (2008a, b). Dorst & Dandelot (1970) took P. pennantii to encompass all red colobus other than badius and temminckii. Groves (1993) followed a similar course but excepted preussi and rufomitratus (and restored waldronae to badius). Dandelot (1974), Napier (1985) and Grubb (1990) restricted P. pennantii to include bouvieri. Kingdon (1997) and Groves (2001, 2005c) took P. pennantii to include both bouvieri and, provisionally, epieni. This is the taxonomy adopted here. Grubb et al. (2003) placed preussi, bouvieri and epieni in P. pennantii.Vocal repertoire (Struhsaker 2010) and molecular data (Ting 2008b) suggest that epieni is more closely related to the red colobus of East Africa than to P. pennantii. Groves (2007b) and Oates (2011) treat pennantii, preussi, bouvieri and epieni as full species. Polymorphic in epieni and pennantii, less certain in bouvieri – but likely (Colyn 1993). Synonyms: bouvieri, epieni, likualae. Chromosome number: not known. Description  Medium-size, arboreal, reddish and black monkey with white cheeks. A highly variable species. For P. p. pennantii, adult

// have, on average, slightly greater body linear measurements than adult ??. Adult // are, however, more gracile than adult ??, as indicated by their body weight, which is about 94% that of the adult ??. Canines of adult ?? more than twice as long as for adult // (see measurements below). Muzzle relatively short (Verheyen 1962). Facial skin black with contrasting pink eyelids, nostrils and lips (most visible in younger animals). Cheeks and throat whitish, dirty white, or pale grey. Crown black or deep brown. Back and tail variable in extent of black, red or brown, but sometimes entirely black. Flanks and limbs predominantly orange or reddish. Ventrum whitish, dirty white, or faint peach. Hands and feet black. Unusual for red colobus in that P. p. epieni exhibits traces of agouti freckling on the crown and back. One infant P. p. pennantii estimated to be 1800 m in Schefflera-dominant forest on Pico Basile (Butynski & Koster 1994, T. Butynski pers. obs.). González-Kirchner (1997b: 99) states that ‘The Pennant’s Red Colobus was always observed under 2000 m above sea level’ but he does not actually state the highest level at which he observed this species. He also states that P. p. pennantii prefer primary montane forest. Procolobus p. pennantii is largely absent from degraded or secondary forest, but this is likely due entirely to heavy hunting of this monkey in such habitats. Procolobus p. bouvieri on the margins of major rivers, but habitat-use poorly known. Procolobus p. epieni in mangrove swamps of Niger Delta (Werre & Powell 1997). Annual mean rainfall ranges from ca. 2000 to >10,000 mm. Abundance  In 1986, the highest density (0.6 groups/km) of P. p. pennantii occurred in the Gran Caldera de Luba, SW Bioko (T. Butynski pers. obs.). Other encounter rates are 0.18 groups/km in 2008 along 44 km of transect in the Gran Caldera de Luba, and 0.31 groups/km in 2009 along 48 km of transect and 0.34 groups/ km in 2010 along 50 km of transect at Badja North, SW Bioko (T. Butynski, G. Hearn, M. Kelly & J. Owens pers. obs.). The Gran Caldera de Luba and Badja North are remote sites where hunting is relatively uncommon and there are no other anthropogenic impacts. As such, the encounter rates at these two sites are likely close to what is expected for an undisturbed population of P. p. pennantii. This species has been extirpated from much of Bioko as a result of unsustainable hunting with shotguns (Hearn et al. 2006). Large

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Niger Delta Red Colobus Procolobus pennantii epieni adult male.

groups of colobus, presumed to be P. p. bouvieri, have been seen on the right bank of the Congo R. in recent years (R. O’Hanlon pers. comm.). Museum specimens indicate that the range of P. p. bouvieri covers a linear distance of at least 200 km. Thus, even if P. p. bouvieri is primarily a riverine species, which is uncertain, it seems likely that there are still substantial numbers along the western bank of the Congo and its tributaries (e.g. Sangha R. and Léfini R.). Adaptations  Diurnal and arboreal. This species poses puzzling questions as to what adaptive or maladaptive features restrict the

distinctive subspecies to two or three widely separated geographic locations. Their situation contrasts strongly with their eastern neighbour, P. r. oustaleti, which is well distributed across a vast range. Likewise, their western neighbour, the Western Red Colobus Procolobus badius, was highly successful and until the twentieth century had a more or less continuous distribution from Senegal to Ghana. The present very restricted populations of P. pennantii imply that the species has suffered some biological inhibition that has prevented it from expanding out of its current enclaves. Understanding that adaptive shortcoming is highly relevant to 139

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ensuring the future conservation of this red colobus monkey. Some measure of its relictual status is the distance of ca. 1200 km between the range of P. p. epieni in the Niger Delta and that of P. p. bouvieri on the right bank of the Congo R. There are no known populations of Procolobus over these 1200 km. The presence of P. p. pennantii on Bioko I. is puzzling since the population on the mainland opposite Bioko I. is that of Preuss’s Red Colobus Procolobus preussi – which appears to have a different affinity, being morphologically closer to P. badius. Furthermore (assuming that P. p. epieni belongs in pennantii) P. preussi is interposed between it and P. p. bouvieri; how did it get there? (Possible explanations for this anomalous distribution are discussed in the profile of P. preussi.) Is P. pennantii an early form of red colobus that has been widely displaced by later, more adaptable species? Could competition from Colobus satanas have displaced P. pennantii throughout the intervening area? Perhaps, but the diets of these two species probably differ considerably, and the two species are sympatric on Bioko I. – so why not on the mainland? On Bioko I. González-Kirchner (1997b) found that these two species use the various levels of the forest strata to different extents. On present evidence, P. pennantii would appear to be a particularly poor disperser but the cause of its inability to ‘regain lost ground’ remains unknown. Kingdon (1997) noted the exceptional floristic and faunal richness of the Bight of Bénin, particularly the diversity of primates, and he listed competition with other primates, climate change, past hunting and species-specific disease pandemics as possible influences. Whatever the causes, they are not likely to have been recent. While it is obvious that all red colobus species have a common ancestor, the timing of their dispersal across equatorial Africa, and the details of their speciation pattern, await a comprehensive molecular study. When molecular trees of the red colobus group are eventually constructed, it seems likely that P. pennantii will be seen to belong to an early, possibly conservative, lineage. While all living species of red colobus, under current conditions, appear to be slow dispersers, P. pennantii seems to be the poorest colonist of them all. This conclusion is reinforced by their survival close to the focal centre of primate evolution in Africa, presumably the area where they might be expected to have had the longest tenancy. This suggests that their occupation of Bioko I. was the result of an early colonization that took place before the species’ decline on the mainland. Foraging and Food  Folivorous. No detailed studies have been made of P. pennantii. This species is unlikely, however, to differ from other red colobus species in the broader outlines of its diet. See the profiles for the other Procolobus spp. However, the three subspecies of P. pennantii live under quite different ecological regimes (especially rainfall), with likely implications for their diet and feeding habits. The main tree species in their diets are likely to differ considerably. Procolobus p. pennantii covers the altitudinal range from sea level to at least 800 m on Bioko I., and the range may be as much as 1800 m. On Bioko this species is present in coastal forest, ‘monsoon forest’ (rainfall >10,000 mm/year), mid-altitude (transition) forest and montane forest (Butynski & Koster 1994). Over this range, the composition of the tree community differs greatly, meaning that the diet of P. pennantii must also differ greatly over a horizontal distance of ca. 10 km.Therefore, P. p. pennantii is likely to have a more diversified diet than P. p. bouvieri or P. p. epieni, both of which live

at relatively low altitude on relatively flat ground. Sightings of P. p. bouvieri have been mostly along the margins of major rivers but it should be remembered that the pre-eminence of river transport in the Congo Basin could give a false idea of the ecological limits of P. p. bouvieri. Procolobus p. epieni is likely to have the most localized and peculiar diet, living, as it does, in a lowland delta close to the sea. From what is known of seasonal phenology in such littoral habitats it is possible that green fruit is taken more during the wet season while leaves and buds are the staple food during the dry season. Procolobus p. pennantii spends most of its time in the mid-canopy at ca. 15–30 m above the ground, but does forage in the upper canopy to >45 m (González-Kirchner 1997b) and, at least occasionally, on the ground (Struhsaker 2000a, T. Butynski pers. obs.). Observed feeding on flower buds of Allophylus africanus (T. Butynski pers. obs.). Social and Reproductive Behaviour  Social. P. p. pennantii groups seem to typically have >20 individuals and some have >30 individuals (Butynski & Koster 1994). Counts of 14 groups by Struhsaker (2000a) yielded a mean size of ca. 14 individuals (range = 5–100 m but usually much less than this (T. Butynski pers. obs.). Procolobus p. pennantii observed in polyspecific associations with Bioko Black Colobus Colobus satanas satanas, Bioko Red-eared Monkey Cercopithecus (c.) erythrotis erythrotis and Golden-bellied Crowned Monkey Cercopithecus (m.) pogonias pogonias. Of ten encounters during censuses conducted in 1986, P. p. pennantii in association with groups of other species of primate 40% of the time. Similarly, of 13 encounters in SW Bioko in 1992, Struhsaker (2000a) found that 38% of the P. p. pennantii groups were in a polyspecific association. During surveys conducted on Bioko in the Gran Caldera de Luba in 2008, two (25%) of the eight P. p. pennantii groups encountered were in a polyspecific association (Butynski & Owens 2008). Polyspecific associations are thought to confer anti-predator and foraging advantages to the participants (Struhsaker 2000a). The vocal repertoire of P. p. pennantii has the least overlap with other taxa of Procolobus. The calls given include: ‘chist’, ‘nyow’, ‘copulation quaver’ and ‘convex’. The ‘2-unit honk’, ‘2-unit chist’, ‘nasal scream’ and ‘nasal sqwack’ are very distinctive calls unique to P. p. pennantii. Procolobus p. epieni gives the ‘wheet’, a call which is absent from the vocal repertoire of P. p. pennantii (Struhsaker 1981b, 2010). The loud, squeaky ‘eeeyak’ and loud ‘honk’ calls of P. p. pennantii are highly variable in length and intensity. Both calls appear to be given only by adult ??. The ‘eeeyak’ can be heard to >250 m and the ‘honk’ to >400 m. The ‘honk’ may be the loudest call given by any Procolobus spp. and probably serves some of the same functions as the loud calls of adult ?? of other primate taxa (e.g. Colobus spp., Lophocebus spp., Cercopithecus spp.). These calls are given in times of excitement (e.g. intra-group aggression, loud noise from a falling tree, detection of a human). Adult // give sharp ‘ik’ and soft ‘honk’

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warning calls. Soft ‘whistles’ also given; these may be analogous to the ‘wheets’ of mainland Procolobus spp. (T. Butynski pers. obs.).

the same time, (2) rigorous protection of all of those populations that are known to exist. Providing adequate protection to viable populations of these three Reproduction and Population Structure  Few data available. subspecies of red colobus would greatly assist the conservation of Adult // exhibit large perineal swellings, sometimes protruding to numerous sympatric threatened taxa.Among primates, these include: >6 cm (T. Butynski pers. obs.). Bioko Preuss’s Monkey Allochrocebus preussi insularis; C. e. erythrotis; C. p. pogonias; Bioko Stampfli’s Putty-nosed Monkey Cercopithecus Predators, Parasites and Diseases  The Central African Rock (n.) nictitans martini; Bioko Black Colobus Colobus satanas satanas; Python Python sebae is a likely predator of all three subspecies of P. Bioko Drill Mandrillus leucophaeus poensis; Western Chimpanzee Pan pennantii, perhaps particularly of P. p. pennantii, which frequently troglodytes verus; and Nigeria Chimpanzee P. t. vellerosus. If a concerted moves on the ground, as Leopards Panthera pardus, African Golden effort is to be made to save all of the diversity present within the red Cats Profelis aurata and Nile Crocodiles Crocodylus niloticus are all colobus, then the major international conservation NGOs will need absent from Bioko I. These are all, however, likely predators of P. p. to focus their efforts on this taxonomic group and work closely with epieni and P. p. bouvieri. Likewise, the African ‘monkey-eating eagle’, national conservation NGOs and national protected area authorities. the African Crowned Eagle Stephanoaetus coronatus, is absent from Bioko I. but is expected to be second only to humans as the primary Measurements predator of P. p. epieni and P. p. bouvieri. Procolobus pennantii P. p. pennantii Conservation  IUCN Category (2012): Critically Endangered HB (MM): 505 (470–554) mm, n = 12 as P. pennantii, P. p. epieni and P. p. bouvieri, and Endangered as P. p. HB (FF): 519 (470–583) mm, n = 48 pennantii. CITES (2012): Appendix II. T (MM): 587 (520–630) mm, n = 12 Procolobus p. epieni listed as one of the worlds 25 most threatened T (FF): 639 (600–710) mm, n = 48 primates in 2008 (Oates & Werre 2009). Procolobus p. pennantii HF (MM): 154 (142–162) mm, n = 12 previously (2004–08) listed as one of the world’s 25 most threatened HF (FF): 158 (140–176) mm, n = 51 primates (Butynski et al. 2007). Procolobus p. pennantii probably has E (MM): 30 (26–35) mm, n = 12 the most restricted range of all of Bioko’s 11 species of primates, E (FF): 30 (26–33) mm, n = 50 and is now only known for certain from an area of 1000 mm. Abundance  Extremely common at some sites and rare at others. Population densities of P. r. tephrosceles in Kibale range from about 25 to 300 ind/km2 (Struhsaker 1975, 1997, Skorupa 1988, Chapman & Chapman 1999, Chapman & Lambert 2000, Teelen 2005). Densities of P. r. rufomitratus along the Tana R. range from 33 to 253 ind/km2

Adaptations  Diurnal and arboreal. See the subgenus and genus Procolobus profiles, as well as the Subfamily Colobinae profile for anatomical and physiological adaptations. Foraging and Food  Folivorous. Daily travel distance for P. r. tephrosceles in Kibale is highly variable within and between groups, ranging from ca. 180 to 1185 m. During a 15-month sample period, the daily travel distance of one group of 22 individuals ranged from 222 to 1185 m. Average daily travel distance among five groups in Kibale was between 500 m and 600 m (Struhsaker 1975, Struhsaker & Leland 1987). Daily distances are similar amongst the smaller groups living in the drier and more seasonal riparian forests of the Tana R., Kenya (Decker 1994a). There is disagreement as to whether or not group size affects travel distance (Struhsaker & Leland 1987, Gillespie & Chapman 2001, Struhsaker 2010, Isbell 2012). Mean annual home-range size varies from ca. 35 ha (Kibale) to 100 ha (Gombe) for P. r. tephrosceles (Clutton-Brock 1975, Struhsaker 1975, Struhsaker & Leland 1987), whereas they are only 4–19 ha for P. r. rufomitratus in the riverine forest patches along the Tana R. (Decker 1994a). Territoriality is absent amongst the populations studied and groups often have extensive, if not complete, overlap in home-ranges (Struhsaker 2000b). Exceptions exist in heavily logged areas of Kibale where there is little overlap in home-ranges and inter-group encounters are rare (Skorupa 1988, Struhsaker 2000b). Feeding occurs throughout the day, but is frequently alternated with periods of rest and travel (Struhsaker 1975, Marsh 1981). Time spent feeding during the daylight hours is ca. 23–30% for P. r. rufomitratus (Decker 1994a) and ca. 45% for P. r. tephrosceles (Struhsaker 1975). Young leaves dominate (ca. 30–50%) the diets of all three subspecies for which there are data, i.e. P. r. tephrosceles at Kibale (Struhsaker 1975, 1978b, Clutton-Brock 1975, Chapman & Chapman 2000, Isbell 2012), P. r. rufomitratus at Tana R. (Marsh 1981, Decker 1994a) and P. r. tholloni at Salonga N. P., DR Congo (Maisels et al. 1994). Mature leaves are eaten to a much lesser extent and even then it is usually the petioles and not the lamina that are consumed (Struhsaker 1975, 1978b). In the Salonga N. P., DR Congo, P. r. tholloni eats large quantities of seeds (31% of diet). Seeds sometimes dominate the diet

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of P. r. tephrosceles in Kibale for periods of several weeks (T. Struhsaker pers. obs.). Hundreds of tree and liana species are fed upon. Some of the common food species are: (1) P. r. tephrosceles: C. africana, C. durandii, N. buchananii, M. platycalyx, Aningeria altissima, Milletia dura, L. swynnertonii, P. excelsa and A. grandibracteata; (2) P. r. rufomitratus: F. sycomorus, Sorindeia obtusifoliolata, Acacia robusta, A. gummifera and Pachystela brevipes; and (3) P. r. tholloni: Guibourtia demeusei, Dialium sp., Symphonia globulifera, Cynometra pedicellata, Gilbertiodendron dewevrei and Daniella pynaertii. Procolobus r. tephrosceles of Kibale occasionally eats soil from the castings of subterranean termites (T. Struhsaker pers. obs.). Social and Reproductive Behaviour  Social. Groups of P. r. tephrosceles average about 45–50 individuals (range 8–80) in Kibale, and 55–59 individuals (range 30–82) in Gombe (Struhsaker 1975, 2000a, b). Groups smaller in the high-altitude and disturbed Mbisi Forest with means of ca. 25 (range 1500 m mean annual precipitation is >800 mm, with much of this falling as snow from Dec to Mar (snow may fall Sep– May). In Deag’s (1984) Aïn Kahla (Middle Atlas, Morocco) study area, snow fell during 39 days and lay on the ground in appreciable quantities for 82 days. Complete snow cover has a marked effect on the monkeys’ feeding behaviour (Fa 1982, Deag 1984, Mehlman 1984). Winter temperatures in the Moyen Atlas and Rif Mountains are consistently low and drop to –18 °C (Deag 1984, Drucker 1984, Mehlman 1984). Summer temperatures here are high, however, at >30 °C. Abundance  In 1984, Fa et al. (1984) estimated the total natural population of M. sylvanus to be 14,000–23,000 individuals (9000–17,000 in Morocco, 5000–6000 in Algeria). In 1992, Lilly

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& Mehlman (1993) indicated that the total population had declined to 10,000–16,000 individuals and, in 2005, Modolo et al. (2005; cf. Camperio Ciani & Palentini 2003) reported a further decline from 10,000 individuals. The number of M. sylvanus in Morocco declined from 4000–5000 individuals in 2005 to ca. 3000 individuals in 2008 (Van Lavieren & Wich 2010, A. Camperio Ciani pers. comm.). The Rif Mountains macaque populations, assessed in 1980 by Fa (1982) to be >1000 individuals in five sub-populations, were recently surveyed by Waters et al. (2007) and found to hold only ca. 300 individuals. The current situation for M. sylvanus in Algeria is unstudied. Current world wild population ca. 5000–6000 (Majolo et al. 2013). Population density in M. sylvanus (12–70 ind/km2) apparently attains its maximum in relatively undisturbed cedar or mixed cedar/ oak habitats (Deag 1984, Ménard & Vallet 1996, Van Lavieren & Wich 2010). As expected, degraded habitats, particularly those in the Moroccan Rif, support population densities that are much lower at (0.4–4.5 ind/km2; Mehlman 1989). Adaptations  Diurnal and semi-terrestrial. Macaca sylvanus is a highly adaptable species that is found in a variety of habitats with very different climates. The species exhibits much ecological plasticity (Ménard 2003). Fa (1994) discusses anatomical gut characteristics that correlate with M. sylvanus’s high herbaceous diet. Macaca sylvanus spends most of the daylight hours on the ground; reported mean frequency of daytime terrestriality varies from 68% to 83% in Morocco, and from 58% to nearly 100% in Algeria. Infants and juveniles tend to be less terrestrial than adults (Merz 1976, Deag 1985, Ménard 1985, Ménard & Vallet 1986, Machairas et al. 2003). At Afennourir and Cèdre Gouraud (=Gouroud), Morocco, juveniles were 70% terrestrial and adult ?? were 81% terrestrial (Machairas et al. 2003). Frequency of terrestriality also varies seasonally (Deag 1985, Ménard & Vallet 1986, 1997). Flee into trees to escape danger (Merz 1976, Deag 1985). Sleep in trees (Taub 1977, de Turckheim & Merz 1984, Mehlman 1989, Hammerschmidt et al. 1994) or in caves on rocky cliffs (MacRoberts & MacRoberts 1971, Alvarez & Hiraldo 1975, Fa et al. 1984, Mehlman 1984). Alvarez & Hiraldo (1975) report that M. sylvanus in the Rif Mountains migrate to lower altitudes during winter, but this is anecdotal. Foraging and Food  Omnivorous. Home-ranges of groups of M. sylvanus are, on average, smallest (18 ha, 12–25, n = 2) in the Moroccan Moyen Atlas (Fa 1986b, Drucker 1984), largest (804 ha, 307–1200, n = 6) in the Moroccan Rif (Fa 1986b, Mehlman 1989) and intermediate (280 ha, 39–424, n = 3) in the Algerian Grand Kabylie (Ménard et al. 1990, Ménard & Vallet 1996). Group homeranges frequently overlap in all three areas (Deag & Crook 1971, Rumsey & Whiten 1972, Ménard & Vallet 1997, Mehlman 1989). A group in cedar-oak forest (Tigounatine-Djurdjura, Algeria) with a home-range of 376 ha shared 48% of its home-range with other groups, while a group in deciduous oak forest (Akfadou) with a home-range of 424 ha shared 80% of its home-range with other groups (Ménard & Vallet 1996). Day ranges vary considerably from site to site and from day to day at each site. In cedar-oak forest day ranges were 473–3240 m (mean 1856, n = 115 days) at Tigounatine-Djurdjura, 892–2274 m (mean 1583, n = 41 days) at Aïn Kahlaj and 1401–4188 m (mean 2794, n = 40 days) at Seheb, Middle Atlas, Morocco. In deciduous oak

forest at Akfadou, day range was 799–3472 m (mean 2336, n = 104 days) (Ménard & Vallet 1997, N. Ménard pers. comm.). Diet of M. sylvanus includes a wide variety of plants (Fa 1984b). In the Moroccan Moyen Atlas at least 107 species of plants are eaten (cf. Deag 1983, Drucker 1984); in the Moroccan Rif, at least 100 species are eaten (Fa 1983a, Mehlman 1988); and in the Algerian Grand Kabylie, at least 130 species are eaten (cf. Ménard 1985, Ménard & Vallet 1986, 1996). The 100 species of food plants in the Moroccan Rif constitute 51% of 195 species of seed plants identified as present in that area. Similarly, the 130 species exploited in the Algerian Grand Kabylie constitute 48% of 271 species identified as present in that area. Also consumes fungi, lichens, mosses and animals (Deag 1983, Fa 1984b, Ménard 1985). Agricultural crops have been raided by M. sylvanus since at least the early sixteenth century (Leo Africanus 1896 edition, Mehlman 1988). Eats flowers, fruits, seeds, seedlings, leaves, buds, bark, gum, stems, roots, bulbs and corms (Fa 1984b, Mehlman 1988, Ménard & Qarro 1999). Fa (1994) compared M. sylvanus diets with other Macaca spp. to show the species’ high reliance on herbaceous plants, in comparison to the more frugivorous Asian macaques. Diet of M. sylvanus shows high seasonal variation (Deag 1983, Mehlman 1984, Ménard 1985, Ménard & Vallet 1986). Diet also varies by habitat. Seeds and leaves are the main foods (ca. 60–75%) in lowland oak forests in the Algerian Grande Kabylie (Ménard & Valet 1986), but more fruits are consumed in the Moroccan Moyen Atlas (Deag 1983, Drucker 1984, Ménard & Qarro 1999). In the higher altitude coniferous forests they eat large volumes of fir and cedar leaves during periods of high snowfall when conditions impede them from feeding on ground vegetation (Deag 1983, Drucker 1984, Mehlman 1988). Animal prey includes snails, earthworms, scorpions, spiders, centipedes, millipedes, grasshoppers, termites, water striders, scale insects, beetles, butterflies, moths (including larvae), ants (including nests) and tadpoles (Fa 1983a, 1984b, Mehlman 1984, 1988, Ménard & Vallet 1986). Semi-free-ranging M. sylvanus monkeys pursue and/or catch birds, Red Squirrels Sciurus vulgaris and young European Rabbits Oryctolagus cuniculus but have not been observed to eat them (Kaumanns 1978, de Turckheim & Merz 1984); mice are, apparently, ignored. Feeding occupies an average of 24% and 25% of daytime hours at two localities in the Moroccan Moyen Atlas (Fa, 1986b, Machairas et al. 2003), and also occupies 24% and 25% of daytime hours at two localities in the Algerian Grande Kabylie (Ménard & Vallet 1997). In winter, water may be obtained by eating snow (de Turckheim & Merz 1984, Mehlman 1988). Social and Reproductive Behaviour  Social. Mean size of 68 groups is 27.1 individuals (7–88). Mean group size is smallest (18.3 individuals, 10.0–27.5, n = 27) in the Moroccan Rif, largest (50.2 individuals, 27–88, n = 8) in the Algerian Grande Kabylie and intermediate (28.6 individuals, 12–40, n = 33) in the Moroccan Moyen Atlas. Group size generally is stable, but it is unstable in the population that inhabits a rocky habitat in the Djurdjura Mts, Algeria (Ménard et al. 1985, 1990, Ménard 2002); in this marginal habitat, groups frequently split into subgroups that subsequently reunite in various combinations. Solitary ??, as far as 7 km from the nearest group, occur in the Moroccan Rif (Mehlman 1985, 1986). Within natural groups, the number of adult ?? averages only slightly less than the number of adult //. The ratio of adult ?? to adult // averages 0.70 in the Moroccan Moyen Atlas, 0.99 in 161

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the Moroccan Rif and 0.84 in the Algerian Grande Kabylie (Whiten & Rumsey 1974, Taub 1980a, Fa 1982, 1986b, Deag 1984, Drucker 1984, Ménard et al. 1986, 1990, Mehlman 1989, Ménard & Vallet 1993a, Hammerschmidt et al. 1994, Ménard & Qarro 1999, Camperio Ciani & Machairas 2003, Machairas et al. 2003). Most studies of M. sylvanus groups indicate that their composition is reasonably constant. Adult // to immatures (infants and babies) ratio at Aïn Kahla, Moyen Atlas (Deag 1984) was 1:0.9 (1:0.5–1:1.2, n = 5), and 1:1.3 and 1:1.4 for the same area in a later study (Taub 1978). For the Rif Mountain groups studied by Mehlman (1984), the adult /: immature ratio averaged 1:1.2.The proportion of immatures in Algerian groups varied between 0.41–0.59 at Tigounatine, and 0.42–0.58 at Akfadou, according to the year (Ménard & Vallet 1996). During the mating season, pairs of ?? and oestrous // form consortships (i.e. temporary sexual associations) in the course of which copulations occur (Taub 1978, 1980a, de Turckheim & Merz 1984, Fa 1986b).The duration of consortships varies from 0.10), the number of ? newborns equals or exceeds that of / newborns in five of the seven available samples. Neonatal sex ratio is related to maternal rank in the Salem sample (Paul & Kuester 1990): the ? : / sex ratio for newborns by highrank mothers (102/74 = 1.38) significantly exceeds that for infants produced by low-rank mothers (86/95 = 0.91; p 100 mm), limp, medium grey to blackish-brown hairs, parted down the middle, sweeping back and to the sides, and falling over the ears. Dorsum pale yellowish-grey to greyish-brown, tinged olive. Throat and ventrum yellowish-white. Ventrum pelage long and sparse. Outer lower forelimbs dark grey to blackish-brown. Inner limbs white to yellowish-grey. Hands and feet dark grey to blackishbrown.Tail dark grey to blackish-brown with paler terminal ca. 25%. Tail with slight tuft. Hairs of crown, neck and shoulders annulated. Callosities joined in ?? and separate in //. Occasionally holds tail in ‘question-mark’ pose above the back. Infants with pink face, ears and limbs, and without the characteristic crest on crown. Tana River Mangabey Cercocebus galeritus adult male.

Geographic Variation  None recorded.

Taxonomy  Monotypic species. Originally given full species status by Peters (1879), and that classification retained by Elliot (1913b), Dobroruka & Badalec (1966), Groves (1978, 2001, 2005c) and Kingdon (1997). Considered by some to be a subspecies C. g. galeritus, with the conspecifics Sanje Mangabey C. g. sanjei, Golden-bellied Mangabey C. g. chrysogaster and Agile Mangabey C. g. agilis (Schwarz 1928d, Dandelot 1974, Hill 1974, Napier 1981, Grubb et al. 2003). Synonyms: none. Chromosome number: 2n = 42 (Groves 1978).

Similar Species  None within the small geographic range of this species. Distribution  Coastal Forest Mosaic BZ. Endemic to flood-plain forests along 60 km of the lower Tana R., SE Kenya, from Kanjonja in the north to Tana Delta in the south (01° 24´ S to 02° 24´ S, 40° 06´ E to 40° 19´ E, 20–40 m asl) (Butynski & Mwangi 1994, 1995, Hamerlynck et al. 2012). 167

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above 10 m (n = 1 group; J. Wieczkowski pers. obs.). Cercocebus spp. have a dental morphology and muscular jaws believed to be adapted to eating seeds and hard nuts (Fleagle & McGraw 2002). This interpretation is supported by the preponderance in the diet of seeds (Kinnaird 1990a, Wieczkowski 2003) that have high crushing resistance values (Wieczkowski 2009). Also adapted to the seasonality of fruit availability, and the temporal and spatial heterogeneity of its habitat, through flexibility in diet, grouping, ranging patterns and inter-group interactions (Homewood 1976, Kinnaird 1990a, Wieczkowski 2003). Spends more time foraging and moving when food less available, and more time in social behaviours when food more available (Kinnaird 1990a).

Cercocebus galeritus

Habitat  Flood-plain forest and adjacent woodland and bushland. Forest within the geographic range occurs in 71 fragments that range in size from 1 to 1100 ha and comprise a total forest area of ca. 37 km2. In 1994 mangabeys inhabited 27 of these forests and occupied a total area of ca. 26 km2 (Butynski & Mwangi 1994, 1995). Mangabeys move up to 1 km through non-forest habitat between forests (Wieczkowski 2010). Flood-plain forest comprised of plant species from four floristic regions, and characterized by high inter-forest species variation that is determined by forest location on the flood-plain (Medley 1992). The most common tree species are Phoenix reclinata (13%), Polysphaeria multiflora (12%), Garcinia livingstonei (7%) and Sorindea madagascariensis (5%) (percentages are of all trees ≥10 cm DBH sampled in 49,850 m2 in 31 forests; D. Mbora & J. Wieczkowski pers. obs.) Forest size and density of trees >10 cm DBH are the only variables that are significantly positively correlated with mean number of mangabey groups/forest (Wieczkowski 2004). Lower Tana R. is a highly seasonal environment. Mean annual rainfall 470 mm (120–1020 mm; Decker 1994a). Rainfall mostly limited to Mar–Jun and Nov–Dec. Mean monthly minimum daily temperatures are 17–25 °C, and mean monthly maximum daily temperatures are 30–38 °C (Butynski & Mwangi 1994). The coolest months are Jul–Sep and the hottest months are Oct–Jun. Abundance  Common within its small ca. 26 km2 range. Densities within individual forests range from 0–6.8 animals/ha. Density within the entire forested area of the range is ca. 0.45 animals/ha. A total of 48 groups located during a survey of the entire range in 1994 when the total population was estimated at 1000–1200 animals (Butynski & Mwangi 1994). This is a decline from the 1975 estimate of 1200–1600 (Marsh 1978). Changes in the size of this population from 1972–94 are summarized in Butynski & Mwangi (1994). Adaptations  Diurnal and semi-terrestrial. Spends 56% of time on ground, 32% of time in vegetation to 10 m, and 12% of time

Foraging and Food  Frugivorous. Average time spent feeding (eating and foraging) is 58% (46–65, S.D. = 8, n = 6 groups; Homewood 1976, Kinnaird 1990a, Wieczkowski 2003). Time spent eating is fairly constant throughout day, while foraging peaks morning and mid-day (Kinnaird 1990a). Feeds predominantly on the ground and up to 2 m (Homewood 1978a). Average daily travel distance for 431 sample days is 1511 m (1040–2618, S.D. = 562, n = 10 groups). Annual home-ranges ca. 17, 19, 20, 30, 47, 51, 53, 57, 70 and 101 ha (mean= 46.5 ha). Amount of overlap with neighbouring groups varies from 25% (70 ha range) to 36% (53 ha range) to 100% (17 and 19 ha ranges) (Homewood 1976, Kinnaird 1990a). Home-range size varies negatively with habitat quality and population density, and positively with group size (Homewood 1976, Kinnaird 1990a, Wieczkowski 2005b, Mbora et al. 2009). Predominantly eats seeds and fruit, but also stems, leaves, insects and fungi. Adult / observed with a small bird that was discarded (M. F. Kinnaird pers. comm.) and adult ? photographed repeatedly pulling an adult African Wood Owl Strix woodfordii from a tree-hole but left without killing the owl (Schuetz & Razakarivony 2004). Average annual diet is 44% fruit (26–71, S.D. = 18, n = 6 groups) and 32% seed (7–46, S.D. = 16, n = 6 groups; Homewood 1976, Kinnaird 1990a, Wieczkowski 2003), although there appears to be a shift to a preponderance of seeds in the latter two studies: fruit 32% (26–36, S.D. = 5, n = 4 groups) and seeds 42% (34–46, S.D. = 5, n = 4 groups). Eats unripe, ripe and dry fruit and seeds (Homewood 1976, Kinnaird 1990a, Wieczkowski 2003). Observed feeding on total of 96 species of plants, though eight species each individually account for >10% of the annual diet (Aporrhiza paniculata, Acacia robusta, Diospyros mespiliformes, Ficus sycomorus, Hyphaene compressa, Pachystela msolo, Phoenix reclinata and Saba comorensis) (Homewood 1976, Kinnaird 1990a, J. Wieczkowski pers. obs.). Species and items in the monthly diet closely follow the fruiting seasons of the top food species. High food availability from Nov–Apr; low food availability from Jun–Oct (Homewood 1976, Kinnaird 1990a). Social and Reproductive Behaviour  Social. Lives in multifemale groups with one or more adult ??. Changes in group size from 1972 to 1992 are summarized in Butynski & Mwangi (1994). Mean group size has fluctuated over time: 26 (17–36, n = 4; Homewood 1976); 20 (15–28, n = 7; Kinnaird & O’Brien 1991); and 31 (6–62, n = 17; J. Wieczkowski pers. obs.). Mean for all years is 27 animals/group, consisting of a mean 2.2 adult ??, 7.0 adult //, 2.4 subadult ??, 2.0 subadult //, 9.6 juveniles and 3.3 infants (n  = 9; Kinnaird & O’Brien 1991, J.Wieczkowski pers. obs.).

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Agonistic behaviour includes eyelid flashes, lunges, chases, grabs, bites, grapples, branch shaking and vocalizations. These are described by Gust (1994), who did not observe damaging contact or serious wounding during a 210 h, 6-week study. Amicable behaviour includes stylized presentations, grooming and play. Territorial behaviour varies temporally.When fruit is scarce, groups avoid one another, using different areas of their overlapping ranges. When fruit is abundant and uniformly distributed, groups often move and feed together for several hours. When fruit is patchily distributed and defendable, territorial behaviour is exhibited. This includes approaching the other group, which may lead to an aggressive encounter. Aggressive encounters have site-dependent outcomes (Kinnaird 1990a, 1992b). The dominant ? secures the majority of copulations with oestrous // (Kinnaird 1990b). Copulation described by Gust (1994). Adult ?? emit a loud, long ‘whoop-gobble’ call that aids in inter-group spacing. Mean duration of the whoop-gobble is 90.5 sec (S.E. = 10.0, n = 136; Gust 1994). About 66% of whoop-gobbles are given between 06:30h and 11:00h (n = 562; Kinnaird 1992b). This call is audible to a distance of >1 km. Other vocalizations include ‘screams’ and ‘wherrs’ that are given during aggressive encounters (Gust 1994), as well as ‘grunts’, a bleating contact call and various alarm calls (J. Wieczkowski pers. obs.). Does not form polyspecific associations with other species of primates. Although often found with Pousargues’s White-collared (Sykes’s) Monkey Cercopithecus mitis albotorquatus, associations do not occur more often than expected by chance (Homewood 1976). Sometimes grooms Sykes’s Monkey and the Tana River Red Colobus Procolobus rufomitratus rufomitratus (J. Wieczkowski pers. obs.). Interactions with Yellow Baboon Papio cynocephalus are variable (fights, avoidance, supplants, toleration). Seen mounting and grooming Harvey’s Duiker Cephalophus natalensis harveyi on several occasions (Homewood 1976, M. F. Kinnaird pers. comm., J. Wieczkowski pers. obs.). Reproduction and Population Structure  Adult // exhibit large, monthly, oestrous swellings lasting 4–5 days (Kinnaird 1990b). Mean gestation is 180 days (S.E. = 4.49, n = 7 pregnancies; Kinnaird 1990b). Details of parturition given in Kinnaird (1990b). Single births during Aug–Apr (Kinnaird & O’Brien 1991), generally a time of high food availability (Homewood 1976; Kinnaird 1990a). Twins not observed. About 63% of adult // give birth during a given year (9–100%, n = 6 groups; Homewood 1976, Kinnaird 1990b). Infants suckle until 6–10 months; inter-birth interval is 18–24 months (Homewood 1978b). Infanticide by adult ?? during dominance turnovers is thought to occur (Kinnaird 1990b). Postconception sexual swelling lasting 8–9 days occurs after the first two months of pregnancy (mean = 62 days, S.E. = 3.6, n = 7), and two of seven pregnant // under study copulated at this time (Kinnaird 1990b). Based on studies of closely related species, // probably first breed at ca. 6.5 years. Males probably first breed at seven years. Longevity estimated at 19 years (Homewood 1976, Kinnaird & O’Brien 1991). Adult ? to adult / ratio in groups ranges from 1 : 2 to 1 : 6 (n = 9 groups). Adult and subadult ? to adult and subadult / ratio in groups ranges from 1 : 1.2 to 1 : 6 (n = 11 groups). Adult to young (subadult, juvenile and infant) ratio in groups ranges

from 1 : 0.8 to 1 : 2.8 (n = 9 groups; Homewood 1976, Kinnaird & O’Brien 1991, J.Wieczkowski pers. obs.). In one well-studied group of 20 mangabeys, two out of four adult ??, and one out of five infants died in one year (Homewood 1976). Predators, Parasites and Diseases  Central African Rock Python Python sebae thought to be the most common and important predator (Homewood 1976, M. F. Kinnaird pers. comm., J. Wieczkowski pers. obs.). Likely predators include African Crowned Eagles Stephanoaetus coronatus (Wieczkowski et al. 2012), Martial Eagles Polemaetus bellicosus, Nile Crocodiles Crocodylus niloticus (Homewood 1976, J. Wieczkowski pers. obs.) and Leopards Panthera pardus. An adult / attacked by an (unidentified) eagle died of her wounds two days later. Twelve nematodes (Abbreviata sp., Ascaridia galli, Capillaria sp., Heterakis sp., Oesophagostomum sp., Physaloptera sp., Streptopharagus sp., Strongyloides fuelleborni, Toxascaris sp., Toxocara sp., Trichostrongylus sp. and Trichuris trichura) and three protozoans (Entamoeba coli, E. hystolytica, E. hartmani) found in mangabey faecal samples from 82 individuals. The most common parasites were E. coli (20% of individuals), T. trichura (20%), Heterakis sp. (10%) and Trichostrongylus sp. (6%). Entamoeba hystolytica, pathogenic in humans, was found in 1% of individuals (Mbora & Munene 2006). Conservation  IUCN Category (2012): Endangered. CITES (2012): Appendix I. Ranked in 2002 as one of the world’s 25 most threatened primates (Konstant et al. 2003). Greatest threat is forest degradation through taking of forest products and loss of forest for farmland (Butynski & Mwangi 1994, 1995), both of which increased dramatically after 1994 (Wieczkowski & Mbora 2000, Wieczkowski 2005a, Moinde-Fockler et al. 2007). Of special concern is decimation of local P. reclinata populations by humans (Kinnaird 1992a, Wieczkowski & Mbora 2000); this palm is the mangabey’s top food resource (Homewood 1976, Kinnaird 1992a, Wieczkowski & Kinnaird 2008). Between 1994 and 2000, ca. 30% of the forest cover within the range of C. galeritus was lost to clearance for agriculture (Butynski & Mwangi 1994, Wieczkowski 2005a). There was a 20% loss of forest inside the Tana River Primate National Reserve (TRPNR; 169 km²) and a 41% loss of forest outside this Reserve. In addition to C. galeritus, there is another Endangered primate that is endemic to the forests of the lower Tana R., P. r. rufomitratus. As such, the forests along the lower Tana R. represent the most important site in East Africa for primate conservation actions ( De Jong & Butynski 2012). The history of research and conservation actions on behalf of C. galeritus, P. r. rufomitratus and the forests of the lower Tana R. is reviewed in Butynski & Mwangi (1994) and Wieczkowski (2005a). A five-year Kenya Wildlife Service (KWS) and Kenya Forest Department Project, funded by World Bank’s Global Environmental Facility (GEF), was initiated in 1996 to enhance conservation and protection of the biodiversity and forests of the lower Tana R. Unfortunately, this potentially important project was terminated prematurely due to poor project management. This left the responsibility for the conservation and protection of the Tana River’s biodiversity and forests entirely to KWS. The TRPNR was gazetted in 1976 in approximately the northern half of the distribution of C. galeritus and P. r. rufomitratus (Marsh 1976). Officially a County Council Reserve, the Tana River County 169

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Council had given management authority of the Reserve to KWS. In February 2007 the High Court of Kenya ruled in favour of Tana R. residents who brought a lawsuit stating the Reserve had been gazetted without their permission. Therefore, the TRPNR must be degazetted. Consequently, none of the habitat of C. galeritus or P. r. rufomitratus is legally protected. The residents say that they are interested in creating a community wildlife sanctuary but the way forward for the formal establishment of a community wildlife sanctuary and its effective management is unclear at this time (Mbora & Butynski 2007, Allen & Mbora 2012). Habitat degradation and loss along the lower Tana R. has been further exacerbated by the failure of the 250 km2 Tana Delta Irrigation Project’s (TDIP) rice-growing scheme (under the administration of the Tana and Athi Rivers Development Authority [TARDA] with financing from Japan International Cooperation Agency [JICA]) to protect forest patches on their land. Some of the best forest habitat for for C. galeritus and P. r. rufomitratus has been lost to TDIP (Butynski & Mwangi 1994, Moinde-Fockler et al. 2007). Now TARDA is promoting the establishment of a 400 km2 sugar-cane plantation in the Tana Delta and of a 300 km² sugar-cane plantation slightly up-stream of the Delta. Beyond this, two jatropha biofuel farms (500 km2, 280 km2) are being proposed for near the Delta (Hamerlynck et al. 2012). These new plantations will result in loss of forest, a large influx of people and an increase in the demand for forest resources, thereby putting even more pressure on the last remaining habitat for these two threatened monkeys (Mbora & Butynski 2007, Hamerlynck et al. 2012). Priorities for research on C. galeritus include long-term monitoring and ecological studies in the southern half of the geographic range.

Priority conservation actions include habitat protection, community conservation education, establishment of forest corridors, planting of woodlots, creation of a permanent field research station at Mchelelo, and surveys of the newly discovered population in the Tana Delta (Butynski & Mwangi 1994, Wieczkowski 2005a). Measurements Cercocebus galeritus HB (??): 600, 620 mm, n = 2 HB (/): 450 mm, n = 1 T (??): 620, 730 mm, n = 2 T (/): 520 mm, n = 1 HF (??): 158, 160 mm, n = 2 HF (/): 133 mm, n = 1 E (?): 39 mm, n = 1 E (/): 32 mm, n = 1 WT (??): n.d. WT (/): ca. 3.7 kg, n = 1 GLS (??): 123 (122–127) mm, n = 5 GLS (//): 107 (106–107) mm, n = 3 GWS (??): 82 (79–84) mm, n = 5 GWS (//): 70 (68–72) mm, n = 3 Tana R. (Elliot 1913b, Allen & Lawrence 1936, C. P. Groves pers. comm., T. Butynski & J. Wieczkowski pers. obs.) Key References  Butynski & Mwangi 1994; Homewood 1976; Kinnaird 1990a; Wieczkowski 2003, 2004, 2010. Julie A. Wieczkowski & Thomas M. Butynski

Cercocebus agilis  Agile Mangabey Fr. Mangabé agile; Ger. Olivmangabe Cercocebus agilis Milne-Edwards, 1886. Revue Scientifique 12: 15. Republic Poste des Ouaddas (junction Oubangui R. and Congo R.), DR Congo.

Taxonomy  Monotypic species. Often considered a subspecies of Cercocebus galeritus, along with other subspecies galeritus, sanjei and chrysogaster (Dandelot 1974, Napier 1981, Gautier-Hion et al. 1999, Grubb et al. 2003). Groves (1978) revised the genus, resurrecting Cercocebus agilis. (See also Groves 2001, 2005c.) Synonyms: fumosus, hagenbecki, oberlaenderi. Chromosome number: 2n not known, but probably 42, as for all Papionini for which chromosome number has been determined (Romagno 2001). Description  Medium-sized, lanky, brownish-grey, semiterrestrial monkey with long tail. Sexes alike in colouration. Adult // ca. 60% the weight of adult ??. Muzzle moderately prognathic with short vibrissae. Face, ears, palms and soles black. Capacious cheek-pouches. Eyelids pale grey, but not as light as in Red-capped Mangabey Cercocebus torquatus. Face with white border formed by light bases to the hairs. Crown with whorl of hairs radiating 360° out from naked whitish skin, parting (creating a projecting brow). Crown, dorsum, outer limbs and upper tail heavily speckled brownish-grey, darkest on crown and lower limbs; hairs short, fine and agouti-banded. Chin, throat, inner limbs, ventrum and undertail unspeckled yellowish-white. Tail long

Agile Mangabey Cercocebus agilis adult male.

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Cercocebus agilis

Lateral, palatal and dorsal views of skull of Agile Mangabey Cercocebus agilis adult male.

(ca.140% of HB) and tapered, with variable presence of a whitish terminal tuft. Tail often carried arched or horizontal above the back, with tip almost touching the head. Ischial callosities separate in //, continuous in ??. Infants born with red faces, which become black over time. Geographic Variation  Groves (1978) distinguishes a light morph and a dark morph, based on pelage colour; these co-occur, in different proportions, throughout the range of the species. Although four taxa (agilis, hagenbecki, fumosus and oberlaenderi) were described from different parts of the range in the early 1900s, Groves assessed that the level of geographic variation is not sufficient to warrant subspecies differentiation. Body size is larger in the west of the species’ geographic range (Groves 2001). Similar Species Cercocebus torquatus. Geographic range to the west of C. agilis; only zone of contact is around Meyo/Sangmelima, Cameroon (Gautier-Hion et al. 1999). Crown chestnut. Collar white. Lophocebus albigena. Widely sympatric with C. agilis. Pelage dark brown, longer and scruffier. Mane (= cape = mantle) over neck and shoulders. Distribution  Endemic to equatorial central Africa. Rainforest BZ. From SE Cameroon, NE Gabon, SW Central African Republic and N Congo to E DR Congo (Gautier-Hion et al. 1999). In Gabon from left bank of Ivindo R. as far south as Koungo Waterfalls, and

possibly along Mvoung R. (S. Lahm pers. comm.). Unclear how far west the range extends in the Minkebe area of N Gabon, although present on Sing R. and Nouna R. (S. Lahm pers. comm.), and on Mvoula R., a tributary of the Ntem R. (L. White pers. comm.). Western limit thought to be Lobo R., around Sangmelima, ca. 75 km west of Dja R, Cameroon (Gautier-Hion et al. 1999), but recently reported farther west at Campo-Ma’an N. P., SW Cameroon (Matthews & Matthews 2002, Etoga & Foguekem 2009). Distribution extends north in Cameroon to Nyong R. In Central African Republic the range extends north following the forest limit between Nola and Berberati, dipping down into the Ngotto Forest near Mbaiki. Agile Mangabeys were in the hills outside Bangui, but the forest there had been heavily degraded (N. Shah pers. obs.) so now probably absent there. From Bangui the distribution is to south of the left bank of Oubangui R., south of Gbadolite, DR Congo, then north again to the forests around Bangassou (A. Blom pers. comm.). Between the Oubangi R. and Congo R., DR Congo, distribution uncertain, as forests are highly fragmented and have not been much surveyed. Hicks (2010), however, found them in most areas surveyed north and south of Uele R. between Mbomu R. to the north and Rubi/Itimbiri R. to the south in the area around Aketi and Bambesa. Present almost as far east as Garamba (E. de Merode pers. comm.).The eastern limit in DR Congo likely the forest-savanna ecotone. Southern limit in DR Congo not clear: present in Ituri Forest north to Nepoko Forest and south of the Ituri R. (Hart & Thomas 1986) and in the Maiko N. P. (Hart & Sikubwabo 1994) but not in the Kahuzi-Biega lowlands (J. Hart pers. comm.). In Congo southern limit probably the limit of the forest block, around Likouala R., as this species is not found in forest fragments along Alima R. (A. Gautier-Hion pers. comm.), nor at Léfini or Conkouati. Reports (Sabater Pi & Jones 1968) of Agile Mangabeys in Equatorial Guinea (Rio Muni) require verification. Habitat  Often in riverine, seasonally inundated, or swamp forests, but can inhabit terra firma forest exclusively in some places. 171

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Uses both primary and secondary forests, but prefers habitat with dense ground vegetation. Uses all forest strata, from ground to canopy. Occasionally in more open Gilbertiodendron-monodominant forest (Shah 2003, Devreese 2011). Travels and forages primarily on the ground, but climbs into trees to find fruit and to sleep. Large groups may spend more time on ground (72%; Devreese 2011) than small groups (12–22%; Quris 1975, Shah 2003). Adult ?? more terrestrial than adult // (36% vs. 24% of time on ground; Shah 2003). Abundance  More often heard than seen, and thought to be uncommon throughout most of its range. Difficult to estimate densities due to human hunting pressure, its semi-terrestrial nature and preference for habitats with dense ground vegetation. Quris (1975) estimated a density of 6.7–12.5 ind/km2 along riverbanks in swamp forest in NE Gabon. At Mondika, in Ndoki Forest, S Central African Republic/N Congo, density ca. 6.9 ind/ km2 (Shah 2003) in terra firma forest. In Ituri Forest, DR Congo, Thomas (1991) estimated 0.25 groups/km2, or ca. 2 ind/km2, whereas Kambale Saambili (1998) estimated 38.3 ind/km2 in the same area. In 1999, D. Brugière (pers. comm.) found 0.92 groups/ km2, or ca. 18.9 ind/km2 in a narrow strip of flooded forest along the Mbaéré R. in the Ngotto Forest, Central African Republic. Densities ranged from 0.4 to 2.0 groups/km2 (or ca. 7.2–41.0 ind/km2) in different stretches of this habitat; densities related to human hunting pressure. At this site Agile Mangabeys are restricted to a narrow strip of flooded forest along the river (i.e. not the entire flooded forest habitat). Adaptations  Diurnal and semi-terrestrial. Capacious cheekpouches for storing food, and extra-laryngeal air sacs for longdistance vocalizations. Large molarized posterior premolars with thick enamel for crushing seeds, and well-developed forelimb flexor muscles for aggressive manual foraging (Fleagle & McGraw 1999, 2002). Fruits and seeds are available to Agile Mangabeys on a longer temporal scale than for other sympatric monkeys, since they are able to consume many fruits before they are ripe and then dig up seeds that persist on the forest floor for months after the fruiting season. Additionally, they procure food at all forest levels, from the ground to the canopy, expanding their food niche relative to strictly arboreal monkeys. Foraging and Food  Frugivorous. Agile Mangabeys spend 64– 76% of feeding time eating fruits, including seeds (Quris 1975, Kambale Saambili 1998, Shah 2003, Devreese 2011). At Mondika, of those observations where foods could be identified, 76% were fruit (including seeds), 16% pith and shoots of terrestrial herbs, 5% invertebrates, 2% mushrooms and 2% roots (Shah 2003). At Bai Hokou, SW Central African Republic: 68% fruit (including seeds), 21% plant structural parts, 6% animal matter and 5% mushrooms (Devreese 2011). Agile Mangabeys eat a wide variety of fruits and seeds in ripe, unripe and over-ripe (i.e. rotting) stages. They also consume old seeds and nuts, which persist on the forest floor for months, or that they find by digging up or by sifting through Forest Elephant Loxodonta cyclotis dung (Ekondzo & Gautier-Hion 1998, N. Shah pers.

obs.) or Western Gorilla Gorilla gorilla dung (N. Shah pers. obs.). They use their powerful jaws, broad cheekteeth and thick dental enamel to open tough pods and fruits, crunch hard seeds, and their incisors to scrape a hole to open lignified fruits. These morphological adaptations allow them to consume foods that most other monkeys cannot access. During a one-year study at Mondika, the three species of fruit most eaten by Agile Mangabeys were Diospyros pseudomespilus, Erythrophleum ivorense and Anonidium mannii. The second-mosteaten category of food was the protein-rich shoots and terminal tips of Marantaceae herbs, especially Haumania danckelmaniana (Kambale Saambili 1998, Shah 2003). Raphia shoots are also often eaten (Quris 1975). Other plant food items include mushrooms, roots, tubers, seedlings and flowers. Animal prey includes termites, centipedes, butterflies, millipedes, beetles, gastropods, birds’ eggs, rodents and small snakes (Shah 2003, Devreese 2011, A. Todd pers. comm.). Agile Mangabeys hunt larger mammals at Bai Hokou (Knights et al. 2008, L. Devreese pers. comm.). Prey taken include infant Blue Duikers Philantomba monticola, infant Water Chevrotain Hyemoschus aquaticus and infant Peters’ Duikers Cephalophus callipygus. Preliminary data indicate that infant Blue Duikers are taken ten times as often as other prey. Only adult ? Agile Mangabeys were observed to hunt these species. Hunts are opportunistic and solitary, and meat sharing has not been observed (although other individuals will take dropped pieces of meat). Preliminary data yield an average of 2–3 hunts/month (0–6; Knights et al. 2008). For a small group at Mondika, about 33% of the time is spent feeding, 31% travelling, 13% inactive, 10% engaged in social/sexual behaviour, 8% foraging and 5% in other behaviours (Shah 2003). Adult // spend more time searching for food (i.e. foraging and travelling) than adult ?? (39% vs. 26%; Shah 2003). For a very large group at Bai Hokou (ca. 130 animals), about 25% of time spent feeding, 42% travelling, 10% inactive, 6% in social/sexual behaviour, 15% foraging, and 3% in other behaviours (Devreese 2011). Average daily travel distance is 1155 m (390–1985, n = 54) in terra firma at Mondika (Shah 2003), and 1215 m (n = 12, range unreported) in inundated habitat in NE Gabon (Quris 1975). For the much larger group at Bai Hokou, average daily travel distance is ca. 3884 m (Devreese 2011) to 3200 m (n = 79, range unreported; C. Cipolletta pers. comm.). During periods of fruit scarcity, Agile Mangabeys at Mondika travel longer distances, spend more time on the ground and spend a greater proportion of time searching for food (Shah 2003). Home-range for the group at Mondika was >303 ha (Shah 2003).The group in NE Gabon had a long and narrow home-range of 200 ha, following the course of a marshy river (Quris 1975). The very large group at Bai Hokou ranged over 1500 ha (L. Deveese pers. comm., A. Todd pers. comm.). Social and Reproductive Behaviour  Social. Group sizes vary enormously. Difficult to obtain accurate group counts, because of Agile Mangabeys’ terrestrial locomotion in habitats with dense undergrowth. Smaller group counts are 8–18 individuals in NE Gabon (n = 1; Quris 1975), 21 individuals at Mondika (n = 1; Shah 2003), 24 individuals in Ituri Forest (9–55, n not given; Kambale Saambili 1998) and ca. 20 individuals in the Ngotto Forest (D. Brugiere pers. comm.).

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Large groups (50 to >200 animals) are occasionally reported in SE Cameroon (Usongo & Fimbel 1995), in NE Gabon (Quris 1975), in Ituri Forest (Kambale Saambili 1998) and in SW Central African Republic (A. Turkalo pers. comm., C. Cipolletta pers. comm., N. Shah pers. obs.). It is not always clear whether these counts represent larger groups, temporary aggregations of groups, or greater population densities. At Bai Hokou one group maintained a size of ca. 125 individuals for several months, appeared to merge with another group and maintained a size of ca. 230 individuals for 2 years, dropped to 134 for several months, then increased to 330 individuals (C. Cipolletta, A. Todd, K. Knights, M. Santochirico & L. Devreese pers. comm.). Smaller groups have one adult ? (Quris 1975), while larger groups are age-graded or multimale (Quris 1975, Shah 2003, Devreese 2011). One group at Mondika comprised two adult ??, two subadult ??, 7–8 adult // and 11 juveniles and infants (Shah 2003). At Bai Hokou the group of ca. 230 individuals comprised 32 adult ?? and 22 subadult ?? (M. Santochirico pers comm.), and when it was 134 individuals there were 19 adult ?? and 48 adult // (Devreese 2011). In NE Gabon ?? and // both transferred between groups during inter-group encounters. Solitary ?? were observed at this site (Quris 1975). In NE Gabon neighbouring groups have overlapping home-ranges. Here, a group of 7–18 individuals with a long and narrow home-range along a river had extensive overlap with other groups (Quris 1975), whereas at Mondika, a group of 21 individuals had a home-range of >303 ha in terra firma forest, with minimal overlap with other groups (Shah 2003). Relations between conspecific groups are variable: sometimes affiliative, with individuals intermingling in temporary associations called ‘supergroups’ (Quris 1975, Shah 2003), and at other times agonistic (Shah 2003). During these agonistic encounters, adult ?? vocalize, display and chase ?? of other groups. It is not clear whether relations with the same neighbouring groups are affiliative at some times, and agonistic at others, or whether relations with certain neighbouring groups are always affiliative, and with others always agonistic. Groups temporarily fragment into subgroups (Quris 1975, Kambale Saambili 1998, L. Devreese pers. comm.). Adult // display oestrous swellings and have visible menses. Males sometimes mate-guard oestrous //. There can be high levels of aggression between ?? over an oestrous / (N. Shah pers. obs.). Weaning conflicts between mothers and their offspring begin when infants are about seven months old, but // occasionally nurse offspring as old as 18 months. Infants are sometimes carried by adult and subadult ??, particularly in tense encounters between ??, where they potentially serve to buffer aggression (N. Shah pers. obs.). Adult ?? emit long-range vocalizations, beginning with a loud ‘whoop’ (very similar to the ‘whoop’ of the sympatric Greycheeked Mangabey Lophocebus albigena) followed by a ‘gobble’ or ‘cackle’. These calls, audible to observers at up to 1000 m, are thought to play a role in both intra-group coordination and intergroup communication (Quris 1973, 1980). Most ‘whoop-gobbles’ (or ‘whoop-cackles’) are emitted around dawn. Individuals within a group also communicate using a variety of other vocalizations, including a soft ‘contact’ grunt that is audible only to ca. 25 m and that is thought to help maintain group cohesion in dense understorey (N. Shah pers. obs.).

Agile Mangabeys occur in polyspecific associations with other primate species 11% of the time at Mondika (Shah 2003) and 6% of the time in NE Gabon (Quris 1976), but these are usually shortlived associations, often at shared feeding trees. Inter-specific interactions are generally neutral, but occasionally may be agonistic or affiliative. Agile Mangabeys sometimes supplant or chase other monkeys (e.g. L. albigena, Putty-nosed Monkeys Cercopithecus nictitans, Moustached Monkeys Cercopithecus cephus, Crowned Monkeys Cercopithecus pogonias) out of feeding trees (Shah 2003). Juveniles, however, occasionally engage in reciprocal grooming bouts with adult ?? and juveniles of other monkey species (e.g. C. cephus and C. pogonias) (Shah 2003). Other animals, such as guineafowl (several species), Red River Hogs Potamochoerus porcus and various species of duikers (Philantomba monticola, Cephalophus spp.), often forage with Agile Mangabeys. Agile Mangabeys react to alarm calls of all of these species (A. Todd, M. Santochirico & N. Shah pers. obs.). Reproduction and Population Structure  When in oestrus, // have perineal swellings that they sometimes present to ??. Gestation is ca. 24 weeks in captivity (E. Dols pers. comm.). At Mondika one / gave birth six months after she was last observed copulating (N. Shah pers. obs.). One infant is born at a time. Twins not reported. Birth-weights are not available. Inter-birth intervals at Mondika are greater than 21 months (N. Shah pers. obs.). In NE Gabon infants are born in Dec–Feb (Quris 1975). At Mondika births occur during two periods: Dec–Feb and Jun–Aug (N. Shah pers. obs.). At Bai Hokou, ca. 60 km to the north of Mondika, births occur in May–Aug (K. Knights & M. Santochirico pers. comm.). Infants are weaned at 7–18 months at Mondika (N. Shah pers. obs.) and at about six months in captivity (E. Dols pers. comm.). In a small group at Mondika the ratio of adults and subadults to juveniles was 1 : 1, and the ratio of adult ?? to adult // varied from 1 : 3.5 to 1 : 4.0 (Shah 2003). In a group of 134 animals at Bai Hokou, the ratio of adult ?? to adult // was 1 : 2.6 (Devreese 2011). Longevity in the wild not known. One animal in captivity lived to 21 years of age (E. Dols pers comm.). Predators, Parasites and Diseases  Gabon vipers Bitis gabonica, Leopards Panthera pardus and African Crowned Eagles Stephanoaetus coronatus are known predators of Agile Mangabeys (A. Todd & L. Devreese pers. comm.). Central African Rock Pythons Python sebae and cobras (Naja spp.) unsuccessfully attacked Agile Mangabeys (A. Todd pers. comm.). Agile Mangabeys carry high levels of parasites, such as Entamoeba histolytica, Entamoeba coli, Balantidium coli, Iodamoeba butschlii and trichomonads. All of these parasites are transmitted back and forth between humans and the monkeys (Lilly et al. 2002). Agile Mangabeys also harbour a strain of simian immunodeficiency virus (SIV) (Apetrei et al. 2002). Conservation  IUCN Category (2012): Least Concern. CITES (2012): Appendix II. The primary threat to Agile Mangabeys is hunting for the bushmeat trade. Because of their semi-terrestrial habits, they are vulnerable to snare hunting. A secondary threat is habitat loss, degradation and fragmentation. Agile Mangabeys are notorious crop 173

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raiders (Kambale Saambili 1998), which may make them vulnerable to reprisals in areas where they live close to plantations. Measurements Cercocebus agilis HB (??): 572 (500–625) mm, n = 6 HB (//): 489 (440–530) mm, n = 5 T (??): 684 (570–760) mm, n = 6 T (//): 530 (450–600) mm, n = 5 HF (??): 169 (153–180) mm, n = 5 HF (//): 139 (130–150) mm, n = 4 E (??): 370 (350–400) mm, n = 5 E (//): 360 (340–400) mm, n = 3 Various localities (Hill 1974)

HB (??): 550 (?–?) mm, n = 11 HB (//): 465 (?–?) mm, n = 11 T (??): 745 mm, n = 11 T (//): 635 mm, n = 11 WT (??): 8.8 (4.8–10.0) kg, n = 7 WT (//): 5.4 (4.3–6.2) kg, n = 5 Makokou area, Gabon (Gautier-Hion et al. 1999) WT (??): 9.0, 10.0 kg, n = 2 WT (//): 4.3, 6.2 kg, n = 2 Ngotto Forest, Central African Republic (Colyn 1994) Key References  Devreese 2011; Gautier-Hion et al. 1999; Groves 1978; Kambale Saambili 1998; Quris 1975; Shah 2003. Natasha F. Shah

Cercocebus chrysogaster  Golden-bellied Mangabey Fr. Mangabé à ventre doré; Ger. Goldbauchmangabe Cercocebus chrysogaster Lydekker, 1900. Novitates Zoologicae 7: 279. Upper Congo, DR Congo.

Golden-bellied Mangabey Cercocebus chrysogaster young adult male.

Taxonomy  Monotypic species. Originally given full species status by Lydekker (1900), and that classification retained by Elliot (1913b), Dobroruka & Badalec (1966), Kingdon (1997) and Groves (2001, 2005c). Also classified as Cercocebus galeritus chrysogaster (Schwarz 1928d, Dandelot 1974, Hill 1974, Napier 1981, Grubb et al. 2003) and as Cercocebus agilis chrysogaster (Groves 1978, 1993, Gautier-Hion et al. 1999). Synonyms: none. Chromosome number: 2n = 42 (Dutrillaux et al. 1979).

Description  Robustly built monkey with a golden-yellow to orange-gold or reddish-gold belly. Only mangabey without a brow (frontal) fringe. Adult / like adult ?, but less robust and smaller; body weight ca. two-thirds that of adult ?. Muzzle robust. Bare skin of chin, lips, muzzle, face and ears dark brown to blackish. Eyes brown. Eyelids whitish or pinkish. Cheek whiskers creamyellow, long and swept back from near corner of mouth to behind ears giving a ‘mutton-chop’ appearance, especially in mature ??; pelage bordering face and sides of head off-white. Light cream to reddish patch behind ears. Forehead lacks parting or whorl in adults, but whorl present in some juvenile museum skins (Groves 1978). Crown and neck brownish-olive to reddish-olive, speckled with black, tipped yellow or light orange. Shoulders, back, flanks and outer limbs colour of crown and neck but paler and less speckled, especially on the flanks and outer hindlimbs. Inner forelimbs light yellow or pale orange proximally, becoming cream towards wrists and ankles. Inner hindlimbs light reddish-gold. Hands and feet grey, dark greyish-brown to blackish. Throat, front of upper arms and chest pale orange to light reddish-gold, darker towards midline. Shoulders and upper arms of adult ? with a mane (= cape = mantle) of long, thick pelage. Belly light yellow to golden-yellow to reddishgold, becoming brighter towards the lower belly. Belly with median fringe of long hairs. Rump broad, poorly furred. Buttocks of adult ? each have a patch of cream-white pelage and a patch of pink bare skin to either side of base of tail; absent in //. Ischial callosities wide, light pink, rosy-pink, or violet-grey; fused in ??, separate in //. Broad ring of off-white pelage around ischial callosities. Tail pelage short; above speckled like dorsum at base, rest unspeckled grey or sooty-black, paler below, especially near base. Tail about equal in length to HB. Penis bright scarlet. Scrotum bluish. Infant colouration differs from adult; head pelage black, skin pale pink and belly pale beige or white. A golden band appears on forehead at ca. 8 weeks of age and adult colouration gradually expands over the head; skin darkens to greyish-brown by 14 weeks

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with contrasting non-pigmented eyelids visible by 20 weeks (Field 2007). Sexes markedly dimorphic in size (Dorst & Dandelot 1970, Groves 1978); adult ?? noticeably more robust, with canines about three to four times longer than in adult // (Field 2007). GLS for adult / (n = 2) is 82% that of adult ? (n = 9; Groves 1978). In captive animals weight of adult // ca. 62% that of adult ??, and HB length of // ca. 83% that of ?? (Field 2007). Geographic Variation  Upon examination of 15 study skins, the only variation that Groves (1978: 17) found was that the one specimen from the westernmost locality (Luaza) had a belly that ‘is hardly yellow at all,’ in sharp contrast to the golden-yellow or bright orange colouration on the belly of the other 14 specimens. Both this specimen, and the one from the south-easternmost locality (between Lusambo and Pania), were only weakly speckled on the flanks. Similar Species  None within geographic range. Distribution  Endemic to the western and central Congo Basin, DR Congo. Rainforest BZ. Geographic distribution not well-known. There is no evidence for C. chrysogaster in the NE Congo Basin; absent in the Lomako Forest and in the 70,000 km2 ‘Maringa–Lopori–Wamba Landscape’ as indicated by extensive ground surveys in the region and by the absence of C. chrysogaster from among the ca. 12,000 carcasses examined in the Basankusu (01° 13´ N, 19° 49´ E) bushmeat market. This market is fed largely by hunters operating in forests along, and between, the Maringa and Lopori Rivers (J. Dupain pers. comm.). Based on a specimen from Irebu Village (00° 37´ S, 17° 45´ E), the western limit is the Congo R. (Schouteden 1944a, Hill 1974). A specimen from Lulonga (= Lubonga) Village suggests that the north-west limit (and northern extreme) is the lower Lulonga R. (ca. 00° 24´ N, 18° 14´ E; Groves 1978, Gauthier-Hion 1999). Cercocebus chrysogaster is present, but uncommon, in the bushmeat market south of Lulonga R. at Mbandaka (00° 03´ N, 18° 15´ E; J. Hart pers. comm.). Absence of C. chrysogaster from the Basankusu bushmeat market (see above) to the north of the Lulonga R. indicates that this species does not occur along the upper reaches of the Lulonga R., nor north of the Lulonga R. Distribution appears to be south-south-east from Lulonga R. (Groves 1978) to Momboyo R. at about Imbonga Village (00° 41´ S, 19° 39´ E; J. Hart pers. comm.), and then to the Lokoro R. at Luikotale Village (which is the western boundary of the South Sector of the Solanga N. P.). J. Eriksson (pers. comm.) found C. chrysogaster to be uncommon at Luikotale, but already more common just 10 km to the west, and fairly abundant ca. 50 km to the west at Lokolama Village and Mimia Village, as well as between Lokalama and the right bank of the Lukénie R. at Oshwe. From Luikotale, the range appears to extend south-east to the Ngendo R. (ca. 03° 28´ S, 21° 13´ E), a northern tributary of the Lukénie R. Inogwabini & Thompson (2004) state that C. chrysogaster occurs west of the Ngendo R., but not to the east. From here the distribution becomes particularly poorly known, but at some point the range probably meets the Sankuru R. to the south. The distribution likely extends east along both the Lukénie and Sankuru Rivers to at least Samangwa Village (04° 14´ S, 24° 06´ E). The south-east limit

Cercocebus chrysogaster

appears to be between Lusambo Village and Pania Village (05° 00´ S, 23° 24´ E). At least four specimens obtained in the vicinity of Samangwa, Lusambo and Pania (Schouteden 1944a, Hill 1974, Groves 1978). Samangwa is only ca. 75 km from the west bank of the Lomami R. As such, Hill (1974) suggests that the Lomami R. is the likely eastern limit for C. chrysogaster. Known south-west limit, based on a specimen, is Luaza Village (03° 25´ S, 17° 11´ E) on the Kwilu R., a southern tributary of the Kasai R. One specimen collected at Oshwe (03° 23´ S, 19° 30´ E) on the south bank of the Lukénie R. (Schouteden 1944a, Hill 1970, Groves 1978, GautierHion et al. 1999), and J. Eriksson found C. chrysogaster to be common here. Inogwabini & Thompson (2004) did not find C. chrysogaster east of 20° 30´ E along the Kasai-Sankuru R. and, thus, believe that the Lukénie R. is the southern boundary for C. chrysogaster in this region, not the Kasai-Sankuru R. as indicated by Gautier-Hion et al. (1999). The information available suggests that C. chrysogaster may occur in two populations (a western population and an eastern population), or else these two ranges are connected by a narrow corridor that runs along, or in the vicinity of, the Lukénie R. and/or Sankuru R. A. Gautier-Hion (pers. comm.) notes that there are patches of savanna to the south of the South Sector of the Salonga N. P. and that this presence of unsuitable habitat may account for what appears to be a fragmented distribution for C. chrysogaster in this region. It is of conservation importance that C. chrysogaster appears to be absent from the North Sector of Salonga N. P. (Gautier-Hion et al. 1999, G. Reinartz pers. comm., J. Hart pers. comm., J. Thompson pers. comm.). J. Hart (pers. comm.) and his colleagues undertook surveys over much of Salonga N. P. (36,560 km2), encountered >200 groups of primates and never observed C. chrysogaster. J. Thompson (pers. comm.) conducted surveys in the southern half of the South Sector of Salonga N. P. and never encountered C. chrysogaster. The map in Gautier-Hion et al. (1999) shows C. chrysogaster as present in the South Sector of Salonga N. P., although this map is based on information collected from interviewees and not on the authors’ 175

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direct observations of C. chrysogaster in this region (A. Gautier-Hion pers. comm.). If C. chrysogaster is present anywhere in the Salonga N. P. it is most likely in the south-west corner of the South Sector on the Lula R. between Luikotale Village and the Ngendo R. Not known to be sympatric with Agile Mangabey Cercocebus agilis, the two species being separated by the Congo R. (Groves 1978, Gautier-Hion et al. 1999). Habitat  Prefers seasonally flooded and swamp forests (Groves 1978, Gautier-Hion et al. 1999, Inogwabini & Thompson 2004). Can be common in secondary forest (J. Eriksson pers. comm.). The altitude limits of the distribution of C. chrysogaster are ca. 300 and 500 m (Inogwabini & Thompson 2004). Abundance  Few data. What information is available strongly suggests that C. chrysogaster not only has a small and fragmented distribution, but that the area actually occupied is small. Adaptations  Diurnal and semi-terrestrial (Hill 1974, GautierHion et al. 1999). Not studied in the wild. J. Eriksson (pers. comm.) is of the opinion that C. chrysogaster moves mainly on the ground. Foraging and Food  Unknown. Kingdon (1997) suggests diet is largely frugivorous. J. Eriksson (pers. comm.) observed C. chrysogaster eating seeds out of Forest Elephant Loxodonta cyclotis dung and often saw duikers Cephalophus spp. foraging within C. chrysogaster groups. Social and Reproductive Behaviour  Social. No detailed information available on social structure or social organization from wild populations. Gautier-Hion et al. (1999) suspect that group size averages ca. 15 animals, if similar to C. agilis. J. Eriksson (pers. comm.) estimated group size for C. chrysogaster as often >100 animals, and sometimes had the impression that groups might be between 200–300 animals (in the vicinity of Lokolama, Mimia and Oshwe). Data from captive heterosexual pairs of C. chrysogaster indicate sex differences in behaviour, with ?? displaying significantly more aggression, and // more social grooming and vocalization (Mitchell et al. 1988). Posture is more similar to that of macaques (Macaca spp.) than to other Cercocebus spp. (Hill 1974), and overall appearance reminiscent of some of the more robust macaque species; these are the strong impressions one gets upon seeing this species for the first time (T. Butynski & C. L. Ehardt pers. obs.). Unlike all other mangabeys, immatures and adults both carry the tail in a backward arch with the tip directed at the heels. While apparently never arched high over the shoulders and/or back (Dandelot 1974, Kingdon 1997), the tail may be swung forward at such an acute angle that the mid-part of the tail touches a shoulder and the tip touches an upper arm (T. Butynski pers. obs.). In captivity at least one aggressive display involves a wide yawning expression with the upper lip pulled back, all teeth showing, and eyebrows raised (Hill 1974, T. Butynski pers. obs.). One vocalization is described by Hill (1974: 165) as ‘a deep guttural croak, somewhat like a baboon’s bark’. A rapid, low, ‘oohooh-ooh-ooh’ given by a captive ? in what appears to be greeting behaviour (C. L. Ehardt & T. Butynski pers. obs.). A ‘ha-ha-ha-’ call

given in aggressive situations (Mitchell et al. 1988). Not known to give the ‘whoop-gobble’ loud-call of some other Cercocebus spp. Reproduction and Population Structure  No data available from wild populations. Data on reproductive parameters collected on five captive // (two wild-caught). Two // began cycling at 2.5 and 2.6 years with first menses at 2.7 years; menses heavy and highly visible. Mean menses is three days. Oestrous cycles average 30.7 days (20–51, n = 149 cycles), with duration of peak perineal swelling averaging 5.8 days (2–22, n = 151 cycles). First pregnancy at 4.9 years (Walker et al. 2004). Gestation ca. 5.8–5.9 months (n = 2 births). Mean interval from parturition to resumption of swelling 8.6 months (5.5–10.0, n = 3 //). Inter-birth interval for captive // with infants surviving >1 month averages 19.9 months (16.6–24.8, n = 4 // producing nine births; Walker et al. 2004). There is a post-conception swelling. Females solicit adult ? cage-mates during periods of post-conception swelling, and copulations have occurred at this time (Walker et al. 2004, Field 2007). No twin births observed in captivity (n = 15). Birth-weight of one individual was 750 g (Field 2007). No pronounced birth season in captivity (Field 1995a, 2007). Predators, Parasites and Diseases  No information. Most important predators are likely to include Leopards Panthera pardus and African Crowned Eagle Stephanoaetus coronatus. Humans are undoubtedly the most important predator (see below). Conservation  IUCN Category (2012): Data Deficient. CITES (2012): Appendix II. As indicated above, and in Inogwabini & Thompson (2004), it now appears that C. chrysogaster has a considerably smaller range and lower numbers than once believed. Assessment by the IUCN Primate Specialist Group at this time would likely find that C. chrysogaster deserves threatened species status. Habitat degradation and loss, as well as hunting by humans, are major threats (Wolfheim 1983, Inogwabini & Thompson 2004). Hunting rates are high, as indicated by the many C. chrysogaster on the streets of Kinshasa and elsewhere, both for meat and the pet trade; it is also an agricultural pest in some areas. Young are often kept as pets as they seem to tame readily (Inogwabini & Thompson 2004, G. Reinartz pers. comm., J. Eriksson pers. comm.). Sixteen wild- and captive-born C.chrysogaster (seven ??, nine //) are present in six North American zoos (Field 2007); four European zoos currently house ten ?? and 18 // (ISIS 2007).This is one of Africa’s least-known primates and, potentially, one of Africa’s most unique primates. Research is needed on all aspects (distribution, abundance, ecology, conservation status, threats) of this likely threatened monkey. Measurements Cercocebus chrysogaster T (??): 510 (470–550) mm, n = 4 T (/): 460 mm, n = 1 WT (??): 11.6 (10.1–13.6) kg, n = 4 WT (//): 9.0 kg, n = 1 Captive individuals at Sacramento Zoo (L. Field pers. comm.) HB (?): 790 mm, n = 1 T (?): 430 mm, n = 1

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Cercocebus sanjei

HF (?): 130 mm, n = 1 Locality not stated (Elliot 1913b) HB (??): 530 mm HB (//): 440 mm T (??): 540 mm T (//): 450 mm WT (??): 11–15 kg WT (//): 8 kg Based on an unknown number of captive individuals at various sites (Field 2003); ranges and samples sizes not available

GLS (??): 131 (129–134) mm, n = 9 GLS (//): 105, 109 mm, n = 2 GWS (??): 85 (82–89) mm, n = 9 GWS (//): 67, 68 mm, (n = 2) From various localities (RMCA) (Groves 1978, C. P. Groves pers. comm.) Key References  Elliot 1913b; Gautier-Hion et al. 1999; Groves 1978. Carolyn L. Ehardt & Thomas M. Butynski

Cercocebus sanjei  Sanje Mangabey Fr. Mangabé Sanje; Ger. Sanje-Mangabe Cercocebus sanjei Mittermeier, 1986. In: Else & Lee (eds), Primate Ecology and Conservation, p. 338. Sanje Waterfall, Mwanihana Forest, Udzungwa Mts, Tanzania.

Description  Medium-sized, long-tailed, semi-terrestrial, grizzled-grey monkey. Sexes alike in colour. Adult ?? moderately larger than //, but no body measurements exist against which to accurately assess sexual dimorphism. Muzzle grey to dark grey, moderately projecting with numerous dark vibrissae. Face pale pinkish and grey. Eyelids slightly less pigmented, pale beige, contrasting with surrounding skin. Skin on forehead and under eyes pale pinkish-cream. Cheek skin along hair line pale blue. Skin on body bluish-white, with skin on hands, feet and ears dark greyish. Crown hairs long, slightly parted along midline or forming a slight whorl, with shorter seam of hair extending forward along the brow. Hairs on crown, brow and extending back around face blackish at base, then dark greyish-brown. (Note: Previous descriptions of crown hairs swept back and upward to give a ‘bouffant’ appearance are inaccurate. These were based on the appearance of the crown of a captive adult ? at the Mount Meru Game Sanctuary, Arusha, Tanzania, which did not resemble any observed free-living animal. The ‘bouffant’ crown of this captive might have been due to the fact that it received a haircut as a juvenile pet and/or repetitive rubbing of the crown against the wire mesh of its cage.) Dorsum hairs long, light creamy-grey at base, then a darker grey band followed by a yellowish-orange band and black tip. Ventrum hairs long, pale orange. Pelage darker grey or blackish on distal part of limbs and on hands and feet. Paracallosal skin greyish with pink tinge. Ischial callosities pink; fused in ??, separate in //. Tail long, grey, with slight tuft at tip. Infants have dark greyish-black coat and pink skin on face, ears, hands and feet. Sanje Mangabey Cercocebus sanjei adult male.

Geographic Variation  None recorded. Similar Species  None within geographic range.

Taxonomy  Monotypic species (Kingdon 1997, Groves 2001, 2005c). Originally considered a subspecies (Cercocebus galeritus sanjei) (Homewood & Rodgers 1981). No museum specimen exists and no holotype has been designated. Synonyms: none. Chromosome number: 2n = unknown, but 42 for all Cercocebus spp. and Lophocebus spp. for which the chromosome number determined (Dutrillaux et al. 1979, T. Disotell pers. comm.).

Distribution  Coastal Forest Mosaic and Afromontane–Afroalpine BZs. Endemic to two forests within the Udzungwa Mts, SC Tanzania: Mwanihana Forest (7° 40´ –7° 57´ S, 36° 46´ –36° 56´ E) within Udzungwa Mountains N. P. (UMNP), and Udzungwa Scarp F. R. (USFR; 7° 39´ –7° 51´ S, 35° 51´ –36° 02´ E) (Rodgers & Homewood 1982, Ehardt et al. 1999, 2005, Dinesen et al. 2001).The area of closed 177

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Abundance  Size of fragmented population uncertain but estimated at 30 m tall), clumped trees such as P. excelsa. Study group in Mwanihana Forest utilized eight areas of tall trees for sleeping, scattered through their large home-range; each site might or might not be used during consecutive nights (C. L. Ehardt pers. obs.). Adult ?? emit ‘whoop-gobble’ loud-calls, audible to >1 km, which likely function as a group-spacing mechanism. These are given at all times of the day, but are most common in early morning, with ca. 70% given before 12:00h. Whoop-gobbles are frequently given in sleeping trees before the group begins foraging, and when conspecific groups are encountered. Other vocalizations include: high-pitched, repetitively emitted ‘barks’ given when the group is alarmed, which may differ in structure depending on the source of the threat (alarm calls); low volume, low frequency, short duration ‘moo’ calls that group members emit periodically when the group is spread out and resting (contact calls); multi-syllabic ‘hee-aw’ calls by oestrous // after ? ejaculates and / runs forward, breaking copulatory mounted position (post-copulatory calls); and rapidly repeated ‘geckers’ given by infants and young juveniles, especially in context of weaning (C. L. Ehardt pers. obs.). Foraging and Food  Omnivorous. Forages in all strata of the forest, but most often on the ground and in understorey trees and shrubs (Ehardt et al. 2005). On the forest floor Sanje Mangabeys manually search through leaf litter and decomposing wood for invertebrates, fallen seeds and nuts, and fungi, as well as dig for subterranean roots as deep as 500 mm (e.g. Costus sp.). The Sanje Mangabey has large posterior premolars, which are similar to other Cercocebus mangabeys (Fleagle & McGraw 2002), used to crack open hard seeds and nuts (e.g. P. excelsa) (C. L. Ehardt pers. obs.). Groups often fission into foraging parties, regrouping ≤6 h later (Ehardt et al. 2005). Invertebrates, such as ants, millipedes, slugs and snails, are taken from epiphytes in the branches of trees, and from rotting wood and leaf litter. When foraging on abundant fruit in single trees (e.g. Ficus sur), or on large fruits that cannot be consumed quickly, Sanje Mangabeys frequently place whole fruits or chunks of fruit in their cheek-pouches and move into other trees to process and consume. Also observed to place P. excelsa nuts gathered while moving along the forest floor into cheek-pouches to consume in trees, often in

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early evening when moving toward sleeping trees (C. L. Ehardt pers. obs.). Diet includes fruit pulp (ca. 50% of diet items consumed; n = 5084 food item scores over 19 months), seeds and nuts (27%), invertebrates (6%), shoots and stalks (4%), fungi (4%), mature and young leaves (4%), flowers (2%) (C. L. Ehardt pers. obs.). Consumed in smaller relative amounts (each ≤1% of total diet items) are buds, petioles, herbs, roots, bark, lichen, tree gum or latex, birds, amphibians and reptiles (e.g. frogs and chameleons), and several invertebrates, such as snails and crabs found in or near rivers and streams (Wasser 1993, Ehardt et al. 2005, C. L. Ehardt pers. obs.). Plants utilized by nonsystematically observed groups (near Sanje River Falls, ca. 600 m in Mwanihana Forest [Wasser 1993]), and by one study group at 700– 900 m in the Sonjo River Valley in Mwanihana Forest (Ehardt et al. 2005, C. L. Ehardt pers. obs. ), are: Acacia polyacantha, Acacia siberiana, Aframomum sp., A. gummifera, A. senegalensis, A. grandiflora, Antiaris toxicaria, B. micrantha, Celtis gomphophylla, Costus sp., Diospyros natalensis, Dovyalis sp., Dracaena mannii, Entada rheedii, Ficus cyathistipula, F. sur, Ficus vallis-choudae, H. madagascariensis, Hoslundia sp., Kigelia africana, L. pallidiflora, Lettowianthus stellatus, Macaranga capensis, Mangifera indica, Milicia excelsa, Olyra sp., Oxytenanthera abyssinica, P. excelsa, P. filicoidea, Psychotria capensis subsp. riparia, Rhaphiostylis beninensis, Saba comorensis, Sorindeia madagascariensis, Strombosia scheffleri, Syzygium cuminii, T. pachysiphon, Tarenna pavettoides, Toddalia asiatica, T. africana, Trema orientalis, Tricholysia sp., Trilepisium madagascariensis,V. mariacancia, V. doniana andVoacanga africana. Foraging occurs most frequently in the morning, early afternoon, late afternoon and early evening (groups tend to rest for 1–2 h at mid-afternoon). Home-range of Mwanihana Forest study group is ca. 2 km and overlaps that of two conspecific groups (Ehardt et al. 2005, C. L. Ehardt pers. obs.). Rovero et al. (2009) report home-ranges of 4–6 km² with overlap of home-range with up to three other groups. No evidence of territoriality. Intra-specific group encounters produce frequent ‘whoop-gobble’ vocalizations and alarm calls, with occasional chasing/fleeing. Mean daily path length ca. 1350 m (500– 1650 m, n = 190 days; C. L. Ehardt pers. obs.). Social and Reproductive Behaviour  Social. Groups are multimale/multifemale. From 3–8 adult ?? in Mwanihana study group; // are philopatric. Group size counts and estimates in Mwanihana range from 1 to 40 individuals (mean 10, Wasser 1993; mean = 15, n = 14, Ehardt 2001). Rovero et al. (2009) report that mean group size is between 40 and 60 individuals. The study group in Mwanihana increased from 39 to 58 animals across ca. 3.5 years (C. L. Ehardt pers. obs.); another group in UMNP grew from 35 to 49 members over five years (Jones et al. 2006). Solitary adult ?? occur (Homewood & Rodgers 1981, Wasser 1993, Dinesen et al. 2001, Ehardt 2001, Ehardt et al. 2005). In 2005 the study group of 47 animals in Mwanihana was comprised of five adult ?? (number fluctuated from two to five), 23 adult //, ten subadults, five juveniles and four clinging infants (ratio adult ?? to adult // = 1 : 4.6; immatures to adults = 1 : 1.47) (C. L. Ehardt pers. obs.). Groups form polyspecific associations with most of the other diurnal primate species in the Udzungwa Mts (Udzungwa Red Colobus Procolobus gordonorum, Peter’s Angola Colobus Colobus angolensis palliatus, Sykes’s Monkey Cercopithecus mitis) (Wasser 1993, Ehardt et al. 2005). One adult / Udzungwa Red Colobus moved and foraged

with the Mwanihana Forest study group of Sanje Mangabeys for three consecutive days; interactions between this / and group members were infrequent, although juvenile and subadult Sanje Mangabeys groomed her (C. L. Ehardt pers. obs.). In Mwanihana Forest Sanje Mangabeys were in polyspecific associations for ca. 28% of the sightings; the most frequent interspecific association for the Sanje Mangabeys was with Sykes’s Monkeys (ca. 52%, n = 25), ca. 54% of which involved a single adult ? Sykes’s Monkey. Associations with Udzungwa Red Colobus (28% of mangabey sightings) and Peter’s Angola Colobus (20% of mangabey sightings) were less frequent. Sanje Mangabey groups also associate with Natal Red Duiker Cephalophus natalensis and Crested Guineafowl Guttera pucherani (C. L. Ehardt pers. obs.). Oestrous adult // copulate with multiple adult ??; adolescent and juvenile ?? mount young adult // in first oestrus without interruption by adult ??. Dominant adult ? observed numerous times travelling and resting with an infant clinging to his ventrum. Male emits low, repetitive ‘ooh-ooh-ooh grunts’ when infant is clinging, especially following locomotion and before ? sits and infant dismounts. Male arches tail up and over back with tip at crown or side of head when giving the vocalization. Mother of infants follows behind ? and retrieves infant when it dismounts (C. L. Ehardt pers. obs.). Reproduction and Population Structure  Little known. Females exhibit perineal swellings and emit post-copulatory vocalizations; ?? are single-mount ejaculators. Infants are carried on the ventrum during the first year; young juveniles sometimes carried ventrally for short distances. Singletons usually born, but one set of twins born in the habituated study group in Mwanihana Forest (n = >12 births). No pronounced mating/birth seasons, although birth peaks may exist; births in the habituated Mwanihana study group were not highly clumped across the year-long study but did not occur in all months (C. L. Ehardt pers. obs.). Predators, Parasites and Diseases  Predators include African Crowned Eagles Stephanoaetus coronatus, which are common in the Udzungwas and seen or heard on ca. 50% of observation days in Mwanihana Forest (Ehardt et al. 1999, 2005). Sanje Mangabeys give an alarm call when an eagle is detected. An adult African Crowned Eagle / was attacked and killed by an adult Sanje Mangabey ? as the bird attacked a subadult mangabey feeding in a Ficus tree (Jones et al. 2006). Other predators known to take primates in the Udzungwa forests are Leopards Panthera pardus, Lions Panthera leo, various venomous snakes, and humans (see below). There is no information on parasites or other diseases. Conservation  IUCN Category (2012): Endangered. CITES (2012): Appendix II. Sanje Mangabeys are threatened due to habitat loss and alteration, continued fragmentation of their small populations, and hunting by local people (Ehardt et al. 2005, Ehardt & Butynski 2006a, Rovero 2007, Rovero et al. 2012). Hunted with dogs and nets by local nonMuslim people (Homewood & Rodgers 1981). Hunting is largely controlled in UMNP, but mangabeys are sometimes caught in snares (A. R. Marshall pers. comm., C. L. Ehardt pers. obs.), that were likely set for other prey such as small antelope. Concern for the persistence of this Tanzanian endemic monkey is great, especially given that ca. 40–50% of the world’s population 179

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resides outside of UMNP, in the poorly protected USFR. The two most important actions that can be taken on behalf of the longterm conservation of the Sanje Mangabey are to upgrade the status of USFR to that of a Nature Reserve, and to establish the ‘Mngeta Conservation Corridor’ as this would link USFR with the southern forests of UMNP (Marshall et al. 2007, Rovero et al. 2012).

GWS (//): 72, 76 mm, n = 2 No body measurements available, and only two skulls, both collected in Mwanihana Forest, one by A. R. Marshall and one by F. Rovero. Key References  Ehardt 2001; Ehardt & Butynski 2006a; Ehardt et al. 1999, 2005; Homewood & Rodgers 1981; Rovero et al. 2011; Wasser 1993.

Measurements Cercocebus sanjei GLS (//): 104, 113 mm, n = 2

Carolyn L. Ehardt & Thomas M. Butynski

Cercocebus atys  Sooty Mangabey (Smoky Mangabey) Fr. Mangabé fuligineux; Ger. Russmangabe Cercocebus atys (Audebert, 1797). Histoire Naturelle des Singes et des Makis 4 (2) 13. West Africa.

Sooty Mangabey Cercocebus atys adult male.

Taxonomy  Monotypic species. Considered by some to be a subspecies of the Red-capped Mangabey Cercocebus torquatus (Dandelot 1974, Groves 1978, Napier 1981, Grubb et al. 1998) but not by most authorities, particularly in recent years (Booth 1956a, 1958b, Hill 1974, Oates 1996a, Kingdon 1997, Groves 2001, 2005c, Grubb et al. 2003). Type locality given as ‘Indes orientales’ but type label is marked ‘Afrique occidentale’ (Schwarz 1928d). White-naped Mangabey Cercocebus lunulatus often treated as a subspecies of C. atys (e.g. Booth 1956a, 1958b, Groves 1978, 2001, 2005c, Kingdon 1997, Grubb et al. 2003) but recognized as a species by Oates (2011) and here. Synonyms: aethiopicus, aethiops, fuliginosus. Chromosome number: 2n = 42 (Brown et al. 1986). Description  Medium-size, slender, slate-grey (sometime light brown) monkey with long limbs and tail. Sexually dimorphic. Body

Cercocebus atys

weight of adult // about 60% that of adult ??. Sexes similar in colour. Muzzle and ears blackish. Whiskers light grey. Face greyishpink or pinkish. Eyelids off-white (not pure white). Iris olive. Crown usually without crest or whorl. Dorsum usually slate-grey though light brown in some individuals. Ventrum and inner limbs cream to light grey. Hands, feet and top of tail slightly darker grey than dorsum. Palms and soles black. Scrotum pinkish. Sexual skin of / rosy pink. Depressions in the skull’s suborbital region combined with facial prognathism give a hollow-cheeked appearance. Infants and juveniles like adults, though suborbital excavation not as pronounced. Geographic Variation  None recorded. Similar Species Cercocebus lunulatus. Between Sassandra and Volta Rivers. Nape (posterior crown) with concentric, V-shaped, or oval whitish

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patch. Whorl of hairs on crown. Crown hairs without strawcoloured band. Ventrum pure white. Distinct, dark spinal stripe. Distribution  Rainforest BZ. Endemic to Upper Guinea Forests from Niadiou Village, Senegal (12° 30´ N, 16° 05´ W; Struhsaker 1971a) to the Nzo–Sassandra River System, Côte d’Ivoire (Wolfheim 1983, Kingdon 1997, Grubb et al. 1998, Groves 2003). Habitat  Primary forest preferred, but present, even abundant, in secondary forest. In high forest, gallery forest, coastal forest, Raphia palm swamp and mangrove, and farm bush. Probably always near water (Booth 1956a, Oates et al. 1990, Fimbel 1994b, Grubb et al. 1998, McGraw & Sciulli 2011). A frequent crop raider able to effectively utilize cultivated areas (Hill 1974, Fimbel 1994b). Abundance  One of the more common monkeys in West Africa (Wolfheim 1983, Kingdon 1997). Surveys and reports from Côte d’Ivoire, Liberia and Sierra Leone suggest that this species’ abundance is due to its ability to exploit a variety of habitat types (Davies 1987, Oates et al. 1990, Fimbel 1994a). Reported densities are 11.9 ind/km2 at Taï N. P., Côte d’Ivoire (McGraw & Zuberbühler 2007), and 38.5 ind/km2 on Tiwai I., Sierra Leone (Oates et al. 1990). The following estimates are based on a 2006– 08 study in Taï N. P. (3300 km²); 10.5 ind/km², 0.64 groups/km², and total of ca. 63,000 individuals (N’Goran et al. 2012). Adaptations  Diurnal and predominantly terrestrial. Males have large canines. Light-coloured eyelids are flashed as threats during agonistic encounters. During these threats ?? commonly arch the tail over the rump in combination with yawns to display canines. The high masticatory forces needed to crush hard nuts are evident in various craniodental characteristics: these monkeys possess powerful jaws and teeth, their premolars are greatly expanded and the cheekteeth become heavily worn at early ages (Fleagle & McGraw 1999, Daegling et al. 2011, McGraw et al. 2011, 2012). Features of the humerus, ulna and radius reflect the frequent and aggressive use of the forelimbs to search for and process foods from the forest floor (Nakatsukasa 1996, Fleagle & McGraw 1999, 2002). When alarmed on the ground, Sooty Mangabeys jump into short trees. Flight from predators, however, occurs on the ground. Experimental evidence from the Taï Forest indicates that of the seven sympatric cercopithecids present, C. atys is the best at detecting ground predators from the greatest distance (McGraw & Bshary 2002). Vocal repertoire consists of 19 distinct vocalizations including ‘grunts’, ‘twitters’, ‘screams’ and ‘growls’ (Range & Fischer 2004). Copulation calls given by // only. Adult ?? give ’whoop-gobble’ long/loud call, that is similar to whoop-gobbles given by Lophocebus (Struhsaker 1971a, Waser 1982). Males and // both give distinct alarm calls to snakes (e.g. Gabon Viper Bitis gabonica, Black-necked Spitting Cobra Naja nigricollis), African Crowned Eagles Stephanoaetus coronatus and Leopards Panthera pardus (Range & Fischer 2004). Foraging and Food  Omnivorous. Foraging occurs at all forest levels but most food is obtained from the forest floor and includes fallen fruits and seeds, mushrooms, insects and leaves (Bergmueller 1998,

Fleagle & McGraw 2002, McGraw & Zuberbühler 2008, McGraw et al., 2011). In Taï N. P., spends 67% of time, 85% of travel, and 71% of foraging on the ground (McGraw 2007a). Mean home-range size for groups in Taï N. P. is 4.92 km2 with the largest home-range being 8.0 km2. Average daily path length for one group followed for 58 days was 2.2 km (0.8–3.8) (Rutte 1998). Sooty Mangabeys have spatial memory of fruiting states of trees and this helps shape foraging routes (Janmaat et al. 2006). Two particularly important foods are Sacoglottis gabonensis and Anthonata fragrans (Bergmueller 1998, Rutte 1998, Daegling et al. 2011, McGraw et al. 2011). Considerable foraging time is spent pawing through the leaf litter on the forest floor looking for fallen fruits, nuts and seeds. Skeletal adaptations of the forelimb and dentition reflect this reliance on manual foraging and seed predation. Compared to arboreal mangabeys (genus Lophocebus), the forelimb bones of C. atys possess much larger muscle markings indicative of frequent and aggressive use of forelimbs to access food on or near the ground. In these respects, the foraging ecology and accompanying morphology of Cercocebus are similar to those of Drills Mandrillus leucophaeus and Mandrills Mandrillus sphinx (Fleagle & McGraw 1999, 2002). Social and Reproductive Behaviour  Highly social. Live in large, multimale, multifemale groups with a complex social organization. Typical groups number 75–100 individuals. One group of 120 individuals studied for 10 months consisted of 6–10 adult ??, 24–34 adult //, 29–34 juvenile ??, 17–26 juvenile // and 4–22 infants (Range & Noë 2002, 2004, Range 2005, 2006).The group’s core consists of related //; ?? disperse from their natal groups. Home-ranges overlap significantly with those of neighbouring groups. Territorial encounters between groups are infrequent and inter-group spacing appears to be maintained by the whoop-gobble calls of adult ??. During inter-group encounters, both sexes may engage in threats and chases though such incidents usually involve // only (F. Range pers. comm.). Non-resident adult ?? are often seen travelling and foraging alone. The dominance system in captive C. atys is not based on maternal dominance rank (Bernstein 1976, Ehardt 1988, Gust & Gordon 1994, Gust 1995). In contrast, studies on grooming partners and association frequencies of freeranging populations in Taï N. P. indicate that the dominance system is matrilineal-based (Range & Noë 2002, Range et al. 2007). Polyspecific associations with arboreal monkeys are common but there are no data quantifying the frequency of these associations. Arboreal monkeys often respond to the presence of Sooty Mangabeys by descending and foraging to lower forest levels, including the ground (McGraw & Bshary 2002). In captivity and the wild, // typically carry infants but ?? also do so (Busse & Gordon 1984, W. S. McGraw pers. obs.). Reproduction and Population Structure  Visible changes in sexual skin of // include a bright pinkening in the peri-anal region and correspond to ovulation (Gust 1995). Gestation (captivity) is ca. 175 days and a single infant is born (n = 198; Gust et al. 1990, Gordon et al. 1991). Twins have not been reported (Gust et al. 1990). There is a distinct mating season in Taï N. P. from Jun–Oct and the birth season is Oct–Mar (n = 52 births) with a peak during the Dec– Feb dry season. Interbirth interval ca. 2 years (Range et al. 2007). Females (captivity) first reproduce at 3.1 years (Ross 1991). Males 181

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(captivity) reach sexual maturity at ca. 7 years (Gust & Gordon 1991, Gust et al. 1998). Birth rate (captivity) is 0.92. Maximum life-span (captivity) is 18 years (Ross 1991). Predators, Parasites and Diseases  Sooty Mangabeys fre­ quently preyed upon by African Crowned Eagles Stephanoaetus coronatus and Leopards Panthera pardus (Shultz et al. 2004, McGraw et al. 2006a, Shultz & Thomsett 2007, Zuberbühler & Jenny 2002, 2007). Occasionally eaten by Robust Chimpanzees Pan troglodytes (Boesch & Boesch-Acherman 2000). The Sooty Mangabey is the primate reservoir of HIV-2, a less common strain of the AIDS virus. Transmission of this disease to humans probably occurred the first half of the twentieth century and involved the butchering of monkeys killed for consumption (Hirsch et al. 1989, Chen et al. 1996, Hahn et al. 2000, Lemey et al. 2003, Silvestri 2005). Conservation  IUCN Category (2012): Near threatened. CITES (2012): Appendix II. There are no recent census data on the species, but numbers are undoubtedly decreasing owing to habitat loss and poaching (McGraw 2007b, Oates 2011). Dwindling habitat has forced this monkey to exploit cultivated lands, where farmers hunt them with dogs.

Measurements Cercocebus atys HB (?): 580 mm, n = 1 HB (//): 500 (470–520) mm, n = 3 T (?): 600 mm, n = 1 T (//): 580 (520–645) mm, n = 2 HF (?): 157 mm, n = 1 HF (//): 146 (145–147) mm, n = 3 E (?): 28 mm, n = 1 E (//): 31 (26–35) mm, n = 3 WT (??): 10.6 (9.5–11.4) kg, n = 4 WT (//): 6.2 (5.6–7.0), kg, n = 4 GLS (??): 132 mm, n = 11 GLS (//): 115 mm, n = 2 GWS (??): 87 mm, n = 11 From various localities. Linear body measurements from Hill (1974). Body weights from Oates et al. (1990) and W. S. McGraw (pers. obs.). Skull measurements from Groves (1978); ranges not provided. Key References  Bergmueller 1998; Fleagle & McGraw 2002; Gust et al. 1990; McGraw & Zuberbühler 2008; McGraw et al. 2007; Oates 2011; Range & Noë 2002. W. Scott McGraw

Cercocebus lunulatus  White-naped Mangabey (White-crowned Mangabey) Fr. Mangabé couronné; Ger. Weißcheitelmangabe Cercocebus lunulatus (Temminck, 1853). Esquisses Zoologiques sur la Côte de Guiné, p. 37. Forest along Boutry R., Gold Coast [Ghana].

White-naped Mangabey Cercocebus lunulatus.

Taxonomy  Monotypic species. Described, named and first recognized as a species by Temminck (1853). This designation subsequently supported for many years by a number of taxonomists, including Pocock (1906) and Elliot (1913b), and is the taxonomy used by Oates (2011) and in this profile (see below). Note that the type locality, ‘Boutry R.’ is better known (at least today) as the ‘Ankobra R.’ with Princes’ Town (= ‘Butri’) at its mouth.

Treated as a subspecies of the Red-capped Mangabey Cercocebus torquatus by Schwarz (1928d) and others, including Dandelot (1974), Groves (1978d) and Napier (1981). More recently regarded as a subspecies of the Sooty Mangabey Cercocebus atys by Booth (1956a, b, 1958b), Dobroruka & Badalec (1966), Hill (1974), Grubb (1978, 1982), Kingdon (1997), Groves (2001, 2005c), Grubb et al. (2003) and McGraw & Fleagle (2006). Grubb (1978, 1982) and McGraw & Fleagle (2006) argue that lunulatus derived from C. atys and that C. torquatus derived from lunulatus. However, both phenotypically and morphologically, lunulatus appears to be intermediate to C. atys and C. torquatus (Groves 1978, 2001) – although the number of available lunulatus specimens for study is small. For example, lunulatus is intermediate in colour of the eyelids, colour and banding of the hairs of the crown, colour of the dorsum, ventrum, tail and limbs, extent of white on the head and neck, development of the dorsal stripe, and size of the skull (perhaps also size of the body). In addition, the geographic distribution of lunulatus lies between C. atys and C. torquatus. As such, C. P. Groves, J. Kingdon and W. S. McGraw (pers. comm.) now suspect that lunulatus derived from an ancient hybridization between C. atys and C. torquatus. Synonyms: none. Chromosome number: 2n = 42 (Groves 1978). Description  Medium-sized, gracile, brownish-grey monkey with long limbs and tail, and white or off-white patch on posterior of crown (i.e. nape). Sexes similar in colour but // smaller; skull

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measurements of adult / ca. 90% that for adult ?? (Groves 1978). Adult // body weight ca. 54% that of adult ??. Face and ears pinkish. Muzzle sometimes light grey (A. Galat-Luong pers. comm.). Eyelids off-white. Whiskers form horizontal crest half-way down cheeks with convergence of dark grey hairs of upper cheek with upwards-directed white hairs of lower cheek. Forehead with line of sparse, black, vibrisssal hairs. Anterior of crown with blackish-brown whorl; hairs not banded or speckled straw-yellow. Nape with large V-shaped, oval, or crescent-shaped patch of pale yellowish-white or white, bordered with black. Parietal-occipital and temporal lines bounding crown brownish-black or indistinct. Dorsum variable, from pale gold-blond to dark sooty-grey (A. Galat-Luong pers. comm.). Flanks, outer limbs, tail tip and underside of tail usually brownish-grey or smoky-grey, sometimes yellowish-brown. Dorsal stripe from neck to tail distinct, dark brown to greyish-brown. Dark flanks sharply demarcated from light underparts. Tail dark grey or blackish above and on sides – almost as dark as dorsal stripe. Hands and feet brownish-black, only slightly darker than outer limbs. Sides of head, front of shoulders, throat, ventrum and inner legs pure silvery-white, sometimes yellowish-white on belly. Throat and upper chest sometimes yellow (A. Galat-Luong pers. comm.). Callosities pink. Sexual skin of adult / bright rosy pink. Juvenile with dorsum more yellowish or reddish, especially on limbs; nape-patch slightly rusty (Hill 1974). Infant born with pale skin on face, hands and feet, and without dorsal stripe or white patch on nape. Dorsal stripe and white on nape begin to appear at about four days and about ten weeks, respectively (Field 1995a). Geographic Variation  None recorded. Similar Species Cercocebus atys.Apparently narrowly sympatric.West of Nzo-Sassandra R. System, Côte d’Ivoire. Booth (1958b) observed both C. atys and C. lunulatus, but no intermediate forms, between the Nzo R. and Sassandra R. in the vicinity of Guiglo (06° 31´ N, 07° 30´ W; on Lac de Buyo near mouth of Nzo R.). Groves (1978), however, reports an intermediate (hybrid?) specimen from this region that lacks the white on the nape yet has a whitish ventrum. Nape black or blackish. Hairs of crown with straw-coloured band. Crown without a whorl. Dorsal stripe absent or indistinct. Ventrum light grey. More robust (A. Galat-Luong pers. comm.). Distribution  Endemic to Côte d’Ivoire, Ghana and Burkina Faso. Rainforest BZ. Distribution highly fragmented. East of NzoSassandra River System, W Côte d’Ivoire, from coast north to near Guiglo (ca. 06° 44´ N, 07° 20´ W), and near Goudi (ca. 06° 07´ N, 05° 06´ W, near Lamto along Bandama R.; Bourlière et al. 1974), eastward into SW Ghana where southern limit is the coast, eastern limit known to approach to ca. 55 km of the Volta R., northern limit is the Afram R. (Booth 1958b) and north-east limit is the Digya N. P. (07° 23´ N, 00° 37´ W; R. Dowsett & F. Dowsett-Lemaire pers. comm.; S. Gatti & S. Wolters pers. comm. to J. Oates). From the distribution map in Grubb et al. (1998), northern limit in Ghana does not reach the Tain R., or the towns of Wenchi or Techiman, and is at ca. 07° 24´ N. Formerly ‘regularly’ encountered in forest islands and gallery forest of the Comoé N. P., Côte d’Ivoire (Mühlenberg & Steinhauer-

Cercocebus lunulatus

Burkart 1982, G. Galat & A. Galat-Luong pers. comm.). Present as an isolated population along the Comoé R. in southern Comoé N. P. (ca. 09° 01´ N, 03° 44´ W; Fischer et al. 2000). Present also in a newly discovered, and apparently isolated, population along the Comoé R., ca. 140 km farther up river in AGEREF/Comoé–Léraba Reserve, SW Burkina Faso (09° 55´ N, 04° 37´ W; Galat & GalatLuong 2006b). Mangabeys reported to be to the north of Guiglo between Nzo R. and Sassandra R. on Mt Péko and in Mt Sangbé N. P. If present, the species of Cercocebus there needs to be determined (G. Campbell pers. comm.). Extent of occurrence roughly 51,000 km² (Y. de Jong & T. Butynski pers. obs.) but area of occupancy much less than this. Habitat  In primary and secondary moist forest, mangrove, coastal forest, gallery forest and inland swamps, especially Raphia palm swamps. Of 11 encounters in Comoé N. P., seven in gallery forest, three in forest islands and one on a cliff (G. Galat pers. comm.). B. Kunz (pers. comm.) encountered C. lunulatus 22 times in Comoé N. P. and estimates that these represented four or five groups. Sixteen encounters in or on the edge of gallery forest, three in savanna, and three in or on the edge of forest islands. Apparently always in or near damp or wet habitats (e.g. palm swamps and seasonally flooded forest). Enters rice paddies and farm bush (Booth 1956a, 1958b). Mean annual rainfall over geographic range of C. lunulatus ca. 900 mm in SW Burkina Faso to 2000 mm on coast of Ghana and Côte d’Ivoire. Mean annual temperature over geographic range ca. 25–28 °C. Altitudinal range is from near sea level to roughly 300 m (e.g. at Comoé N. P.; F. Fischer pers. comm.). Abundance  Already rare throughout most of range during 1990s (see Conservation). ‘Regularly’ encountered in forest islands and gallery forest of the Comoé N. P. Of the 183 groups of primates encountered by G. Galat & A. Galat-Luong (pers. comm.) during 1980–86, 11% were C. lunulatus. Of the eight species of diurnal 183

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primates in Comoé N. P., C. lunulatus was the fourth most abundant behind the Olive Baboon Papio anubis (34%), White-thighed Colobus Colobus vellerosus (19%) and Lowe’s Monkey Cercopithecus lowei (12%). Density in gallery forest of the Comoé R., in AGEREF/Comoé– Léraba Reserve, is about 5 ind/km² (G. Galat & A. Galat-Luong pers. comm.). In the protected areas in Ghana where Magnuson (2002) found C. lunulatus, the encountered rate was 0.03–0.08 groups/km. Observed seven times during 2006–08 in Ankasa Resource Reserve, Ghana (0.07/h, n  = 2468h; 0.002/km, n = 3704 km; Gatti 2009). Adaptations  Diurnal and semi-terrestrial. Sleeps in trees in gallery forest or on forest islands. Foraging and Food  Omnivorous. In AGEREF/Comoé–Léraba Reserve group home-range extends for >1.5 km in the ca. 100 m wide gallery forest along the Comoé R. and adjacent savanna. Cercocebus lunulatus enters savanna for a distance of ca. 1 km to feed in fruiting trees (G. Galat & A. Galat-Luong pers. comm.). One group of ten individuals at AGEREF/Comoé–Léraba Reserve had a homerange of >2 km² (G. Galat & A. Galat-Luong pers. comm.). Cercocebus lunulatus probably spends the majority of its time on the forest floor but uses all forest strata. In Comoé N. P. eats ripe fruits of Lannea welwitschii, Tamarindus indica and Dialium guineense, unripe and ripe fruits of Lannea acida and Diospyros mespiliformis, unripe fruit and leaves of Sarcocephalus latifolius, unripe seeds of Daniellia oliveri, Cynometra megalophylla and Parkia biglobosa, flower buds of Ceiba pentandra and the bases of green grasses (B. Kunz pers. comm.). Eats maize and rice in Ghana (Booth 1958b, Jeffrey 1970), and fruits of Saba senegalensis and Dialium guineense in Burkina Faso (Galat & GalatLuong 2006b). Social and Reproductive Behaviour  Social. Groups of 3–23 animals in Comoé N. P.; one group of 23 comprised six infants in May 1998 (Fischer et al. 2000). Here, B. Kunz (pers. comm.) made complete counts of three groups (23, 25–30, 58 individuals, mean= ca. 36). Two groups in AGEREF/Comoé–Léraba Reserve comprised six and 13 individuals. The group of 13 comprised one adult ?, four adult //, seven young and one clinging infant (A. Galat-Luong & G. Galat pers. comm.). In Ghana hunters commonly report historic sightings of groups of >50 individuals (L. Magnuson pers. comm.). Vocalizations include: ‘chirps’, ‘shreeks’, ‘coh coh’ grunts, ‘woof woof’ grunts, ‘whoop-gobbles’ and ‘karakoo’ barks. Whoopgobble and karakoo barks only given by adult ??. Whoop-gobble + karakoo bark bouts include 2–8 whoops followed by 10–75 sec silence, followed by four to many karakoo barks. The karakoo barks may continue to be given for >20 min. For some karakoo bark bouts, the last call is a ‘karakoo oo oo’. Whoop-gobble + karakoo barks most frequent at night (01:00–05:00h) in series of two or three bouts, and in the early morning (05:00–07:45h). Duets of numerous whoop-gobbles occur between two groups, with only the last whoop-gobble followed by karakoo barks (A. Galat-Luong & G. Galat pers. comm.). In captivity / emits ‘coh’ call before copulation and ? emits ‘oh oh oh’ call during copulation (A. Galat-Luong pers. comm.). In AGEREF/Comoé–Léraba Reserve territorial conflicts include whoop-gobbles and karakoo barks of adult ?, karakoo bark

choruses of other adults and of subadults, chirps of young and other individuals, and contact fights between adults (A. Galat-Luong & G. Galat pers. comm.). In Comoé N. P., G. Galat & A. Galat-Luong (pers. comm.) observed C. lunulatus in associations with other species of monkey 4% of the time (n = 183 encounters); C. lowei, Lesser Spot-nosed Monkey Cercopithecus petaurista, P. anubis and C. vellerosus. Cercocebus lunulatus was sometimes in association with up to at least three other species at one time; for example, with C. lowei, C. petaurista and P. anubis, or C. lowei, C. petaurista and C. vellerosus. In AGEREF/Comoé– Léraba Reserve C. lunulatus forms polyspecific associations with Green Monkeys Chlorocebus sabaeus (Galat & Galat-Luong 2006a). In Ghana observed with C. lowei and Roloway Monkeys Cercopithecus roloway (L. Magnuson pers. comm.). Inter-specific interactions include supplantation of an adult / + clinging infant C. lowei; whoop-gobble + karakoo bark bouts in response to Patas Monkey Erythrocebus patas and P. anubis barks; and karakoo bark-induced C. lowei loud-calls (A. Galat-Luong & G. Galat pers. comm.). On one occasion B. Kunz (pers. comm.) observed several Olive Baboons chase 3–5 C. lunulatus from a fruiting D. mespiliformis in which they were feeding. On another occasion one C. lunulatus fed near a group of Olive Baboons on unripe pods of P. biglobosa. Cercocebus lunulatus in captivity spontaneously use sticks (tools) to scratch (groom) themselves in order to decrease stress. Sticks 10–40 cm long are prepared by removing the leaves and twigs. If the stick is too long it is broken into two pieces.Two sticks may be used simultaneously, either hand + hand, or hand + foot. Body parts that are difficult or impossible to reach with the hands or feet are scratched (e.g. inside of the ears) (Galat-Luong 1984, A. Galat-Luong pers. comm.). Reproduction and Population Structure  Minimum length of oestrous cycle in captivity is 19 days. Gestation is reported as 152–180 days (Field 1995b). Gestation at London Zoo and Dublin Zoo reported as 5.5–6.0 months and 5.0 months, respectively (A. Payne pers. comm.). Flamingo Land reports a gestation of 5.5 months. Over 51 births in captivity, including 36 at Ménagerie du Jardin des Plantes (G. Pothet pers. comm.). Thirty-seven per cent of the 51 infants born in captivity died, most of them when 220 births at DRBC. Inter-birth interval variable (mean = 473 days, 209–991 days, n = 140). Inter-birth interval significantly shorter after an infant death (Wood 2007). Many "" reproduce annually. As breeding is seasonal at DRBC, infants are born into ready-made peer groups (Wood 2007). Drill mothers do not actively wean their young; as infants become less dependent on their mothers they still nurse opportunistically until the next offspring is born. Juveniles spend most of their time in playgroups. With the onset of puberty at three years "" begin to break away from playgroups and join adult society. While sexually mature !! do not reach their full size, including expression of secondary sexual characteristics until 8–10 years. No observations reported on social structure or reproductive parameters of wild Drills. At DRBC, family members, particularly "", maintain lifelong affiliations. There is one dominant !, and other adult !! are either group-associated or solitary. Group-associated !! interact with other group members, but may be aggressively pursued by the dominant ! when attempting to mate. Solitary !! appear to avoid group contact, leaving an area when a group approaches (Wood 2007). DRBC !! show signs of aging by 14 years and sometimes as early as 11 years, and typically die of ‘old age’ without specific pathology at 16–19 years (E. Gadsby pers. obs.). Probably die earlier in the wild. Mortality of wild-born !! in all age classes at DRBC is significantly higher than for "". At 20 years, oldest " at DRBC continues to

cycle and bear young. Longevity record in captivity is 28 years for !! and 37 years for "" (Jones 1962, Knieriem & Cox 2002). Predators, Parasites and Diseases Few data. Leopards Panthera pardus are probably predators on the mainland. Leopards absent from Bioko. CentralAfrican Rock Pythons Python sebae are probably a predator both on the mainland and on Bioko. Humans are the major predator of the Drill, both on the mainland and on Bioko (see Conservation below). Parasites found in wild Drill faeces from Afi Mountain, Nigeria are: Balantidium coli, Blastocystis hominis, Endolimax nana, Entamoeba chattoni, E. coli, E. hartmanni, E. histolytica dispar, Enteromonas hominis, hookworm sp., Iodamoeba buetschlii and Trichomonas sp. (J. Lewis pers. comm.). Drills have their own simian immunodeficiency virus (SIVdrl) (Clewley et al. 1998) found asymptomatically in about 20% of incoming wild Drills at DRBC. Other species-specific viruses isolated from wild-born Drills at DRBC are cytomegalovirus (DrCMV) and foamy virus (SFV-drl) (Blewett et al. 2003). Conservation IUCN Category (2012): Endangered. CITES (2012): Appendix I. The Drill is the African primate with highest conservation priority (Oates 1996a). Populations reduced throughout small historic range and eliminated from much of range due to commercial bushmeat hunting and habitat loss (Wolfheim 1983, Lee et al. 1988, Gadsby 1990, Oates 1996a). In the early 1980s commercial hunting for bushmeat became the greatest threat for the Drill. Both on the mainland (Gadsby et al. 1994) and on Bioko I. (Butynski & Koster 1994, Hearn et al. 2006), Drill is a preferred bushmeat and hunting is widespread and often intense. Drills are hunted at all sites with shotguns and sometimes with dogs. Dogs hold a group at bay in trees while one or more hunters massacre the animals in the group (Gadsby et al. 1994, Waltert et al. 2002); without dogs, hunters are unlikely to kill more than two or three Drills during an encounter. In Korup hunters claim to kill from 2 to 25 Drills during these encounters, with a mean of 7.2 taken (Steiner et al. 2003). In many areas commercial hunters work from semi-permanent camps in the forest, periodically carrying out head-loads of smoked or fresh meat to traders who transport it to urban markets. As a result of widespread and intensive hunting, Drill super-groups have rarely been seen since the mid-1980s in Nigeria but still occurred, albeit at lower frequency, or with smaller-sized super-groups, in Cameroon (Gadsby & Jenkins 1998, Wild et al. 2005). According to Gadsby et al. (1994: 443): ‘The relentless persecution reduces group size, lowers density, increasingly isolates groups of Drills, and may also be affecting behavioural and ecological strategies. It is becoming apparent that the formation of super-groups, which may play a crucial role in transfer of individuals, and thus genetic material, is occurring with decreasing frequency.’ In Nigeria, >60% of remaining Drill habitat lies within Cross River N. P. (3440 km2 in two discontiguous divisions). In Cameroon, Korup N. P. (1259 km2) supports Drills and has a 17 km common boundary with Cross River N. P. On Bioko I. Drills occur both in the Pico Basile N. P. (330 km2) and in the Gran Caldera and Southern Highlands Scientific Reserve (510 km2). In none of these ‘protected areas’, however, is protection effectively enforced, and Drill subpopulations in all areas are probably in decline (Gadsby et al. 1994, Waltert et al. 2002, Steiner et al. 2003, Hearn et al. 2006). There is meaningful protection for Drills in Afi Mountain Wildlife Sanctuary,

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Mandrillus leucophaeus

a small (ca. 100 km2) out-lying habitat at the north-west edge of Drill range (see below). However, the global population of Drills may be losing viability as subpopulations become smaller and increasingly isolated by habitat fragmentation (Gadsby & Jenkins 1998). Habitat loss and hunting continue to drive population decline. With reduced and scattered subpopulations, large aggregations of Drills (hordes or super-groups) that may facilitate both the exploitation of seasonally abundant fruit and the transfer of genetic material are increasingly rare. See also Ting et al. (2012). On Bioko I., Drills are sympatric with four other threatened species of primate (IUCN 2010); Red-eared Monkey (Vulnerable), Preuss’s Monkey Allochrocebus preussi (Endangered), Pennant’s Red Colobus Procolobus pennantii (Critically Endangered) and Black Colobus (Vulnerable). In addition, seven of Bioko’s 11 species of primate are listed as ‘Endangered’ at the subspecies level (Butynski & Koster 1994, Hearn et al. 2006, IUCN 2010). Six subspecies of primate are endemic to Bioko. No place in Africa, perhaps no place in the world, has so many threatened endemic taxa of primate in such a small area (2017 km2). None the less, hunting of all seven of Bioko’s monkey species for the commercial bushmeat trade continues unabated, driving all species closer to extinction on the island (Fa et al. 1993, Colell et al. 1994, Hearn et al. 2006). Drill group encounter rates during primate census on Bioko declined ca. 33% during the 20 years from 1986 to 2006 (Hearn et al. 2006). Bushmeat surveys were conducted at the Malabo bushmeat market for 5–6 days/week from Oct 1997–Sep 2007. During this period, 2366 Drill carcasses were tallied. The total number is certainly greater as the market surveyor was not present all day every day. Island-wide questionnaire surveys were used to assess the percentage of Drill carcasses brought to this market; results indicated that ca. 60% of the Drills killed on Bioko are sold at the Malabo bushmeat market. If so, the total number of Drills killed on Bioko by hunters during this period is estimated at ca. 3940 (W. Morra & G. Hearn pers. comm.). In 1998, 226 Drills were counted at the Malabo bushmeat market during 283 days of survey. In 2006, 544 Drills were counted at the same market during 304 days of survey. Of these, 243 (45%) were adult !!, 198 (36%) were adult "", 96 (18%) were immature and 7 (1%) had no age/sex data recorded (W. Morra & G. Hearn pers. comm.). If 544 Drills is 60% of the number killed, then roughly 900 Drills were killed by hunters on Bioko in 2006. Continued rapid decline in Drill distribution and abundance on Bioko indicates that this level of exploitation is far from sustainable. The mean price paid per adult ! Drill at the Malabo bushmeat market changed from ca. US$31 in 1997 to ca. US$142 in 2007, a more than four-fold increase (Reid et al. 2005, W. Morra & G. Hearn pers. comm.). Less than 0.1% of the people of Bioko hunt monkeys. Monkey hunting accounts for 3300 m), in any habitat, from evergreen forest to semi-desert, that affords food, a night refuge on rock faces or in tall trees, and surface water. Papio baboons are, however, notably absent from western central African rainforest areas occupied by Mandrills Mandrillus sphinx or Drills Mandrillus leucophaeus, and from the central Congo Basin. Papio exhibits the distinctive features of cercopithecine and papionin monkeys (e.g. buccal pouches, dental traits). They are distinguished from their closest relatives, the other African papionins (Mandrillus, Kipunji Rungwecebus kipunji, drill-mangabeys Cercocebus spp. and, especially, Geladas Theropithecus gelada and baboonmangabeys Lophocebus spp.) by the following combination of features, some of which are probably ancestral for the African papionin clade: size large (adult !! >14 kg, >20 kg in most populations); muzzle prominent, defined by marked concavity of the ante-orbital

Olive Baboon Papio anubis

Yellow Baboon Papio cynocephalus

Chacma Baboon Papio ursinus

Skulls of four baboon Papio species.

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and habitat diversity. The ecological diversity of the genus makes it especially amenable to studies of the interaction between habitat and behaviour – especially social behaviour (e.g. Hill & Dunbar 2002). Most inter-populational differences in physique and physiology, however, are not obviously related to ecological adaptation. The one major exception is P. hamadryas, whose social system, and correlated features of pelage, development and physiology, can be seen as adapted to the semi-arid environments. Genetic and palaeontological information suggest that the last common ancestor of the extant Papio clade lived in southern Africa ca. 2 mya (Delson 1988, Wildman et al. 2004, Burrell et al. 2009, Zinner et al. 2009b). Baboons seem to have spread rapidly from this base during the Pleistocene, presumably diversifying as their range was dissected by climatically driven changes in habitat distribution. Until the late Pleistocene, however, Papio is far rarer in the fossil record than its close relative Theropithecus, which is now reduced to a single, relict species. As the species accounts indicate, some populations of Papio have been studied in depth for more than 30 years, but these studies divulge but a small fraction of the variation within this ecologically diverse genus. The natural history and behaviour of other populations, including the widespread and distinct Kinda Baboon (regarded here as a subspecies of the Yellow Baboon P. c. kindae, but see Zinner et al. 2011), remain largely undocumented. Though the main outlines of intra-generic diversity of Papio are relatively clear, the taxonomy of Papio is disputed, largely because of conflicting species definitions. Diagnosable geographical ‘forms’ within the genus have parapatric ranges, and most, perhaps all, interbreed at their boundaries, forming hybrid zones (Jolly 1993, Kingdon 1997). Thus, they might be distinguished as full (phylogenetic) species, or regarded as subspecies of a single, polytypic (biological) species (Papio hamadryas) (Jolly 1993, Sarmiento 1998a, b, Groves 2001, Frost et al.

2003).The five-species solution, adopted here, is a practical compromise that groups forms of generally similar external appearance. Another configuration, less defensible but commonly adopted (e.g. Smuts et al. 1987), separates P. hamadryas (‘the Desert Baboon’) as a distinct species, but groups all others (‘the Savanna Baboons’) as subspecies of a single species, P. cynocephalus.The latter taxon, however, appears not to be monophyletic, and the implication of an ecological and behavioural dichotomy is overly simplistic and even misleading. Regardless of the taxonomy used to express it, diversity within the genus Papio includes features hinting at a complex evolutionary history. Papio papio, for example, exhibits physical and behavioural traits (Jolly & PhillipsConroy 2006) that ally it most closely with the P. hamadryas, from which it is currently separated by at least 5500 km of P. anubis range. Genetic information suggests a history that includes deep genetic introgression between species (‘mitochondrial capture’), and possibly the formation of species by hybridization (Wildman et al. 2004, Burrell 2009, Zinner et al. 2009a, b, Keller et al. 2010, Zinner et al. 2011). The species (and subspecies) within the genus Papio are identified primarily by the colour and texture of the pelage (Hill 1970, Jolly 1993, Rowe 1996, Kingdon 1997, Groves 2001). Besides overall colour, important diagnostic features are the extent of development, if any, of a mane (= cape = mantle) of waved hair over the forequarters, or of a fringe of long, straight hairs on the trunk and nape; the extent to which pelage of the cheeks contrasts in colour and/or length with that of the crown; the presence/absence of contrastingly lighter ventral pelage; and the facial profile, especially the projection of the nose. All these diagnostic features are most fully developed in adult !!. Clifford J. Jolly

Papio papio GUINEA BABOON Fr. Babouin de Guinée; Ger. Guinea-Pavian Papio papio (Desmarest, 1820). Encyclopédie Méthodique, Mammalogie 1: 69. ‘Coast of Guinea’.

Taxonomy Monotypic species. Individuals of appearance intermediate between Papio papio and Olive Baboon Papio anubis

occur in Mali (Pollock in Sharman 1981) but little is known about this hybrid zone (Sarmiento 1998a). See molecular information in Zinner et al. (2011). Synonyms: olivaceus, rubescens, sphinx. Chromosome number: 2n = 42 (Romagno 2001). Description Medium sized, uniformly grizzled reddish-brown baboon. Female like !, but smaller, with barely half the body weight of the !. Face dark pinkish-purple. Male with distinct mane (= cape = mane) on shoulders. Tail arched; not ‘kinked’ or ‘broken’. Perineum varies from bluish-grey to mottled. Female has largest oestrous swelling of any monkey. Pelage changes from black to brown, skin from pink to black, by seven months of age. Whitish individuals (albinos?) occur (Dupuy & Gaillard 1970, A. Galat-Luong pers. obs.). Geographic Variation

Guinea Baboon Papio papio adult male.

None recorded.

Similar Species Papio anubis. Closely adjoining and probably parapatric range in Mali and perhaps Guinea. Said to be sympatric in Sierra Leone (T. S.

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Jones in Booth 1958b). Larger, with darker, greyish-brown pelage; mane of adult ! less pronounced; tail ‘broken’. Distribution Endemic to West Africa. Sudan Savanna and Northern Rainforest–Savanna Mosaic BZs. Atlantic coast eastwards to ca. 12°W, ca. 11–18° N. Historical Distribution Booth (1958b) set the historic northern limit in Mauritania, whereas Dupuy (1971) set the north-western limit at St Louis and Podor, Senegal. One ecological limit is the absence of broad-leaved trees and the dominance of Acacia nilotica (A. GalatLuong pers. obs.). Northern limit has moved south due to decreasing rainfall (Verschuren 1982). Some fragmented populations may still occur in Casamance, Senegal (13° 05´ N, 16° 20´W; Galat-Luong et al. 2006). Tahiri-Zagret (1976) noted that the Edinburgh Zoo, UK, received two P. papio from Ghana and speculated about the presence of the two species in Côte d’Ivoire.There are, however, no confirmed records for Ghana and G. Galat & A. Galat-Luong (pers. obs.) only found P. anubis in Côte d’Ivoire during nine years of fieldwork. Current Distribution S Mauritania south-east through Senegal, Gambia, Mali, Guinea-Bissau, Guinea into Sierra Leone; an area of >200,000 km2. Range of reintroduced individuals in Saloum, Senegal, is expanding (G. Galat & A. Galat-Luong pers. obs.). Habitat In all types of savannas. Preferred habitats include Sudanese shrubby wooded savannas and sub-Guinean mosaic woodlands (400–1200 mm annual rainfall). In Niokolo Koba N. P., Senegal, a representative area of the preferred habitat, time spent in scrub about 40%, in open woodland 29%, in forest 21%, in grass 6%, in bush 4% and in gallery forest 1000 m (Fouta Djalon, Guinea) and over the temperature range ca. 20–50 °C. In Niokolo Koba N. P. they sleep in tall trees, including Ceiba pentandra (85% of the sleeping trees, n = 52), Cola cordifolia, Erythrophleum suaveolens, Afzelia africana (Sharman 1981), Anogeissus leiocarpus, Antiaris africana (Ndiaye 1983) and B. aethiopium, near stream beds or on branches overhanging rivers (Sharman 1981, Adie et al. 1997). The same sleeping sites are often used (92 of 133 observation nights; Anderson & McGrew 1984). Daytime sleeping sites are located in the shadow of large trees, thickets, cliffs and caves (A. Galat-Luong pers. obs.). Guinea Baboons require surface water and typically drink at least once per day.

Papio papio

encounters; Lavocat 1997). In Upper Niger N. P., Guinea, Touré et al. (1997) estimated 46 ind/km2.Verschuren (1982) estimated 100,000 Guinea Baboons for an 8000 km2 area (12.5 ind/km2 ) in Senegal that included Niokolo Koba N. P. He rejected estimations of 200,000– 300,000 baboons made for this same area in 1977. Adaptations Diurnal and semi-terrestrial. In Senegal, although water is still available at the end of the dry season in river beds, Guinea Baboons (and Robust Chimpanzees Pan troglodytes) dig holes in sand near stagnant, putrid water. Thus, they drink sandfiltered water, cleaned of pathogenic microbes (Galat-Luong & Galat 2000).

Foraging and Food Omnivorous. In Niokolo Koba N. P., Guinea Baboons spend 24% of time feeding and 37% of time moving (Sharman 1981). Locomotion and feeding peaks occur 09:00– 11:30h and 15:30–18:00h (Boese 1973). Water pool use showed two peaks, 07:00–10:00h and 16:00–18:00h (Galat et al. 1997, Lavocat 1997). Moving also occurs during two periods, 08:00– 09:00h and 16:00–17:00h (Galat et al. 1997). In Niokolo Koba N. P. they feed on fruits (60% of feeding records), mainly of Adamsonia digitata, Saba senegalensis, Lannea acida, Vitex madiensis, Spondias mombin and B. aethiopicus. Also eaten are the shoots of Oxytenanthera abyssinica, seeds (17% of B. aethiopicus and Combretum spp.), various parts of C. pentandra, as well as buds, flowers, new leaves, roots, fungi, invertebrates, eggs and small vertebrates (n = 2024 feeding records, 58 food species; Sharman 1981). Other foods include the fruits of Mangifera indica, Parkia biglobosa, Borassus flabellifer, Parinari Abundance In Niokolo Koba N. P., Sharman (1981) estimated macrophylla and Bombax costatum (Ndiaye 1983), and the flowers of 5.5–8.7 ind/km2 (n = 2 groups), Verschuren (1982), Galat et al. Mitragyna inermis and leaves of Andropogon sp. (Lavocat 1997). Feed (1998a, b) 6.3 ind/km2 in 1990–93 (n = 305 group encounters), on floating water plants while wading in the Gambia R. (A. Galatand 7.3 ind/km2 in 1994–98 (n = 237 group encounters), while Luong pers. obs.). the densities of the ungulates were decreasing. In this National Park, Guinea Baboons open termitariums of Cubitermes sp., roll over density near water was higher, up to 19 ind/km2 (n = 365 group laterite boulders (Fady 1972, Sharman 1981, A. Galat-Luong pers. 219

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obs.), and follow fire in order to catch invertebrates and small vertebrates to eat (Ndiaye 1983, A. Galat-Luong pers. obs.). They ‘fish’ for oysters Etheria sp. (Ndiaye 1983); also feed on grasshoppers and Agama Lizards Agama agama; occasionally hunt Scrub Hares Lepus saxatilis, Bushbucks Tragelaphus scriptus and Red-flanked Duikers Cephalophus rufilatus (McGrew et al. 1978, Sharman 1981). Guinea Baboons enter mangrove swamps to feed on Fiddler Crabs Uca tangeri (A. Galat-Luong pers. obs.), raid crops, steal stored grain in villages and food left out at field camps. Local people say Guinea Baboons feed on the rumen and the intestines of recently dead cattle. They dig in the ground to reach salt (A. Galat-Luong pers. obs.). Day range is 4–13 km (mean 8, n = 49; Sharman 1981). Home-ranges of two neighbouring groups were 19 km2 and 43 km2, with 9 km2 overlap (Sharman 1981). Social and Reproductive Behaviour Social. In Niokolo Koba N. P., Guinea Baboons show a multi-level group structure (GalatLuong et al. 2006). First-level social unit is a ‘one-male unit’ (OMU) (Stammbach 1987), which is probably a matrilineal kin group (Sharman 1981). The OMU is best seen during feeding, foraging and sleeping periods. While moving, OMUs are led by an adult !. While resting, a subadult ! assumes vigilance (Boese 1973). OMUs (Boese 1973) join with larger subgroups (second-level subgroups) to form a ‘troop’ before they begin to move or while sleeping at night (A. Galat-Luong pers. obs.). Multimale troops (Dunbar & Nathan 1972, Boese 1975) move in long columns (Bert et al. 1967a, b, Boese 1973) where the OMU (Boese 1973) and the second-level subgroups are still identifiable (A. Galat-Luong pers. obs.). Juveniles occasionally move from one OMU to another within these larger subgroups. At night the second-level subgroups sleep separately (Anderson & McGrew 1984) or together (Dunbar 1972). Several troops may join forming sleeping aggregations (Sharman 1981). In Niokolo Koba N. P. mean size of troops varies with climatic conditions between years (Boese et al. 1982). Mean number of instantaneously visible individuals in groups changes: 14 in 1990, 15 in 1991, 10 in 1992, 6 in 1993, 9 in 1994, 8 in 1995, 11 in 1998 (n = 539 group encounters, same transects, Feb.) (G. Galat & A. Galat-Luong pers. obs.). Size of troops declines in the dry season (50–90 individuals, n = 2 troops) and increases during the wet season (135–250 individuals, n = 2 troops; Sharman 1981). Mean number of visible individuals in groups also varies with time of day: 8 at 07:00h, 12 at 08:00–11:00h, 15 at 17:00h, 8 at 18:00h (n = 96 group encounters; G. Galat & A. Galat-Luong pers. obs.). In Niokolo Koba N. P. mean sizes of the different categories of groups are: First-level social unit: mean ca. 8 individuals (1 adult !, 3–4 adult "" and their young; Dekeyser 1956); 10 individuals (3–23, n = 30, 1 adult !, 3 adult "", 1 subadult !, 3 juveniles and 3 infants; Boese 1973). Second-level moving and day rest subgroups: mean 19 individuals (5–65, n = 45; Galat-Luong et al. 2006), second-level sleeping subgroups median 20–24 individuals (8–65, n = 92; Anderson & McGrew 1984). Third-level troops: mean 64 individuals (10–200, n = 10; Boese 1973); 193 individuals (135–250, n = 2; median = 55 individuals, n = 16;

Sharman 1981); 91 individuals (13–223, n = 19; Boese et al. 1982); 100 individuals (63–122, n = 3; Galat et al. 1998a, b); 62 individuals (22–249, n = 111; Galat-Luong et al. 2006). To the south-east outside the Niokolo Koba N. P. group size is 72 individuals (24–200, n = 14; Galat-Luong et al. 2006); to the west (Saloum), 51 individuals (30–80, n = 7; A. Galat-Luong pers. obs.). In Upper Niger N. P. the distribution of group size was: 1–20 individuals, 20%; 21–50, 27%; 51–100, 47%; >100, 7% (n = 871 individuals; Touré et al. 1997). Sleeping aggregations number up to 630 individuals (Sharman 1981). Separate behaviours described total 35: seven friendly, five agonistic, six sexual, six subgroup-specific, 11 mother–infant relations (Boese 1973). ‘Noisy branch shaking’, for example in Ronier Palms, and ‘prancing’ are frequent during agonistic displays. ‘Kick press’, recorded in captivity, has not been seen in the wild (Boese 1973). Spacing behaviour described (Boese 1973); territorial behaviour not observed. Guinea Baboons spend 19% of their time in social activities and 21% resting (Sharman 1981). Inter-subgroup herding (Galat-Luong et al. 2006) and intra-subgroup sexual herding occur (Boese 1973).Young are carried ventrally for up to four months and then in the jockey position (Boese 1973). Young are cared for by mother, sisters and aunts. Infant care and carrying by adult !! occurs (Boese 1973). One mother carried her dead newborn for three days (A. Galat-Luong pers. obs.). Few vocalizations are described. Boese (1973) and Byrne (1981) postulate an inter-group spacing role to the adult male’s loud two-syllable ‘wahoo’ bark. Muffled gruntlike vocalization given by "" in 39% of the copulations, but is not specific to copulation only (Boese 1973). Green Monkeys Chlorocebus sabaeus chase Guinea Baboons from trees and water pools. Guinea Baboons and Robust Chimpanzees avoid each other (A. Galat-Luong pers. obs.). Reproduction and Population Structure First oestrous cycle at 3.5–4.5 years. First large perineal swelling at 4.5 years (Boese 1973). Mean age at sexual maturity for "" is 3 years 8 months, and first pregnancy at 4 years, 3 months (Gauthier 1994). Length of gestation is 26 weeks (Rowell 1967). A birth peak during Jan–Mar at Niokolo Koba (Dunbar 1974). Male to " ratio 1 : 1.4 (1 : 1 and 1 : 1.5, n = 2 groups; Boese 1973). Group composition: 23% adult !!, 32% adult "", 45–47% immatures (Boese 1973, Sharman 1981). Longevity >23 years of age for two wild-born "" living in the Parc Zoologique de Paris (MNHN). Predators, Parasites and Diseases Humans, Leopards Panthera pardus (one Leopard for one troop of baboons; Verschuren 1982), Central African Rock Pythons Python sebae, Spotted Hyaenas Crocuta crocuta and African Wild Dogs Lycaon pictus are the main predators. Attacks observed by Nile Crocodiles Crocodylus niloticus, Leopards (five dead baboons found at a sleeping site after a nocturnal attack; Ndiaye 1983) and Spotted Hyena (three hyenas chasing a group of 80 baboons fleeing and climbing vertical cliffs; A. Galat-Luong pers. obs.). Since 1994, attacks by Lions Panthera leo have increased in Niokolo Koba N. P. due to reduced numbers of large ungulates (A. Galat-Luong pers. obs.). Side-striped Jackals Canis adustus, Caracals Felis caracal, Servals Felis serval and large eagles, like the Martial Eagle Polemaetus bellicosus, perhaps prey on young.

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Walker & Spooner (1960) noted Histoplasma infections. Identified intestinal parasites and the percentage of animals infected are: Niokolo Koba – 98%: Entamoeba coli (30%), Nematoda (68%), Strongylidea (33%), Strongyloides stercolaris (22%), Trichuris trichura (30%), Ascaris lumbricoides (21%) (n = 63; Pourrut et al. 1997). Assirick, Senegal – Nematoda: Strongyloides sp. (26%), Necator sp. (38%), Physaloptera sp. (31%), Trichuris sp. (28%), Streptophargus sp. (23%), Trematoda Schistosoma mansoni (23%.), Stringeodea sp. (44%); Protozoa: Balantidium coli (72%), E.coli (87%), Iodamoeba butschill (38%) (n = 39; McGrew et al. 1989a). See Howells et al. (2010) for infection rates at Fongoli, Senegal. Susceptible to malaria, filariasis, tuberculosis; healthy carriers of amaril virus. Particularly susceptible to epilepsy, thus, sleep and encephaloelectrophysiology has been studied in the wild (Bert et al. 1967a, b, Bert 1971, Balzamo et al. 1975, 1982). No simian immunodeficiency virus detected (n = 484; Durand et al. 1990). Conservation IUCN Category (2012): Near Threatened. CITES (2012): Appendix II. Habitat degradation and loss due to expanding agriculture and livestock grazing have led to significant population declines outside the national parks (Galat et al. 2000). Hunted for meat and to stop crop-raiding. Mean number traded per year (1989–93) was 131 (118 from Senegal) (Butynski 1996). Guinea Baboons still common in large protected areas in Senegal, Mali and Guinea.

T: 560 mm, n = 1 No locality provided (BMNH; Napier 1981) HB (!!): 600, 620 mm, n = 2 WT (!!): 25, 27 kg, n = 2 WT (""): 14 (7–21) kg, n = 21 Born and raised in captivity (MNHN) HB (!!): 642 (407–780) mm, n = 13 HB ("): 530 mm, n = 1 T (!!): 555 (360–650) mm, n = 13 T ("): 500 mm, n = 1 HF (!!): 190 (140–213) mm, n = 13 HF ("): 160 mm, n = 1 E (!!): 49 (43–56) mm, n = 13 E ("): 46 mm, n = 1 !! from Kudang, Gambia; Passe de Soufa, Mauritania; Tambacounda, Senegal. " from Kudang, Gambia (USNM; compiled by E. E. Sarmiento pers. comm.) Key References Boese 1973; Galat-Luong et al. 2006; Oates 2011; Sharman 1981; Zinner et al. 2011. Anh Galat-Luong & Gérard Galat

Measurements Papio papio HB: 687 mm, n = 1

Papio hamadryas HAMADRYAS BABOON (SACRED BABOON) Fr. Babouin Hamadryas; Ger. Mantelpavian Papio hamadryas (Linnaeus, 1758). Systema Naturae, 10th edn, 1: 27. Egypt.

Taxonomy Monotypic species. Mitochondrial evidence suggests that populations of Hamadryas in the Arabian peninsula have been separated from those in the Horn of Africa for at least 37,000 years. The time of separation is estimated at 37,000–74,000 years ago by Wildman et al. (2004) and at 85,000–119,000 years ago by Winney et al. (2004). Synonyms: aegyptiaca, arabicus, brockmani, chaeropithecus, cynamolgus, nedjo, wagleri. Chromosome number 2n = 42 (www. snprc.org/baboon/baboonGenomics.html, Romagno 2001). Description Distinguished from other Papio spp. by lighter pelage, lighter and redder faces, and large greyish-white mane (= mantle = cape) on adult !. Face skin and ears pink to reddish-grey to dark greyish-black. Muzzle prognathic. Perineum pink in both !! and "", tail medium-length and held in gentle arch. Sexes differ in colour of pelage. Adult "" about 59% of the weight of adult !!. Adult !: pelage light greyish-brown to greyish-white with short hair on crown of head, forelimbs below elbows, hindlimbs, posterior torso and tail. Mane large, formed by long, thick hair on shoulders, anterior torso, cheeks and sides of head, ranging from dark greyish-brown to silvery grey to off-white. Large, prominent areas of bare skin, usually bright pink, lateral to ischial callosities and extending to sides of buttocks. Ischial callosities not separated. Tail has tuft at tip. Adult ": more

Hamadryas Baboon Papio hamadryas adult male.

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uniform in colour, golden brown, no mane, smaller body size and smaller area of paracallosal skin. Paracallosal skin pale to bright pink depending on reproductive state (colour of face immediately around eyes may also vary from grey to pink depending on reproductive state). Ischial callosities separated. Tail lacks tuft at tip. Infant pelage black until 6–12 months of age, when it turns brown.

of Arabia by African Hamadryas, one in the early late Pleistocene and again sometime between 37,000 and 119,000 years ago (Wildman et al. 2004, Winney et al. 2004), though Kummer (1995) regards such a lengthy separation to be unlikely. Hamadryas distribution meets that of P. anubis, with which they hybridize (Phillips-Conroy et al. 1991, 1992), in Awash N. P. and elsewhere in Ethiopia and in Eritrea.

Geographic Variation No consistent morphological differences among regional populations. Among Horn of Africa populations, pelage and skin are darker in colour in more western parts of range (near areas of hybridization with Anubis Baboon Papio anubis) and lighter (with whiter mane in adult !!) in eastern parts of range (Kummer 1968, Kummer et al. 1985, Jolly 1993). African and Arabian populations distinguished by mitochondrial haplotypes (Wildman et al. 2004).

Habitat Usually in arid semi-desert dominated by Acacia spp. trees and shrubs, Grewia spp. and Dobera glabra (Kummer 1968), but also occur where annual rainfall is >900 mm (Zinner et al. 2001a). Found from sea level up to 3300 m in the Simien Mts, NC Ethiopia (Crook & Aldrich-Blake 1968, Yalden et al. 1996) and up to 3000 m in Eritrea (Zinner et al. 2001a); also in highland regions of SW Saudi Arabia and Yemen (Biquand et al. 1992, Al-Safadi 1994). Important components of the habitat are permanent sources of drinking water and vertical rock faces on which to sleep.

Similar Species Papio anubis. Parapatric or narrowly sympatric above ca. 500 m on eastern edge of range in Ethiopia and Eritrea. Sympatric at Debre Libanos (ca. 2000 m; C. Jolly pers. comm.). Olive-brown to olivegrey pelage. Mane short to medium and same colour as rest of pelage. Face purple-black. Perineum black. Tail kinked (i.e. ‘broken’). Theropithecus gelada. Sympatric in highlands of N Ethiopia above 1700 m, but usually above 2400 m. Dark to light brown pelage. Face skin dark brown to black. Less prognathic. Mane of adult ! brown instead of grey as in Hamadryas. Mane extends to below elbows. Patch of naked pink skin on upper chest in both sexes. Distribution Endemic to arid zone of Horn of Africa and SW Arabian Peninsula. Sudan Savanna and Afromontane–Afroalpine BZs. Throughout N, C and E Ethiopia. Also in NE Sudan, Eritrea, Djibouti, N Somalia, SW Saudi Arabia and SW Yemen. It is not clear how Hamadryas originally dispersed to the Arabian Peninsula, nor whether they speciated from other Papio spp. on the Arabian Peninsula or in the Horn of Africa. Mitochondrial data suggest two Pleistocene invasions

Papio hamadryas

Abundance Population density ranges from 1.8 ind/km2 in the Erer Gota region of Ethiopia (Kummer 1968) to 23.9 ind/km2 in the Durfo region of Eritrea (Zinner et al. 2001a). Adaptations Diurnal and terrestrial. Well adapted to dry habitats and widely dispersed, scarce resources. Hamadryas sleep on cliffs throughout range and in Doum Palms Hyphaene thebaica at one location where cliffs are not available (Schreier & Swedell 2008). Compared with Olive Baboons, Yellow Baboons Papio cynocephalus, Rhesus Macaques Macaca mulatta and humans, Hamadryas are able to maintain their blood plasma volume when dehydrated by reducing evaporative water loss and urine flow and thus appear to be physiologically betteradapted to water scarcity (Zurovsky & Shkolnik 1993). Foraging and Food Omnivorous. Larger home-ranges and longer daily travel distances than most other Papio spp. (Sigg & Stolba 1981, Sigg 1986, Swedell 2002b, Schreier 2010). Home-range size for two well-studied bands in Ethiopia was 28 km2 (Sigg & Stolba 1981) and 38 km2 (Schreier 2009); but 9 km2 for a commensal population in Saudi Arabia (Boug et al. 1994). No territorial behaviour occurs other than occasional inter-band aggression over access to sleeping sites. Hamadryas travel up to 19 km/day, leaving sleeping cliffs in early to mid-morning and returning (to the same or a different sleeping cliff) before dusk (Kummer 1968). Mean daily travel distance 6.5–13.2 km at three sites in C Ethiopia (Kummer 1968, Nagel 1973, Sigg & Stolba 1981, Swedell 2002b, 2006, Schreier 2010). Approximately 57% of daytime spent travelling and foraging, and 43% resting and grooming (Schreier 2009). Relies mainly on plant foods. Common food items include flowers, leaves and seeds of Acacia spp. trees and shrubs, Grewia spp. berries, and grasses such as Cyperus rotundus and Seddera bagshawei (Kummer 1968, Al-Safadi 1994, Swedell et al. 2008, Schreier 2010). They feed opportunistically on insects, small mammals such as Abyssinian Hares Lepus habessinicus, agricultural crops and refuse from yards or garbage dumps. Foods that constitute a sizable portion of diet in limited parts of their range include the fruits of H. thebaica in the Awash region of C Ethiopia (Swedell et al. 2008) and the fruit and young shoots of Prickly Pear Opuntia spp. in Ethiopia (Kummer 1968) and Eritrea (Zinner et al. 2001a). The latter may be an important source of water, as its water content is over 96% (Zinner et al. 2001a). Diet

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Hamadryas Baboons Papio hamadryas.

varies seasonally, with flowers and young leaves constituting a greater portion of the diet during the long rains of Jul–Aug (Schreier 2010). There are no reported sex differences in foraging behaviour or diet. Social and Reproductive Behaviour Social, with a complex, multi-level social structure. Smallest stable social unit is the one-male unit (OMU), comprising one adult ‘leader’ !, 1–9 "", dependent offspring and sometimes one or more ‘follower’ !!. Cohesion of OMUs maintained by aggressive herding of the leader !, who threatens and bites "" to condition them to stay near him (Swedell & Schreier 2009). Several OMUs comprise a ‘band’ (the social unit analogous to the ‘group’ or ‘troop’ of other papionins) whose members coordinate their movements. Size of bands varies from about 30 to over 400 individuals. Bands are larger in areas of greater food abundance: 150–400 individuals (mean 192, n = 3; Schreier & Swedell 2012) at Filoha, Ethiopia, where range includes Doum Palm forests, vs. 30–95 at Erer Gota, Ethiopia (Kummer 1968: 30–90; Sigg & Stolba 1981: 62–95; Abegglen 1984: 52–90). Also within bands are ‘solitary’ !! who, along with older juvenile !!, move freely within the band and interact mainly with other solitary !! and juveniles (Pines et al. 2011). Two or more bands sharing a common sleeping site comprise a ‘troop’, a temporary aggregation that does not function as a consistent social group (Kummer 1968).Abegglen (1984) and Schreier & Swedell (2007, 2009) observed a fourth level of social organization, the ‘clan’: a subset of a band composed of several OMUs whose ! leaders share affiliative relationships and may be related. Unlike other baboons, Hamadryas are more ‘male-bonded’ than ‘female-bonded’. Social relationships among !! may take the form of grooming (among solitary !!) or ritualized ‘notifications’ (among leader !! or between leaders and followers) whereby one ! approaches, looks at, presents his buttocks to and quickly leaves another !. In general, Hamadryas social organization is based largely on competition among !! over exclusive access to and control of "", but " choice and relationships among "" appear to play a role as well (Kummer 1968, Bachmann & Kummer 1980,

Abegglen 1984, Colmenares 1992, Colmenares et al. 1994, Swedell 2002a, 2006, Pines & Swedell 2011, Pines et al. 2011). Current evidence suggests composition of Hamadryas bands is quite stable over time compared with other baboons (Sigg et al. 1982, Swedell et al. 2011). Males at least occasionally disperse among bands, probably to gain reproductive access to "" (PhillipsConroy et al. 1991, 1992), and "" are forcibly transferred among OMUs, clans and (less often) bands by leader !! during takeovers (Kummer 1968, Sigg et al. 1982, Abegglen 1984, Swedell 2000, Swedell & Schreier 2009, Swedell et al. 2011). Genetic data from Eritrean and Saudi Arabian populations support a pattern of transfer among bands mainly by "" (Hapke et al. 2001, Hammond et al. 2006), while microsatellite data from an Ethiopian population suggest high levels of relatedness among all individuals in a band, suggesting relatively little gene flow overall (Woolley-Barker 1999, Swedell & Woolley-Barker 2001). Copulations occur almost exclusively between "" and their leader !!. Subadult follower and solitary !! occasionally gain sexual access to "", but fully adult non-leader !! rarely copulate and appear to be waiting for future reproductive opportunities (Kummer 1995, Swedell 2006, Swedell & Saunders 2006, Pines et al. 2011). Copulations occur, on average, about once an hour for oestrous "". Most copulations involve multiple mounts, averaging 7.5 thrusts per mount (1–14, n = 66), five minutes between mounts (1–17, n = 8), and one ejaculation per four mounts (Swedell 2006). Juveniles remain in natal OMU until 2–3 years of age, by which point !! spend most of their time in play groups and "" have been incorporated into another OMU. Infants and juveniles sometimes carried by adult and subadult !! in addition to their mothers (Kummer 1968, Swedell 2006). Vocalizations are similar to other Papio spp. ‘Grunts’ given during affiliative interactions and at onset of group movement. ‘Alarm barks’ emitted in response to predators. ‘Contact barks’ given when "" or juveniles lose contact with other group members. ‘Wahoo barks’ given by adult !! during inter-band encounters, aggressive interactions, 223

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" herding, and loss of contact with group. ‘Kecks’ or ‘staccato-coughs’ ("" only) and ‘screams’ (all age and sex classes) given during agonistic interactions and in response to aggression or threat. ‘Copulation calls’ given by some "" during and/or after copulation (Swedell 2006, Swedell & Saunders 2006, J. Saunders pers. comm.). Reproduction and Population Structure Female ovarian cycles average 39 days in the wild (31–52, n = 17; Swedell 2006) and 42 days in captivity (33–49, n = 9; D. Zinner pers. comm.). Like other baboons, Hamadryas "" undergo pronounced swelling of the perineal region (medial to the ischial callosities) during the periovulatory period. Sexual swelling generally coincides with behavioural oestrus (Caljan et al. 1987, Swedell 2006). Reproductive synchrony occurs in some wild populations (Kummer & Kurt 1963, Kummer 1968) but not others (Swedell 2006), and occurs in captivity (Schwibbe et al. 1992, Zinner et al. 1994). Gestation averages 26 weeks (24.4–27.3, n = 52; Kaumanns et al. 1989); singleton births are the norm. Twins not reported. Birth weight ca. 900 g (n = 1; D. Zinner pers. comm.). Interval between births of surviving infants ranges 18–28 months (mean 22, n = 12) at Erer Gota (Sigg et al. 1982), though this interval may be shorter (mean 19 months, 15.5–21.5, n = 3) in richer habitats (Swedell 2006). In general, no birth seasonality occurs, though Kummer (1968) observed two birth peaks over one year at Erer Gota (however, the timing of these peaks varied among groups in the same area). In the wild, adolescent "" undergo their first oestrous cycles at about four years of age (mean 4.3, n = 13) and first birth at about six years of age (mean 6.1, 5.5–7.0, n = 8), at which point they have reached adult size (Sigg et al. 1982). Female reproductive maturation occurs more than a year earlier in captivity (Caljan et al. 1987, Kaumanns et al. 1989). Adolescent !! reach the size of an adult " at about five years of age, at which point the testes have descended but the mane has not yet developed. By ten years of age, !! have attained adult body size and have a full mane (Sigg et al. 1982). Although "" give birth to their first surviving infant by six years of age, !! in the wild probably do not reproduce until they are at least nine years of age (Sigg et al. 1982). The sex ratio within bands is 1.1–2.4 adult and subadult "" per adult and subadult !. There are 1.1–1.6 adults and subadults per infant or juvenile (Kummer 1968, Kummer et al. 1985, Zinner et al. 2001b, Swedell 2006). Birth rates in captivity average 0.6 infants/"/year, with a peak in " fertility at 9–14 years of age and a sharp reduction in fertility (to zero) after 20 years of age (Caljan et al. 1987, Chalyan et al. 1994). Infant survival to one year of age is 82% at Erer Gota (Sigg et al. 1982) and 87% at Filoha (Swedell pers. obs.). These survival rates are higher than those of many other Papio spp. populations, suggesting that the OMU social structure may provide better protection for Hamadryas infants compared with other baboons (Sigg et al. 1982). Longevity in the wild is not known, but most Hamadryas in captivity live to an age of about 20 years and few survive beyond 30 years (Lapin et al. 1979). Predators, Parasites and Diseases Potential predators include Lions Panthera leo, Leopards Panthera pardus, Cheetahs Acinonyx jubatus, Spotted Hyenas Crocuta crocuta, Striped Hyenas Hyaena hyaena, Blackbacked Jackals Canis mesomelas, Nile Crocodiles Crocodylus niloticus and Verreaux’s Eagles Aquila verreauxii. Over a period of 20 months near

Awash, Lions and Spotted Hyenas (and baboon alarm calls) were heard frequently near the sleeping cliffs at night and snake bites were a suspected cause of at least two deaths (Swedell 2006). In the same region a group of 180 Hamadryas, upon encountering three Spotted Hyenas at dawn at their sleeping cliff, ran faster and farther from the cliff than they had ever been observed to do before, suggesting that Spotted Hyenas are indeed a threat (Swedell 2006). At Erer Gota two Leopards, fresh blood and two dead " Hamadryas were observed at dawn at the base of a sleeping cliff, and body parts of one of the Hamadryas were found in a tree, presumably put there by a Leopard (Kummer 1995). In Eritrea, Verreaux’s Eagles observed interacting with Hamadryas in a manner highly suggestive of hunting behaviour, and the Hamadryas responded by giving alarm calls, seeking protective cover and, in the case of adult !!, threatening the birds (Zinner & Peláez 1999). Hamadryas are also threatened by farmers and their dogs in Eritrea, but adult !! can successfully repel dogs (Zinner et al. 2000). Overall, the vertical cliffs used as sleeping sites (ranging from 10 to over 50 m in height) presumably afford Hamadryas adequate protection against nocturnal terrestrial predators, and Hamadryas do not, in general, appear to be at great risk from predation. Intestinal parasites such as Giardia spp., Entamoeba spp., Balantidium coli, Hymenolepis nana, Schistosoma mansoni, Ascaris sp., Enterobius sp., Trichuris sp. and hookworm found in wild and commensal populations in Saudi Arabia (Nasher 1988, Ghandour et al. 1995), though few, if any, parasites found in Ethiopian populations. Prevalence of parasites appears to vary depending on proximity to human habitation (Ghandour et al. 1995). It is not known what other diseases occur in wild populations of Hamadryas. Conservation IUCN Category (2012): Least Concern. CITES (2012): Appendix II. Not greatly threatened by the nomadic pastoralists with whom they share most of their range, but by the extension of agriculture into dry river valleys via irrigation (D. Zinner pers. comm.). Not hunted for food, but sometimes shot for skins, for their callosities (which are used in traditional medicine in some parts of Eritrea), or as a result of cropraiding (Wolfheim 1983, Biquand et al. 1992, Zinner et al. 2001c). In Eritrea young are used as pets (Zinner et al. 2001c). Main threat overall is loss of habitat to agriculture and human settlement. Measurements Papio hamadryas HB (!): 750 mm, n = 1 T (!!): 565 (460–660) mm, n = 37 T (""): 480 (460–500) mm, n = 3 HF (!!): 210 (190–220) mm, n = 34 HF (""): 180 (170–190) mm, n = 2 WT (!!): 17 (13–24) kg, n = 41 WT (""): 10 (7–13) kg, n = 39 Central Ethiopia (Phillips-Conroy & Jolly 1981, C. J. Jolly & J. E. Phillips-Conroy pers. comm.) HB: Napier (1981) Key References Abegglen 1984; Kummer 1968, 1995; Swedell 2006. Larissa Swedell

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Papio ursinus CHACMA BABOON Fr. Chacma; Ger. Bärenpavian Papio ursinus (Kerr, 1792). Animal Kingdom, p. 63. Western Cape Province, Cape of Good Hope, South Africa.

Chacma Baboon Papio ursinus adult male.

Taxonomy Polytypic species.Treated as a subspecies in a monotypic genus by some authorities (e.g. Skinner & Chimimba 2005). Groves (2001, 2005) recognizes three subspecies within P. ursinus. Grubb et al. (2003) recognize two subspecies. The taxonomy of Groves (2001, 2005) is followed here. For recent molecular findings, see Sithaldeen et al. (2009), Keller et al. (2010) and Zinner et al. (2011). Synonyms: capensis, chacamensis, chobiensis, comatus, griseipes, ngamiensis, nigripes, occidentalis, orientalis, porcaria, ruacana, sphingiola, transvaalensis. Chromosome number: 2n = 42 (Romagno 2001). Description Large, robust baboon with ventrum and sides of muzzle noticeably paler than dorsum, and tail ‘broken’ near base. Adult "" like adult !!, but much smaller; body weight of adult "" half that of adult !!. Pelage coarse, blackish, dark brown, or dark yellowish-grey (griseipes) above, paler below. Male mane (= cape = mantle) relatively thin, often with back-curling hairs on nape of neck. Skin of face, extremities and around the ischial callosities grey or black. Muzzle long, robust, usually more downwardly-flexed than in other baboons. Nostrils do not protrude beyond plane of upper lip or snout. Tail ‘broken’: proximal one-third of tail held up, distal two-thirds hangs down at sharp angle. Geographic Variation Little is known of these subspecies, so the following should be treated as preliminary (Hill 1970, Groves 2001). P. u. ursinus Southern Chacma.Widespread across S Botswana and South Africa. Black or charcoal grey in western and south-western part of range, but lightens to grey and brown towards the east (although still with dark extremities). Face, hands, feet and tail black. P. u. griseipes Grey-footed Chacma. SW Zambia, Zimbabwe, N Botswana, Mozambique (south of Zambezi R.) and NE South Africa. Pelage fawn. Hands, feet and tail grey rather than blackish. P. u. ruacana North-western Chacma. SW Angola and Namibia. Small. Feet black. Crown and back blackish, tending to contrast with lighter flanks and limbs.

Papio ursinus

Similar Species Papio cynocephalus. Sympatric or parapatric at southern extreme of range. Smaller with yellow-brown dorsum and off-white ventrum. Distribution Endemic to southern Africa. Zambezian Woodland, South-West Arid, Highveld, and South-West Cape BZs. Widespread throughout the Southern African Subregion south of Zambezi R. to SW Angola and SW Zambia, southwards through much of Namibia, Zimbabwe and South Africa to the Cape. Habitat Papio ursinus is an adaptable, semi-terrestrial generalist that occurs in most habitats, including desert, savanna grassland and woodland, montane grassland and Cape Fynbos. Limited by the availability of water and safe sleeping sites (tall trees or cliff faces). Occurs from sea level to at least 3000 m where there is often snow and temperatures below freezing (Hall 1966). Abundance Population density varies substantially among habitats: 1.4 baboons/km2 in montane grassland (Whiten et al. 1987); 3.2/km2 in savanna grassland (Anderson 1981); 5.3/km2 in desert oases (Hamilton et al. 1976); and 24.0/km2 in savanna woodland (Hamilton et al. 1976). Adaptations Diurnal and semi-terrestrial. There is substantial variation in body mass among sites, especially for adult !! (mean adult ! weight 23–31 kg, mean adult " weight 14–16 kg, across 11 sites). This variation related to local patterns of rainfall and temperature; body size tends to be larger in wetter, cooler 225

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habitats, presumably reflecting higher habitat quality (Barrett & Henzi 1997). High temperatures can also cause thermal stress. In response, P. ursinus is able to tolerate substantial fluctuation in core body temperature – as much as 5.3 °C – and undertake behavioural actions such as ‘sandbathing’ (Brain & Mitchell 1999). Adaptations shared with other Papio spp. include cheek pouches. In P. ursinus these are used primarily to accumulate food rapidly when faced with competition from other group members, e.g. when food is limited and when foraging in the centre of the group (Hayes et al. 1992). Foraging and Food Omnivorous. Forage during daylight hours and frequently cover substantial distances over the course of the day, e.g. 4.1 km across a home-range of 14.5 km2 (Whiten et al. 1987). Travelling and feeding occupy about 30% and 38% of daylight hours, respectively, while the remaining hours are spent resting and grooming (Hill 1999a). Habitats are selected in order to both maximize food intake rates and minimize predation risk. Food-rich habitats avoided if high risk, in favour of safer habitats where food is less abundant (Cowlishaw 1997a). As such, foraging preferentially takes place close to refuges, such as large trees and cliffs, to reduce the risk of predation (Cowlishaw 1997b). Vigilant to predators (Cowlishaw 1998). Foraging "" adopt similar patterns of anti-predator vigilance across populations (Hill & Cowlishaw 2002). As in all baboons, diet of P. ursinus is diverse and highly flexible. Diet typically includes fruits and pods (including seeds), flowers, leaves and subterranean items (e.g. roots and corms). The predominant foods are usually fruits/pods (Hill 1999a). However, the relative importance of the different dietary constituents varies both among sites and seasons. Animals are also included in the diet; most commonly insects (Hamilton et al. 1978), but on occasions tortoises, birds, mammals and fish (Hamilton & Busse 1982, Hamilton & Tilson 1985, Hill 1999b). Although the diet of P. ursinus is broad, it is also selective. Individuals preferentially select foods high in protein and lipid, and avoid foods high in fibre, phenolics and alkaloids (Whiten et al. 1991). A comparison between low-altitude and high-altitude montane groups found that individuals in both groups obtained the same nutrient yields despite a high degree of seasonality and different foraging substrates (Byrne et al. 1993). During periods of food shortage, adults switch to less-preferred foods, and juveniles learn of these by observation of the adults (Hamilton 1986). Prefer to drink daily, but can go without drinking for 11 days (Brain 1991) or longer (Brain & Mitchell 1999). Social and Reproductive Behaviour Social. Live in stable social groups, or ‘troops’, of about 22–79 individuals (Henzi et al. 1999). The adult sex ratio within these groups is variable, although always female-biased; e.g. 0.15–0.81 !! per "" (Henzi et al. 1999). Within groups "" tend to be philopatric whereas !! disperse to other groups at adulthood, although there are exceptions in both cases (Hamilton & Bulger 1990, Henzi et al. 2000b). Following immigration into new groups and/or the acquisition of high social rank (see below), !! often attempt to kill infants in the group. This behaviour benefits the ! since it leads to the resumption of oestrous cycling by previously lactating "", thereby

maximizing his own opportunities to father offspring (Palombit et al. 2000). In response, "" often mate with many !! to confuse paternity (thus reducing the likelihood that any one ! will subsequently attempt infanticide), a strategy that may be assisted through both sexual swellings and copulation calls (O’Connell & Cowlishaw 1994). In addition, following conception, "" often develop and maintain ‘friendships’ with particular !! with whom they have mated. These ! friends help protect the infants, for example by carrying them out of danger (Anderson 1992, Palombit et al. 1997, Weingrill 2000). Competition for limited, but monopolizable, resources within groups leads to the development of dominance hierarchies in which high-ranking individuals benefit most. Amongst !!, dominant individuals monopolize "" when they are most likely to conceive (through mate-guarding ‘consortships’), and thus achieve the highest mating success (Bulger 1993, Weingrill et al. 2000). Amongst "", dominant individuals may obtain more food, potentially leading to higher birth rates (Bulger & Hamilton 1987). They also occupy positions of greater safety from predators, potentially leading to higher survival rates (Ron et al. 1996). In addition, dominant "" can experience higher infant survival rates (Bulger & Hamilton 1987), possibly as a result of their ability to monopolize access to ! friends (Palombit et al. 2001). The strength of such rank effects are variable among sites depending upon the local availability of limited resources. Individuals may elicit tolerance and support from others during competition through grooming them. Grooming can be viewed as a ‘commodity’ that is valuable in itself (it is associated with the release of endorphins into the bloodstream and plays a role in ectoparasite removal), and group members can exchange this commodity for either reciprocal grooming or for tolerance at, and thus access to, limited resources (Barrett et al. 1999, 2002). Active coalitionary support, in contrast, appears to be rare in P. ursinus, regardless of grooming relationships (Silk et al. 1999). Grooming is often, but not always, directed towards kin and high-ranking individuals (Seyfarth 1976, Barrett et al. 1999, Silk et al. 1999), and typically reflects social bonds between individuals. Social bonds tend to be strongest between "", although strong bonds also occur between !! and "" (including ‘friendships’; see above) (Henzi et al. 2000a). Females spend about 12% of their day grooming (Hill 1999a), during which time they strive to groom all other "" in the group. However, when there is insufficient time to groom everyone, "" focus on their key social partners (Henzi et al. 1997b, Silk et al. 1999). Bonds between social partners are also mediated through vocalizations. ‘Soft grunts’ are used by dominant individuals to reassure subordinate animals and to reconcile combatants after fights (Cheney et al. 1995, Silk et al. 1996). Even when not socializing, group members tend to stay close to one another. Adults are usually within 5 m of at least one other adult, and rarely more than 25 m away. This probably reflects a response to predation risk (these distances are greater where predators are absent), although spatial proximity within groups appears to be most strongly influenced by ! defence of infants (Cowlishaw 1999). When social partners lose sight of one another, loud ‘contact’ barks are used to maintain contact (Cheney et al. 1996). Males, similarly, use loud two-syllable ‘wahoo’ calls when they become separated from the group. However, ! ‘wahoos’ are primarily used as alarm

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calls or as vocal signals of stamina and competitive ability (Fischer et al. 2002, Kitchen et al. 2003). Not territorial. Encounters between groups can be infrequent, e.g. once every five days (Cowlishaw 1995). On occasion, groups attempt to monopolize valuable ecological resources (Hamilton et al. 1976), but more commonly resource-defence is absent and groups encounters are relatively peaceful (Cowlishaw 1995). Males primarily use inter-group encounters to assess potential mating opportunities in neighbouring groups. The ensuing mate-guarding behaviour by resident !! leads to aggressive chasing, or ‘herding’, of "" away from the approaching group (Cheney & Seyfarth 1977, Henzi et al. 1998, Kitchen et al. 2004). Reproduction and Population Structure Gestation averages 187 days (173–193, n = 14). Newborn weighs 600–800 g and has black pelage and pink skin (Gilbert & Gillman 1951). Adult "" give birth to a single infant. Inter-birth interval is 20–38 months (Hill et al. 2000). Although births occur throughout the year, birth peaks reported both in the Drakensburg Mts, South Africa, and Okavango Delta, Botswana. These birth peaks most likely reflect improved conception rates following periods of high food abundance (Lycett et al. 1999, Cheney et al. 2004). At De Hoop, South Africa, infants begin weaning at about 4–5 months, although suckling can continue until 12–13 months (Barrett & Henzi 2000). High maternal dominance rank can increase growth rates in infant and juvenile "", but the same effect is not seen in ! offspring (Johnson 2003). Population structure is primarily determined by group size (and thus the number of discrete units that comprise the population). Minimum group size is determined by predation risk and the minimal requirements for safety, whereas maximum group size is determined by food abundance and the time available to maintain grooming relationships with other group members. As groups grow in size there is no corresponding increase in time available for grooming additional group members. In fact, the time available for grooming can even decline, due to the demands of foraging time, since feeding competition can intensify as groups grow. Hence "" find it increasingly difficult to sustain all of their grooming relationships and begin to focus only on their key social partners. As a result, the social coherence of the group is weakened and large groups eventually fission (Henzi et al. 1997a, b). Predators, Parasites and Diseases Leopards Panthera pardus are the most important predator of P. ursinus. Other predators include Lions Panthera leo, Brown Hyenas Hyaena brunnea, Spotted Hyena Crocuta crocuta, Nile Crocodiles Crocodylus niloticus and Southern African Rock Pythons Python natalensis (Cowlishaw 1994, Cheney et al. 2004). Verreaux’s Eagles Aquila verreauxii will attack P. ursinus to defend their nests, but do not appear to prey on them (Gargett 1990). Adult P. ursinus !!, who are least vulnerable to predation (due to their size and ferocity), will often take an active role in group defence against predators – occupying the most dangerous position in the group during travel (Rhine & Tilson 1987) and often retaliating against predators following attack (Cowlishaw 1994). Papio ursinus is vulnerable to a variety of parasites and pathogens. Patterns of infection with gastrointestinal parasites, primarily

protozoans and helminths, vary both with altitude and habitat (Appleton & Henzi 1993, Appleton & Brain 1995). Ectoparasites are relatively rare, although one case of heavy tick infestation has been recorded (Brain & Bohrmann 1992). In this case, the ticks (genus Rhipicephalus) appeared to be directly or indirectly responsible for over half of all infant deaths. An epidemic disease (possibly bacterial yersiniosis, or an unknown haemorrhagic/enteric viral infection) also recorded (Barrett & Henzi 1998). The disease killed 85% of members in one group, and 32% of members in a second group, before heavy rains appeared to terminate the epidemic. Males appeared to be particularly vulnerable to this infection (and facilitated its transmission between the groups). Patterns of mortality in P. ursinus are complex. In the Okavango Delta mortality is highest among infants, and can largely be attributed to infanticide. In contrast, the lower mortality rates seen among juveniles and young adults are driven primarily by predation. Mortality from both sources shows a seasonal peak that occurs when groups are more dispersed and travel along more predictable routes (Cheney et al. 2004). The relationship between social rank and mortality is variable across populations. Predation can affect all "" equally (Cheney et al. 2004), or low-ranking "" in particular (Ron et al. 1996). Similarly, infanticide may be most severe among high-ranking and low-ranking "" (Cheney et al. 2004), or infant mortality may be highest among low-ranking "" (Bulger & Hamilton 1987). Infant mortality can also increase in larger groups (Bulger & Hamilton 1987). As well as infanticide and predation, P. ursinus also suffers mortality from disease (see above) and wounds sustained during fights (Brain 1992). In addition, a food and water shortage in a Namib Desert oasis led to widespread mortality from starvation. In this case, adult "", juveniles and infants were more susceptible to starvation than adult !! (Hamilton 1985). Conservation IUCN Category (2012): Least Concern. CITES (2012): Appendix II. The widespread geographic range of P. ursinus, together with its ability to survive over a wide range of habitats and to live commensally with people, should ensure its long-term survival. However, P. ursinus can experience local persecution as a result of crop-raiding and livestock predation. In addition, P. ursinus is subject to trophy hunting and live-trapping for biomedical research, although analyses of the known legal trade in the early 1990s suggested that its impact on wild populations is minimal (Butynski 1996). Measurements Papio ursinus ursinus HB (!): 720 (670–755) mm, n = 5 HB (""): 613 (550–681) mm, n = 15 T (!!): 566 (530–605) mm, n = 5 T (""): 471 (415–515) mm, n = 15 HF (!!): 209 (197–220) mm, n = 5 HF (""): 176 (170–184) mm, n = 15 E (!!): 59 (55–63) mm, n = 5 E (""): 48 (45–54) mm, n = 15 WT (!!): 28.3 (26.6–30.0) kg, n = 5 WT (""): 15.1 (11.1–18.3) kg, n = 15 Tsaobis, Namibia (G. Cowlishaw pers. obs.). 227

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Papio ursinus (probably ursinus and griseipes combined) TL (!!): 1450 (1320–1570) mm, n = 9 TL (""): 1190 (1080–1160) mm, n = 5 T (!!): 725 (598–840) mm, n = 9 T (""): 585 (556–610) mm, n = 5 HF (!!): 223 (217–236) mm, n = 9 HF (""): 184 (176–194) mm, n = 5 E (!!): 58 (54–65) mm, n = 8 E (""): 50 (44–52) mm, n = 5

WT (!!): 31.8 (27.2–43.5) kg, n = 9 WT (""): 15.4 (14.6–17.2) kg, n = 5 Botswana (Smithers 1971). See Skinner & Chimimba (2005) for more WT data. Key References Barret et al. 1999; Bulger 1993; Cheney et al. 2004; Cowlishaw 1997a; Henzi et al. 1997b; Whiten et al. 1991. Guy Cowlishaw

Papio cynocephalus YELLOW BABOON Fr. Babouin cynocéphale; Ger. Gelber Pavian Papio cynocephalus (Linnaeus, 1766). Systema Naturae, 12th edn, 1: 38. Inland from Mombasa, Kenya.

Yellow Baboon Papio cynocephalus adult male.

Taxonomy Polytypic species. The Yellow Baboon presently retains its own species designation, Papio cynocephalus, with three subspecies – Central cynocephalus, Ibean ibeanus and Kinda kindae (Grubb et al. 2003). Some researchers suggest separating baboons into two species, Papio hamadryas for the Hamadryas or Sacred Baboon, and P. cynocephalus for the Savanna Baboons (Groves 2001). Under this construct, the Yellow Baboon would be a subspecies of Savanna Baboon. Alternatively, Jolly (1993) suggests lumping all baboons under one species, P. hamadryas, which would result in at least five subspecies. Synonyms: antiquorum, babouin, basiliscus, flavidus, ibeanus, jubilaeus, kindae, langheldi, ochraceus, pruinosus, ?rhodesiae, ruhei, strepitus, sublutea, thoth, ?variegata. Chromosome number 2n = 42 (Romagno 2001). Description Slender baboon with dorsum light brown to yellowishbrown to pale reddish-brown, contrasting with whitish ventrum. Sexes alike in colour of pelage. Adult !! weigh about twice as much as adult "". Adult !: skull not flattened behind the supraorbital ridge. Head appears pointed when viewed from the front, sometimes with a crest. Forehead not parallel with the angle of the muzzle (Alberts & Altmann 2001). Muzzle predominantly bare, greyish to black, often with varying amounts of sparse and patchy white pelage. Nostrils set back from the lips. Mane (= cape = mantle) absent or greatly reduced relative to other Papio spp. Dorsum, tail and outer limbs range from light brown to yellowish-brown to pale reddish-brown. Ventrum,

inner limbs and cheeks lighter, almost white, and pelage more sparse. Pelage long, especially on sides. Skin grey to black on primarily bare hands and paracallosities, but paracallosities of Kinda can be rosy-pink both on adult !! and adult "" (Y. de Jong & T. Butynski pers. comm.). Skin on rest of body, in densely pelaged areas, and in armpits and crotch, ranges from grey to pinkish or almost white, often in a splotchy pattern. Tail tends to be tapered with a sharp bend or hook between a proximal ascending portion and descending, distal one; tail shape is highly individually variable, however, and is useful in individual recognition. Angle of tail becomes more vertical during ontogeny (Hausfater 1977). Scrotum grey. Paracallosal skin fused. Adult ": paracallosal skin split vertically. Nipples pinkish and button-like until " has nursed an infant. Nipples of multiparous "" are dark, and the two nipples tend to differ considerably in length and often in colouration. Immatures: infants of Central and Ibean, but not Kinda, have a black natal coat that is characteristic of all other baboon species. According to Groves (2001), Kinda newborns are unique among baboons in that the coat is reddish, not black. Kinda newborns at Mahale N. P., Tanzania, at the north-east corner of the range for this subspecies, have whitish pelage, pink muzzle and ears, but older infants have a reddish-brown coat. Infants in transition between these two pelage colours are pale yellowish-orange (Y. de Jong & T. Butynski pers. comm.). Between 6 and 12 months of age pelage gradually changes to the species-typical coat. Muzzle, ears, ischial callosities, paracallosities and scrotum are pink, and the ischial callosities are split in both sexes. Between 7 and 15 months of age, skin colour, except for scrotum, changes to the grey of adults and the paracallosities of !! fuse (Altmann et al. 1981). Body mass growth is approximately 5 g/day for both sexes through 3–4 years of age, after which !! experience an adolescent growth spurt (Altmann & Alberts 2005). Geographic Variation P. c. cynocephalus Central or TypicalYellow Baboon. South coast of Kenya southwards through most of Tanzania, Malawi, east of the Luangwa R. in Zambia and into N Mozambique. Straight, soft, silky pelage. Mane absent (Jolly 1993, Groves 2001, Zinner et al. 2009b). Newborn with black pelage. P. c. ibeanus Ibean Yellow Baboon. Central and S Somalia, SE Ethiopia, and E and SC Kenya. Hill (1970) indicates that P. c. ibeanus meets P. c. cynocephalus at the Galana-Sabaki R. Wavier and coarser pelage.

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Trace of a mane. More like the Olive Baboon Papio anubis and Guinea Baboon Papio papio (Jolly 1993, Groves 2001, Zinner et al. 2009b). Newborn with black pelage. P. c. kindae Kinda Yellow Baboon. From Cunene R. in S Angola north to the Congo R., then eastward across southern DR Congo to SW L. Tanganyika and C and N Zambia (south to Zambezi R.) (Jolly 1993, Groves 2001, Zinner et al. 2009b). Probably also up west side of L.Tanganyika (Mahale Mts) to Malagarasi R. (T. Butynski & Y. de Jong pers. comm.). Straight, soft, silky pelage. Mane absent. Bare skin around eyes pink. Body size is unusually small (Hill 1970, Jolly 1993, Groves 2001). Adults of both sexes can have rosy-pink callosities. Newborn with whitish pelage at Mahale Mts (Y. de Jong & T. Butynski pers. comm.). Numerous photographs of the three subspecies of P. cynocephalus at many sites in Kenya and Tanzania are available at: www.wildsolutions.nl Similar Species Papio anubis. Sympatric or parapatric in W Somalia, SE Ethiopia, C and S Kenya, N Tanzania and south-east DR Congo. More robust. Grizzled, olive-brown dorsum. Mane thick over neck and shoulders. Top of head appears flat when viewed from the front. Tail appears ‘broken’. Nose not ‘upturned’. Papio ursinus. Sympatric or parapatric in S Angola, SW Zambia and NW Mozambique. More robust. Grey, dark brown, to blackish dorsum. Distribution Endemic to tropical Africa, mostly south of the equator. Southern Rainforest–Savanna Mosaic, Somalia–Maasai Bushland, Zambezian Woodland and Coastal Forest Mosaic BZs. Widely distributed in south-central and East Africa. Ranges from Angola through south DR Congo to E Kenya, SE Ethiopia and C Somalia through much of Tanzania, Malawi, most of Zambia to the Zambezi R. Valley and into N Mozambique. Whereas Yellow Baboons and Olive Baboons both inhabit the central latitudes of Africa, and their distributions overlap in a number of hybrid zones (Maples & McKern 1967, Jolly 1993, Alberts & Altmann 2001, Zinner et al. 2009b),Yellow Baboons typically inhabit low-altitude woodlands and savannas. Their distribution may be correlated more with vegetation than geography (Jolly 1993). Two areas of Yellow–Olive hybridization are known. One runs through Amboseli N. P., SC Kenya, and the surrounding area, extending north and south of the Amboseli Basin. Genetic models and previous surveys suggest that the hybrid zone is relatively narrow and historically stable through this region, with Olive Baboons to the west of Amboseli and Yellow Baboons to the east (Charpentier et al. 2012; see also Maples & McKern 1967, Altmann & Altmann 1970, Samuels & Altmann 1986, Alberts & Altmann 2001). A second, broad, clinal hybrid zone occurs between the Laikipia Plateau in C Kenya and the Lower Tana R./Indian Ocean. This cline appears to start just to the north-east, east and south-east of Mt Kenya and covers an upper altitudinal range of from roughly 1000 m asl at Mwea National Reserve (to the south of Mt Kenya) to roughly 600 m asl at Meru N. P. (to the north of Mt Kenya). The zone then continues south-eastwards towards the lower Tana R. to at least 30 m asl, perhaps to the Indian Ocean. Baboons in this >200 km wide region are intermediate and cannot be readily allocated to either Olive or Yellow Baboons. As one moves south-eastwards towards the

Papio cynocephalus

Kenya coast, however, the baboons become increasingly Yellow-like in their phenotypes (T. Butynski & Y. de Jong pers. comm.). A potential Yellow Baboon–Chacma Baboon Papio ursinus hybrid zone exists in the Zambezi R. Valley. Some confusion exists as to whether Central or Kinda are in areas of Zambia. In the Zambezi R. Valley the Yellow Baboon range is thought to be only north of the Zambezi R., whereas the predominantly southern range of the Greyfooted Chacma Baboon P. u. griseipes extends north of the Zambezi R. as well, perhaps creating a hybrid zone there. Habitat Primarily in open and woodland savanna. Associated with miombo (Brachystegia spp.) woodland over much of the range. In East Africa, Fever Trees Acacia xanthophloea and Tortilis Trees Acacia tortilis are used as sources of food and shelter. Yellow Baboons use woodland groves for sleeping at night, as well as for sources of shade during hot days. A water source within a day’s walk appears to be necessary (Altmann & Altmann 1970). Distribution between wet and dry season lengths varies across the range. Most parts of the range experience one long wet season and one dry season. However, the Amboseli area usually experiences two wet and two dry seasons: one long and one short (Altmann et al. 2002). Mean annual rainfall over the range of the Yellow Baboon varies from ca. 320 mm (e.g. Garissa on the Tana R., EC Kenya) to ca. 1200 mm (e.g. Mombasa, SE Kenya; T. Butynski pers. comm.). Mean annual rainfall at two of the mainYellow Baboon study sites is as follows: 348 mm in Amboseli N. P. (over 25 years; Altmann et al. 2002); 842 mm in Mikumi N. P., SC Tanzania (over 20 years; Norton et al. 1987). Yellow baboons range in altitude from sea level to at least 1800 m (Mahale Mts, WC Tanzania; Kano 1971, T. Butynski &Y. de Jong pers. comm.) and to at least 1900 m in the Udzungwa Mts, SC Tanzania (Rovero et al. 2009). Altitude is ca. 1100 m at Amboseli and 450–740 m at Mikumi. Abundance Abundant in parts of their range, with densities of 10–60 ind/ km2 (Wolfheim 1983). Population density in the 229

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Amboseli Basin decreased from 73 to 4 baboons/km2 during the 1960s (Altmann et al. 1985). Density in the mid-1980s was 1.2 baboons/km2 (Samuels & Altmann 1991). Almost two decades later, the density remains similar, although the distribution of groups shifted within the Basin, primarily to the south and west. Adaptations Diurnal and semi-terrestrial. Behaviour and movement are adjusted to the thermal environment and microhabitats encountered (Stelzner 1988). Sitting position is adjusted relative to wind (Stelzner & Hausfater 1986). Behaviours include huddling for warmth, particularly by mothers with infants, and by young juveniles with each other, and resting on tree limbs or under trees for shade during the day. In Ruaha N. P., Tanzania, sun avoidance behaviour is regulated by temperature in the dry season and by humidity in the wet season (Pochron 2000). Other adaptations are those characteristic of the genus, with Yellow Baboons perhaps exhibiting Papio’s ecological and social adaptability to the greatest extent among the species. Foraging and Food Omnivorous. Yellow Baboons forage throughout the day. Movement patterns are influenced by season and the availability of food. Completely wild-foraging groups spend ca. 70–75% of their time foraging (feeding + walking), and travel as much as 8–10 km/day, whereas groups that exploit garbage dumps reduce their foraging time to ca. 35–40% and travel 2–4 km/day (Muruthi et al. 1991, Altmann et al. 1993). Less time is spent feeding during the wet seasons and in years of high rainfall (Bronikowski & Altmann 1996, Alberts et al. 2005). These differences in foraging time are more pronounced for wild-foraging groups than for those that exploit garbage dumps. Yellow Baboons appear to be obligate drinkers: they drink almost daily and their home-ranges tend to include a water source within a half-day’s journey (Altmann 1998). Yellow Baboons are not territorial, but have overlapping homeranges of approximately 24 km2 (for a group of about 40 animals). Yellow Baboons have a highly diverse diet that incorporates a wide variety of plant and animal species. At the same time, they are extremely selective, as is evident in their differential use of plant parts of high nutritive value and their avoidance of toxic ones (Altmann 1998). Yellow Baboons incorporate new foods as they become available, whether through season or habitat change (Alberts et al. 2005). In Mikumi N. P., 85 plant foods are eaten (Norton et al. 1987) compared with 277 foods (plant & animal) for Amboseli (Altmann 1998). Foods available or utilized differ seasonally and, to a lesser extent, from year to year. Consequently, the duration, timing of study, and criteria for ‘splitting’ or ‘lumping’ food types influences the number of foods reported in the diet. The numerous foods that Yellow Baboons consume include all or parts of various species of trees (particularly Acacia spp.), grasses, sedges and bushes, as well as animal matter, including insects (e.g. grasshoppers, beetles and larvae), and meat of several species of mammals. In Amboseli these include Cape Hare Lepus capensis, Thomson’s Gazelle Eudorcas thomsonii and Grant’s Gazelle Nanger (granti) granti and, more rarely, Impala Aepyceros melampus, Vervet Monkey Chlorocebus pygerythrus, Northern Lesser Galago Galago senegalensis, birds, reptiles and bird and reptile eggs. The inclusion of meat in the diet is largely opportunistic. Vertebrate prey are caught by juveniles and adults of both sexes, but consumption of larger prey is primarily restricted to adult baboons, particularly adult !!.

Human refuse piles near settlements and tourist lodges are also exploited (Muruthi et al. 1991). Availability of these food sources results in less energy expenditure, more rapid juvenile growth, earlier physical maturation, more frequent reproduction, higher infant survival and adults that are larger and obese (Altmann et al. 1993, Altmann & Alberts 2005). Social and Reproductive Behaviour Social. Yellow Baboons typically live in multimale, multifemale groups ranging in size from 18 to 100 individuals. The number of adult !! in a group is correlated with the number of adult "". Males tend to leave groups with few reproductive opportunities and join ones with many (Alberts & Altmann 1995a). Single-male groups also exist in Amboseli. These relatively ephemeral single-male groups occasionally join a multimale group; more commonly, additional !! join and thereby create a multimale group. Groups in Amboseli sometimes fission at approximately 60–70 individuals for wild-foraging groups and at larger sizes for groups with high food availability, but there is no simple relationship between group size and fission. Females remain in their natal group for life; exceptions occur when a female’s natal group fissions or fuses with another group. Females form a linear dominance hierarchy that tends to be stable among matrilines and across generations. Maternal rank acquisition determines a young female’s rank, even in the absence of her mother. Specifically, older juvenile "" usually attain a rank immediately below their mother, but above their older sisters. The daughters of the family matriarch are therefore ranked in inverse age-order. All long-lived "" that have adult daughters and that are not members of the top-ranking family lose rank to their adult daughters (Combes & Altmann 2001). Daughters of high-ranking "" reach maturity earlier and conceive their first offspring earlier than those of lowranking "" (Altmann et al. 1988), particularly when groups are large. Males are the dispersing sex. Natal dispersal occurs at ca. 8.5 years of age (6.8–13.4), although recent evidence suggests that Olive !! and hybrid Yellow–Olive !! in the Amboseli area disperse earlier than Yellow !! (Alberts & Altmann 1995b, 2001). Secondary dispersal is common. Group tenure averages 24 months in non-natal groups. Male maturation is also affected by mother’s dominance rank. Sons of high-ranking "" physically mature earlier, as indicated by testicular enlargement, and attain adult dominance rank earlier than sons of low-ranking "" (Alberts & Altmann 1995b). Males form a linear hierarchy, but one that is much less stable than that of "" (Hausfater 1975). Fighting ability and age influence a male’s rank. Male dominance rank predicts mating success. Mating success and offspring production are coincident with the time a ! is highranking in a non-natal group (Alberts et al. 2006). Females have prominent oestrous swellings that are closely related to reproductive condition. When the " is in oestrus, !! and "" form close associations, called ‘consortships’. This form of mateguarding is characterized by a ! following and mating exclusively with the oestrous " for periods ranging from hours to several days (Rasmussen 1985). Fertilization is most likely to occur within the five days prior to the deturgescense of the sexual skin (Hendrickx & Kraemer 1969). Oestrogen levels are highest during this period, and consortships are most likely then, particularly with the highestranking ! (Gesquiere et al. 2007). Males, especially middle- and

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lower-ranking ones, sometimes form coalitions in order to take over a consortship. These !! are usually older and past their prime, and have been resident in the group for a relatively long time (Noë 1992). Approximately half of the !! in Amboseli commence reproducing (i.e. begin consorting) in their natal group. Maternal siblings are usually strongly avoided as consort partners. Although consortships between paternal siblings do occur, these consort pairs exhibit lower levels of cohesion and sexual behaviour than do nonkin pairs (Alberts 1999). Aggressive behaviours include lunging, staring, displaying the canines, and/or raising the eyebrows to show the white skin of the eyelids. Submissive gestures include cowering (of the whole body or part of the body), baring teeth while pulling back lips (in a grimace), screaming and raising the tail. Noisy and obvious fights between animals sometimes occur. More common, particularly among "", are the more subtle threats, displacements and responses to eyebrowraising. Infant deaths from infanticide or kidnapping occur rarely (J. Altmann & S. Alberts pers. obs.). Affiliative behaviours include reaching out a hand, huddling, grooming and remaining in close proximity. Grooming is common, and easily identifiable by the groomer’s active brushing and searching of another’s fur (sometimes removing dead skin flakes and ectoparasites) and by the relaxed posture of the individual being groomed. Adult and juvenile "" are the most common age/sex classes to engage in grooming. They groom each other, their infants and adult !!. New mothers are particular targets of grooming behaviour by other "" in the group. Adult !! groom "", primarily during consortship. Female infants become more reciprocal groomers with their mothers than ! offspring and at a younger age. Females tend to disproportionately groom and stay near certain individuals within their social group; these ‘friends’ are most commonly, but not exclusively, their close maternal and paternal kin (Smith et al. 2003, Silk et al. 2006). Infant Yellow Baboons ride ventrally on their mothers for the first few months and then gradually transition to predominantly ride dorsally or ‘jockey’ style by eight months. Contact is maintained primarily by the mother during the first month or two; as the infants age, however, they become more responsible for maintaining proximity to or finding their mothers (Altmann 1980). Infants and juveniles of both sexes spend considerable time playing with each other. By four years of age, play behaviour of the two sexes differentiates, and play groups tend to become single-sex; !! spend more time playing, and the play of !! becomes more rough (Pereira & Altmann 1985). The behavioural repertoire includes at least ten vocalizations, including contact calls, ‘grunts’ and ‘screams’. Grunts are given during foraging and may facilitate affiliative interactions and close spatial proximity. ‘Lip-smacking’ (a rapid movement of the tongue between the lips) is also an affiliative vocalization. Screams occur during agonistic interactions. Alarm calls and contact ‘barks’ also occur. Both sexes produce almost all of the vocalizations. Males produce a loud bark, a ‘wahoo’, more frequently than "" and in more varied contexts, including alarms and aggressive displays. Females produce individually identifiable copulation calls that vary in form over the menstrual cycle (Semple 2001). Specifically, calls are longer and contain more units during matings with higher-ranking !! (Semple et al. 2002). Infants produce a ‘coo’ distress call that is

Yellow Baboon Papio cynocephalus adult male.

virtually never given by adults. This rather mournful-seeming call is usually produced while the infant is crouching, and the call sometimes alternates with higher intensity screeches and ‘ikks’ (aka ‘geckers’). Reproduction and Population Structure Polygynandrous. A single infant is born after a gestation of ca. 180 days. Twinning is rare (twice in 700 births in Amboseli; in one case the twins were stillborn, in the other one infant died after ten days and the other survived). Infants weigh ca. 850 g at birth (Ross 1991). Yellow Baboons are not seasonal breeders; both conceptions and births occur at appreciable frequencies year-round. However, under harsh conditions, such as drought, reproduction is more likely to fail at each stage – cycling, conception and foetal survival (Beehner et al. 2006). Weaning is completed between 12 and 18 months of age. Nutritional intake of "" during their weaning period predicts their lifetime reproductive success (Altmann 1991). Males reach full adulthood at ca. 7–8 years of age. Although testicular enlargement, which is indicative of sperm production, occurs at a median age of 5.7 years (5.0–6.2, n = 32), the transition from subadulthood to adulthood occurs when !! enter the adult ! dominance hierarchy. At this time !! are large and strong enough to win fights with other adults. Median age of attainment of first adult dominance rank is 7.4 years (6.7–8.4). Adult !! then quickly rise in rank when young, but usually maintain high-ranking tenure for less than a year; eight months on average in Amboseli (Alberts et al. 2003; see Hamilton & Bulger 1990 and Packer et al. 2000 for similar patterns in Chacma and Olive Baboons, respectively). Attainment of adult dominance rank always precedes first consortship. Median age of first consortship is 7.9 years (7.4–8.5). High-ranking !! essentially monopolize consortships and, therefore, infant paternity during their tenure. As a result, age cohorts sometimes represent paternal sibships, although considerable variation exists in the extent to which this is true. Females mature, as indicated by first sexual swelling, at ca. 4.5 years (Rhine et al. 2000, including a table comparing ! life-history milestones for Mikumi and Amboseli). Median cycle length is 39 days, including adolescent and immediate postpartum cycles that 231

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are often longer than others (Gesquiere et al. 2007). Daughters of high-ranking mothers reach menarche and first conception earlier than those of low-ranking "". Following a period of adolescent sub-fertility, a " first gives birth at ca. 6.5 years (Rhine et al. 2000). Pregnancy is marked by pink colouration around the edge of the callosities, on the paracallosal skin and sometimes by pink under the eyes in late pregnancy. Pregnancy is usually characterized by an absence of sexual swelling. Inter-birth intervals average two years in wild-feeding groups, and as little as one year during times of food abundance or in garbage-feeding groups. If the infant dies, "" resume cycling within one month of the death and conceive within one or two cycles (Altmann et al. 1988). If the infant survives, the mother experiences a postpartum amenorrhoea of 10–12 months and experiences three or four cycles before conceiving. Sex ratio at birth is 1 : 1. Adult sex ratio is female-biased. In Amboseli wild-feeding groups have, on average, 1.6 adult "" per adult !, and groups with some garbage feeding have 2.5 adult "" per adult !; approximately half the population consists of sexually mature animals (0.61–1.35; Samuels & Altmann 1991). Infant mortality is approximately 30% within the first two years of life (Alberts & Altmann 2003). This is in addition to about 14% of pregnancies resulting in miscarriage (Altmann et al. 1988, Beehner et al. 2006). After the first two years of life, mortality rates are low until late adulthood. Median adult life-span is approximately 12 years in the wild. Maximum known life-span of wild Yellow Baboons is 27 years (Alberts & Altmann 2003). In captivity they can live into their early 30s (Bronikowski et al. 2002). Predators, Parasites and Diseases Known predators of Yellow Baboons include Leopards Panthera pardus, Lions Panthera leo, Spotted Hyenas Crocuta crocuta and Nile Crocodiles Crocodylus niloticus. Robust Chimpanzees Pan troglodytes communally kill and eat immature Yellow Baboons in Mahale Mountains N. P. (Wrangham & Van Zinnicq Bergmann-Riss 1990, Nishie 2004). Potential predators include Cheetahs Acinonyx jubatus, jackals, raptors and pythons. Black-backed Jackal Canis mesomelas and raptor predation attempts have been observed on juvenile Yellow Baboons only (Altmann & Altmann 1970). Leopards appear to be particularly adept predators of baboons due to their nocturnal hunting and ability to climb trees, but Spotted Hyenas or Lions may be the predominant predator in some locales or years, depending on abundance. Humans occasionally kill Yellow Baboons as pests. Starting >30 years ago (Kalter 1973), parasite screening of blood or faeces has occasionally been conducted for laboratory and field populations of various baboon species (see the recent, ongoing public database at www.mammalparasite.org). None the less, prevalence, incidence, temporal changes within populations and extent of pathogenesis remain largely unknown for virtually all parasites and baboon populations. This gap may soon be redressed as a recent surge of interest in primate disease has already resulted in one book (Nunn & Altizer 2006). The malaria-like parasite Hepatocystis simiae occurs in Yellow Baboons (Phillips-Conroy et al. 1988, Tung et al. 2009). In Amboseli screening for gastrointestinal parasites has been conducted several times and most recently reported in Hahn et al. (2003). Coxsackie virus type B2, a paralytic disease, has been found in wild populations, including Amboseli (Kalter 1973). SIV has been reported in two Yellow Baboons in

Mikumi N. P. (Kodama et al. 1989). In a serum viral screening (M. Isahakia pers. comm.) no SIV was found in approximately 80 animals in the Amboseli area. Specific causes of death may differ by location and over time even in the same population as predator presence, disease presence and environmental factors change. More than half of the deaths in the Amboseli population are probably due to predation. Conservation IUCN Category (2012): Least Concern. CITES (2012): Appendix II. Although theYellow Baboon is not currently threatened, the effects of human encroachment on numbers remain unclear. The baboons’ tendency for crop-raiding and foraging in areas of human habitation has caused them to be treated as vermin in many areas, creating a situation that might lead, in the short-term, to local extinction, and in the long-term to more broad endangerment. However, their prevalence in non-farmland areas in Kenya and Tanzania reduces their vulnerability to human–animal conflict. Habitat changes may also influence population size, density and ranging patterns. Although the cause(s) of decline in the baboon population in Amboseli in the 1960s is unknown, the dependence of Yellow Baboons on woodland savanna, and the degradation of this habitat in the Amboseli area, has caused local changes in range and range use in the decades since then. The woodland loss in Amboseli since the 1970s is associated with temperature increases in the area as a result of global climate change (Altmann et al. 2002). Measurements Papio cynocephalus HB (!!):730 (620–840) mm, n = 6 HB (""): 620 (550–680) mm, n = 4 T (!!): 600 (450–660) mm, n = 6 T (""): 500 (380–560) mm, n = 4 WT (!!): 24.9 (22.8–28.3) kg, n = 3 WT (""): 13.6 kg, n = 1 BMNH, various locations (Napier 1981) WT (!!): 25.8 kg, n = 20 WT (""): 11.9 kg, n = 18 Wild-foraging individuals at Amboseli N. P., Kenya; see source for body measurements for garbage-feeding individuals (Altmann et al. 1993) WT (!!): 24.7 (21.6–29.4) kg, n = 33 WT (""): 13.0 (10.5–16.1) kg, n = 43 Wild-foraging individuals at Amboseli N. P., Kenya (2006–08; S. Alberts & J. Altmann pers. obs.) WT (!!): 22.6 (18.6–27.7) kg, n = 35 WT (""): 12.1 (9.1–16.8) kg, n = 35 Wild-foraging individuals at Mikumi N. P., Tanzania (J. Rogers pers. comm.) Key References Altmann 1980, 1998; Amboseli Baboon Project website: www.princeton.edu/~baboon; Rhine et al. 2000. Jeanne Altmann, Stephanie L. Combes & Susan C. Alberts

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Papio anubis OLIVE BABOON (ANUBIS BABOON) Fr. Babouin Doguera; Ger. Anubispavian Papio anubis (Lesson, 1827). Manuel de Mammalogie ou Histoire Naturelle des Mammifères, p. 27. Upper Nile.

some populations. Tail well-furred, sometimes bent at acute angle midway (due to fused tail vertebrae), appearing as if ‘broken’. Ischial callosities variable shades of grey. Adult !! much larger than adult "" and with heavy, but not large, mane (= cape = mantle). Adult "" are about 54% the weight of adult !!. Canines of adult !! long and pointed (worn down or broken in older individuals). Adult " with much less well developed mane and smaller canines than !. Fertile "" undergo monthly cycles of conspicuous swelling of the pink/red perineal sexual skin. Paracallosal skin pink during pregnancy. Infants have black natal coat, pink face and paracallosal region; skin typically changed to black by 10–12 months of age, though maturational change in pelage colouration is more variable. Numerous photographs of P. anubis at many sites in Kenya and Tanzania are available at: www.wildsolutions.nl

Olive Baboon Papio anubis adult male.

Taxonomy Monotypic species. The ‘tangle’ characterizing baboon taxonomy (Groves 2001: 237) has generated at least three classifications for ‘Olive Baboon’: (1) a species, closely allied to Yellow Baboon Papio cynocephalus, Guinea Baboon Papio papio and Chacma Baboon Papio ursinus; or (2) a subspecies of a single species (P. cynocephalus) uniting these four forms under the common name ‘Savanna Baboon’; or (3) part of a ‘superspecies’ comprising these four taxa plus the Hamadryas Baboon Papio hamadryas (Sarmiento 1998a, b). Mitochondrial data argue compellingly against the second of these taxonomies and underscore the close phylogenetic relationship of Olive Baboons and Yellow Baboons (Newman et al. 2004, Zinner et al. 2009a, b). Four to seven geographic variants (subspecies) of Olive Baboon have been recognized (Hill 1967, 2000, Napier & Napier 1967). Currently, however, no subspecies are recognized (Groves 2001, 2005c, Grubb et al. 2003). Synonyms: doguera, furax, graueri, heuglini, lestes, lydekkeri, neumanni, nigeriae, niloticus, olivaceus, silvestris, tessellatum, tibestianus, vigilis, weneri, yokoensis. Chromosome number: 2n = 42 (Romagno 2001). Description Large, semi-terrestrial, diurnal monkey. Nares frequently projecting beyond nose (cf. ‘upturned’ nose of Yellow Baboon). Top of head appears flat when viewed from the front. Face naked, dark grey to black, framed by prominent ruffs of hair at cheeks. Ears large, though usually obscured by surrounding pelage. Pelage coarse, varying from dark grey to olive-brown, sometimes grading into olive- or light brown (khaki or grey). Dorsum and ventrum similarly coloured. Pelage of hands and/or feet black in

Geographic Variation Four to eight geographic variants differentiated as subspecies (Hill 1967, Napier & Napier 1967) or even species (Elliot 1913b). Nevertheless, in spite of geographic variation in coat colour, the distribution of black pelage on hands and feet, and cranium size, Jolly (1993: 7) emphasizes how ‘remarkably similar’ Olive Baboons are across their entire distribution. Based on cranial measurements, the forms found in Uganda and DR Congo appear largest, while the smallest are Saharan isolates and populations in Tanzania and Ethiopia where distribution adjoins that of the Yellow Baboon and Hamadryas Baboon, respectively (Jolly 1993). One commonly cited form, the so-called ‘Heuglin’s Baboon’ of S Sudan and SW Ethiopia, is of unclear status: its wavy hair and mane are shared in common with other Olive Baboons, but its lighter colour and pale cheeks and undersides are distinctly different (Sarmiento 1998a). Similar Species Papio cynocephalus. Sympatric or parapatric in SE Ethiopia, W Somalia, C and S Kenya, N Tanzania and south-east DR Congo. More gracile (slender). Mane of !! generally absent or much less developed. Dorsum light brown to yellowish-brown. Tail not ‘broken’. Nose ‘upturned’ (see above). Head appears pointed when viewed from the front. Papio papio. Closely adjoining and probably parapatric in Mali and perhaps Guinea. Said to be sympatric in Sierra Leone (T. S. Jones in Booth 1958b). Smaller, with lighter, uniformly grizzled reddishbrown pelage; mane of adult ! more pronounced; tail arched. Papio hamadryas. Sympatric or parapatric from above ca. 500 m on western edge of range in Ethiopia and Eritrea. Body smaller. Facial skin bright pink to red. Cheek tufts long, laterally projecting and silvery.Tail gently arched at distal end. Mane of adult !! generally much more prominent (to elbows) and silvery, contrasting with back. Male anogenital area is reddish. Theropithecus gelada. Sympatric in highlands of N Ethiopia. Altitudinal overlap from ca. 2300–3800 m. Less prognathic. Mane extends to below elbows. Tail not ‘broken’. Patch of naked pink skin on upper chest in both sexes. 233

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Distribution Endemic to tropical Africa, mostly north of the equator. Sudan Savanna, Guinea Savanna, Northern Rainforest– Savanna Mosaic, Eastern Rainforest–Savanna Mosaic, Afromontane– Afroalpine, and Somalia–Masai Bushland BZs. Distribution more extensive than any other baboon; in fact, most African primates generally (only 3 of 64 species have larger latitudinal range; Cowlishaw & Hacker 1997). Straddles circumtropical Africa from Mauritania to N Cameroon eastward to C Ethiopia and SW lowlands of Eritrea, southwards through East Africa as far as SE DR Congo, Burundi and NC Tanzania (Wolfheim 1983). Southern-most population in Tanzania is probably at Mt Hanang (4° 28´ S, 35° 24´ E, 2050 m asl; T. Butynski & Y. de Jong pers. comm.). Isolated populations occupy Tibesti Plateau (20° N, 16° E) and Aïr Massif in Saharan Chad. In the wild a broad hybrid zone with Yellow Baboon runs along a north-east/south-west line from at least Meru N. P. in the north, through Tsavo East N. P. to the south-west Amboseli Basin, Kenya, to L. Manyara N. P., Tanzania (Alberts & Altmann 2001, Y. de Jong & T. Butynski pers. comm.). Hybridizes with Hamadryas Baboon in Ethiopia (Nagel 1973), SC Eritrea (Zinner et al. 2001c, 2009b), and Somalia (J. Beehner pers. comm.). In one stable hybrid zone along a 20 km stretch of the Awash Valley, C Ethiopia, admixture is maintained by movements of !! of both parental species, as well as of hybrid stock, among 8–12 groups (Phillips-Conroy et al. 1992). Hybridizes with Geladas Theropithecus gelada in Ethiopia (Dunbar & Dunbar 1974c, Jolly et al. 1997). Hybridization is suspected, though unsubstantiated, where distributions of Olive Baboons and Guinea Baboons presumably abut in Mali (Groves 2001).

Mt Orobo, Ethiopia, which is about 500 m above the treeline (Bolton 1973). Lowest altitude reported for East Africa (where the Yellow Baboon occupies the lower regions) is at 540 m in Meru N. P., C Kenya (Y. de Jong & T. Butynski pers. comm.). Highest altitudes reported for East Africa are 2500 m in the Echuya F. R., SW Uganda (E. E. Sarmiento pers. comm.), 2300 m in the Bwindi Impenetrable N. P., SW Uganda, 2370 m at Nyahururu (Thompson’s Fall), C Kenya, and 2550 m at Empakai Crater in the Ngorongoro Conservation Area, NC Tanzania (Y. de Jong & T. Butynski pers. comm.). Typically an open-country species, and thus common in Sudan and Sahel savannas, grassland, woodlands and rocky hill habitats. Individuals in some populations, however, spend up to 50–60% of their activity period in forest (Rowell 1966); mixed forest-mosaic and mid-altitude and montane forest (e.g. W Uganda, NE DR Congo), and high-altitude bamboo Arundinaria alpina forest (DR Congo). When in closed-canopy moist forest, P. anubis is seldom found more than 2 km into the forest. Papio anubis is nowhere known to live entirely within closed-canopy moist forest (T. Butynski pers. comm.). In the dry montane forest of the Mathews Range, C Kenya, P. anubis is common and appears to spend almost all of the time deep within forest, although there is some use of the limited ‘open habitats’ (cliffs, tallus slopes, burnt sites). Here it is important to note that all other cercopithecines are absent except for De Brazza’s Monkey Cercopithecus neglectus (which is uncommon here). As such, this might be a case of ‘competitive release’, perhaps especially in the absence of Sykes’s Monkey Cercopithecus mitis (De Jong & Butynski 2010a). Also inhabits semi-desert steppe and arid thorn scrub with gallery forest (Ethiopia) (Aldrich-Blake et al. 1971, Dunbar & Dunbar 1974b), though may be limited to river beds and gallery forests in these habitats (Zinner et al. 2001c). Makes use of mangrove forest in Kenya (T. Butynski & Y. de Jong pers. comm.) and in Ghana (L. Depew & I. Gordon pers. comm.) but does not appear to be able to live solely in this habitat. Habitat selection is limited primarily by availability of water and secure sleeping sites. These baboons require regular access to water, and moisture from subterranean plant parts is important in dry seasons. Where studied, P. anubis inhabits areas with mean annual rainfall of 2022 mm in E Nigeria (Gashaka-Gumti N. P., Higham et al. 2009), 1400–1500 mm in SW Uganda (Bwindi Impenetrable N. P., Butynski 1985; Budongo F. R., Plumptre 1996; Kibale N. P., Struhsaker 1997), to 570 mm in Ethiopian semi-desert (J. Beehner pers. comm.), and ca. 300–900 mm in W Eritrea (Zinner et al. 2001c), with intervening values elsewhere, such as 710–756 mm in the Eastern Rift Valley, Kenya (Harding 1976) and 550 mm on the Laikipia Plateau, Kenya (Barton et al. 1996). Must have access to communally used sleeping refuges providing safety from predators: either large trees (e.g. Fever Trees Acacia xanthophloea in gallery forests [R. Palombit pers. obs.], Oil Palms Elaeis guineensis along L.Victoria [A. Matsumoto-Oda pers. comm.] or steep cliff faces or rocky inselbergs (‘koppies’) [DeVore & Hall 1965]).

Habitat As befitting its wide geographic range, P. anubis occupies an enormous variety of vegetation and climatic conditions from lowlands to high mountains. Found near sea level in Ghana (Depew 1983, L. Depew & I. Gordon pers. comm.) and probably also Togo, Bénin and SW Nigeria (Wolfheim 1983, Sarmiento 1998a). Occurs at 500–3300 m in Ethiopia (Yalden et al. 1977). Sighted at 3850 m on

Abundance Considered ‘abundant or common’ in at least eight countries (Wolfheim 1983). Population density varies from 4 ind/km2 in arid savanna–woodland habitats (DeVore & Hall 1965), 11–14 ind/ km2 in moist forests in W and SW Uganda (Rowell 1966, Butynski 1985, Plumptre & Reynolds 1994), to 30–35 ind/km2 in moist forests in W Tanzania (Ransom 1981) and WC Uganda (Struhsaker 1997).

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Adaptations Diurnal and semi-terrestrial. Primary adaptation is extreme adaptability and flexibility to conditions, as exemplified by ability to exploit foods of many kinds. Digitigrady (body weight borne on volar surfaces of fingers) represents morphological adaptation for increased efficiency of terrestrial locomotion (Whitehead 1993), convergent in kind with ungulate specialization. ‘Sunbathing’ at the sleep tree or sleep cliff in early morning is common (R. Palombit pers. obs.). Ambient temperature affects activity budgets (Dunbar 1994) and social behaviour, such as ventro-ventral contact and huddling of mothers with infants, which are negatively correlated with temperature (Brent et al. 2003). Foraging and Food Omnivorous. Feeding occurs throughout daylight hours. Of the daily activity budget, feeding variably accounts for 20% (Ghana; Depew 1983), 26% (Tanzania; Ransom 1981), 31% (Ethiopia; Nagel 1973), 31% (Nigeria; Warren 2003), 40% (Kenya; Barton 1989), 41% (Côte d’Ivoire; Kunz & Linsenmair 2008b) and 51% (Kenya; Harding 1976). Diet shifts continually with season and even time of day, allowing exploitation of a range of items as they become available in space and time.Time spent feeding does not vary significantly across seasons, however (Bercovitch 1983). Diets do not differ qualitatively between the sexes, but "" spend significantly more time feeding than do !! (except when engaged in sexual consortships) (Bercovitch 1983). Ecological adaptability of P.anubis is exemplified by a dietary diversity so pronounced that early researchers remarked it would be easier to list foods not eaten, than to attempt a complete inventory. Tallies of plant species eaten vary from 22+ (Rowell 1966), 45+ (Barton et al. 1993), 62+ (Ransom 1981), 84 (Kunz & Linsenmair 2008b), 94+ (DeVore & Hall 1965), to 111 (Warren 2003). Plants constitute the majority of diet, up to 98% in Kenya (DeVore & Hall 1965) and Côte d’Ivoire (Kunz & Linsenmair 2008b). Digging up rhizomes – as well as other forms of underground storage parts in plants (e.g. bulbs, tubers, corms) – represents a principal ecological adaptation made possible by baboons’ combination of prehensile hands and committed terrestriality. Underground storage parts account for up to 16% of the plant diet (Barton et al. 1993). Grass (e.g. Paspalum conjugatum) is a principal food for Olive Baboons in savanna/woodlands, but also for ‘forest dwelling’ Olive Baboons, which forage extensively in nearby grass plains (Rowell 1966). Diverse grass parts are utilized: young meristems growing in moist soil, seeds (filtered by pulling distal ends of intact stems through the mouth [R. Palombit pers. obs.]) and nutrient- and water-rich subterranean rhizomes. Ripe and unripe fruits eaten, particularly in forests where preference is for fleshy fruits, such as figs Ficus spp. (DeVore & Hall 1965, Barton et al. 1993). In more arid regions they eat less pulpy fruits of trees and bushes/shrubs (e.g. Carissa edulis, Scutia myrtina [R. Palombit pers. obs.] and Parkia biglobosa [Kunz & Linsenmair 2007]). Olive Baboons are likely dispersal agents for numerous plants (e.g. Securinega virosa, Azadirachta indica, Nauclea latifolia, Lannea acida, Diospyros mespiliformis, Tapura fischeri, Oxyanthus racemosus [Lieberman et al. 1979, Kunz & Linsenmair 2008a]). Seeds are also eaten, particularly of drier fruits (e.g. Acacia tortilis, Acacia drepanolobium [R. Palombit pers. obs.]). Partially digested seeds are harvested from the fresh faeces of herbivores (e.g. Impala Aepyceros melampus, African Buffalo Syncerus caffer, Savanna Elephant Loxodonta africana). Flowers are eaten seasonally (e.g. A. xanthophloea, A. drepanolobium, Cullumia squarrosa

[DeVore & Hall 1965]). Along waterways Olive Baboons eat aquatic plants (e.g. Trifolium sp. and roots/storage parts of Nymphaeaceae [R. Palombit pers. obs.]). Numerous species among the herbaceous ground cover provide food in the form of fruits, seeds, flowers and, occasionally, young leaves. Fungal mychorriza and fruiting sporophores are exploited (R. Palombit pers. obs.); discovery of large mushrooms excites as much feeding competition as predatory capture of meat (see below). Gum is an important dietary supplement in drier habitats (e.g. A. drepanolobium-dominated woodland in C Kenya). Adult Olive Baboons access tree cambium by peeling bark off or, more often, by snapping saplings (requiring strength more often possessed by adult !!). Papio anubis is a human commensal in some locales, feeding in garbage dumps near towns, small settlements and tourist lodges (Kemnitz et al. 2002). They also exploit foods introduced by humans (e.g. the base stem of prickly pear cactus Opuntia vulgaris [R. Palombit pers. obs.] and plants domesticated for agriculture, see below). Insects are eaten consistently but opportunistically, usually via random discovery of individuals (particularly orthopterans and lepidopterans) in grass or underbrush, or small numbers of ants and termites exposed as searching baboons systematically overturn rocks (DeVore & Hall 1965, Rowell 1966). Olive Baboons of Laikipia Plateau, C Kenya, regularly eat harvest ants (Crematogaster spp., Camponotus spp., Tetraponera spp.) residing symbiotically inside galls of A. drepanolobium (R. Palombit pers. obs.). Also eaten are temporarily superabundant insects, e.g. termite alates during nuptial flights and infestations of army worm caterpillars (DeVore & Hall 1965). Other invertebrates taken include scorpions and snails (terrestrial and aquatic) (DeVore & Hall 1965, Rowell 1966). Although the Olive Baboon’s catholic diet is unambiguously vegetarian, meat constitutes a potentially important protein supplement. In two populations occupying different habitats, a successful predation event was observed every 22 h (Harding 1973) and 30 h (Rowell 1966). As with plant foods, a great variety of vertebrate prey are eaten, including fish, frogs, lizards, crocodile eggs, terrapins, birds (caught on the ground or occasionally on the wing, e.g. guineafowl Agelastes spp., Yellow-necked Spurfowl Francolinus leucoscepus, nightjars, quail, plover), birds’ eggs, various rodents (mice, ground squirrels, tree squirrels), bats, Cape Hares Lepus capensis,Vervet Monkeys Chlorocebus pygerythrus, small antelopes (e.g. Guenther’s Dikdik Madoqua guentheri), Oribi Ourebia ourebi,Thomson’s Gazelle Eudorcas thomsonii and Grant’s Gazelles Nanger (granti) granti, and the young only of larger ungulates (Impala, Bushbuck Tragelaphus scriptus, Hartebeest Alcephalus buselaphus) (Rowell 1966, Kingdon 1971, Harding 1973, Brashares & Arcese 2002). Of these animals, hares, mice and small antelopes are the most common prey. The ecological relationship with prey such as Impalas, Bushbucks and Vervet Monkeys is curious, since Olive Baboons also associate with these animals without causing alarm (see below). Carrion is exceptional as a food. Prey is located by (literally) stumbling upon it, and captured by seizing it and immediately commencing eating (usually while the prey is still alive). Behaviour reminiscent of more deliberate ‘hunting’ also occurs. Careful and apparently purposeful scanning of vegetation, flushing of prey, and pursuit precede some instances of successful captures, suggesting organized predatory behaviour (Harding 1973). Olive Baboons hunt individually, however, not cooperatively. Juveniles, as well as adults, are able to capture small prey (e.g. mice and small birds), which is eaten quickly in a gulp or two; larger prey (the size of an adult hare and above) requires a long processing time 235

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and are most often captured by adult !! (Harding 1975). Capture of large prey arouses social tension as well as overt aggression, as the carcass makes its way ‘up the hierarchy’, being surrendered to progressively higher-ranking !! arriving at the scene of the kill (R. Palombit pers. obs.). Direct food sharing (cf. Robust Chimpanzees Pan troglodytes) has not been observed, although adult !! tolerate the proximity of certain individuals (particularly fertile ""), which will snatch scraps of meat from the ground. An interesting, but as yet unsubstantiated, proposition is that variation in predatory behaviour reflects the action of cultural transmission, generating contrasting ‘traditions’ of meat-eating (Strum 1975). Polyspecific associations are relatively rare, but Olive Baboons associate with Impalas, Bushbucks, Plains Zebras Equus quagga and Vervet Monkeys in apparent mutualism. Ungulates and Olive Baboons beneficially attend to each other’s alarm calls (DeVore & Hall 1965), while young Vervets and Olive Baboons sometimes play with one another (Kingdon 1971). Social and Reproductive Behaviour Social. Olive Baboon groups vary from 12 to as many as 130 individuals. Average group size is reported as 87.5 individuals (S.D. = 20.4, n = 4) in C Kenya (Berger 1972b), 65 individuals (S.D. = 34, n = 7) in Kenya (Harding 1976), 30 individuals (S.D. = 24.8, n = 6) in Ethiopia (Brett et al. 1982), 32 individuals (S.D. = 12.8, n = 8) in Tanzania (Ransom 1981), 30 individuals in Ghana (Depew 1983), 20.7 individuals (S.D. = 5.1, n = 22) in Nigeria (Higham et al. 2009), and 15 individuals (n = 8) in Côte d’Ivoire (Kunz & Linsenmair 2008b). Socionomic sex ratio of adult "" per adult !! varies from 1.65 (Tanzania; Ransom 1981), 2.02 (Kenya; Barton 1989), 2.22 (Ghana; Depew 1983), 2.5 (Kenya; DeVore & Hall 1965) to 3.83 (Kenya; Harding 1976). Greater preponderance of adult "" arises more through sex differences in maturation rates rather than differential mortality. Immature individuals typically outnumber adult "" 2 : 1. Males typically disperse from natal groups at 6–9 years of age, although emigrations at ages as young as four years occur (Packer 1979a). Given the rarity of sightings of solitary individuals, they apparently soon enter another group rather than live alone for prolonged periods. Females are philopatric, remaining in their natal groups their entire lives (with rare exceptions).This sex difference generates the matrilineal structure of Olive Baboon groups: related "" affiliate with one another and compete with other sets of "" relatives. Male and " relationships are organized into dominance hierarchies that are maintained by a rich repertoire of vocal, visual and tactile communicative displays (e.g. the subordinate ‘grimace’ facial expression), and by occasional aggression. Females usually acquire dominance status via ‘youngest daughter ascendancy’, in which a maturing " assumes a rank position immediately below her mother and above her older sisters (as well as all of the "" ranking below her mother) regardless of body size (Hall & DeVore 1965, Ransom 1981, Strum 1987). Female hierarchies are typically linear and highly stable, changing little over lifetimes. Male social relationships are also generally organized around dominance status, but in contrast to "" hierarchies are more variable, dynamic and even obscure at times (Packer 1979b, Harding 1980, Ransom 1981, Strum 1982, Sapolsky 1993). Male hierarchies are not always linear, e.g. when individual alliances generate ‘clusters’ of !! that collectively dominate one another (Hall & DeVore 1965). Males also experience substantial changes in rank during

their lives. This is partly because immigration of new male(s) may temporarily destabilize the hierarchy (Sapolsky 1993), and partly because coalitionary behaviour undermines the stability of dominance relationships. Thus, ! rank is apparently influenced by body and canine size, and physical stamina, but also by social skill in forming and maintaining coalitions. In addition to their unambiguous competitive basis, social relationships among !! also show conspicuous affiliative components, which are likely related to maintenance of these alliances (Harding 1980, Smuts & Watanabe 1990). Olive Baboons are polygynous. Adult "" can copulate at any time, but proceptivity and receptivity generally track the monthly menstrual cycle (Hall & DeVore 1965, Ransom 1981, Bercovitch 1991). Adult ! sexual interest depends largely on the condition of the female’s sexual skin, which is generally correlated to ovulatory status (Wildt et al. 1977, Higham 2008a, b, Daspre et al. 2009). Males closely follow and groom fertile "" while the sexual skin increases gradually in size, but cease this ‘sexual consortship’ after the rapid ‘deflation’ of the skin 2–3 days following ovulation (Bercovitch 1986). Females ‘present’ hindquarters to !! to solicit close examination of the sexual swelling and/or copulation. Copulation rarely involves conspicuous vocalizations (Bercovitch 1991). There is debated evidence that "" of greater reproductive quality (i.e. earlier menarche or greater offspring survival) have consistently longer swellings (Domb & Pagel 2001, Zinner et al. 2002a). This suggests an intriguing, but unsubstantiated, potential for !! to use visible variation in females’ swellings to discriminate among potential mates and to mediate mating competition with rival !!. Male Olive Baboons compete intensely with one another to maintain sexual consortships – and thus copulatory access – with swollen fertile "", especially maximally swollen "". The strong sexual dimorphism of the species is a likely consequence of this competition. Dominant !! are generally more successful than subordinate rivals in obtaining periovulatory matings, but coalitionary confrontations by multiple !! may override an individual’s dominance advantage (Bercovitch 1988). Typically, two or more ‘follower’ !! tag along behind a consort pair for hours or even days (Danish & Palombit 2008), and then cooperatively displace a (sometimes higher-ranking) ! from his consortship through threats and/or aggression; one of the coalitionary challengers then becomes the new consort of the " (Hall & DeVore 1965, Ransom 1981, Strum 1987, R. Palombit pers. obs). This behaviour was originally interpreted as an example of reciprocal altruism, in which unrelated ! allies presumably take turns obtaining the mating opportunities achieved through successive coalitionary episodes (Packer 1977). Unambiguous symmetry of benefits has not been substantiated by subsequent research, however (Noë & Sluijter 1995). Middle-ranking !! are more likely than high- or low-ranking !! to develop the affiliative bonds that engender successful coalitionary cooperation. Newly immigrant !! are disproportionately the targets of such coalitions. Although most conspicuous in the reproductive context, ! coalitions also occur during disputes over meat, defence of infants, general aggression and for no obvious reason (Smuts 1985). Stable alliances between !! can obscure dominance relationships by altering the rank of a ! in the presence of his ally. Thus, a positive correlation between non-natal adult ! rank and mating success has been documented in some studies (Packer 1979a, b), but not in others (Bercovitch 1986). Variation in male–male aggressiveness and affiliation is also attributed to cultural transmission of contrasting social ‘traditions’ (Sapolsky & Share 2004, Sapolsky 2006).

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Olive Baboons Papio anubis.

Lactating "" (and sometimes pregnant "") associate conspicuously with a particular adult ! or two (Smuts 1985, R. Palombit pers. obs.). These cohesive ‘friendships’ may beneficially promote ! protection of "" and/or their dependent infants from harassment from other (higher-ranking) "" and especially !!. This has been substantiated by playback experiments, which show that !! respond significantly more strongly to the distress vocalizations of their "" friends than control "" of similar rank and reproductive status (Lemasson et al. 2008). Furthermore, cortisol levels in lactating "" suggest that ! friends buffer "" from harassment-induced stress (Shur 2008). In particular, the hormonal data suggest that lactating "" are susceptible to stress from harassment by adult !! (rather than higher-ranking ""), and that friendships with !! may ameliorate this stress. Mating patterns suggest that these ! associates are often, but not always, the fathers of the infants of their " ‘friends’. In cases where a ! is not the father of his " friend’s infant, Smuts (1985) hypothesized that he will be preferentially selected by the mother as sire of her next infant. Genetic data are currently unavailable to test these alternatives directly. Higher-ranking "" generally achieve greater lifetime reproductive success than lower-ranking rivals, due to earlier menarche, faster reproductive rate (e.g. inter-birth intervals up to six months shorter), or greater offspring survivorship (Smuts & Nicolson 1989, Packer et al. 1995, Garcia et al. 2006). Compared to subordinates, however, dominant "" experience higher rates of spontaneous abortion and miscarriage (Packer et al. 1995), though the explanation that this results from higher circulating levels of androgens is questioned (Altmann et al. 1995). In any event, any greater difficulties in completing pregnancies do not override other reproductive advantages of high rank, which derive primarily from priority of access to resources via supplanting of subordinate rivals from food sources. Thus, "" at the top of the hierarchy may obtain food at rates 30% higher than those at the bottom (Barton & Whiten 1993). In addition to these nutritional issues, rank-related reproductive rates may be influenced by psychosocial stress (Rowell 1970a, Bercovitch

& Strum 1993) and access to !! as protective associates (Smuts 1985). Agonistic interaction accounts for a larger proportion of the activity budget of "" than of !! (Bercovitch 1983). Coalitions among related "" do occur, but usually less frequently than among !! (Johnson 1987, Barton et al. 1996). Reconciliation behaviour following conflicts occurs among all age/sex classes, but is more common among " kin (Castles & Whiten 1998). The Olive Baboon has a rich and diverse vocal repertoire that has not been rigorously studied since Hall & DeVore’s (1965) initial description (see also Ransom 1981). The loud bi-phasic ‘wahoo’ is arguably the most conspicuous call, audible up to 3.0 km, given primarily by adult !!, and elicited by intense male–male aggression (intra- and intergroup), encounters with predators, or spontaneously (in sleep trees usually). This vocalization, however, occurs far less frequently than the more common barks, growls, grunts, screams and coughs that mediate intra-group social interactions in, currently, unclear ways. There is great variation in mean home-range size; 4–5 km2 in moist forest or semi-forest habitats (Rowell 1966, Ransom 1981); 0.4–1.7 km2 (Kunz & Linsenmair 2008b), 1.5 km2 (Warren 2003), 19.7 km2 (Harding 1976), 31.0 km2 (Smuts 1985) and 43.6 km2 (Barton et al. 1992) in drier savanna/woodlands; 4.3 km2 (AldrichBlake et al. 1971) and 0.9 km2 (Dunbar & Dunbar 1974b) in arid thorn scrub. Mean daily distance travelled is 2.4–6.0 km in savannas (Harding 1976, Barton et al.1992, Kunz & Linsenmair 2008b), 2.4 km in forests (Rowell 1966) and 1.2 km in arid Ethiopia (Dunbar & Dunbar 1974b). In savanna/woodland habitats day range increases as resources become seasonally scarcer, suggesting a time-minimizing (rather than energy-maximizing) foraging strategy (Barton et al. 1992). Access to waterholes particularly influences ranging in dry season. Groups are not territorial. Home-ranges overlap extensively. Inter-group interactions are frequently peaceful, after which one group (often the smaller) moves off (DeVore & Hall 1965). Chases may occur, but these are often adult !! herding "" of their own group away from the other group. Individuals from neighbouring 237

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groups sometimes commingle completely, but tensions run high and intense fighting can suddenly break out, involving numerous individuals of both sexes; in one episode in Kenya multiple !! and "" mobbed a subadult ! from another group, fatally wounding him (R. Palombit pers. obs.). Reproduction and Population Structure Onset of puberty in !! (i.e. testicular enlargement) occurs at 5–6 years of age (Packer 1979a) when !! are ca. 7–8 kg (Jolly & Phillips-Conroy 2003). Testes, body size and mane length attain maximal adult proportions at around the same time (Strum 1991, Jolly & PhillipsConroy 2003), which has been reported at 6.5–7.5 years (Packer 1979a) and 9–10 years of age (Glassman et al. 1984, Strum 1991). Canine eruption occurs at about eight years (Strum 1991). Females reach sexual maturity (i.e. commence monthly menstrual cycling) at ca. 4.5–5 years, pass through a period of adolescent sterility and give birth for the first time at ca. 6–7 years (Packer 1979a, Scott 1984, Bercovitch & Strum 1993, Williams-Blangero & Blangero, 1995). Mean inter-birth interval (in months) ranges from 22.2 (Packer 1979b), 23.5 (Kenyatta 1995), 25.2 (S.E. = 1.2, n = 13; Smuts & Nicolson 1989), 29.9 (Higham et al. 2009), 30.3 (Depew 1983). Inter-birth intervals are much shorter for "" that obtain additional food through captive provisioning (mean = 15.0 months, S.D. = 0.70, n = 21; Garcia et al. 2006) or crop-raiding (16.5 months) (Higham et al. 2009). Breeding occurs throughout the year (Bercovitch & Harding 1993). In some (not all) populations a peak in births occurs at the onset of rains (e.g. in Oct–Dec in Kenya), just before food supplies also peak (DeVore & Hall 1965). Single young are born after a gestation of 180–185 days (154–185 days; Packer 1979a, Smuts & Nicolson 1989, Garcia et al. 2006). Weight at birth in captivity is 980 g for !! (670–1220 g, n = 77) and 920 g for "" (700–1400 g, n = 66; Coelho 1985). Twins not reported. Direct care of infants (e.g. nursing, carrying) is predominantly by mothers, although mothers’ " kin and ! ‘friends’ (see above) may interact affiliatively with infants at high rates. Weaning is gradual and difficult to demarcate, but is generally complete by 300 days (Packer 1979a) to 420 days of age (Nicolson 1982). Adolescents of both sexes experience a growth spurt, which is delayed and more intense in !! (Glassman et al. 1984). Mean inter-birth intervals are 22–26 months for Tanzanian and Kenyan populations (Packer 1979a, Smuts & Nicolson 1989, Kenyatta 1995), and 30 months for a Ghanaian population (Depew 1983). If infants die, mothers resume cycling within 1–3 months and are shortly, thereafter, pregnant again (Collins et al. 1984, Smuts & Nicolson 1989). Infant mortality is 57% among primiparous mothers, 16% in multiparous "" (Nicolson & Smuts 1989), and is due primarily to disease, predation and nutritional/energetic stress. Infanticide by !! is widespread but uncommon (accounting for 80% of encounters. Mixed groups include either one species (57% of encounters), two species (37%) or three species (6%; McGraw 1994). At both sites, such associations include Grey-cheeked Mangabey Lophocebus aterrimus in >80% of encounters.This pattern is similar to C. pogonias, which most frequently associates with L. albigena. Cercopithecus wolfi also often associates with C. ascanius (50% of encounters). Less often, mixed groups include Angola Colobus Colobus angolensis (Lomako and Salonga) and/or Tshuapa Red Colobus Procolobus rufomitratus tholloni (Salonga). Reproduction and Population Structure No field data available. It is likely that life history characteristics are similar to those of C. pogonias.Two captive-born !! gave birth for the first time when five years old.Then they reproduced at one to three year intervals with a mean of about two years (n = 11 births; T. Petit pers. comm.).

Predators, Parasites and Diseases Little is known about predation or disease in C. wolfi. African Crowned Eagle Stephanoaetus coronatus, Central African Rock Python Python sebae, African Golden Cat Profelis aurata are likely predators. Conservation IUCN Category (2012): Least concern as C. p. wolfi. CITES (2012): Appendix II. Habitat loss and hunting for the bushmeat trade are the two primary threats. Cercopithecus wolfi is an alert and fast-moving species, characteristics that make it relatively difficult to hunt. This, together with a small body size, probably makes C. wolfi one of the least attractive targets in the diurnal primate community (Butynski & Sanderson 2007). Measurements Cercopithecus wolfi HB (""): 485 (445–511) mm, n = 3 T (""): 779 (695–822) mm, n = 3 HF: n. d. E: n. d. WT (""): 3.9 (2.6–5.0) kg, n = 17 WT (!!): 2.9 (1.8–3.7) kg, n = 120 Body measurements: locality not stated (Napier 1981) WT: DR Congo (Gautier-Hion et al. 1999) Key References

Maisels & Gautier-Hion 1994; McGraw 1994. Annie Gautier-Hion

Cercopithecus pogonias CROWNED MONKEY Fr. Cercopithèque couronné; Ger. Kronenmeerkatze Cercopithecus pogonias Bennett, 1833. Proc. Zool. Soc. Lond. 1833: 67. Fernando Po (=Bioko I.), Equatorial Guinea.

Taxonomy Polytypic species in the Cercopithecus (mona) Group (or Superspecies). Some authorities include wolfi as a subspecies within C. pogonias (e.g. Grubb et al. 2003). Based on analyses of chromosomes (Dutrillaux et al. 1988b), proteins (Ruvolo 1988) and vocalizations (Gautier 1988) the two species are, indeed, phylogenetically close together. This profile follows Groves (2001, 2005c) in recognizing the subspecies: Golden-bellied Crowned Monkey C. p. pogonias, Black-footed Crowned Monkey C. p. nigripes and Gray’s Crowned Monkey C. p. grayi. A fourth subspecies, Schwarz’s Crowned Monkey C. p. schwarzianus from Mayumbe, DR Congo, was put in synonymy by Napier (1981) but is recognized by Groves (2001, 2005c). This profile follows Grubb et al. (2003) in leaving poorlyknown C. p. schwarzianus in synonymy. Synonyms: erxlebeni, grayi, nigripes, pallidus, petronellae, schwarzi, schwarzianus. Chromosome number: 2n = 72 (Dutrillaux et al. 1988b).

Crowned Monkey Cercopithecus pogonias adult male.

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Gray’s Crowned Monkey Cercopithecus pogonias grayi adult male.

Description Arboreal, long-tailed, medium-sized monkey with three broad black stripes on crown and prominent ear-tufts. Sexes similar in colour but adult ! smaller, weighing ca. 65–75% as much as adult ". Facial skin bluish or grey with pinkish eyelids and muzzle. Broad black central crest on crown and broad black stripes on temples separated by white or yellow patches. Ear-tufts prominent and pointed, orange-yellow or whitish. Black or grey ridge down middle of back. ‘Saddle’ on lower back black or dark red. Sides grizzled khaki to grey-olive. Outer arms black or blackish. Outer parts of lower hindlimbs yellowish or buffy-grey. Underside and inner sides of limbs whitish, yellow or orange. Toes black. Tail dorsum black, at least distally; tail ventrum pale yellowish-grey to orange. Geographic Variation C. p. pogonias Golden-bellied Crowned Monkey. Bioko I. (former Fernando Po), Equatorial Guinea, and the adjacent mainland between Cross R., Nigeria and Sanaga R., Cameroon. On Bioko I., limited to the southern ca. 25% of the island and to the lower southern slope of Pico Basilé (Butynski & Koster 1994, Hearn et al. 2006). Gautier-Hion et al. (1999) believe it possible that the Cameroon form may be an undescribed subspecies. Crown and nape dark grey with yellowish speckling; has least brightly coloured crest. Cheeks yellowish, lightly speckled with agouti near ear. Ear-tufts orange to red. Saddle black, sharply defined with variably tinted agouti on flanks. Underside and inner sides of limbs yellow to orange. On Bioko, underside of adult "" is darker orange than in adult !! (T. Butynski pers. comm.). Outer lower hindlimbs yellowish-agouti. Hands and feet black. Black on outer surfaces of forelimbs extends up to elbow or higher. Tail as above. C. p. nigripes Black-footed Crowned Monkey. Endemic to Gabon from south of Ogooué R. southwards to perhaps the Kouilou R. (Gautier-Hion et al. 1999). Crown and nape dark grey with yellowish speckling; has strongly contrasting crest but frontal part of crest pale with central crown dark only on distal part. Cheeks

Cercopithecus pogonias

yellowish, lightly speckled with agouti. Ear-tufts yellow or orange. Saddle black, sharply defined with variably tinted agouti on flanks. Underside and inner sides of limbs orange. Outer lower hindlimbs buffy-grey agouti. Hands and feet black. Tail dorsum orange. C. p. grayi Gray’s Crowned Monkey. Sangha Basin of SE Cameroon, S Central African Republic and Congo, eastward to north of Itimbiri R., NC DR Congo, southwards to north bank of Congo R. to Cabinda (Gautier-Hion et al. 1999). Crown and nape dark chestnut-red with yellowish speckling; well-defined crest with dark central stripe extending onto brow. Cheeks yellowish, lightly and partially speckled with agouti. Ear-tufts whitish or pale yellow. Saddle dark red blending with orange-tinted agouti on flanks. Underside and inner sides of limbs orange to yellow. Outer lower hindlimbs and feet buffy-grey agouti. Only toes of feet black. Tail dorsum yellowish-grey. A large zone of hybridization between the three subspecies may exist in the Atlantic coastal basin between Sanaga R. and Ivindo R., along the upstream tributaries of the Congo R. (see map p. 37 in GautierHion et al. 1999). Similar Species No sympatric monkeys are likely to be confused with this species. Distribution Rainforest BZ. Endemic to western central Africa from Cross R. south to Congo R. On Bioko I., otherwise limited by the Atlantic Ocean on the west and extending eastwards to north bank of Itimbiri R. (Gautier-Hion et al. 1999). See details of distribution in Geographic Variation. Habitat Preferentially inhabits mature lowland rainforests with tall trees and clear understorey. Also in inundated forests and old secondary forests. Avoids young secondary forests with dense understorey (Gautier-Hion et al. 1983, Butynski & Koster 1994).

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Foraging and Food Omnivorous. Fruit and seeds dominate the diet (60–87% depending on the site). Relative amount of seeds, taken from immature fleshy fruit, dry pods or fruit with wind dispersed seeds, varies from 3% (NE Gabon; Gautier-Hion 1980) to 50% in a forest dominated by Leguminosae (Forêt des Abeilles; Brugière et al. 2002). At both sites, arils may account for up to 50% of fleshy pulp ingested. Leaves and flowers make up about 15–17% of diets. In NE Gabon, 67 fruit species in the diet; mostly from tall trees and lianas belonging to three families: Annonaceae, Apocynaceae and Euphorbiaceae. Throughout the year, fruit of the liana Cissus dinklagei (Vitaceae) was the most consumed item. During the period of fruit Lateral view of skull of Crowned Monkey Cercopithecus pogonias adult male. scarcity, arils of Myristicaceae (Coelocaryon and Pycnanthus) are the staple plant food (the same was observed at Lopé Reserve; Tutin et Rarely encountered in gallery forests and never seen in small forest al. 1997a). At Forêt des Abeilles, seeds and leaves of Caesalpiniaceae fragments that extend into savanna (Tutin et al. 1997b). Not reported contribute 52% to the annual plant diet and Burseraceae contribute to be crop-raider. Altitude range is from sea level to 1200 m (south 12%. During the period of fruit scarcity, pulp and seeds of drupes of Bioko I.; Butynski & Koster 1994). Mean annual rainfall ranges several species of Dialium may account for 75% of monthly feeding from1500 mm on the mainland to 10,000 mm on south Bioko I. scores. However, the fruiting of these species is irregular from year to year, so they cannot be considered a true keystone resource. Animal Abundance Biomass is 9–11 kg/km2 in C Gabon (Forêt des prey makes up 6–16% of the diet of C. pogonias and includes mainly Abeilles and Lopé Reserve; White 1994, Brugière et al. 2002), orthoptera and caterpillars, and to a lesser extent ants, cocoons, 60 kg/km2 in NE Gabon, and 115 kg/km2 in Ngotto Forest, spiders, insect larvae, moths and butterflies. Compared to sympatric Central African Republic (Gautier-Hion & Gautier 1974, Gautier- Putty-nosed Monkey Cercopithecus nictitans and Moustached Monkey Hion 1996). Density is 4–48 ind/km2. Minimal density occurs at Cercopithecus cephus, C. pogonias has the least seasonal variation in diet the forest-savanna ecotone (Tutin et al. 1997b). In Ngotto Forest C. and the least dietary difference between !! and "" (Gautierpogonias has the lowest density and biomass of the arboreal guenons. Hion 1980). Encounter rates of 0.04 groups/km of transect on Bioko I. during Cercopithecus pogonias forage in groups or in polyspecific an island-wide survey in 1986 (373 km of census; Butynski & Koster associations. Home-range size varies from 55 to 148 ha depending 1994). Encounter rate of 0.34 groups/km in 2008 along 44 km of partly on whether alone or in a polyspecific association. Monospecific transect in the Gran Caldera de Luba, and 0.56 groups/km in 2009 C. pogonias groups rarely occur and they have the smallest homealong 48 km of transect and 0.52 groups/km in 2010 along 50 km ranges. One group of 18 individuals (followed for 900 h) associated of transect at Badja North, south-west Bioko (T. Butynski, G. Hearn, all the time with a C. nictitans group of 20 individuals and ranged M. Kelly & J. Owens pers. comm.). The Gran Caldera de Luba and over 148 ha. When both groups associated with a C. cephus group of Badja North are remote sites where hunting is relatively uncommon 15 individuals (42% of the time), home-range declined to 119 ha; and where there are no other anthropogenic impacts. As such, the home-range size appears to depend on which species are involved, encounter rates at these two sites are likely close to what is expected not on the size of the association. Mean day range of C. pogonias for an undisturbed population of C. pogonias. monospecific groups estimated at 1600 m. Mean day range of C. Of 108 groups of monkeys encountered on Bioko during the pogonias when associated with C. nictitans was 1825 m and increased island-wide survey in 1986, 15 (14%) were C. pogonias (Butynski & to 1980 m when C. cephus was present (Gautier-Hion & Gautier 1974, Koster 1994). During a 2008 survey in the Gran Caldera de Luba, Gautier-Hion et al. 1983). Cercopithecus pogonias strongly favour upper south-west Bioko, C. pogonias accounted for 24% of the 62 groups strata (20–25 m with >50% of observations over 20 m); descending of monkeys (six species) encountered. At Badja North, south-west occasionally to 200 m (T. Butynski pers. be present in some groups as indicated by their loud ‘barks’ that comm.). An ‘arched’ posture, accompanied by ‘pouting’, is common accompany the boom sequences of the group adult " (A. Gautierin receptive !!.Tail-twining postures are common in resting groups Hion pers. obs.). (Gautier & Gautier-Hion 1977). They also perform a ritualized head On Bioko I. the group adult " typically gives ‘booms’ in series display (Kingdon 1997). of twos (43% of the time) or threes (51%), but sometimes once 337

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(4%) or four times (2%) (n = 51 series). The interval between booms given in a series is usually 5–7 sec (range 4–9). When a series of three booms is given, the time interval between the first and second booms is ca. 1–2 sec shorter than between the second and third booms. Adult !!, subadults, and probably juveniles, give soft ‘honk’ and (louder) ‘myaow’ contact calls. Myaows can be heard to >200 m. Adult !!, by giving a chorus of ‘strained honks’, are able to elicit booms from the group’s adult "". This is reminincent of when adult !! Gentle Monkeys Cercopithecus mitis give a chorus of ‘strained grunts’ that elicits a single boom from the adult "". On Bioko, adult "" frequently give loud, sharp two or three syllable hacks (‘padunk’ and ‘padunkaka’). These calls vary greatly in volume and often grade into ‘hack-trains’ (similar to the ‘ka-trains’ of adult " C. mitis). Hacks can be heard to >200 m and are given in the context of alarm/warning. Adult "" Red-eared Monkey Cercopithecus erythrotis sometimes give ‘hacks’ (which are shorter than those of C. pogonias) in response to the hack call of C. pogonias. Calls similar to the ‘trill’, ‘grunt’ and ‘chirp’ of the sympatric C. erythrotis and other species in the C. (cephus) Group are not given by C. pogonias (T. Butynski pers. comm.). No all-male groups observed. Solitary adult "" are less frequent than in other arboreal guenons, partly because they associate easily with groups of other species. Group cohesion is maintained by the modulated ‘myaow’ exchanged among adult !! and immature animals. Territorial conflicts occur. When two groups come in contact, adult "" exchange aggressive ‘hacks’ until they space out again after which one " in each group gives boom calls. No overlap between home-ranges described. Infants carried only by the mother (Gautier-Hion & Gautier 1976). Cercopithecus pogonias is rarely in monospecific groups: 0–15% of encounters in Central African Republic (Fay 1988, Gautier-Hion 1996), less than 5% both at Lopé Reserve (Ham 1994) and Forêt des Abeilles (A. Gautier-Hion pers. obs.) and 20% in NE Gabon. Occurs most often in bi-specific groups with C. nictitans or Greycheeked Mangabey Lophocebus albigena, and in tri-specific groups with C. nictitans and/or C. cephus, and/or L. albigena. Bi-specific groups with C. cephus are rare, the latter species being found with C. pogonias in the presence of at least a third species. Both at Lopé Reserve and Forêt des Abeilles, the association between C. pogonias and L. albigena accounted for at least 55% of all observed associations. Some groups may include up to six species (Gautier & Gautier-Hion 1969). Contrary to bi- or tri-specific groups, which may be stable over years (Gautier-Hion et al. 1983), associations including more than four species are temporary. Lone C. pogonias adult "" may associate with L. albigena groups (Ham 1994) or with Black Colobus Colobus satanas groups (Fleury & Gautier-Hion 1997). A lone C. pogonias was regularly observed within a group of C. satanas for three years. Cercopithecus pogonias is particularly adept at catching the more mobile of insects that have been flushed by other species, one benefit that they apparently obtain by associating with other primates. This species, which is often high in the canopy, is more alert to aerial predators than other monkeys, and the first to give alarm calls (Gautier & Gautier-Hion 1983). Male C. pogonias are the first to give loud-calls, thereby providing a vocal control in the formation and disbanding of mixed groups. This also serves to coordinate movements and spacing among groups, suggesting a supraspecific organization in which C. pogonias plays a leading role.

When the association includes L. albigena, this species may lead the mixed group (Ham 1994). On Bioko I., C. pogonias forms associations with C. nictitans, C. erythrotis and Pennant’s Red Colobus Procolobus pennantii (Butynski & Koster 1994, T. Butynski pers. comm.). Cercopithecus pogonias has a graded vocal repertoire that is comprised of at least nine calls (see above in this section). Low-pitched cohesion calls and high-pitched contact calls are both non-quavered.These two call types may be associated or even merged. High-pitched warning calls are given by !! and immatures (Gautier 1988). Reproduction and Population Structure Like the majority of guenons, C. pogonias has a mating season centred on the main dry season (Jul–Aug) and a birth season centred on the short dry season (Dec–Feb; Butynski 1988). Gestation ca. 5.5 months. The single newborn weighs ca. 300 g. In captive animals the onset of " puberty occurs at about six years following a large increase in body weight. However, social maturity and especially a male’s ability to give boom calls depend not only on age but both may be inhibited by the presence of a calling leader " within the captive group. In !! sexual maturity is reached around four years (Gautier-Hion & Gautier 1976). Ratio of "" to !! is 1 : 2.8, and adults to immatures 1 : 1.5 (n = 11; Maisels 1995). Predators, Parasites and Diseases Crowned Monnkeys are highly vigilant towards the African Crowned Eagle Stephanoaetus coronatus (observed to kill a juvenile ! in Ngotto Forest; A. GautierHion pers. obs.). Upon sensing a predator, adult "" often stay in the tree canopy and bark.Warning calls by !! follow.Then !! and immatures may plunge into the understorey. Other likely predators are Leopards Panthera pardus (Henschel et al. 2005) and large snakes. Humans are the primary predator throughout the range. Conservation IUCN Category (2012): Least Concern as a species, but C. p. pogonias is Vulnerable. CITES (2012): Appendix II. Like other arboreal monkeys, C. pogonias is vulnerable to hunting by humans for the commercial bushmeat trade over much of its range. Despite their vigilance, C. pogonias constituted ca. 15% of 397 arboreal guenons and mangabeys killed for bushmeat in Cameroon (P. Auzel pers. comm.). On Bioko I. (2017 km²), during 2005, about 320 C. p. pogonias carcasses were brought to the main bushmeat market in Malabo. Hunting with shotguns is the only threat to C. p. pogonias on Bioko, but this activity may extirpate this species from the island. The total number of C. p. pogonias killed on Bioko I. during 2005 for the bushmeat trade was ca. 720. The price paid per carcass in 2005 was ca. US$27. It is unlikely that there were >5000 C. p. pogonias on Bioko I. in 2005 (Hearn et al. 2006). Forest clearance also threatens this species, which prefers tall primary forest. Protection of the population in the Gran Caldera & Southern Highlands Scientific Reserve (510 km²) on south Bioko is critical to the longterm conservation of this monkey on Bioko (Hearn et al. 2006). Measurements Cercopithecus pogonias Cercopithecus pogonias (subsp. ?) HB (""): 540 (520–550) mm, n = 5 HB (!!): 440 (440–480) mm, n = 5 T (""): 820 (750–870) mm, n = 5

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T (!!): 724 (710–740) mm, n = 5 Localities not given (Napier 1981) Cercopithecus p. nigripes WT (""): 4.4 (3.3–4.5) kg, n = 6 WT (!!): 2.9 (2.4–3.2) kg, n = 10 Makokou area, NE Gabon (Gautier-Hion et al. 1999) Cercopithecus p. pogonias HB (""): 407 (370–480) mm, n = 46 HB (!!): 372 (340–410) mm, n = 40 T (""): 624 (560–730) mm, n = 47 T (!!): 557 (480–610) mm, n = 42 HF (""): 124 (118–140) mm, n = 47 HF (!!): 114 (110–120) mm, n = 41

E (""): 27 (22–30) mm, n = 47 E (!!): 26 (22–30) mm, n = 41 WT (""): 3.7 (3.0–5.1) kg, n = 45 WT (!!): 2.8 (2.2–3.8) kg, n = 39 Upper canine (""): 14 (10–20) mm, n = 48 Upper canine (!!): 10 (7–14) mm, n = 32 Lower canine (""): 10 (6–13) mm, n = 48 Lower canine (!!): 7 (4–12) mm, n = 33 Bioko I., Equatorial Guinea (Butynski et al. 2009) Key References Gautier & Gautier-Hion 1983; Gautier-Hion 1980; Gautier-Hion et al. 1983; Tutin et al. 1997b. Annie Gautier-Hion

Cercopithecus hamlyni OWL-FACED MONKEY (HAMLYN’S MONKEY) Fr. Cercopithèque à tête de hibou; Ger. Eulenkopfmeerkatze Cercopithecus hamlyni Pocock, 1907. Ann. Mag. Nat. Hist. ser. 7, 20: 521. Ituri Forest, DR Congo.

while in some of the younger individuals the white nose-stripe was not clear. On the other hand, the white nose-stripe is variably present and often reduced in lowland populations of C. hamlyni in the Ituri Forest and South Kivu (Itebero and Shabunda regions, DR Congo; J. Hart, J. Mwanga & P. Kaleme pers. obs.). Described on the basis of three immature animals, and on characters that are variably present in immature C. h. hamlyni, it is not clear that C. h. kahuziensis is a valid subspecies. While we are doubtful of the validity of C. h. kahuziensis, we provisionally accept this subspecies – pending further study. Rahm (1970) speculated that highland forms have longer tails than lowland forms, and may be separated on this basis, but makes no mention of the nose-stripe or other features. In addition to the lack of a white nasal stripe, C. h. kahuziensis may have a darker face and a reduced diadem (photo in Rahm & Christiaensen 1963: 24). Concerning relative tail length and variation in the colour of the dorsum, Colyn (1988: 115) says: Owl-faced Monkey Cercopithecus hamlyni adult male.

Taxonomy Polytypic species.Two subspecies recognized by Colyn & Rahm (1987), Kingdon (1997), Gautier-Hion et al. (1999), Groves (2001, 2005c) and Grubb et al. (2003): the nominate lowland form C. h. hamlyni and a montane subspecies C. h. kahuziensis (Colyn & Rahm 1987). Cercopithecus h. kahuziensis described from one juvenile and two subadult specimens collected in 1959, and reputedly restricted to a small area of bamboo forest in the Kahuzi-Biega N. P., DR Congo. Field studies over the past two decades in Kahuzi-Biega N. P., however, cast doubt on the validity of C. h. kahuziensis. All C. hamlyni observed on primate surveys in the Kahuzi-Biega N. P., in areas within the reported range of C. h. kahuziensis (Colyn & Rahm 1987), had prominent white nose-stripes, the primary diagnostic character for C. h. hamlyni; no individuals without white nose-stripes were observed (J. Hall, J. Hart, P. Kaleme & B. Finch pers. obs.). Similarly, during eight encounters with three groups at 2100–2400 m in Kahuzi-Biega N. P., Maruhashi et al. (1989) found that all adults had white nose-stripes,

Rahm (1970) emphasizes the difference in relative length of head-body and tail existing between the mountain forest (Kivu Ridge) and the lowland forest populations.This character, however, has no taxonomic importance, as similar differences were found in a single population around Kisangani, DR Congo; the same applies to the differences in mantle colour, which range from greenish to dull yellow-buff, some times tinged with orange.

Cercopithecus hamlyni is most closely related to the recently discovered Lesula C. lomamiensis (Hart et al. 2012; see this volume p. 17). Otherwise, not closely related to any other species, as borne out by the unique structure of the skull (Raven & Hill 1942, Hill 1966). Blood protein analyses (Ruvolo 1988) place C. hamlyni close to L’Hoest’s Monkey Allochrocebus lhoesti, as do similarities in palatine bone shape, coat colour and texture, external nose hair distribution, molar cusp relief, and genital colour and morphology (Schwarz 1928b, Groves 2000a, E. E. Sarmiento pers. obs.), but their karyotypes differ (2n = 64 for C. hamlyni and 2n = 60 for A. lhoesti; Romagno 339

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2001) and molecular data do not support a close relationship (Hart et al. 2012). Similarities between De Brazza’s Monkey Cercopithecus neglectus and C. hamlyni in most of their (relatively few) vocalizations (Gautier 1988), ritualized scent-marking behaviours (Loireau & Gautier-Hion 1988), and natal coat colour and age-related changes in coat colour (Hill 1966), suggest that C. neglectus is relatively close to C. hamlyni. These similarities, however, are probably all characteristic of the primitive Cercopithecini condition and do not reflect a uniquely shared relationship between the two. They more likely reflect conservative evolution in these two lineages since their divergence from the ancestral Cercopithecini stock. Synonyms: aurora, kahuziensis. Chromosome number: 2n = 64 (Romagno 2001, Moulin et al. 2008). Description Medium-sized, semi-terrestrial, stocky, largeheaded, grizzled olive-grey monkey, with conspicuous white nosestripe in nominate race. Sexes alike in colour but adult ! ca. 64% as heavy as adult ". Muzzle relatively heavy and prolonged with contrasting white stripe running along midline from crown, down nose to upper lip. De-pigmented pink skin underlying white hair stripe continues onto glabrous portions of upper and lower lip midline giving the appearance that the stripe crosses mouth. Whitestripe absent in C. h. kahuziensis and variably absent in juveniles and adult C. h. hamlyni. Face skin dark brown in C. h. hamlyni, covered with tiny dark brown hairs interspersed with white hairs on upper and lower lip. Face entirely black in C. h. kahuziensis, except for interspersed white hairs in orbits around eyes and on chin. Neck, throat, chin and cheeks of C. h. hamlyni with black tipped, tan hairs banded pale yellow. This results in an olive hue that progressively lightens from crown to throat. Wider white or pale yellow bands on the hairs of the crown result in a pale yellow or white diadem that, together with the nose-stripe, forms a characteristic ‘T’ that demarcates the face. Brow of C. h. kahuziensis indistinct (no diadem), not demarcated from cheeks or crown. Wide white or pale yellow bands on hair surrounding face result in a lighter olive hue than is typical of C. h. hamlyni. Iris brown or brick red. Crown hairs long, soft and continuous with bushy cheek whiskers extending to ears to form a smooth, compact, ‘hood’ over crown, cheeks and throat, completely hiding the ears. Hood gives animals a distinctive, largeheaded, ‘owl-like’ appearance. Ears largely bare with no tuft. Nape and upper back greyer than crown; hairs silver at base usually with three alternating pale yellow and black bands ending in a white tip (n = 19; E. E. Sarmiento pers. obs.). Lower back, flanks and rump hairs may have as many as four to five alternating bands (Hill 1966, Groves 2001, E. E. Sarmiento pers. obs.). Dorsum and flanks yellowish-grey or olive-grey, becoming paler towards base of tail. Variably darker yellow or orange banding on hairs of dorsum may produce a yellow or orange tinged mantle. Dorsum of C. h. kahuziensis with a more olive-green hue than typical of C. h. hamlyini. Outer thigh has white tipped grey/brown hairs with a single wide black band and narrow yellow band, producing a darker grey hue than on dorsum. Upper limbs, hands, inner thighs, legs and feet black or dark brown. Proximal two-thirds of tail with silver-green hue produced by whitetipped black or dark grey hairs with no banding. Distal third of tail black with slight tuft at tip. Tail slightly longer than HB. Ventrum, black or dark brown. Pelage of ventrum not as thick as on dorsum. Callosities blackish-brown. Scrotum, perineum and lower abdomen of " a striking aquamarine or malachite green.

Lateral view of skull of Owl-faced Monkey Cercopithecus hamlyni adult male.

Newborn lacks facial pattern and is uniformly light yellowishbrown with a paler (fawn) face (photo in Hill 1966: 513). Young juvenile (four months of age) differs both from infant and adult by having brighter colours and more golden-yellow on the face, throat, sides of neck and upper chest; medium yellow over the lower back, limbs, hands and feet. Tail mostly greenish-yellow proximally and greyish-black distally (Hill 1966). Juveniles that are half adult size, and that are still carried by mothers, have adult markings and pelage colour (see photos in Schouteden 1944a: 50–51). M1 erupts when juvenile about half adult size. Geographic Variation C. h. hamlyni Nose-stripe Owl-faced Monkey. Found over entire range of C. hamlyni, including the Bamboo Sinarundinaria alpina zone (2000–3000 m) of Mt Kahuzi (Maruhashi et al. 1989). Nose with white stripe from between eyes to mouth. Diadem white. C. h. kahuziensis Mt Kahuzi Owl-faced Monkey. Only known from the bamboo zone and the marshy zone below the bamboo zone (2000–3000 m) on Mt Kahuzi, DR Congo. Type from the vicinity of Musisi Swamp (02° 18´ S, 28° 42´ E) between Mt Kahuzi and Mt Biega (Colyn & Rahm 1987). The montane portion of KahuziBiega N. P. is at 02° 04´ –02° 37´ S, 28° 36´ –28° 46´ E; 2000– 3308 m). No white vertical stripe on face. Similar Species None that is parapatric or sympatric. Similar C. lomamiensis is separated from C. hamlyni by two major rivers, the Lualaba R. and the Lomami R. (Hart et al. 2012). See map on p. 341 and illustration on p. 344. Distribution Endemic to CE DR Congo and W Rwanda. Rainforest BZ. Geographic range not well known, but range east of Congo R. similar to that of A. lhoesti. Present in the Lindi River Basin in the north-west, Nepoko R. in the Okapi Faunal Reserve in the north (J. Hart pers. obs.), southward through Ituri Forest and along right bank of Lualaba R. to at least 50 km south of confluence with the Elila R. (A. Vosper & J. Hart pers. obs.). Eastward to the Albertine (Western) Rift Valley to within ca. 70 km south of L. Albert in the north and to the north end of L. Tanganyika in the south. Several isolated, outlying populations in extreme E DR Congo and in W Rwanda. Extent of occurrence roughly 193,000 km², but area of occupancy much less than this (Y. de Jong & T. Butynski pers. obs.). The following are the known range limits for C.hamlyni (Schouteden 1944a, Rahm 1965, 1970, Colyn 1988, Dowsett & Dowsett-Lemaire 1990, J. Hart pers. obs.). All sites are in DR Congo unless otherwise indicated. Western limit: ca. 25° 10´ E to north of Congo R. near

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& E. E. Sarmiento pers. obs.). If this is a valid record, C. hamlyni has been extirpated from Uganda. Locations where museum specimens were collected, but where the species is now apparently extirpated, include the Virunga Mts and several sites in NW Rwanda (e.g. Gishwati Forest and Gisenyi Bamboo Forest; A. Plumptre pers. comm.). All sites were greatly reduced in size during the twentieth century. The most recent record for C. hamlyni in this region is for Gishwati Forest in 1989 (J. Ray pers. comm.).

Cercopithecus (hamlyni) Group

Kisangani, and to ca. 24° 14´ E to south along Lualaba R. Northern limit: ca. 02° 24´ N, just south of Nepoko R. North-eastern and eastern limit: ca. 01° 57´ N, 30° 01´ E at Mongbwalu (Kilo Mines). Limit of contiguous moist forest and great lakes of Albertine Rift Valley are the apparent barriers to the north-east and east. Recently recorded for Semliki Forest in the Virunga N. P. (Nixon & Lusenge 2008). Southern limit: ca. 05° 20´ S at Butondo (ca. 80 km north of Nyunzu). Limit of moist forest and/or the Lukuga R. the apparent barriers. Butondo (05° 20´ S, 27° 52´ E) and Nyombe (03° 53´ S, 27° 25´ E) are both isolated forests far south of the main distribution for C. hamlyni. At least one specimen collected at each of these two sites. South-western limit: ca. 03° 05´ S, 25° 58´ E, about 16 km south of Kindu. Southeastern limit: ca. 02° 47´ S, 29° 27´ E in Nyungwe N. P., SW Rwanda. Important, but isolated, populations present in upland sector of Kahuzi-Biega N. P. (Hall et al. 2003), Mt Tshiaberimu in the Virunga N. P. (Sarmiento & Butynski 1997), and Nyungwe N. P. (ca. 02° 36´– 02° 48´ S, 29° 12´–29° 29´ E; Dowsett & Dowsett-Lemaire 1990, Ntare et al. 2006, Easton et al. 2011, N. Barakabuye, A. Vedder & A. Plumptre pers. comm.). The south-eastern limit is in Nyungwe N. P. at 02° 47´ S, 29° 29´ E. Although there are no reports of C. hamlyni in Burundi, this species may well occur there in the bamboo zone of the Kibira N. P., which is contiguous with the bamboo zone at Nchili in Nyungwe N. P. where C. hamlyni is present (A.Vedder, N. Barakabuye & B. Kaplin pers. comm.). Rahm (1970) says C. hamlyni present in ‘bamboo forest near Kabale (Uganda)’. His locality map indicates that what he is referring to is the Echuya F. R., a now isolated bamboo forest centred on 01° 17´ S, 29° 49´ E. This is apparently the only reference for C. hamlyni in Uganda. Rahm (1970) does not indicate the basis for this locality record. There is no museum specimen from any site in Uganda (E. Sarmiento & T. Butynski pers. obs.). While Echuya F. R. (34 km², 2270–2570 m) appears to be suitable habitat for C. hamlyni (as was once much of extreme SW Uganda), C. hamlyni is almost certainly not present there today (T. Butynski

Habitat In lowland, montane and bamboo forest (J. Hart, J. Hall & P. Kaleme pers. obs.). The lowest altitude record is 450 m (east of Kisangani). The nominate race occurs in various types of evergreen forest, from ca. 450 m (Yamagiwa et al. 1989, Hall et al. 2003) in lowland forest and older secondary forest through submontane, montane and bamboo forest to ca. 3000 m. The highest sites are Nyungwe Forest N. P., Kahuzi-Biega N. P. and Mt Tshiaberimu (Rahm & Christeaensen, 1963, Rahm 1965, 1966, Dowsett & DowsettLemaire 1990, Sarmiento & Butynski 1997). In Nyungwe N. P. (970 km²) C. hamlyni restricted to 2260–2570 m within bamboo forest (Dowsett & Dowsett-Lemaire 1990, A. Vedder pers. comm., N. Ntare pers. comm.), even though there is a large area of montane forest here. There is an extraordinary record of a mummified head found in 1927 at ca. 4500 m on Mt Karisimbi,Virunga Mts, Rwanda–DR Congo border (Raven & Hill 1942). This is the only record for the Virunga Mts. Whether this animal was a ‘wanderer’ that reached this altitude on its own accord, or whether the head was carried there by another species (e.g. White-necked Raven Corvus albicollis) is a matter for speculation. In Ituri Forest (ca. 740–1100 m) and in relatively low altitude forests in Kivu District (down to 600 m), C. hamlyni is present in the extensive monodominant stands of Gilbertiodendron dewevrei, as well as in mixed canopy moist forests (Hart & Bengana 1996, Hall et al. 2003). Cercopithecus hamlyni appears to be restricted to terra firma forests. Except for the museum specimen that represents the southernmost location (at Butondo), there is no evidence that C. hamlyni ranges into the forest savanna mosaic. Cercopithecus h. kahuziensis reported only from the bamboo zone and marshy zone below the bamboo zone (2000– 3000 m) on Mt Kahuzi. Mean annual rainfall over the geographic range of C. hamlyni ca. 1200–2500 mm (perhaps 3000 mm at 3000 m asl at Kahuzi-Biega N. P.; Inogwabini et al. 2000). Night-time temperature sometimes 400 primate specimens from Kisangani through the Ituri Forest from 1909–1915, never encountered a live C. hamlyni, although they did purchase dead specimens (Allen 1925). Density in central Ituri Forest estimated at 0.1 ind/km2 (Thomas 1991). Based on frequency of dawn call, C. hamlyni is widespread and common in the Okapi Faunal Reserve, where the dawn call was heard at least once during 40% of 115, 30-minute ‘dawn call point counts’. Cercopithecus hamlyni especially prevelant in monodominant Gilbertiodendron forests in the Epulu area, central Ituri Forest (J. Hart pers. obs.). 341

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Widely distributed and common in Kahuzi-Biega N. P. and the adjoining Kasese region between the Lowa R. and Oku R. Hall et al. (2003) provide the following estimates for C. hamlyni in the KB1 Lowland Sector (700–800 m) of Kahuzi-Biega N. P.: 2.5 groups/km², 6.7 ind/km², 18.4 kg/km² and the following estimates for the KB2 Lowland Sector: 2.0 groups/km², 5.3 ind/km² and 14.7 kg/km². In the Mountain Sector (2000–3308 m) of Kahuzi-Biega N. P., C. hamlyni is also widespread and common, with the ‘boom’ call being heard by primate survey teams on about half of the days, a rate similar to that heard in the lowland sectors (Inogwabini et al. 2000). Encountered rate 0.08 groups/km in Nyungwe N. P. (Easton et al. 2011). Adaptations Semi-terrestrial and diurnal. The impression is that C. hamlyni spends more time on the ground than any other forest guenon (J. Hart pers. obs.). Although C. hamlyni uses all forest strata, a preliminary study in Nyungwe N. P. found that, during the daytime, C. hamlyni spends ca. 61% of time on the ground; ca. 81% of play, 68% of feeding, 64% of travel, 43% of grooming and 47% of resting occurs on ground. About 18% of time spent both at 0–2 m and 2–12 m above ground, with only 3% of time >12 m above ground (N. Ntare pers. comm.). When threatened, C. hamlyni often flees quietly on the ground rather than climbs. Initial reports (e.g. Allen 1925) that C. hamlyni is nocturnal are not supported by field observations (Rahm 1970, J. Hart & J. Hall pers. obs.). The brilliant aquamarine scrotum and perineum of the adult "" is typical of other semi-terrestrial guenons (i.e. C. neglectus, the Mountain Monkeys Group Allocrocebus (preussi), the Savanna Monkeys Group Chlorocebus (aethiops) and Patas Monkey Erythrocebus patas). Cercopithecus hamlyni has a distinctive odour, readily detected when the animals are nearby. Male and ! captives mark their surroundings by rubbing with their chests (Kingdon 1997, D. Messenger pers. comm.), on which there are scent-producing sternal (apocrine) glands.The only other guenons for which ritualized olfactory marking has been observed are C. neglectus, Green Monkey Chlorocebus sabaeus, Vervet Chlorocebus pygerythrus, Allen’s Swamp Monkey Allenopithecus nigroviridis, and a free-living C. pygerythrus × Sykes’s Monkey Cercopithecus mitis hybrid (De Jong & Butynski 2010b). All four of these species (and the hybrid) are semi-terrestrial. The ritualized olfactory marking in C. neglectus is believed to be related to that species’ low development of visual and vocal signalling, small group size, cryptic behaviour and small home-range size (Gartlan & Brain 1968, Gautier & Gautier-Hion 1977, Gautier-Hion & Gautier 1978, Loireau & Gautier-Hion 1988). Like C. neglectus, C. hamlyni is a highly cryptic species with a relatively limited vocal repertoire (Gautier 1988) and small group size. This suggests that C. hamlyni will also be found to have a small visual signal repertoire and small home-ranges relative to other Cercopithecus spp. as well as to Allochrocebus spp. With more colobine-like molars than any other guenon (Hill 1966), C. hamlyni is probably less dependent on fruits than other guenons. As such, C. hamlyni is expected to do well in monodominant forests (e.g. bamboo forest and Gilbertiodendron forests) where the yearround availability of fruit is relatively low and where, concomitantly, competing species (e.g. Stuhlmann’s Blue Monkey Cercopithecus mitis stuhlmanni and A. lhoesti) are absent or at low densities. Kingdon (1997: 78) notes that: ‘The hands of owl-faced monkeys are unique among guenons in the elongation of the phalanges. This is the opposite of a terrestrial trait and, combined with a relatively

Visual suppression of facial expression in the Owl-faced Monkey Cercopithecus hamlyni.

strong thumb, suggest a powerful grip (as would be needed for climbing slippery bamboo stalks).’ Foraging and Food Poorly known. Probably omnivorous. Forages mainly on the ground, often in dense bamboo and herbaceous vegetation (Dowsett & Dowsett-Lemaire 1990, J. Hart & J. Hall pers. obs.). Bamboo Sinarundinaria alpina shoots (leaves) and fruits of Syzygium guineense in stomach of an individual from Mt Kahuzi (Rahm & Christiaensen 1963). Local people at Mt Tshiaberimu state that C. hamlyni feeds largely on fungi and bamboo, and cleanly breaks off young bamboo shoots from the stem base to feed on them. In contrast C. m. stuhlmanni tease apart shoots with hands separating individual leaves from the shoots (E. E. Sarmiento pers. obs.). Removal of individual blades from bamboo shoots also observed for Doggett’s Blue Monkey Cercopithecus mitis doggetti in Nyungwe N. P. (N. Ntare pers. comm.). Main foods during one brief study in Kahuzi-Biega N. P. were the fruits of Macaranga kilimandscharica and Maesa lanceolata (Maruhashi et al. 1989). Eats fruits of Maranthaceae (Rahm 1966). Raids crops (e.g. Maize), but this is not common (Mwanza et al. 1989). In Nyungwe N. P., at least 17 species of plants eaten (Ntare et al. 2006). Items eaten include, piths, stems, leaves, shoots, sheaths, flowers, roots, insects, mushrooms and lichens. During the dry season, Triumfetta cordifolia and Anisosparum humberti consumed. In October, diet dominated by young bamboo shoots; a highly seasonal food only available during the wet season. Diet comprised 36% stems, 36% pith, 10% leaves, and 7% bamboo shoots – which is yet another source of leaves (Ntare et al. 2006). This is a unique diet for an African monkey, with fruit comprising a minor part of the diet. Fruits of M. kilimandscharica, S. guineense and Rubus pinatus eaten (N. Ntare pers. comm.). Fruits are relatively uncommon in bamboo forest. Cercopithecus hamlyni living in mid-altitude and montane forest probably eat much more fruit than those living in bamboo forest. In the lowland and midaltitude monodominant primary forests, however, periods of low fruit availability are prevalent and fruit availability at these times may not be that different from the situation in bamboo forests. In the Epulu area C. hamlyni feeds on the ground on fallen seeds of Erythropleum suaveolens and on the sprouting seeds of G. dewevrei.

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Stomach contents of two animals in the Ituri Forest during a period of low fruit availability only contained fungi. Mbuti pygmies here report that C. hamlyni joins Blue Duikers Phlantomba monticola and other duikers Cephalophus spp. in foraging on the ground under feeding groups of arboreal primates. Observed accompanying Olive Baboons Papio anubis and Robust Chimpanzees Pan troglodytes in south Ituri Forest (J. Hart pers. obs.). An adult C. hamlyni " seen chasing a C. m. doggetti ! out of a fruiting Maesa tree (Maruhashi et al. 1989). Social and Reproductive Behaviour Social. Groups described as small (Dowsett & Dowsett-Lemaire 1990), not exceeding ten individuals (Rahm 1970, Gautier-Hion et al. 1999). Usually encountered in groups of 2–4 individuals, but larger groups also occur (J. Hart & J. Hall pers. obs.). Fourteen observations on the Terrain Scientifique de Lenda (an area of no hunting, 10 km southeast of Epulu), where group size was determined with certainty, included three single animals (twice adult "", once sex not determined), five groups of two animals (" and !, or sex unknown), two groups of three, two groups of four, one group of six (including two adult "" and two !! with young), and one exceptional group of 30–35, including multiple adult "", which was accompanied by one White-bellied Duiker Cephalophus leucogaster (J. Hart pers. obs.). Mean minimum group size for three groups encountered during censuses in the lowland sector of Kahuzi-Biega N. P. was 2.7 individuals (Hall et al. 2003). During eight encounters with three groups at 2100–2400 m in Kahuzi Biega N. P., Maruhashi et al. (1989) judged all three groups to be comprised of at least five individuals, including one adult ". Cercopithecus hamlyni was in association with C. m. doggetti during three of seven group encounters. Solitary adult C. hamlyni "" present here. One study group in Nyungwe N.P. comprised 24 individuals, including two adult "". The two adult "" fought when they met, suggesting that the study occurred during a period when a satellite " was attempting to usurp the harem ". C. hamlyni and C. m. doggetti form polyspecific associations in Nyungwe N. P. (N. Ntare pers. comm.). Ranger-Based Monitoring Patrols in Nyunge N. P. recorded an average of 5.3 individuals/encounter (n = 78 groups), but this method is likely to underestimate group size (Easton et al. 2011). Vocalizations include the ‘boom’ loud-call and ‘uh-uh-uh’ or ‘tyotyo-tyo’ alarm call of the adult ". The boom may be given once, or more than once, with a brief pause in between. Other calls include the ‘pitiak’ alarm call, and the ‘moan’ or ‘oooh-oooh’ contact call (Gautier 1988, Gautier-Hion et al. 1999, N. Ntare pers. comm.). A distinctive ‘barking’ call (‘krot, krot, kro-krot …’) described from Nyungwe Forest N. P. (Dowsett & Dowsett-Lemaire 1990). The loud, high-pitched warning ‘chirps’ of most guenons is given by infant C. hamlyni but is not part of the vocal repertoire of older animals (Kingdon 1997). In the Ituri Forest and Kahuzi–Biega lowlands, the distinctive descending boom call is usually uttered for a brief period before dawn. Hall et al. (2003) and Hart & Bengana (1996) used the boom call to determine the presence and relative abundance of C. hamlyni on wide-ranging surveys. However, if the boom call is not known, the presence of this species can easily be overlooked.

Diverse modelling of hair on the crowns of Owl-faced Monkeys Cercopithecus hamlyni.

Cercopithecus hamlyni is often described as being a discrete and quiet monkey that is relatively difficult to detect and observe. When encountered by humans it usually remains quiet, retreating on the ground without giving warning calls (N. Ntare pers. comm., J. Hart & J. Hall pers. obs.). Reproduction and Population Structure Females carrying infants recorded in Ituri Forest in Feb, May and Aug. Birth season in western portion of range (i.e. Kisangani and Kindu) is Jul–Nov based on the size of embryos in 13 collected specimens. As such, births occur during the single annual dry season (Jun–Aug) and well into the subsequent wettest period of the year (Gevaerts 1992). Records from Singapore Zoo show a gestation of 5–6 months. Twins not reported. No birth weights available, but one 3-day-old " infant at Edinburgh Zoo weighed 320 g (G. Catlow pers. comm.). The European Endangered Species Breeding Program (EEP) Studbook indicates the following for C. hamlyni in captivity: gestation = 180 days; youngest ! at first birth = 2.25 years; oldest ! to give birth = 24 years. Captive " lived to >23 years and captive ! lived to >28 years. Predators, Parasites and Diseases Four C. hamlyni captured in net drives on the Terrain Scientifique de Lenda were equipped with radio collars. Within 45 days all had been killed: one by an African Crowned Eagle Stephanoaetus coronatus, and three by Leopards Panthera pardus. The four animals were caught over three 343

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days during a food shortage and unusual drought. They were readily detected as they moved through dry forest litter, and appeared to be in weakened condition, making them relatively easy to capture. Hairs of C. hamlyni found in two (0.9%) of 222 Leopard scats in Ituri Forest (Hart, J. A. et al. 1996). Although no C. hamlyni hairs were found in 60 African Golden Cat Profelis aurata scats examined during this study, P. aurata is a likely predator of C. hamlyni. Robust Chimpanzees and African Rock Pythons Python sebae are probable predators. The most important predator for C. hamlyni is almost certain humans. The semi-terrestrial habit of C. hamlyni makes this species especially susceptible to snares and hunters with dogs. They are more frequently caught in snares set for duikers than any other primate species in the Ituri Forest (J. Hart pers. obs.). No information on diseases and parasites.

HB (""): 460 (430–480) mm, n = 3 T (!!): 570 (500–630) mm, n = 3 T (""): 530 (490–560) mm, n = 3 HF (!): 148 mm, n = 1 HF (""): 133 (120–145) mm, n = 3 E (!): 44 mm, n = 1 E (""): 29 (28–30) mm, n = 3 WT (!!): 5.5 (4.4–7.3) kg, n = 14 WT (""): 3.6 (2.6–4.5) kg, n = 18 GWS (!!): 110, 112 mm, n = 2 GWS (!!): 74, 74 mm, n = 2 Various localities (Hill 1966, Rahm 1966, Gevaerts 1992, GautierHion et al. 1999, P. Kaleme pers. comm., E. Gilissen & W. Wendelen pers. comm., J. Hart pers. obs.)

Conservation IUCN Category (2012): Vulnerable. CITES (2012): Category II. Probably extirpated from Uganda (depending on validity of Rahm’s (1970) record), and restricted in Rwanda to the bamboo zone in Nyungwe N. P. (Easton et al. 2011, R. Dowsett, A. Vedder & A. Plumptre pers. comm.). The population on Mt Tshiaberimu must be very small and, as such, may not be viable. Most important threats are habitat degradation (including the harvesting of bamboo), loss and fragmentation of forest as a result of agricultural expansion, as well as hunting for bushmeat (Mwanza et al. 1989, Inogwabini et al. 2000, Easton et al. 2011). Protected areas important for the longterm survival of C. hamlyni include Okapi Faunal Reserve, Maiko N. P., Kahuzi-Biega N. P. and Nyungwe N. P. Cercopithecus hamlyni is a survivor of a unique primate lineage. None the less, it remains one of Africa’s least studied species of primate. A long-term, detailed, study of the ecology, behaviour and habitat requirements of C. hamlyni would not only be exceedingly interesting and help fill a major gap in African primatology, it would also contribute valuable information towards the conservation of this species.

Key References Easton et al. 2011; Gautier-Hion et al. 1999; Hall et al. 2003; Hill 1966; Rahm 1970; Raven & Hill 1942.

Measurements Cercopithecus hamlyni HB (!!): 540 (510–550) mm, n = 3

Lesula Cercopithecus lomamiensis adult male.

John A. Hart, Thomas M. Butynski, Esteban E. Sarmiento & Yvonne A. de Jong

Cercopithecus (nictitans) GROUP Nictitans Monkeys Group Cercopithecus nictitans (Linnaeus, 1766). Systema Naturae, 12th edn, 1: 40. Benito R., Rio Muni, Equatorial Guinea.

The name Cercopithecus nictitans has two different taxonomic expressions. One restricts the name to a single species, the Puttynosed Monkey. The other, much more complex expression, Cercopithecus (nictitans), refers to a more inclusive taxon, a speciesgroup (or superspecies) that ranges from West Africa to Zanzibar I., and from SW Ethiopia to the southern tip of South Africa. In this appellation, the C. (nictitans) Group, described in 1766, includes both the Putty-nosed Monkey Cercopithecus (nictitans) Subgroup and the Gentle Monkey Cercopithecus (mitis/albogularis) Subgroup (first described in 1822 and 1831, respectively) (Grubb et al. 2003).

While 52 forms have been named within the C. (nictitans) Group, we provisionally recognize 21 forms here. It has been a matter of convention and convenience that the western C. nictitans has been profiled separately from the rest of the C. (nictitans) Group in this and many other works. Three species are frequently recognized: C. (n.) nictitans, Blue Monkey C. (n.) mitis and Sykes’s Monkey C. (n.) albogularis. The boundaries between taxonomic subgroups and sections of all monkeys of the C. (nictitans) Group remain poorly understood (Grubb et al. 2003).There is the strong likelihood that at least a third/fourth species, C. (n.) opisthostictus, should be distinguished as it, like C. (n.) nictitans, has a chromosome count of 2n = 70, whereas all of the other forms

344

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boutourlinii stamflii

nictitans stuhlmanni zammaranoi heymansi mitis

doggetti

albogularis group

opisthostictus moloneyi

labiatus

Schematic distribution of populations in the Cercopithecus (nictitans) Group.

in the C. (nictitans) Group that have so far been assayed have 2n = 72 chromosomes (Dutrillaux et al. 1980). In addition, opisthostictus may be sympatric with moloneyi (Ansell 1958, O. Burnham pers. comm., T. Davenport pers. comm.). Some outlying and geographically separate forms in the C. (nictitans) Group appear to share certain conservative traits. This implies a complex history of population expansions and contractions out of and back into climatically determined enclaves. Recent molecular studies hint at just such complications, reinforcing the recognition that nictitans and albogularis belong to the same complex and are closely related in spite of coming from opposite sides of Africa (Tosi et al. 2005). The latter authors’ use of X chromosomes as an indicator of affinity has also confirmed the relationship of albogularis with mitis. The phylogenetic tree offered here attempts to sketch out one possible sequence of events whereby seven regional clusters might have evolved, but until detailed genetic profiles become available, any phylogenetic tree must be regarded as tentative and provisional. Taking Tosi et al.’s (2005) study of X chromosomes and their associated molecular clock as a guide, this tree supposes the initial spread of a large, relatively unspecialized ancestor across those parts of Africa that were webbed at that time by a network of riverine forests. Molecular clocks are consistent in positioning this spread during a warm spell that preceded the cold, arid period of 3.2–2.8 mya (mid-Pliocene). This prolonged dry period would have fragmented forests and with them early C. (nictitans) populations. The main fracture-lines between forest blocks would have fragmented this lineage, much as they did many other forest lineages (see map of biogeographical sub-regions in Volume I, Chapter 6). Regional subpopulations would have emerged in far Upper Guinea, on both sides of the northern Congo Basin and, divided by the Congo R., on both sides of the southern Congo Basin. Forests watered by moist Indian Ocean winds would have sustained a separate population along the eastern African littoral but these too would have fragmented. Climate has fluctuated many times over the

past 2.8 million years and it is currently impossible to correlate the emergence of specific contemporary populations with particular past climatic events. However, differences among contemporary members of the C. (nictitans) Group encourage the identification of seven ‘deep’ lineages. These are consistent with geography and with the forest refugia listed above. On the eastern side of the south Congo Basin opisthostictus is the most likely candidate for direct descent from the founding lineage. It may be that opisthostictus still lives in the vicinity of, or in a part of, the region in which the ancestors of the C. (nictitans) Group emerged. It has already been pointed out that, with the exception of C. (n.) nictitans, opisthostictus has a smaller number of chromosomes than other members of the C. (nictitans) Group (2n = 70 instead of 2n = 72; Dutrillaux et al. 1982a). (Cercopithecus (n.) heymansi, which most resembles C. (n.) opisthostictus, possibly shares the same count.) Cercopithecus (n.) heymansi occupies what looks like a relict range, sandwiched between two major rivers, with the implication that it belongs to a group that was formerly more widespread. When more is known about primate populations in the Congo Basin the two forms may actually be shown to represent a clinal continuum. Assuming that their primary spread reached the farthermost parts of their present range it seems significant that geographically isolated populations from the extreme west, north-east and south of the range of the C. (nictitans) Group should show striking similarities. Thus C. (n.) n. stamflii, from West Africa, C. (n.) albogularis labiatus from South Africa, C. (n.) albogularis zammaranoi from the Juba R., Somalia, and C. (n.) m. boutourlinii from SW Ethiopia all have white throats and upper chests, dark olive backs, intensely black arms graduating to dark agouti grey on upper shoulders, and dark grey agouti legs. Some further resemblances between these four populations and opisthostictus and heymansi are best explained by retention of conservative genotypes shared by the most isolated populations in their common ancestor’s once extensive range. In spite of their likely genetic heritage, these outliers are commonly assigned to three different species. The isolation of C. (n.) n. stamflii in the west is enough to explain its differentiation from the Eastern Putty-nosed Monkey C. (n.) n. nictitans. On the face of it, the latter should descend from the same nictitans ancestor, yet its close resemblance to C. (n) m. stuhlmanni suggests many complications, including the possibility that the latter genotype has mixed with that of nictitans long after their parental stocks diverged. Should this turn out to be so, C. (n.) n. nictitans would represent a stabilized hybrid, or even, in places, a hybrid swarm. Late genetic crossing might also help explain mixed characteristics in boutourlinii, which combine many opisthostictus-like features with some of those of its nearest neighbour, stuhlmanni. Should boutourlinii be allied with stuhlmanni (as it now is) or are there any ways in which its likely links to an older heritage could find expression? Some of the ancestors of boutourlinii were probably shared with those of zammaranoi at the time of their first entry into north-east Africa. Yet today there are decisive differences in body size, habitat and geographic range. Both forms have continued to evolve adaptations to their localities. Their current taxonomic allocations are certainly artificial and are likely to be changed in the future. The penetration of geographic extremities includes an altitudinal dimension and it is possible that descent from an earlier nictitans may be exemplified in the mountains of the Western Rift Valley by doggetti, 345

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Some monkeys in the Nictitans Monkeys Group Cercopithecus (nictitans) radiation. Top row, left to right: Eastern Putty-nosed Monkey Cercopithecus nictitans nictitans. Angola Pluto Monkey Cercopithecus mitis mitis. Moloney’s Monkey Cercopithecus mitis moloneyi. Stuhlmann’s Blue Monkey Cercopithecus mitis stuhlmanni. Kolb’s Monkey Cercopithecus mitis kolbi. Bottom row, left to right: Martin’s Putty-nosed Monkey Cercopithecus nictitans martini. Lomami River Monkey Cercopithecus mitis heymansi. Rump-spotted Monkey Cercopithecus mitis opisthostictus.Doggett’s Silver Monkey Cercopithecus mitis doggetti. Tanzania Sykes’s Monkey Cercopithecus mitis monoides.

kandti and, farther south, by moloneyi.The isolation of such distinctive types on cool upland suggests that past global glacials encouraged the spread of an appropriately adapted morpho-type and that subsequent climatic changes led to regional differentiation. Thus, doggetti, kandti, moloneyi and possibly another outlying and isolated population, C. (n.) m. mitis (which occurs south of the Congo R. mouth both in upland and low-lying areas of N Angola), might all have a common ancestry and have been connected across the temperate southern African highlands. The exceptionally successful stuhlmanni is predominantly a lowland form but probably represents a late derivative from the same stock as doggetti. Thus there appear to be multiple temporal levels in a slow-growing evolutionary radiation that may well have been strung out over some 3 million years. These are but a few of the phylogenetic questions. As such, it is not surprising that current taxonomic allocations are confused, contradictory, and sometimes arbitrary. Since the C. (nictitans) Group represents one of the most promising exemplars of ‘evolution in action’, these monkeys beg much more study. In the interests of provoking further study of these ecologically and evolutionarily significant monkeys, we list and map the ranges of identifiable regional populations and allocate them, provisionally, to seven regional ‘clusters’ (Kingdon 1997) that have also been called ‘sub-groups’ and ‘sections’ (Grubb 2001, Grubb et al. 2003).We have used established names to tentatively rank each of these clusters and while these imply that each could be regarded as a species in its own right we regard formal recognition at the species level as premature, pending deeper molecular studies. We believe our restraint might help move the study of these interesting monkeys towards a less superficial and more eco-biogeographic and evolutionarily based treatment. The 22 forms listed here are generally recognized as morphologically and geographically distinct. All of the seven proposed clusters embrace more than one subspecies. Cluster I: Cercopithecus opisthostictus Cluster C. (n.) opisthostictus. A highly distinctive form with a different chromosome count from all others in the C. (nictitans) Group

except for C. (n.) nictitans (2n = 70 instead of 2n = 72, Dutrillaux et al. 1982a). Appears to be sympatric without interbreeding in a narrow region of overlap with C. (n.) moloneyi (see below). The dense, light olive to steel-grey agouti pelage of the dorsum is exceptionally soft, resembling that of Owl-faced Monkey Cercopithecus hamlyni and De Brazza’s Monkey Cercopithecus neglectus in colour and texture. Cheek-fur particularly long, hiding the ears and drooping down towards the shoulders. Muzzle, chin and throat off-white. Diadem upwardly arched, ‘sculpted’ and poorly defined in colour, but paler than rest of the crown (which matches colour of dorsum). Arms and underside black. Hindlimbs a darker shade of agouti than dorsum. Muzzle longish in adult ". C. (n.) o. opisthostictus Rump-spotted Monkey. Crown relatively monochromatic agouti. Throat off-white. Face pale. Inhabits forest mosaics, especially ground-water swamp forests, within the moister miombo woodlands of the south-eastern Congo Basin and upper Zambezi Basin to western littoral of L. Tanganyika. In lowlying forests along the southern eastern littoral of L. Tanganyika (T. Davenport pers. comm.). Kasai R. possibly forming western boundary with L. Tanganyika and Muchinga Uplands defining much of eastern limit. C. (n.) o. heymansi Lomami River Monkey. Similar to C. (n.) o. opisthostictus but black band across temples and nape and diadem near-white, narrow. Face black. White on throat less extensive. Crown, neck and shoulders blue-grey. Ventrum lighter than back. Between Lualaba R. and Lomami R., E DR Congo. Some authors allocate heymansi to other clusters (Colyn & Verheyen 1987b, Lawes et al. this volume). Colyn & Verheyen (1987) suggest that heymansi and opisthostictus hybridize near Lusambo, DR Congo, but it is also plausible that there is (or has recently been) a more or less continuous cline between the two forms. The singular distribution pattern of the opisthostictus Cluster implies a formerly more extensive range. If so, displacement to the east could have been due to expansion by C. m. stuhlmanni. To the

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Sanaga R. and Cameroon Highlands, disjointedly, westwards to far western Upper Guinea. Probably the most conservative form within this cluster. Synonyms: insolitus, ludio. Cluster III: Cercopithecus mitis Cluster C. (n.) mitis. Back dark grizzled agouti. Crown with paler diadem. Chin pale. Cheek-whiskers broad. Muzzle longish in adult ". Populations appear to be relictual. C. (n.) m. mitis Angola Pluto Monkey. Diadem very pale. Muzzle with short, white hairs. Crown, neck and limbs black. Dorsal and ventral pelage dark grey to black. Synonyms: diadematus, dilophus, leucampyx, pluto, nigrigenis. W Angola. C. (n.) m. maesi Kutu Pluto Monkey. The validity of this apparently rare form has been challenged and the provenance (Kutu, near the centre of the Congo Basin) of the holotype questioned (Colyn & Verheyen 1987, Groves 2001), but Schouteden (1947) allocated several specimens from west of Lomami R. and south of Congo R. Martin’s Putty-nosed Monkey Cercopithecus nictitans martini adult male. to this subspecies. Whatever taxonomic designation is eventually west, competition from what are now rare forms of the C. (nictitans) arrived at, it is clear that C. (n.) mitis is of sporadic occurrence Group seems unlikely. However, species that are rare today need through the Congo Basin south of the Congo R. and west of not have been rare in the past. Furthermore, if the opistostictus the Lomami R. The occurrence of the C. (n.) mitis form in this Cluster represents an early form of (nictitans), then displacement region needs further study. It should be noted that this heavily by subsequent descendant populations is plausible. With regard to forested region is well separated from both C. (n.) mitis and C. (n.) understanding the dynamics of speciation/sub-speciation in the stuhlmanni (the two forms maesi has been commonly allied with). C. (nictitans) Group, it is important to document details of the Schouteden’s descriptions imply most resemblance with C. (n.) m. relationships of C. (n.) opisthostictus with C. (n.) m. stuhlmanni and C. mitis but with a narrower brow-band, a black temporal streak and (n.) m. doggetti to the north-east and with some form of C. (n.) mitis fine agouti cheek-fur tones that graduate from paler near the face (possibly C. (n.) m. maesi) to the west. to darker on the margins. Cluster II: Cercopithecus nictitans Cluster C. (n.) nictitans. Most strikingly distinguished by its white ‘putty nose’. Back pelage greyish-olive or kaki-olive agouti and relatively coarse (compared with opisthostictus). Arrangement of cheekfur differs between subspecies. Arms black. Hindlimbs a darker shade of agouti than dorsum. Muzzle medium length in adult ". Cercopithecus (n.) nictitans has a lower number of chromosomes (2n = 70) than all other members of the C. (nictitans) Group (2n = 72) with the exception of opisthostictus (2n = 70). Based on protein analyses, the C. nictitans Cluster, the four C. (n.) mitis-like clusters (i.e. mitis, doggetti, moloneyi and stuhlmanni Clusters) and the C. (n.) albogularis Cluster are phylogenetically extremely close. In the eastern parts of the range of C. (n.) nictitans the possibility of long-term hybridization, even replacement of earlier stuhlmanni populations, should be borne in mind. C. (n.) n. nictitans Eastern Putty-nosed Monkey. Back, head and underside warm, greyish-olive. Laterally bunched fur on cheeks. Chest black. Some features of this form may have been influenced by hybridization, possibly on a broad scale, with stuhlmanni. Sanaga R. and Cameroon Highlands eastwards to Congo R. and Itimbiri R. (DR Congo), and southwards to Congo R. C. (n.) n. martini Martin’s Putty-nosed Monkey. Khaki-olive back and head.Throat off-white. Chest and abdomen dusky grey. Restricted to Bioko I., Equatorial Guinea. C. (n.) n. stampflii Stampfli’s Putty-nosed Monkey. Khaki-olive back and head. Cheek-fur downwardly deflected giving face a narrower appearance. Throat, chest, inner surfaces of upper arms and underside with variable amounts of white, cream or light grey.

Cluster IV: Cercopithecus doggetti Cluster C. (n.) doggetti. Back grizzled grey or golden. Crown black with sharply defined diadems. Cheek-whiskers high, well-developed. Muzzle of adult " long. Isolated populations associated with Western Rift Valley of DR Congo, Uganda, Rwanda, Burundi and Tanzania. C. (n.) d. doggetti Doggett’s Silver Monkey. Back grizzled varying from ash-grey to tawny-grey. Arms, hands and feet intense shiny black. Legs dark grey with some agouti on upper thighs. Occurs in both upland and lower-lying forests from western shore of L. Victoria westwards to Bwindi Impenetrable N. P. southwards to northern shore of L. Tanganyika. Synonym: sibatoi. C. (n.) d. kandti Golden Monkey. Cape and base of tail red or orange. Cheeks and diadem with ‘golden’ tints. Crown, arms and tail black.The amount of red varies individually with some individuals scarcely distinguishable from doggetti. Inhabits montane and bamboo forests on Virunga Mts (where Uganda, Rwanda and DR Congo meet). Synonym: insignis. C. (n.) d. schoutedeni Schouteden’s Silver Monkey. An island isolate possibly deriving from hybridization between doggetti and kandti or an example of founder-effect. Idjwi and Shushu Is. in L. Kivu and western Virunga Mts, DR Congo. Diadem very pale agouti. Crown, neck and forelimbs black. Back pale olive-grey. Underside lighter. Cluster V: Cercopithecus moloneyi Cluster C. (n.) moloneyi. Until the ambiguous affinities of these monkeys have been clarified we treat them, provisionally, as a distinct cluster. 347

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Pousargues’s Monkey Cercopithecus mitis albotorquatus adult male. Moloney’s Monkey Cercopithecus mitis moloneyi adult female. BELOW LEFT: Stuhlmann’s Blue Monkey Cercopithecus mitis stuhlmanni adult male. ABOVE:

ABOVE LEFT:

distinguished by red ear-tufts and by red and white hairs under tail. Restricted to Vipya/Nyika plateau and Mt Waller, Malawi.

This cluster has been variously associated with doggetti (Kingdon 1971), albogularis (Groves 2001) and mitis (Kingdon 1997). A flat ‘cap’ and light diadem are conspicuous features and, for all higheraltitude populations, a dark mahogany ‘saddle’. Muzzle of adult " medium length. Restricted to montane areas to north and west of L. Malawi. On the extreme western edges of range may be sympatric with C. (n.) opisthostictus without interbreeding (Ansell 1958, O. Burnham pers. comm., T. Davenport pers. comm.). This separation appears to be facilitated by opisthostictus inhabiting swamp or lower-altitude forests while moloneyi occupies montane forests or narrow riverine strips descending from higher altitudes. May form a phenotypic cline with C. (n.) albogularis monoides in the Udzungwa Mts, SC Tanzania (T. Butynski pers. comm.). C. (n.) m. moloneyi Moloney’s Monkey. Cheek-fur broad, grizzled. Throat pale grey. Dorsum with mahogany saddle. Sides and thighs light grey. Individuals from lower altitudes may have olive dorsum: whether this is due to admixture with C. (n.) albogularis monoides is not known. Arms, hands and feet black. Ventrum of tail sometimes reddish. Widely distributed in the Southern Highlands of Tanzania, from the north shore of L. Malawi westwards along riverine forests draining the Lavusi/Muchinga Highlands and the Luangwa R., Zambia. C. (n.) m. francescae Red-eared White-collared Monkey. Often subsumed as a synonym of moloneyi but regarded as a distinct montane isolate by Ansell (1960). Resembles moloneyi but darker overall and

Cluster VI: Cercopithecus stuhlmanni Cluster C. (n.) stuhlmanni Cheek-whiskers broad. Cheek-whiskers, back, sides and base of tail deep slate-blue agouti. Diadem paler. Crown and arms black. Legs dark blueish-grey agouti. Muzzle relatively short in adult ". Expansive range in E and NE DR Congo and East Africa. Possibly into Ethiopia. C. (n.) s. stuhlmanni Stuhlmann’s Blue Monkey. As above. From east of Itimbiri R. and north of Congo/Lualaba R., DR Congo to Eastern Rift Valley, north of L. Victoria, SW Kenya. Also isolated massifs in N and W Uganda and SE Sudan. Includes neumanni, carruthersi, mauae, elgonis (elgonis is a particularly dark form from the montane forests of Mt Elgon). C. (n.) s. boutourlinii Boutourlini’s Blue Monkey. Crown grizzled (not black). Diadem undifferentiated from crown. Dorsum with greenish or yellowish tinge. Dandelot & Prévost (1972) emphasize similarity with opisthostictus. Genetically, might be allied to a hypothetical class of ‘relictual populations on the extremities’, so the possibility of stuhlmanni and an earlier relict type meeting and hybridizing in Ethiopia should be borne in mind. SW Ethiopia from L. Turkana northwards to L. Tana, along west side of Eastern Rift Valley. Synonym: omensis. Cluster VII: Cercopithecus albogularis Cluster C. (n.) albogularis. Back grizzled and mostly relatively light in colour. Cap and diadem grizzled, not clearly differentiated from one another. Diadem peaked, long and pointed in centre. Boundary between white or off-white chin/chest fur and grizzled cheek-fur highly variable.Tail mainly black. Muzzle medium length in adult ". This cluster is distributed from S Somalia to Eastern Cape Province, South Africa, along the littoral and up most (perhaps all) Indian Ocean major river basins. It could be argued that the dark, apparently conservative populations at the northern (C. (n.) a. zammaranoi) and southern (C. (n.) a. labiatus) extremities of this range should be excised from this cluster.Were these two populations to be excluded, a more

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the Aberdares Range and Mt Kenya. In contrast, there are sharp differences between albotorquatus and C. (n.) a. zammaranoi, the two being separated by ca. 100 km of unsuitable habitat along the dry littoral of S Somalia. Synonyms: phylax, rufotinctus. C. (n.) a. monoides Tanzania Sykes’s Monkey. Crown, cheeks, neck and shoulders yellowish-olive. Rump reddish-brown. Underside grey. Otherwise similar to albogularis (and only marginally separable taxonomically). Occurs on coastal littoral from Rufiji Basin southwards to the Rovuma Basin. Also Mafia I. Synonym: rufilatus. C. (n.) a. erythrarchus Stairs’s Monkey. Similar to monoides but with variable infusions of yellow (non-agouti) colouring on back, crown, cheeks, ear-tufts and root of tail (where red fur may surround ischial callosities). Underside off-white to grey. Inhabits Indian Ocean littoral (including Bazaruto I.) and Mozambique interior from Mualo Basin south to Limpopo Basin and Manica Highlands. Synonyms: mossambicus, nyasae, schwarzi, stairsi, stevensoni. C. (n.) a. zammaranoi Zammarano’s Monkey. The smallest of all forms Pousargues’s Monkey Cercopithecus mitis albotorquatus. in the C. (nictitans) Group. Once given the Italian vernacular name restricted albogularis Cluster might turn out to represent a selfof scimmia nera (black monkey) (Funaioli 1957, 1971), this is a contained radiation centred on the tropical Indian Ocean littoral, dark form (in spite of coming from the arid S Somali coastal/ but embracing most of the major river basins between the Zambezi riverine region) (de Beaux 1923, 1937, Zammarano 1930, Patrizi R. and the Tana R. 1935). Resembles C. (n.) a. labiatus and C. (n.) n. martini in white throat and chest, dark olive back, intensely black arms graduating C. (n.) a. albogularis Zanzibar Sykes’s Monkey. Ear-tufts small, white. to dark agouti grey on upper shoulders, and dark grey agouti legs. Neck collar narrow, white. Back pale khaki agouti graduating to Belly ash grey. Cercopithecus (n.) a. zammaranoi differs in lacking darker reddish-yellow on rump. Head and shoulders agouti grey. black on head, the crown being grizzled dark olive graduating at Distributed along the Indian Ocean coast and inland between the the temples to dark grey on the cheeks. Diadem not differentiated Galana/Sabaki River Basin and the Ruvu River Basin. Also Mt in colour from the crown but is prominently peaked. Nape paler Kilimanjaro, Mt Meru, Taita Hills and Zanzibar (Nguja) I. After grey. Ears protrude only slightly and are without tufts (unlike its observing monkeys in the field at many sites within and at the nearest neighbour, the pale, white bibbed, white ear-tufted C. extremes of the range of C. (n.) a. albogularis, De Jong & Butynski (n.) a. albotorquatus, to which it is not closely related) (Funaioli & (2009) conclude that there is gradual but considerable phenotypic Simonetta 1966, Varty 1988, Gippoliti 2003). variation along north–south and west–east clines. For example, C. (n.) a. labiatus Samango Monkey. Like C. (n.) a. zammaranoi this is monkeys at the extremes of the range (e.g. at Gedi, EC Kenya, and a dark form but significantly larger. Cercopithecus (n.) a. labiatus west of Mt Kilimanjaro, NC Tanzania) differ greatly in appearance shows some resemblances with C. (n.) o. heymansi. The similarities from those on Zanzibar I., the type locality for C. (n.) a. albogularis. might be superficial or convergent but are more likely to signify Multiple photographs of several of these subspecies are available the retention of a conservative genotype at the extremities of the at: www.wildsolutions.nl Synonym: kibonotensis. range of the C. (nictitans) Group. Cheek-whiskers dark olive agouti, C. (n.) a. kolbi Kolb’s Monkey. Neck collar broad, nearly encircles the long and downwardly deflected. Diadem prominent, strongly neck, and pure white, contrasting strongly with narrow brown peaked and sometimes contrasts strongly with black crown. Back agouti cheeks and jet black arms. Crown brown agouti, sometimes dark grey agouti tinged with yellow. Arms black. Legs grey. Found nearly black. Ear-tufts long, prominent, white. Back varies from from Eastern Cape Province to the Pongola R. Valley. Synonym: khaki to deep brown or mahogany-red. Legs variable shades of samango. Like zammaranoi and boutourlinii, this form may require grey. Cercopithecus (n.) a. kolbi forms a west–east cline with C. (n.) a. re-allocation once its genotype has been examined and compared albotorquatus down the east side of the Kenya Highlands then down with those of other members of the C. (nictitans) Group. the Tana R. to the Indian Ocean (De Jong & Butynski 2009). Found in forests in the Kenya Highlands east of the Rift Valley (mainly Of all the true forest guenons, C. (nictitans) spp. and ssp. are the Aberdares Range and Mt Kenya). Cercopithecus (n.) a. kolbi may also only ones with sufficient ecological plasticity to sustain a wide be the form in the Chuylu Hills, SC Kenya. Synonyms: hindei, nubilus. distribution in southern and eastern Africa. Showing a striking C. (n.) a. albotorquatus Pousargues’s Monkey. Back and sides pale adaptability to both altitude and latitude, they range up into cool agouti yellow ochre. Upper cheek-patches narrow. Legs and montane habitats and south into temperate South African forests. shoulders dove-grey. Arms black. Conspicuous and extensive The secret of their success in peripheral forests appears to derive white ear-tufts and collar. Found on the lower Tana R., Tana Delta from a physiological ability to fall back on leaves as a staple during and north along the coast, perhaps as far as the Caanoole R., periods when fruit and invertebrates are lacking or in short supply. SE Somalia. Also Pate I. It is presumably albotorquatus that is on These relatively large, mainly arboreal monkeys are therefore Lamu I. and Manda I., Kenya (De Jong & Butynski 2009). Along relatively generalized compared to other arboreal forest guenons the course of the Tana R., albotorquatus graduates with kolbi on (which specialize in fruit and/or invertebrates, leaving leaf-eating 349

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to appropriately adapted colobines). Within the crowded primate communities of the equatorial forests C. (nictitans) are frequently rare, even absent, and it would seem to be competition from other guenons (and perhaps colobines) that constrains, or excludes them from some areas. Outside the main forest block this susceptibility to competition may not include the mangabeys (Cercocebus and Lophocebus), with which they co-exist over parts of their range. Indeed, under conditions of food stress it is the mangabeys that may be too specialized to compete with C. (nictitans). The relatively large body-size of C. (nictitans) must operate as a constraint under some climatic and ecological states, as well as in some competitive contexts. Thus it may be significant that one population, zammaranoi, isolated in botanically impoverished gallery forests in Somalia in the absence of other forest monkeys, is relatively small. The same trend was probably followed in far western Africa, resulting in the emergence of a dwarfed lineage ancestral to the Cercopithecus (cephus) lineage. For this initially restricted population small size opened new opportunities that are discussed in the C. (cephus) Group profile. With regard to their conservation, although the C. (nictitans) Group, taken as a whole, is common and widespread, several forms, notably mitis, zammaranoi, stampflii, francescae, kandti and labiatus, are rare and localized. All forms deserve to be studied and conserved as representatives of one of the most complex and interesting of all pan-tropical primate radiations. Tentative phylogenetic tree for the Nictitans Monkeys Group Cercopithecus (nictitans) (J. Kingdon reconstruction).

Jonathan Kingdon

Cercopithecus nictitans PUTTY-NOSED MONKEY (GREATER SPOT-NOSED MONKEY) Fr. Pain à cacheter; Ger. Große Weißnasemeerkatze Cercopithecus nictitans (Linnaeus, 1766). Systema Naturae, 12th edn, 1: 40. Benito R., Rio Muni, Equatorial Guinea.

Taxonomy Polytypic species that is treated here as a species within the Cercopithecus (nictitans) Group or Superspecies (see previous profile). This profile follows Dandelot (1971), Groves (2001, 2005c)

Eastern Putty-nosed Monkey Cercopithecus nictitans nictitans.

and Grubb et al. (2003) in recognizing two subspecies, Eastern Putty-nosed Monkey C. n. nictitans and Martin’s Putty-nosed Monkey C. n. martini. While the validity of C. n. stampflii is in question, this subspecies is recognized by several authorities, as well as in the C. (nictitans) Group profile presented above. Oates (1988b, 2011) and Grubb et al. (2000) recognize an additional two subspecies; C. n. ludio and C. n. insolitus. Cercopithecus nictitans has fewer chromosomes (2n = 70) than most members of the C. (nictitans) Group (2n = 72), although the Rump-spotted Monkey Cercopithecus mitis opisthostictus also has 2n = 70 chromosomes (Moulin et al. 2008). Based on protein analyses, C. nictitans and forms in the Cercopithecus mitis/albogularis Subgroup are phylogenetically extremely close (Dutrillaux et al.1988b, Ruvolo 1988). They also possess similar vocal repertoires (Gautier 1988). Thorington & Groves (1970) suggested they should be considered as conspecific, a conclusion that was later retracted (Groves 2001, 2005c). Synonyms: insolitus, laglaizei, ludio, martini, stampflii, sticticeps. Chromosome number: 2n = 70 (Dutrillaux et al. 1988b, Ruvolo 1988, Moulin et al. 2008). Description A moderately large, long-tailed monkey with a white nose spot on a grizzled greyish-olive or khaki-olive face. Sexes alike in colour but adult ! smaller, weighing ca. 60% as much as adult " in the nominant subspecies and ca. 80% as much as adult

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populations of stuhlmanni might be in a late process of being absorbed genetically by C. n. nictitans. Ceropithecus petaurista. Sympatric with C. n. stampflii. Body smaller and coat lighter. Ventrum white. White stripe on lateral sides of face. Distribution Endemic to West Africa and western central Africa. Rainforest BZ. See details for distribution in Geographic Variation. Northern limit in central Africa is at ca. 08° 20´ N in Central African Republic to ca. 05° S in Congo. Absent from the left (south) bank of Congo R. (Schouteden 1947, Colyn 1988, Oates 1988b, 2011, Gautier-Hion et al. 1999).

Cercopithecus nictitans

" in C. (n.) n. martini on Bioko I. (Butynski et al. 2009). Nose with white oval spot. Whiskers, diadem, crown, shoulders, back, legs and basal part of tail dark greyish-olive or khaki-olive due to ringed (grizzled) hairs. Arms, hands, feet, belly and distal part of tail black. Young similar in colour to adults but white nose spot not present at birth. Geographic Variation C. n. nictitans Eastern Putty-nosed Monkey. Occurs mainly south of Sanaga R., Cameroon, southwards through Equatorial Guinea (Rio Muni), Gabon and Cabinda (Angola) to Congo R. and eastwards across Central African Republic and Congo into DR Congo to north of Congo R. and west of Itimbiri R. (Oates 1988b, GautierHion et al. 1999, Grubb et al. 2000). The Sanaga R. is not, however, a clear-cut barrier as at least one population occurs north of Sanaga R. Overall dark greyish-olive with broad, largely blackish crown and rounded face. Underside as dark as upperside. Chest black. C. n. martini (including stampflii) Martin’s Putty-nosed Monkey. Disjunct distribution; N Liberia and SW Côte d’Ivoire and then in S Nigeria and SW Cameroon to Sanaga R. (Oates 1988b, 2011, Grubb et al. 2000). Also Bioko I., Equatorial Guinea, where it appears to be limited to the lower southern slope of Pico Basilé and to the remote and extremely wet southern ca. 25% of the island (Butynski & Koster 1994). Overall, khaki-olive (lighter than C. n. nictitans). Crown with black, narrow sides. Whiskers downward deflected giving face a narrower appearance. Throat and inner surfaces of upper arms white or off-white. Underside dusky grey. Similar Species Cercopithecus mitis stuhlmanni. Mainly allopatric. Bluer and lacks distinctive white nose spot. Kingdon (1980), however, points out that spot-nosed individuals resembling C. m. stuhlmanni are described from places as far apart as Gabon (Pocock 1907) and Ubangi, DR Congo (Elliot 1909a). He suggests that relict

Habitat Lowland and medium-altitude forests. Typically lives in primary forest with tall trees, but also in riverine and old secondary forests. In relict patches of high forests within forest–savanna mosaics (Oates 1988b for West Africa). In gallery forests and patches of forest in Central African Republic (Fay 1988) and Gabon (Tutin et al. 1997b). Prefers middle and upper strata of the canopy, at similar height to Crowned Monkey Cercopithecus pogonias. Spends 56% of time above 20 m and only 3% below 10 m. Rarely observed on the ground (Gautier-Hion & Gautier 1974) except to cross savanna between forest patches/forest galleries and continuous forest (C. Tutin pers. comm.). On Bioko I. observed only in pristine forest and in slightly degraded primary forest, not in secondary forest (T. Butynski pers. comm.). From sea level to >1000 m on the mainland. From 0–900 m on Bioko I. where it appears to have the most limited altitude range of any of the seven species of primates (Butynski & Koster 1994). Annual rainfall from ca. 1500 mm to ca. >4000 mm on the mainland and from ca. 4000–10,000 mm on Bioko I. Abundance Biomass for C. n. nictitans in primary forests ranges from ca. 40 kg/km2 in the Forêt des Abeilles, C Gabon (Brugière 1988), to ca. 480 kg/km2 at Odzala N. P., Congo (Bermejo 1999). At most sites the greatest biomass is in mature forest. At Odzala N. P., biomass varies from 41 kg/km2 in forest patches, 60 kg/km2 in riverine forests, 90 kg/km2 in secondary forests to 480 kg/km2 in mature forest (adapted from Bermejo 1999). In Lopé Reserve, C Gabon, biomass is lower in the continuous forests (Marantaceae forests with dense undergrowth) than in gallery forests and forest patches of the neighbouring savanna (81 kg/km2 vs. 135 kg/km2; Tutin et al. 1997a, b). In gallery forests of St Floris N. P., Central African Republic, the biomass is less than 10 kg/km2 (Fay 1988). At most sites, in both mainland mature forest and riverine forest, C. n. nictitans is more abundant than its congenerics C. pogonias and Moustached Monkey Cercopithecus cephus. In secondary forest its density is generally lower than that of C. cephus. On the mainland, in northern Korup N. P., W. Cameroon, the density of C. n. martini ca. 1.1–1.5 groups/km² and biomass at 51 kg/km² (A. Edwards quoted by J.Oates pers. comm.). Another study in Korup N. P., conducted in 2004–05, found 0.08–0.37 groups/km2 (Linder & Oates 2011). Uncommon in Okomu N. P., SW Nigeria, where Akinsorotan et al. (2011) sighted only 0.02 groups/km. In Liberia and Côte d’Ivoire, C. nictitans is usually rare and occurs only in the drier, more deciduous forest north of the main evergreen forest (H.-J. Kuhn quoted by J. Oates pers. comm.). This might be influenced by competition with Diana Monkey Cercopithecus diana (Oates 1988b). 351

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Lateral view of skull of Eastern Putty-nosed Monkey Cercopithecus nictitans nictitans adult male.

Perhaps the rarest primate on Bioko I. Encounter rate of 0.01 groups/km of transect during an island-wide survey in 1986 (373 km of census; Butynski & Koster 1994). Encounter rate of 0.02 groups/km in 2008 along 49 km of transect the south slope of Pico Basilé, and 0.06 groups/km in 2009 along 48 km of transect and no groups encountered in 2010 along 50 km of transect at Badja North, SW Bioko (T. Butynski, G. Hearn, M. Kelly & J. Owens pers. comm.). The south slope of Pico Basilé and Badja North are remote sites where hunting is relatively uncommon and where there are no other anthropogenic impacts. As such, the encounter rates at these two sites are likely close to what is expected for an undisturbed population of C. nictitans living near the upper altitude range for the species (i.e. 500–900 m). In contrast, at Arihá, SE Bioko, an area in which there is a moderate level of hunting for primates but that is at the lower altitude range for C. nictitans, Maté & Colell (1995) encountered 0.10 groups/km in 1992 along 100 km of transect. They estimated 0.05 groups/km² and ca. 0.3 ind/km² at Arihá.

fruit and leaf intake. Adult "" are more frugivorous than adult !!, especially when fruit is abundant, while the ingestion of leaves by adult !! is twice that of adult "". Seventy-one plant species identified in the diet, mainly taken from Annonaceae, Apocynaceae, Burseraceae and Euphorbiaceae. Females eat more animal matter. Sedentary prey forms the great majority of captures (>90%), caterpillars and ants being the most common prey. In Forêt des Abeilles, the annual plant diet comprised 36% fruit (including 11% arils), 57% seeds and 11% leaves. Seeds and leaves of Caesalpiniaceae comprised 46% of the diet (Brugière et al. 2002). At Lopé Reserve, diet of C. nictitans in a continuous forest differed from that in neighbouring forest fragments by more fruit eating (59% vs. 44%) and seed eating (11% vs. 4%) and by less insect eating (3% vs. 24%; Tutin et al. 1997a, b). Forages in groups or in polyspecific associations. Most active in early morning and late afternoon. Home-range size ca. 55–100 ha; daily range ca. 1500 m (Gautier-Hion 1988).

Social and Reproductive Behaviour Social. Bisexual groups contain only one adult " who gives ‘pyow’ calls, especially at dawn and dusk (Gautier & Gautier-Hion 1977). These loud-calls help to maintain space between groups and rally group members. When two groups are close to each other, ‘pyow’ calls are accompanied by loud aggressive ‘barks’. Territorial conflicts occur. Mean group size varies from 11 individuals at Forêt des Abeilles (8–19, n = 35; Brugière et al. 2002), to 14.6 individuals at Odzala N. P. (5–27, n = 61; Maisels 1995), to 18 individuals at Ngotto Forest, Central African Republic (15–20, n = 6; Gautier-Hion 1996). In large groups the number of adult !! may reach 11. Solitary adult "" are frequent (up to 28% of encounters during a census). Cercopithecus n. nictitans is in polyspecific associations with one or more arboreal monkey species 50% of the time on average (30–87% of the time, depending on site). The lowest incidence is at Odzala N. Adaptations Diurnal and arboreal. As a species, C. nictitans is a P., which harbours the highest density of C. n. nictitans; suggesting successful monkey, able to colonize different habitats and to come to that not all groups can find partners with which to associate. The the ground occasionally to cross open areas. This generalist species species that associate most frequently with C. n. nictitans are C. cephus has two adaptive advantages: highly developed arboreal skills and (45% of cases), C. cephus + C. pogonias (32%), and C. pogonias (16%). the ability to eat leaves and insects during periods when fruit is On Bioko I., C. n. martini in association with C. pogonias, Red-eared scarce. The large white spot on the nose provides a distinctive cue Monkey Cercopithecus erythrotis, Black Colobus Colobus satanas and for species recognition. The main function of the white nose spot Pennant’s Red Colobus Procolobus pennantii (Butynski & Koster 1994, seems to be to serve as a visual distraction from the eyes. The nose- T. Butynski pers. comm.). spot becomes especially conspicuous during ‘head flagging’, which In tri-specific associations that include C. pogonias + C. cephus, the Kingdon (1988b, 2007) considers part of ‘cut-off’ behaviour. This adult " C. n. nictitans generally gives his ‘pyow’ calls after the ‘boom’ behaviour has resulted in the French name of ‘hocheur’ (i.e. ‘head calls of the adult " C. pogonias. This is true for the call sequences shaker’) for this species. However, this name is confusing because the given ritually at dawn, during which the adult " nictitans called after behaviour also occurs in other guenons and, in DR Congo, the Red- the adult " pogonias in 77% of cases, as well as when the mixed group tailed Monkey Cercopithecus ascanius is also named ‘hocheur’. Like faced an avian predator (adult " nictitans called first in 11% of cases) other cercopithecines, C. nictitans possesses large cheek-pouches. or a climbing predator (adult " nictitans called first in 8% of cases). These are used to store large amounts of fruit before moving to These figures suggest reduced vigilance by the adult " nictitans. The ingest the fruit in a place more sheltered from predators and while adult " nictitans called first mostly after violent, loud, perturbations foraging for more nutritious insects. Adult "" have large air such as a tree fall or a rumble of thunder (Gautier & Gautier-Hion sacs used for producing loud-calls that are highly specific to the C. 1983, Gautier-Hion et al. 1983). When in polyspecific association, (nictitans) Group (Gautier 1971). the adult " nictitans may actively pursue African Crowned Eagles Stephanoaetus coronatus even when the eagles’ attack was on a monkey Foraging and Food Omnivorous. In Makokou area, NE Gabon, of another species (Gautier-Hion & Tutin 1988). annual diet of C. nictitans dominated by fruit and seeds (70%), followed Cercopithecus n. nictitans in Gabon gives the boom call. The boom by leaves (17%) and animal matter (10%; Gautier-Hion 1980). Great of C. nictitans is weaker and lower-pitched (112 Hz) than the boom seasonal variations in diet occur with an inverse relationship between of De Brazza’s Monkey Cercopithecus neglectus or Crowned Monkey 352

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Cercopithecus pogonias (150 Hz). In this regard, the boom of C. n. nictitans is similar to that of the Gentle Monkey Cercopithecus mitis (Gautier 1973, J.-P. Gautier pers. comm.). A particularly interesting question is, does C. nictitans give the boom over its entire geographic range? The opinion of T. Butynski (pers. comm.) is that C. n. martini on Bioko does not give the boom, or else gives this call so infrequently that it has not, as yet, been detected by researchers. Cercopithecus n. martini is a common monkey in Korup N. P., but J. Linder has not heard this species give the boom there, nor has J. Oates heard this call from C. n. martini in the Cross R. forests of Nigeria. Struhsaker (1970) makes no mention of the boom call for C. n. martini in Cameroon. In Gashaka Gumti N. P., NE Nigeria, C. n. martini does give the boom, but much less frequently relative to Campbell’s Monkey Cercopithecus campbelli (K. Arnold pers. comm.). Reproduction and Population Structure Cercopithecus nictitans reproduces seasonally in synchrony with other cercopithecines (Gautier-Hion 1968, Butynski 1988). Mating takes place in the main dry season (most often Jul–Aug) and births peak around the short dry season (Dec–Feb). Sexual maturity is reached around six years for "" and four years for !!. Gestation length is about 5.5 months (Gautier-Hion & Gautier 1976). The single infant weighs about 350 g (Gautier-Hion 1968). Structure of 36 groups in Odzala N. P. averaged 8% adult "", 35% adult !!, 20% subadults, 24% juveniles and 14% infants (Maisels 1995). Solitaries account for about 9% of a population in C Gabon (Brugière et al. 2002). Predators, Parasites and Diseases Leopard Panthera pardus is a predator of C. nictitans (Henschel et al. 2005, 2011). Humans are the most frequent predators of C. nictitans on Bioko I. where S. coronatus, Leopards and Golden Cats Profelus aurata are absent (Struhsaker 2000a, T. Butynski pers. comm.). No information on diseases and parasites. Conservation IUCN Category (2012): C. nictitans is Least Concern, whereas C. n. martini is Vulnerable. CITES (2012): Appendix II. Among arboreal monkeys, C. nictitans may be the most tolerant of heavy hunting pressure, but near villages, this species is often decimated by hunting (Linder & Oates 2011). There remain large, dense populations in several places.There is particular concern for C. n. martini (including stampflii) as this subspecies has a relatively small, highly fragmented range and is heavily hunted both on the mainland (Oates et al. 2004) and on Bioko I. (Hearn et al. 2006). On Bioko I.

(2017 km²), hunting with shotguns is the only threat to C. n. martini. The price paid per carcass in 2005 was ca. US$31. This is possibly the least common monkey on Bioko I. and is unlikely to number >1000 individuals (Hearn et al. 2006). Forest clearance also threatens this species, which prefers primary lowland forest. Protection of the population in the Gran Caldera & Southern Highlands Scientific Reserve (510 km²) is critical to the long-term conservation of this monkey on Bioko (Hearn et al. 2006). Measurements Cercopithecus nictitans Cercopithecus n. nictitans HB (""): 550 mm, n = 9 HB (!!): 435 mm, n = 3 T (""): 910 mm, n = 9 T (!!): 765 mm, n = 3 HF: n. d. E: n. d. WT (""): 6.7 (3.5–9.8) kg, n = 56 WT (!!): 4.1 (2.7–6.1) kg, n = 48 Makokou area, NE Gabon (Gautier-Hion et al. 1999); ranges not available for linear measurements Cercopithecus n. martini HB (""): 485 (420–570) mm, n = 14 HB (!!): 439 (400–500) mm, n = 20 T (""): 740 (700–790) mm, n = 13 T (!!): 648 (558–700) mm, n = 19 HF (""): 139 (130–150) mm, n = 14 HF (!!): 125 (112–132) mm, n = 18 E (""): 30 (28–35) mm, n = 15 E (!!): 29 (26–32) mm, n = 20 WT (""): 5.1 (4.0–6.0) kg, n = 14 WT (!!): 4.1 (3.0–5.6) kg, n = 20 Upper canine (""): 16 (12–20) mm, n = 13 Upper canine (!!): 9 (6–12) mm, n = 16 Lower canine (""): 11 (10–12) mm, n = 13 Lower canine (!!): 6 (4–10) mm, n = 18 Bioko I., Equatorial Guinea (Butynski et al. 2009) Key References Gautier-Hion 1980; Gautier-Hion et al. 1983; Oates 1988b, 2011; Tutin et al. 1997b. Annie Gautier-Hion

Adult female Putty-nosed Monkey Cercopithecus nictitans presenting genitalia during oestrus.

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Cercopithecus mitis GENTLE MONKEY (DIADEMED MONKEY, BLUE MONKEY, SYKES’S MONKEY) Fr. Cercopithèque à diadème; Ger. Diademmeerkatze Cercopithecus mitis Wolf, 1822. Abbild. Beschreib. Merkw. Naturgesch. Gegenstandes 2: 145. Angola (holotype a menagerie animal and not in existence).

Golden Monkey Cercopithecus mitis kandti adult male.

Taxonomy Polytypic species. Several classifications place Cercopithecus mitis and Cercopithecus nictitans in the Cercopithecus (nictitans) Group or Superspecies (Hill 1966, Dandelot 1974, Lernould 1988, Kingdon 1997, Grubb et al. 2003). See Cercopithecus (nictitans) Group profile. This classification is supported by DNA analysis (Van der Kuyl et al. 1995, Tosi et al. 2005), vocalizations (Gautier 1989a), facial pattern (Kingdon 1980, 1988b, 1997), proteins (Ruvolo 1988), chromosomes (Sineo 1990), and external morphology and distribution patterns (Hill 1966). A recent molecular study recognizes C. nictitans, C. mitis and C. albogularis as a single genetic entity (Tosi et al. 2005). This profile deals with the Gentle Monkeys C. mitis/albogularis Subgroup of the C. (nictitans) Group. Highly polytypic species (Kuhn 1967, Rahm 1970, Groves 1993) within which Grubb et al. (2003) recognize 16 subspecies. Two species, Blue Monkey C. mitis and Sykes’s Monkey C. albogularis, have been widely recognized (Hill 1966, Dandelot 1974, Napier 1981, Lernould 1988). Groves (2001) recognizes four species in the C. mitis/albogularis Subgroup; C. mitis, C. albogularis, Silver Monkey C. doggetti and Golden Monkey C. kandti. The great variability in this taxon and its disputed taxonomy is indicated by the use of non-traditional nomenclature in previous classifications including

‘subspecies-groups’ (Napier 1981), ‘clusters’ (Kingdon 1997), ‘sections’ (Grubb 2001, Grubb et al. 2003), ‘species-groups’ and ‘species-subgroups’ (Grubb et al. 2003). In the C. (nictitans) Group profile presented above, Kingdon presents a taxonomy that recognizes 18 forms of Gentle Monkeys in six ‘clusters’. Here we recognize 17 subspecies in five sections in two clusters. The difference is that Kingdon recognizes maesi. Both of these taxonomies are similar to Grubb et al. (2003) except that Grubb et al. (2003) do not recognize maesi or zammaranoi. The five sections put forth here follow Grubb et al. (2003). Hybridization between Red-tailed Monkey Cercopithecus ascanius and C. mitis occurs in East Africa at several sites (Aldrich-Blake 1968, Struhsaker et al. 1988, Detwiler 2002, Detwiler et al. 2005). There are also three instances of a inter-generic hybridization between C. mitis and Vervet Chlorocebus pygerythrus in Kenya (De Jong & Butynski 2010b). Several authors report intra-specific hybridization in C. mitis. Individuals showing intermediate pelage patterns reported by Rahm (1970), Colyn (1988, 1991) and Twinomuguisha et al. (2003) – C. m. doggetti × C. m. kandti, C. m. stuhlmanni × C. m. schoutedeni, C. m. opisthostictus × C. m. stuhlmanni, C. m. heymansi × C. m. opisthostictus, C. m. stuhlmanni × C. m. kandti and C. m. doggetti × C. m. stuhlmanni. Booth (1968) noted a hybrid swarm (C. m. stuhlmanni × C. m. albogularis) in the Ngorongoro–L. Manyara area of N Tanzania. Synonyms: albogularis, albotorquatus, beirensis, boutourlinii, carruthersi, chimango, diadematus, dilophos, doggetti, elgonis, erythrarchus, francescae, heymansi, hindei, insignis, kanti, kibonotensis, kima, kolbi, labiatus, leucampyx, maesi, maritima, mauae, moloneyi, monoides, mossambicus, neumanni, nigrigenis, nubilus, nyasae, omensis, opisthostictus, otoleucus, phylax, pluto, princeps, rufilatus, rufotinctus, samango, schoutedeni, schubotzi, schwarzi, sibatoi, stairsi, stevensoni, stuhlmanni, zammaranoi (Groves 2001, 2005c, Grubb et al. 2003). Chromosome number in C. mitis (including C. albogularis): 2n = 72 (Chiarelli 1962b, 1968a, b, Bender & Chu 1963, Sineo 1990, Hirai et al. 2000, Moulin et al. 2008). Dutrillaux et al. (1980) report 2n = 70 for a captive hybrid C. m. opisthostictus × C. m. stuhlmanni and a C. m. opisthostictus !. Description A moderately large, long-tailed arboreal monkey. Face dark with backward- and downward-directed whiskers and often with oval-shaped cheeks giving face a round appearance. Lacks a beard. Forelimbs, hands, feet and distal half of tail black or blackish. Saddle and shoulders variously coloured from dark grey to grey suffused with green, yellow or orange. Shoulder/saddle hair can be long, giving appearance of a mantle. Ventrum black or grey to white. Sexes alike in colouration but adult ! smaller than adult ", weighing ca. 60% as much. Adult " has a more prognathous jaw and larger canines than adult !. Newborns black/brown, without grizzled pelage; sometimes with faint diadem. General descriptions of this species are here divided into two clusters: one of eight subspecies found north and west of the Eastern

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Rift Valley, and one of nine subspecies found east and south of the Eastern Rift Valley. Northern and Western Cluster: West of the Eastern Rift Valley in SW Ethiopia, S Sudan, Uganda,W Kenya, DR Congo, Zambia and Angola, includes subspecies boutourlinii, doggetti, heymansi, kandti, mitis, opisthostictus, schoutedeni and stuhlmanni. Pale brow-band (diadem) contrasting in colour with dark crown, except in opisthostictus; cheeks rounded, speckled; chin pale; ear-tufts white. Crown and neck dark grey or black. Back dark, usually grey or greenish, except in kandti; black band across shoulders. Southern and Eastern Cluster: East of the Eastern Rift Valley from SE Somalia to the Eastern Cape Province in South Africa, includes subspecies albogularis, albotorquatus, erythrarchus, francescae, kolbi, labiatus, moloneyi, monoides and zammaranoi. Diadem not distinct; ear-tufts white, buff, or red; brow hairs long, speckled, stiff and projecting forward; chin and cheeks white; throat-patch pale and forms partial neck collar in northern forms. Back grey, yellowishgrey, or dark olive, in some shows gradual increase in yellow or red from the shoulders to back of rump; shoulders same colour as crown and without black band. Ventrum light. Undersurface of tail base with orange, red or brown hairs, except in labiatus. Photographs of several of these subspecies are available at: www.wildsolutions.nl Geographic Variation South and East Cercopithecus mitis albogularis Section: C. m. zammaranoi Zammarano’s Monkey. S Somalia, along course of Jubba R. and Shabeele R. Small size; back, shoulders and rump olive-green; ventrum ashy-grey; no rufous tint on inner thighs or lumbar region; limbs dark, almost black; white collar reduced compared with nearby albotorquatus. C. m. albotorquatus Pousargues’s Monkey. Extreme S Somalia, Pate I., and middle and lower course of Tana R., Kenya. Diadem and crown dark olive; throat and (near complete) neck collar white. Back and shoulders dark olive; rump olive, yellowish, or reddish-brown; inner thighs may also be reddish-brown. Ventrum ashy-grey or cream. See De Jong & Butynski (2011) for details. Synonyms: phylax, rufotinctus. C. m. kolbi Kolb’s Monkey. Kenya Highlands east of the Rift Valley. Eartufts long, white; collar broad, white, and nearly complete. Back russet, slightly darker than albogularis. Ventrum dark. Synonyms: hindei, nubilus. C. m. albogularis Zanzibar Sykes’s Monkey. SE Kenya, Zanzibar I., Mt Kilimanjaro, Mt Meru, NE Tanzania. Head and shoulders grey; ear-tufts small and white; throat white; collar narrow. Rump reddish-yellow. Synonym: kibonotensis. C. m. monoides Tanzania Sykes’s Monkey. Coastal Tanzania, Mafia I., NE Mozambique. Throat-patch variable in size; crown, cheeks, neck and shoulders yellowish-olive. Back reddish-brown.Ventrum dark slate-grey. Synonym: rufilatus. C. m. francescae Red-eared White-collared Monkey.West of L. Malawi, Malawi. Collar short and grey; ear-tufts red. Shoulders dark grey. Back brownish-grey. Ventrum dark grey. C. m. moloneyi Moloney’s Monkey. SW Tanzania to northern shore of L. Malawi, Zambia east of Luangwa R., N Malawi. Throat-patch cream. Back with dark red saddle. Sides and thighs light grey. Ventral surface of tail reddish.

C. m. erythrarchus Stairs’s Monkey or Samango Monkey. N South Africa (Limpopo Province, N KwaZulu–Natal Province), Mozambique (incl. Bazaruto I.), NE Zimbabwe. Ear-tufts yellowish-white. Back light grey to olive-green, especially on saddle, grizzled. Ventrum whitish or pale grey. Ischial callosities with yellow, orange or red hairs. Tail black. Synonyms: beirensis, mossambicus, nyasae, schwarzi, stairsi, stevensoni. C. m. labiatus Samango Monkey. Eastern Cape Province to KwaZulu– Natal midlands and southern Mpumalanga Province, South Africa. Crown almost black. Back dark-grey, darkest of all subspecies in the albogularis Section. Ventrum pale ashy grey. Tail with dark dorsal band, buff laterally and ventrally; base of tail with no red. Synonym: samango. North and West Cercopithecus mitis heymansi Section: C. m. heymansi Lomami River Monkey. Between Lualaba R. and Lomami R., DR Congo. Face black; diadem white and narrow; crown, neck and shoulders blue-grey. Ventrum lighter than dorsum. Cercopithecus mitis mitis Section: C. m. opisthostictus Rump-spotted Monkey. S DR Congo, N Zambia, N Zimbabwe, E Angola. Lips, chin, throat white; diadem grey, speckled; crown like back. Back uniformly olive to light grey; shoulders, neck and ventrum black. Hindlimbs dark but not black. C. m. mitis Angola Pluto Monkey. Coastal Angola. Diadem whitish and conspicuous; nose, lips, chin with short, white hairs; crown, neck, shoulders and hindlimbs black. Back and ventrum dark grey to black. Synonyms: diadematus, dilophos, leucampyx, nigrigenis, pluto. Cercopithecus mitis boutourlinii Section: C. m. boutourlinii Boutourlini’s Blue Monkey. SW Ethiopia. Diadem not differentiated from crown; lips, chin and throat white. Back dark green or yellowish-grey. Shoulders black with grey speckling. Hindlimbs and ventrum black. Synonym: omensis. Cercopithecus mitis stuhlmanni Section: C. m. stuhlmanni Stuhlmann’s Blue Monkey. NE DR Congo, Uganda, W Kenya, SE Sudan. Chin and throat white; diadem grey; crown and neck black. Back steel blue-grey, but sometimes faintly greenish. Ventrum lighter than dorsum. Synonyms: carruthersi, elgonis, maesi, mauae, neumanni, otoleucus, princeps. C. m. schoutedeni Schouteden’s Silver Monkey. Idjwi I. in L. Kivu and western Virunga Mts, E DR Congo. Diadem white and speckled; crown and neck black. Back pale olive-grey. Ventrum lighter than dorsum. C. m. doggetti Doggett’s Silver Monkey. Burundi, Rwanda, SW Uganda, NW Tanzania, E DR Congo. Crown and neck black, contrasting sharply with diadem. Back light grey-brown. Hindlimbs blackishgrey. Synonym: sibatoi. C. m. kandti Golden Monkey. E DR Congo near L. Kivu, Virunga Mts and Nyungwe N. P., SW Rwanda. Diadem dark yellowishgrey; crown and nape black. Back large amount of red or orange, amount of red individually variable; shoulder band narrow. Ventrum rust or orange. Synonym: insignis. 355

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Family CERCOPITHECIDAE

Similar Species Cercopithecus nictitans. Western central Africa and West Africa. Parapatric and, perhaps, narrowly sympatric at eastern edge of geographic range. Nose with large white spot. Distribution Endemic to Africa south of the Sahara. Rainforest, Afromontane–Afroalpine, Somalia–Masai Bushland, Zambezian Woodland, and Coastal Forest Mosaic BZs. Widespread in all forest types in central, East and southern Africa. Nominal subspecies in extra-limital populations in W Angola. Occurs south of ca. 11° N on the Ethiopian Plateau (C. m. boutourlinii; Napier 1981), in SE Sudan (C. m. stuhlmanni; Butler 1966), SE Somalia (C. m. zammaranoi; Gippoliti 2003), S Somalia and NE Kenya, including Pate I. (C. m. albotorquatus; Lernould 1988). Cercopithecus m. stuhlmanni east of Congo R. and to west of Eastern RiftValley in Kenya. Cercopithecus m. stuhlmanni common on right bank of Congo/Lualaba River, from Itimbiri R. confluence to ca. 05° S (Colyn 1991). Range of C. m. heymansi is known with certainty only from northern part of forest between Lualaba R. and Lomami R. (E DR Congo; Colyn 1988). Cercopithecus m. opisthostictus in E Angola along the High Zambezi (Machado & Crawford-Cabral 1999). Cercopithecus m. stuhlmanni and C. m. opisthostictus in contact and may hybridize north of Lukuga R., E DR Congo (Colyn 1991). Cercopithecus m. kandti is restricted to Virunga Mts of SW Uganda, NW Rwanda and E DR Congo (Aveling 1984, Twinomugisha 2000), and possibly Nyungwe N. P., E Rwanda (A. Plumptre & B. Kaplin pers. comm.). Distribution of C. m. schoutedeni limited to Idjwi I. in L. Kivu (DR Congo) and small area to north (Lernould 1988). Cercopithecus m. kolbi confined to Kenya Highlands (Kingdon 1971, De Jong & Butynski 2009). Cercopithecus m. monoides in E Tanzania to the coast and bounded in the north by the Pangani R. and by C. m. albogularis whose range extends into SE Kenya (Lernould 1988, De Jong & Butynski 2009). Cercopithecus m. albogularis also on Unguja I. (formally Zanzibar). Cercopithecus m. moloneyi in vicinity of L. Rukwa, southern L. Tanganyika and NE Zambia (Lernould 1988). In Malawi C. m. francescae replaces C. m. moloneyi in north from Chombe Mt and is replaced by C. m. erythrarchus south of Ntchisi Mt (Ansell & Dowsett 1988). Exact boundary between coastal distributions of C. m. monoides and C. m. erythrarchus in N Mozambique unknown (Lernould 1988). Cercopithecus m. erythrarchus extends down eastern seaboard of southern Africa, including the eastern highlands of Zimbabwe, but not south of Umfolozi R. Remnant population of C. m. erythrarchus on Bazaruto I., S Mozambique (Downs & Wirminghaus 1997). Both C. m. erythrarchus and C. m. labiatus found in South Africa, but latter subspecies confined to higher-altitude forests and coastal forests of afromontane origin to ca. 33° S, Eastern Cape Province (Lawes 1990a). Habitat In all types of evergreen forest from primary and secondary lowland rainforest, riverine, swamp, gallery, coastal, through montane forest, including bamboo zone, and up to 3800 m on Rwenzori Mts, Uganda (A. Plumptre pers. comm.). Prefers primary forest, but also in secondary forest, logged forest and thicket (Chapman et al. 2000, Fashing et al. 2012). More tolerant of poor habitat quality than most guenons, accounting for wide African distribution and use of diverse forest types (Lawes 1990a, Thomas 1991). Only forest guenon with an extensive range outside lowland rainforest. Occupies three broad forest types, many subspecies occurring in at least two: (1) afromontane (stuhlmanni, schoutedeni, boutourlinii, doggetti, kandti, kolbi, francescae,

Cercopithecus mitis

albogularis, labiatus); (2) central lowland forests (stuhlmanni, doggetti, maesi, heymansi, opisthostictus, moloneyi, albogularis, mitis); and (3) Indian Ocean coastal lowland and riparian forests (zammaranoi, albotorquatus, albogularis, monoides, erythrarchus) (Stott 1960, Butler 1966, Kingdon 1971, Bolton 1973, Colyn 1988, Gippoliti 2003, De Jong & Butynski 2009). Cercopithecus m. stuhlmanni is a denizen of larger lowland and montane forests. Cercopithecus m. kolbi occupies montane forests of the Kenya Highlands and ventures into pine (Pinus spp.) plantations adjacent to forest (De Vos & Omar 1971, Maganga & Wright 1991); it shares this behaviour with C. m. francescae and C. m. labiatus (Von dem Bussche & Van der Zee 1985, Beeson 1987). Cercopithecus m. kandti inhabits montane forests of the Virunga Mts, including the bamboo zone (Aveling 1984). Cercopithecus m. doggetti uses mature montane forests, bamboo forest, and papyrus swamps in marshy lowlands, but is more common in moist valley and riverine forest (Macaranga spp.) (Kaplin 2001). Cercopithecus m. albotorquatus in riparian forest patches along the middle and lower Tana R. and in coastal forests north of the Tana Delta (Butynski & Mwangi 1994). Subspecies in coastal lowland forest use coastal thicket where it is adjacent to high forest. Cercopithecus m. erythrarchus in a variety of forest types from coastal lowland forest and thicket, to riverine, swamp, deciduous dry and coastal dune forest on the mainland (Lawes 1992), and in low-quality swamp forest and mixed woodland on Bazaruto I. (Downs & Wirminghaus 1997). Cercopithecus m. labiatus in afromontane forests only (Lawes 1990a). Abundance A shy and sometimes difficult species to observe, but nevertheless common throughout the geographic range. Can be a pest around lodges, human habitation and gardens (Chapman et al.

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Cercopithecus mitis

1998). Occurs at moderate density – 0.7 ind/ha (0.05–2.0) or 4.3 groups/km2 (0.4–9.0) – over most of its range (Aldrich-Blake 1970, Moreno-Black & Maples 1977, Rudran 1978b, Schlichte 1978, Scorer 1980, Rodgers & Homewood 1982, Van der Zee & Viljoen 1984, Butynski 1990, Lawes et al. 1990, Thomas 1991, Cordeiro 1992, Kaplin & Moermond 1998, Kaplin 2001). At 1.2 ind/ha in gallery forest along the Tana R., Kenya (Butynski & Mwangi 1994). At greatest density in montane forests of East and central Africa (1.2–2.2 ind/ha; De Vos & Omar 1971, Beeson 1987, Cords 1987b, Fashing & Cords 2000, Twinomugisha 2000, Cords & Chowdhury 2010), and coastal forests of S Mozambique and Maputaland (>2.0 ind/ha; KwaZulu–Natal; Lawes 1992). At these localities C. mitis is usually the only resident guenon species. Low-density populations (1300 mm mean annual rainfall) lowland, swamp, gallery, lakeshore, mid-altitude and montane forests from 0 to 2500 m asl, including forest islands, degraded forest and secondary forest. Ranges into Brachystegia woodland (eastern shore L. Tanganyika), undifferentiated woodlands, exotic plantations (e.g. Blue Gum Eucalyptus spp.), and dryer forest (1100–1300 mm mean annual rainfall) adjoining moist forest habitat. Inhabits small forest patches devoid of other monkeys. Absent from the interior of primary forests where secondary vegetation is uncommon (Schouteden 1944a). Spends most time in lower and middle forest strata (10–20 m), but occasionally seen on ground (Haddow 1952, Gathua 2000a). Abundance Cercopithecus a. schmidti in East Africa is often most abundant at forest edge and in secondary forest, unless disturbance is extreme. Density ca. 8–184 ind/km2 (1.0–13.3 groups/km2) (Cords 1987b, Plumptre & Reynolds 1994, Fashing & Cords 2000, Mitani et al. 2001, Fashing et al. 2012). Within the same forest, density can vary three-fold across distances of 50 animals) will fission, with resultant groups dividing original home-range (Struhsaker & Leland 1988, Windfelder & Lwanga 2002). Crop-raiding parties of up to 200 members (Haddow 1952) probably include several groups. Groups usually include one adult resident ". Adult !! make up, on average, 36% of group, and immatures the remaining 60%. During annual mating season, up to six adult "" per month can join group. Groups in which four adult "" resided simultaneously for >1 year have been reported (Central African Republic; Galat-Luong 1975). Males leave natal groups as subadults (>4 years old), and can spend >3 years away from groups containing C. ascanius !! (Struhsaker & Pope 1991), living either alone or in loose ephemeral associations. Females remain in natal groups for life. Intra-group amicable behaviours are more frequent than aggressive behaviours and include grooming and sitting in contact. Grooming bouts in which adult "" receive grooming from other group members, and adult !! groom each other, occur disproportionately often (Struhsaker & Leland 1979). Play-wrestling and chasing are most common among young animals. Aggressive behaviour includes shaking of head and forequarters, stare-threats, aggressive growls, chases and contact fights with slapping and biting.

Schmidt’s Red-tailed Monkey Cercopithecus ascanius schmidti.

Most agonistic interactions comprise two individuals. Overlap of group home-ranges is 0–64%. Groups defend territorial boundaries with aggressive inter-group encounters once every 3–6 days, and more frequently after group fissions (Cords 1987b, Struhsaker & Leland 1988, Windfelder & Lwanga 2002). Females involved much more than "" in inter-group aggression. Occasionally adjacent groups do not interact, or they supplant one another without obvious aggression. Pre-copulatory behaviour includes persistent following by either partner, head-flagging by "" and lip-puckering by !!. Copulations often involve multiple mounts with intromission and thrusting before final mount ending in a coital pause, possibly associated with ejaculation. Vaginal semen plugs often visible after copulation. Juveniles frequently harass copulating partners and sometimes disrupt copulation. Males gain reproductive access to !! in several ways. Some "" take over groups aggressively to become sole residents. Resident "" occasionally copulate with !! from neighbouring groups. Non-resident "" sometimes join a heterosexual group for a few days to several months during the mating season. Often several "" join a group at once, resulting in a multimale influx. Influx "" usually confine their visits to just one heterosexual group in a given year (Jones & Bush 1988, Struhsaker 1988). During influx, fights between "" are frequent, and can lead to severe wounds. Initially !! respond to incoming "" with varying degrees of aggression and tolerance, but often mate with multiple "" (up to five) in a given oestrous period. Influx "" copulate less frequently than the resident " (Cords 1984a, Struhsaker 1988). Only "" with full adult body size seen to copulate. Within a month after group takeover, the sole resident " sometimes kills (and eats) young infants. Loss of the suckling infant probably hastens the mother’s return to oestrus and increases the infanticidal male’s chance of siring offspring (Leland et al. 1984). Group members resist infanticide with counter-aggression

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Cercopithecus ascanius

Schmidt’s Red-tailed Monkey Cercopithecus ascanius schmidti subadult male.

(Struhsaker 1977). Newborns are highly attractive to older group members, especially adult !! and juveniles. Group members often nuzzle and handle infants but seldom remove them from their mother before 1–2 months of age. Attractiveness to group members diminishes as natal pelage disappears, although juveniles carry and cuddle older infants. Adult "" seldom interact directly with infants. Infants older than six months are seldom carried (Struhsaker & Pope 1991, Gathua 2000a). At least eight vocalizations recognized (Marler 1973, Struhsaker 1977, Gautier 1988). Adult "" give three loud-calls. Short coughlike ‘hack’ or ‘pop’ often given during group disturbances, repeated rapidly when group is alarmed, often interposed between ‘pyows’ of sympatric C. mitis "". ‘Ka’, a low-pitched (1.15–1.39 kHz) call given singly or in rapid sequence of 2–7 calls (average 4.1, n = 12, ‘ka-train’; Marler 1973), is usually a response to large raptors (Cords 1987b). Prolonged ‘waa’ nasal scream sometimes given during male–male fights (Struhsaker 1977, Cords 1984b). Female and juvenile calls lower in volume than those of adult "". ‘Phrased grunts’ given during and preceding active periods (feeding, moving). Shrill, bird-like ‘chirps’ often given repeatedly when alarmed by a predator or during territorial encounters. Searing, high-pitched ‘trills’ (3.93 kHz mean top frequency, range 2.6–5.0, n = 14; Marler 1973) given as submission signals and as vocal exchange when caller is alert but not moving quickly. During aggressive encounters, adult !! and juveniles often threaten each other with growls, and scream shrilly if attacked. Cercopithecus mitis have a similar vocal repertoire but C. ascanius calls generally lower in volume and higher-pitched. Cercopithecus ascanius often forms mixed-species associations with individuals or groups of other guenon species, and with Guerezas Colobus guereza, Ashy Red Colobus Procolobus rufomitratus tephrosceles and Grey-cheeked Mangabeys Lophocebus albigena (Cords 1987b, Chapman & Chapman 2000, Teelen 2007). In East Africa they avoid De Brazza’s Monkeys Cercopithecus neglectus and Robust Chimpanzees

Pan troglodytes (Struhsaker 1981a, Wahome et al. 1993). Solitary C. a. whitesidei sometimes travel with Gracile Chimpanzees (Bonobos) Pan paniscus (Maté et al. 1996). Associations reduce predation risk and facilitate finding food (Struhsaker 1981a, Cords 1987b). Behavioural interactions with association partners most often involve aggression but also include play and grooming (Struhsaker 1981a, Cords 1987b, Gathua 2000b). Because of relatively small body size, C. ascanius usually loses inter-specific aggressive confrontations with sympatric primates. Cercopithecus ascanius responds to alarm calls from sympatric monkeys, birds (e.g. Crested Guinea Fowls Guttera pucherani, Black-and-white-casqued Hornbills Bycanistes subcylindricus, Great Blue Turacos Corythaeola cristata) and duikers (e.g. Blue Duiker Philantomba monticola, Peter’s Duiker Cephalophus callipygus) (Struhsaker 1981a, T. Butynski pers. comm., M. Cords pers. obs.). Duikers and G. pucherani occasionally move beneath C. ascanius groups to eat dropped fruits (Struhsaker 1981a). Cercopithecus a. schmidti hybridizes with C. mitis in three forests in Uganda and one in Tanzania. Hybrids with C. m. stuhlmanni rare in Budongo F. R., Itwara F. R. and Kibale N. P., where only 2–10 hybrids were identified. Hybrids with Doggett’s Monkey C. m. doggetti much more common in Gombe Stream N. P. (18% of all individuals in groups including C. m. doggetti or C. ascanius). As deduced from physical appearance and ! hybrid maternity, hybrids are fertile, backcross with either parental species, and reside in groups of either parental type. In Kibale N. P., hybrids known to reside only in C. a. schmidti groups (Struhsaker et al. 1988). At Budongo F. R. and Gombe Stream N. P., hybrids are in groups of either parental species as well as in mixed-species groups (Aldrich-Blake 1968, Detwiler 2002, Detwiler et al. 2005, E. Sarmiento pers. obs.). Genetic studies documenting " hybrid paternity are wanting. Reproduction and Population Structure Females are in oestrus (accept and/or solicit copulation) for, on average, 6.9 days (1–28, n = 10 periods). Most !! solicit copulations more than once during an annual mating season of up to nine months, with ca. 11–60 day intervals of non-acceptance. Mating appears not to be closely tied to ovulation, and !! sometimes mate when pregnant (Cords 1984a). No external signs of ovulation or menses observed. Gestation length not known. Mean weight of C. a. katangae newborns is 257 g (245–265, n = 3) (E. E. Sarmiento pers. obs.). Births most common during 2–6 month period corresponding with end of wet season and subsequent dry season (Nov–Feb) for C. a. schmidti in East Africa (Cords 1984a, Butynski 1988), and end of dry season and subsequent wet season (Apr–Nov) for a compiled sample of C. a schmidti, C. a. katangae and C. a. whitesidei from around Bondo (03° 29´ N, 23° 24´ E), Kisangani (00° 19´ N, 25° 19´ E) and Kindu (02° 33´ S, 25° 33´ E), DR Congo (Gevaerts 1992). Peak birth periods correspond with high fruit and arthropod abundance in East Africa (Butynski 1988). Degree of birth seasonality can differ from group to group within a single forest, or annually for populations as a whole (Struhsaker 1997). In Kakamega Forest, !! are usually >4 years old when they first give birth (M. Cords pers. obs.), and are only known to give birth to one offspring. Inter-birth intervals average 54 months (49–60, n = 3) when previous infant survives >12 months, and 25 months (12–50, n = 3) when previous infant dies 2500 mm in the Niger Delta (where only Nov–Feb are relatively dry). Cercopithecus erythrogaster typically frequents the lower levels of the forest canopy, and dense tangled growth in canopy gaps and along rivers. Altitudinal range ca. 0–400 m.

Cercopithecus erythrogaster

Geographic Variation C. e. erythrogaster Red-bellied Monkey. S Bénin and far eastern edge of Togo. Ventrum bright rust-red. C. e. pococki White-throated Monkey. SW Nigeria and Niger Delta. Ventrum brownish-grey, sometimes with slight reddish tinge. Although the name ‘pococki’ was used on the label of the holotype in the British Museum (Natural History) by J. G. Dollman, and referred to by Napier (1981), it was not validated until 1999 (Grubb et al. 1999). Similar Species Cercopithecus petaurista. Not sympatric with C. erythrogaster, but present to the west from Senegal to W Togo. Nose-spot, ears, stripe below the ears and belly white. Cercopithecus sclateri. Possibly sympatric with C. e. pococki in east. SE Nigeria, between Niger R. and Cross R. Nose-spot and ears white. Muzzle pinkish. Ventral surface of proximal part of tail red. Distribution Endemic to E Togo, S Bénin and S Nigeria. Rainforest BZ. Restricted to dry and, particularly, moist forest. In Togo restricted to the Togodo Faunal Reserve (310 km2) adjacent to the Bénin border. In Bénin in Lama Forest (a forest relict in the Dahomey Gap), in Lokoli Forest, in several small forest patches in the lower Ouémé R. Valley (most of which are sacred groves), along Okpara R. and Mono R., and possibly at Banon (08° 29' N) (Oates 1996b, Sinsin et al. 2002a, Campbell et al. 2008b, Nobimè et al. 2009, 2011). In Nigeria on both sides of Niger R., from near IjebuOde in the west to Orashi R. at eastern edge of Niger Delta in east (Oates 1985, Powell 1995). On west bank of Orashi R., in vicinity of Upper Orashi F. R., there may be a hybrid zone between C. e. pococki and C. sclateri (see C. sclateri profile). Current distribution of C. e. pococki in Nigeria is probably similar to historical distribution, but populations are today greatly fragmented due to forest destruction for agriculture. Distribution of

Abundance Common in suitable habitat when hunting pressure is low. The second most frequently encountered monkey in Okomu N. P., SW Nigeria, where, in 1994 there were >30 ind/ km2 (Robinson 1994). In Okomu N. P., in 2008–09, 0.11 groups/ km (2.7 group/km2; Akinsorotan et al. 2011). In Lama Forest, ca.10.4 ind/km2 in ‘dense’ (= mature) forest and 7.5 ind/km2 in disturbed forest (Goodwin 2006). Throughout its range, however, C. erythrogaster is now generally rare due to intense commercial hunting. There are >3400 C. erythrogaster in the core of Okomu N. P. (the former Wildlife Sanctuary) (Robinson 1994), while estimates for the Lama Forest are 300–800 individuals (Kassa 2001, Campbell 2005, Goodwin 2006). Adaptations Diurnal and arboreal. Like other members of the C. (cephus) Group, this small, highly arboreal monkey is an agile quadruped, walking, running and climbing quietly through the forest on small and medium-sized supports. Cercopithecus erythrogaster appears to have high aural and visual acuity. Will quickly drop out of sight on detecting approaching humans, and creep away silently through the lower canopy (Robinson 1994). Foraging and Food Omnivorous. Foraging and feeding behaviour of C. erythrogaster have not been the subject of systematic study. In a few sightings of undisturbed wild animals in Nigeria, they forage (as a group) in a dispersed fashion, carefully searching for such food items as small fruits and insects (Oates 1985). In Lama Forest, fruit (especially Mimusops andongensis and Diospyros mespiliformis) is the predominant food item, while groups living in sacred groves raid farm crops (Sinsin et al. 2002b). Often in close association with other monkeys, especially Mona Monkey Cercopithecus mona; in 127 sightings of C.erythrogaster in Lama Forest, in association with C. mona on 50% of occasions (Goodwin 2006). Social and Reproductive Behaviour Lives in social groups, but group size not accurately measured; no groups yet habituated to humans, and the species is cryptic in its behaviour. In Nigeria most groups probably range in size from 5 to 20; average group size may be 34 mya, were found at a late Eocene site in the Fayum Depression in Egypt (Seiffert et al. 2003, 2005b). The phylogenetic relationships among lorisiforms remain ambiguous despite several attempts to resolve them with molecular, morphological and behavioural evidence. Adaptive radiation within the Galagidae is considerable – even within the same genus. Two genera (Euoticus and the squirrel galagos Sciurocheirus) are restricted to the moist forests of the Congo Basin and Gulf of Guinea, one (the dwarf galagos Galagoides) occurs across tropical Africa from the forests of West Africa and central Africa to the coastal forests along the east coast, and two (Otolemur and Galago) have representatives in tropical forests as well as in sub-tropical woodlands and bushlands. It remains unclear whether tropical forest forms colonized the sub-tropical regions, or the other way round. Molecular finding place the Otolemur–Galago split at 15.4 mya (midMiocene; Perelman et al. 2011). Taxonomic controversies have been considerable, undoubtedly because of the highly cryptic characteristics of museum specimens and the difficulties of studying galagos in the wild. Hill (1953: 211), for example, notes: ‘The classification of the Galagidae is a vexed question. There is no doubt that 5 main types or groups of galagos at present exist in Africa, but whether each of these is to be regarded as a nominal species or whether they should be treated as genera or sub-genera is difficult to decide.’ The groups in question are: 1 the large forms of the crassicaudatus type; 2 medium-sized forms, long-fingered, alleni type; 3 small forms typified by senegalensis type;

4 small forms with specialized, needle-pointed nails typifed by elegantulus type; 5 very small, mouse-like animals typified by demidovii type. The taxonomy of the group has come full circle, largely returning to the treatment proposed by Gray (1863) who was followed, on the basis of cranial and dental peculiarities, by Mivart (1864). The number of species recognized by most authors has risen from six in 1967 to >20 in 2009, mainly on the basis of their species-specific vocal profiles and correlated distinctions in penile morphology. The rate at which new species have been recognized over the past two decades suggests that several more species have yet to be uncovered (Bearder 1999). This volume presents profiles for 18 species of galagos within five genera: 1 2 3 4 5

Otolemur for the largest galagos Sciurocheirus for the long-fingered, forest understorey galagos Galago for the small leaping, long hind-limbed galagos Euoticus for the needle-clawed, gum-eating, forest galagos Galagoides for the dwarf, ‘running’, forest galagos.

No profile is presented here for the recently resurrected, and little known, Malawi Dwarf Galago Galagoides nyasae (Grubb et al. 2003, Nekaris & Bearder 2011). The genus Galagoides is the least consistent in terms of morphology, ecology and behaviour, representing a ‘wastebasket’ genus for the smallest galagos that may be separated further when more is known about their adaptations and genetics. Simon K. Bearder & Judith Masters

GENUS Otolemur Greater Galagos Otolemur Coquerel, 1859. Revue Zoologique, Paris 11: 458.

Mwera Greater Galago Otolemur sp. nov.? adult male.

Otolemur is a polytypic genus endemic to the woodlands and forests of the southern half of Africa. There are two currently-recognized and named species; Small-eared Greater Galago O. garnettii and Largeeared Greater Galago O. crassicaudatus (Olson 1979). A third species, Miombo Silver Greater Galago O. monteiri, is sometimes recognized

(Groves 2001, 2005c, Grubb et al. 2003, Nekaris & Bearder 2011). This volume follows Olson (1979) and Jenkins (1987) in recognizing two species. Otolemur garnettii and O. crassicaudatus can be distinguished based on a number of characters, including body size and vocal profile. Distributed throughout most of eastern and south-eastern Africa from coastal S Somalia in the north to KwaZulu–Natal in SE South Africa. From Angola eastwards through Tanzania. Northern distribution limited by the forests of the Congo Basin and deserts of N Kenya and S Somalia. In southern Africa, Otolemur does not penetrate the peripheral habitats of the Namib Desert, Kalahari Desert or High Veld of South Africa (Olson 1979, Nash et al. 1989, Kingdon 1971, 1997, Groves 2001) . A thorough review of the systematic history of the genus Otolemur is provided by Olson (1979). He describes this genus as part of his detailed morphological study of >4000 specimens. His diagnosis (p. 328) for dentally mature individuals is as follows: ‘Head plus body length greater than 23 cm, hind foot greater than 8 cm, body weight over 500 grams, cranial length greater than 5.5 cm, length of upper pre-molar-molar series greater than 1.85 cm 407

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Family GALAGIDAE

Small-eared Greater Galago Otolemur garnettii.

and length of lower pre-molar-molar series greater than 1.65 cm. Cranial features associated with masticatory musculature well developed: marked postorbital constriction, robust zygomatic arches, deep maxillary root of zygomatic bone, relatively long zygomatic arch posterior to postorbital process, large lateral pterygoid plates, coronoid and angular processes of the mandible robust. Foramen magnum directed posteriorly, minimum basicranial flexion, fissure between orbital and temporal fossae large, palatine canals tiny, large triangular area of the horizontal plate of the palatine bones posterior to M3. Lingual margins of maxillary tooth rows parallel or only

slightly divergent posteriorly. Muzzle large and robust, broad not pointed. Molars and P4/4 with low rounded cusps, crowns lacking prominent crests. Diploid number 62. Glans penis clavate, gradually incrassate from base to truncated tip, the tip obliquely inclined from its superior surface downwards. Extraocular recti muscles inserted around equator of eyeball. Pronograde quadruped. Lateral surfaces of limbs more or less the same colour as dorsal body pelage. Dark circumocular rings and light coloured interocular stripe absent. Skin between palmar and plantar pads granular. Caecum unsacculate and rather small’.

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Otolemur crassicaudatus

Large-eared Greater Galago Otolemur crassicaudatus.

Olson (1979) provides a detailed description of the genus and a comprehensive list of features that distinguish Otolemur from each of the other genera within the Galagidae, of which the most obvious is their larger body size. Other characteristics that he describes include an intermembral index of 65–70; digital formulae IV>III>V>II>I; pedal digit II with toilet-claw; tarsal elongation not as pronounced as in most other galagos; overall colouration of limbs similar to body, lacking bright golden or yellowish colours; tail long and bushy; ventral and dorsal body pelage of different colours except in melanistic individuals; large areas of glandular skin frequently present in scrotal, pectoral and submental regions of mature adults. Male external genitalia with long and slightly curved penis, which gradually thickens towards the tip, glans penis covered with either unidentate or tridentate spines, urethral opening situated in triangular depression below projecting baculum, tip of baculum and urethra surrounded by wrinkled collar; " external genitalia with long thick clitoris, large labia with fine lamellae that converge towards the vagina. Dentition: I 2/2, C 1/1, P 3/3, M 3/3; deciduous dentition i 3/3, 1 c /1, m 3/3; molariform teeth of both jaws with low rounded cusps and not exhibiting prominent crests between cusps. Postcranial skeleton rather generalized except for elongation of hindlimb, and the calcaneus and navicular elements of the tarsus. Simon K. Bearder

Otolemur crassicaudatus LARGE-EARED GREATER GALAGO (THICK-TAILED GREATER GALAGO / BUSHBABY) Fr. Galago à queue touffue; Ger. Großohr-Riesengalago Otolemur crassicaudatus (É. Geoffroy, 1812). Ann. Mus. Hist. Nat. Paris 19: 166. Quelimane, Mozambique.

Large-eared Greater Galago Otolemur crassicaudatus adult male.

Taxonomy Polytypic species. Olson (1979) focused on the genus Otolemur and his classification, based on measurements from 4949 galago specimens (including all type specimens) from museums and private collections in Europe, Africa and North America, is used here. This species was referred to as Galago

crassicaudatus in most classifications prior to 1979, with garnettii as a subspecies (Hill 1953, Napier & Napier 1967, Groves 1974, Petter & Petter Rousseaux 1979). Recognition of two species belonging to the genus Otolemur (O. crassicaudatus and Smalleared Greater Galago O. garnettii) was established by Olson and substantiated by Jenkins (1987), Clark (1988), Zimmermann (1990), Masters (1991) and DelPero et al. (2000). Each species has a distinctive vocal profile (Bearder et al. 1995) with no obvious vocal differences among the subspecies. Olson (1979) recognizes three subspecies, O. c. crassicaudatus, O. c. monteiri and O. c. argentatus, whereas Kingdon (1997) recognizes argentatus as a species, and Groves (2001, 2005c), Grubb et al. (2003) and Nekaris & Bearder (2011) recognize monteiri as a species. This volume follows the taxonomy of Olson (1979). Honess (1996b), Kingdon (1997), Groves (2001), Grubb et al. (2003) and Nekaris & Bearder (2011) recognize a ‘dwarf’ form of Large-eared Greater Galago (Mwera Greater Galago Otolemur sp. nov.?) based on a population of extremely small individuals (50 ind/km² at forest/beach ecotone, but much less than this in the forest interior (T. Butynski & Y. de Jong pers. comm.). Adaptations Nocturnal and arboreal. Hindlimbs slightly longer than forelimbs but quadrupedalism is the norm; unable to land feet first when leaping (Bearder 1974, Olson 1979, Crompton 1983, 1984, Nash et al. 1989). Least agile of the galagos, generally walking or running along the top of broad, horizontal supports, or on the ground (sometimes over 100 m). Able to leap 3 m between trees and hop along the ground bipedally if distressed. Frog-like, quadrupedal hopping on the ground appears unique to O. crassicaudatus. Ability to maintain a grip when hanging upside-down beneath a wide horizontal branch to reach gum is remarkable (Bearder & Doyle 1974a, Crompton 1983). Most common sleeping site is dense tangles of creepers and branches at a height of 5–12 m above ground. At one site in Mahale N. P. some sleep among the dense fronds at the top of >10 m high Oil Palms (T. Butynski &Y. de Jong pers. comm.). Adult "" make nests when they have infants – inaccessible leafy platforms, depressed in the middle with foliage above for shelter (Bearder & Doyle 1974a). Individuals have more than one sleeping site and are not known to move away from a sleeping site during the day (Bearder & Doyle 1974a). Caves and roof spaces in human dwellings also used as shelters. Chest glands produce three major volatile compounds, which are different from those of O. garnettii (Katsir & Crewe 1980, Clark 1988). Foraging and Food Omnivorous. Diet comprised of invertebrates, fruit and gum. Individuals follow regular pathways to reach well-known sources of gum or fruiting trees (Bearder & Doyle 1974a). Usually forages alone when searching for small sources of gum and insects (Clark 1985), but move as a group where large fruit trees are common (Bearder 1974). In South Africa, trees that 411

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Lateral and palatal views of skull of Large-eared Greater Galago Otolemur crassicaudatus adult male.

produce abundant gum from established wounds (usually Sweet Thorn Acacia karoo) are visited regularly, particularly during the cold, dry winter (Harcourt 1986b, Nash & Weisenseel 2000). In NE South Africa, diet includes 33% fruit, 62% gum and 5% invertebrates where fleshy fruit is readily available (Bearder 1974) but 41% gum and 59% invertebrates where fruit is absent (Clark 1985). Flowers, seeds, nectar and millipedes also consumed (Coe & Isaac 1965, Crompton 1984, Clark 1985, Harcourt 1986b). Feed on hard-shelled and woody, dried fruits in South Africa (Masters et al. 1988), and arthropods from the orders Coleoptera, Orthoptera, Hymenoptera, Odonata, Chilopoda and Isoptera. Millipedes (Diplopoda) taken during the summer months (Harcourt 1986b). Termites, Macrotermes sp., eaten in Malawi (Happold & Happold 1992). Fish captured from a basin and eaten in captivity (Welker 1976). Many reports of birds being captured in the wild and their brains eaten. This, however, is probably a local tradition as it appears to be absent from some populations (Bearder 1974). Water is obtained from the diet or by licking dew. Social and Reproductive Behaviour Dispersed groups. Most gregarious of all galagos, probably related to large body size and diet. Where fruit is abundant, the young stay with the mother during the long period of immaturity (15 months) and they frequently move with her as a cohesive group. If an individual becomes separated from the group, it, unlike any other galago, gives a ‘buzz’ call until reunited (Bearder 2007). Cohesive groups not formed where food sources are scattered in small clumps (Clark 1985, Bearder 1987). Grouping also occurs at sleeping sites during the day when a mother and up to three offspring may be joined by an adult !. Adult "" occupy separate territories, which they share with their offspring of one or more generations. The sex ratio at birth appears to be biased towards !!. This has been interpreted as an adaptation to reducing competition for food resources (gum) that are shared among related "". Males on the other hand tend to disperse (Clark 1978b). Male ranges are larger and overlap those of "". Adult "" occupy adjacent territories that are visited by up

to six adult !!. Young adult !! have less frequent access to the "" but all age/sex classes engage in amicable social interactions, especially grooming, with the exception of territorial !!, which never come together. Juveniles engage in object play, locomotor play and social play, including group play between a mother, two juveniles and an adult ! (Bearder 1974). Females may have mating access to up to six !! during their oestrus (3–5 days) once each year, indicating a polygynandrous (multimale/multifemale) mating system (Clark 1985). Oestrus periods are synchronized within populations during two weeks during winter (Jun/Jul). Prolonged copulation is common (up to 45 minutes) and has been interpreted as a form of mate-guarding (Dixson 1995). At parturition, "" may become unusually aggressive to cage-mates (including previous offspring) and mothers cease to join their usual sleeping partners (Bearder & Doyle 1974a, Bearder 1987). Communication involves a wide range of auditory, visual, tactile and olfactory signals, including 18 structurally distinct calls (Bearder 1974, Clark 1978a, 1988, Petter & Charles-Dominique 1979, Masters 1991, Bearder 2007). The loud child-like cries, audible at 300 m, are the origin of the name ‘bushbaby’. Raucous whistles, yaps and cackles of alarm are also given. Conspicuous scent-marking behaviours include cheek-rubbing, chest-gland-rubbing, ano-genital rubbing, rhythmic urination, urine-washing of the hands and feet, and foot-rubbing, which is peculiar to Otolemur (Welker 1973, Clark 1982a, b, 1988). An individual will rub the roughened area of the sole of one foot against a branch and then the other, making a distinctive scraping noise (Bearder & Doyle 1974a). Foot-rubbing is done mainly by adult !! and may accompany urine-washing, rhythmic urination and chest-gland-marking when disturbed in social situations or in the presence of a predator (Bearder 1974, Hager 2001). Chest-gland-marking by adult !! in captivity is testosterone-dependent (Bullard 1984). Reproduction and Population Structure Gestation is 132.8 ± 2.6 days (n = 3) in the wild (Bearder 1974). Of 20 pregnancies in captivity, six (30%) resulted in singletons and 14 (70%) multiple births, two of which were triplets and 12 twins (Masters et al. 1988). In South Africa there is a single birth season during Nov which coincides with the start of the rains (Bearder & Doyle 1974a). In E Zimbabwe (Smithers & Wilson 1979) and Zambia (Ansell 1960) births occur in Aug/Sep. No defined birth season observed in captivity. Infants born in nests, which, at other times, are used as resting places. Just before giving birth the " relines the nest with fresh green leaves and twigs. At birth the neonate weighs ca.40 g, the eyes are open. Neonate can crawl within 30 min of birth. At first the mother carries each infant, one at a time, in her mouth, holding it by a fold of skin on the flanks or by the back. After about eight days up to three infants may cling to their mother’s back. At about three days infants vocalize by giving ‘squeaks’, and at nine days emit ‘clicks’ and ‘crackles’. In the wild the young travel with the mother after about 25 days of age, either following her or being carried (Bearder 1974). Lactation lasts around ten weeks (Bearder 1974). Mother–infant cannibalism can occur in captivity after the death of an infant (Tartabini 1991). Young move independently after 17 weeks. Maximum longevity in captivity is about 15 years (Doyle 1979).

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Predators, Parasites and Diseases Robust Chimpanzee Pan troglodytes is a predator of O. c. monteiri (Uehara 1997). Other predators include Leopards Panthera pardus, large owls Bubo spp., large snakes and genets Genetta spp. (Crompton 1984). A wide variety of parasites and pathogens reported for prosimians in captivity although they have few health problems in captivity (Kohn & Haines 1982, Benirschke et al.1985).

HF (!!): 93 (84–101) mm, n = 15 HF (""): 83 (80–88) mm, n = 5 E (!!): 61 (54–65) mm, n = 15 E (""): 55 (49–63) mm, n = 4 WT (!!): 1270 (550–1650) g, n = 9 WT (""): 740, 740 g, n = 2 Former Transvaal, South Africa (Rautenbach 1982)

Conservation IUCN Category (2012): Least Concern. CITES (2012): Appendix II. The conservation status of O. c. argentatus is of considerable concern as most of the habitat of this isolated subspecies has been destroyed by human activities (N. S. Svoboda & D. Roberts pers. obs.). The population identified by Olson (1979) in the Kahemba District, SE DR Congo (see Geographic Variation), is in particular need of study.

O. c. crassicaudatus TL (!!): 681 (640–710) mm, n = 10 TL (""): 619 (590–637) mm, n = 3 T (!!): 359 (280–430) mm, n = 10 T (""): 325 (300–345) mm, n = 3 KwaZulu–Natal, South Africa (Taylor 1998)

Measurements Otolemur crassicaudatus HB: 313 (255–400) mm, n = 360 T: 410 (300–550) mm, n = 357 HF: 93 (70–108) mm, n = 340 E: 62 (48–72) mm, n = 344 WT: 1131 (567–1814) mm, n = 157 Data from numerous museums. All subspecies represented in this sample (Olson & Nash 2002); sexes combined O. c. crassicaudatus TL (!!): 712 (630–785) mm, n = 16 TL (""): 588 (501–715) mm, n = 5 T (!!): 383 (350–440) mm, n = 16 T (""): 319 (285–388) mm, n = 5

O. c. monteiri TL (!!): 739 (685–798) mm, n = 23 TL (""): 727 (685–780) mm, n = 12 T (!!): 416 (360–450} mm, n = 23 T (""): 407 (355–450) mm, n = 12 HF (!!): 96 (90–101) mm, n = 23 HF (""): 91 (84–100) mm, n = 13 E (!!): 60 (54–65) mm, n = 23 E (""): 59 (53–65) mm, n = 13 WT (!!): 1220 (940–1640) g, n = 24 WT (""): 1130 (990–1460) g, n = 13 Zimbabwe (Smithers & Wilson 1979) Key References Bearder & Doyle 1974a; Clark 1985; Harcourt 1980; Masters 1985; Olson 1979. Simon K. Bearder & Nadine S. Svoboda

Otolemur garnettii SMALL-EARED GREATER GALAGO (GARNETT’S GALAGO / BUSHBABY) Fr. Galago de Garnett; Ger. Kleinohr-Risengalago Otolemur garnettii (Ogilby, 1838). Proc. Zool. Soc. Lond. 1838: 6. Zanzibar I., Tanzania (designated by Thomas 1917).

Taxonomy Polytypic species. Originally called Otolicnus garnettii by Ogilby (1838), with no provenance given to the type specimen; the type locality was designated by Thomas (1917: 48) to be Zanzibar I. (now Unguja I.). Since then, numerous synonyms for both the generic and specific name have been used (for details see Olson 1979). Until recently, this taxon considered a subspecies of Otolemur (also called Galago) crassicaudatus (e.g. Hill 1953, Petter & Petter-Rousseaux 1979). This taxon now generally accepted to be a full species (Olson 1979, Harcourt 1984, Jenkins 1987, Masters 1988, Nash et al. 1989, Groves 2001, 2005c, Grubb et al. 2003, Nekaris & Bearder 2011). Following Groves (2001, 2005c) and Grubb et al. (2003), four subspecies are recognized. Chromosome number: 2n = 62 (Masters 1986, Jenkins 1987, Groves 2001). Synonyms: agisymbanus, hindei, hindsi, kikuyuensis, lasiotis, panganiensis. Small-eared Greater Galago Otolemur garnettii.

Description Relatively large galago (size of small domestic cat) with long bushy tail. Second largest galago. Occurs in forests. 413

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Sexes alike, but !! slightly heavier than "". Head colour varies with colour of dorsum (see below), but may have a whitish face (A. Perkin & T. Butynski pers. obs.) Muzzle blunt and dog-like. Forehead sometimes with darker vertical furrow. Eye-rings not obvious. Ears small relative to size of head and to other galagos. Dorsum varies from reddish-brown to greyish-brown to silvery (Olson 1979, Nash et al. 1989), sometimes with a greenish tinge (Groves 2001). Ventrum varies from creamy-white to buff-brown. Tail colour highly variable even within same population (Harcourt 1984). Generally proximal half, or more, of tail is same colour as dorsum, with distal half, or less, varying from black, dark brown to white. Chin, throat and ventrum generally same colour as distal part of tail (Y. de Jong & T. Butynski pers. comm.). Nails are convex. Penile spines usually tridentate, with some bidentate. Baculum elongated, extending beyond glans penis (Dixson 1989, 1995). Photographs of O. garnettii from Kenya and Tanzania available at: www.wildsolutions.nl Geographic Variation O. g. garnettii Zanzibar Small-eared Galago. Zanzibar I., Pemba I. and Mafia I. Dorsum rich reddish-brown. Ventrum yellow, slightly greenish toned. Tail almost black over distal half (Jenkins 1987, Groves 2001). O. g. panganiensis Pangani Small-eared Galago. Loita Hills and at Tavetta, extreme SC Kenya, Tanzania from Tanga, Mt Kilimanjaro, Mt Meru and L. Manyara to south (right) bank of Ruvuma R., extreme N Mozambique (Olson 1979). Dorsum greyish-brown, sometimes with yellow wash. Lacking greenish tones. Ventrum grey-white. Tail usually brown or dark brown over distal quarter (Jenkins 1987, Groves 2001), but sometimes whitish at tip (e.g. Usa R., Mt Meru;Y. de Jong & T. Butynski pers. comm.). O. g. lasiotis White-tailed Small-eared Galago. Juba R., Somalia, south along Kenya and Tanzania coasts to Tanga. Inland to Taita Hills and Kibwezi, Kenya (Jenkins 1987, Groves 2001). Dorsum greyish, greyish-brown or silvery. At Diani, extreme SE Kenya, dorsum varies from dark brown to pale brown. Individuals at WatamuGedi, central coast of Kenya, are exceptionally variable in colour (Olson 1979, De Jong & Butynski 2009). Ventrum greyish-white; always paler than dorsum. Distal half or less of tail highly variable, ranging from black, dark brown to white, even at the same locality (Harcourt 1984, De Jong & Butynski 2009). O. g. kikuyensis Kikuyu Small-eared Galago. Kenya Highlands, east of the Eastern Rift Valley; Nairobi, Ngong, Masinga, Aberdares and Mt Kenya. Dorsum grey, often iron grey, with a tinge of green. Muzzle, eye-rings, ears, hands and feet blackish. Ventrum yellowwhite. Tail very full, light brown, often nearly black over distal quarter, but sometimes with whitish tip (Groves 2001, De Jong & Butynski 2009). Similar Species Otolemur crassicaudatus. Narrowly sympatric or parapatric on the coast of East Africa from Mombasa (e.g. Kaya Teleza; A. Perkin pers. obs.), SE Kenya, to N Mozambique. Sympatric in Loita Hills, SC Kenya (Butynski & De Jong 2012). Also sympatric in Tanzania from Usambara Mts to Ngorongoro Crater (Nash et al. 1989). Larger with mean weight of adult !! ca. 1250 vs. 900 g for O. garnettii. Ears larger, and larger relative to the head (ca. 60

Small-eared Greater Galago Otolemur garnettii adult male.

vs. 46 mm). Pelage greyer. Loud ‘trailing call’ (or ‘cry’) distinctive (Nash et al. 1989, Bearder et al. 1995). Confusion between these two species makes the earlier literature difficult to interpret. Distribution Endemic to eastern Africa. Somalia–Masai Bushland and Coastal Forest Mosaic BZs. In coastal and riverine forests from Jubba R., Somalia, south to N Mozambique. Northernmost record is in the Mathews Range, C Kenya (01° 15´ N, 37° 18´ E, 1414 m; De Jong & Butynski 2010a). On Manda, Pemba, Zanzibar and Mafia Is. Inland in forests of Kenya Highlands east of Eastern Rift Valley, Tsavo, Taita Hills, Chyulu Hills, Mt Kasigau, Mt Kilimanjaro, Mt Meru, L. Manyara and most Eastern Arc Mts (Olson 1997, De Jong & Butynski 2009, A. Perkin pers. obs.). Only known site in Southern Highlands is Milo Forest (Honess 1996b, A. Perkin & T. Davenport pers. obs.). Although the map in Nash et al. (1989) shows O. garnettii in the Udzungwa Mts, SC Tanzania, there is not yet evidence of this (Honess 1996b, Butynski et al. 1998, Perkin 2001) except for Mbatwa riverine forest in north Udzungwa Mountains N. P. (Rovero et al. 2009). Olson (1979) indicates that O. garnettii panganiensis occurs just south of the Ruvuma R. in extreme N Mozambique, and that it may occur farther south. See Geographic Variation. Habitat In forested and forest-agriculture mosaic from sea level to 2000 m, rarely higher; in Tanzania to 2400 m on Mt Kilimanjaro (Grimshaw et al. 1995) and in Kenya to 2290 m on Aberdares Range (M. Dodds pers. comm. to Y. de Jong). Mean annual rainfall over geographic range ca. 600–1500 mm (Olson 1979, Y. de Jong & T. Butynski pers. comm.). Gedi and Diani coastal forests, Kenya, are lowland, dry forest on coral rag (Moomaw 1960). These forests are multistratal, often with a thick understorey, a canopy at 15–20 m, mostly of Combretum schumannii, and emergents to 25 m (Harcourt & Nash 1986b). In submontane and montane forests of Mt Kenya, Aberdares Range, Mt Meru, Mt Hanang and Eastern Arc Mts, O. garnettii is most common at forest edges and in secondary vegetation (A. Perkin,Y. de Jong & T. Butynski pers. obs.).

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Otolemur garnettii

Abundance In Diani and Gedi Forests, Kenya, ca. 31–38 ind/km2 (Nash & Harcourt 1986). Brief foot and/or vehicle surveys of >20 sites in Kenya and Tanzania yielded encounter rates of 1–5 ind/h, with highest rates in Kenya at Tana River Primate National Reserve, Meru F. R., Ngaia F. R. and Diani (De Jong & Butynski 2009), and in Tanzania at Ngezi-Vumawimbi Nature F. R. (NW Pemba I.), Zanzibar I., Arusha, Zaraningi Forest (in Sadaani N. P.) and L. Manyara (Y. de Jong & T. Butynski pers. comm.). Adaptations Nocturnal and arboreal. Day spent sleeping in tangled vegetation in tall bushes or trees. Not known to use treeholes. Loud ‘trailing call’ given by both sexes to announce their presence to conspecifics; most other calls are associated with alarm situations (Harcourt 1984, Bearder et al. 1995). Predator and prey detection and localization are associated with well-developed visual and hearing systems. Olfactory communication is important: urinewashing and chest- and foot-rubbing. Glands on chest and abdomen produce an oily, yellowish apocrine secretion (Kingdon 1997). Both sexes have spiky patches on soles of the hindfeet, which are used to rub a substrate and generate sound (Hager 2001). Locomotion in O. garnettii is quadrupedal; when leaping it usually lands hindfeet first, or on all four feet (like O. crassicaudatus) (Harcourt 1984); bipedal hopping when on the ground (Harcourt 1984, Harcourt & Nash 1986b). On Mt Kilimanjaro, shows a preference for horizontal supports in mature trees; 51% of 420 observations on horizontal supports and 42% of 527 observations at >10 m in canopy (Svoboda 1999). Foraging and Food Omnivorous. Forages mostly in trees, rarely on ground. About half of the time spent above 5 m (Harcourt & Nash 1986b). Mostly forages alone, though several animals may congregate in fruiting trees (Nash & Harcourt 1986, A. Perkin pers. obs). Faecal samples indicate that diet at Diani is ca. 50% animal matter and 50% fruit. Fruits eaten include Ficus spp., Grewia sp.,

Lateral, palatal and dorsal views of skull of Small-eared Greater Galago Otolemur garnettii adult male.

Lannea stuhlmanni and Vitex strickeri (Harcourt 1984, Harcourt & Nash 1986b). Stomach samples indicate that 50% of diet is of animal matter and 50% is fruits and seeds (Masters et al. 1988). Invertebrates make up the majority of animal matter, mostly beetles, orthopterans and centipedes. Spiders, ants, caterpillars, millipedes, heteropterans, snails and termites also eaten. Observed feeding actively on invertebrates disturbed by swarming army ants (= safari ants = driver ants) Dorylus sp. (T. Butynski & Y. de Jong pers. comm.). Birds taken on occasion and probably include, at Diani, Kenya Crested Guinea Fowl Guttera pucherani (Harcourt & Nash 1986b). Also forages in farmland, taking Bananas Musa sp., Breadfruit Artocarpus altilis, Mangos Mangifera indica, Papaw Carica papaya and other fruit crops, plus Coconut Palm Cocos nucifera sap, which is tapped by local people for the manufacture of ‘palm wine’ (Masters et al. 1988, A. Perkin pers. obs.). Social and Reproductive Behaviour Solitary. Mean homerange size at Gedi and Diani, calculated from trapping, radiotracking and sleeping site data is 12.0 ha (10.8–13.0, n = 4) for adult "" and 17.1 ha (16.6–17.8, n = 3) for adult !!. Homeranges of resident adult !! overlap slightly or not at all, though they overlap ranges of younger !!. Transient !! move through the home-ranges of resident !! and "". Same-age "" also tend to have non-overlapping home-ranges, though they can share homeranges with others, which are probably relatives. At Gedi both sexes travel, on average, 1.6 km/night; at Diani one radio-collared adult ! travelled, on average, farther than the one radio-collared adult ", 3 km and 1.8 km, respectively. Adults spend most of the night alone and, usually, sleep alone as well, though grooming and play between individuals occurs. The apparently less social behaviour of this species, compared with O. crassicaudatus, may be due to fewer infants 415

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being born (O. crassicaudatus frequently has twins or triplets and many of the interactions seen are between adults and youngsters), or to differences in diet (Nash & Harcourt 1986). Otolemur garnettii has an extensive vocal repertoire, with 12 spectrographically different call types used by adults of both sexes (Harcourt 1984, Zimmermann 1990, Bearder et al. 1995, Honess 1996b, Becker et al. 2002). The loud ‘trailing call’ starts with two lower frequency introductory units followed by 5–8 units, which are repeated and trail away. Alarm calls – ‘squawks’, ‘chatters’ and ‘cackles’ – given frequently, are mostly repetitive and are generally not replied to. Low frequency ‘growls’ given in a state of anxiety. Other calls recorded in captivity are the low frequency ‘flutter/hum’ and ‘short growls’, high frequency ‘infant clicks’, and high frequency adult ! ‘clicks’ and ‘spits’ (Becker et al. 2002). Little is known about the mating system of O. garnettii. Dixson (1998) suggests O. garnettii has a ‘dispersed’ multimale-multifemale mating system inferred from social organization, copulatory patterns and mating activity in captivity, as well as complex penile morphology and large testes. Non-receptive "" avoid !!. Males initiate copulations with receptive "". Copulations are lengthy with intromission lasting 13–260 min; this may be related to mateguarding (Dixson 1998). In the wild it is thought that olfactory cues play an important role in signalling the sexual condition of the " and in attracting mates in the nocturnal non-gregarious society of O. garnettii (Dixson 1998). Reproduction and Population Structure Not well known. It appears that in the Kenyan coastal forests, infants are born Aug– Nov with "" giving birth once per year (Nash 1983, Harcourt 1984). Of 95 pregnancies in captivity, 91 (96%) yielded singletons, while four (4%) yielded twins (Izard & Simons 1986). Mothers transport infants in their mouths and ‘park’ them when foraging. In captivity, ovarian cycle is 39–59 days (mean 44), oestrus 7–24 days (mean 12.4), and there is a restrictive phase of receptivity of 2–10 days (mean 5.8) with a peak of 1–2 days (Eaton et al. 1973). Eaglen & Simons (1980) give gestation in captivity as 119–138 days. Predators, Parasites and Diseases Predators probably include large snakes, genets Genetta spp., Two-spotted Palm Civets Nandinia binotata, large owls Bubo spp. and monkeys. When a potential predator is located, O. garnettii mobs the predator while emitting a series of loud ‘squawks’ that can go on for >40 minutes (Honess 1996b, A. Perkin pers. obs.). Other conspecifics generally do not join in this behaviour but may gather round. Prey avoidance strategies enabled by excellent hearing, smell and vision combined with rapid arboreal locomotion skills and cryptic colouration. Will move around during the day when disturbed by humans (A. Perkin pers. obs.).

Conservation IUCN Category (2012): Least Concern. CITES (2012): Appendix II. The discontinuous distribution and small size of many of the forests in which O. garnettii occurs makes this species vulnerable to clearing for agriculture, logging, settlement and tourism. This is especially the case along the coast and on Zanzibar I. In many areas, killed as a presumed agricultural pest and a symbol of bad luck. Hunted for meat in several localities, such as in the Makonde tribal area, SW Tanzania. There is small-scale collecting for the pet trade (Perkin 1998, A. Perkin pers. obs.). Measurements Otolemur garnettii HB: 266 (230–338) mm, n = 368 T: 364 (308–440) mm, n = 363 HF: 91 (80–103) mm, n = 359 E: 45 (34–55) mm, n = 356 WT: 767 (550–1040) g, n = 269 Data from numerous museums. All subspecies represented in this sample (Olson & Nash 2002). Sexes combined O. g. lasiotis HB (both sexes): 278 (260–294) mm, n = 7* T (both sexes): 360 (330–410) mm, n = 14** WT (!!): 846 (690–1060) g, n = 14 WT (""): 805 (604–985) g, n = 11 Gedi and Diani, Kenya (Nash & Harcourt 1986) *Gedi; **Diani O. g. lasiotis HB (!!): 295 (270–350) mm, n = 4 HB (""): 284 (280–291) mm, n = 3 T (!!): 340 (330–350) mm, n = 4 T (""): 319 (314–323) mm, n = 3 HF (!!): 90 (85–94) mm, n = 4 HF (""): 84 (82–88) mm, n = 3 E (!!): 47 (43–54) mm, n = 4 E (""): 46 (45–47) mm, n = 3 WT (!!): 916 (820–990) g, n = 4 WT (""): 755 (650–815) g, n = 3 Taita Hills, Kenya (Perkin et al. 2002) Key References Harcourt 1984; Harcourt & Nash 1986b; Nash & Harcourt 1986; Olson 1979. Caroline S. Harcourt & Andrew W. Perkin

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GENUS Sciurocheirus Squirrel Galagos Sciurocheirus Gray, 1873. Proc. Zool. Soc. Lond. 1872: 857 [1873].

Lateral, palatal and dorsal views of skull of Bioko Squirrel Galago Sciurocheirus alleni alleni adult.

Squirrel galagos or the ‘Allen’s Galago Group’ have generally been treated as Galago by most recent authors, although Gray (1873) erected a separate genus, Sciurocheirus (squirrel galagos) for S. alleni. Masters et al. (1994) and Crovella et al. (1994) have, on the basis of genetic similarities, allied this species with the greater galagos Otolemur spp. Bayes (1998) found considerable genetic differences between Otolemur and Sciurocheirus, implying an ancient separation. He placed this divergence at ca. 37 mya (mid-Eocene). Sciurocheirus spp. differ considerably from Galago spp. in skull shape (Hill 1953), anatomy of the foot (Jouffroy & Gunther 1985) and vocal repertoire, including the loud call (Ambrose 2003). Taxonomic placement of the squirrel galagos has been a recurrent problem. Jouffroy & Gunther (1985) showed that, in their locomotor anatomy and in their behaviour, the squirrel galagos stood well apart from all other galagos. Bearder et al. (1995) categorized the alleni Group within the Galago senegalensis/moholi and matschiei Group. Groves (1989, 2001) recorded

his misgivings in placing these distinctive animals in Galago but could find no clear affinity with any other group of galagos. In their most recent molecular study Masters et al. (2007) contend that the closest genetic affinities of these galagos are with Otolemur, not Galago. This discovery is currently the focus for various re-appraisals of both genera, in the hope of a better diagnosis of their common ancestry and a more refined appreciation of galago evolution. Groves (2001, 2005c) designated three allopatric forms as full species: Allen’s Squirrel Galago Galago alleni, Cross River Squirrel Galago G. cameronensis and Gabon Squirrel Galago G. gabonensis. Ambrose (2003) and Grubb et al. (2003) follow Gray (1873) in placing the squirrel galagos in the genus Sciurocheirus. Ambrose (2003) considers the loud call repertoires of alleni and cameronensis to be identical, thereby invalidating the specific distinction for cameronenis. There is, however, a significant difference in body weight, with alleni being about one-third heavier than cameronensis. On this basis, Ambrose (2003) retained cameronensis as a subspecies of S. alleni. A third species of Sciurocheirus, with a distinct vocal repertoire, facial markings and pelage colouration, was discovered in 1993 in the Makandé region, C Gabon, and is formally described and named here for the first time. Sciurocheirus is a genus of medium-sized forest galagos with a distinct preference for feeding on or close to the floor in forests between the Niger R. and Congo R. These are greyish-brown galagos with russet tinges on the limbs.The pointed muzzle has a pale median stripe and the reddish eyes are set within well-defined mask-patches. Nipples = 2 + 2 + 2 = 6. Sciurocheirus bound from one vertical support to another, clinging and leaping like a tree-frog. They land hands first, unlike other galagos, which land feet first or with all limbs simultaneously. Given that their closest genetic relationship appears to be with Otolemur (Masters et al. 2007), there is the implication that their common ancestor had a wider ecological and geographic range than either descendant lineage. Furthermore, their current occupation of a restricted ecological niche in a restricted geographic region suggests contraction from a wider range of habitats and behaviours. The co-existence and probable competition of five other lorisoids might have influenced just such a contraction and refinement of niche. There are interesting implications for ‘use of space’ by these galagos, for understanding their preferred foraging zones and the physical structure of their micro-environment. Colin P. Groves & Jonathan Kingdon

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Sciurocheirus alleni ALLEN’S SQUIRREL GALAGO Fr. Galago d’Allen; Ger. Allen-Buschwaldgalago Sciurocheirus alleni (Waterhouse, 1838). Proc. Zool. Soc. Lond. 1837: 87 [1838]. Fernando Po (= Bioko I.) Equatorial Guinea.

Sciurocheirus alleni

Bioko Squirrel Galago Sciurocheirus alleni alleni.

Taxonomy Polytypic species. Gray (1873) placed this species in a new genus, Sciurocheirus (squirrel galagos), but most recent authors (Jenkins 1987, Kingdon 1997, Groves 2001, 2005c) have kept alleni with the lesser galagos Galago. This species is, however, distinct from Galago in a number of characters, including the proportions of the skull (Hill 1953) and foot (Jouffroy & Gunther 1985). The vocalizations are also distinct from all other galagos (Ambrose 2003). Recent genetic studies place alleni in a clade with the greater galagos Otolemur spp. (Crovella et al. 1994, Masters et al. 1994, 2007). According to Bayes (1998), there is considerable genetic divergence between the squirrel galagos and the greater galagos, emphasizing their taxonomic distinctiveness; based on this evidence, Sciurocheirus has now been re-adopted as a full genus (Grubb et al. 2003, Nekaris & Bearder 2011). In recent taxonomies three subspecies were recognized, but S. a. gabonensis has now been reinstated to full species (Ambrose 1999, 2003) and is now widely recognized (Groves 2001, 2005c, Grubb et al. 2003, Nekaris & Bearder 2011). Synonym: cameronensis. Chromosome number: 2n = 40 (Dutrillaux et al. 1982b). Description Medium-sized galago of forests, vocalizing long ‘whistles’ either as single units, or in phrases of one to six descending units (Ambrose & Perkin 2000, Ambrose 2003). Sexes similar in colouration but !! probably slightly larger. Snout prominent with pale grey nose-stripe, which forms a broader patch on the forehead.

Cheeks, chin, throat, ventrum and inside of legs whitish to pale grey. Broad black eye-rings make a dark face-mask. Eyes chocolatebrown, large and rounded. Ears bare, black, front and back. Base of ears sometimes ringed with pale grey. Dorsum brown, grizzled dark greyish-brown or grey. Shoulders, flanks, and front and outside of limbs medium to bright rust. Hands and feet greyish-black. Breaststripe red, about 4 mm wide, in some individuals. Tail evenly bushy, longer than (ca. 120%) HB length, dark grey to black, sometimes with whitish tip (T. Butynski pers. comm.). Old infant/young juvenile/old juvenile all have colour of adult (A. Croce & T. Butynski pers. comm.). Geographic Variation S. a. alleni Bioko Squirrel Galago. Bioko I. Larger (WT 300–455 g) than S. a. cameronensis. Long ‘whistles’ nearly always given in descending phrases (Ambrose & Perkin 2000, Ambrose 2003). S. a. cameronensis Cross River Squirrel Galago. South-east Nigeria and SW Cameroon. Smaller (WT 220–355 g) than S. a. alleni. Long ‘whistles’ most commonly given as single units (Ambrose & Perkin 2000, Ambrose 2003). Variation exists in pelage colour. Some individuals on Mt Kupé, SW Cameroon, have a pale grey tail, which gets progressively paler distally. About 25% of individuals on Mt Cameroon, W Cameroon, have brown dorsum and tail, little or no rust on limbs and flanks, and no obvious eye-rings (Ambrose 1999). Similar Species Sciurocheirus gabonenesis. Allopatric. South of Sanaga R. S Cameroon south to N Gabon. Colouration similar in Cameroon but redder in Gabon. Tail dark charcoal grey or black, sometimes distal ca.

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3 cm is white. Readily distinguished by the contact and alarm call; short, rapid ‘whistles’ in phrases of 1–10 units (Ambrose 2003). Distribution Endemic to western central Africa. Rainforest BZ. In forests on Bioko I., Equatorial Guinea, and between Niger R., SE Nigeria and Sanaga R., C Cameroon. Sciurocheirus a. alleni widespread on Bioko I. Sciurocheirus a. cameronensis in SE Nigeria at Elele and Oban Group Forest Reserves; in S Nigeria at Itu, Tombia, Wilberforce I. and Gbanraun (Bayelsa State); in SW Nigeria in Okomu Forest; in SW Cameroon at Korup Mundemba, Korup Nguti, L. Barombi (Mbo near Kumba), Mt Cameroon and Mt Kupé (Jewell & Oates 1969b, Eisentraut 1973, Bearder & Honess 1992, Butynski & Koster 1994, Ambrose & Perkin 2000, Ambrose 2003, E. Pimley pers. obs.). Habitat High rainfall lowland, mid-altitude and montane forest. Prefers open understorey in primary forest and old secondary forest. Occurs in plantations and farms on Bioko I. and in Cameroon, but these visited primarily for foraging (Ambrose 2003,T. Butynski pers. comm.). In secondary forest at Elele, Nigeria (Oates & Jewell 1967), and in isolated trees and forest patches in grassland at Moka, Bioko I. (Jewell & Oates 1969b, T. Butynski pers. comm.). In degraded forest fragments around Itu and in Niger Delta swamp forest, S Nigeria (E. Pimley pers. obs.). Occurs from sea level to at least 2250 m on Bioko I. (Butynski & Koster 1994), and up to at least 2000 m in SW Cameroon (Ambrose 1999). Mean annual rainfall over the geographic distribution of S. alleni ranges ca. 2000–10,000 mm (T. Butynski pers. comm.). There are two ‘dry’ seasons on Bioko I.; Dec–Feb when mean monthly rainfall is 500 ind/km2) heard calling at some sites compared to 200 ind/km2 (Butynski et al. dividuals seen making about ten trips each to collect fresh leaves to line 2006). Densities of G. z. udzungwensis highly variable. Common in the tree hole 8 m up (A. Perkin pers. obs.). Coconut palm Cocos nucifera lowland Udzungwa Mts where 10.0 animals/h were encountered fibre and parts of ferns also found in nests (Lumsden & Masters 2001). 448

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Galagoides zanzibaricus

Reproduction and Population Structure One or two infants produced. One G. z. udzungwensis ! caught in Sep 1994 aborted twins the same day, which were subsequently cannibalized (Honess 1996b). Among a sample of adult G. z. zanzibaricus on Zanzibar, the " : ! ratio was 8 : 22 (Masters et al. 1993). Observations of pairs of G. z. udzungwensis in tree-hole nests (Honess 1996b) suggest a social system (similar to that of G. cocos) of a dispersed monogamy with one adult " in close association with one or two adult !! (Harcourt & Nash 1986a, Bearder 1987, Harcourt & Bearder 1989). However, Lumsden & Masters (2001) report nest-sharing by up to five G. z. zanzibaricus (two adult "", one subadult ", one adult !, one subadult !). Predators, Parasites and Diseases No data, but likely to be killed by snakes, owls and mammalian carnivores (e.g. Two-spotted Palm Civet Nandinia binotata and genets Genetta spp.). No information on parasites or diseases. Conservation IUCN Category (2012): Least Concern. Endangered as G. z. zanzibaricus. CITES (2012): Appendix II. Major threats are habitat degradation and loss. Galagoides z. zanzibaricus mainly confined to S and E Unguja I., Zanzibar (1660 km2), where the most significant areas of habitat remain in JozaniChwaka Bay N. P. (3 km2) (Burgess & Clarke 2000). Galagoides z. udzungwensis present in several relatively large Forest Reserves and receives most protection in the Udzungwa Mountains N. P., Sadaani N. P. and Amani Nature Reserve. Zanzibar Dwarf Galago Galagoides zanzibaricus zanzibaricus.

Foraging and Food Omnivorous. Little information. Diet of fruit and invertebrates, with preference in captivity for invertebrates. Fruits include those of Trichilia emetica and Vitex sp. Observed to hang upside down to feed on ants on a vine below and taking insects in the leaf litter driven out by army ant columns (A. Perkin pers. obs.). Major feeding bouts are shortly after emergence at dusk, around midnight, and shortly before dawn. Not observed to eat gum in the wild. In captivity will take crickets, grasshoppers and moths; the wings are discarded. Insect prey is ambushed but may be taken with the hands if in flight (P. Honess pers. obs.). Social and Reproductive Behaviour Predominantly solitary foragers; only 11 of 141 (8%) observations were of pairs. Groups larger than two not observed (Honess 1996b). ‘Urine wash’ and then rub the sternal gland on a branch (Honess 1996b).Vocal advertisement call is a ‘single unit rolling call’ often used as a ‘gathering call’; it is most commonly given at dusk on emergence before first feeding and before dawn for reassembly of sleeping groups (Honess 1996b, Bearder et al. 2003). The single unit rolling call, composed of trilled units that increase then decrease in intensity, is highly variable in length (mean 14.1 units per call (1–46, n = 2122) (Honess 1996b).This call is given more frequently than other calls in the vocal repertoire (>90% of calls recorded; Honess 1996b). Other calls, primarily reflecting differing levels of alarm, include the ‘buzz’, ‘rapid whistle’, ‘descending shriek’, ‘screech’, ‘screech-grunt’ and ‘yap’, which may be graded in intensity or given in combination, making a total repertoire of at least 25 loudcalls (Honess, 1996b).Young are parked whilst the mother forages and are carried by mouth (A. Perkin pers. obs.).

Measurements Galagoides zanzibaricus G. z. zanzibaricus HB: 143 (125–150) mm, n = 11 T: 214 (198–235) mm, n = 11 HF: 56 (51–59) mm, n = 11 E: 32 (31–35) mm, n = 11 WT: 127 (104–172) g, n = 10 GLS: 42 mm, n = 8 Museum specimens from Zanzibar I. (Butynski et al. 2006); sexes combined G. z. udzungwensis HB: 162 (139–180) mm, n = 17 T: 222 (202–270) mm, n = 17 HF: 58 (50–70) mm, n = 17 E: 31 (25–37) mm, n = 17 WT: 145 (118–195) g, n = 6 GLS: 42 mm, n = 1 GWS: 27 mm, n = 1 Live specimens from Matundu F. R. (Honess 1996b, Honess & Bearder 1996), Pugu F. R., Pande G. R. (A. Perkin pers. obs.); museum specimens from Kissarawe, Bagilo (Uluguru Mts), Amboni (Tanga) (Butynski et al. 2006). Sexes combined Key References Butynski et al. 2006; Groves 2001; Grubb et al. 2003; Honess 1996b; Honess & Bearder 1996. Paul E. Honess, Andrew W. Perkin & Thomas M. Butynski 449

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Galagoides rondoensis RONDO DWARF GALAGO Fr. Galago de Rondo; Ger. Rondo-Galago Galagoides rondoensis Honess, 1996. Soc. Biol. Hum. Affairs 61(1): 9. Rondo F. R., 10° 07´ S, 39° 23´ E, Rondo Plateau, Lindi District, Tanzania.

Rondo Dwarf Galago Galagoides rondoensis adult.

Taxonomy Monotypic species. First collected from sites in SE Tanzania (near Newala, Makonde Plateau, in 1953, and Rondo Plateau in 1955) and provisionally identified as Demidoff’s Dwarf Galago ‘Galago demidovii’ and later ‘Galago demidovii orinus’ (Honess 1996b, Lumsden & Masters 2001). First recognized and described as a species, based on differences in vocalizations and morphology, by Honess (1996b) and the formal species description published by Honess (1996a). Note that the authority for the name Galagoides rondoensis is ‘Honess 1996’, not ‘Honess 1997’ as stated in Honess & Bearder (1996), Groves (2001) and Grubb et al. (2003). Subspecies not known. Synonyms: demidoff, demidovii. Chromosome number: not known. Description One of Africa’s two smallest primates. Little or no sexual dimorphism but pelage colour varies according to the maturity of individuals (see below). Muzzle long and slender, with a narrow, pale nose-stripe extending to the forehead. Area on muzzle between nosestripe and cheek sparsely haired, with yellowish skin pigmentation in young animals and dark brown in mature animals (A. Perkin pers. obs.). Crown and forehead reddish-brown (in young animals) to dark brown (in mature animals). Ears mostly slate-grey, with yellow pigmentation on the auricular opening and edges. Yellow pigmentation of ears, lips and chin especially marked in young animals. Eye-rings absent (Honess 1996b) or thin and dark. Dorsum rich brown extending onto thighs and forelimbs. Ventral pelage creamy white with some yellow staining on the chest in some individuals. Tail reddish-orange in immature animals and greyish-brown in mature animals. Sparsely haired until tip where hair is longer, giving

Galagoides rondoensis

a ‘bottle brush’ shape unique to G. rondoensis. Mature animals have thicker hair on tail than immature animals.Tail often held in a curled-up position when resting (Honess 1996b, Honess & Bearder 1996, Perkin 2003). Penis conical and diagnostic in shape, broadening towards distal end (Honess 1996b, Anderson 2000). In mature "", where the distal end of penis enlarges, there is a diagnostic small semi-concentric patch of ‘robust single pointed spines’ (1–2 mm) situated just behind the tip (spine terminology after Dixson 1995 and see Anderson 2000). Rest of penis lacks spines in northern populations but heavy spines at base in southern populations (A. Perkin pers. obs.). In immature "", or possibly non-breeding "", spines greatly reduced or not present (A. Perkin pers. obs.). The species-specific advertising call, a double unit ‘rolling’ call, is diagnostic (Honess 1996b, Honess & Bearder 1996). Geographic Variation No subspecies described but there are differences in call structure and penile morphology between southern nominate population and northern populations (A. Perkin pers. obs.). Limited data (see Measurements) suggest that G. rondoensis of the nominate population is smaller than animals of northern populations. Similar Species Galagoides zanzibaricus udzungwensis. Sympatric in Zareninge F. R., Pugu/Kazimzumbwi F. R. and Pande G. R. on coastal Tanzania. Larger by ca. 100–150%, greyish-brown dorsum, broad nose-stripe, tail not bushy, tail hairs wiry, penile spine patterns and species-specific advertisement call, the single unit ‘rolling’ call, diagnostic (Honess 1996b, Honess & Bearder 1996, Bearder 1999, Perkin 2003).

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Galagoides granti. Sympatric in Rondo F. R., Litipo F. R. and Ziwani F. R., coastal Tanzania. Larger by ca. 100–150%, dorsum brown, tail not bushy, ears large and blackish. Penile spine patterns diagnostic, as is species-specific ‘incremental’ advertising call (Honess 1996b, Honess & Bearder 1996, Perkin 2003). Distribution Coastal Forest Mosaic BZ. Endemic to and discretely distributed in six small moist forests in coastal Tanzania: Zareninge F. R. (06° 05´ S, 38° 23´ E) (Perkin 2000a), Pande G. R. (06° 25´ S, 39° 03´ E), Pugu/Kazimzumbwi F. R. (06° 32´ S, 39° 03´ E) (Perkin 2003, 2004), Rondo F. R. (10° 06´ S, 39° 06´ E), Litipo F. R. (10° 01´ S, 39° 17´ E) and Ziwani F. R. (10° 13´ S, 39° 09´ E) (Honess 1996b, Honess & Bearder 1996). Habitat Occurs in East African coastal dry forest and mist-fed forest, and East African coastal scrub forest within the East African Zanzibar–Inhambane coastal forest belt sensu Clarke & Sorensen (2000). Found only in forest patches between 100 and 900 m asl that are wetter than the surrounding habitats (mean annual rainfall 936–1110 mm). Often associated with liana tangles around treefalls. Abundance Sight and trap data indicate G. rondoensis is locally common but has a highly variable distribution within and among forests. In Pande G. R. densities estimated at 3–6 ind/ha (Perkin 2003). Four individuals trapped in one night in Pugu F. R. in a 0.5 ha plot (Perkin 2004). Encounter rates (number of animals seen or heard per survey hour) range 3–10 animals/h in Pande G. R. and Pugu/Kazimzumbwi F. R. (Perkin 2003, 2004), and 3.9 ind/h in Rondo F. R. (Honess 1996b). Adaptations Nocturnal and arboreal. Nests for daytime sleeping are in thick liana tangles normally 10–30 m above the ground. Three animals seen to occupy a flat leafy nest only 5 m off the ground in Rondo F. R. After leaving the nest at dusk most time is spent in the forest understorey (less than 3 m off the ground) (Honess 1996b). Locomotion is mainly vertical, clinging to thin stems (less than 5 cm diameter) and leaping. Seen hindleg-hopping on ground to cross small gaps, including single-lane tracks (40 min, whilst conspecifics situated close by remain silent until the threat has gone (A. Perkin pers. obs.). Alarm calls comprise rapid high frequency phrases of ‘rapid whistles’ and/or ‘shivering twitters’ several seconds apart linked 451

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Family GALAGIDAE

with ‘yaps’ (Honess 1996b). Such calls also given in presence of G. granti, which is known to hunt vertebrates (S. K. Bearder pers. comm.). Unidentified yellow mites occasionally on edges of ears of mature adults in Pugu F. R. (A. Perkin pers. obs.) and orange mites on head of one individual from Rondo F. R. (Honess 1996b).

HF: 50 mm, n = 8 E: 28 mm, n = 7 WT: 60 g, n = 5 Rondo F. R., SE Tanzania (wild and museum labels) (Honess 1996b). Ranges not provided. Sexes combined.

Conservation IUCN Category (2012): Critically Endangered. CITES (2012): Appendix II. Currently listed as among the 25 most threatened primate taxa in the world (Honess et al. 2009). Main threat is habitat loss. Known distribution 92.6 km2 of coastal forest (Pande G. R. 2.4 km2, Rondo F. R. 25 km2, Ziwani F. R. 7.7 km2, Pugu/Kazimzumbwi F. R. 33.5 km2, Litipo F. R. 4 km2 and Zareninge F. R. 20 km2) (Burgess & Clarke 2000, Perkin 2004). All sites require improved management. Further surveys in potential habitat areas and research on variation among populations are priorities.

HB (""): 131 (123–137) mm, n = 7 T (""): 168 (174–177) mm, n = 7 HF (""): 46 (40–46 mm, n = 7 E (""): 28 (29–30) mm, n = 7 WT (""): 69 (60–73) g, n = 7 Pugu/Kazimzumbi F. R. and Pande G. R., central coastal Tanzania (Perkin 2003, 2004). Pande G. R. is only 10 km from Pugu/ Kazimzumbi F. R., thus data lumped.

Measurements Galagoides rondoensis Data for two populations are presented owing to intra-population variation in vocalization and body measurements. HB: 107 mm, n = 7 T: 184 mm, n = 8

GLS: 35 mm, n = 3 Localities not given (Groves 2001) Key References Bearder 1996.

Bearder et al. 2003; Honess 1996b; Honess & Andrew W. Perkin & Paul E. Honess

Galagoides orinus MOUNTAIN DWARF GALAGO Fr. Galago uriner; Ger. Berggalago Galagoides orinus (Lawrence & Washburn, 1936). Occas. Pap. Boston Soc. Nat. Hist. 8: 259. Bagilo, Uluguru Mts, C Tanzania.

Taxonomy Monotypic species. Originally described as Galago demidovii orinus. Recognized as a full species by Honess (1996b) and Honess & Bearder (1996) based on differences in vocalizations and morphology, and subsequently accepted by Kingdon (1997), Groves (2001) and Grubb et al. (2003).

Mountain Dwarf Galago Galagoides orinus adult.

Description A small, dark galago with a long-haired tail. No sexual dimorphism apparent; sexes alike in colour and pattern of pelage. Muzzle slender and slightly up-turned. Nose-stripe conspicuously white, contrasting with dark brown on either side. Eye-rings thin and dark. Ears with yellow pigmentation on anterior and outer edges; posterior dark brown.Yellow pigmentation decreases with age. Chin and neck yellowish-white. Crown, dorsum, forelimbs, thighs and flanks dark brown. Ventrum, inner-forelimbs and inner-hindlimbs creamy white. Dark yellow staining sometimes visible on chest due to glandular secretions. Lower forelimbs and lower hindlimbs yellowish-brown. Tail morphology is variable, with tails of wildcaught animals long but not densely haired, giving a bushy appearance, but Lawrence & Washburn 1936 describe tail as ‘noticeably shorthaired’. Colour varies from completely reddish-brown to brown over proximal two-thirds and black over distal one-third. Penis is slightly cone-shaped, widening towards the distal end. Baculum protrudes from the end. Small, simple, spines cover the distal half and ca. 14 robust, single, pointed spines cover the proximal half, mostly on the ventral side (Perkin 2007) (spine terminology after Dixson 1995; see Anderson 2000). Species-specific advertisement call (double or triple unit scaling call), and alarm call ‘yaps’ and ‘descending

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Galagoides orinus

Habitat Lives in sub-montane and montane moist forests as well as giant heather Erica sp. forest at the limit of the tree zone (Honess 1996b, Butynski et al. 1998, Perkin 2000b, 2001, 2004). It appears that disturbed forest, such as tree-fall zones, is preferred, especially areas of thick vine tangles (Perkin 2001). The canopy, mid- and understorey are utilized. Altitude range 600–2600 m (Butynski et al. 1998, Rovero et al. 2009). Mean annual rainfall 1000–>2000 mm per year (Lovett & Wasser 1993).

Galagoides orinus

screeches’ diagnostic (Honess 1996b, Perkin et al. 2002). Synonyms: none. Chromosome number: not known. Geographic Variation Poorly known. Data suggest variation in vocalizations among populations in Tanzania (Udzungwa Mts, Uluguru Mts, Rubeho Mts, East Usambara Mts, Mt Rungwe) and N Malawi (Misuku Hills) (Perkin et al. 2002, Bearder & Karlsson 2009). Similar Species Galagoides zanzibaricus udzungwensis. In coastal, lowland and submontane forest from sea level to ca. 1070 m (Butynski et al. 1998). Narrowly sympatric with G. orinus from ca. 600–900 m at Mkungwe F. R. in the Uluguru Mts, but generally parapatric with G. orinus occurring at higher altitudes. About 50% larger. Overall pelage greyish-brown. Tail shorter, more thickly haired and held strait. Species-specific advertisement call a single unit ‘rolling call’ (Honess 1996b, Perkin et al. 2002). Penile morphology different (Perkin 2007). The Galagoides sp. from the montane forests of the Taita Hills, SE Kenya, is similar in pelage and morphology but the species-specific advertisement call differs. Dorsal pelage cinnamon-brown with orange-brown tinge on shoulders and thighs. Tail tip appears to be bushier. It remains to be determined whether this is G. orinus or another taxon (Perkin et al. 2002). Distribution Afromontane–Afroalpine BZ. Endemic to the montane and mid-altitude forests of most of the Eastern Arc Mts, Tanzania, southwards to Mt Rungwe in SC Tanzania, and Misuku Hills in N Malawi (Allen & Loveridge 1927, Lawrence & Washburn 1936, Honess 1996b, Butynski et al. 1998, Perkin 2000b, 2001, Doggart et al. 2006, Bearder & Karlsson 2009). Perhaps in Taita Hills, SE Kenya (Perkin et al. 2002).

Abundance Abundance appears to be variable but measuring is difficult since G. orinus spends much time in the canopy, which probably reduces detection rates. In undisturbed forest Perkin (2001) in the Uluguru Mts, and Honess (1996b) in the East Usambara Mts report enounter rates of 2.7 animals/h (n = 30) and 1.2 animals/h (n = 34), respectively. In disturbed forest Perkin (2001) in the Uluguru Mts and Honess (1996b) in the East Usambara Mts report encounter rates of 4.5 animals/h (n = 74) and 4.7 animals/h (n = 14), respectively. Low encounter rates were also noted in the less disturbed sub-montane and montane forests of the Udzungwa (Butynski et al. 1998) and Rubeho Mountains (Perkin 2004). It is suspected that G. orinus occurs at a low density throughout much of its range (Butynski et al. 1998). Adaptations Nocturnal and arboreal. Tree-holes and nests used for sleeping. One nest in the East Usambara Mts, which held three G. orinus, was round (ca. 30 cm diameter), and constructed of leaves and twigs 15 m up in a clump of lianas (Bearder et al 2003). Locomotion mainly vertical clinging and leaping. Quadrupedal running on horizontal supports and running head first down tree trunks. Will hop to the ground but quickly returns to vertical stems. Utilizes all forest strata. Fast-moving; capable of jumps of >5 m. Utilizes a combination of hearing, sight and olfactory senses to locate prey, communicate with conspecifics and detect predators. Will mob potential predators with intense bouts of alarm calling. Foraging and Food Omnivorous. Eats moths, cockroaches, nectar of wild bananas Ensete edule and gum from the liana Toddalia asiatica. Forages in trees and occasionally in leaf litter. Takes baits of banana and peanut butter (Perkin et al. 2002, Perkin 2004). In captivity accepted geckos (A. Perkin pers. obs.). Social and Reproductive Behaviour Individuals move out of the sleeping site together at dusk but soon start to forage solitarily while maintaining contact by calling. Soon after leaving the sleeping site there is a bout of advertisement calling. There is a second calling peak at dawn (Perkin 2004). Sleeping group size ranges from 1 to 9 animals (mean 4.3, n = 6; Perkin 2000b, 2001, Bearder & Karlsson 2009). One tree nest hole held one mature ", one immature ", one mature ! and one immature !) (A. Perkin pers. obs.). Reproduction and Population Structure Little known. Like other members of the genus Galagoides, G. orinus probably mouth carries infants and ‘parks’ them while foraging (Bearder et al. 2003). Reproductive parameters probably similar to those of other small, montane forest Galagoides spp. (e.g. Demidoff’s Dwarf Galago G. demidovii and Thomas’s Dwarf Galago G. thomasi). 453

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Family GALAGIDAE

Predators, Parasites and Diseases Unknown, but Usambara Eagle-owls Bubo vosseleri, genets Genetta spp., Two-spotted Palm Civets Nandinia binotata, Gentle (Sykes’s) Monkeys Cercopithecus mitis and large snakes are likely predators. Usambara Eagle-owls, genets, African Wood Owls Strix woodfordii and humans may provoke intense episodes of alarm calling. Alarm calls by one individual can last for >1 hour, whilst conspecifics situated close by remain silent until the threat has gone (A. Perkin & T. Butynski pers. obs.). Of the 3–4 alarm calls known for G. orinus the ‘yaps’ and ‘descending screeches’ are given in situations of extreme threat from predators (Honess 1996b, Perkin 2004). Conservation IUCN Category (2012): Near Threatened. CITES (2012): Appendix II. Under the IUCN (2012) Degree of Threat criteria, and based on current data, G. orinus could be categorized as Endangered (category B,1,a,b,i,ii,iii). Conservation dependent on habitat preservation. Main threats are habitat clearance for agriculture, collection of building poles and pit-sawing. Research is required to confirm the range of this species. There is preliminary evidence of interpopulation variation that may have taxonomic and conservation implications (Perkin et al. 2002).

Measurements Galagoides orinus HB: 132 (125–138) mm, n = 4 T: 180 (169–199) mm, n = 4 HF: 46 (43–48) mm, n = 4 E: 30 (25–32) mm, n = 4 WT: 90 (74–98) g, n = 3 One specimen each from Udzungwa Mts (New Dabaga F. R.), Kilanze Kitungulu Forest and Uluguru Mts (Bagilo, Mkungwe) (Lawrence & Washburn 1936, A Perkin pers. obs.). Sexes combined. GLS: 39 mm, n = 1 Locality not stated (Groves 2001) Key References Butynski et al. 1998; Honess & Bearder 1996; Lawrence & Washburn 1936; Perkin et al. 2002. Andrew W. Perkin, Paul E. Honess & Thomas M. Butynski

Galagoides granti MOZAMBIQUE DWARF GALAGO (GRANT’S DWARF GALAGO) Fr. Galago du Mozambique; Ger. Mosambik-Galago Galagoides granti (Thomas & Wroughton, 1907). Proc. Zool. Soc. Lond. 1907: 286. Coguno, Inhambane District, S Mozambique.

Taxonomy Monotypic species. Originally described as a full species Galago granti and accepted by Elliot (1913a). Subsequently, classified as Galago senegalensis granti (Schwarz 1931a) then, following subdivision of G. senegalensis and recognition of Zanzibar Dwarf Galago G. zanzibaricus by Kingdon (1971), classified as a southern subspecies of Zanzibar Dwarf Galago Galago zanzibaricus granti (Jenkins 1987) or Galagoides zanzibaricus granti (Olson 1979, Meester et al. 1986, Nash et al. 1989, Skinner & Smithers 1990). Placed in its current genus and confirmed at full species status by Honess (1996a, b) based on species-specific advertisement calls, and penile and hair morphology (see also Anderson, M.J. 2000, 2001, Butynski et al. 2006). Synonym: mertensi. Chromosome number: not known.

Mozambique Dwarf Galago Galagoides granti adult.

Description A small galago with a long, bushy tail and notably long, rounded, blackish ears. Gives a distinctive ‘incremental call’ as its vocal advertisement. This call begins quietly, increases and then decreases in volume composed of 1–17 units (mean 5.8, n = 211), each made up of an increasing number of sub-units (Honess 1996a, b). Sexes alike in colour and pattern of pelage. Forehead greyer than top of head. Pale band on the top of the snout from forehead to nostrils (interocular stripe). Eye-rings black and conspicuous. Ears relatively long (>37 mm), broad, blackish behind. Dorsal surface of head, neck, back and hindlimbs drab-brown, tipped buffy-brown with slight pinkish tint. Hairs ca. 12 mm. Outside of the forelimbs drab-brown fading to white on the forefeet.Ventrum and inner surface of legs cream-buff; in some specimens upperparts of the limbs have a yellowish tinge.Ventral hairs with basal three-fifths slate-grey. Tail long and bushy, wider over distal ca. 80%, hairs dense, with hairs c. 15 mm long, soft. Tail darker

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than dorsum with distal ca. 10–60% blackish-brown. Some with tail tipped white. No information available on sexual dimorphism in body size or colouration. Penis cylindrical with spines in mature "" concentrated in the mid-region. Baculum does not protrude beyond the glans (Honess 1996b, Anderson 2000, Perkin 2007). Geographic Variation Current data suggest this species is largely consistent across its described range (Butynski et al. 2006). The exclusion of specimens from Newala (6) and the Uluguru Mts (3) from his analysis of G. granti from Mozambique suggests that Groves (2001) was not confident of their identity. However, whilst those from Newala are G. granti (Lumsden & Masters 2001) specimens of a similar size from the Uluguru Mts are most likely Matundu Dwarf Galago G. z. udzungwensis (Honess 1996b, Perkin, 2000b). A recent field study of populations identified in Malawi as Malawi Dwarf Galago Galagoides nyasae (Elliot 1907) and the nearby Mount Thyolo Dwarf Galago, Galagoides sp. nov. 2 (Groves 2001, Grubb et al. 2003), suggests that they are most likely G. granti, based on appearance, calling patterns and habitat use (Wallace 2006). However, a population studied at Kalwe, near Nkata Bay on the western shore of L. Malawi (Galagoides sp. nov. 1) is more distinctive in both appearance and vocalizations and merits further study (Courtenay & Bearder 1989, Bearder & Karlsson 2009). Similar Species Kenya Coast Dwarf Galago Galagoides cocos, G. zanzibaricus and G. granti replace each other from north to south in the evergreen forests of the coastal strip of eastern Africa from N Kenya (perhaps S Somalia) to extreme S Mozambique and extreme E Zimbabwe. G. cocos is the northern species, G. zanzibaricus the central species and G. granti the southern species (Butynski et al. 2006). Galagoides granti is parapatric with Southern Lesser Galago Galago moholi in Mozambique and sympatric with Rondo Dwarf Galago Galagoides rondoensis in S Tanzania. Galaogides zanzibaricus udzungwensis. Parapatric. In Tanzania south to Kihansi and Rufiji/Kilombero River System. Ears shorter (seldom longer than 33 mm) and dusky behind. Hair of dorsum ca. 9 mm. Tail hairs of even length over tail, sparse, ca. 11 mm, wiry. Proximal ca. 75% of tail same colour as dorsum (i.e. buffybrown); distal ca. 25% slightly darker brown or dusky. ‘Single unit rolling call’ (Honess 1996b, Butynski et al. 2006). Galago moholi. Sympatric or parapatric. In savanna woodland. Pelage greyer. Tail thinner and more uniform coloured. Muzzle long (palate length: >17 mm versus 90% of observations at night (n = 130) are solitary animals (Honess 1996b). The incremental call accounts for 78% of loud calls (n = 773). This call is often answered by conspecifics and is most frequently given in the first two hours after sunset and last two hours before sunrise; corresponding with emergence from, and gathering for, sleeping. A wide range of different calls are given, alone and in mixed sequences, indicating the importance of vocal communication (Honess 1996b). These include primary alarm calls such as the ‘buzz’ (‘single drawn out, fading unit’), ‘sweep-screech’ (‘single unit resembles a shorter, more intense buzz’), ‘screech’ (‘harsh, intense single unit, often given in a series’), ‘descending screech’ (‘series of screeches descending in volume and intensity’), ‘yap’ (‘short, dog-like, single unit, often given in series’) and ‘screech-grunt’ (‘as screech but followed by a quiet grunt that is often only audible at close range’) (Honess 1996b). Reproduction and Population Structure Female with two foetuses recorded in Dec in southern Africa. Likely that young are

Conservation IUCN Category (2012): Least Concern. CITES (2012): Appendix II. Higher population densities in mildly disturbed habitats and agriculture mosaics suggests no imminent extinction threat, locally or regionally. Remains vulnerable to extensive habitat reduction to meet fuel and agricultural demands of expanding human populations. Measurements Galagoides granti HB: 153 (140–160) mm, n = 12 T: 230 (216–237) mm, n = 12 HF: 58 (54–63) mm, n = 12 E: 38 (36–43) mm, n = 12 Coguno and Tambarara, Mozambique. Specimens obtained by C. H. B. Grant during the Rudd Expedition and housed at BMNH. Coguno is the type locality for G. granti (Butynski et al. 2006). Sexes combined. HB: 162 mm, n = 10 T: 232 (214–254) mm, n = 10 HF: 62 (59–63 )mm, n = 10 E: 40 (38–41) mm, n = 9 WT: 165 (139–178) g, n = 6 Extreme E Zimbabwe (Smithers & Wilson 1979); sexes combined HB: 164 (154–181) mm, n = 3 T: 214 (208–222) mm, n = 3 HF: 58 (58–59) mm, n = 3 E: 37, 38 mm, n = 2 WT: 136 (110–160) g, n = 3 Combined measurements for two "" and one !. Tanzania: Kichi Hills F. R. (n = 2) and Lulunda, Udzungwa Mts (n = 1) (A. Perkin pers. obs.) GLS: 42 mm, n = 17 Localities not stated (Groves 2001); sexes combined Key References Butynski et al. 2006; Courtenay & Bearder 1989; Honess 1996b; Perkin 2000b; Lumsden & Masters 2001. Paul E. Honess, Simon K. Bearder & Thomas M. Butynski

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Galagoides cocos

Galagoides cocos KENYA COAST DWARF GALAGO (DIANI DWARF GALAGO) Fr. Galago de Diani; Ger. Diani-Galago Galagoides cocos (Heller, 1912). Smith. Misc. Col. 60: 1. Mazeras, Kenya.

Galagoides cocos

Kenya Coast Dwarf Galago Galagoides cocos.

Taxonomy Monotypic species. The Kenya Coast Dwarf Galago was originally named Galago moholi cocos, then elevated to Galago cocos, then, for many years, considered a subspecies or synonym of the Zanzibar Dwarf Galago Galago zanzibaricus. On the basis of its distinct loud advertising call, penile morphology and facial markings, G. cocos recently revived as a species (Grubb et al. 2003, Butynski et al. 2006, Perkin 2007). As such, most literature dealing with the ecology and behaviour of the Kenya Coast Dwarf Galago prior to 2003 is under the name ‘Galago zanzibaricus’ (e.g. Harcourt 1986a, Harcourt & Nash 1986a, b, Nash et al. 1989, Bearder et al. 1995). Synonyms: none. Chromosome number: not known. Description Small, brown galago with distinctive ‘incremental’ advertising call. Sexes similar in size and colour. Muzzle long, pointed, with broad white streak continuing well above eyes. Eye-rings prominent, formed by dark skin that continues down sides of muzzle to form ‘tear’ marks at the base of the muzzle. Ears large, held ca.

45° angle from the vertical plane rather than upright. Dorsum buffybrown. Chin, chest and ventrum greyish-white, but strong yellow or orange wash may be present due to plant stains obtained while scentrubbing (De Jong & Butynski 2011). Tail same colour as dorsum with distal one-third dark buffy-brown in some. Penis with pinnate, robust spines over most of length. Penis enlarges slightly in middle (where largest spines are located) before tapering off to the tip. Glans penis does not protrude from baculum (Perkin 2007). Immatures like adults, but white nose-stripe often incomplete towards rhinarium and penile spines absent or small. Geographic Variation

None recorded.

Similar Species Galagoides zanzibaricus udzungwensis. Probably sympatric, or at least parapatric, in northern part of range in NE Tanzania (Butynski et al. 2006). Single unit ‘rolling’ advertising call distinctive (Bearder et al. 1995). Nose-stripe greyish-white, less well defined. Patch on either side of muzzle less dark and prominent. Ears more erect, shorter. Tail short, evenly haired. In coastal and lowland forests of E Tanzania (Butynski et al. 2006). Galago senegalensis. Marginally sympatric (e.g. lower Tana R.). Larger (ca. 200 g). Loud ‘woo’ (or ‘honk’) advertising call distinctive. Dorsum grey or brownish-grey. Tail grey to brown, bushier towards distal end. In woodland and acacia bushland (Butynski & De Jong 2004, Butynski et al. 2006, De Jong & Butynski 2011). Galago gallarum. Probably marginally sympatric in southern part of range. Larger (ca. 200 g). ‘Trumpeting quack’ advertising call 457

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distinctive. Ears black front and back. Tail grey proximally, dark brown and longer haired distally. In Acacia–Commiphora bushland (Butynski & De Jong 2004, Butynski et al. 2006).

faecal sample in Diani suggest that small birds are sometimes eaten (Harcourt 1984). Not observed eating gum naturally in the wild (Harcourt & Bearder 1989), but will eat gum when provisioned (Nash 1989).

Distribution Endemic to coastal strip of Kenya and NE Tanzania. Perhaps in SE Somalia. Northern limit perhaps Juba R. or Shabeelle R., south coast of Somalia. Confirmed northern, eastern and inland limits presented in De Jong & Butynski (2011). Southwards through coastal Kenya, to Mgambo F. R. and Kilulu Hill F. R., extreme NE Tanzania. Largely confined to the coastal strip and gallery forests (e.g. those of the lower Tana R.) from 0 to 210 m, but there is one record for Nairobi at ca. 1850 m (Butynski et al. 2006), but this requires confirmation.

Social and Reproductive Behaviour Social. Unlike other galagos studied to date, adult "" consistently sleep with the same one or two adult !! and their offspring. Night-time ranges of adult "" closely coincide with ranges of those adult !! with which they sleep. Home-ranges of adult "" overlap slightly (see Figure 1 in Harcourt & Nash 1986a) with those of neighbouring "". When adult " leaves his territory (which happens rarely), increased calling and chases occur (Harcourt & Nash 1986a). At Gedi there is Habitat Dry, mixed, coastal forests and thickets, and flood-plain some indication that two classes of adult "" exist (dominants and forests. Coastal Forest Mosaic BZ. Where G. cocos has been most subordinates) in the population as has been reported for Southern studied (i.e. at Gedi and Diani Forests, Kenya) there is a fairly thick Lesser Galago Galago moholi (Bearder & Martin 1979). Same-age understorey, commonly including Lecaniodiscus fraxinifolius, Fagara !! usually occupy almost exclusive home-ranges, but in some cases chalybea and Meyna tetraphylla at Gede, and Diospyros abyssinica, Grewia there is considerable overlap of ranges of two !!. Females with goetzeanai, Lantana camara and Zizyphus mucronata at Diani. Canopy overlapping ranges regularly sleep together and are probably related. in both areas at 15–20 m, dominated by Combretum schumannii, Mean home-range size is 3.4 ha (1.8–5.1, n = 6) for adult "" and while others, including Ficus spp. and Tamarindus indica, are also 1.9 ha (1.3–2.6, n = 8) for adult !!.Young !! generally remain common. Emergents reach to 25 m (e.g. Adansonia digitata, Sterculia in their natal range, while "" disperse (Harcourt & Nash 1986a). appendiculata and Lannea stuhlmannii). Rainfall bimodal, with long Females leave their sleeping groups and sleep alone just before they rains Apr–Jun and short rains in Oct–Nov. Mean annual rainfall ca. give birth and for a few weeks afterwards (Harcourt 1986a). Infant 1040 mm (Harcourt & Nash 1986b). In acacia woodland where G. carried in mother’s mouth and ‘parked’ on a branch while she forages. senegalensis is absent, such as north-east of Bodhei on the north coast ‘Incremental’ advertising call often, but not always, starts with a of Kenya (De Jong & Butynski 2011). series of high-pitched, rapidly uttered, ‘chirrups’ followed by units arranged in phrases that are high in frequency and amplitude, and Abundance Variable, about 170–180 ind/km2 at Gedi and gradually become lower in amplitude. The number of units within Diani, but at much lower densities at some sites (Harcourt & Nash each phrase typically increases ‘incrementally’; often, phrases with 1986a). same number of units are repeated. This call has a fundamental frequency of 0.8–1.2 kHz, with harmonic spectra visible up to Adaptations Nocturnal and arboreal. Spends day in tree hollows the tenth or eleventh harmonic at 9.3 kHz, frequency range 0.65– either alone or, more often, in groups of one adult ", one or two 11.15 kHz, range of unit frequency modulation 0.68–10.37 kHz !! and their offspring (Harcourt & Nash 1986a, Bearder et al. (Courtney & Bearder 1989, Bearder et al. 1995, Butynski et al. 2003). Sleeping site use varies. In Diani a " watched at dusk used 2006). 29 sites (n = 82), while one in Gedi used only seven sites (n = 96). There is a peak of calling at the beginning and end of the night Sleeping in groups may help thermoregulation in this small species, (Nash 1986, Butynski et al. 2006), and no sex difference in the rate though temperatures do not drop below ca. 24 °C during the day. of calling (Harcourt 1984). About half the calls are given in answer This is probably also a predator avoidance strategy (Harcourt to a call or are answered (Harcourt 1984). A common alarm call is & Nash 1986a, b). Insect prey is located by hearing and vision. the ‘buzz and rapid chatter’. This consists of an explosive buzz unit Communication is through calling and, probably, olfaction. followed by a descending, rapid series of 15–20 units. Another alarm call, ‘yaps and chirrups’, consists of a series of high-pitched ‘yap’ Foraging and Food Omnivorous. Forages only at night, most units about a second or less apart interspersed with a rapid series of frequently alone, and usually