Gibbon Conservation in the Anthropocene 9781108479417, 9781108785402, 9781108743037, 1108479413

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Gibbon Conservation in the Anthropocene Hylobatids (gibbons and siamangs) are the smallest of the apes, distinguished by their coordinated duets, territorial songs, arm-swinging locomotion and small family group sizes. Although they are the most speciose of the apes, boasting 20 species living in 11 countries, 95 per cent are critically endangered or endangered according to the IUCN’s Red List of Threatened Species. Despite this, gibbons are often referred to as being ‘forgotten’ in the shadow of their great ape cousins because comparably they receive less research, funding and conservation attention. This is only the fourth scientific book since the 1980s devoted to gibbons, and presents cutting-edge research covering a wide variety of topics including hylobatid ecology, conservation, phylogenetics and taxonomy. Written by gibbon researchers and practitioners from across the world, the book discusses conservation challenges in the Anthropocene and presents practicebased approaches and strategies to save these singing, swinging apes from extinction. Susan M. Cheyne is co-director of Borneo Nature Foundation International and ViceChair for the IUCN Primate Specialist Group Section on Small Apes. She received the 2017 Marsh Award for Conservation Biology in partnership with the Zoological Society of London. She is also a Royal Geographical Society Fellow and an IUCN Cat Specialist Group member. Carolyn Thompson is an early career interdisciplinary researcher with University College London and the Zoological Society of London’s Institute of Zoology. She has more than 15 years’ experience working in the field of primatology. The majority of her research has focused on Asian primates, with the exception of lemurs in Madagascar. Her research interests include human–primate interactions, ethnoprimatological methods, conservation education and primate conservation. Carolyn is the Student Representative for the IUCN Primate Specialist Group Section on Small Apes. Peng-Fei Fan is a Professor in the School of Life Sciences, Sun Yat-Sen University, Guangzhou, People’s Republic of China. He has been studying the behaviour, ecology and conservation of primates, mostly gibbons, in China since 2002. Along with his colleagues, he discovered the white-cheeked macaque (Macaca leucogenys) and skywalker hoolock gibbon (Hoolock tianxing). He has published more than 80 peerreviewed papers and currently serves as Associate Editor or Editorial Board Member for five scientific journals. Helen J. Chatterjee is Professor of Human and Ecological Health at University College London. Her research is focused on biodiversity conservation and evidencing the links between the health of the environment and the health of people. Helen serves on the Executive Committee for the IUCN Primate Specialist Group Section on Small Apes. In 2015 she received an MBE for services to Higher Education and Culture.

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Gibbon Conservation in the Anthropocene Edited by S US A N M . CH EY N E Borneo Nature Foundation

CAROLYN THOMPSON University College London

PENG-FEI FAN Sun Yat-Sen University

HELEN J. CHATTERJEE University College London

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Shaftesbury Road, Cambridge CB2 8EA, United Kingdom One Liberty Plaza, 20th Floor, New York, NY 10006, USA 477 Williamstown Road, Port Melbourne, VIC 3207, Australia 314–321, 3rd Floor, Plot 3, Splendor Forum, Jasola District Centre, New Delhi – 110025, India 103 Penang Road, #05–06/07, Visioncrest Commercial, Singapore 238467 Cambridge University Press is part of Cambridge University Press & Assessment, a department of the University of Cambridge. We share the University’s mission to contribute to society through the pursuit of education, learning and research at the highest international levels of excellence. www.cambridge.org Information on this title: www.cambridge.org/9781108479417 DOI: 10.1017/9781108785402 © Cambridge University Press & Assessment 2023 This publication is in copyright. Subject to statutory exception and to the provisions of relevant collective licensing agreements, no reproduction of any part may take place without the written permission of Cambridge University Press & Assessment. First published 2023 A catalogue record for this publication is available from the British Library. Library of Congress Cataloging-in-Publication Data Names: Cheyne, Susan M., 1976– editor. | Thompson, Carolyn, 1985– editor. | Fan, Peng-Fei, 1981– editor. | Chatterjee, Helen J., editor. Title: Gibbon conservation in the Anthropocene / edited by Susan M. Cheyne (Borneo Nature Foundation), Carolyn Thompson (University College London), Peng-Fei Fan (Sun Yat-Sen University), Helen J. Chatterjee (University College London). Description: Cambridge, United Kingdom : Cambridge University Press, 2023. | Includes bibliographical references and index. Identifiers: LCCN 2022047140 (print) | LCCN 2022047141 (ebook) | ISBN 9781108479417 (hardback) | ISBN 9781108743037 (paperback) | ISBN 9781108785402 (epub) Subjects: LCSH: Gibbons. | Gibbons–Conservation. Classification: LCC QL737.P943 G53 2023 (print) | LCC QL737.P943 (ebook) | DDC 599.88/2–dc23/eng/20221018 LC record available at https://lccn.loc.gov/2022047140 LC ebook record available at https://lccn.loc.gov/2022047141 ISBN 978-1-108-47941-7 Hardback Additional resources for this publication at www.cambridge.org/gibbonconservation Cambridge University Press & Assessment has no responsibility for the persistence or accuracy of URLs for external or third-party internet websites referred to in this publication and does not guarantee that any content on such websites is, or will remain, accurate or appropriate.

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Contents

List of Contributors Foreword

page viii xv

David J. Chivers

List of Abbreviations Introduction: Overview of the Gibbons and the IUCN Primate Specialist Group Section on Small Apes

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1

Susan M. Cheyne, Helen J. Chatterjee, Carolyn Thompson and Peng-Fei Fan

1

Taxonomy, Ecology and Conservation of Cao Vit Gibbon (Nomascus nasutus) since Its Rediscovery

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Peng-Fei Fan and Chang-Yong Ma

2

Conservation Status of the Northern Yellow-Cheeked Crested Gibbon (Nomascus annamensis) in Vietnam: An Update

24

Duc Minh Hoang, Bang Van Tran, Chuong Van Hoang and Herbert H. Covert

3

Strategies for Recovery of the Hainan Gibbon (Nomascus hainanus): Twenty Years of Multidisciplinary Conservation Effort

40

Bosco Pui Lok Chan and Yik Fui Philip Lo

4

Gibbons in the Anthropocene: Lessons from a Long-Term Study in Indonesia

57

Susan M. Cheyne, Abdulaziz K, Supiansyah, Twentinolosa, Adul, Claire J.H. Thompson, Lindy Thompson, Reychell Chadwick, Hélène Birot, Carolyn Thompson, Cara H. Wilcox and Eka Cahyaningrum

5

Demography of a Stable Gibbon Population in High-Elevation Forest on Java

78

Susan Lappan, Rahayu Oktaviani, Ahyun Choi, Soojung Ham, Haneul Jang, Sanha Kim, Yoonjung Yi, Ani Mardiastuti and Jae Chun Choe

6

A Tale of Two Gibbon Studies in Thailand Sompoad Srikosamatara and Intanon Kolasartsanee

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Accessibility as a Factor for Selecting Conservation Actions for Pileated Gibbons (Hylobates pileatus)

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Intanon Kolasartsanee and Sompoad Srikosamatara

8

Calling from the Wild: Mentawai Gibbon Conservation Fieldwork

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Arif Setiawan and Damianus Tateburuk

9

Demography and Group Dynamics of Western Hoolock Gibbons (Hoolock hoolock) in a Community Conserved Village Population in Upper Assam, India

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Jihosuo Biswas, Diplob Chutia, Jayanta Das, Joydeep Shil and H.N. Kumara

10

Challenges and Prospects in the Conservation of Hoolock Gibbon in India

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Dilip Chetry, Rekha Chetry and Parimal Chandra Bhattacharjee

11

Gibbons of Assam: Impacts of Environment and Anthropogenic Disturbance

167

Jayashree Mazumder

12

Movement Ecology of Siamang in a Degraded Dipterocarp Forest

188

Christopher D. Marsh, Stephanie A. Poindexter, Ross A. Hill, Matthew G. Nowak, Abdullah Abdullah and Amanda H. Korstjens

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Sympatric Gibbons in Historically Logged Forest in North Sumatra, Indonesia

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Emma L. Hankinson, Vincent Nijman, Amanda H. Korstjens, Matthew G. Nowak and Ross A. Hill

14

Adopting an Interdisciplinary Biosocial Approach to Determine the Conservation Implications of the Human–Gibbon Interface: A Systematic Review

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Carolyn Thompson, Helen J. Chatterjee, Samuel T. Turvey, Susan M. Cheyne and Peng-Fei Fan

15

Listen to the People, Hear the Gibbons Sing: The Importance of Incorporating Local People’s Perceptions in Conservation

253

Jaima H. Smith, Anton Ario, Rahayu Oktaviani, Arif Setiawan, Agung Gunawan and Vincent Nijman

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Long-Term Outcomes of Positive Cultural Value for Biodiversity: Historical Insights from Chinese Gibbons Samuel T. Turvey

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Gibbon Phylogenetics and Genomics

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286

Lucia Carbone, Mariam Okhovat and Christian Roos

18

The Use of Microsatellites in the Management of Captive Gibbons

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Lauren Lansdowne, Matyas Liptovszky, Kristiana Brink, Katie Dripps, Vivienne Li, Edward J. Hollox and Richard M. Badge

Index

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Contributors

Abdulaziz K Borneo Nature Foundation Indonesia, Palangka Raya, Central Kalimantan, Indonesia Abdullah Abdullah Department of Biology, Universitas Syiah Kuala, Banda Aceh, Aceh, Indonesia Adul Borneo Nature Foundation Indonesia, Palangka Raya, Central Kalimantan, Indonesia Anton Ario Konservasi Indonesia; Javan Gibbon Centre, Bogor, West Java, Indonesia Richard M. Badge Department of Genetics and Genome Biology, University of Leicester, Leicester, UK Parimal Chandra Bhattacharjee Department of Zoology, Gauhati University, Guwahati, Assam, India Hélène Birot Borneo Nature Foundation International, Tremough Innovation Centre, Penryn, UK Jihosuo Biswas Primate Research Centre Northeast India, Guwahati, Assam, India Kristiana Brink Department of Genetics and Genome Biology, University of Leicester, Leicester, UK Eka Cahyaningrum Borneo Nature Foundation Indonesia, Palangka Raya, Central Kalimantan, Indonesia

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List of Contributors

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Lucia Carbone Knight Cardiovascular Institute, Department of Medicine, Oregon Health and Science University; and Division of Genetics, Oregon National Primate Research Center, Portland, Oregon, USA Reychell Chadwick Borneo Nature Foundation International, Tremough Innovation Centre, Penryn, UK Bosco Pui Lok Chan Kadoorie Conservation China Department, Kadoorie Farm and Botanic Garden, Hong Kong SAR, People’s Republic of China Helen J. Chatterjee Genetics, Evolution and Environment, School of Life Sciences, University College London, London, UK Dilip Chetry Primate Research and Conservation Division, Aaranyak, Guwahati, Assam, India Rekha Chetry Department of Zoology, Jawaharlal Nehru College, Boko, Assam, India Susan M. Cheyne School of Social Sciences, Oxford Brookes University, Oxford; and Borneo Nature Foundation International, Tremough Innovation Centre, Penryn, UK Jae Chun Choe Division of Ecoscience, Ewha Womans University, Seoul, South Korea Ahyun Choi Interdisciplinary Program of EcoCreative, Ewha Womans University, Seoul, South Korea Diplob Chutia Barekuri EDC, Dighal Haku Village, Tinsukia, Assam, India Herbert H. Covert Department of Anthropology, University of Colorado Boulder, Boulder, Colorado, USA Jayanta Das Wildlife Areas Development and Welfare Trust, Guwahati, Assam, India

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List of Contributors

Katie Dripps Department of Genetics and Genome Biology, University of Leicester, Leicester, UK Peng-Fei Fan School of Life Sciences, Sun Yat-Sen University, Guangzhou, People’s Republic of China Agung Gunawan Balai Besar Taman Nasional Gunung Gede Pangrango, Cianjur, Jawa Barat, Indonesia Soojung Ham Division of Ecoscience, Ewha Womans University, Seoul, South Korea Emma L. Hankinson School of Social Sciences, Oxford Brookes University, Oxford, UK Ross A. Hill Science and Technology, Bournemouth University, Poole, UK Chuong Van Hoang GreenViet, Da Nang City, Vietnam Duc Minh Hoang Southern Institute of Ecology, Vietnam Academy of Science and Technology, Ho Chi Minh City, Vietnam Edward J. Hollox Department of Genetics and Genome Biology, University of Leicester, Leicester, UK Haneul Jang Department of Human Behavior, Ecology and Culture, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany Sanha Kim Biodiversity Foundation, Seoul, South Korea Intanon Kolasartsanee Ecoliteracy and Conservation in Action Group, Department of Biology, Faculty of Science, Mahidol University, Bangkok, Thailand Amanda H. Korstjens Science and Technology, Bournemouth University, Poole, UK

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List of Contributors

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H.N. Kumara Sálim Ali Centre for Ornithology and Natural History, Anaikatty, Tamil Nadu, India Lauren Lansdowne Department of Genetics and Genome Biology, University of Leicester, Leicester, UK Susan Lappan Department of Anthropology, Appalachian State University, Boone, North Carolina, USA; and Malaysian Primatological Society, Kulim, Malaysia Vivienne Li Department of Genetics and Genome Biology, University of Leicester, Leicester, UK Matyas Liptovszky Perth Zoo, South Perth, WA, Australia Yik Fui Philip Lo Kadoorie Conservation China Department, Kadoorie Farm and Botanic Garden, Hong Kong SAR, People’s Republic of China Chang-Yong Ma College of Life Sciences, Guangxi Normal University, Guilin, Guangxi Province, People’s Republic of China Ani Mardiastuti Department of Forest Resources Conservation and Ecotourism, Faculty of Forestry and Environment, IPB University, Darmaga Bogor, West Java, Indonesia Christopher D. Marsh Department of Life and Environmental Sciences, Bournemouth University, Poole, UK; and Department of Biology, University of New Mexico, Albuquerque, New Mexico, USA Jayashree Mazumder Department of Humanities and Social Sciences, Indian Institute of Science Education and Research, Mohali, Punjab, India Vincent Nijman School of Social Sciences, Oxford Brookes University, Oxford, UK Matthew G. Nowak The PanEco Foundation – Sumatran Orangutan Conservation Programme, Berg am Irchel, Switzerland; Sumatran Orangutan Conservation Programme, Medan Selayang,

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List of Contributors

North Sumatra, Indonesia; and Department of Anthropology, Southern Illinois University, Carbondale, Illinois, USA Mariam Okhovat Knight Cardiovascular Institute, Department of Medicine, Oregon Health and Science University, Portland, Oregon, USA Rahayu Oktaviani Javan Gibbon Research and Conservation Project, Bogor; and Yayasan Konservasi Ekosistem Alam Nusantara (KIARA), Kabupaten Bogor, West Java, Indonesia Stephanie A. Poindexter Department of Anthropology, State University of New York at Buffalo, Buffalo, New York, USA Christian Roos Gene Bank of Primates, Primate Genetics Laboratory, German Primate Center, Leibniz Institute for Primate Research, Göttingen, Germany Arif Setiawan SWARAOWA, Kalipenthung, Yogyakarta; and Coffee and Primate Conservation Project, Central Java, Indonesia Joydeep Shil Manipal Academy of Higher Education, Manipal, Karnataka; and Sálim Ali Centre for Ornithology and Natural History, Anaikatty, Tamil Nadu, India Jaima H. Smith School of Social Sciences, Oxford Brookes University, Oxford, UK Sompoad Srikosamatara Ecoliteracy and Conservation in Action Group, Department of Biology, Faculty of Science, Mahidol University, Bangkok, Thailand Supiansyah Borneo Nature Foundation Indonesia, Palangka Raya, Central Kalimantan, Indonesia Damianus Tateburuk Malinggai Uma Traditional Mentawai, Mentawai, Sumatra, Indonesia Carolyn Thompson Genetics, Evolution and Environment, School of Life Sciences, University College London; and Institute of Zoology, Zoological Society of London, London, UK

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List of Contributors

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Claire J.H. Thompson Borneo Nature Foundation International, Tremough Innovation Centre, Penryn, UK Lindy Thompson Borneo Nature Foundation International, Tremough Innovation Centre, Penryn, UK Bang Van Tran Southern Institute of Ecology, Vietnam Academy of Science and Technology, Ho Chi Minh City, Vietnam Samuel T. Turvey Institute of Zoology, Zoological Society of London, London, UK Twentinolosa Borneo Nature Foundation Indonesia, Palangka Raya, Central Kalimantan, Indonesia Cara H. Wilcox Borneo Nature Foundation International, Tremough Innovation Centre, Penryn, UK Yoonjung Yi Laboratory of Animal Behaviour and Conservation, College of Biology and the Environment, Nanjing Forestry University, Nanjing, People’s Republic of China; and Division of Ecoscience, Ewha Womans University, Seoul, South Korea

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Foreword

I first set foot in the jungles of Southeast Asia 64 years ago, following in the footsteps of the great pioneer of primate field studies, Clarence Ray Carpenter, whom I had first followed to study the howler monkeys of Barro Colorado Island in the Panama Canal Zone in 1967 with the Smithsonian Tropical Research Institute. I first met him in September 1967 while on my way back to the UK. I had detoured to visit most of the howler monkey and gibbon researchers based in the USA. He was a really charming and modest man, very supportive of my research, and was living in a house on the campus of Pennsylvania State University. That was an auspicious month because my first contact in the USA was at Berkeley, California, with Colin Groves, that great gibbon taxonomist, with whom I maintained close contact until his sad death a few years ago. Then I went down to the redwoods of La Honda, California, to meet John Ellefson, the second gibbon field worker, who studied lar gibbons (Hylobates lar) on the coast of the Malay Peninsula, while his wife Judy studied long-tailed macaques (Macaca fascicularis) in the Singapore Botanic Garden. Carpenter had studied lar gibbons in Thailand as part of the Asian Primate Expedition in 1937 with the great primate anatomist Adolf Schultz and the anthropologist Sherry Washburn, at the invitation of that famous zoologist with an interest in gorillas, Harold Jefferson Coolidge, Founding Director of the International Union for Conservation of Nature (IUCN) and then World Wildlife Fund. Sadly, as this was still the age of collectors, they collected 233 gibbons and then, while Carpenter continued his seminal field study, they went on to Sabah, Malaysia, to collect 47 more, and seven orangutans. If there is any good news about this, Schultz’s meticulous studies provided the substantial basis of gibbon skeletal anatomy that has been invaluable to many, including Colin Groves. I met Carpenter and Schultz again in 1970 at the Third Congress of the International Primatological Society (IPS) in Zurich, Switzerland, where I gave my first paper on gibbons. While Carpenter was a generous chairman, the co-chairman, Helmut Hofer, rudely told me to conclude as soon as I overran! And so I started my two-year field study of the siamang (Symphalangus syndactylus) in May 1968 with seven months of surveys all over the Malay Peninsula, and then 17 months in two sites in Pahang (Ulu Sempam in the Main Range in the west, and Kuala Lompat in the Krau Game Reserve, lowland forest at the foot of the central massif of Gunung Benom).

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Foreword

Within 15 years sufficient data had been generated on gibbons – the ‘small’ rather than ‘lesser’ apes – to hold a conference in 1980 at Schloss Reisensburg, near Ulm, on the German Danube, hosted by Holger Preuschoft, on all aspects of gibbon biology. It was here that I learnt about ‘round-table discussions’, which were even more productive than the day-time sessions, lasting well into the night. We gathered in round turrets with round tables within falling distance of fridges full of German beer and wine. There were 48 contributors to 46 chapters covering over 709 pages, edited by Preuschoft, Chivers, Brockelman and Creel, published in 1984, with sections on conservation; functional morphology; ecology, feeding and ranging; social behaviour; and evolutionary biology. The University of Cambridge field input was made by myself, Jeremy Raemaekers, Paul Gittins and Tony Whitten, all of whom are sadly deceased, with the involvement of John Fleagle from Harvard University, and John and Kathy MacKinnon from the University of Oxford. From overseas, the players included Rich Tenaza and Ron Tilson, Dede Leighton, Markus Kappeler, Warren Brockelman and Sompoad Srikosamatara. Following on 25 years later, the second major synthesis was initiated at the 2002 IPS Congress at a symposium organised by Thomas Geissmann, and published in 2009 by Susan Lappan and Danielle Whitaker, entitled The Gibbons: New Perspectives on Small Ape Socio-ecology and Population Biology. There were 45 contributors to 24 chapters covering over 523 pages, with sections on biogeography, diet and community ecology, relationship between ecology and social organisation, mating systems and reproduction, and conservation biology. The University of Cambridge contribution came from Susan Cheyne, Kim McConkey and Achmad Yanuar in Indonesia. And so to 2022, another 13 years on, with this third synthetic volume, Gibbon Conservation in the Anthropocene, edited by Helen Chatterjee, Susan Cheyne, PengFei Fan and Carolyn Thompson. What I find incredible is that, nearly 40 years on from the first volume, there is apparently just one contributor still researching gibbons: Sompoad Srikosmatara in Thailand (with Warren Brockelman lurking in the background). Again, the scope is more restricted, with the focus on ecology and, especially, conservation, but there are 65 (the most yet) contributors to the 18 chapters. The initial emphasis is on the endangered crested gibbons of China and Vietnam (Nomascus spp.), as well as on the moloch gibbon of Java (Hylobates moloch), the Kloss’s gibbon (Hylobates klossii) of the Mentawai Islands, the pileated gibbon (Hylobates pileatus) of Thailand and the hoolock gibbons (Hoolock spp.) of Assam, India. Sadly, there is nothing from Myanmar, Cambodia and Laos. There is an emphasis on cultural and historical perspectives, with a final reference to genetics and phylogenetics. The diversity and intensity of threats to gibbons are alarming. The coronavirus pandemic has led to an increase in the significance of local researchers, well reflected in this volume in relation to international collaboration. The 2020 survey of members of the IUCN Primate Specialist Group Section on Small Apes identifies 22 priority areas for future gibbon research and conservation, with eight main recommendations emerging.

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It was a privilege to be in the first generation of gibbonologists, to supervise the doctoral theses of a dozen of them that followed, and it is an honour to welcome this new, dynamic and very productive volume. Professor David J. Chivers Professor Emeritus in Primate Biology and Conservation University of Cambridge March 2022

https://doi.org/10.1017/9781108785402.001 Published online by Cambridge University Press

Abbreviations

ANOVA APFD ASCR a.s.l. AUC BCE BNF bp CALS CE CIMTROP CITES CVGCA CWRC DBH DEM DSM EAZA ENM FFI GGPNP GHSNP GPS HGWS HR IBI ICU IFAW IUCN JGC kb KFBG KSD

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analysis of variance Arunachal Pradesh Forest Department acoustic spatial capture–recapture above sea level area under the receiver operating curve Before Common Era Borneo Nature Foundation base pair Cagar Alam Leuweung Sancang Common Era Centre for International Cooperation in Management of Tropical Peatland Convention on International Trade in Endangered Species of Wild Fauna and Flora Cao Vit Gibbon Conservation Area Centre for Wildlife Rehabilitation and Conservation diameter at breast height digital elevation model digital surface model European Association of Zoos and Aquaria environmental niche modelling Fauna and Flora International Gunung Gede-Pangrango National Park Gunung Halimun-Salak National Park Global Positioning System Hoollongapar Gibbon Wildlife Sanctuary home range inter-birth interval intensive care unit International Fund for Animal Welfare International Union for Conservation of Nature Javan Gibbon Rescue and Rehabilitation Centre kilobase Kadoorie Farm and Botanic Garden Khao Soi Dao Wildlife Sanctuary

List of Abbreviations

KY LEK LiDAR MSF MU NGO(s) NLPSF NP NR NSF NTFPs PCR PHVA PPKAB SD SDM SfM SINE SMART SNPs SOCP SRTM SSA SSP STRs SVAA TEK TEs TNGL UAVs USGS UTM VNTR WTI

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Khao Yai National Park local ecological knowledge light detection and ranging mixed swamp forest Mahidol University non-governmental organisation(s) National Laboratory of Peat-Swamp Forest national park nature reserve National Science Foundation non-timber forest products polymerase chain reaction population and habitat viability analysis Pusat Pendidikan Konservasi Alam Bodogol standard deviation species distribution modelling structure from motion software short interspersed nuclear element Spatial Monitoring and Reporting Tool single nucleotide polymorphisms Sumatran Orangutan Conservation Programme Shuttle Radar Topography Mission IUCN’s Primate Specialist Group’s Section on Small Apes Species Survival Plan short tandem repeats Sauvegarde de la Vie Animale Arboricole traditional ecological knowledge transposable elements Taman Nasional Gunung Leuser unmanned aerial vehicles United States Geological Survey Universal Transverse Mercator variable number tandem repeat Wildlife Trust of India

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Introduction Overview of the Gibbons and the IUCN Primate Specialist Group Section on Small Apes Susan M. Cheyne, Helen J. Chatterjee, Carolyn Thompson and Peng-Fei Fan

Gibbons and siamangs (termed ‘gibbons’ hereafter) are members of the family Hylobatidae and are the smallest of the apes, distinguished by their coordinated duets, territorial songs, arm-swinging locomotion and small family group sizes. They are the most speciose of the apes with four extant genera (Hylobates, Hoolock, Symphalangus and Nomascus) distributed across East and Southeast Asia. Of the 20 species, 95 per cent are considered critically endangered or endangered according to the International Union for Conservation of Nature (IUCN) Red List of Threatened Species (Rawson et al., 2011; Fan and Bartlett, 2017; IUCN, 2021). Under the IUCN umbrella are a number of primate specialist groups focusing on specific taxa. The IUCN’s Section on Small Apes (SSA) consists of 105 gibbon conservation practitioners across 21 countries. Steered by an executive committee and connected through a website (https://gibbons.asia/), an email list and social media (Twitter, Instagram and Facebook), the SSA brings together experts to determine the most urgent in-situ and ex-situ actions needed for gibbons. The SSA aids communication between gibbon experts worldwide, assists with direct conservation action and funding, and helps to raise awareness through public engagement events (such as International Gibbon Day held annually on 24 October). SSA members work with gibbons in a wide variety of ways, and much of the scope of the work of SSA members is reflected in this book.

Overview of Chapters This volume contains a diverse mix of chapters covering hylobatid ecology, conservation, phylogenetics and taxonomy. Conservation challenges, practice-based approaches and strategies for recovery are presented for several of Southeast Asia’s rarest species, including the Cao vit gibbon, Nomascus nasutus (Chapter 1); northern yellow-cheeked gibbon, Nomascus annamensis (Chapter 2); Hainan gibbon, Nomascus hainanus (Chapter 3); Bornean white-bearded gibbon, Hylobates albibarbis (Chapter 4); silvery gibbon, Hylobates moloch (Chapter 5); pileated gibbon, Hylobates pileatus (Chapters 6 and 7); Kloss’s gibbon, Hylobates klossii

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Susan M. Cheyne et al.

(Chapter 8); western hoolock gibbon, Hoolock hoolock (Chapters 9, 10 and 11); siamang, Symphalangus syndactylus (Chapters 12 and 13); and white-handed gibbon, Hylobates lar (Chapter 13). All the aforementioned studies reveal the importance of regular field surveying to monitor population dynamics, whilst also assessing key conservation threats and implementing locally relevant conservation strategies. These critically important studies highlight the urgent need for ongoing funding to support field work, particularly for species that are surviving with critically low population numbers, in high-risk areas. Furthermore, they highlight the need to identify sustainable funding models to support conservation programmes that actively involve the local human populations who live alongside critically endangered species. Several chapters argue for the importance of integrating anthropological and historical perspectives, including social, political and cultural approaches, into primate conservation (see Chapters 14, 15 and 16). As these chapters demonstrate, the cultural significance of gibbons to humans is both an asset to understanding how best to engage people in contemporary conservation efforts, as well as a clue to understanding patterns of past and future species loss. The final section of this volume addresses wider issues pertinent to conservation, including hylobatid genetics and phylogenetics. Chapter 17 provides an upto-date assessment of the phylogenetic interrelationships among hylobatids and elucidates the seemingly elusive relationships between the four genera, shedding light on the complexity of hylobatid genomics. Chapter 18 addresses the use of microsatellites in the management of captive gibbons, assessing their use in the feasibility and sustainability of captive breeding programmes and for resolving paternity questions.

The Future of Gibbon Research All gibbons are threatened to varying degrees by a perfect storm of issues: habitat loss through legal and illegal logging and conversion to plantations (large and small scale); habitat fragmentation due to roads, power plants, hydrodams and mining (Rainer et al., 2014); hunting for both bushmeat and traditional medicine; the illegal pet trade (Rainer et al., 2021); and climate change leading to increased forest fires and further habitat loss. A new global threat presented itself in December 2019 in the form of a coronavirus (COVID-19), an infectious disease caused by the SARS-CoV-2 virus. Since then, there has been increased research on the impacts of COVID-19 on fieldwork (Santos et al., 2020), ecotourism (Molyneaux et al., 2021), emerging diseases and landscape conservation (Harrison et al., 2020), and individual species conservation (Hansen et al., 2021). What is less well understood are the long-term impacts of our inability to be on the ground to conserve and protect wildlife habitats, the knock-on effects of reductions in or total loss of funding, the possible decline of small populations due to increased anthropogenic pressures caused by the pandemic, and the susceptibility of

https://doi.org/10.1017/9781108785402.002 Published online by Cambridge University Press

Introduction

3

most primates to the virus. This presents several challenges and opportunities for continuing effective gibbon conservation into the future. Because of the travel bans caused by the outbreak of COVID-19, many gibbon practitioners and researchers were forced to cancel or postpone their fieldwork. The importance of gibbon-range researchers has therefore never been more prominent. Local researchers play key roles in the running of long-term field sites that provide crucial knowledge and information for decision-makers, as well as being more actively involved and more influential in policy-making compared with international researchers (Hu et al., 2019). We are proud that this volume provides a platform for many researchers and conservationists from gibbon-range countries (e.g. China, India, Vietnam, Indonesia and Thailand) to share their knowledge, experiences and ideas for gibbon research and conservation. Unfortunately, none of the authors come from Myanmar, Cambodia or Laos, which still support viable populations of numerous gibbon species. We are also delighted to see international collaborations demonstrated in this volume. The four editors of the volume include one from a gibbon-range country, China, and three from the UK. Among the 18 chapters, 7 are the results of international collaboration, where at least one author from a gibbon-range country has teamed up with at least one international expert. Collaborations can bring new perspectives, ideas, technologies, frameworks and funding, and build capacity in gibbon-range countries. As gibbons know no borders, international collaborations are imperative for their future conservation. Between 11 May and 1 June 2020, SSA members were invited to answer an anonymous semi-structured survey regarding urgent priorities for studying gibbons. Of the 105 SSA members, 81 responded (77 were actively working with gibbons at the time of the survey) across 68 non-governmental organisations and institutions. All gibbon-range countries were represented. Twenty-two priority areas were identified for future gibbon research (number of respondents is shown in parentheses): 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14.

Accurate current and future population projections (n ¼ 24). Habitat loss and restoration (n ¼ 19). Conservation planning and evaluation (n ¼ 14). Understanding general gibbon behaviour (in response to anthropogenic factors) (n ¼ 9). Illegal trade (n ¼ 7). More community engagement in gibbon-range countries (n ¼ 6). Incorporating social science approaches to elucidate conservation issues (n ¼ 6). Supporting long-term projects and datasets (n ¼ 6). Gibbon health (n ¼ 6). Providing guidelines on release and translocations (n ¼ 5). Improved law enforcement (n ¼ 5). Genetic diversity (n ¼ 5). Education and awareness-raising (n ¼ 3). Improve population survey methods through novel approaches (n ¼ 2).

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Susan M. Cheyne et al.

15. 16. 17. 18. 19. 20. 21. 22.

Taxonomy and identification (n ¼ 2). Welfare and health in captivity (n ¼ 2). Reproduction (n ¼ 2). Anti-poaching actions (n ¼ 2). Climate change (n ¼ 1). Encouraging more researchers to study gibbons (n ¼ 1). Comparative studies (n ¼ 1). Collaborations (n ¼ 1).

When asked what challenges respondents faced when bridging research and conservation practice, 28 per cent stated a lack of funding. More than one-fifth of respondents highlighted a lack of support from local partners, communities and/or policy-makers (22 per cent), followed closely by a lack of capacity/time (18 per cent), expertise (e.g. training in research methods; 15 per cent), language barriers (4 per cent) and access to literature (4 per cent). Nine per cent of respondents mentioned ‘other’ challenges associated with current research outputs not being useful for direct conservation action, a lack of support from host country research departments, a lack of interdisciplinary international collaborations, a lack of skilled manpower and political barriers. With this in mind, here we present recommendations for the future of gibbon conservation and research. In general, conservation project actions need to be implemented at a multi-level scale using multiple and adaptive local conservation management approaches. This must include local leadership, integration, capacity building and education to support on-the-ground conservation efforts that are underpinned by scientific monitoring research. In addition, projects need to ensure effective collaboration with multiple stakeholders including government. More specifically to gibbons, each gibbon-range country needs to consider national and local areas of knowledge gaps and barriers to the implementation of gibbon conservation research and action. The following actions are recommended across all gibbon-range countries.  Strengthening coordination among gibbon conservation projects worldwide, including zoos, sanctuaries and rehabilitation centres.  Increase awareness of scientifically sound practice in gibbon conservation and, where possible, ensure publications are open access.  Clearly justify how future research can directly inform conservation action.  Provide multi-lingual IUCN-endorsed guidelines to conservationists, field scientists and decision-makers.  Develop conservation action plans that clarify priorities in gibbon conservation for practitioners, decision-makers and donors.  Ensure the IUCN Red List of Threatened Species is thorough and up to date.  Provide direct technical support and training to implement projects engaged with gibbon conservation, including early-career researchers in gibbon-range countries.  Strengthen collaborations, most notably among gibbon-range country researchers, and share resources (e.g. funding, equipment) and knowledge.

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References Fan, P. and Bartlett, T.Q. (2017). Overlooked small apes need more attention! American Journal of Primatology, 79: ee22658. Hansen, M.F., Gill, M., Nawangsari, V.A., et al. (2021). Conservation of long-tailed macaques: implications of the updated IUCN status and the COVID-19 pandemic. Primate Conservation, 35: 1–11. Harrison, M.E., Wijedasa, L.S., Cole, L.E.S., et al. (2020). Tropical peatlands and their conservation are important in the context of COVID-19 and potential future (zoonotic) disease pandemics. PeerJ, 8: e10283. Hu, Y., Luo, Z., Chapman, C.A., et al. (2019). Regional scientific research benefits threatenedspecies conservation. National Science Review, 6: 1076–1079. IUCN (International Union for the Conservation of Nature) (2021). The IUCN Red List of Threatened Species. Version 2020-1. Available at www.iucnredlist.org/ Molyneaux, A., Hankinson, E., Kaban, M., et al. (2021). Primate selfies and anthropozoonotic diseases: lack of rule compliance and poor risk perception threatens orangutans. Folia Primatologica, 92: 296–305. Rainer, H., White, A. and Lanjouw, A. (eds.) (2014). State of the Apes: Extractive Industries and Ape Conservation. Cambridge University Press, Cambridge. Rainer, H., White, A. and Lanjouw, A. (eds.) (2021). State of the Apes: Killing, Capture, Trade and Ape Conservation. Cambridge University Press, Cambridge. Rawson, B.M., Insua-Cao, P., Manh, H.N., et al. (2011). The Conservation Status of Gibbons in Vietnam. Fauna & Flora International and Conservation International, Hanoi, Vietnam. Santos, W.J., Guiraldi, L.M. and Lucheis, S.B. (2020). Should we be concerned about COVID-19 with nonhuman primates? American Journal of Primatology, 82(8): e23158.

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Taxonomy, Ecology and Conservation of Cao Vit Gibbon (Nomascus nasutus) since Its Rediscovery Peng-Fei Fan and Chang-Yong Ma

1.1

Introduction Gibbons (family Hylobatidae) are small arboreal apes that inhabit tropical and subtropical forests of Southeast Asia, Northwest India and Bangladesh. They are well known for their coordinated vocal duets, small group sizes and acrobatic locomotion, all three characteristics being distinct from great apes (Fan and Bartlett, 2017). All gibbon species prefer fruits when they are available, and rely heavily on ripe juicy fruit (Bartlett, 2011). Because of their critical ecological requirements and low reproductive rate, gibbons are very sensitive to habitat degradation and destruction and to illegal hunting. The Hainan gibbon (Nomascus hainanus), endemic to Hainan Island of China, is the most endangered primate species in the world. Its population declined to nine known individuals in two groups in the 1980s (Liu et al., 1989), but has since increased to more than 30 individuals in five groups after intensive conservation management (Chan et al., 2020). Except for N. hainanus, populations of all other gibbon species are declining (IUCN, 2021). In addition, all gibbon species are suffering habitat loss; on average, each species has lost 11 (range 3–28) per cent of its potential habitat between 2000 and 2014 (Fan and Bartlett, 2017). Consequently, except for the eastern hoolock gibbon (Hoolock leuconedys), which is described as vulnerable, all the other 19 species recognised by the International Union for Conservation of Nature (IUCN) Red List of Threatened Species are listed as endangered (15 species) or critically endangered (four species) (IUCN, 2020). However, gibbons receive little conservation and research attention relative to the great apes (Fan and Bartlett, 2017). Against the background of a global conservation crisis, the rediscovery of the Cao vit gibbon (Nomascus nasutus) in 2002 (La et al., 2002) was one of the most exciting events for gibbon conservationists in the twenty-first century. However, its importance was largely hindered by disputation of its species status. Since its rediscovery, a great deal of research and conservation actions have been taken to conserve this species and its habitat. This chapter provides a comprehensive review of its taxonomy, ecology and conservation.

1.2

Taxonomy and Morphology of Cao Vit Gibbon (N. nasutus) At present, there are seven species of crested gibbons (genus Nomascus) (Thinh et al., 2010a; Mootnick and Fan, 2011; Mittermeier et al., 2013), including three species of

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black gibbons (black crested gibbon, Nomascus concolor; N. hainanus; and N. nasutus) and four species of buff-cheeked gibbons (northern white-cheeked gibbon, N. leucogenys; southern white-cheeked gibbon, N. siki; northern buff-cheeked gibbon, N. annamensis; and yellow-cheeked gibbon, N. gabriellae). As the adult males are almost completely black and their morphological differences are subtle (Figure 1.1a–c), the taxonomy of black gibbons has long been under dispute. Kunckel d’Herculais (1884) first described a specimen of black gibbon from northeastern Vietnam as Hylobates nasutus (there was only one genus – Hylobates – in the Hylobatidae family at that time; see Fan, 2012). Another new species, H. hainanus, was described from a captive male black gibbon from Hainan Island by Thomas (1892). However, de Pousargues (1904) and Pocock (1927) both thought H. nasutus and H. hainanus were synonyms of H. concolor, a species first described by Harlan (1826). Delacour (1951) recognised two subspecies in H. concolor: H. c. concolor in the mainland and H. c. nasutus on Hainan Island. Later, H. c. hainanus was used for the island subspecies (Simonetta, 1957; Groves, 1972). In 1983, Dao Van Tien reported that both of these subspecies were distributed in the mainland of Vietnam and he was the first to suggest the Red River as the geographical boundary between them (Dao, 1983). Geissmann (1989) described a female crested gibbon at the Tierpark in Berlin, which originated from the east bank of the Red River in northeastern Vietnam. This female resembled H. c. concolor in some characteristics but was different in others, and he therefore suggested that this female might represent a new subspecies. Groves and Wang (1990) and Geissmann (1995) considered H. c. nasutus from the east bank of the Red River in the mainland as a distinct subspecies of H. c. hainanus on the island. In 2004, Brandon-Jones et al. (2004) elevated N. nasutus as a species, including N. n. nasutus and N. n. hainanus, different from N. concolor (Nomascus was elevated to a genus by Roos and Geissmann in 2001), and first assigned an English name for N. c. nasutus as the eastern black crested gibbon. However, the taxonomy of black gibbons from the east bank of the Red River remained unsolved because gibbons were thought to be extinct from this area in both China (Tan, 1985) and Vietnam (Geissman et al., 2003). In 2002, Fauna and Flora International (FFI) Vietnam discovered a small gibbon population in a karst forest patch in Trung Khanh district of Cao Bang Province, Vietnam, close to the China–Vietnam international border (La et al., 2002). This population was located on the east bank of the Red River, and it was initially reported as a population of ‘Nomascus sp. cf. nasutus’ (La et al., 2002). In 2006, another three groups were discovered in the neighbouring forest patch on the China side (Chan et al., 2008). Since the rediscovery of this population, more data have been collected regarding its morphology (Mootnick and Fan, 2011), vocalisations (Thinh et al., 2010b, 2011; Feng et al., 2013) and genetics (Monda et al., 2007; Thinh et al., 2010a, 2011). Although males of all three species are black, they can be easily distinguished by the shape of the crest, colour of the chest and visibility of the ear (Figure 1.1a–c). Nomascus concolor and N. hainanus have a sharp crest while N. nasutus has a short crest, creating a round face. In addition, males of N. nasutus have a brown chest.

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(a)

(b)

(c)

(d)

(e)

(f)

Figure 1.1 Diagnostic morphological characteristics of three black crested gibbon species (black crested gibbon, N. concolor; Cao vit gibbon, N. nasutus; Hainan gibbon, N. hainanus). Nomascus concolor: male has a sharp crest (a); female has black chin and a black abdomen with ageing; newborn infant is buff yellow (d). Nomascus nasutus: male has a short crest and a brown chest (b); female has a white face ring and big black crown; newborn infant is black (e). Nomascus hainanus: male has a moderate crest and ears are visible (c); female has a round face and yellow chin; newborn infant is yellow with black forehead (f ). Sources: (a) Zhao Chao; (b) Huang Songhe; (c) Zhao Chao; (d) Tang Yun; (e) Huang Songhe; (f ) Bosco P.L. Chan.

Probably due to the short hair in N. hainanus, the ears are visible from the front (Mootnick and Fan, 2011; Figure 1.1). There are also obvious morphological differences in adult females between N. nasutus, N. concolor and N. hainanus (Mootnick and Fan, 2011). Adult females of N. nasutus have an obvious white face ring and the black crown extends past the nape and across the shoulders. Adult females of N. concolor have a small crown, black chin and black abdomen with age. Adult females of N. hainanus have yellow chins and round faces (Mootnick and Fan, 2011; Figure 1.1d–f). Noticeably, the newborn infant of N. nasutus is black. The newborn infant of

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N. hainanus is grey to buff yellow with some black hairs on the forehead, while the newborn infant of all other Nomascus species are buff yellow (Mootnick and Fan, 2011; Figure 1.1d–f). Both male and female sequences produced in the coordinated duet are also distinguishable (Thinh et al., 2010b, 2011; Feng et al., 2013). Interestingly, not only are male and female acoustic spectrograms different, but also the ways in which males and females coordinate their singing. In N. nasutus, males continue to produce ‘aa’ notes (a short note produced by males) when females start singing the great call sequence, and males respond to the female great call with a coda that consists of more modulated notes. In N. concolor, males stop singing soon after females have sung the great call and respond with a coda that is similar to the normal male sequence after a female has finished the great call. In N. hainanus, males stop when the females begin singing the great call, but the male will respond before the end of the great call sequence (Figure 1.2). Whether this difference in structure is genetically determined or learned by young gibbons (i.e. culture) remains unknown and needs more investigation.

Figure 1.2 Duet sequence produced by three black crested gibbons: (a) Cao vit gibbon, N. nasutus; (b) black crested gibbon, N. concolor; (c) Hainan gibbon, N. hainanus.

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Furthermore, genetic studies also support the theory that these three taxa are distinct species (Monda et al., 2007; Thinh et al., 2010a, 2011). Thinh et al. (2010a) showed that the divergence between N. hainanus and N. nasutus is actually the deepest within Nomascus, and this sister-species pair is a sister clade to all other Nomascus gibbons. They represent the most divergent and evolutionarily distinct species within the genus. If so, the black infant of N. nasutus should be an ancestral trait of Nomascus. How and why newborn infants have evolved a white-grey to buff yellow natal coat in other Nomascus species needs further investigation. ‘Cao vit gibbon’, a name used by local people in some areas of northeastern Vietnam, was used to represent this population in Vietnam and since 2004 has been accepted by primatologists (La and Trinh, 2004).

1.3

Distribution and Population Nomascus nasutus was originally thought to be widespread east of the Red River in both southern China and northern Vietnam, which is dominated by a karst limestone formation (Zhou et al., 2003; Do Tuyet, 2010). However, because of uncontrolled logging and agricultural encroachment (Do Tuyet, 2010), much of the forest in this area has been severely degraded. As a result, the N. nasutus population had declined rapidly and was considered extinct in China in the 1950s (Tan, 1985) and in Vietnam in 1960s (Geissmann et al., 2003). Numerous field and interview surveys were conducted during the 1990s in the previous range of the species in Vietnam, but no population was confirmed (reviewed in La and Trinh, 2004) until a small remnant population was rediscovered by an FFI survey team in Trung Khanh district of Cao Bang Province, Vietnam, in 2002 (La et al., 2002, Figure 1.3). After that, several surveys were conducted at the site and a population of up to 10 groups was confirmed (Geissmann et al., 2003; Trinh, 2004; La, 2005; Vu et al., 2005). In 2006, a small population with three groups was observed in the same forest patch on the China side (Chan et al., 2008). To obtain accurate information of population size in both countries, two transboundary surveys were conducted in 2007 and 2016. The surveys indicated that there were 17–18 groups including 102–110 individuals in 2007, and this population increased to 20–22 groups with 107–136 individuals in 2016 (Ma et al., 2019; Figure 1.3), making it the second rarest ape species in the world, after N. hainanus (Zhou et al., 2005). It is now listed as critically endangered on the IUCN’s Red List of Threatened Species (IUCN, 2020), and considered one of the ‘world’s 25 most endangered primates’ (Long and Nadler, 2009).

1.4

Habitat and Climate The last refuge of N. nasutus is a karst forest patch that is bordered by two branches of the Quay Son River (22
490 5900 N, 106
220 3500 E, 486–926 m above sea level; Fan et al., 2013a). However, there are historical gibbon records (e.g. in Difangzhi) from

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Figure 1.3 Distribution of the only known Cao vit gibbon (Nomascus nasutus) population along

the China–Vietnam international border.

widely across Guangxi Province, showing a wider distribution of gibbons that may well have been this species, and presumably reported from landscapes that were not just karst. This refuge is characterised by a typical karst limestone landscape consisting of densely packed outcrops, sharp-peaked mountains with very steep slopes and ridges, doline depressions and interconnected collapsed valleys. The site is surrounded by broad alluvial valley bottoms consisting mainly of cultivated land, settlements and secondary vegetation on isolated karst features (Fan et al., 2013a). At first glance, the karst forest habitat of N. nasutus is a highly unusual gibbon habitat; besides N. nasutus, only two gibbon populations are known to live in karst forest, namely the white-cheeked gibbons N. siki and N. leucogenys in Phong Nha-Ke Bang National Park in Vietnam (Ruppell, 2007). The forest was not protected before the rediscovery of the species and was degraded by intensive human activities (as indicated by charcoal-making signs in nearly every valley). Local people used the forest for timber and fuelwood collection, charcoal production, agricultural cultivation, livestock grazing and food gathering before the reserves were established (La and Trinh, 2004; Fan et al., 2011). The mean canopy height in the site was 10.5 m, with 71 per cent of trees between 5 and 10 m high (Fan et al., 2013a), making it the gibbon habitat with the lowest canopy height reported. However, tree density was high and the number of

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trees with diameter at breast height of 10 cm or more in one 20  20 m plot was on average 21 (range 9–36, n ¼ 44). Plant diversity was also high, with 113 tree species and 46 woody liana and epiphyte species in 113 genera in 60 families recorded in 44 plots (Fan et al., 2011). Climate in the area shows great seasonal and annual variation. The monthly mean temperature varied from 9.8
C in February 2008 to 26.6
C in September 2008 (Fan et al., 2010). The lowest temperature was below 8
C and mean monthly temperature was below 20
C between November and March, during which rainfall was very limited. The rainy season normally starts from May to October with the coming of monsoon, but annual variation exists. Annual precipitation was 1804 mm in 2008 and 1363 mm with less rainfall between August and October in 2009 (Fan et al., 2010). Fruit production shows seasonal variation, with more fruit availability between May and September (Fan et al., 2012), generally in accordance with the rainy season. The abundance of buds peaks in April. Figs do not show the obvious pattern of seasonal abundance observed in fruits and buds, but few figs were available between March and April 2009. The mature leaves eaten by the gibbons were available throughout the year (Fan et al., 2012).

1.5

Habitat Use and Locomotion Pattern Nomascus nasutus occupies home ranges of approximately 130 ha (Fan et al., 2010), which is comparable with the home range size of gibbons living in northern seasonal habitats (N. hainanus, 300–500 ha, Liu et al., 1989; N. concolor, 151 ha, Fan and Jiang, 2008a; H. leuconedys, 93 ha, Zhang et al., 2014), but substantially larger than that of gibbons living in tropical forests (on average 40 ha, reviewed in Bartlett, 2011). Important food trees were patchily distributed in their habitat (Fan et al., 2015). In order to secure food requirements across different seasons, N. nasutus occupies a large home range to cover the distribution of different food species. Low densities of important food species caused by human activities may also explain why N. nasutus occupies such large home ranges. However, comparative phylogenetic analyses have shown that the large home range in N. nasutus is likely natural for the species rather than an artefact of a remnant population existing in a possibly suboptimal habitat refuge (Bryant et al., 2015). Although canopy height is noticeably lower compared with the habitat of other gibbons, the combination of locomotion modes performed by N. nasutus is dominated by brachiation (59.6 per cent) for foraging and travelling in the canopy, like other gibbons (Fleagle, 1976; Gittins, 1983; Cannon and Leighton, 1994; Fan et al., 2013a). Nomascus nasutus climbs (including bridging) more often (20.5 per cent) and walks less often (1 per cent) compared with other gibbon species, except the largest gibbon, the siamang Symphalangus syndactylus (reviewed in Fan et al., 2013a). Differences in body weight and support size may explain the differences in locomotion patterns observed. The larger the size of the gibbons, the less likely they are able to brachiate and jump because large animals are more liable to break supports and risk falling. The

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structure of the lower karst forest may also cause this difference. As previously mentioned, tree density is still high in this site. Gibbons always climb in trees with dense branches (personal observation of several gibbon species); in contrast, tall trees with large branches which provide support for walking are rare in their habitat. Brachiation is energy conserving because of the alternating transformation of potential energy into kinetic energy and vice versa (Fleagle, 1974; Preuschoft and Demes, 1984; Bertram et al., 1999), and has less energetic cost than climbing (Jungers and Stern, 1984). Therefore, N. nasutus may spend more energy when travelling compared with other gibbons. Nomascus nasutus confines locomotion chiefly to the middle stratum of 5–10 m height (84.4 per cent) because the canopy connectivity of this stratum is greater than that of the upper canopy (>10 m in height), and moving close to the ground in the lower stratum may be dangerous due to the presence of terrestrial predators. Branches (2–10 cm) are most frequently used as supports (62.4 per cent), followed by twigs (10 cm, 2.5 per cent) (Fan et al., 2013a). Nomascus nasutus also shows age–sex variation in their locomotion pattern (Fan et al., 2013a). Climbing and bridging (with at least one limb attached for support) are thought to be safer than faster brachiation and leaping. Compared with males and juveniles, females climb and bridge more often regardless of whether they are carrying infants or not. In summary, the ability to negotiate low trees and small branches enables N. nasutus to efficiently forage in their degraded karst forest and defend their territories.

1.6

Diet Flexibility During 2,432 observation hours, N. nasutus were observed to consume items from 81 plant species (approximately 50 per cent of total plant species recorded on the site) and several animal species (Fan et al., 2011). They did not use plant species based on their abundance, and relied heavily on some uncommon species, such as Ficus hookeriana, Spondias lakonensis and Choerospondias axillaris (Fan et al., 2011). However, these species have been targeted by local people and densities are therefore low in the forest (Fan et al., 2011). Fig species (genus Ficus) and liana species play a very important role in the diet of N. nasutus. The gibbons have been observed consuming eight different fig species. However, they consume three of them more often than others and these species make up a large proportion of their diet (Ficus glaberrima, 13 per cent; Ficus hookeriana, 6.6 per cent; Ficus microcarpa, 1.9 per cent; Fan et al., 2011). Nomascus nasutus consume F. glaberrima and F. hookeriana whenever they are available. They are considered important monthly food items, defined as the minimum number of foods comprising 75 per cent of the monthly diet (Hill, 1997) during a 23-month study (Fan et al., 2011). The gibbons occasionally consume other fig species, and as a result these gibbons do not show a positive relationship between total fig availability and

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consumption (Fan et al., 2012). However, nutritional analyses have shown that these two species do not contain more crude protein, water-soluble sugar or crude fat compared with other fig species (Ma et al., 2017). Twenty-seven liana species contributed 18.9 per cent of the diet of N. nasutus (Appendix A in Fan et al., 2011). Tetrastigma pubinerve provides fruit between October and December and young leaves year round. In the study by Fan et al. (2011), it proved to be another important species for N. nasutus in 7 out of 23 months, and it contributed more than 5 per cent to the overall diet. Trichosanthes kirilowii produces young leaves year round and N. nasutus consumes the young leaves of this species between December and February (total contribution, 3.1 per cent; Fan et al., 2011). Nomascus nasutus is less frugivorous compared with other gibbons living in southern tropical forest (reviewed in Bartlett, 2011), but their diet of fruit is similar to that of N. concolor (Fan et al., 2009), H. leuconedys (Fan et al., 2013b) and S. symphalangus (reviewed in Bartlett, 2011). This is mainly caused by the unavailability of fruit between December and April (Fan et al., 2012). Like all other gibbons (Bartlett, 2011), N. nasutus prefer fruit when it is available (Fan et al., 2012). Here we provide proportional diet details to supplement the actual feeding times published in Fan et al. (2012). Nomascus nasutus spent more than 60 per cent of their feeding time on fruit between May and October when fruit was more abundant, except in July for one group (Figure 1.4). Leaves and buds contributed less than 2 per cent between June and September for both groups (Figure 1.4). They shifted to a diet consisting mainly of leaves and buds (>50 per cent) when fruit was not abundant between December and April (Figure 1.4). Leaves and bud consumption reached a peak in March (>95 per cent) while the proportion of fruit and figs was less than 2 per cent. Animal prey, especially invertebrates, contributed substantially between July and September during the rainy season. As a result, fruit including figs accounted for 52 per cent of the annual proportional diet; the remainder was made up of leaves and buds (35.2 per cent), animals (9.2 per cent) and others (averaged from two groups in figure 3 in Fan et al., 2012).

1.7

Activity Budget Nomascus nasutus left their sleeping trees just after sunrise, and entered sleeping trees on average 88 minutes before sunset (Fei et al., 2012). On average, they spent 10.4 hours outside sleeping trees during which they spent 37.3 per cent resting, 23.9 per cent feeding, 24.4 per cent travelling and 14.2 per cent engaging in social behaviour (averaged from monthly proportional activity time budget of two groups between January and December 2009). In comparison with other gibbons, N. nasutus did not increase active time (Table_1.1) or feeding time (reviewed in Fan et al., 2008). Increased foraging time would translate into much more intensive use of the available resources, and thus gibbons appear to ensure continued access to highly favoured resources by exploiting their ranges less intensively (Bartlett, 2009).

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Figure 1.4 Proportional diet of two Cao vit gibbon (N. nasutus) groups between January and

December 2009.

Nakayama et al. (1971) reported that the energy expenditure of outdoor-living captive Japanese macaques (Macaca fuscata) at 5.2
C is 2.5 times greater than that at 29.5
C. Although similar research has never been conducted in gibbon species, it seems there are thermoregulatory costs for N. nasutus at high altitudes in cold months: the gibbons increased resting time and decreased time engaging in social activities (Fan et al., 2012); in addition, they always huddled together in the sunshine in the tops of trees (personal observation) and huddled together in sleeping trees in cold months (Fei et al., 2012). These behavioural strategies were also adopted by N. concolor, H. leuconedys and skywalker hoolock gibbons (Hoolock tianxing) living in montane forests (Fan et al., 2008; Fan et al., 2013b; Fei et al., 2019).

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Table 1.1 Time leaving and entering sleeping trees and active period of different gibbon species.

Species

Study site

Nomacus concolor Nomascus nasutus Hoolock hoolock Hoolock leuconedys Symphalangus syndactylus

Dazhaizi, Wuliangshan, China Bangliang, Jingxi, China Lawachara and Chunati, Bangladesh Nankang, Gaoligong, China Ulu Sempam Kuala Lompat Sungai Dal Siberut Khao Yai, Thailand

Hylobates agilis Hylobates klossii Hylobates lar

Time leaving sleeping trees after sunrise (minutes)

Time entering sleeping trees before sunset (minutes)

33 4 –2

128 88 153

A few minutes –12 7 2 –15 to þ15

120 126 85 204

Active time period (hours) 8.6 10.1 9.1 10.1 11.1

8.7

Reference Fan and Jiang (2008b) Fei et al. (2012) Ahsan (2001) Fan et al. (2013b) Chivers (1974) Gittins (1982) Whitten (1980) Bartlett (2009)

Cao Vit Gibbon: Taxonomy, Ecology, Conservation

1.8

17

Social Structure and Reproduction Most groups consisted of one adult male and two adult females, and the mean group size was 6.3 individuals in 2007 and 6.4 in 2016 (Ma et al., 2019). According to intensive population monitoring of three groups in China, both females bred repeatedly (Fan et al., 2015). The inter-birth interval was 31 months (range 23–38 months, n ¼ 8), which is comparable to other gibbon populations (Fan et al., 2015).

1.9

Conservation Since the rediscovery of this population, conservation activities including the establishment of patrol teams, livestock removal (e.g. goats in Vietnam), fuelwood plantation, energy-saving stove construction, conservation education and ecological research have been implemented by FFI, our research team and local governments in both countries (Ma et al., 2019). Transboundary cooperation between the governments of China and Vietnam was established to counter wildlife hunting, protect against forest fires and exchange experience on monitoring, programme management, public education and law enforcement (Ma et al., 2019). No hunting of gibbons has been reported since the discovery of the species. The Cao Vit Gibbon Conservation Area (CVGCA) was established in Vietnam in 2007. In China, the Bangliang Gibbon Nature Reserve was established in 2009 and was upgraded to a National Nature Reserve status in 2013. All suitable habitat currently used by N. nasutus has been legally protected by these reserves. Charcoal making, fuelwood collection and trap setting disappeared completely. Non-timber production has only occasionally occurred inside the reserves. No forest has been cleared for cultivation but some corn fields were maintained inside reserves. The current main threat to N. nasutus habitat is cattle grazing in China (Ma et al., 2019). However, with the construction of a patrol road inside the nature reserve by border armies in 2012, it is easier for local people to graze their goats and cows inside the forest. The effect of grazing must be evaluated. Because of the strict conservation of this gibbon population and their habitat in the past decade, sympatric macaque (rhesus macaque, Macaca mulatta; Assam macaque, M. assamensis; and stump-tailed macaque, M. arctoides) populations have increased rapidly. Increased macaque populations may compete for food with gibbons in this small forest patch, which deserves more investigation and research (Chen et al., 2020). Habitat evaluation and a population viability analysis suggested that this population is close to its carrying capacity (Fan et al., 2013c). Remote sensing and geographic information system techniques estimated the high-quality forest in the area to be 2,176.8 ha (Fan et al., 2013c). Given that the home range of one group is approximately 130 ha (Fan et al., 2010) and that the area used exclusively by the group is 107 ha (Fei et al., 2012), this forest can support approximately 20 groups. It can support approximately 26 groups if the low-quality habitat was rehabilitated to support gibbons. In 2016, 20–22 groups were recorded in this area (Ma et al., 2019),

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suggesting it was very close to reaching the carrying capacity. Two potential habitats were located in a neighbouring forest. These potential habitats connected with the current gibbon habitat by a narrow forest corridor (900 m in length) above an underground river (Fan et al., 2013c). Forest quality in potential habitats was not as good as gibbon habitat, but fine-scale habitat surveys have not yet been conducted. As this forest patch is the last habitat for N. nasutus, we suggested that it should be strictly protected and any grazing and agriculture should be prohibited (Fan et al., 2013c). Habitat restoration to increase carrying capacity is urgently required for N. nasutus conservation (Fan et al., 2013c). Because natural regeneration of karst forest takes a long time and large food trees have been extracted in peripheral areas whilst other species have remained, planting indigenous important food species in suitable degraded habitats to accelerate forest restoration was suggested (Fan et al., 2011). Currently, the two potential habitats, mostly in Vietnam, are outside the CVGCA and have not been protected. There is only a narrow corridor connecting these potential habitats and the current gibbon habitat. We suggest that the Vietnam government expands the CVGCA in order to protect this corridor and the potential habitats (Fan et al., 2013c).

1.10

Conclusions Nomascus nasutus is a distinct species of N. concolor and N. hainanus. There is only one confirmed population of approximately 120 individuals surviving in a small karst forest along the China–Vietnam border, making it the second rarest ape species in the world. Although their habitat has been degraded by human activities, they seem well adapted to life in karst forest and have demonstrated a series of adaptive behavioural strategies, including (1) maintaining similar locomotor patterns as other gibbons while using smaller supports in lower forest; (2) consuming diverse food types and species, and digesting and obtaining energy from fallback foods (leaves) when preferred foods (fruit) are not available in winter; (3) occupying a large home range in response to the patchy distribution and low density of important food species and (4) increasing resting and huddling together in winter to conserve energy. However, the deaths of two juveniles in a cold winter (Fan et al., 2010) suggest that N. nasutus might face a serious energy stress in winter. Future research should focus on (1) long-term population monitoring to obtain life-history and reproductive parameters of this population, (2) techniques to restore the karst forest, (3) evaluating impacts of goat grazing on habitat restoration, (4) evaluating impacts of increasing human disturbance along the border patrol road on gibbon behaviour and (5) evaluating the impacts of intra- and inter-species food competition on the reproductive and social systems of N. nasutus. Habitat conservation and restoration is crucial for the long-term survival of this population and planting indigenous important food species in degraded sites should be considered a part of the long-term management of the site. As this population and its habitat cross the international border between China and Vietnam, conservation of

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this species would benefit from the close cooperation between conservation agencies in the two countries.

Acknowledgements Our long-term study was supported by the National Natural Science Foundation of China (#30900169; #31822049), International Foundation for Science (IFS), Conservation Leadership Programme (CLP), Fauna and Flora International (FFI), Idea Wild, and Association of Zoos and Aquariums (AZA). We would like to thank the Bangliang Nature Reserve for giving us the research permission and thank reserve staff for their needed support.

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Feng, J.J., Ma, C.Y., Fei, H.L., Cui, L.W. and Fan, P. (2013). Call sonograms of eastern black crested gibbon (Nomascus nasutus). Acta Theriologica Sinica, 33: 203–214. Fleagle, J.G. (1974). Dynamics of a brachiating siamang Hylobates (symphalangus) syndactylus. Nature, 248: 259–260. Fleagle, J.G. (1976). Locomotion and posture of the Malayan siamang and implications for hominoid evolution. Folia Primatologica, 26: 245–269. Geissmann, T. (1989). A female black gibbon, Hylobates concolor subspecies, from northeastern Vietnam. International Journal of Primatology, 5: 455–476. Geissmann, T. (1995). Gibbon systematics and species identification. International Zoo News, 42: 467–501. Geissmann, T., La, T.Q., Trinh, D.H., et al. (2003). Rarest ape rediscovered in Vietnam. Asian Primates, 8: 8–10. Gittins, S.P. (1982). Feeding and ranging in the agile gibbon. Folia Primatologica, 38: 39–71. Gittins, S.P. (1983). Use of the forest canopy by the agile gibbon. Folia Primatologica, 40: 134–144. Groves, C.P. (1972). Systematics and phylogeny of gibbons. In Rumbaugh, D.M. (ed.), Gibbon and Siamang, Vol. 1. Karger, Basel: 1–89. Groves, C. and Wang, Y.X. (1990). The gibbons of the subgenus Nomascus (Primates, Mammalia). Zoological Research, 11: 147–154. Harlan, R. (1826). Description of a hermaphrodite orangutang, lately living in Philadelphia. Journal of the Academy of Natural Sciences of Philadelphia, 5: 229–236. Hill, D.A. (1997). Seasonal variation in the feeding behaviour and diet of Japanese macaques (Macaca fuscata yakui) in lowland forest of Yakushima. American Journal of Primatology, 43: 305–322. IUCN (International Union for the Conservation of Nature) (2021). The IUCN Red List of Threatened Species. Version 2020-1. Available at www.iucnredlist.org/ Jungers, W.L. and Stern, J.T. (1984). Kinesiological aspects of brachiation in lar gibbons. In Preuschoft, H., Chivers, D.J., Brockelman, W.Y. and Creel, N. (eds.), The Lesser Apes. Edinburgh University Press, Edinburgh: 119–134. Kunckel d’Herculais, J. (1884). Le Gibbon du Tonkin. Sci. Nature, 2(33): 86–90. La, Q.T. (2005). Integrated report on capacity assessment of the community patrol group in training on using equipment for and recommendation of an annual work plan for monitoring the Eastern black crested gibbon (Nomascus nasutus nasutus) population. Fauna and Flora International, Indochina Programme, Hanoi, Vietnam. La, Q.T. and Trinh, D.H. (2004). Status review of the Cao vit black crested gibbon (Nomascus nasutus nasutus) in Vietnam. In Nadler, T., Streicher, U. and Ha, T.L. (eds.), Conservation of Primates in Vietnam. Haki Publishing, Vietnam: 90–94. La, Q.T., Trinh, D.H., Long, B. and Geissmann, T. (2002). Status review of black crested gibbons (Nomascus concolor and Nomascus sp. cf. nasutus) in Vietnam. In Caring for Primates. Abstracts of the XIXth Congress of the International Primatological Society, 4–9 August, 2002, Beijing, China: 131–132. Liu, Z.H., Zhang, R.Z., Jiang, H.S. and Southwick, C. (1989). Population structure of Hylobates concolor in Bawangling Nature Reserve, Hainan, China. American Journal of Primatology, 19: 247–254. Long, Y.C. and Nadler, T. (2009). Eastern black crested gibbon Nomascus nasutus (Kunkel d’Herculais, 1884) China, Vietnam. In Mittermeier, R.A., Wallis, J., Rylands, A.B., et al. (eds.), Primates in Peril: The World’s 25 Most Endangered Primates 2008–2010. IUCN/

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SSC Primate Specialist Group (PSG), International Primatological Society (IPS), and Conservation International (CI), Arlington, VA: 60–61. Ma, C.Y., Liao, J.C. and Fan, P. (2017). Food selection in relation to nutritional chemistry of Cao vit gibbons in Jingxi, China. Primates, 58: 63–74. Ma, C.Y., Trinh-Dinh, H., Nguyen, V.T., et al. (2019). Transboundary conservation of the last remaining population of the Cao vit gibbon Nomascus nasutus. Oryx, 54(6): 776–783. Mittermeier, R.A., Rylands, A.B. and Wilson, D.E. (2013). Handbook of the Mammals of the World. Volume 3: Primates. Lynx Edicions, Barcelona. Monda, K., Simmons, R.E., Kressirer, P., Su, B. and Woodruff, D.S. (2007). Mitochondrial DNA hypervariable region-1 sequence variation and phylogeny of the concolor gibbons, Nomascus. American Journal of Primatology, 69: 1285–1306. Mootnick, A.R. and Fan, P. (2011). A comparative study of crested gibbons (Nomascus). American Journal of Primatology, 73: 135–154. Nakayama, T., Hori, T., Nagasaka, T., Tokura, H. and Tadaki, E. (1971). Thermal and metabolic responses in the Japanese monkey at temperatures of 5–38
C. Journal of Applied Physiology, 31: 332–337. Pocock, R.I. (1927). The gibbons of the genus Hylobates. Proceeding of the Zoolological Society of London, 97: 719–741. Preuschoft, H. and Demes, B. (1984). Biomechanics of brachiation. In Preuschoft, H., Chivers, D.J., Brockelman, W.Y. and Creel, N. (eds.), The Lesser Apes. Edinburgh University Press, Edinburgh: 96–118. Roos, C. and Geissmann, T. (2001). Molecular phylogeny of the major Hylobatid divisions. Molecular and Phylogenetic Evolution, 19: 486–494. Ruppell, J. (2007). The gibbons of Phong Nha-Ke Bang National Park in Vietnam. Gibbon Journal, 3: 50–55. Simonetta, A. (1957). Catalogo e sinonimia annotata degli ominoidi fossili ed attuali (1758–1955). Atti della Società toscana di scienze naturali Set B, 64: 53–113. Tan, B. (1985). The status of primates in China. Primates Conservation, 5: 63–81. Thinh, V.N, Rawson, B., Hallam, C., et al. (2010a). Phylogeny and distribution of crested gibbons (genus Nomascus) based on mitochondrial cytochrome b gene sequence data. American Journal of Primatology, 72: 1047–1054. Thinh, V.N., Nadler, T., Roos, C. and Hammerschmidt, K. (2010b). Taxon-specific vocal characteristics of crested gibbons (Nomascus sp.). In Nadler, T., Rawson, B. and Thinh, V.N. (eds.), Conservation of Primates in Indochina. Frankfurt Zoological Society and Conservation International, Hanoi, Vietnam: 121–132. Thinh, V.N., Hallam, C., Roos, C. and Hammerschmidt, K. (2011). Concordance between vocal and genetic diversity in crested gibbons. BMC Evolutionary Biology, 11: 36. Thomas, O. (1892). Note on the gibbon of the island of Hainan (Hylobates hainanus, sp. n.). Annals and Magazine of Natural History, 9(6): 145–146. Trinh, D.H. (2004). A survey on the Cao vit gibbon (Nomascus nasutus) in Trung Khanh, Cao Bang Province: survey results and training for local people in survey techniques. Fauna and Flora International, Indochina Programme, Hanoi, Vietnam. Vu, N.T., Nguyen, X.D., Nguyen, M.H., Luu, T.B. and Nguyen, T.H. (2005). Survey and assessment of the Cao vit gibbon population, Phong Nam – Ngoc Khe Proposed Species/ Habitat Conservation Area, Trung Khanh District, Cao Bang Province. Fauna and Flora International Vietnam Programme, Hanoi.

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Whitten, P.L. (1980). The Kloss gibbon in Siberut rainforest. PhD thesis, University of Cambridge. Zhang, D., Fei, H.L., Yuan, S.D., et al. (2014). Ranging behavior of eastern hoolock gibbon (Hoolock leuconedys) in a northern montane forest in Gaoligongshan, Yunnan, China. Primates, 55: 239–247. Zhou, J., Wei, F.W., Li, M., et al. (2005). Hainan black crested gibbon is headed for extinction. International Journal of Primatology, 26: 453–465. Zhou, Y.Y., Li, S.S. and Huang, T.F. (2003). Features of karst forest ecosystem in China and its conservation in utilization: a case study on Maolan, Mulun, Nonggang typical karst forests in southwest China. Journal of Guangxi Teachers College (Natural Science Edition), 20: 1–7.

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Conservation Status of the Northern Yellow-Cheeked Crested Gibbon (Nomascus annamensis) in Vietnam An Update Duc Minh Hoang, Bang Van Tran, Chuong Van Hoang and Herbert H. Covert

2.1

Introduction The northern yellow-cheeked crested gibbon (Nomascus annamensis) was formally diagnosed in 2010 following years of discussion about the taxonomic uncertainty of gibbons distributed between the currently understood species’ boundaries for the yellow-cheeked gibbon (N. gabriellae) and the southern white-cheeked gibbon (N. siki) (Van et al., 2010), and now is listed as endangered by the International Union for Conservation of Nature (IUCN) (Van et al., 2020). In Vietnam, its distribution range is between approximately 14
000 and 16
500 N, with potential overlap with N. siki in the northernmost portion of this range (Nguyen et al., 2017; Hoang et al., 2018). Nomascus annamensis is found in evergreen and semievergreen forests (Rawson et al., 2011) at elevations between 400 m and as high as 1,500 m above sea level in Vietnam (Ha et al., 2011), but is also recorded at a lower elevation of approximately 100 m in Veun Sai-Siam Pang or in Ratanakiri Province, Cambodia (Rawson et al., 2011; Kidney et al., 2016). Hoang et al. (2018) reported the presence of at least 305 groups of this species in Vietnam, primarily confined to protected areas. We assume that the total population of the species must be larger than 305 groups because there have been only a few studies focusing on gibbon surveys in a small number of protected areas, and many of the reports are opportunistic records from other biodiversity surveys. While the species is known to be distributed across the Central Annamites, there are large forested areas on the eastern slopes of this range in Quang Ngai and Binh Dinh provinces that have not been adequately surveyed. This chapter aims to provide an estimate of population size of N. annamensis on the eastern slope of the Central Annamites and update the conservation status of this species in Vietnam. We conducted acoustic surveys to estimate the density of N. annamensis in An Toan Nature Reserve (NR) and two adjacent forest areas in Binh Dinh and Quang Ngai provinces. We also review all available documentation on

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the species, collected reliable coordinates of gibbon groups and predict the potential distribution of this species using environmental niche modelling (ENM).

2.2

Materials and Methods

2.2.1

Study Area The surveys were conducted in contiguous forested areas across the eastern slope of the Central Annamites in Binh Dinh and Quang Ngai provinces, Vietnam (Figure 2.1). We focused on three areas, including the 20,140-ha West Ba To Proposed NR of Quang Ngai Province in the north; An Toan NR, a 22,450-ha protected area in the centre; and a 15,000-ha forest block in Vinh Son Commune, Vinh Thanh District of Binh Dinh Province in the south. This area has a mountainous terrain, ranging from 400 to 1,300 m above sea level, with a complex stream system. The study area experiences a tropical climate with two distinct seasons, a rainy season from May to November and a dry season from December to April. The annual rainfall ranges between 2,000 and 3,300 mm (Nguyen et al., 2000; Biodiversity Conservation Agency, 2014). The vegetation types are dominated by low montane evergreen forest interspersed with grassland patches, scattered shrubs and cultivated land (FIPI, 2014). There are three villages with at least 900 people living inside the unprotected area of An Toan NR (An Lao Statistical Department, 2019) and more than 3,300 people living in Vinh Son Commune (Vinh Thanh Statistical Department, 2019). Over 90 per cent of people belong to the Bahnar ethnic group whose livelihood relies partly on forest products (Nguyen and Ho, 2019). There is a road to the interior of An Toan NR and another road cutting through the forest of Vinh Son Commune.

2.2.2

Survey Methods Field surveys were conducted between January and April 2015 and in April 2016. Gibbon density was estimated using fixed-point counts as described by Brockelman and Ali (1987). This method relies on the frequent morning loud calls of gibbons (Brockelman and Ali, 1987; Brockelman and Srikosamatara, 1993). In total, 54 listening posts, comprising 30 posts in An Toan NR, 14 posts in West Ba To PNR and 10 posts in Vinh Son Commune, were set up (Figure 2.1). Of the posts, 38 were surveyed for 3 days and 16 were surveyed for 2 days. Since listening posts were arranged approximately 2–3 km from one another to allow coverage of a large survey area (Gilhooly and Cheyne, 2012), they are not suitable for triangulation for many calls (Brockelman et al., 2009; Gilhooly and Cheyne, 2012). To minimise the uncertainty in determining the distance from the listening post to the calling group, surveyors identified the distance from their locations to all nearby mountain or hill summits in advance. We conducted surveys in the morning from 05:00 to 08:30 hours. For every gibbon call, the surveyors recorded start and end times of the bout, compass bearing and

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Figure 2.1 Map of field study area.

estimated distance to the group or individual (in metres). It was also noted whether the call was a solo male or female or a mated pair duet. We mapped locations of all individual groups using the recorded compass bearings, estimated distances from listening posts to the animal/group, and coordinates of the listening posts. Records are considered separate groups if they were mapped more than 500 m apart (Brockelman and Ali, 1987). If two duets were heard at the same time or overlapped in time, and more than 500 m apart, they were judged to be produced by two groups (Jiang et al., 2006).

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To assess gibbon group density, only duet vocalisations are used following Rawson et al. (2009). Gibbon calling probability (p1) at each survey area and the correction factor for an m-day survey (pm) is calculated following Jiang et al. (2006): pm ¼ 1  ð1  p1 Þm and

p1 p1 N1 ¼ ¼ ; pm 1  ð1  p1 Þm N 2

(2.1)

where p1 is calling probability, N1 is averaged number of gibbon groups detected in one day, and Nm is cumulative number of gibbon groups detected in m-day period. For m ¼ 2, p1 is estimated by expanding the denominator of Eq. (2.1) as: 2  p1 ¼

N2 N2 or p1 ¼ 2  N1 N1

For m ¼ 3, p1 is estimated by expanding the denominator of Eq. (2.1) as: p21

rffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi  N3 1 4  N3  3p1 þ 3 ¼ ð 0 < p1 < 1 Þ ! p 1 ¼ 3 3 N1 N1 2

The total estimated number of gibbon groups at each listening post (Xi) and the density of gibbon groups in the total survey area (D) were then estimated using the following equations: Pn Ni Xi Xi ¼ and D ¼ Pi¼1 n pm i¼1 ai , groups heard in the m-day period at a where Ni is the cumulative number of gibbon listening post i, Xi is an estimated number of gibbon groups at the listening post i, ai is the survey area at the listening post i, and n is the number of listening posts. Standard deviation (SD) is calculated following Vu and Rawson (2011) as follows: Var ðM Þ Var ðNGÞ ¼ Var ðDGÞ  A2 ¼ Pn  A2 i¼1 ai SDðNGÞ ¼ 1:96  SQRT ðVar ðNGÞÞ where NG is the number of groups in the whole area, DG is group density, A is the P total suitable habitat, M is estimated group per post, and ni¼1 ai is total survey areas around posts. Since the surveys were conducted in each location on different dates, we predicted p1 for each area separately. Reports on the maximum hearing distance for gibbon surveys vary from study to study. Some studies suggest that in good conditions one can hear a gibbon’s vocalisation 1.5 km in all directions (Duckworth et al., 1995; Traeholt et al., 2005); however, in hilly terrains, it has been suggested that not all groups within 1 km can be heard (Brockelman et al., 2009). In contrast, a maximum hearing distance of about 2 km was reported for N. annamensis in the mountainous area of Kong Cha Rang NR (Vu and Dong, 2015). In this study, we conservatively

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applied the maximum hearing distance of 1.5 km (Kidney et al., 2016) to estimate the density of gibbons in the area, meaning each post covered an area of 7.07 km2.

2.2.3

A Review of Conservation Status and Predicting Species Distribution We reviewed all available documents on the distribution, density and population size of the species in Vietnam. Information and/or data were classified based on the scale and method of original studies (e.g. acoustic survey, line transect survey or opportunistic observation). We collected all reliable locations of groups of gibbons from scientific papers and unpublished reports, including Hoang et al. (2005), Vu et al. (2007), Nguyen et al. (2010), Van et al. (2010), Ha et al. (2011), Bui et al. (2019) and information from this study for species distribution modelling (SDM). Since most presence-only records are associated with just a few protected areas, we thinned our dataset by setting the minimum distance between records to at least 1 km to reduce spatial sampling bias (Aiello-Lammens et al., 2015) and avoid inflation of accuracy measures (Veloz, 2009). We modelled the suitable habitat for the gibbons using MaxEnt version 3.4.1 (Phillips et al., 2006). We applied the default setting of MaxEnt as recommended by the model developers (e.g. regularisation multiplier ¼ 1, maximum number of background points ¼ 10,000, maximum iterations ¼ 5,000, prevalence ¼ 0.5) (Phillips and Dudik, 2008). To evaluate the performance of the model, we applied cross-validated replicated run types with 30 replications (Jarnevich and Young, 2015). Model performance was evaluated using the area under the receiver operating curve (AUC), which is a common practice in ecological modelling (Merow et al., 2013). In MaxEnt, AUC ranges between 0.0 and 1.0; values above 0.5 are considered better than random, and those above 0.9 are considered highly accurate (Elith et al., 2011). We prepared 19 available bioclimatic variables for Vietnam from WorldClim at a resolution of 30 arc-second (approximately 1 km2) (Hijmans et al., 2005). We first conducted our modelling using all variables to determine the most useful predictive variables as well as variables that made very low contributions to the spatial distribution model. We then explored the correlation between variables in our study area using the ENM tool (Warren et al., 2008, 2010), and excluded highly correlated variables (r  0.7) (see Appendix 2.1, available online at www .cambridge.org/gibbonconservation) and low contributed variables to reduce model sensitivity to overfitting from using too many environmental variables (KramerSchadt et al., 2013). Finally, elevation layer (digital elevation model, DEM) and six bioclimatic variables were chosen for the model – three temperature and three precipitation – comprising annual temperature (Bio01), temperature seasonality (Bio04), mean temperature of the wettest quarter (Bio08), annual precipitation (Bio12), precipitation of driest month (Bio14) and precipitation of driest quarter (Bio17).

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Status of Nomascus annamensis in Vietnam

2.3

Results

2.3.1

Status of Nomascus annamensis on the Eastern Slopes of the Central Annamites

29

In total, 84 gibbon calls were recorded and 46 groups were identified. The number of groups heard during the survey period at each listening post ranged from zero to three, with an average of 0.85 groups per post. Gibbon calls were heard from 33 of the 54 posts (61.1 per cent). We did not hear any gibbon calls in the Vinh Son Commune. Calling probability, estimated density and estimated groups for each area is presented in Table 2.1. The average estimated densities of 30 posts in An Toan NR and 14 posts in West Ba To PNR were 0.15 and 0.41, respectively. With no gibbons detected in Vinh Son Commune, the total estimated population on the eastern slopes of the Central Annamites was 114 groups.

2.3.2

Conservation Status of Nomascus annamensis in Vietnam The distribution of N. annamensis was confirmed as ranging from 14
000 to 16
500 N in Vietnam. The northernmost distribution of the species was reported in Bac Huong Hoa NR, north of the Thach Han River, a previously proposed barrier of the species, based on sonogram analysis (Nguyen et al., 2017; Hoang et al., 2018). The southernmost record was in Kon Ka Kinh National Park (NP), north of the Ba River (Ha et al., 2011; Hoang et al., 2018). In The Conservation Status of Gibbons in Vietnam, about 195 groups of N. annamensis were confirmed in the country but it was also recognised that the actual population must be higher because there are many areas of suitable habitat that have yet to be surveyed (Rawson et al., 2011). In a recent review on the distribution of N. annamensis, 305–306 groups were confirmed, mostly confined to a few protected areas (Hoang et al., 2018), and only a handful of key areas support stronghold populations of the species in Vietnam (Rawson et al., 2011; Hoang et al.,

Table 2.1 Estimated density and population size of gibbons in the study areas.

Study area

Average no. of groups heard in one day (N1)

Cumulative no. of groups heard Calling in m-days probability (Nm) (p1)

Estimated density (group/ Habitat Estimated km2) (km2) groups

An Toan NR (21 posts for 3 days) An Toan NR (9 posts for 2 days) West Ba To PNR (7 posts for 3 days) West Ba To PNR (7 posts for 2 days) Vinh Son (10 posts for 3 days)

9.3 5.5 6.0 5 0

16 9 12 9 0

0.12 0.24 0.32 0.51 0

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0.57 0.36 0.38 0.20 0

303 162 –

47 (95% CI 36–60) 67 (95% CI 34–16) –

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Duc Minh Hoang et al.

2018). One of the most important populations was found in the contiguous forest of Dak Rong NR of Quang Tri Province (Nguyen, 2007) and Phong Dien NR of Thua Thien-Hue Province (Rawson et al., 2011). Another stronghold area is the contiguous forest in Kon Tum, Gia Lai, Quang Ngai and Binh Dinh provinces. Acoustic surveys in this area have confirmed 13 groups and 20 groups estimated in Kon Cha Rang NR (Vu and Dong, 2015), nine groups confirmed and 42 groups estimated in Kon Ka Kinh NP (Ha et al., 2011), four groups in the green corridor between Kon Ka Kinh and Kon Cha Rang NR (Nguyen et al., 2017), six groups recorded by automated recorders in Ngoc Linh NR (Vu et al., 2017), and 46 groups from this study. Opportunistic records of 19 groups were made in three separate areas in Kon P’long District during line-transect surveys for grey-shanked doucs (Pygathrix cinerea), from September 2015 to January 2016 (Trinh et al., 2016). Gibbon density in this area was also quite high compared with other areas in Vietnam: 0.53 groups/ km2 in Kon Cha Rang NR (Vu and Dong, 2015) and 0.39 groups/km2 in West Ba To PNR (this study). Furthermore, the forest areas in Bach Ma NP and surrounding areas such as Hue Sao La NR, A Luoi watershed protection and Nam Dong watershed protection likely support a large population of N. annamensis. We lack an estimate of the population in this area, but it should be noted that surveys covering a small portion of this region have confirmed 52 groups (Van et al., 2007; Nguyen et al., 2010). The species was also recorded to be widespread in the remnant forests of Quang Nam Province and Da Nang City, with at least 17–18 groups recorded in Song Thanh NR, 13 groups in Ngoc Linh NR (Hoang et al., 2005) and 14–16 groups in Ba Na – Nui Chua NR (Bui et al., 2019). In western Kon Tum Province, an acoustic survey of a small portion of Chu Mom Ray NP detected a population of 14 groups (Vu et al., 2007; Lippold et al., 2011). Based on these reports, we identified 217 records of this species that are associated with coordinates. After refining the dataset by applying a 1-km spatial thinning, the final dataset comprised 105 occurrences for species distribution modelling (see Appendix 2.2, available online at www.cambridge.org/gibbonconservation). The modelling result based on six bioclimatic layers plus elevation is illustrated in Figure 2.2. The model performs quite well in closely aligning with the known geographical range of N. annamensis in Vietnam. The potential range of this species is from Bac Huong Hoa NR, north of the Thach Han River (approximately 16
80 N) rather than just south of Thach Han (approximately 16
50 N) to Kon Ka Kinh NP in Gia Lai Province. With the 10-percentile training presence threshold applied (0.389) and suitable habitat of 50 per cent, the total suitable area predicted for the gibbon is about 12,843 km2 and 9,460 km2, respectively. The average test AUC for the replicate runs of 0.972 and the standard deviation of 0.018 indicated solid levels of performance. The most important variable contributing to the model was temperature seasonality (47.7 per cent), followed by elevation (24.1 per cent), precipitation of driest month (11.7 per cent), annual precipitation (7.6 per cent) and precipitation of driest quarter (7 per cent). The jackknife analysis suggests that the environmental variable that had the highest gain when added to the model was temperature seasonality. Likewise, the

https://doi.org/10.1017/9781108785402.004 Published online by Cambridge University Press

https://doi.org/10.1017/9781108785402.004 Published online by Cambridge University Press

Figure 2.2 Habitat suitability map of Nomascus annamensis at 10 percentile presence training threshold (a) and 50 per cent probability (b).

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environmental variable that decreased the gain the most when omitted is also temperature seasonality, which therefore has the highest predictive value of all variables. The species occurs mainly in areas where temperature seasonality ranges between 2.0 and 3.2
C, with a high annual rainfall (2,000–3,300 mm), and some precipitation in the driest month (20–50 mm) (see Appendix 2.3, available online at www .cambridge.org/gibbonconservation). Elevation is also an important factor influencing the distribution of N. annamensis in our models since most occurrence records in Vietnam were at higher elevations. The area with suitable habitat equal to or more than 50 per cent shows a high degree of fragmentation and is limited in size. Only six forest blocks are larger than 100 km2 and comprise a total area of 8,433 km2. Eighteen forest blocks are between 10 and 99 km2 in size and 225 forest blocks are less than 10 km2 in size, comprising a total forest area of about 1,028 km2. Most suitable habitat areas are confined to higher elevations, especially on mountaintops.

2.4

Discussion

2.4.1

Density and Population Status of Nomascus annamensis The differences in group density between An Toan NR and West Ba To PNR is likely related to the forest areas being easily accessed by local people in the former. The average distance from our listening posts to the closest villages in Ba To PNR is further than that in An Toan NR: 8.17  2.21 km (range 4.42–11.06 km, n ¼ 14) and 4.64  1.73 km (range 1.88–8.23 km, n ¼ 30), respectively. Furthermore, the forest of Ba To PNR is only accessed by trails, while there is a road system in An Toan NR left from timber exploitation before it was established as a protected area in 2009. The average distance from listening posts to the closest villages in Vinh Son Commune is about 6.56  3.58 km (range 2.41–13.09 km, n ¼ 10) but this is not a protected area and local people can access the forest by vehicles through a trail and road system. The high disturbance is likely the cause for the lack of gibbon calls (and lack of gibbons) in Vinh Son Commune. Gibbon group densities in this study are comparable with those from other studies on N. annamensis and other congeners in Vietnam. Since our surveyed area is in hilly terrains where not all groups within 1 km can be heard (Brockelman et al., 2009), the number of groups detected and group densities are considered as a minimum number. A high density of 0.53 groups/km2 based on 17 listening posts was reported in Kon Cha Rang NR (Vu and Dong, 2015), a contiguous forest (one of the six large areas noted above), while a density of 0.12 groups/km2 was estimated for the species in Kon Ka Kinh NR (Ha et al., 2011), a neighbouring protected area. Higher group densities were recorded in about 78 km2 of forest between Dak Rong and Phong Dien NR (0.59 groups/km2, Nguyen et al., 2010) and Bach Ma NP (1.3 groups/km2, Geissmann, 2007) but a survey in the latter only focused on a small area of 6 km2. A similar group density of 0.32 groups/km2 was found in a large-scale survey in Veun Sai-Siam Pang

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Conservation Area, Ratanakiri Province, Cambodia, with at least 77 confirmed groups (Kidney et al., 2016). In Virachey NP of Ratanakiri and Stung Treng provinces (Cambodia), a remarkably high density (2.21 groups/km²) was reported based on an acoustic survey using 15 listening posts (Traeholt et al., 2005). The average group density of most Nomascus species is less than 1 group/km2 and is dependent on the level of human impacts and/or size of forest blocks (Harding, 2012). An estimation for northern white-cheeked gibbon (N. leucogenys) and southern white-cheeked gibbon (N. siki) in a 210-km2 forest of Nam Kading National Protected Area in central Laos gave an average density of 0.21 groups/km2 (Hallam et al., 2016). In Nam Et-Phou Louey (Laos) the density of N. leucogenys in the mixed deciduous forest was higher than that in evergreen forest (0.74 and 0.09 groups/km2, respectively), probably due to the consequence of long-term hunting in evergreen forest areas (Syxaiyakhamthor et al., 2019). Gibbon density in Pu Mat NP, Vietnam differs by elevation: in forested areas under 700 m and above 700 m altitude, densities were 0.051 and 0.271 groups/ km2, respectively (Luu and Rawson, 2011). Harding (2012) suspected that the relatively low level of forest fragmentation and the wide distribution may result in the relatively high density of Laotian black crested gibbon (N. concolor lu) of 2.2 groups/ km2 in the Nam Kan Valley of Laos, as reported by Geissmann (2007). In good habitats, gibbons can live in very high density as reported for the eastern hoolock gibbon (Hoolock leuconedys, 2.4 groups/km2) in Myanmar (Brockelman et al., 2009). Geissmann et al. (2013) reported that gibbon density varies across Myanmar and is lowest in areas affected by human hunting and forest fragmentation. The known population size of N. annamensis in Vietnam is at least 317 groups. The distribution of N. annamensis stretches north for almost 4
of latitude (about 280 km north to south) but the total area is quite small compared to its congeneric species. The total natural forest area within its geographical range in Vietnam in 2018 was 22,790 km2 (FPD, 2019), but our model suggests that the suitable habitat of the species was about 9,460 km2 and quite fragmented. Forest loss also poses a big threat to the gibbons. Natural forest loss between 2000 and 2018 in the Central Highlands, the main range of the species, comprised about 3,130 km2, being mainly converted to industrial tree plantations (Ho et al., 2020). Illegal hunting of gibbons for traditional uses and the pet trade are some of the main threats that have resulted in the overall decline of the gibbon population in Vietnam (Van et al., 2020). Possession of live gibbons is the most common gibbon crime reported in Vietnam, and one live gibbon recorded in captivity equates to about 20 individuals killed during hunting events (Beyle et al., 2014). The distribution and population status of the six Nomascus species found in Vietnam have recently been reviewed by Rawson et al. (2011). The known population size of N. annamensis in Vietnam is comparable to that of N. gabriellae and N. siki, and is much larger than the population size of N. leucogenys, black crested gibbon (N. concolor) and Cao vit gibbon (N. nasutus). Nomascus gabriellae (Rawson et al., 2011) represents the largest population of Vietnam’s gibbons, with at least 472 confirmed groups and an estimated 873 groups (unpublished data). At present, 252 groups of N. siki have been confirmed in several protected areas and state forest enterprises in

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the north Central Annamites (Dang et al., 2017; Nguyen et al., 2020). The population of N. leucogenys is small, with a total of 84 confirmed groups dispersed across fragmented forest areas (Rawson et al., 2011). The population of N. nasutus has increased slightly, from about 102–110 individuals in 2011 (Rawson et al., 2011; Ma et al., 2019) to 107–136 in 2016 for both China and Vietnam (Ma et al., 2019). The population status of N. concolor in Vietnam is quite grim, with only 22–25 confirmed groups distributed across fragmented forest areas (Rawson et al., 2011). Given the fact that many areas have not been surveyed or re-surveyed in the last 10 years, it is important to conduct surveys or reassessment of the conservation status not only for N. annamensis but also for the other gibbons of Vietnam.

2.4.2

Habitat Preference of Nomascus annamensis Nomascus gibbons are found in a wide range of habitats but prefer living in evergreen forest at a range of elevations (Rawson et al., 2011; Reichard et al., 2016). It appears that temperature seasonality explains the range boundary between N. annamensis and N. gabriellae. Nomascus annamensis lives in areas where the range in temperature seasonality is wide (2.0–3.2
C), meaning greater variability of temperature, while N. gabriellae occurs in areas with a narrower seasonal temperature range (1.0–1.5
C) (unpublished data). This explains the large gap between the ranges of the two species in the central Gia Lai Province. To the north, N. annamensis and N. siki share the forest area in Bac Huong Hoa NR (Nguyen et al., 2017). Nomascus siki favours areas where the seasonal temperature ranges between 2.0 and 4.0
C (unpublished data), partly overlapping with areas where N. annamensis occurs. Since the Thach Han River is not the natural barrier between the two (Hoang et al., 2018), the reason why N. annamensis is not distributed farther northward is still unknown, but possibly they are not able to compete successfully with N. siki. The crested gibbons (Nomascus spp.) are reported to live at a wide altitude range of about 50 to 2,800 m above sea level (Dao, 1983; Li et al., 2011; Rawson et al., 2011) and even at relatively high altitudes in ecologically challenging and highly seasonal mountain habitats as reported for N. concolor (Li et al., 2011; Ning et al., 2019). Our ENM showed that most suitable habitat areas are confined to higher elevations and the elevation influences the distribution of N. annamensis. This is likely related, in part, to the occurrence records used in our model, which date to after 2000. Over 75 per cent of the central region of Vietnam is mountainous and the remaining 25 per cent mainly comprises lowlands and plains that have been occupied by humans for thousands of years. The high degree of deforestation in the low altitudinal zones that has occurred over the past few decades, along with the high hunting pressure in the remnant forests of these areas, have eradicated gibbon populations. This is similar to what Kirkpatrick (1998) has reported for colobines (Colobinae) in much of Asia. Also, as noted above, N. annamensis was found at about 100 m above sea level in Veun Sai, Siam Pang Conservation Area, Cambodia (Kidney et al., 2016) so they are capable living in lowaltitude forests.

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2.5

35

Conclusions We detected at least 46 groups of N. annamensis in the study areas and estimated the population size at 114 groups within suitable forest areas on the eastern slopes of the Annamites. This area plays an important role in the conservation of N. annamensis, but given the lack of long-term monitoring here we are unable to directly address population changes for this taxon. In addition, the densities of gibbons in our study areas are comparable to those in other areas of Vietnam and the Indochina region more generally, where declines in gibbon populations have been documented over the past few decades. Furthermore, many of the areas where N. annamensis still occur in Vietnam are small and/or disturbed forests where local extirpation is likely without concerted conservation efforts. The bioclimatic conditions that shape the distribution of N. annamensis are temperature seasonality, precipitation of driest month, annual precipitation and precipitation of driest quarter. Elevation also contributes to the distribution of the species and fewer records in the lower altitudinal zone likely relate to human impacts in lowland areas. The highly suitable habitat of N. annamensis in Vietnam comprises about 9,460 km2 and is quite fragmented. Only six areas may support stronghold populations and many subpopulations and are therefore under high threat of habitat fragmentation and thus directly exposed to human impacts.

Acknowledgements We express our deep gratitude to the SIE researchers, who worked in the forest to obtain the species occurrence data that we have used in our research. We also acknowledge Dr Ha Thang Long, Dr Nguyen Van Thien, Dr Nguyen Manh Ha, Mr Bui Van Tuan, Mr Vu Ngoc Thanh and Mr Nguyen Ai Tam for providing us with their original species occurrence data. The field survey was financially supported by US Fish and Wildlife Service Grant No. F14AP00878 and the Space Science and Technology Program Project No. VT-UD.09/18-20.

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Nguyen, H.M. (2007). Survey for southern white-cheeked gibbons (Nomascus leucogenys siki) in Dakrong Nature Reserve, Quang Tri Province, Vietnam. Vietnamese Journal of Primatology, 1: 61–66. Nguyen, K.V. and Ho, T.T. (2019). Forest and forestry ecocultural system in Central Highlands, Vietnam. VNU Journal of Science: Policy and Management Studies, 35(2): 39–52. Nguyen, K.V., Nguyen, T.H., Phan, K.L. and Nguyen, T.H. (2000). Bioclimatic Diagrams of Vietnam. Vietnam National University Publishing House, Hanoi, Vietnam. Nguyen, T.V., Nguyen, A.H.Q., Van, T.N., Le, K.V. and Roos, C. (2017). Distribution of the northern yellow-cheeked gibbon (Nomascus annamensis) in Central Vietnam. Vietnamese Journal of Primatology, 2: 83–88. Ning, W.H., Guan, Z.H., Huang, B, Fan, P.F. and Jiang, X.L. (2019). Influence of food availability and climate on behavior patterns of western black crested gibbons (Nomascus concolor) at Mt. Wuliang, Yunnan, China. American Journal of Primatology, 81(12): e23068. Phillips, S.J. and Dudík, M. (2008). Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography, 31(2): 161–175. Phillips, S.J., Anderson, R.P. and Schapire, R.E. (2006). Maximum entropy modeling of species geographic distributions. Ecological Modelling, 190(3): 231–259. Rawson, B.M., Clements, T. and Hor, N.M. (2009). Status and conservation of yellow-cheeked crested gibbons (Nomascus gabriellae) in the Seima Biodiversity Conservation Area, Mondulkiri Province, Cambodia. In Lappan, S. and Whittaker, D.F. (eds.), The Gibbons. Springer, New York: 387–408. Rawson, B.M., Insua-Cao, P., Nguyen, H.M., et al. (2011). The Conservation Status of Gibbons in Vietnam. Fauna and Flora International/Conservation International, Hanoi, Vietnam. Reichard, U.H., Hirai, H., Barelli, C. and Nowak, M.G. (2016). The evolution of gibbons and siamang. In Reichard, U.H., Hirai, H. and Barelli, C. (eds.), Evolution of Gibbons and Siamang: Phylogeny, Morphology, and Cognition. Springer, New York: 3–41. Syxaiyakhamthor, K., Ngoprasert, D., Toasensio, N. and Avini, T. (2019). Identifying priority areas for the conservation of the critically endangered northern white-cheeked gibbon Nomascus leucogenys in northern Laos. Oryx, 54(6): 767–775. Traeholt, C., Bunthoen, R., Rawson, B., et al. (2005). Status review of pileated gibbon, Hylobates pileatus, and yellow-cheeked crested gibbon, Nomascus gabriellae in Cambodia. Fauna and Flora International – Indochina Programme, Phnom Penh, Cambodia. Trinh, D.H., Nguyen, V.T., Rawson, B., et al. (2016) Report on grey-shanked douc langur (Pygathrix cinerea) survey in Kon Plong District, Kon Tum Province, Central Highlands, Vietnam. Fauna and Flora International Vietnam Programme, Hanoi, Vietnam. Van, N.T., Nguyen, H.M., Dickinson, C., et al. (2007). Primate conservation in Thua Thien Hue Province, Vietnam: with special reference to white-cheeked crested gibbons (Nomascus leucogenys siki) and red-shanked douc (Pygathrix nemaeus nemaeus). WWF Greater Mekong Program and Forest Protection Department, Thua Thien Hue Province, Vietnam. Van, N.T., Mootnick, A.R., Vu, T.N., Nadler, T. and Roos, C. (2010). A new species of crested gibbon, from the central Annamite mountain range. Vietnamese Journal of Primatology, 4: 1–12. Van, N.T., Roos, C., Rawson, B.M., et al. (2020). Nomascus annamensis. The IUCN Red List of Threatened Species 2020. Available at www.iucnredlist.org/species/120659170/120659179 (accessed 30 November 2022). Veloz, S.D. (2009). Spatially autocorrelated sampling falsely inflates measures of accuracy for presence-only niche models. Journal of Biogeography, 36(12): 2290–2299.

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Vinh Thanh Statistical Department . (2019). Vinh Thanh Statistical Yearbook 2018. Binh Dinh Statistics Office. Vu, T.N., Le K.V., Le, Q.K., et al. (2007). Survey on primates of Chu Mom Ray National Park, central Vietnam, with special reference to douc langurs (Pygathrix spp.). Technical Report, Hanoi University of Science, Hanoi, Vietnam. Vu, T.T. and Dong, H.T. (2015). Estimation of northern yellow-cheeked gibbon (Nomascus annamensis) population size in Kon Cha Rang Nature Reserve: a new method using a weighted correction factor. Vietnamese Journal of Primatology, 2: 41–48. Vu, T.T. and Rawson, B. (2011). Package for calculating gibbon population density from auditory surveys. Conservation International and Fauna and Flora International, Hanoi, Vietnam. Vu, T.T., Tran, D.V. and Nguyen, K.K. (2017). A study on the status of northern yellowcheeked gibbon (Nomascus annamensis) in Ngoc Linh Nature Reserve, Quang Nam Province using bioacoustics methods and automated recorders. Science and Technology Journal of Agriculture and Rural Development, 17: 142–148. Warren, D.L., Glor, R.E. and Turelli, M. (2008). Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution, 62(11): 2868–2883. Warren, D.L., Glor, R.E. and Turelli, M. (2010). ENM Tools: a toolbox for comparative studies of environmental niche models. Ecography, 33(3): 607–611.

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Strategies for Recovery of the Hainan Gibbon (Nomascus hainanus) Twenty Years of Multidisciplinary Conservation Effort Bosco Pui Lok Chan and Yik Fui Philip Lo

3.1

Introduction The Hainan gibbon (Nomascus hainanus) is the only insular species of the crested gibbons (genus Nomascus) and is endemic to Hainan Island of China (Mittermeier et al., 2013). Hainan lies within the tropics at 18
90 to 20
100 N, 108
370 to 111
30 E, with a land area of about 33,900 km2. It has a mountainous interior, with 81 peaks rising to over 1,000 m. According to the latest official statistics, Hainan currently has about 6,600 km2 of natural forest, including around 1,400 km2 of old-growth forest; most natural forests are located in the central mountains. Various biogeographic, palaeomagnetic and volcanism studies indicate that Hainan Island is more closely associated with northern Vietnam and southwest Guangxi Province in China, with a strongly tropical Asian biotic affinity (Zhu, 2016). The Hainan gibbon is the rarest primate species on earth and has been on the verge of extinction since the 1970s. Based on results of a hunter interview survey conducted in the early 1980s, scientists extrapolated there were about 2,000 Hainan gibbons in the early 1950s, but with rampant hunting and forest clearance in the ensuing years, the species experienced substantial population and range declines, with only seven to eight groups remaining in five forest tracts in 1978, and only three relict populations of 30–40 gibbons in 1983. The situation further deteriorated with increased forest accessibility and unchecked hunting, and by 1990 gibbons only persisted on the forested slopes of Mt. Futouling (summit 1,438 m above sea level, approximately 19
60 15.200 N, 109
130 11.9800 E) (Liu et al., 1984). In 1980, Mt. Futouling and the surrounding forest measuring roughly 13 km2 was gazetted as Bawangling Nature Reserve (NR) in a last-ditch effort to protect the species (Liu et al., 1987). The reserve has undergone two subsequent expansions, the first in 1988 when it was enlarged to 66 km2 and upgraded to a national-level NR, and the second in 2003 where it was further expanded to 300 km2 (Chan et al., 2005). Until the end of 2019, all gibbons were distributed in the foothills of Mt. Futouling, which is at the eastern boundary of the reserve bordered by village settlements. A new group was confirmed in early 2020 at Mt. Dongbengling, a mountain about 8 km north of the known gibbon range (Chan et al., 2020a) (Figure 3.1). For simplicity ‘Bawangling’ refers to Bawangling National NR for the rest of this chapter, unless otherwise stated.

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Figure 3.1 Map of the Mt. Futouling area in Hainan Bawangling National Nature Reserve, showing approximate locations of Hainan gibbons (Nomascus hainanus) in June 2020, and major peaks and places mentioned in text. Gibbon groups are marked A, B, C, D and E as they are named; X shows location where two adult females have been regularly detected since August 2019.

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Since the establishment of Bawangling, various research institutes and organisations have offered technical and financial assistance to prevent the first primate extinction in modern history, including the South China Institute of Endangered Animals (Guangzhou), Kadoorie Farm and Botanic Garden (KFBG), Fauna and Flora International – China, East China Normal University, Chinese Academy of Sciences, Guizhou Normal University, South China Normal University, Zoological Society of London, Zoological Society of Paris, Gibbon Conservation Alliance, The Conservancy Association and Rotary Club of Hong Kong. The collective perseverance appears to be paying off, with the latest surveys confirming a population of at least 34 gibbons, including five family groups and a pair of adult females regularly detected about 2 km south of the known range since August 2019. This is a conservation milestone as it represents the highest population and group numbers recorded in half a century. Most of the conservation and research projects over the years have been short term, but we have been running a conservation project for KFBG since 2003. This chapter details the multidisciplinary conservation actions implemented by KFBG over the last 17 years, and attempts to discuss what worked, what did not and what will be the priority steps for the future.

3.2

The Turning Point for Hainan Gibbon: Population Census and Conservation Workshop in 2003 In March 2003, after years of trust-building and discussions, the Forestry Department of Hainan Province invited KFBG to make concerted efforts in conserving the species. To understand the status of the Hainan gibbon and the key conservation challenges it faced, we started by organising a systematic population survey in October 2003, leading 16 teams to survey all potential gibbon habitats in Bawangling over a 16day period. The results were stark: only two family groups (of five and six individuals, respectively) and two solitary males, totalling 13 individuals, were confirmed. Gunshots were regularly heard, snaring and forest product extraction were prevalent, illegal forest camps were scattered all over the forest, and forest encroachment along the boundary was intense. The reserve management was severely underfunded and understaffed, with nine staff and an annual budget of less than US$40,000 to protect 40 km2 of steep gibbon forest surrounded by a human population frequently engaging in extraction activities and land encroachment. KFBG convened the first Hainan gibbon conservation workshop succeeding the survey, during which we identified key conservation challenges, formulated and prioritised actions, and drafted the first conservation action plan for the species. With the critically low gibbon numbers, issues were brought into the open during the 3-day workshop; dialogue was frank and sometimes heated, and it was clear that proactive conservation measures had to be established quickly in a bid to prevent extinction of the Hainan gibbon. The survey and workshop were co-organised with the provincial and local conservation authorities, and engaged local, national and international stakeholders, with the results and outcomes being embraced by the authorities (Chan et al., 2005).

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3.3

43

Population Changes in Hainan Gibbon Despite its small population size, the population dynamics of Hainan gibbon in Bawangling have been confusing. The founding population size in 1978 was uncertain, and the various research groups have found highly variable figures over the years (Table 3.1). In summary, official statistics reported around 20 gibbons in four groups up to 2002, but our systematic simultaneous survey by a 50-member team confirmed only 13 gibbons in two groups in 2003 (Chan et al., 2005; Figure 3.2). Table 3.1 Population dynamics of the Hainan gibbon at Bawangling between 1978 and mid-2002, prior to intervention of the KFBG project.

Year

Family group number

Individual number

1978

2–3

7–10

1983 1989 1989–1990 1993 1998 2001 2001–2002

4 4 N/A 4 4 4 4

16 21 10 15 17 23 12–19

Sources Xu and Liu (1984); Liu et al. (1987); Liu and Tan (1990); Zhang (1992) Xu and Liu (1984) Liu et al. (1989) Zhang (1992) Zhang and Sheeran (1994) Kadoorie Farm and Botanic Garden (2001) SFA and Bawangling Management Office (2001) Wu et al. (2004)

Figure 3.2 Population dynamics of Hainan gibbon at Bawangling between 2003 and August 2020. Dips in the graph were due to difficulties in detecting and identifying dispersed solitaries.

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Table 3.2 Group composition of Hainan gibbon at Bawangling, August 2020. Social group

Paired male

Paired female

Offspring

Other individuals

Total

A B C D E X

1 1 1 1 1 0

2 2 2 2 1 0

3 5 6 2 1 0

0 0 1 male 0 0 2 females

6 8 10 5 3 2

While it is possible that two of the four groups reported from 1984 to 2002 had disbanded and vanished prior to the 2003 survey, it seems more likely that the discrepancies in gibbon demography stem from the lack of wide-scale simultaneous surveying and from unexpressed assumptions about ranging pre-2003; these were confirmed in personal communications with the main researcher before 2000, Professor Liu Zhenhe and his leading assistant Chen Qing of Bawangling. Nevertheless, the inconsistency in published figures and home range means it is difficult to draw conclusions regarding past population and group sizes, as well as distribution, before 2003. Determined multidisciplinary conservation intervention started in 2003 (Fellowes et al., 2008), and gibbon population and ranging data were collected by a fixed team based on regular monitoring and annual population surveys using the same method in the same month as in 2003. Our longitudinal data indicates an increasing population trend and range expansion, with a third group formed in 2011 by the forest edge near villages, a fourth group in 2015 and a fifth group at the turn of 2019–2020, with a roughly 4-year interval for new group formation (Figure 3.2). The latest monitoring data confirmed five gibbon groups and two solitary females, comprising at least 34 gibbons in 2020 (Chan et al., 2020a; KFBG, unpublished data; Table 3.2; Figure 3.2).

3.4

Conservation Strategy: A Multidisciplinary Approach With the precarious status of the Hainan gibbon, many conservation recommendations have been made by concerned parties (Chan et al., 2005; Turvey et al., 2015). A number of key issues limiting population growth were identified in the 2003 workshop, including loss of optimal lowland habitat and forest connectivity, ongoing hunting and other disturbances by the local human population, and limited capacity for Bawangling to tackle these issues. Workshop participants also agreed there is a need to provide alternative, sustainable livelihoods for the forest-dependent local residents in the long term. Urgent multidisciplinary conservation measures were identified, including intensifying patrol and gibbon monitoring efforts, building up the management capacity of Bawangling, restoring degraded lowland habitats in strategic locations, surveying gibbons outside Bawangling, research, awareness-raising and community

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engagement, and these have guided the KFBG Hainan gibbon conservation project over the past 17 years. KFBG believe it is essential to have a good understanding of the local political, socioeconomic and ecological situations and to build trust with local partners for a conservation project to be effective. So, before implementing actions prematurely, we spent several trips familiarising ourselves with the project site and the local people, exploring the wider Bawangling forest, asking foresters and villagers questions on forest change, gibbons and other wildlife, and exploring the situation with regard to hunting, logging and other forest uses. We also had multiple meetings and social gatherings with the reserve director, managers and wardens to understand their challenges and aspirations, and to clarify the expectations, roles and responsibilities in our partnership. Our work included the following major elements.

3.4.1

Reserve Management: Gibbon Monitoring, Patrol Effectiveness and Capacity-Building KFBG began funding regular gibbon monitoring in 2005 and this investment continued until 2021. The priority at the outset was to stop poaching in order to safeguard the last two gibbon groups, and concurrently to collect ecological information. A team of eight wardens were selected to form a gibbon monitoring team, who were trained in basic gibbon knowledge, conservation concepts and field skills. Members were divided into two teams of four to carry out successive rosters of 5-day monitoring. The continuous presence of wardens camping in the forest has been an effective deterrent to poachers, as temporal analysis of the authors’ field notes showed increased encounter rates with game species such as silver pheasant (Lophura nycthemera), black giant squirrel (Ratufa bicolor) and wild boar (Sus scrofa). As the management budget was limited, we provided a field allowance and all essential field equipment for gibbon monitoring and built four permanent forest base camps at key locations (Figure 3.3). To boost the reserve’s morale, in 2005 we designed a reserve logo endorsed by the reserve management. Wardens were encouraged to join our surveys on other taxon groups, as we believe a genuine interest in nature would enhance their performance in patrolling and gibbon monitoring. Over the years, KFBG also donated two four-wheel drive vehicles to Bawangling to enhance patrolling efficiency, and funded the reserve management and forestry police to conduct special enforcement operations in poaching blackspots. To build up their capacity, KFBG has been sponsoring reserve managers and key wardens to join our field surveys and study tours both inside and outside Hainan, as well as to the Cao Vit Gibbon Conservation Area in northeast Vietnam. Between 2009 and 2010, Group A shifted its home range to the eastern slopes of Mt. Futouling, and we expanded our monitoring coverage by forming a community monitoring team. The local forestry police helped to select candidates from indigenous villagers who were enthusiastic and responsible. We additionally suggested inviting members of influential clans to join the monitoring team, as powerful clans are respected in rural communities. We currently employ four villagers to conduct regular

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Bosco Pui Lok Chan and Yik Fui Philip Lo

Figure 3.3 (a) First author (far left) with part of the gibbon monitoring team in new uniforms and equipment provided by KFBG in 2005. (b) The authors visiting a base camp built by KFBG in the Group B home range.

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monitoring on the three gibbon groups occurring east of Mt. Futouling; most of them are former hunters/loggers, and including them in conservation directly reduces their impacts and garners support and understanding from their respective villages. The intensity of poaching in this forest has much reduced since 2010, and continues to decline with a reported recovery of game species such as the silver pheasant.

3.4.2

Habitat Management: Forest Restoration and Canopy Connectivity Prior to 2010, the two gibbon groups were restricted to the western slopes of Mt. Futouling, where the forest on the lower slopes below 900 m has long been cleared (Figure 3.4). According to extensive botanical studies (Jiang et al., 2002), 900 m elevation is the division between lowland rainforest and montane rainforest in Hainan; favourite gibbon food tree species such as figs (Ficus spp.), bishop wood (Bischofia javanica), wild rambutan (Nephelium topengii) and wild lychee (Litchi chinensis) are predominantly lowland rainforest species, while the montane rainforest supporting gibbons is floristically less diverse. The Bawangling Forestry Bureau planted pines (Pinus spp.) in these fire-maintained grasslands in 1984, and these plantations are never used by the gibbons. However, belts of natural forest extend down to 650 m in some ravines, and monitoring data indicate that gibbons regularly visit these ravine forests while foraging. One of our priority actions was to restore these pine plantations to a more naturalistic state and to do this we sought advice from tropical forest and restoration ecologists whom we invited for a field trip in December 2003. In 2004, we identified seven critical restoration corridors based on an acquired satellite image, and established two native tree nurseries to produce seedlings. Wardens were trained to identify a list of fast-growing gibbon food trees, and we also employed four local villagers as nursery workers to manage the nurseries. By the rainy season of 2005, the first 14,000 seedlings of 20 locally collected food plant species

Figure 3.4 Western side of Mt. Futouling prior to the 1980s. The Bawangling Forestry Bureau conducted large-scale planting of pines (Pinus spp.) in 1984, and these grassy slopes are currently covered in pine plantation unusable by the gibbons.

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had been planted in the pine plantation, and a total of over 84,000 seedlings of 53 native gibbon food plant species had been planted in 150 ha of pine plantations adjoining gibbon forest by 2008. Today, some trees of fast-growing species like Endospermum chinense are over 10 m tall and hardy species like Syzygium acuminatissimum are starting to bear fruit. Figs are a favourite group of food trees for the Hainan gibbon, so we also trialled the use of stem-cutting to propagate fig saplings; while these stem cuttings performed well in the nursery, the survival rate of planted cuttings in pine plantations was very low. In July 2014, super typhoon Rammasun, the strongest typhoon in modern Chinese history, hit Hainan. One of the main ‘arboreal highways’ (sensu Chivers, 1974) of Group C was damaged by a major landslide averaging 15 m wide, and we observed gibbons crossing the forest gap with difficulty, especially the adult females and juveniles. To avoid accidental injuries or deaths we constructed a canopy rope bridge network across the gully in 2015 with the assistance of professional tree climbers. The gibbon group was habituated to the canopy bridge after 6 months and now regularly use it. Rope bridges have been used by three of the four extant gibbon genera (Hoolock, Hylobates and Nomascus), are inexpensive, materials are readily available and easy to transport in remote hilly regions, are technically simple to install and may be the most cost-effective artificial canopy bridge type for Hylobatidae (Chan et al., 2020b). We considered the artificial canopy bridge as a temporary measure in the conservation management of the Hainan gibbon, and launched a reforestation project at various landslides in gibbon home ranges as a long-term solution. Large saplings (average c. 2 m tall) of the fast-growing native bishop wood were planted concurrently underneath the canopy bridge and have grown into young trees; together with regenerated pioneer trees, they have provided an alternative passage route for the gibbon group since late 2018. With corporate financial support, an additional 12,000 seedlings of native gibbon food tree species were planted in 17 ha of typhoon-damaged forest and forest edge during 2015–2016.

3.4.3

Scientific Research To enhance our understanding of the Hainan gibbon, KFBG sponsored five postgraduate studies in the first 5 years of our project on topics covering basic ecology and potential distribution of the species, as well as a policy review related to Hainan gibbon conservation. Since considerable effort and budget was spent on restoration of lowland forest, we also sponsored two postgraduate students to assess our forest restoration effort (Table 3.3). In addition, we have facilitated and provided guidance for two postgraduate students from British universities since 2009. These KFBG-funded researchers usually formed close working relationships with us and shared our passion for gibbon conservation, and frequently engaged in discussions giving their insights into how best to improve our conservation actions; for example, poaching hotspots were identified and enhanced patrol efforts were dispatched to these areas, and information about solitary gibbon sightings were added to our database. They also acted as supervisors in helping KFBG to monitor and train the gibbon monitoring teams.

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Table 3.3 Scientific research on Hainan gibbon funded by KFBG. Year

Name

Degree Institute

Research topic

2004

Zhou Jiang

PhD

Guizhou Normal University

Ranging, habitat selection, diet and social organisation in Hainan gibbon in Bawangling Nature Reserve, Hainan

2004

Zhang Ming Xia

PhD

Kunming Institute of Zoology, Chinese Academy of Sciences

Analysis of habitat selection and potential distribution of Hainan gibbon

2004

Lin Jia Yi

PhD

South China Agricultural University

Phenology and ecology of the main feeding plants of Hainan gibbon

2006

Xie Yi

PhD

Beijing Forestry University

Policy review of endangered species conservation: case study of Hainan gibbon

2007

Li Zhi Gang

MPhil

Guizhou Normal University

The study of social structure in the Hainan black crested gibbon

2009

Gan Wei Ping

MPhil

South China Agricultural University

A preliminary study on the effects of afforestation in habitat restoration for Hainan gibbons in Bawangling Nature Reserve, Hainan

2019

Yin Chong Min

MPhil

South China Agricultural University

Plant community study of the Hainan gibbon’s habitat restoration project

3.4.4

Publicity and Community Work Gaining support from local communities is key to the success of protecting the Hainan gibbon. The human population around Bawangling consists mainly of ethnic minority groups – the predominant Li and the Miao; in addition, from 1957 to the 1970s the Bawangling Forestry Bureau brought in many Han Chinese immigrants from the mainland as a workforce. While all three ethnic groups hunt and extract forest resources, the Miao are known for their skill and propensity in hunting, including the gibbons (Liu et al., 1984). The closest village cluster to the gibbon forest is east of Mt. Futouling, including a Miao village and two Li villages (Figure 3.1). During the 2003 survey, hunting with rifles was particularly severe on the eastern side of Mt. Futouling (Chan et al., 2005), and hunting intensity continued until 2010 when our team started to work in this forest. To bring public attention to the conservation plight of the Hainan gibbon, we started by launching a large-scale publicity campaign in collaboration with Bawangling and the major local press in 2005. We designed four gibbon-themed Fai chun, a traditional paper decoration for Chinese New Year, and printed 180,000 copies before the Chinese New Year; 10,000 copies were distributed to households in the surrounding communities during visits co-organised by Bawangling and KFBG, and the rest were enclosed in the newspaper on 26 January 2005 for island-wide distribution. This was followed by a collaboration with the University of Hong Kong and Hainan Normal University during the summer holiday of the same year, when we

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Bosco Pui Lok Chan and Yik Fui Philip Lo

organised a summer camp for 40 undergraduate students to commemorate the forest restoration project, during which we invited senior forestry officials, past and present directors of Bawangling and the first Hainan gibbon researcher, Professor Liu Zhenhe, to inaugurate the project. Throughout the years we also engaged the press and used social media in reporting news on the gibbons to enhance public awareness, and more than 100 articles and documentaries have been published by local, national and international media. In the second phase, we focused our education work on the local communities as they are likely to exert the biggest influence on gibbon conservation, organising school funfairs on both sides of Mt. Futouling and reaching out to about 1,000 teenagers who live around Bawangling (Figure 3.5) to engage the local community in gibbon conservation. In addition to recruiting villagers to form a community monitoring team (inaugurated in 2010), we also launched a sustainable agriculture programme in the rural community, providing agricultural training, seed grants, crop seedlings and beehives to lessen their reliance on forest products as an income source. We have recently held a publicity campaign in Hong Kong on the plight of the Hainan gibbon, as most people in Hong Kong have no idea that the rarest ape on Earth lives just 600 km from their home.

3.4.5

Identification of Hainan Gibbons outside Bawangling KFBG has been actively searching for the possible presence of gibbons outside Bawangling via community interviews and communications with forestry personnel since the project started. Major field expeditions targeting gibbons, some involving over 50 team members over 5-day surveys, have been conducted at remote sites with persistent anecdotal reports: Yinggeling National NR throughout 2003–2007, Exianling NR in March 2007, Limushan NR in February 2011 and Jiaxi NR in April 2012. None of these surveys yielded any positive results. Although the chance of isolated individuals surviving outside Bawangling cannot be entirely discounted, it is likely that Bawangling is the last refuge for the Hainan gibbon, as reported by a large-scale interview survey across Hainan (Turvey et al., 2017).

3.4.6

Policy Advocacy With long-term and good working relationships with Bawangling, the KFBG team has been a close ally for gibbon conservation. In early 2020, the national conservation authority, the National Forestry and Grassland Administration, decided to formulate a conservation action plan for the Hainan gibbon, and invited KFBG to draft part of the plan. The Hainan Tropical Rainforest National Park, in which Bawangling is a key part and the Hainan gibbon is seen as a flagship species, was officially gazetted in late 2020. A Hainan gibbon expert advisory committee has been formed under the recently established Hainan Tropical Rainforest National Park Institute, with the aim of coordinating conservation efforts and providing technical and strategic advice to the government. KFBG had been invited to expert advisory meetings, and the need to

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Figure 3.5 (a) Honourable guests and undergraduate students during the inauguration ceremony of the Hainan gibbon habitat restoration project in 2005. (b) A Hainan gibbon conservation funfair held at a local school in 2015.

enhance lowland forest protection and restoration, and expansion of the current gibbon monitoring team, have been repeatedly stressed as priority actions during high-level meetings. Some of our recommendations have already been adopted, such

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Bosco Pui Lok Chan and Yik Fui Philip Lo

as laying an overhead power line underground near the gibbon forest, and other actions are committed, such as decommissioning the associated hydropower plants and restoration of artificial plantations adjoining gibbon forest.

3.5

Scale of Conservation Investment The conservation of endangered species need not be expensive. Between 2003 and 2019, the total programme spending (excluding salaries of KFBG staff ) was a modest US$720,000. The biggest budget was to sponsor long-term monitoring and patrol enhancement, which cost US$280,000; the second biggest spending was on forest restoration, which cost US$210,000. The average annual project budget in recent years was approximately US$100,000. Instead of providing funding, we invested heavily in human resources, and visited Bawangling on a monthly basis in the first few years of the project as it took a lot of effort to convince partners about novel actions, train wardens and monitor progress of our key programmes. Two KFBG staff worked full-time on our Hainan gibbon project in the first 3 years; since then, one fulltime staff member has been overseeing the project, with technical inputs from other experts when and where needed.

3.6

Which Actions Did Not Work? While the gibbon population has been increasing and our overall experience implementing the project has been smooth, the 17-year partnerships with the reserve management and local communities has not been without failures.  Data collection for research questions: at the beginning, we trained and provided subsidies for wardens to collect scientific data; research topics we initiated included gibbon ranging patterns, gibbon diet, food plant phenology, food plant distribution and abundance, and seedling survival rate at restoration sites. These worked at the start, but the quality and quantity of data collected declined with time. It appears that relying solely on wardens for regular scientific data collection, despite detailed initial training, does not work without sustained on-site supervision.  Elimination of illegal activities: hunting and collection of forest products are deeply rooted in the local cultures; although much reduced and subject to heavy penalties, there are still cases of poaching, even by rifle, and exploitation of valuable forest products such as agar wood (Aquilaria sinensis) resin and lingzhi fungi (Ganoderma spp.). While the incentive to extract valuable forest products is mainly economic, hunting is seen by many as a recreational activity, as found in a case study in tropical Yunnan (Chang et al., 2017). The issue of poaching is serious throughout rural Hainan (Turvey et al., 2017), and much education work needs to be done for a genuine behavioural change among the rural communities.

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 Cessation of incompatible economic activities: logging of natural forest has been banned in Hainan since 1994. The Bawangling Forestry Bureau, established in 1957 for timber production, must generate alternative revenue to support over 1,000 past and present staff after the logging ban, and pine resin and hydropower production have been their major income sources. Despite the obvious negative impacts for gibbons, the management has been reluctant to stop these activities until very recently since environmental protection has become a greater priority on the national agenda.  Prioritisation of reserve management objectives: with the world’s most critically endangered primate species found only in Bawangling, one would have thought the management goals of the reserve and duties of all reserve personnel would be gibbon-centric, with all resources focusing on protecting the gibbons. However, there are different annual institutional targets to meet in addition to gibbon conservation, and each warden has the legal responsibility to patrol pre-assigned forest patches. This means that the Bawangling workforce may not be as readily available for gibbon-related work as would be desirable, especially on ad hoc actions that require a rapid response, such as tracking a newly discovered solitary gibbon or a poaching gang.  Public awareness and community conservation on Hainan gibbon: despite sustained efforts by the conservation authority and KFBG, using channels such as traditional media, social media and educational billboards throughout the community, many forestry workers and residents are reluctant to be connected and engaged, and low awareness of Hainan gibbon in the surrounding community was reported by Turvey et al. (2017) and a Masters student from the University of Exeter in the UK. Our attempts to introduce alternative livelihoods such as sustainable agriculture have been successful to a degree, even though some farmers are reluctant to be connected, and collection of valuable forest products, especially lingzhi fungi, is ongoing.

3.7

Conclusions The KFBG Hainan gibbon conservation project appears to be meeting its predetermined target in reversing the population decline of the Hainan gibbon, with population and group numbers showing increasing trends since our conservation intervention in 2003, and the recent range extensions to forests close to human settlements suggest that poaching and other detrimental human disturbance are declining. We believe our efforts in having a regular presence and building trust with local partners are key to our apparent success; in-depth knowledge of the project site and the local human population have enabled us to select feasible conservation options under the local political and socioeconomic situation, and to have open and honest dialogue with Bawangling in resolving differences. For the Hainan gibbon to thrive again across a larger landscape, we recommend the following conservation and research actions.

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3.7.1

Conservation  The extensive lowland, the Nanchahe valley, between the home range of the new gibbon group and Mt. Futouling measures about 70 km2 and is covered in regenerating and logged-over forest (Chan et al., 2020a). It adjoins current gibbon ranges and is likely to be used by the expanding gibbon population, which would provide prime lowland habitat supporting many more gibbon groups if not disturbed. Although within Bawangling, this area receives relatively little patrol effort and is an intrusion blackspot; there is an urgent need to increase patrol effort and awareness-raising in the surrounding area.  The Nanchahe valley, together with the selectively logged forests of Mt. Heiling and Mt. Yajiadaling where gibbons used to exist (Liu and Tan, 1990), provide about 150 km2 of forest contiguous with Mt. Futouling and could be naturally recolonised by the gibbons. It is imperative to step up patrol effort to halt poaching and other human disturbance in these areas.  The greater Bawangling area managed by the Bawangling Forestry Bureau measures about 744 km2, and over 97 per cent is reportedly covered in forest (including plantations). It would be wise to start converting the plantations to natural forest to provide extensive forest landscape for future gibbon population growth. As already mentioned, patrol effort should also be enhanced across this greater Bawangling area.  The presence of on-site NGO staff overseeing project implementation and providing support and guidance to Bawangling will be beneficial to gibbon conservation.

3.7.2

Research  Dispersed gibbons are extremely difficult to detect and thus to protect. Understanding the ecology, especially the ranging pattern of solitary gibbons and mechanisms of pair formation, are a research priority.  Members of the newly formed Group E have been roaming in the wider forest area north of Mt. Futouling before establishment of its territory on Mt. Dongbengling (Chan et al., 2020a). It is a priority to study the floristic composition of this mountain in order to understand habitat selection of Hainan gibbons during group formation.  None of the previous studies managed to collect genetic samples of all gibbon individuals in order to investigate the genetic relatedness of the entire population. A coordinated effort to collect samples from all living gibbons to understand the population dynamics, especially dispersal and group formation mechanisms, of Hainan gibbon will be beneficial.  Botanical studies in the Nanchahe valley and the greater Bawangling area should be conducted to understand the vegetation composition and investigate whether enhancement planting of gibbon food trees is needed. The most cost-effective forest enhancement/restoration method in Bawangling specifically for Hainan gibbon

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should also be investigated, for example whether to allow natural succession with thinning of non-native species, or conduct active restoration with enrichment planting of hardy, early-successional gibbon food tree species to accelerate succession.

Acknowledgements We are grateful to Bawangling National Nature Reserve and the Forestry Department of Hainan for their trust in us, and all the hard work of colleagues and partners in saving the species. This project has been funded by the Kadoorie Farm and Botanic Garden.

References Chan, B.P.L., Fellowes, J.R., Geissmann, T. and Zhang, J.F. (2005). Hainan Gibbon Status Survey and Conservation Action Plan – Version I. Kadoorie Farm and Botanic Garden Technical Report No. 3. KFBG, Hong Kong. Chan, B.P.L., Lo, Y. and Mo, Y. (2020a). New hope for the Hainan gibbon: formation of a new group outside its known range. Oryx, 54(3): 296. Chan, B.P.L., Lo, Y.F.P., Hong, X.J., et al. (2020b) First use of artificial canopy bridge by the world’s most critically endangered primate the Hainan gibbon Nomascus hainanus. Scientific Reports, 10: 15176. Chang, C.H., Barnes, M.L., Frye, M., et al. (2017). The pleasure of pursuit: recreational hunters in rural Southwest China exhibit low exit rates in response to declining catch. Ecology and Society, 22(1): 43. Chivers, D.J. (1974). The Siamang in Malaya. A Field Study of a Primate in Tropical Rainforest. Karger, Basel. Fellowes, J.R., Chan, B.P.L., Zhou, J., et al. (2008). Current status of the Hainan gibbon (Nomascus hainanus): progress of population monitoring and other priority actions. Asian Primates Journal, 1: 2–9. Jiang, Y.X., Wang, B.S. and Zang, R.G. (2002). Biodiversity of Tropical Forests of Hainan Island and its Formation Mechanism (in Chinese). Science Press, Beijing. Kadoorie Farm and Botanic Garden. (2001). Report of rapid biodiversity assessments at Bawangling National Nature Reserve and Wangxia Limestone Forest, Western Hainan, 3 to 8 April 1998. South China Forest Biodiversity Report Series No. 2. KFBG, Hong Kong. Liu, Z.H. and Tan, C.F. (1990). An analysis of habitat structure of the Hainan gibbon (in Chinese with English summary). Acta Theriologica Sinica, 10: 163–169. Liu, Z.H., Yu, S.M. and Yuan, X.C. (1984). Resources of the Hainan black gibbon and its present situation (in Chinese). Chinese Wildlife, 6: 1–4. Liu, Z.H., Jiang, H.S., Zhang, Y.Z., et al. (1987) Field report on the Hainan gibbon. Primate Conservation, 8: 49–50. Liu, Z.H., Zhang, Y.Z., Jiang, H.S. and Southwick, C. H. (1989). Population structure of Hylobates concolor in Bawangling Nature Reserve, Hainan, China. American Journal of Primatology, 19: 247–254.

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Mittermeier, R.A., Rylands, A.B. and Wilson, D.E. (eds.) (2013). Handbook of the Mammals of the World. Vol. 3 Primates. Lynx Edicions, Barcelona. SFA (State Forestry Administration Survey and Planning Institute) and Bawangling Management Office. (2001). Hainan Bawangling National Nature Reserve master plan (2002–2010) (in Chinese). Internal Report. Turvey, S.T., Traylor-Holzer, K., Wong, M.H.G., et al. (eds.) (2015). International Conservation Planning Workshop for the Hainan Gibbon: Final Report. Zoological Society of London/IUCN SSC Conservation Breeding Specialist Group, London. Turvey, S.T., Bryant, J.V., Duncan, C., et al. (2017). How many remnant gibbon populations are left on Hainan? Testing the use of local ecological knowledge to detect cryptic threatened primates. American Journal of Primatology, 79(2): e22593. Wu, W., Wang, X.M., Claro F., et al. (2004). The current status of the Hainan black-crested gibbon Nomascus sp. cf. nasutus hainanus in Bawangling National Nature Reserve, Hainan, China. Oryx, 38: 452–456. Xu, L.H. and Liu, Z.H. (1984). Gibbon calls at Bawangling: survey report of Hainan gibbon (in Chinese). Chinese Wildlife, 4: 60–62. Zhang, Y. (1992). Hainan gibbon (Hylobates concolor hainanus) threatened. Asian Primates, 2(1): 6. Zhang, Y. and Sheeran, L. (1994). Current status of the Hainan black gibbon (Hylobates concolor hainanus). Asian Primates, 3: 3. Zhu, H. (2016). Biogeographical evidences help revealing the origin of Hainan Island. PLoS ONE, 11(4): e0151941.

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Gibbons in the Anthropocene Lessons from a Long-Term Study in Indonesia Susan M. Cheyne, Abdulaziz K, Supiansyah, Twentinolosa, Adul, Claire J.H. Thompson, Lindy Thompson, Reychell Chadwick, Hélène Birot, Carolyn Thompson, Cara H. Wilcox and Eka Cahyaningrum

4.1

Introduction This work was initiated by the Borneo Nature Foundation (BNF) in May 2005 using triangulation to determine where the different gibbon groups were in order to facilitate the habituation process (Cheyne, 2010). Following the mapping of the group territories, systematic habituation began. Gibbons were not disturbed while singing, but the morning songs were used to locate gibbons for following. The first successful follow (i.e. the gibbons did not flee) took place in July 2005, though it was not until March 2006 that groups were considered fully habituated. Since then, a full-time team has been following seven different groups to obtain behavioural ecology data as well as monitor the density and population of gibbons within the main study area (Brockelman and Srikosamatara, 1993). Following Groves (2001) and Geissmann (2007) the Bornean agile gibbon (also referred to as the Bornean white-bearded or southern gibbon) has been recognised as a separate endemic Bornean species designated Hylobates albibarbis. This gibbon is classified as endangered by the International Union for Conservation of Nature (IUCN) Red List of Threatened Species, is on the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) Appendix 1, and is protected under Indonesian law. This species occurs within the Kalimantan regions of Indonesian Borneo, east of the Kapuas River (west Kalimantan), west of the Barito River (Central Kalimantan), south of the Busang River (Central Kalimantan) and to the north and west of the Schwaner Mountains (Marshall et al., 2020). Some of the main areas with substantial populations are in Central Kalimantan, i.e. Sebangau National Park (including the Natural Laboratory for the Study of Peat-swamp Forest (NLPSF)), Tanjung Puting NP, Bukit Baka Bukit Raya NP, Hampapak Nature Reserve (NR), Tahura, Lamandau, Tuanan, Kendawangan NR and Arut Blantikan; and in West Kalimantan, i.e. Rongga Perai LH, Gunung Palung NP and Sungai Putri (Campbell et al., 2008). Female H. albibarbis gibbons reach sexual maturity at about 48 months (SD 3.67) (Cheyne and Chivers, 2006; Cheyne et al., 2008a; BNF, unpublished data) and the menstrual cycle interval lasts 26 days (SD 0.65), with peri-ovulatory swelling

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persisting for about 6.3 days (Cheyne and Chivers, 2006). Gestation is 7–9 months and the inter-birth interval (IBI) is 2.4–3.7 years (Cheyne, 2010; BNF, unpublished data). Gibbons do not exhibit reproductive suppression and mature sub-adults are ejected from the natal group by the same-sex parent (Chivers, 1972). Males weigh 6.1–6.9 kg and females 5.5–6.4 kg. Pelage can vary but generally H. albibarbis has black hands and feet with brown arms and legs. White eyebrows and/or cheeks are common but not universal, and the main body colour is usually dark brown with dark chest and head cap. Newborns are very pale brown with no hair on their face, palms or soles of the feet, all of which are black (S.M. Cheyne, personal observation). Hylobates albibarbis is found in primary forest and disturbed (logged) secondary forest, and in lowland and montane habitats including peat-swamp forest (Cheyne et al., 2008b, 2016; Hamard et al., 2010). As a result of the habitat, the average heights of gibbons in the forest are very dependent on the type of forest they inhabit. Hylobates albibarbis gibbons have also been studied at Gunung Palung NP with reference to feeding ecology (Marshall, 2004; Dillis et al., 2014), population demographics (Marshall, 2009) and for niche overlap (Marshall et al., 2009a), as well as in Tuanan, Mawas Reserve, where research focused on feeding ecology (Vogel et al., 2009) and the impact of smoke (Haag, 2007). This chapter reviews all the literature and showcases the scope of research topics covered by the BNF, looking at lessons learnt that could be applied to other sites to help inform conservation actions and efforts.

4.2

Methods

4.2.1

Study Site The study site is the Natural Laboratory for the Study of Peat-swamp Forest. NLPSF is located in the northeastern part of the Sebangau National Park, Central Kalimantan, Indonesia (Figure 4.1). The Sebangau National Park covers an area of 5,600 km2 of peat-swamp forest (Page et al., 1999). The research area is a 4-km2 grid transect system containing seven habituated gibbon groups. The Sebangau National Park is characterised by low-elevation peat-swamp forest, presenting three different forest types: mixed swamp forest (MSF), low pole forest and tall interior forest (Cheyne et al., 2008b). Our study was carried out in MSF, which occupies 40 per cent of the total area of Sebangau National Park (Shepherd et al., 1997). The MSF extends approximately 4 km from the margin of the forest into the interior. It is beyond the location of the river flooding zone. The forest is tall and stratified, with an upper canopy at approximately 35 m, a closed layer between 15 and 25 m, and an understorey of smaller trees at 7–12 m. Trees grow on hummocks interspersed with hollows, which fill with water during the wet season. Many of the species have stilt or buttress root systems and pneumatophores are common. Typical trees of the upper and mid-canopy include Aglaia rubinigosa, Calophyllum hosei, C. lowii, C. sclerophylum, Combretocarpus rotundatus, Cratoxylum galucum, Dactylocladus

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Base Camp Rivers NLPSF Forest Cover

Figure 4.1 Location of the Natural Laboratory for the Study of Peat-swamp Forest (NLPSF) within the Sebangau National Park. Forest cover is shaded grey, non-forested areas white. Source: Ehlers Smith et al. (2013).

stenostachys, Dipterocarpus corieus, Dyera costulata, Ganua mottleyana, Gonstylua bancanus, Mezettia leptopoda (Lucas et al., 2011), Neoscortechinia kingii, Palaquium cochleariifolium, P. leiocarpum, Shorea blangeran, S. teysmanniana and Xylopia fusca (Page et al., 1999; Coiner-Collier et al., 2016). Owing to large-scale peat drainage, dry-season fires are now the most serious threat to tropical peat-swamp forests and were prevalent again in 2015. In 2006, an El Niño event led to particularly dry conditions and extensive peatland and forest fires in Kalimantan. In the Sebangau National Park, we observed differences in both litter-fall (much higher in smoky 2006 than in largely smoke-free 2001; Harrison et al., 2007) and gibbon singing behaviour (gibbons sang less during smoky periods in 2006; Cheyne, 2007), which were most probably caused by the thick smoke clouds enveloping the area from September to November 2006. This indicates that even though most burning occurs in cleared areas, high smoke levels may be having serious effects on forest flora and fauna in unburned forested areas. Furthermore, it is likely that the effects of smoke on forest dynamics and wildlife are not limited to these two examples, and that the effects could be quite widespread and potentially even more

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serious for the forest as a whole. Despite their preliminary nature, these observations provide further evidence of the negative impacts of fire and smoke on the wild systems of Kalimantan and, as such, strengthen the argument for making available increased resources to prevent and fight these fires. In conclusion, it seems likely that increased smoke during fire seasons could be affecting both litter-fall and gibbon singing. There are two important implications of these findings. Firstly, they indicate that the effects of smoke on the forest and its wildlife can be important even in unburnt areas (previously, discussion has been limited to only burnt areas). Secondly, it is likely that the effects of smoke on forest dynamics and wildlife are not limited to the two examples discussed here, and that their effects could therefore be widespread, and even more serious for the forest as a whole.

4.2.2

Data Collection Groups are located by their morning singing or by searching within their known territory if no sleeping tree was located the previous day. Gibbon groups are then followed until they enter the afternoon sleeping tree or are lost. Active periods average 8 hours (range 5.87–9.25 hours). Data are collected using 5-minute instantaneous focal sampling (Altmann, 1974; Cheyne, 2010) and include the following.










Primary activity. Secondary activity. Distance moved in last 5 minutes. Height of gibbon in the tree. Height of the tree. GPS location every 5 minutes. Size, height and species of any feeding trees. Singing behaviour. Interactions between focal group and any other gibbons or other species (e.g. orangutans).
Characteristics of sleeping trees and the location of the gibbon(s) within these trees.
Mother–infant interaction data. These data are entered into a custom Microsoft Access database for archiving and data analysis (for further details see Cheyne, 2010).

4.3

Summary of Gibbon Work Since 2005, the BNF team has collected a substantial amount of baseline behaviour data on feeding, ranging, sociality, population composition and activity patterns in relation to anthropogenic disturbance, subsequently publishing 50 peer-reviewed articles across 21 journals (Table 4.1). It is important to note that we have not undertaken any research that could be classified as ‘cultural’, though we continue to

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Table 4.1 Summary of all projects carried out since 2005 and related publications.

Topic

Time/duration of study

Reference

Current/future projects

Activity budgets

2005 and ongoing

Cheyne (2010); Cheyne et al. (2013a, 2013b)

Ongoing to look for changes over time and to assess impacts of forest fire haze and habitat loss

Reproduction and mating

2005 and ongoing

Cheyne (2010); Cheyne et al. (2019); Thompson et al. (2022)

Gibbon group dynamics, changes over time

Ranging patterns

2005 and ongoing

Singh et al. (2018); Cheyne et al. (2019)

Daily path length and seasonal variation over time

Travel order

2005 and ongoing

This chapter

Social structure

2005 and ongoing

Cheyne (2009, 2010)

Social network analysis including proximity of non-adults

Vocalisations

2005 and ongoing

Wanelik et al. (2013)

Assessing signalling of female reproductive status (ovulation) in their song using automatic recording units

Dominance/aggression

2005 and ongoing

Cheyne et al. (2010b)

N/A

Foraging and energetics

2005 and ongoing

Cheyne et al. (2010a)

1. Female Pivot (complete)

Diet and feeding

2005 and ongoing

Cheyne et al. (2005); Cheyne (2008a); CoinerCollier et al. (2016)

Differences in female and male feeding ecology (i.e. species, duration, bouts)

Anthropogenic impact on populations

2005 and ongoing

Cheyne (2007); Harrison et al. (2007)

Ongoing to look for changes over time and to assess impacts of forest fire haze and habitat loss

Population estimates

2005 and ongoing

Buckley et al. (2006); Cheyne et al. (2008b, 2016); Cheyne (2011a)

Improve gibbon triangulation/survey methods based on IPS symposium

Mother–infant dyads and individual development

2005 and ongoing

Thompson et al. (2022)

1. Polygyny in southern Bornean gibbons 2. Infant development

Habitat

2005 and ongoing

Harrison et al. (2005); Cheyne et al. (2010a, 2018)

Habitat defendability index

Conservation

2005 and ongoing

Campbell et al. (2008); Cheyne et al. (2012a)

Ongoing with best practice guidelines for (1) rehabilitation and reintroduction and (2) gibbon population survey methods

Locomotion

2005 and ongoing

Cheyne (2011b); Cheyne et al. (2013a)

N/A

Cognitive abilities

2012–2013

Gibbon hand preference analysis (in preparation)

N/A

Health

2011

Hilser (2011)

Parasites and calling as an indication of gibbon health

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seek opportunities to do so. The long-term research aims of BNF’s gibbon behaviour project are as follows. 1. To monitor gibbon population size, distribution, behaviour, diet and health in Sebangau National Park. 2. To monitor gibbon population density at both the main site and at remote sites in Sebangau National Park. 3. To monitor food availability and overall productivity in the forest. 4. To monitor gibbon energy intake, and to assess how this is governed by food availability and how it relates to the behaviour and health of the population. 5. To monitor the effects of anthropogenic disturbance and conservation measures on the gibbon population and food availability/forest productivity. 6. To investigate the changes in gibbon singing behaviour in response to changing climactic conditions. The results in the following sections are collated from data collected on seven different groups since 2005 (unless otherwise stated).

4.3.1

Activity Budgets Gibbons in Sebangau National Park spend 40 per cent of their time resting, with feeding and travelling accounting for 23 per cent each (Figure 4.2). The gibbons spend on average the same time in travel, singing, social and resting behaviour categories.

Figure 4.2 Average percentage of time in the six primary activity categories for two groups.

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Figure 4.3 Percentage of time spent in (a) travel, (b) singing, (c) social and (d) resting behaviour categories.

Brachiation is the clear preferred mode of travel (Figure 4.3a) and duets form the largest category of singing (Figure 4.3b), with females not joining the male on 21 per cent of occasions. Allogrooming is the dominant social activity (Figure 4.3c) and the favoured resting posture is sitting on a branch (Figure 4.3d).

4.3.2

Reproduction and Mating Gibbon IBI (c. 3.7 years, based on 17 births), although slightly longer than that at other sites, suggests the population is reproducing as expected despite the previous disturbance in the forest. Gibbon births are spread throughout the year and given the energetic demands of reproduction and lactation, it is expected that most births would occur during periods when high-quality food is available (Knott, 1998, 2005; Cheyne, 2008b; Coiner-Collier et al., 2016), not during the dry season, a time of low productivity and low food availability (Vogel et al., 2015; Harrison et al., 2016). Sex ratio appears to favour females at adulthood, hence suggesting a cost for males. Furthermore,

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interesting observations of polygyny (where a single male has more than one female mate) have been documented in one gibbon group in Sebangau National Park (Thompson et al., 2022). This is the first case of polygyny recorded in this species and is potentially due to a lack of neighbouring groups and competition for food and space, coupled with delayed male dispersal and a female skew in the population. These data present new information on gibbon demographics and highlight the importance of species- and habitat-specific differences in this highly adaptable species.

4.3.3

Ranging Patterns Gibbons are highly territorial and have two key areas within these territories (Cheyne et al., 2019): the core range, in which we find all sleeping trees and the trees from which the gibbons duet, and the wider home range (HR), which has varying levels of overlap with neighbouring gibbon groups. The core area is strenously defended, with the wider HR being more of a shared area for neighbouring groups (Singh et al., 2018). Gibbon home- and core-range sizes were calculated using 95 and 50 per cent volume contours of kernel density estimates. Home ranges varied between 58.74 and 147.75 ha, with a mean of 95.70  SD 37.75 ha, the highest of comparable Hylobates species (Vogel et al., 2009; Kim et al., 2011; Reisland and Lambert, 2016). Core ranges varied between 20.70 and 51.31 ha, with a mean of 31.70  SD 13.76 ha. Gibbons had consistant site fidelity for their home and core ranges; percentage overlap ranged from 4.30 to 23.97 per cent, with a mean 16.50  SD 8.65 per cent overlap in home-range area. Core ranges did not overlap, with the exception of two groups in which a 0.64-ha (2.7 per cent) overlap occurred. Unsurprisingly, forest loss from fire does affect the location of the HR of the impacted group, but does not appear to affect adjacent groups, though more data are needed to confirm this.

4.3.4

Travel Order Previous preliminary work highlighted that it was the adult female who predominantly led the group, followed by the adult male as leader, and occasionally one of the subadults. Our long-term data indicate that adult females are indeed leading the groups in the majority of cases (46–49 per cent of all travel occasions; Figure 4.4). Studies have shown that adult females are most likely to lead a group. Chivers (1974) found that the adult female of a siamang (Symphylangus syndactylus) group led 65 per cent of travel bouts. Ahsan (2001) found that for hoolock gibbons (Hylobates hoolock) the adult female led 61 per cent of travel bouts, with the adult male leading only 33 per cent of bouts and the juvenile leading 6 per cent of bouts. Gittins (1979) found that for agile gibbons in Malaysia (Hylobates agilis) the female led 36 per cent of travel bouts and the male 53 per cent of bouts. Barelli et al. (2008) also found that females consistently lead the group more than males. Our data are consistent with other studies on adult female gibbon movements and feeding patterns (BNF, unpublished data). Females will actively seek to feed in trees alone and spend more time feeding when alone in a tree. The females preferentially seek trees of 16–20 m, though

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Figure 4.4 Travel order averaged across all groups. AF, adult female; AM, adult male; Sub, sub-adult; Juv, juvenile.

if there were more availability of trees in bigger height classes, we suspect the females would preferentially select these trees. To summarise these results:
females lead group movement in most cases;
females are the pivot point of the group (i.e. while not always in the front, the other group members orientate themselves to the female’s position); females are first into a feeding tree;

females spend longest in feeding trees if other members of the group are present in that tree;
females preferentially feed alone. We conclude that females are leading the groups, modifying their feeding behaviour to prioritise access to food sources and acting as a central pivot for the other group members to orientate themselves around.

4.3.5

Social Structure On average the gibbons are in close proximity to each other, based on the direct observations of the research teams. These data are limited by the human observers, so the focus was moved to following the adult male and female of each group. Using Global Positioning System (GPS) data, we obtained more detailed information about the movements of the adult male and female in relation to each other and their territory. Males often stay close to the female but are also travelling further to ‘patrol’ the edges of the territory. Females have a more direct daily travel route than the male. The gibbons are never more than 50 m apart, and at the closest are in the same tree

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engaging in social behaviour. The adult male and female never sleep together however, and sleeping tree distances range from 2 to 25 m (in the above example, the sleeping trees are 24 m apart). This is another example of the strong pair-bond between adult gibbons.

4.3.6

Vocalisations Gibbons are characterised by their species-specific calls. The frequency of singing is known to be affected by rainfall, with singing occurring less in the wet season (Cheyne et al., 2007; Wanelik et al., 2013; Clink et al., 2017, 2018). Throughout the study period, meteorological factors such as rain and wind significantly influenced onset time of singing, though cloud cover and temperature had no significant effect. None of the astronomical cues proved significant in determining singing behaviour. These findings identify a clear climatic, but not astronomical, influence on the singing behaviour of gibbons and the onset time of singing. Owing to the proximity of this study site to the equator, it is likely that the variation in astronomical cues was too slight to influence the behaviour of the gibbons. Although the light intensity data were not significant, there seems to be a trend and a larger dataset may provide additional information regarding the possible effects of light (Cheyne, 2007). Air quality was significantly worse during smoke months and rainfall was significantly less, yet singing behaviour was also reduced. Although the number of great calls/bouts was not significantly different between non-smoke and smoke months, the number of days per month spent singing is significantly reduced and the total length of singing bouts was significantly less between September and November 2006 (smoke season). This is interesting, as with the reduction in rainfall in the smoke season of 2006, it would be expected that gibbons would sing more frequently and for longer periods when there is less rain (Mitani, 1985; Cheyne et al., 2007). It is possible that one of the effects of smoke is a reduction in singing because of the poorer health of the gibbons.

4.3.7

Dominance and Aggression The gibbons in this area are at a low density of 2.53 groups/km2 (Cheyne et al., 2008b, 2016; Hamard et al., 2010). We have only witnessed territorial encounters on 5 per cent of follows (18 of 360 days, average follow 8 hours/day). Reichard and Sommer (1997) propose that aggressive encounters are not inevitable outcomes of meetings between wild gibbons, possibly due to the proposed degree of affiliation between the groups. However, in all 18 instances of group encounters from this study, there was aggressive chasing, branch shaking and alarm calling (i.e. loud and fast duets; Cheyne, 2010). It is possible that the low density reduces the frequency of encounters but that group encounters remain aggressive. The encounter reported herein is the only one where we have witnessed physical contact between the opposing groups and this is the only occasion we have witnessed aggression between a territorial group and a lone male, resulting in the death of the lone male from his injuries (Cheyne et al., 2010a).

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Haag (2007) briefly described several encounters between a solitary male and her study group of H. albibarbis in Tuanan. Although the solitary male did not die as a result of the encounters, Haag’s report is interesting because the mated female took a particularly active role in attacking the solitary male and once ‘fought him to the ground for more than 2.5 hours, only taking breaks to nurse the infant or copulate with her partner’, whereas the mated male was much more passive. During the last encounter, the lone male was observed to sit within 10 m of the mated male without provoking any reaction. This encounter did not result in injuries of the nature reported from Sebangau National Park. Haag’s study group had a juvenile female and dependant male infant, whereas the group composition reported here consisted of a sub-adult female and dependant male infant. In all other inter-group encounters witnessed in Sebangau National Park, there have been no physical attacks like the one reported here. A driving force behind social monogamy is the tendency of adult gibbons to exclude same-sex conspecifics during group encounters (Ellefson, 1968; Gittins, 1980, 1984; Mitani, 1985; Raemaekers and Raemaekers, 1985; Palombit, 1993). In this case it was the adult male of the group who physically attacked the lone male, although all members of the group contributed to the territorial defence and attacked indirectly by displaying and mobbing the injured lone male. Bartlett’s (2001) suggestion that agonistic encounters between adult pairs provide an opportunity for sub-adults to meet requires further study but is not applicable in this case. Again, the distinction between aggressive encounters between two groups and an aggressive encounter between one group and a lone individual must be clarified. The only hypothesis we can offer for the lone male being so far into the group’s territory is that he may have heard the sub-adult female of the group singing and was attempting to pair with her. Haag (2007) reports that the adult female led the attack and we have observed subadult gibbons being excluded from feeding trees and sleeping trees by the opposite-sex parent (Cheyne, 2010; Cheyne et al., 2013a). The idea that only same-sex gibbons lead these interactions is clearly not the full story. More detailed and long-term observations on different gibbon populations are needed to tease out the sex-specific roles of gibbons. It is clear that we have a very limited understanding of lethal aggression among gibbons, including frequency of occurrence and why it happens. More studies are needed in areas where there are several habituated groups and known lone individuals. It is difficult to ascribe intentions to a non-human primate without sounding anthropomorphic. In this instance, the group members could have continued the attack to ensure the lone male was dead. Instead they disabled the intruder and left (Cheyne et al., 2010a, 2010b). More research is needed to elucidate differences between lethal aggression towards a group male and that directed towards a lone male.

4.3.8

Diet and Feeding We have data from 135 species of tree from 49 families amounting to 153,707 feeding bouts since May 2005. Gibbons maintain a preference for feeding trees from 13 known families (Figure 4.5) (Cheyne et al., 2005; Dunbar et al., 2019): Sapotaceae, Moraceae, Anacardiaceae, Ebenaceae, Menispermaceae, Myrtaceae, Sapindaceae,

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Figure 4.5 Percentage of feeding bout length by plant family.

Figure 4.6 Percentage of time spent feeding on different food classes.

Apocynaceae, Tetrimeristaceae, Gnetaceae, Calophyllaceae, Meliaceae and Annonaceae. Four families (Sapotaceae, Moraceae, Annonaceae and Myrtaceae) account for up to 43 per cent of all species consumed. As expected, the bulk of the diet consists of fruit, including figs (63 per cent), followed by young leaves and shoots (27 per cent), flower buds (8 per cent), invertebrate consumption (1 per cent), water (1 per cent) and fungi (0.02 per cent) (Figure 4.6).

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Figure 4.7 Percentage of time consuming the top eight species.

The proportion of time spent feeding on different species can be split into three categories showing that 77 per cent of food species are fed on for less than 1 per cent of the time. Of the eight species consumed more than 3 per cent of the time, figs (Ficus spp.) are the top species consumed (Figure 4.7).

4.3.9

Anthropogenic Impact on Populations In 2015 the island of Borneo was blanketed in toxic haze from forest fires and burning peatlands. Data on number of fires by location and time period can be obtained through Global Forest Watch (www.globalforestwatch.org/topics/fires/?gfwfires= true). The number of fires quoted here is for the whole of Indonesia from 1 June to 1 November 2015. During this period, 94,588 fires have occurred in Kalimantan and Sumatra, of which 53 per cent occurred outside concessions, 30 per cent in pulpwood concessions, 13 per cent in oil palm concessions; 60 per cent occurred on peatlands and 27 per cent in indicative moratorium areas. The health effects of smoke on gibbons (and other animals) can only be inferred from studies on humans (peer-reviewed publications on the health impacts of smoke and number of premature deaths from the previous severe El Niño fire season of 1997–1998 can be found through the Max Planck Institute). The effects on infant and juvenile gibbon mortality could also be a major problem. Gibbons reproduce once every 2–3 years (Savini et al., 2008; BNF, unpublished data) and increasing mortality

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could have serious repercussions on population recruitment. Behavioural effects are hard to predict without more data, but reduced singing for several months a year (when singing is normally at a peak; Cheyne et al., 2008b, 2016; Hamard et al., 2010) could be detrimental for territorial spacing/defence, communication and, ultimately, reproduction.

4.3.10

Locomotion Uneven canopy and canopy gaps pose a crucial problem for arboreal primates, as they present either a very large break in the canopy or a succession of smaller breaks (uneven canopy) (Cheyne, 2011b; Cheyne et al., 2013b). Efficient, cost-effective travel through the canopy, in terms of reducing distance (and time) of direct travel between two points, is heavily constrained by the presence of gaps (Cannon and Leighton, 1994). Gibbons may be hypothesised to select continuous forest types over discontinuous types, and higher canopies over low. During travel, gibbons tend to follow established routes through the trees, referred to as ‘arboreal highways’ (Chivers, 1974). These routes minimise their chance of encountering gaps and also provides support for the theory that they appear to be actively selecting certain structures for travel. Our results (Cheyne et al., 2013b) indicate that gibbons favour continuous-canopy forest, higher canopy heights and trees with a larger diameter at breast height. Gibbons select these trees despite the study site being dominated by broken-canopy forest and small trees. Gibbons also change frequently between brachiation, climbing, clambering and bipedal walking in this disturbed forest depending on the size of gap to be crossed. Gibbons are shown to be capable of adapting to some human-induced disturbances in forest continuity and canopy height, and to the presence of smaller trees (e.g. after selective logging). The key findings of this study are as follows. 1. Gibbons can adapt their locomotor ecology to the effects of selective logging (i.e. reduce travel by brachiation and increase other modes of travel). 2. The gibbons are choosing a ‘limited’ resource – the continuous tall canopy – but there is evidence of a level of disturbance to which they cannot adapt. Loss of trees 6–15 m high and 7–17 cm diameter at breast height would be severely detrimental to this gibbon population given the limited availability of larger trees following the selective logging. The exact percentage loss of these trees that gibbons could tolerate needs more work. 3. Gibbons clearly prefer continuous canopy. We did not observe crossings of gaps larger than 12 m, which may be a constraint of the gibbons’ physical abilities rather than a direct response to the presence of gaps (i.e. gibbons cannot cross gaps of more than 12 m in one movement).

4.3.11

Health Literature is sparse for parasite assessments in gibbons. Using several indices of parasitism, gibbons had significantly lower infections across all parasite taxa when

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compared with red langurs (Presbytis rubicunda) and orangutan (Pongo pygmaeus wurmbii). Despite variations in specific parasite taxa, a large proportion of parasites found (n ¼ 10) occurred in all three primates, indicating a substantial amount of parasite transmission between sympatric primates at this site (Hilser, 2011). Gibbons harboured the lowest variety and prevalence of parasites yet are known to be highly social. In Sebangau National Park, gibbons spent 24 per cent of their social time playing and 35 per cent allogrooming (Cheyne, 2010), which may be a behaviour for reducing ectoparasites in addition to reinforcing social cohesion, but is likely to increase the pervasiveness of horizontally transmittable pathogens. However, although this may account for the spread of parasites between conspecifics, it does not appear to exacerbate their parasite burdens to that of the levels of the langurs. Many epidemiological questions remain regarding the role that sociality and behaviour have on the spread of infectious disease (Hilser, 2011).

4.4

Discussion Our long-term forest and phenology monitoring has confirmed that the NLPSF is recovering following years of legal and illegal logging (Harrison et al., 2010; Marshall et al., 2009b). Using standard fixed-point triangulation methods (Brockelman and Srikosamatara, 1984; Brockelman and Ali, 1987; Nijman and Menken, 2005; Cheyne et al., 2008b; Hamard et al., 2010), we have been monitoring the gibbon population since 2005. We have identified a gradual increase in the population density across the main study site and five remote sites within the NLPSF. The relatively consistent behaviours across all categories is encouraging, suggesting that gibbons are highly adaptable but also predictable, traits which will help inform their conservation.

4.4.1

Future Research Plans for Borneo Nature Foundation on Gibbon Research 1. Mother–infant relationships and infant development: (a) How does the behaviour of both mother and infant change during the infant’s development? (b) How does this change, if any, impact the mother–infant relationship? (c) How do activity patterns of mothers with different age offspring differ? (d) Are there any behaviour differences between infants of different sex? (e) When do infants start vocalising and imitating their parents in the morning singing bouts? (f ) When do infants start producing mature vocalisations? (g) How soon after producing such vocalisations do they disperse? 2. Polygyny in southern Bornean gibbons: (a) Try to secure funding to investigate the paternity of both infants within the polygynous group. (b) To use this as a launch pad to obtain more funding for paternity testing of all gibbons using long-term DNA samples.

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3. Group cohesion: male–female ranging behaviour: (a) Does the adult male or adult female lead the group? (b) How do movement patterns differ between males and females? (c) How do the male and female move in relation to each other? (d) What factors may impact these ranging differences, if any, between the male and female?

4.5

Conservation Following the Kalimantan-wide density surveys, we estimate there are 115,000 individuals of H. albibarbis living in Kalimantan. There is a severe lack of data on gibbons in non-protected areas or small forest areas, which may also contain viable populations. Current data suggest the population of H. albibarbis to be between 75,000 and 130,000 individuals throughout its range, of which at least 50 per cent are found in tropical peat-swamp forest (Cheyne et al., 2012b, 2016; Gilhooly et al., 2015), although there are limited estimates for tropical peat-swamp forest locations for these species. In the absence of a full population and habitat viability analysis (PHVA) all survey data are vitally important to obtain accurate population estimates of all four species of gibbon on Borneo. Gibbons are able to maintain a good density across habitat types and even in unprotected areas. Our population estimates are based on known forest sizes, predominantly forest with some level of legal protection. The numbers of gibbons living in non-protected forest is a cause for concern as it is almost impossible to extrapolate current population numbers to these areas. It is crucial to remember that while these numbers indicate that gibbon populations are thriving, the habitat loss, wildlife trade and presence of so many populations in non-protected areas means that all gibbons in Kalimantan are still endangered. Gibbons occur in many forests where orangutans are absent, meaning they are the largest frugivore present for seed dispersal and maintaining forest dynamics. The ability of wildlife to recover and adapt following human disturbance is crucial to their long-term survival so these study sites are especially important.

Acknowledgements This work was carried out within the Borneo Nature Foundation research. This work was supported by grants to S.M.C. from the Department of Anthropology, George Washington University, Primate Conservation Inc., Cambridge University Philosophical Society, Rufford Small Grants for Conservation, Columbus Zoo, IdeaWild, Arcus Foundation, US Fish and Wildlife Service, Gibbon Conservation Alliance, Wallace Global Fund, The Orangutan Tropical Peatland Trust and Peoples Trust for Endangered Species. S.M.C. gratefully acknowledges the contribution of all the researchers who assisted with the project: Adul, Ambut, Andri Thomas, Iwan,

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Ramadhan, Santiano, Twentinolosa, Yudhi Kuswanto, Zeri, Adul, Azis K, Aman, Azis, Jono, Ciscoes, Ari, Hendri, Supian, Tommy, Uji, Unyil, Simon J. Husson, Mark E. Harrison, Helen Morrogh-Bernard, Laura J. D’Arcy, Claire J.H. Thompson, Ellie Monks, Grace Blackham, Bernat Ripoll Capilla, Dave Smith, Andrea Höing, Lindy Thompson, Michal Zrust, Reychell Harris, Carolyn Thompson, Hélène Birot, Joana Aragay, Jess Walters, Jeremiah Taylor, Aimee Oxley, Sarah Batty, Connie Miller, Emily von Boucker, Lizzie Walker, and all the many students and volunteers whose work has contributed to our long-term dataset. S.M.C. gratefully thanks the Indonesian Ministry of Research and Technology (RISTEK) and the Indonesian Department of Forestry for permission to carry out research in the NLPSF and thanks Dr Suwido H. Limin and Yunsiska Ermiasi from CIMTROP for sponsoring her research and providing invaluable logistical support since the beginning of this work.

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(eds.), The Gibbons: New Perspectives on Small Ape Socioecology and Population Biology. Springer Science, New York: 161–188. Marshall, A.J., Ancrenaz, M., Brearley, F.Q., et al. (2009b). The effects of forest phenology and floristics on populations of Bornean and Sumatran orangutans. In Wich, S.A., Utami Atmoko, S.S., Mitra Setia, T. and van Schaik, C.P. (eds.), Orangutans: Geographic Variation in Behavioral Ecology and Conservation. Oxford University Press, Oxford: 97–116. Marshall, A.J., Nijman, V. and Cheyne, S. (2020). Hylobates albibarbis. In The IUCN Red Book of Threatened Species 2020. e.T39879A17967053. Available at https://dx.doi.org/10.2305/ IUCN.UK.2020-2.RLTS.T39879A17967053.en (accessed 12 December 2022). Mitani, J.C. (1985). Gibbon song duets and interspacing behaviour. Behaviour, 92: 59–96. Nijman, V. and Menken, S.B. (2005). Assessment of census techniques for estimating density and biomass of gibbons (Primates: Hylobatidae). Raffles Bulletin of Zoology, 53: 169–179. Page, S.E., Rieley, J.O., Shotyk, Ø.W. and Weiss, D. (1999). Interdependence of peat and vegetation in a tropical peat swamp forest. Philosophical Transactions of the Royal Society B, 354: 1807–1885. Palombit, R.A. (1993). Lethal territorial aggression in a white-handed gibbon. American Journal of Primatology, 31: 311–318. Raemaekers, J.J. and Raemaekers, P.M. (1985). Field playback of loud calls to gibbons (Hylobates lar): territorial, sex-specific and species-specific responses. Animal Behavior, 33: 481–493. Reichard, U.H. and Sommer, V. (1997). Group encounters in wild gibbons (H. lar): agonism, affiliation and the concept of infanticide. Behaviour, 134: 1135–1174. Reisland, M.A. and Lambert, J.E. (2016). Sympatric apes in sacred forests: shared space and habitat use by humans and endangered javan gibbons (Hylobates moloch). PLoS ONE, 11 (1): e0146891. Savini, T., Boesch, C. and Reichard, U.H. (2008). Home-range characteristics and the influence of seasonality on female reproduction in white-handed gibbons (Hylobates lar) at Khao Yai National Park, Thailand. American Journal of Physical Anthropology, 135: 1–12. Shepherd, P.A., Rieley, J.O. and Page, S.E. (1997). The relationship between forest structure and peat characteristics in the upper catchment of the Sungai Sebangau, Central Kalimantan. In Rieley, J.O. and Page, S.E. (eds.), Biodiversity and Sustainability of Tropical Peatlands. Samara Publishing, Cardigan, UK: 191–210. Singh, M., Cheyne, S.M. and Ehlers Smith, D.A. (2018). How conspecific primates use their habitats: surviving in an anthropogenically-disturbed forest in Central Kalimantan, Indonesia. Ecological Indicators, 87: 167–177. Thompson, C., Cahyaningrum, E., Birot, H., Aziz, A. and Cheyne, S.M. (2022). A case of polygyny in the Bornean white-bearded gibbon (Hylobates albibarbis). Folia Primatologica, 93(1): 97–105. Vogel, E.R., Haag, L., Mitra-Setia, T., van Schaik, C.P. and Dominy, N.J. (2009). Foraging and ranging behavior during a fallback episode: Hylobates albibarbis and Pongo pygmaeus wurmbii compared. American Journal of Physical Anthropology, 140: 716–726. Vogel, E.R., Harrison, M.E., Zulfa, A., et al. (2015). Nutritional differences between two Orangutan habitats: Implications for population density. PLoS One, 10(10): e0138612. Wanelik, K.M., Azis, A. and Cheyne, S.M. (2013). Note-, phase- and song-specific acoustic variables contributing to the individuality of male duet song in the Bornean Southern gibbon (Hylobates albibarbis). Primates, 54: 159–170.

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Demography of a Stable Gibbon Population in High-Elevation Forest on Java Susan Lappan, Rahayu Oktaviani, Ahyun Choi, Soojung Ham, Haneul Jang, Sanha Kim, Yoonjung Yi, Ani Mardiastuti and Jae Chun Choe

5.1

Introduction Conservation of endangered species is fundamentally linked with their demography (Lande, 1988; Lawler, 2011; Strier, 2014). Extinctions occur when population growth rates are negative for a sufficient period that the population declines to zero (Slobodkin, 1961; Lawler, 2011). Local extinctions can occur abruptly in response to external events such as habitat loss (Estrada and Coates-Estrada, 1988; Deacon and Mac Nally, 1998; Benchimol and Peres, 2015), disease outbreaks (McCallum, 2012) or natural disasters (Michaelski and Peres, 2005; Pries et al., 2009; Finkelstein et al., 2010). Frequently, though, extinction follows a gradual population decline due to environmental changes, such as habitat degradation or fragmentation, competition with or predation by invasive species, unsustainable hunting, or a combination of these factors (Sodhi et al., 2004; Michaelski and Peres, 2005; Corlett, 2007; Benchimol and Peres, 2015). Small populations are at particularly high risk of extinction due to environmental stochasticity, demographic stochasticity, inbreeding depression or other small-population effects, even in the absence of additional extrinsic causes of decline (Lande, 1987, 1998). To prevent extinctions, conservation managers must identify populations at risk and initiate effective conservation actions to prevent further population declines and, where possible, to reverse negative growth rates. Monitoring of threatened populations and modelling of extinction probabilities depend on information about demographic variables (Smith et al., 2017). However, for long-lived animals with slow life histories, accurate information about typical lifespans or ages at first reproduction may not be available for wild populations, despite sustained effort on the part of field researchers (Wich et al., 2004). Among mammals, primates have especially slow life histories, particularly in the Hominoidea or apes (Wich et al., 2004; Reichard and Barelli, 2008). The International Union for Conservation of Nature (IUCN) lists 19 of 20 species of small apes or gibbons (Hylobatidae) as endangered or critically endangered (IUCN, 2020). Gibbons, like great apes (Hominidae), have long periods of infant dependency (Lappan, 2009; Yi et al., 2020a) and long inter-birth intervals (IBIs) (Bartlett, 2011). Gibbons also live in small social groups and are strictly arboreal, often travelling in the upper forest canopy (Bartlett, 2011). When encountered, gibbons tend to hide or flee

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from humans (Brockelman and Srikosamatara, 1993; Nijman, 2004; O’Brien et al., 2004; Nijman and Menken, 2005). In addition, many gibbon species primarily persist in hill and montane forests with terrain that is difficult for human observers (Nijman, 2001). As a result, while occurrence or abundance estimates are available for gibbons in many landscapes (Arcus Foundation, 2018), detailed demographic information is not available from wild populations of most gibbon taxa. In this chapter, we describe reproductive and developmental parameters, including IBI and age at dispersal as well as age-specific survivorship for immature individuals, in a population of wild Javan gibbons (Hylobates moloch) at Citalahab in Gunung Halimun-Salak National Park (GHSNP), West Java, which was monitored intensively from 2007 to 2020. Java is the most densely populated large island on earth, with more than 140 million people living on a landmass of 138,794 km2. Over the last millennium, most of the original forest on Java has been converted to agriculture, urbanisation and infrastructure, leaving less than 10 per cent of the island forested (Nijman, 2013; Malone et al., 2014). The remaining forests are badly fragmented and are concentrated in hill and montane areas (Andayani et al., 2001; Nijman, 2004). Hylobates moloch occurs only in West Java and Central Java and persists in at least 30 forest fragments (Malone et al., 2014) but is unlikely to persist in the long term in fragments of less than 50 km2 (Nijman, 2013). More than half of the remaining population is estimated to live in three large fragments: GHSNP, Ujung Kulon National Park and the Dieng Mountains (Smith et al., 2017). GHSNP is the largest remaining habitat (1,133 km2, with 330–400 km2 of suitable habitat) and is thought to support the largest remaining population of H. moloch (900–1220 individuals; Smith et al., 2017). However, GHSNP contains many high peaks and human enclaves, and therefore the gibbon population may be effectively fragmented into smaller subpopulations with higher risk of local extinction (Smith et al., 2017). While our 13-year dataset constitutes only a little over a single gibbon generation, and therefore can only provide a small window into H. moloch demography in one population, this is the longest-running study of known individuals of this taxon, and the first multi-year behavioural study of H. moloch in the high-altitude forests that characterise most of their remaining habitat. By comparing vital rates from this population with information from other long-term studies of gibbons, and especially other species in the genus Hylobates, we aim to provide new insight into the demography of H. moloch in hill and lower montane forests as well as patterns of demographic variation among gibbons.

5.2

Ecological Influences on Gibbon Demography Gibbons are thought to have evolved their specific set of life-history characteristics in the Miocene in forests of low to moderate seasonality with predictable productivity (Jablonski and Chaplin, 2009). Today, gibbons occur in a variety of tropical and subtropical forest habitats (Jiang et al., 2006; Bartlett, 2011), including strongly (Choudhury, 1990; Brockelman et al., 1998; Fan et al., 2009a) and weakly

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(O’Brien et al., 2003; Kim et al., 2011) seasonal forests, in primary (O’Brien et al., 2003; Fan et al., 2009a) and disturbed (O’Brien et al., 2003; Fan et al., 2009a; Lee et al., 2014) forests, peat-swamp forests (Cheyne et al., 2019), karst forests (Fan et al., 2010, 2012), and habitats spanning elevations from near sea level (O’Brien et al., 2003; Lappan et al., 2017) to 2,790 m above sea level (a.s.l.) (Fan et al., 2009a). Gibbon population densities and reproductive parameters vary across habitat types, indicating that despite the persistence of gibbons across a range of environmental conditions, populations in habitats of marginal quality may be vulnerable to ecological stress (Jablonski and Chaplin, 2009). Gibbon survivorship in the infant and early juvenile age classes varies with habitat quality (O’Brien et al., 2003). In high-quality habitats, survivorship in these age classes is generally also high, with substantially lower survivorship in low-quality habitats. For example, in declining populations of agile gibbons (Hylobates agilis; O’Brien and Kinnaird, 2011) and siamangs (Symphalangus syndactylus; O’Brien et al., 2003), mortality in the infant and juvenile age classes was high, with less than 25 per cent of infants surviving to sub-adulthood. Conversely, in stable populations of white-bearded gibbons (Hylobates albibarbis; Cheyne et al., 2019), white-handed gibbons (Hylobates lar; Brockelman et al., 1998; Savini et al., 2008; Reichard et al., 2012) and S. syndactylus (O’Brien et al., 2003), 60 per cent or more of infants survived to sub-adulthood. Survivorship to sub-adulthood was intermediate at approximately 50 per cent for a population of H. albibarbis that was also described as declining (Mitani, 1990). However, a subsequent study at the same site, Cabang Panti in Gunung Palung National Park, Indonesia, revealed complex metapopulation dynamics among H. albibarbis at the site, with montane habitat within the study area acting as a demographic sink (Marshall, 2009). Habitat quality can be affected by many variables, including plant community composition, history of anthropogenic disturbance, rainfall and temperature regimes, and elevation. As ripe fruit specialists, gibbons appear to achieve their highest densities in habitats with high and consistent food availability (Mather, 1992). Studies comparing gibbon densities across different habitat types have identified different ecological predictors of gibbon densities in different landscapes. Gibbon densities in Cabang Panti, Indonesia, are highest in habitats with high fig (Ficus spp.) density (Marshall, 2010), whereas gibbon densities across a set of habitats in Borneo and Peninsular Malaysia increased with increasing densities of a set of important fruit species (Mather, 1992). Other studies have identified food tree biomass (Phoonjampa et al., 2011), high plant family diversity (Marsh and Wilson, 1981) and high species richness of food plants (Muzaffar et al., 2007) as predictors of gibbon biomass. In Peninsular Malaysia, H. lar densities are also positively related to the percentage of dipterocarps (Dipterocarpaceae; Marsh and Wilson, 1981). However, since dipterocarps are not important food plants for gibbons, this association may reflect a relationship between the abundance of dipterocarps and some other aspect of habitat quality (e.g. the importance of dipterocarps as host trees for hemiepiphytic figs) (Harrison et al., 2003). Habitat disturbance also can affect gibbon density and demography, although the relationships appear to be complex and are not well understood. A longitudinal study

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in the Tekam Forest Reserve, Malaysia, showed very high infant mortality in H. lar during selective logging operations but with a rapid return to background rates of infant mortality within 6 months (Johns and Johns, 1995). In Khao Ang Rue Nai Wildlife Sanctuary, Thailand, evergreen forest cover and distance from the forest boundary, both of which were related to disturbance history, were predictors of pileated gibbon (Hylobates pileatus) densities (Phoonjampa et al., 2011). Symphalangus syndactylus densities in heavily fire-damaged habitat were lower than those in unburned and lightly burned forest more than 15 years after fire (Lappan et al., 2020). Hylobates agilis densities tended to be higher in the most intact areas within the severely disturbed Harapan Rainforest landscape in Indonesia (Lee et al., 2014), but density of the same species was not related to disturbance history in Ulu Muda Forest Reserve, Malaysia (Pang, 2020). Elevation appears to be a particularly important factor affecting gibbon demography. Gibbons in higher-elevation forests, particularly those that are also at higher latitudes, experience nutritional stress as well as cold stress (Fan et al., 2009a), resulting in delayed maturation, longer IBI and lower population densities (Jablonski and Chaplin, 2009). While S. syndactylus, skywalker hoolock gibbons (Hoolock tianxing) and some crested gibbons (Nomascus spp.) occur in forests at or above 2,000 m a.s.l. (Jiang et al., 2006; Fan et al., 2009a, 2009b, 2013; Yanuar, 2009), densities for gibbons in the genus Hylobates generally appear to decline with elevation above 500 m (O’Brien et al., 2004; Marshall, 2009; Nongkaew et al., 2018) and are generally quite low at elevations of more than 800 m a.s.l. (Table 5.1). In the only previous study examining the relationship between elevation and reproductive success or survivorship in any gibbon, Marshall (2009) found that in forests above 750 m a.s.l., H. albibarbis either failed to reproduce or their infants did not survive. However, the effects of altitude likely depend in part on the floristic characteristics of a gibbon habitat, and in evergreen forests with a moderate or high concentration of fruit trees, gibbons may be able to maintain a high-quality diet at higher elevations. For example, densities of H. agilis in Bukit Barisan Selatan National Park, Indonesia peak at around 800 m a.s.l. (O’Brien et al., 2004) and densities in Kerinci-Seblat National Park, Indonesia, are highest between 450 and 1100 m a.s.l. (Yanuar, 2009). Ecological variation may also affect the adult composition of gibbon groups. The most common grouping pattern reported for gibbons is pair-bonded social monogamy (Bartlett, 2011). However, groups containing three or more adults have occasionally been reported in all four gibbon genera (Fuentes, 2000; Malone and Fuentes, 2009), and in some habitats multi-female (Bleisch and Chen, 1991; Zhou et al., 2008; Fan et al., 2010; Huang et al., 2013; Barca et al., 2016; Hu et al., 2018) or multi-male (Brockelman et al., 1998; Lappan, 2007; Reichard et al., 2012) grouping occurs at moderate or high rates. Multi-female grouping is common or universal in black crested gibbons (Nomascus concolor), Hainan gibbons (Nomascus hainanus) and Cao-vit gibbons (Nomascus nasutus) in high-latitude habitats (Fan et al., 2006, 2015; Zhou et al., 2008). This pattern may result from gibbon behavioural responses to low overall productivity, seasonally low fruit

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https://doi.org/10.1017/9781108785402.007 Published online by Cambridge University Press

Table 5.1 Hylobates densities in forests above 800 m a.s.l.

Species

Site

H. agilis

Bukit Barisan Selatan National Park (multiple sites) Kerinci-Seblat National Park, Indonesia Kerinci-Seblat National Park, Indonesia H. albibarbis Cabang Panti, Indonesia H. lar Gunung Benom, Malaysia Gunung Benom, Malaysia Gunung Benom, Malaysia H. moloch Gunung Gede-Pangrango National Park, Indonesia Gunung Gede-Pangrango National Park, Indonesia Gunung Simpang Nature Reserve, Indonesia Gunung Papandayan Protection Forest, Indonesia Gunung Slamet Protection Forest, Indonesia Citalahab Research Area, Indonesia * Calculated from biomass estimates.

Elevation (m a.s.l.)

Density (individuals/km2)

Reference

800–1,300 900–1,100 >1,500 850–1000 915–1,068 1,068–1,296 1,296–1,525 1,551–1,784 764–819 1,075–1,384 1,056–1,194 650–900 950–1,100

6.7 10.8 0 0.05). This is not surprising, as rainfall and temperature regimes at Citalahab are quite stable throughout the year. Availability of preferred foods does vary between months, but the patterns of variation

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https://doi.org/10.1017/9781108785402.007 Published online by Cambridge University Press

Table 5.2 Group sizes in wild Hylobates groups.

Species

Site

H. agilis H. albibarbis

Way Canguk, BBSNP Cabang Panti, GPNP

H. klossii

H. lar

H. moloch

H. pileatus

Elevation (m a.s.l.)

Natural Laboratory of Peat-swamp Forest, SNP

50 0–1,100 0–800 750–1,100 10

Peleonan Forest, Siberut

0–180

Saiba Ulu, Siberut