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Developing a conservation evidence-base for the Critically Endangered Hainan gibbon ( Nomascus hainanus ) Jessica V. Bryant Division of Biosciences, University College London (UCL) Institute of Zoology, Zoological Society of London A thesis submitted for the degree of Doctor of Philosophy, University College London April 2014 1 Declaration I, Jessica Victoria Bryant, confirm that the work presented in this thesis is my own. Where information has been derived from other sources, I confirm that this has been indicated and appropriately referenced within the thesis. © The copyright of this thesis rests with the author. No quotation or information derived from it may be published without the prior written consent of the author and any such use should be explicitly acknowledged. 2 Abstract The Critically Endangered Hainan gibbon ( Nomascus hainanus ) is the world’s rarest ape, with a single population of an estimated 25 individuals surviving in approximately 15 km 2 of suboptimal forest within Bawangling National Nature Reserve, Hainan, China. The existing biological evidence-base for the species is inadequate for conservation planning, precluding evaluation of appropriate recovery actions. I derived comprehensive new baseline data on Hainan gibbon ecology, behaviour and genetics to clarify the species’ biology and population status, and inform urgently required conservation management for the species. Rigorous re- evaluation of Hainan gibbon spatial requirements indicated the species’ home range is much smaller than previously estimated (c. 1.5 km 2) and in line with closely related Nomascus species in similar ecological conditions. Molecular assessment of the genetic status of the surviving population within the context of the species’ historical genetic diversity revealed that the Hainan gibbon has suffered a significant decline in genetic diversity following its past population bottleneck. The current population also shows a high level of relatedness and male-biased offspring sex ratio. Predictive models examining reportedly ‘anomalous’ Hainan gibbon ecological and behavioural traits within a phylogenetic framework indicated that large, polygynous groups may be evolutionarily characteristic for the species, but home range requirements are influenced by both intrinsic factors and current extrinsic conditions. Finally, Population Viability Analysis demonstrated that the species is highly likely to become extinct in the near future without active management, and that multiple actions mitigating extrinsic threats, enhancing habitat carrying capacity and improving survivorship will be required to reduce extinction risk. Together, these findings suggest that landscape-level management actions and intensive manipulation of the population may be necessary to safeguard the future of the Hainan gibbon. This research also has wider implications for improved understanding of gibbon ecology and conservation of species of extreme rarity. 3 Chinese Summary 构建极度濒危物种海南长臂猿 (Nomascus hainanus) 的保护学依据 杰西卡 布莱恩特 英国伦敦大学学院, 生命科学系 伦敦动物学会，动物研究所 提交英国伦敦大学学院的博士学位论文 2014 年 4 月 摘要 极度濒危的海南长臂猿 (Nomascus hainanus ) 是全球最为珍稀的类人猿，它们仅存一个由 25 个个体组成的种群，栖息在中国海南岛霸王岭国家级自然保护区内约 15 km 2 的次优林 中。由于现有的关于该物种的生物学研究不足，理论依据的匮乏进一步限制了制定及评 估其适宜的种群恢复行动。本研究为海南长臂猿的保护构建了一个综合的、全新的基础 数据库，包括反映其生物学及种群现状的生态学、行为学和遗传学方面的数据，同时提 出了该物种亟需的保护管理要求。本研究对海南长臂猿的空间需求进行了一次严谨的二 次评估，结果显示该物种的活动范围比之前估计的 (1.5 km 2) 要小得多，与在相同生态条 件下的、与其十分相近的黑冠长臂猿属一致。另外，针对现存种群进行的种群遗传学分 子评估发现，受到过去种群数量的瓶颈限制，海南长臂猿的遗传多样性与其历史相比经 历了严重的下降。现有的群体表现出了高度的亲缘性及后代的雄性性别偏向性。预测模 型在系统发生学的框架下进一步分析了海南长臂猿的“反常”生态及行为特征，揭示了大 的、一夫多妻的种群可能是该物种的进化特点，而其对活动范围的需求则同时受到内在 因素和当前外在条件的影响。最后，种群生存力分析演示了该物种可能面临的灭绝风险 ，若不采取积极的、多元化的保护管理以缓解外界威胁、提高栖息地承载力及增加存活 率，该物种很可能在不远的将来面临灭绝。总而言之，本研究的发现认为采取景观层面 的宏观管理行动及实施强力的种群保护操作是保证海南长臂猿长远生存的必要手段。同 时，本研究促进了对长臂猿生态学及针对极度稀少物种保护方面的了解，具有更为广泛 的影响及参考意义。 4 Acknowledgements When first contemplating this project I knew I was in for a challenge, that was the lure, but I had little idea it would take me on quite such an epic journey both professionally and personally. I am sincerely grateful to my supervisors, Sam Turvey, Helen Chatterjee, John Fellowes and Guy Cowlishaw, for giving me the opportunity to embark upon this adventure, and for the continual support and guidance throughout. Applied postgraduate research projects at the very coalface of conversation don’t come along very often, and I count myself as extremely fortunate to have been permitted to study and hopefully actively contribute to the conservation of this remarkable animal. A very special thanks to Sam, whose eternal optimism and absolute determination to conserve our world’s biodiversity, often in the face of a seemingly endless barrage of obstacles, can only inspire. Xiè xiè l ǎo sh ī! Wǒ f ēi cháng g ǎn xiè for the endless enthusiasm, constant encouragement, and just for the experience, most especially the eggs in beer! And to Helen for keeping me grounded, focused on the output, and mindful of the learning experience. I am grateful to all of my funding sources for believing in this project. Funding for this study was provided by University College London, Institute of Zoology (Zoological Society of London), and Ocean Park Conservation Foundation Hong Kong, with additional backing from the Mohamed bin Zayed Species Conservation Fund. I would like to say a special thanks to Harold and Olga Fox for financial support awarded via the Harold and Olga Fox Prize in Biology, and to ZSL for funds awarded from the Daisy Balogh Memorial Travel Fund. This study was made possible through collaboration with the Bawangling National Nature Reserve Management Office, Hainan Bawangling Forestry Bureau, Hainan Provincial Forestry Department, Hainan Provincial Taxation Bureau, and Kadoorie Farm and Botanic Garden (KFGB) Hong Kong. My earnest thanks to all parties for your approval and support to carry out this research, without which this thesis would not have been possible. Particular thanks to Directors Zeng Xinyuan, Wang Chundon, Zheng Linmin; Vice Directors Huang Jincheng, Hong Xiaojiang and Wang Yongcun; Deputy Chief Yang Min, and Director’s Assistant Yang Shibin. I’m also extremely grateful to Bosco Chan, Jay Wan and Michael Lau, for the initial introductions and logistical support, and for championing my project (and me!) to a multitude of people in Hainan, from provincial authorities to Bawangling locals. Wǒ h ěn g ǎn xiè to the Bawangling Hainan Gibbon Monitoring Team: Li, Bio, Tao, Chong, Wei, Hai, Mao, Chang, and Neng. I’m sure you all thought I was insane with my constant requests to stay in the forest and stay with the gibbons, but I am enormously appreciative and indebted to you for your xīn k ǔ (hard work), without which I would have had few data! 5 I have several people I would like to thank for assistance with specific components of my thesis. Huge thanks to Dada Gottelli and Chris Durrant for technical guidance with genetic laboratory work and relevant analyses. To the National Museum of Ireland (Dublin), Natural History Museum (London), Museum für Naturkunde (Berlin), South China Institute of Endangered Animals (Guangzhou), and Thomas Geissmann for providing key historical samples. Selina Brace and Ian Barnes for guidance regarding DNA extraction from museum specimens. Thanks also to Dr Bob Murphy for the introduction to your (and now my) collaborators at Kunming Institute of Zoology and Yunnan University, Kunming, and to those collaborators, Professor Zhang Yaping and Dr Jing Luo for permitting my lab visit, and Ms Jing Chai for assistance during that vital lab work. I would also like to thank Rob Freckleton, Valerie Olson and Sarah Whitmee for your statistical insights, which helped me navigate my way through my comparative analysis. And to all those gibbon researchers who very generously provided data for that analysis, it made the analysis substantially more representative and robust. Particular thanks to Ben Rawson and Susan Cheyne for numerous stimulating discussions and allowing me to mine the depths of your individual gibbonological knowledge-banks. Access to the information locked inside key Chinese-text references was made possible through the help of a number of people. I am grateful to Ms Ping Chen, Ms Hu Xiaoyan, Ms Kenisha Yeung and Tim Jeffree for assistance with text translation. I would also like to say xiè xiè to all in Bawangling township and nearby villages, and m̀ hgòi to Billy Hau, Teressa Ma and all at KFBG (Ruthie, Hill, Carrie, Hong Yun, “Mao Ma Mi”), for making me feel so welcome and being so accommodating and kind during my time in Hainan, and Hong Kong, respectively. Back in the UK, my home away from home, I have been kept (mostly!) sane through the love and support of my friends and London-family. Thanks for the tea and sympathy Amelia, Frankie, Jen, Zoe, Melly, Nads, Shane, Siobhan, Elsa, Martina, Emma, Johanna, and Braddles. I am also grateful to everyone at the IoZ for being always approachable and ever happy to help. Finally, a massive thank you to my wonderful family whose support is boundless and borderless. Mum and Dad, your encouragement and belief in me have allowed me to pursue something I am deeply passionate about, and your interest and enthusiasm (even when you have no idea what I am talking about!) are greatly appreciated. Thank you Daniel, for your design help, and for always being just the other end of a web camera for a much-needed chat. And of course, to Justin, for your unconditional patience, reassurance, and love. 6 Table of Contents Declaration _________________________________________________________________ 2 Abstract
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