Ecology and conservation of the southern woolly lemur (Avahi meridionalis) in the Tsitongambarika Protected Area, south-eastern Madagascar By Michela Balestri Oxford Brookes University Thesis submitted in partial fulfilment of the requirements of the award of Doctor of Philosophy May 2018 i Abstract Recent studies question the assumption that folivorous primates rely on ubiquitous and evenly distributed food resources with a low and uniform nutritional quality. They suggest that folivores experience scramble competition and their resources vary in quality, availability, and spatial distribution. Woolly lemurs, Avahi sp., are the only true nocturnal folivorous primates. This study aims to explore whether A. meridionalis experiences food constraints in the Tsitongambarika lowland rainforest of south-east Madagascar, a habitat that is expected to have low variation in quality, availability, and spatial distribution of leaves. I collected data from May 2015 to July 2016 at Ampasy, north of the Tsitongambarika Protected Area, on abundance of lemur species, and ranging pattern, sleeping site selection, diet, and activity pattern of A. meridionalis. I delivered four lessons to teachers in the municipality that hosts Ampasy to raise awareness on the threats that lemurs and forests are facing, and assessed the effective retention of knowledge after one year. The density of the nocturnal folivore Lepilemur fleuretae was very high, suggesting a possible scramble competition with A. meridionalis. Avahi meridionalis adopted a resource-maximising strategy in terms of annual ranges, suggesting a high-quality habitat, and a time-minimising strategy in terms of daily distances travelled, sleeping site selection, and dietary choices, suggesting a seasonal fluctuation of resources. The competition with L. fleuretae may explain the dietary breadth reduction during the lean season and the opportunistic cathemeral activity that I found in A. meridionalis. Teachers retained most of the information provided, which can thus be transferred to students. This is the first step to favour a change in attitude by the local community in the area. My results on A. meridionalis showed several lines of evidence to support the hypothesis that folivores experience similar food constraints to frugivores. ii Acknowledgements I am very thankful to my advisor, Dr. Giuseppe Donati, for his guidance, support, and motivation throughout this project. Thanks for making my PhD experience productive and stimulating, you have been a tremendous mentor for me. I am grateful to my advisor, Prof. Anna Nekaris, for her insightful comments and advice that incentivised me to improve my research from various perspectives. Thanks also for giving me the opportunity to be your teaching assistant, it has been a great and formative experience for me. I wish to express gratitude to Prof. Simon Bearder, Dr. Susan Cheyne, Prof. Kate Hill, Prof. Jeremy McClancy, and Prof. Vincent Nijman, for the help and the opportunities given, your knowledge and dedication are an immense source of inspiration. I thank my external examiner Prof Joerg Ganzhorn and internal examiner Prof Vincent Nijman for feedback and suggestions to improve the dissertation. My sincere gratitude goes to the foundations for providing the funding to carry on this study: Rufford Foundation, the Mohamed bin Zayed Species Conservation Fund, Primate Conservation Inc., the Conservation International Primate Action Fund, and the Primate Society of Great Britain Conservation Grant. I would like to express the deepest appreciation to QIT Madagascar Minerals Rio Tinto, specifically the QMM Environmental Team, for the support and the logistical help in Fort Dauphin and at the research station. Special thanks to Laza Andriamandimbiarisoa, Johny Rabenantoandro, Jean-Baptiste Ramanamanjato, and Cedric Tsagnangara. I am thankful to all the members of Asity Madagascar in Fort Dauphin, with special thanks to Faniry Rakotoarimanana, without your guidance and persistent help in the field this research would not have been possible. I am grateful to the teachers iii of the municipalities of Iaboakoho, Mahatalaky, Mandromodromotra, and Ampasy- Nahampoana for giving their time to realise a valuable part of this study. But my deepest heartfelt appreciation goes to every single employee at the research station, to all the collaborators, and to all the villagers in the municipality of Iaboakoho. Laviky, Bergè, Ronaly, Rabiky, Marianah, Nita, Roger, thanks for making me feel at home, literally. I want to thank Dr. Jacques Rakotondranary and Tolona Andrianasolo for their logistical help and support in Antananarivo, especially for coordinating my research permits/renewals and export permits with the Direction du Système des Aires Protégées, and the Ministère de l’Environnement et Forêts of Madagascar. I am also grateful to Madame Chantal Andrianarivo (Responsable des Recherches au Madagascar National Parks) and Prof. Hanta Razafindraibe (Responsable du Département Biologie Animale de l’Université d’Antananarivo) for approving my research. I would also like to express my gratitude to Irene Tomaschewski for carrying out biochemical analyses on the food items. I wish to thank the volunteers and the Oxford Brookes Primate Conservation MSc students who spent their time in the field. Thanks to the volunteers Julie Mauguiére, George Selley, and Carina Morris for their help with collecting the data and for the nice time we had together. But I owe my deepest gratitude the MSc students Megan Phelps and Fiona Besnard, you made an enormous contribution to this study and I am truly happy I shared this significant experience with you, we are a great team. Thanks to Toky, Natalie, and Fidél, it was nice to know that you were always there to spend time together during my resting days in Fort-Dauphin. I am grateful to Dr. Sergio Tofanelli and Dr. Tim Eppley for helping me especially during the early stages of my study, their encouragement and suggestions were invaluable. iv I owe a very important debt to my closer friends in Italy and the MSc and PhD students I met in Oxford during this journey, you should know that your support and encouragement was worth more than I can express on paper. Special thanks to Jesus Martinéz, Sabrina Reinders, Rachel Sawyer, Aimee Oxley, Hellen Bersacola, Dr. Magdalena Svensson, Katie Reinhardt, Dr. Stephanie Poindexter, and Daniel Bergin. Words cannot express how grateful I am to my parents and to my sister Monica for their unconditional love and for supporting me emotionally and financially. I dedicate this thesis to you all, thanks for the countless sacrifices and for providing me the opportunity to be where I am today. Finally, last but by no means least, thanks to Marco for sharing this significant time of our lives together and for pushing me towards my goals. v Table of contents Abstract ....................................................................................................................... ii Acknowledgements .................................................................................................... iii Table of contents ........................................................................................................ vi List of figures .............................................................................................................. x List of tables ............................................................................................................... xi List of abbreviations .................................................................................................. xii 1. General introduction....................................................................................................... 1 1.1. The folivore paradox ........................................................................................ 1 1.2. The woolly lemurs (Avahi spp.) ........................................................................ 4 1.3. Aims of the study.............................................................................................. 7 2. General methods .......................................................................................................... 11 2.1. Study site ....................................................................................................... 11 2.2. Context ........................................................................................................... 13 2.3. Study animals ................................................................................................ 17 2.4. Phenology of young leaves ............................................................................ 18 2.5. Behavioural data collection ............................................................................ 19 2.6. Ethics statement............................................................................................. 19 3. Lemur abundance in the lowland rainforest of Tsitongambarika and altitudinal comparison of encounter rates within Malagasy rainforests ........................................ 21 3.1. Introduction .................................................................................................... 21 3.2. Methods ......................................................................................................... 24 3.2.1. Study site and species ............................................................................. 24 3.2.2. Data collection ........................................................................................