Ecological flexibility and conservation of Fleurette’s sportive lemur, Lepilemur fleuretae, in the lowland rainforest of Ampasy, Tsitongambarika Protected Area By Marco Campera Oxford Brookes University Thesis submitted in partial fulfilment of the requirements of the award of Doctor of Philosophy May 2018 i Abstract Ecological flexibility entails an expansion of niche breadth in response to different environmental conditions. Sportive lemurs Lepilemur spp. are known to minimise energetic costs via short distances travelled, small home ranges, increased resting time, and low metabolic rates. Very little information, however, is available in the eastern rainforest, the habitat where this genus has its highest diversity. I investigate whether L. fleuretae inhabiting Tsitongambarika (TGK), the southernmost lowland rainforest in Madagascar, shows similar behavioural and ecological adaptations to the sportive lemurs inhabiting dry and deciduous forests. I collected data from July 2015 to July 2016 at Ampasy, northernmost portion of TGK. To understand patterns of resource availability, I collected phenological data on 200 tree species. I explored the ecology of L. fleuretae by gathering data on its diet, ranging patterns, and by reconstructing the activity profiles via a novel method, the unsupervised learning algorithm on accelerometer data. I estimated the anthropogenic pressure in the area and I evaluated whether local management and researchers’ presence had an effect in decreasing it. Lepilemur fleuretae at Ampasy is hyperactive when compared to other species of this genus, with longer distances travelled, larger home ranges, and less time spent resting. The species seems to reduce the competition with the folivorous A. meridionalis by including a higher proportion of fruits and flowers in their diet than other sportive lemurs. The activity of L. fleuretae is influenced by photoperiod and moon luminosity, indicating the importance of synchronizing activities with the seasonal resource availability. A combination of local management and related development strategies, such as the installation of a research station, can assist in preserving the TGK forest. My results on L. fleuretae unveiled the flexibility of the genus Lepilemur and its ability to adapt to different habitats. This study showed that the use of automatic loggers such as accelerometers can provide novel information on cryptic species difficul to achieve via direct observations. The use of these devices may shed the light on new behavioural and ecological patterns and lead to a new approach on the study of cryptic animals. ii Acknowledgements First and foremost, I wish to thank my advisor, Dr. Giuseppe Donati, for the continual support and encouragement during the whole period. Your guidance was of immense value for me to develop myself as a researcher, and I am deeply grateful for all your efforts and for pushing me towards my goals. The opportunities given and advices on both research and my career have been invaluable. I want to sincerely thank my second advisor, Prof. Vincent Nijman, for sharing his expertise and for supporting me, and Prof. Anna Nekaris, Prof. Simon Bearder, Prof. Kate Hill, Dr. Susan Cheyne, and Prof. Jeremy MacClancy for the opportunities given, their assistance during my PhD, and for being a continual source of inspiration. I thank my external examiner Dr. Christoph Schwitzer and internal examiner Prof. Anna Nekaris for feedback and suggestions to improve the dissertation. I thank the foundation that supported 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 also thank QIT Madagascar Minerals Rio Tinto, specifically the QMM Environmental Team, for the support with the logistics in Fort Dauphin and at the research station. My sincere gratitude goes to Johny Rabenantoandro, Jean-Baptiste Ramanamanjato, Laza Andriamandimbiarisoa, and Cedric Tsagnangara. This research would not have been feasible without the support of the members of Asity Madagascar in Fort Dauphin, with special thanks to Faniry Rakotoarimanana. Thanks for all the help provided from the first stage to the very end of the research. But all my gratitude goes to every single employee at the iii research station, to all the collaborators, and to all the villagers in the municipality of Iaboakoho. Bergé, Laviky, Ronaly, Rabiky, Marianah, Nita, Roger, you all are like a family to me and I am grateful to all of you. It was special to live with you all for 15 months. Many thanks for the other people who shared this experience with me, although for a short period (maybe two-three months is not so short…). The volunteers Julie Mauguiére, George Selley, and Carina Morris were of great help both for the data collection and for creating a friendly environment at the research station. I would particularly like to thank the MSc students Megan Phelps and Fiona Besnard; your help was huge and it has been a pleasure spending time with you in the field (especially while stuck at the camp because of the heavy rain!). Special thanks also to the people who contributed to create a friendly environment in Fort Dauphin and to have some fun in town, Toky, Natalie, and Fidél, thanks a lot! I wish to thank Dr. Jacques Rakotondranary and Tolona Andrianasolo for their logistical 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 also thank 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. Special thanks to all my friends in Italy and in Oxford who clearly contributed in the writing up of this dissertation by cheering me up when needed. I am grateful to the other PhD students (and PhD students now doctors!) and master students I met and shared pleasant time with. In particular Jesus Martinéz, Sabrina Reinders, Rachel Sawyer, Hellen Bersacola, Dr. Magdalena Svensson, Aimee Oxley, iv Dr. Stephanie Poindexter, Katie Rainhardt, and Daniel Bergin, you were there at the beginning and you are still there for me. I am also grateful that during this experience I met great people and collaborators such as Tim Eppley who contributed with data and feedback on chapter 7, published on Oryx Journal with him as co-author, and Marianna Chimienti who helped with the data analysis on accelerometers. Many thanks to my family and to Michela’s family for the support and encouragement. They allowed me to follow my dreams. There are not enough words to say thanks to Michela for always being there. v To the person who is always in my mind and who gives me strength even though she is not here anymore vi Table of contents Abstract ........................................................................................................................ ii Acknowledgements ..................................................................................................... iii Table of contents ........................................................................................................ vii List of figures ............................................................................................................. xii List of tables .............................................................................................................. xiv List of abbreviations ................................................................................................... xv 1. General introduction ......................................................................................................... 1 1.1. Ecological flexibility in primates ...................................................................... 1 1.2. Energy saving strategies in primates ................................................................. 3 1.3. The sportive lemurs (Lepilemur spp.) ............................................................... 5 1.4. Aims of the study ............................................................................................. 11 2. General methods.............................................................................................................. 15 2.1. Study site ......................................................................................................... 15 2.2. Context ............................................................................................................ 17 2.3. Abiotic variables in the study area .................................................................. 21 2.2. Study animals .................................................................................................. 22 2.3. Ethics statement ............................................................................................... 26 3. Phenology of the lowland rainforest of Tsitongambarika: prolonged periods of fruit scarcity may explain low diversity of frugivorous lemurs .................................... 28 3.1. Introduction ..................................................................................................... 32 3.2. Methods ........................................................................................................... 32 3.2.1. Phenological data collection ....................................................................