Predicting Biodiversity Loss in Insular Neotropical Forest Habitat Patches
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PREDICTING BIODIVERSITY LOSS IN INSULAR NEOTROPICAL FOREST HABITAT PATCHES Photo: Nina Attias Maíra Benchimol de Souza Thesis submitted for the degree of Doctor of Philosophy School of Environmental Sciences University of East Anglia - UK August 2014 © This copy of the thesis has been supplied on condition that anyone who consults it is understood to recognise that its copyright rests with the author and that use of any information derived there from must be in accordance with current UK Copyright Law. In addition, any quotation or extract must include full attribution. CONTENTS Abstract iii Acknowledgments iv Chapter 1: Introduction 1 Chapter 2: Anthropogenic modulators of species–area relationships in Neotropical primates: a 30 continental-scale analysis of fragmented forest landscapes Chapter 3: Predicting primate local extinctions within “real‐world” forest fragments: a 62 pan‐Neotropical analysis Chapter 4: Edge-mediated forest disturbance drives tree assemblage composition and functional 97 diversity in Amazonian islands after 26 years of isolation Chapter 5: Predicting local extinctions of forest vertebrates in Amazonian land-bridge 133 islands Chapter 6: Widespread forest vertebrate extinctions induced by a mega hydroelectric dam in 170 lowland Amazonia Chapter 7: Conclusions & Future Directions 196 Appendices: 208 ii ABSTRACT Neotropical forests have experienced high rates of biodiversity loss as a result of burgeoning land-use changes. Habitat conversion into cropland, pastures, and more recently hydroelectric lakes, are leading drivers of forest loss and fragmentation of pristine forests in the world’s most biodiverse region. This thesis aims to improve our understanding of the impacts of habitat fragmentation on biodiversity loss in Neotropical forests by evaluating the patterns of floristic changes and vertebrate extinctions in forest patches. Two approaches at different scales were conducted. First, a systematic literature review was carried out on the effects of fragmentation on Neotropical primates at a continental-scale. Second, biodiversity inventories were conducted on medium and large-bodied vertebrates (including mammals, birds and tortoises) and trees ≥10 cm diameter at breast height at 37 islands and three continuous forest sites within the Balbina Hydroelectric Reservoir in Brazilian Amazonia. Patch area was a key driver of species persistence for all study taxa, yet other factors were also important. Hunting pressure exerted a strong influence on patterns of primate persistence within 760 fragments, and edge effects, including edge-related ground-fires, were the main predictors of floristic transitions using data from 87 quarter-hectare forest-plots at Balbina. Additionally, matrix composition and species life-history traits played a key role in explaining patterns of species persistence. This study therefore highlights the importance of considering anthropogenic stressors in assessing the effects of land-use change to explain patterns of species persistence in forest patches, aside from including parameters related to the matrix and ecological life-history traits of focal species. As conservation recommendations, prioritising large (>100 ha) patches, increasing their protection, and enhancing connectivity of surrounding habitats becomes clearly important. For future Amazonian dams, it is recommended that engineers should consider the overall topography of planned reservoirs to maximise landscape connectivity and/or reject plans targeting unfavourable river basins. iii ACKNOWLEDGEMENTS As the popular Madagascan saying goes, a tree does not make a forest. Likewise, a person does not make a thesis. This thesis is the result of a lot of hard work done by several people to whom I will be forevermore grateful. First of all, I would like to thank my supervisor, Carlos Peres, for everything he has done big or small. For trusting in the concept of this project from the beginning, for accepting the challenge of starting it without any funding, for supporting me in those difficult moments, and for becoming not just a great supervisor, but a loyal friend. Without funding, this project could not have happened. I thank the Ministry of Education of Brazil, CAPES, for granting me an overseas PhD studentship that has enabled me to study in the UK (Capes 080410/0). I also thank the University of East Anglia for providing me with a great work environment during my stay in the cosy 01.09A office. The fieldwork could not have happened without the support of many agencies that trusted us to carry out this work: the Wildlife Conservation Society Research Fellowship Program, the Rufford Small Grant Foundation, the Conservation Food and Health Foundation, Idea Wild and the Uatumã Biological Reserve. Many thanks! I am very grateful to all those people who helped me with my field surveys. My “right hand”, Evanir Damasceno, and my “left hand”, Evandro Damasceno: thanks for accepting the challenge of leaving your family behind in the Purus river and coming to the Uatumã for such a long time! I am sure that the quality of this work would not have been achieved without your dedication. I also give huge thanks to Joelson de Souza and Rosinaldo Nascimento, for helping me with the cutting of many transects and the deployment and care of loads of camera traps. You four were my family in Balbina, and I will be always grateful for your assistance. I am grateful to my dearest field trainees, Nina Attias, Marcio Schaffer and Aline Tavares, for their support and commitment to the data collection. It was a great pleasure to have your company in the forest and iv all the amusing moments will always be in my memory. I am greatly indebted to Alex dos Santos, for all his meticulous tree identification work and for having shared some of his knowledge with me. I had many funny moments in all those endless forest plots with you, Tucumã and Joniel Vilar. I could also count on many others, whose willingness helped me during different stages of data collection: André, Sr. Chagas, Claudiane, Cleomar, Danielle, Davi, Filipa, Francival, Lívia, Natali, Oliver and Zé, thank you all a lot for your help! A special thank you to every single person from the Uatumã Biological Reserve. From Caio Pamplona and Bruno Cascardo, who were the first to welcome me to work in the Reserve, to Branca Tressoldi, César Chirosa and Gilmar Klein, thanks for providing all the substantial logistical and financial support. To my ‘angel’, Rayanne, thanks for taking care of my comings and goings to the lake all the time. To Fernando, thanks for your help with the camera data. To Sr. Chagas, thanks for every one of your numerous assistances. The security crew, Sr. Antônio, Sr. João e Rodrigo, thanks for all the coffees, chats and help with the logistics. To all the people from the surveillance team, Juliano and his colleagues, thanks for receiving my field team and I so well at the Waba field station, and many thanks for your help in the lake and with the engine issues. I appreciate the kindness of many people from the Balbina village, who received me with so much affection. Each fisherman who opened your home, made me a coffee and welcomed me in to perform interviews, thanks so much. People from the petrol station, the market, the restaurant, the hospital, Mirandinha, thanks for always receiving me with a large grin. My special thanks to Estéfani Fujita, who became a great friend, and Fatima Lopez, who was much more than a great doctor. Loreno, thanks for allowing my team and I to use your accommodation as a field base. I would also like to acknowledge the company of other researchers, mainly the guys from the Giant Otter, Tucunaré and Bee projects (Cacau, Filipa, Bruno, Andrews, César, Dani, Rafa, Guilherme and their field teams) for all great moments we had together in the field camps and the beautiful friendship we constructed at this time. In Manaus, my big thank v you to Sinomar Fonseca Jr, Camila Freitas, Fernanda Meirelles, Eduardo vön Muhlen and Heloisa Brum, for always being so kind-heartedness to me. I am very thankful to Dr. Marcus Rowcliffe and Dr. Aldina Franco for their careful review of this thesis and for many valuable comments during the viva examination. I would also like to thank all reviewers who provided good comments in the manuscripts included in this thesis, and all field primatologists who contributed to the primate dataset by providing further details on their study landscapes throughout the Neotropics. Life in the UK would have not been so good without the company of great friends. Alessia, thanks for being a marvellous friend, my sweetie housemate. Maria, I have no words to express my gratefulness for your incredible friendship, always giving me your support. Vanessa, ‘honey’, I am so grateful for all your company and friendship; you were a real sister in which I could always count on. Dani, thanks for the wonderful professional partnership, giving me a big hand during my field work and helping me with the landscape metrics, and also for all your affection to me: you are super! Dear Elena, thanks for all your good company, support and this incredible joy that is intrinsic of you! I also thank so much all friends from Carlos’ lab (Sue, Pete, Joe, Vanessa, Mark, Dani, Filipa, Carol, Helena, Óleo, João Victor, Edgar, Rodrigo and Fernanda), office colleagues and neighbours (Martin, Kabelo, Assif, Maxim, Nathalie, Karen, Phil, Ricardo and Elly), and CEEC colleagues for all great moments and good advices on the project. A big thanks to Oleo and the CENAP folks for helping me with Leopardus photographs identification. Mi, Alina, Maribel, Ana, Chris, Carine, Gabriel, Rafa, Marcelo, Juliana, Marcus, Fernanda, Camila, Vikki and Jamille, thanks for the amazing moments we spent together in the fine city of Norwich. I would like to specially thank Eduardo Venticinque (Dadão), for encouraging me to do this project, for accepting to be my tutor and for being a special friend I had the good fortune to meet.