Bats in a fragmented world Tiago Souto Martins Teixeira School of Biological and Chemical Sciences Queen Mary University of London Mile End Road, E1 4NS Submitted in partial fulfilment of the requirements of the Degree of Doctor of Philosophy. Abstract Habitat loss and fragmentation are global threats to biodiversity, however, their impact on ecological function are not well understood. The Atlantic Forest hosts high levels of biodiversity and has experienced a long history of deforestation and fragmentation. To examine the consequences of fragmentation for functional and phylogenetic diversity, and for key ecological interactions, I studied bat metacommunity across this landscape. I conducted repeated surveys of bats in forest fragments and continuous forest sites at the Reserva Ecológica de Guapiaçú. To characterize metacommunity structure and the drivers of species assembly, I combined an “elements of metacommunity structure” analysis with assessments of phylogenetic and functional diversity. I then applied a community occupancy model to evaluate the species- specific responses to habitat fragmentation and test whether landscape configuration or habitat structure predicted species occurrence. Finally, by using DNA barcoding to identify plant species recovered in the guano of bats, I reconstructed mutualistic bat- plant networks and determined how network architecture changed with fragmentation. My results revealed that while the bat metacommunity had a random structure, the meta-ensembles of phyllostomid and animalivorous bats showed nested and quasi- nested metacommunity structures, respectively. Species assembly was driven by stochastic processes in fragments, and by environmental filters in the continuous forest. Species occurrence showed a positive relationship with area, but the community occupancy models were not precise enough to differentiate responses to isolation and habitat structure. The structure of bat-plant networks was maintained in 2 small fragments due to the persistence of generalists that perform seed dispersal. Although fragmentation of the Atlantic Forest has severe impacts on bat communities, this biome harbours a rich bat fauna at the metacommunity level. Small fragments may not support diverse bat faunas, but those surviving species still act as agents of seed dispersal and can contribute to forest regeneration and restoration. 3 Acknowledgements The PhD may look like a long solitary journey in front of the computer, but the truth is that I couldn’t finish without the help of many people, so here are my sincere thanks to all of them. An enormous thank you must go to my supervisors, Elizabeth Clare and Stephen Rossiter. It was a pleasure to study under their supervision. Thanks for all the support, teaching and attention in these last years. I feel extremely lucky to have been at Queen Mary University, and I would like to thank all QMUL teachers and staff, who were always ready to help with everything that I needed. I would like to thank my panel members, Andrew Hirst and Steve LeComber, for all their help and constructive comments on my research through this PhD. A big thanks to Kalina Davies, Georgia Tsagkogeorga, Michael McGowen, Emeline Favreau, Timothy Penny, Orestes Gutierrez, Victoria Kemp and all the PhD students and post-docs with whom I shared my time talking about useful and not so useful things. A special thanks to my friends in the office, Rosie Drinkwater, Dave Hemprich-Bennet, Josh Potter, Omar Rahman, Kim Warren, Sandra Alvarez- Carretero, Ilya Levantis, Joe Williamson, Jane Hallam and James Gilbert, for putting up with my mess, singing and drumming in the office. I promise it was not intentional! I could not forget to give a more than special thanks to my Brazilian friends, Hernani Oliveira and Leandro Santiago, with whom I could share the joy of talking in our native tongue and talk about the wonderful and sometimes frightening experience of living abroad, away from family and old friends. And an even more special thanks to Sarah Secco for all the talks, “resenhas”, laughs and smiles we shared. 4 I also have to thank all the wonderful people in London that welcomed me in this amazing city. Bruno Muniz and Patrischa Muniz, thanks for the wonderful year living in the old Jamaica Road. This was an amazing experience and made my adaptation to living in the UK much easier. Olivia Lopez, for all the support through the first years of the PhD, for the help on fieldwork and all the good times. José Sebastião, Maria Mariga, Kabir Abubaker, Barbara Exposto, Jorge Slavis, Nicole Monaco, Carlos Vale, Pedro Constantino and Luna Constantino for welcoming me as if I were an old friend. I’m waiting all of you in Brazil! And an enormous thanks to Laura Riggi, for all the smiles, comfort and amazing times over the last year, and specially through this last month of writing. This study would never be possible without the help of many people in Brazil. An enormous thanks to Ricardo Moratelli, for helping me with all the necessary permits. João Oliveira Alves and Marcelo Weskler for the support at Museu Nacional and Marcus Vieira from LabVert/UFRJ for the information on the fragments I visited. Roberto Novaes for the help identifying some tricky bats collected. A super special thanks to my friend Victor Miraglia, without his help and friendship through fieldwork this PhD would be another story. Thanks to all the people that helped me during fieldwork: Alexandre Polletini, Mario Mestre, Regina Reis, Liliane Alves, Gabriela Jacob, Juan Porcell, Talise Laifert, Reiner Seffrin, Raphaela Barcelos, and everyone that stayed at the Casa da Pesquisa while I was there. I also need to thank all the wonderful people at REGUA: Jorge Bizarro, Cirilo Vieira, Thomas Locke, Micaela Locke, and Rildo Oliveira. I cannot thank Nicholas Locke and Raquel Locke enough for all the attention and help while I was in the Reserve. Your work is amazing and after spending all that time at REGUA, I can say I’m your fan! 5 I would like to give a big thanks to all my friends in Brazil, that in one way or another were present through the course of my PhD: Felipe Macedo, Lucas Barros, Gustavo Ramos, Guilherme Malvar, Daniel Tavares, Vitor Marigo (thanks for the pictures at REGUA), Rafael Pinto, Fábio Pupo, Raphael Logato, Dudu Muniz and Guilherme Cabeça. And my deepest thanks to Anita Salgado, that took care of our daughter through all these years and raised her into the amazing kid she is. I also have to give all my thanks to my family, Oswaldo Martins Teixeira, Walnice Martins Teixeira, Mateus Martins Teixeira and Barbara Martins Teixeira, you were missed a lot during these 4 years and a more than special thanks to my amazing daughter, Dora Pedrosa Martins Teixeira. Finally, I am very grateful to my funder, CAPES through the ‘Science Without Borders’ programme, which made this project possible. 6 Author’s Declaration I, Tiago Souto Martins Teixeira, confirm that the research included with this thesis is my own work or that where it has been carried out in collaboration with, or supported by others, that this is duly acknowledged below, and my contribution indicated. Previously published material is also acknowledged below. I attest that I have exercised reasonable care to ensure that the work is original and does not to the best of my knowledge break any UK law, infringe any third party’s copyright or other intellectual property rights, or contain any confidential material. I accept that the College has the right to use plagiarism detection software to check the electronic version of the thesis. I confirm that this thesis has not been previously submitted for the award of a degree by this or any other university. The copyright of this thesis rests with the author and no quotation from it or information derived from it may be published without the prior written consent of the author. This work was funded by the Science Without Borders program from CAPES, with additional support from the Queen Mary Postgraduate Research Fund. Signature: Date: Details of collaborations and publications: DNA sequencing of seeds and bioinformatics steps prior to seed identification were performed by Dr. Maria Kuzamina at the Canadian Centre for Biodiversity Genomics, Biodiversity Institute of Ontario (BIO) at the University of Guelph, Canada. 7 Table of Contents Abstract 02 Acknowledgements 04 Author's Declaration 07 Table of Contents 08 List of Figures 11 List of Tables 12 Supplementary Material 13 CHAPTER ONE 14 General Introduction 15 Thesis organization 25 CHAPTER TWO 26 Bat metacommunities in a fragmented landscape in South-eastern 27 Brazil Abstract 27 Introduction 29 Methods 36 Study Area 36 Bat captures 37 Landscape metrics 38 Phylogenetic Diversity 40 Mean Pairwise Distance 41 Functional Diversity 41 Statistical Analysis 42 Results 47 Bat captures 47 Elements of metacommunity structure (EMS) and predictors of community 47 structure All bats 47 Removing species with single occurrence 48 Phyllostomidae: The dominant bat family 48 Plantivores: Species that consume nectar, fruit and pollen 48 Animalivorous: Species that consume arthropods and small vertebrates 49 Species assembly 49 Discussion 51 Figures 58 Box 2.1 64 Tables 68 CHAPTER THREE 76 Habitat structure or landscape configuration as predictors of bat occurrence in a fragmented landscape of Atlantic Forest 77 Abstract 77 8 Introduction 79 Methods 85 Study area and sampling methods 85 Occupancy modelling procedure 85 Modelling bat species using single species occupancy models 89 Model comparisons