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Non-Random Seed Dispersal by Lemur Frugivores

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Non-Random Seed Dispersal by Lemur Frugivores RICE UNIVERSITY Nonrandom Seed Dispersal by Lemur Frugivores: Mechanism, Patterns and Impacts by Onja Harinala F.E. Razafindratsima A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE Doctor of Philosophy APPROVED, THESIS COMMITTEE: ArnyU! Dunham, Chair Assistant Professor of BioScienees Volker H. Associate Professor of BioScienees Evan Siemann Harry C. and Olga K. Wiess Professor of BioScienees Caroline A. Masiello Associate Professor of Earth Science _ Elizabeth M. Erhart Department Chair and Associate Professor of Anthropology TSU San Marcos HOUSTON, TEXAS March 2015 ABSTRACT Nonrandom Seed Dispersal by Lemur Frugivores: Mechanism, Patterns and Impacts by Onja Harinala F.E. Razafindratsima Frugivores act as seed-dispersal agents in many ecosystems. Thus, understanding the roles and impacts of frugivore-mediated seed dispersal on plant spatial structure and plant-plant associations is important to understand the structure of plant communities. Frugivore-mediated seed dispersal is behaviorally driven, generating nonrandom patterns of seed dispersion; but, we know relatively little about how this might affect plant populations or communities. I examined how frugivores affected plants from the individual level to the population and community levels. I used modeling, trait-based and phylogenetic approaches combined with field observations and experiments, focusing on seed dispersal by three frugivorous lemur species in the biodiverse rainforest of Ranomafana National Park, Madagascar. An analysis of traits suggested that 84% of trees in Ranomafana are adapted for animal dispersal, of which 74% are dispersed by these three lemur species, indicating their role as generalist dispersers. The distribution of fruit and seed size of bird-dispersed species was nested within the wide spectrum of size distribution associated with lemur dispersal. Nonrandom seed dispersal by these three frugivores increased per capita recruitment of the seeds of a long-lived canopy tree, Cryptocarya crassifolia, by four-fold compared with no dispersal, even though it was not an overall advantage compared to random dispersal. The three frugivores not only iii dispersed seeds away from parent and conspecific adult-trees, but also biased seed dispersal toward certain microhabitats. By using fruiting trees as seed dispersal foci, lemur frugivores structure the spatial associations between dispersed seeds and adult- trees nonrandomly, in terms of fruiting time, dispersal mode and phylogenetic relatedness. However, lemur-dispersed tree species were not more likely to be each other’s neighbors as adults. Interestingly, co-fruiting neighboring trees sharing lemur dispersers were more phylogenetically distant than expected by chance despite a phylogenetic signal in lemur dispersal mode, although there was no phylogenetic signal in the timing of fruiting among lemur-dispersed tree species. Results suggest an important link between frugivore foraging behavior and the spatial, temporal and phylogenetic patterning of seed dispersal. The important role of frugivores in structuring seed dispersion and seed-adult plant associations has critical implications for plant-plant interactions, biodiversity patterns and community structure. iv Acknowledgments First of all, I would like to express my gratitude to my advisor, Amy Dunham, for being an excellent mentor. Her wisdom, intelligence, guidance, support, encouragement, enthusiasm, and patience have tremendously helped me grow professionally and personally over the years. Thank you in particular for accepting me to work in your lab, letting me explore my passion for lemur ecology, pushing me to think outside the box and be better in everything I do, working closely with me to publish my research findings and to prepare proposals for grants and fellowships, providing me with an excellent atmosphere and guidance for doing research, always making the time for me, and for being my “hiking buddy” along the crazy path of Ranomafana terrain. I have learned a lot from you. I am also thankful to my committee, Evan Siemann, Volker Rudolf, Elizabeth Erhart and Caroline Masiello for their guidance and advice throughout my study, and for their substantial comments and insights on my field research plans and analyses. Thanks also to Thomas Jones for his help with analyzing lemur movement, and for discussions about statistics. I am also grateful to Jean Aroom for her helpful assistance with the use of GIS and associated programs. I have also benefited from advice and assistance from other faculty outside of Rice, including Kenneth Whitney, Clive Nuttman, Joerg Ganzhorn, Andrea Baden, Jonah Ratsimbazafy and Kerry Brown. I am grateful to Barbara Martinez, Nirilanto Ramamonjisoa, Haldre Rogers and Patricia Wright for being such great role models and mentors. Your words of encouragements and wisdom, your friendship and your support have helped me a lot; in many ways, you have been great examples to me of successful women researchers. v My PhD studies and field research would not have been possible without the generous financial support of Philanthropic Educational Organization (International Peace Scholarship), The Leakey Foundation (Franklin Mosher Baldwin Fellowship), Schlumberger Foundation (Faculty For The Future fellowship), Garden Club of America Award in Tropical Botany, International Foundation for Science (grant no. D/4985-1 and D/4985-2), The Rufford Foundation (grant no. 5748-1, 11288-2, and 13874-B), Primate Conservation Inc. (No. 908), The Explorers Club Exploration Fund, Idea Wild, Primate Society of Great Britain, Centre ValBio, and Rice University including the Nettie S. Autrey Fellowship, Wagoner Foreign Study Fellowship and Rice Centennial Award. MICET (Madagascar Institut pour la Conservation des Ecosystèmes Tropicaux) and Centre ValBio were extremely helpful with logistics while I was in Antananarivo and in Ranomafana. I would like to thank all of their staff for making my field experience smooth and for going above and beyond in helping me and my research team. Special thanks to Eileen Larney, John Caddle, Prisca Andriambinintsoa, Pascal Rabeson, Desiré Randrianarisata, Jean de Dieu Ramanantsoa, Paul Rakotonirina, Jean-Claude Razafimahaimodison, Benjamin Andriamiahaja, Benjamin Randrianambinina, Jean Rakotoarison, and Tiana Razafindratsita. I would also like to thank Madagascar National Parks and the Malagasy Ministry of Forest and Water for research permission. Thanks also to the Missouri Botanical Garden in St-Louis for access to their herbarium collections, and to the “Parc Botanique et Zoologique de Tsimbazaza” in Antananarivo for help with plant species identifications. Thanks also to Coke Smith, Stacey Tecot, Noel Rowe and Volker Rudolf for providing awesome lemur pictures. vi I could not have completed my fieldwork without the support and assistance of many people, including field technicians, local villagers, and undergraduates. I am grateful to Jean-Claude Ramanandraibe, Nerée Beson, Paul Rasabo, Justin Solo, Georges Razafindrakoto, Auguste Pela, Armand Razafitsiafajato, Jocelyn Mamiharilala, Victor Rasendry, Marolahy, Leroa, Velomaro, and Letsara for their valuable assistance with fieldwork. Your amazing knowledge of the fauna and flora in Ranomafana has been extremely valuable for my research, and your help greatly improved my skills in botanical identifications and lemur observations. Thanks also for showing me all the wonders of Ranomafana forest and its surroundings, and for teaching me how to survive in the forest. I enjoyed very much your company in the field and learning about your culture. I would also like to thank the undergraduates who helped me in collecting data both in field and in lab: Miora Andriamalala, Raoby Solohely, Parfait Rafalinirina, Savina Venkova, Syia Mehtani, Zo Andriampenomanana and Jake Krauss. Thank you for your valuable contribution. Thanks also to Irene Tomaschewski for help with the biochemical analyses. I am also thankful to all the local villagers in Ranomafana who helped my research team as porters, cooks and messengers during our field expeditions. Thanks also to Dave, José, Claude, Tahiana, Adafi and Sitraka for being great drivers for my team and my humongous field gears making the 11-hours difficult ride to/from Ranomafana less painful, and for being patient with my multiple stops. Thanks also to Franck Rabenahy and the other undergraduate and graduate students working at Centre ValBio for making my stay in Ranomafana a memorable and pleasant one, and for making me laugh during the difficult times of fieldwork. vii I would also like to thank the graduate students and post-docs, in the Ecology and Evolutionary Biology program at Rice University, with whom I have interacted for the past 6 years. Thanks to Brian Maitner, Ben van Allen, Andrew Bibian, Scott Chamberlain, and Patrick Clay for helpful discussions with data analyses. Thanks also to Maria Meza-Lopez, Chris Roy, Ching-Hua Shih, Therese Lamperty, Nick Rasmussen, Chris Dibble, and all the other graduate students in the EEB program for making my experience at Rice enjoyable. I am also thankful to Rice Office of International Students and Scholars for keeping me on the right and legal path from the start of my stay in the US; and to Laura Gibson, Diane Hatton, Lauren Hanson and Andrea Zorbas of the EEB program at Rice University for their logistical and administrative support. The support of my family and friends has also been great through these years. I am so grateful to my husband,
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