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Copyright by Simone Caroline Cappellari 2011 Copyright by Simone Caroline Cappellari 2011 The Dissertation Committee for Simone Caroline Cappellari certifies that this is the approved version of the following dissertation: Evolutionary Ecology of Malpighiaceae Pollination at the Species and Community Levels Committee: Beryl B. Simpson, Supervisor John L. Neff , Co-Supervisor Daniel I. Bolnick Lawrence Gilbert Lauren A. Meyers Michael Singer Evolutionary Ecology of Malpighiaceae Pollination at the Species and Community Levels by Simone Caroline Cappellari, Dipl. Biol. Dissertation Presented to the Faculty of the Graduate School of The University of Texas at Austin in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy The University of Texas at Austin August 2011 Dedication I dedicate this thesis to Christian Rabeling, my life partner, love, and best friend, whose adventurous passion for nature is my daily source of inspiration; to my family and to the memory of my dear grandmother, Etelvina dos Santos (Vó Teté), who enriched my childhood with her stories of frogs singing in the forest and bird parties in the sky. Her simple joys taught me a great deal about what matters in life. “Just living is not enough... One must have sunshine, freedom, and a little flower.” -Hans Christian Andersen Acknowledgements The support, friendship, and help from several people made the work presented in this dissertation possible. A special thanks goes to my adviser, Beryl Simpson, for accepting me as a student in her lab, reading and editing my texts, teaching me how to write papers, diving deeply into the world of ecological networks with me, and for giving me enough freedom to pursue my own interests. I thank Jack Neff, a walking encyclopedia of all matters, for his patience continuously teaching me lessons of bee taxonomy and systematics over the past six years, for sharing so much of what he knows about plant-pollinator interactions with me, and especially for critically reading my manuscripts and grant applications. I am grateful to my other committee members: Lauren A. Meyers, Dan Bolnick, Larry Gilbert, and Mike Singer for their enthusiasm for the topic of this dissertation, for contributing ideas, suggesting papers, and statistical methods that greatly improved the quality of the results presented in this thesis. A special thanks goes to Mike Singer for hosting me in his lab when I needed a quiet space to work, for showing up at random places at random times and giving good advice whenever I felt graduate school was about to swallow me. This study could not possibly have been done without the help of my collaborator and friend Rosana Tidon, who opened the doors of the Universidade de Brasilia (UnB) for me and provided me with all sorts of logistical support I could possibly need during the years of fieldwork in Brasilia. I thank her and her lab also for their great hospitality during my visits at the UnB. I wish to thank the UnB Graduate Program in Ecology for welcoming me as a visiting researcher to their institution, for providing me the permits necessary to conduct fieldwork, and granting access to the field station and other facilities. I thank the staff of the Reserva Ecológica do IBGE for allowing me to conduct my research at the station, for their great hospitality, and logistical support during every field season. A special thanks goes to Sr. Neidimar Bispo for his friendship and for helping me repair all sorts of vehicles, from bikes to cars, I used during my field work. I am also very grateful to the following students: Andre Mendes, Dianne Souza, Gabriela Correa, and Paulo H. Pinheiro who overcame their fears of snakes, and dedicated their weekends and sweat to help me in the field and in the lab. Plant identification was also an important part of this work, which was done with the kind help of the following v experts: Maria Aparecida da Silva (IBGE), Maria Cândida Mamede (IB), and Carolyn Barnes Proença (UnB). I also thank Antonio Aguiar (UnB), and the Hymenoptera research group from the Universidade Federal do Paraná, especially Gabriel Melo, Felipe Vivallo, Kelli Ramos, and Danúncia Urban for spending much of their time with the identification of my bees and for teaching me how to identify them myself. I am very thankful to Marcelino C. Boaventura for contributing with his unpublished data set for the comparative analyses of Chapter 2; and to my collaborators from the Universidade Estadual de Campinas, Brazil, Anita J. Marsaioli and M. Abdul Haleem, for doing the chemical analyses of floral oils, which enabled me to pursue chemo-ecological perspectives in Chapters 3 and 4. My years of fieldwork at the station in Brasilia will remain as a dear memory to me in part due to the presence of other researchers with whom I overlapped – in particular Anita, Daniel, Imma, Amartya, Leonel, Randol, Erika, Sybil, Eric, Lucíola, Aliny, On Lee, Bill, and Marina. These people provided not just good company but also car rides, supplies, scientific discussions about Cerrado, surgical assistance with „bichos- de-pé‟, cold drinks after a day in the field, etc. Thank you all! I would like to thank several people that contributed to the making of this dissertation: Blinda McClelland for having me as her TA for many years and for being supportive of my field research schedule; Erika Hale, from the Division of Statistics and Scientific Computation at UT, whose help and support were essential for the statistical analyses of Chapters 3 and 4; Gwen Gage, from the UT Graphics Department, and Barrett Klein for making the drawing of bees used in Chapter 5; Christian Rabeling for introducing me to the wonderful world of electron microscopy, and for help making images for Chapter 5. I thank Ted Schultz and his group from the Smithsonian Institution for the great atmosphere during the last year of my dissertation, for providing the equipment needed to estimate pollen quantity in Chapter 4, and for access to automontage imaging for Chapter 5. I thank my friend, collaborator, guru of network and food web knowledge, and plant-pollinator enthusiast Samraat Pawar for being a great discussion partner for all sorts of ideas and questions that crossed my mind since the beginning of this work. I thank him and Kate Behrman for encouraging me to learn the computational methods – and I did it! I also wish to thank all the anonymous people out there doing what I call „computational charity‟ for designing websites with tips for using R and creating vi packages that make complicated analysis easy to run. I would not have done my analyses without your help! I thank all my colleagues and friends in Austin whose friendship made the past years so much more enjoyable, especially: Barrett Pupated Klein, Betsy Kreakie, Carlos Guarnizo, Catalina Estrada, Debra Hansen, Deepa Agashe, Dosha Durban, Eben Gering, Elizabeth Ruck, Josh McDill, Juan Santos, Kate Behrman, Krushnamegh Kunte, Mariana Vasconcellos, Natalia Biani, Nikhil Advani, Samraat Pawar, Sasha Mikheyev, Schona Mannig, Scott Solomon, Sze Huei Yek, Vicky Huang, and Xiao Wei; and all past and current members of the Simpson lab with whom I overlapped for the good atmosphere and friendship. Thanks to Sandy Monahan, for saving me from bureaucratic catastrophes and for always being so sweet to all of us. Finally, yet importantly, I would like to thank my family in Brazil, especially my parents, Roselene and Luiz, my siblings, and their partners (Viviane, Cris, Ewerton, Lisa, Vanessa and Yasmin) for always being there for me and for cheering me up with every step that brought me closer to getting this degree. A special thanks goes to my sister, Vica, for helping me buy a field vehicle so I could do my research more effectively. I also thank my family in Germany, especially Renate, Klaus, and Oma Hermine, for their support and for providing a steady supply of chocolates and coffee that sure kept me up and running. My husband Christian Rabeling I thank for his loving support all these years, for believing in me and my work, for coping with my long field trips to Brazil, for brightening up my life, making me happy even when skies became grey, and for making all this worthwhile. I am very grateful for receiving funding from the following sponsors: EEB program departmental funds; Lorraine Stengl and the Dorothea Bennett Memorial Fellowship Fund from which I received support that made it possible for me to collect data over several summers; NSF for a Doctoral Dissertation Improvement Grant (DEB- 0909511); Frank and Fern Blair Fellowship Fund; The Tinker Foundation; Texas Ecolab; and The University of Texas at Austin for providing support through a University of Texas Continuing Fellowship for my last year so I could dedicate myself entirely to the data analysis and writing of this dissertation. vii Evolutionary Ecology of Malpighiaceae Pollination at the Species and Community Levels Publication No._____________ Simone Caroline Cappellari, Ph. D. The University of Texas at Austin, 2011 Supervisor: Beryl B. Simpson Co-Supervisor: John L. Neff Abstract Plant-pollinator interactions figure as key elements promoting the natural regeneration of terrestrial vegetation, as most plants depend on animals to transfer their gametes between flowers and produce seeds. Bees are the most common pollinators of plants and their interactions with flowers have served as model systems for the study of specialized mutualisms since Darwin‟s time. While most plants offer nectar as a reward and attract a variety of floral visitors, others produce distinctive types of resources which are sought by particular groups of pollinators. Such associations may involve specialization at the morphological, behavioral, or physiological levels and are especially common in tropical habitats. The interactions between oil-producing flowers of Neotropical Malpighiaceae and oil-collecting bees are an example of a specialized mutualism in which plants offer lipids to attract pollinators that use the resource to build nest cells and feed their offspring.
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