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Ecological Costs and Benefits of Secondary ECOLOGICAL COSTS AND BENEFITS OF SECONDARY METABOLITES IN ANIMAL-DISPERSED FRUITS by SUSAN R. WHITEHEAD B.A., Oberlin College, 2001 A thesis submitted to the Faculty of the Graduate School of the University of Colorado in partial fulfillment of the requirement for the degree of Doctor of Philosophy Department of Ecology and Evolutionary Biology 2013 This thesis entitled: Ecological Costs and Benefits of Secondary Metabolites in Animal-Dispersed Fruits written by Susan Richardson Whitehead has been approved for the Department of Ecology and Evolutionary Biology (Dr. M. Deane Bowers, Committee Chair) (Dr. William D. Bowman) (Dr. Michael Breed) (Dr. Alexander Cruz) (Dr. Lee A. Dyer, University of Nevada) Date The final copy of this thesis has been examined by the signatories, and we find that both the content and the form meet acceptable presentation standards of scholarly work in the above mentioned discipline. Whitehead, Susan R. (Ph.D., Ecology and Evolutionary Biology) Ecological Costs and Benefits of Secondary Metabolites in Animal-Dispersed Fruits Thesis directed by Professor M. Deane Bowers ABSTRACT Ripe, fleshy fruits function primarily to attract mutualist animals; however, many wild fruits contain secondary metabolites that are distasteful or toxic to consumers. A number of hypotheses have been proposed to explain this apparent evolutionary paradox, but few have been tested experimentally. The goal of my dissertation research was to investigate the evolutionary ecology of fruit chemical traits, integrating quantitative chemical analyses with experiments to elucidate the functional significance of fruit secondary metabolites in natural populations. I conducted a series of field studies using three groups of plants, one temperate and two tropical. First, using the tropical shrub Hamelia patens (Rubiaceae), I investigated the potential for leaf herbivory to affect seed dispersal and showed that plant responses to herbivory can alter fruit chemistry and reduce fruit removal by seed-dispersing birds. Next, using detailed chemical analyses and field observations of fruit-frugivore interactions in the temperate shrub Lonicera x bella (Caprifoliaceae), I showed that fruits can contain higher levels of secondary metabolites than leaves, and that these metabolites serve an important role in defense against insects and pathogens. Finally, using additional chemical analyses and controlled experiments with the tropical plant genus Piper (Piperaceae), I showed that fruit secondary metabolites can be explained as a trade-off between defense against antagonists and attraction of seed-dispersing bats. Together, this dissertation demonstrates the importance of fruit chemical traits in mediating interactions between plants and diverse antagonistic and mutualistic consumers and represents a significant contribution to our understanding of both seed dispersal and plant defense. iii ACKNOWLEDGEMENTS Reflecting on my years as a graduate student, I am full of gratitude for all of the wonderful people who have provided guidance, moments of clarity, and companionship. This work would not have been possible without their support. First and foremost, I would like to thank my advisor, Deane Bowers. I feel so fortunate to have had a mentor that has been so giving with her time, nurturing my development as a scientist through countless discussions, regular feedback, training, and professional development opportunities. But perhaps even more importantly, Deane has nurtured my love of science through her infectious energy and enthusiasm, making my years as a Ph.D. student truly enjoyable, both personally and professionally. I would also like to thank the other members of my committee, Bill Bowman, Mike Breed, Alex Cruz, and Lee Dyer, all of whom have always been willing to offer their insights, support, and encouragement whenever I needed it. An extra thank you goes to Bill for facilitating my experiences with K-12 students and a crazy scheme to get to Antarctica and to Lee for hosting me in his lab and inspiring me to work on Piper, one of the great loves of my life. To my unofficial committee member, Yan Linhart, a heartfelt thank you for all of our wonderful discussions and your continued support from afar. I never could have completed an integrative project involving chemistry, plants, insects, fungi, and bats without a lot of help and collaboration. A huge thank you goes to Maria Fernanda Obando Quesada for teaching me to catch bats, being an amazing field companion and friend, and having endless patience with my terrible Spanish. I would also like to extend a special thank you to Chris Jeffrey for his guidance and collaboration in the world of chemistry, allowing my research to grow in exciting new directions. To my many other collaborators on dissertation chapters and side projects, Katja Poveda, Ellen Reid, Joe Sapp, André Kessler, Craig iv Dodson, Michael Leonard, Andrea Glassmire, Amy Trowbridge, Kallin Tea, Loren Sackett, Ian Schwartz, Justin Baldwin, and Don Cipollini, I have learned so much from all of you and I am forever grateful. I am also forever indebted to the many field assistants that have worked on various aspects of my dissertation over the years, without their help I am certain I would be processing samples for the GC/MS and reviewing bat video for another decade. My veritable army included Jason Hong, Hannah Burk, Heather Stone, Daniel Brunelle, Daniela Azofeifa, Eric Ballestero, Albert Como, Pornsawan “Gift” Poopat, Marisol Luna-Martinez, Jordan Tiramani, Sarah Ha, Timothy Kashiwa, Nina Xiong, Gillian Brooks, Peter Armington, Logan Ganoe, Joel Schulte, and Garrett Smith. Many friends have also helped me along the Ph.D. path in countless and invaluable ways. To the Bowers Lab members (actual and honorary), Kasey Barton, Mary Jamieson, Carolina Quintero, Jessica Vargas, Natalie Robinson, Crystal Boyd, Caitlin Kelly, Megan Blanchard, Toby Hammer, Brian Stucky, Evan Lampert, Cesar Nufio, Ken Keefover-Ring, and Amy Trowbridge, you all are amazing. Thank you for the constructive feedback and all the laughs we have shared in and out of the lab. I have also had so much support from the graduate student community in Ecology and Evolutionary Biology. I couldn’t begin to list all of the people who have offered advice, camaraderie, and essential sanity breaks, but I would like to especially acknowledge Natalie Robinson, Loren Sackett, SeJin Song, Mary Kay Herzenach, Katherine McClure, Kallin Tea, Amy Trowbridge, and Ty Tuff. I never would have made it through the rough patches without you. I am also fortunate to have been a part of an amazing community of tropical biologists at La Selva Biological Station in Costa Rica, without whom my field seasons would have been much lonelier and less adventurous; many thanks to Vanessa Boukili, Kevin Loope, Bonnie Waring, Jenny Stynoski, Shinichi Asao, Virginia Weigand-Noble, Kellie Kuhn, v Diego Dierick, Diego Salazar, Justin Nowakowski, Karin Schneeberger, and Martina Nagy, just to name a few. Finally, to some of my dearest friends outside the biology bubble, Paul Jenkins, Amanda Lewis, Devon Corbet, Candice Evans and Amanda Evans, thank you for reminding me of the existence of the rest of the world. Finally, I am so grateful to my family, who have given me the most solid foundation of love and support I could ever imagine. Many sincere thanks to my parents, Dick and Peggy Whitehead, my sisters Carey and Hilary Whitehead, my darling niece Hattie, and my extended family Kyle, Nancy, Mike, Caid, Alex, Jo, Katie, John W., Susan, Tom, John M., Mickey, Ruth, Chris, Allen, Jordan, Bryan, Gracey, Lola, Anna, Wade, and Pryor. And lastly, but above all, I would like to thank my incredible husband, Abe Lee, whose support, generosity, and humor are seemingly endless. I can’t imagine being on this journey without you. Funding sources for this work included the National Science Foundation (Dissertation Improvement Award DEB 1210884), the National Geographic Waitt Foundation, Bat Conservation International, the Garden Club of America, the Organization for Tropical Studies, the University of Colorado Department of Ecology and Evolutionary Biology, the University of Colorado Beverly Sears Grants, the University of Colorado Museum of Natural History, a John W. Marr Memorial Grant, and the University of Colorado Undergraduate Research Opportunities Program. vi CONTENTS 1 INTRODUCTION 1.1 Research Rationale and Background……………………………………………….…...….1 1.2 Chapter Overview……………………………………………………….……..………..….5 2 HERBIVORE-INDUCED CHANGES IN FRUIT-FRUGIVORE INTERACTIONS 2.1 Abstract……………………………………………………………………….…….………9 2.2 Introduction…………………………………………………………………….…….……10 2.3 Methods……………………………………………………………………….……….…..12 2.4 Results………………………………………………………………………………….….17 2.5 Discussion…………………………………………………………………………………20 3 IRIDOID AND SECO-IRIDOID GLYCOSIDES IN A HYBRID COMPLEX OF BUSH HONEYSUCKLES: IMPLICATIONS FOR EVOLUTIONARY ECOLOGY AND INVASION BIOLOGY 3.1 Abstract………………………………………………………………………………...….24 3.2 Introduction………………………………………………………………………………..25 3.3 Results and Discussion…………………………………………………………………….28 3.4 Conclusions………………………………………………………………………………..37 3.5 Experimental………………………………………………………………………………38 4 EVIDENCE FOR THE ADAPTIVE SIGNIFICANCE OF SECONDARY METABOLITES IN RIPE FRUITS 4.1 Abstract………………………………………………………………………………...….43 4.2 Introduction………………………………………………………………………………..44 4.3 Methods……………………………………………………………………………………47 4.4 Results……………………………………………………………………………………..55 4.5 Discussion…………………………………………………………………………………63 4.6
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