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Copyright 2013 Katherine Ryan Amato Copyright 2013 Katherine Ryan Amato BLACK HOWLER MONKEY (ALOUATTA PIGRA) NUTRITION: INTEGRATING THE STUDY OF BEHAVIOR, FEEDING ECOLOGY, AND THE GUT MICROBIAL COMMUNITY BY KATHERINE RYAN AMATO DISSERTATION Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Ecology, Evolution, and Conservation Biology in the Graduate College of the University of Illinois at Urbana-Champaign, 2013 Urbana, Illinois Doctoral Committee: Professor Paul A. Garber, Chair, Director of Research Associate Professor Angela D. Kent Professor Steven R. Leigh Associate Professor Ripan Malhi ABSTRACT All animals, including primates, face the challenge of obtaining sufficient energy and nutrients despite 1) variation in food availability across habitats and seasons and 2) temporal fluctuations in nutritional requirements due to life history processes. Because variation in food availability or nutritional requirements requires animals to vary energy and nutrient intake, vary energy and nutrient expenditure, or vary digestion and assimilation of energy and nutrients to meet demands, many studies of primates examine shifts in primate activity budgets and foraging patterns across seasons and life history stages. However, few studies establish a direct relationship between activity and diet composition and energy and nutrient intake. Additionally, the mechanisms that primates use to digest and assimilate their food are largely overlooked. Mutualistic gut microbial communities impact host digestive efficiency and assimilation by breaking down otherwise indigestible material and providing hosts with energy and nutrients. Laboratory studies have demonstrated that gut microbial communities shift in response to changes in host diet and physiology, and while these shifts may allow hosts to digest food items more efficiently to meet energy and nutrient demands, no data are currently available to explore this relationship in wild primates. This dissertation describes an integrated 10-month field study investigating the behavioral and physiological mechanisms used by non-human primates to satisfy nutritional demands in response to changes in diet and physiology. Specifically, it examines the relationship between behavior, physiology and nutrition in two groups (N = 16 individuals) of wild, black howler monkeys (Alouatta pigra) in Palenque National Park, Chiapas. The first chapter explores patterns in black howler monkey nutritional intake across time to determine whether howlers employ a foraging strategy that regulates energy and/or nutrient intake and whether this strategy ii changes in response to the amount of ripe fruits or leaves in the howler diet. The second investigates the response of the howler monkey gut microbial community to changes in diet composition across time and the potential effects of changes in the gut microbial community on howler digestive efficiency and nutrition. Finally, the third chapter examines differences in activity, diet, and the gut microbiota among adult male, adult female, and juvenile howler monkeys to determine whether behavioral or physiological mechanisms allows adult females and juveniles to compensate for the increased nutritional demands of reproduction and growth. The data presented in this dissertation suggest that although they are able to consume large quantities of leaves periodically, on an annual basis, black howler monkeys consume more ripe fruits than leaves. They also exhibit a protein-regulating foraging strategy similar to that of ripe-fruit-specialist spider monkeys and consume more protein energy and more total energy than spider monkeys. These results indicate that black howler monkey feeding ecology is similar to that of other primates that consume mostly fruit and that both fruits and leaves are critical to understanding howler monkey nutrition and feeding ecology. Additionally, data from this dissertation show that the impacts of the gut microbial community must be considered when discussing howler monkey ecology and evolution. The howler gut microbial community shifts in response to changes in the howler diet over time, contributing additional energy during periods of reduced energy intake. Similarly, adult female and juvenile howler monkeys are characterized by bacteria that produce more energy and vitamins compared to adult males. These differences, together with differences in nutritional intake, may play a role in allowing females and juveniles to meet the increased nutritional demands of reproduction and growth. As a result, while behavior and foraging patterns are important in understanding how howler monkeys respond to iii temporal variation in food availability while maintaining activity, ranging and life history patterns, the nutritional contributions of the gut microbiota are also critical. Understanding how primate behavior, feeding ecology, and gut microbial processes relate has important implications for the study of primate ecology and evolution. The resources provided by the gut microbial community are typically not accounted for in traditional studies of behavior and feeding ecology but are crucial for understanding primate nutrition. By pinpointing both the causes and effects of changes in gut microbial community composition and improving the understanding of how foragers adjust to changing nutritional demands in variable environments, we can approach studies of primate behavior, nutrition, and health more effectively. While the patterns and mechanisms involved may differ across primate populations in response to differences in phylogeny or habitat, improved knowledge of both nutrition and physiology is critical for primate research worldwide. iv ACKNOWLEDGEMENTS First and foremost, I would like to thank my advisor, Paul Garber, for his guidance and support during this process. Although I introduced us both to new territory, his insight and experience were invaluable and allowed me to navigate through a wide variety of challenges. I would also like to thank my doctoral committee: Angela Kent, Steve Leigh, and Ripan Malhi. All three of them encouraged me to aim high and welcomed me into their labs so that I would have access to a wider set of tools and analyses for this project. I am lucky to have had such outstanding mentors. In addition to my doctoral committee, I am especially grateful to a number of other investigators for providing me with critical resources and feedback. Alejandro Estrada allowed me to work under his permits in Mexico and supplied important logistical support in the field. Rod Mackie offered me important insights into gut microbiology and digestive physiology, and allowed me the use of his lab. Carl Yeoman was an integral part of data analysis. His familiarity with programming and bioinformatics greatly facilitated my own progress, and his friendship and support in the lab were an important part of this process. Emily and Rick Lankau supplied me with a wealth of statistical advice and positive feedback. Carol Augspurger advised me on the collection and preservation of plant specimens in the field. Miguel Martínez Icó assisted me with tree species identification in the herbarium of EcoSur in San Cristobal de las Casas, Chiapas, Mexico, and Dave Seigler made available the collections and supplies of the herbarium of the University of Illinois. I would also like to express my gratitude to a number of other people for their important contributions to my work. First, I thank Nicoletta Righini and Rodolfo Martinez Mota for collecting additional samples for me at their field site. I am also grateful to Nicoletta for v productive discussions regarding howler monkey nutrition and feeding ecology, and am greatly appreciative of her hospitality over the past year. I am lucky to have such a wonderful friend. Liz Mallott provided me with detailed instructions for using ArcGIS that greatly simplified some of my analyses. Alex Ulanov analyzed the metabolite profiles in my plant samples, and Kou-San Ju helped me better understand the data that were produced. Similarly, Inhyuk Kwon and Jong Nam Kim sacrificed their time to train me in volatile fatty acid and ammonia assays. I am grateful for the helpful discussions I had with Andres Gomez about primate gut microbiology, and, finally, I am eternally indebted to the GEEB Microbiology group for their friendship and guidance. Without Cassandra Allsup, Emily Lankau, Sara Paver, and Ariane Peralta, my Ph.D. experience would have been very different. I would like to give a special thank you to the students that assisted me with data collection and analyses: Sarah Wengert and Brianna Wilkinson in the field and Jill Britton and Andrew Schuh in the lab. I am especially grateful to Brianna for assisting me for nearly the entire field period. She was excellent, and this project would not have been the same without her. In the field, I also greatly benefitted from the friendship and sporadic assistance of Sarie Van Belle and all of her field assistants as well as Chiara Castiglioni and David Muñoz. Chiara, especially, has been a constant source of positive energy. Yasminda García del Valle and Ana Guadalupe Rocha Loredo also welcomed me into their homes in Mexico and offered me support in my research endeavours in Mexico for which I am truly grateful. Finally, I would like to thank my familyfor their love and support throughout my education: my husband, Samuel Morales Lopez, my parents, John and Mary Amato, my brother, J.D. Amato, my sister, Allison Amato, my grandparents, Helen and Don Ryan and Frank
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