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THE IMPACT of HABITAT QUALITY on FEMALE RED COLOBUS MONKEY (Procolobus Rufomitratus ) REPRODUCTION

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THE IMPACT of HABITAT QUALITY on FEMALE RED COLOBUS MONKEY (Procolobus Rufomitratus ) REPRODUCTION THE IMPACT OF HABITAT QUALITY ON FEMALE RED COLOBUS MONKEY (Procolobus rufomitratus ) REPRODUCTION BY KRISTA MARIE MILICH DISSERTATION Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Anthropology in the Graduate College of the University of Illinois at Urbana-Champaign, 2012 Urbana, Illinois Doctoral Committee: Associate Professor Rebecca M. Stumpf, Chair Professor Janice M. Bahr Professor Colin A. Chapman Professor Paul A. Garber Assistant Professor Laura L. Shackelford ABSTRACT This study examines the relationship between habitat quality and reproduction in female red colobus monkeys in Kibale National Park, Uganda. Because energetic constraints impact reproductive function in female primates, this dissertation includes data on feeding ecology, activity budgets, mating behaviors, ketone levels, and reproductive hormone concentrations. This multi-faceted approach tests a model in which habitat quality impacts diet and behaviors, which ultimately effect reproductive success. By including four research groups, two in logged areas and two in old-growth areas, this research adds to our understanding of the reproductive behaviors and physiology of red colobus monkeys as well as a comparative perspective for understanding intraspecific differences for primates living in different quality habitats. Red colobus monkeys in logged areas eat more tree species, smaller amounts of each of these species, and include novel foods in their diet compared to red colobus living in old growth forest. They also spend more time feeding than individuals in old-growth areas. Female red colobus monkeys in logged areas are more constrained in their mating behaviors than females in old growth forests. Specifically, they have lower overall copulation rates and focus mating efforts during conceptive periods; whereas, females in old-growth areas mate more often, including during non- conceptive periods. Females in logged areas also have a shorter duration of maximal tumescence. This pattern supports predictions of the cost-of-sexual-attraction hypothesis, where females in poor quality habitats adjust mating behaviors to maximize the likelihood of conception while minimizing their energetic output. However, this energetic strategy may come at a cost of reducing the ability for females to use nonconceptive sex as a reproductive strategy to confuse paternity, avoid infanticide, and enhance male support. Despite differences in habitat quality, females in logged and old-growth areas do not differ as expected in their reproductive ii hormone concentrations, ketone levels, or degree of reproductive seasonality. Phenotypic and behavioral plasticity in diet and energy expenditure may allow female red colobus monkeys to maintain reproductive function in lower quality habitats that are stable and protected. The ability to adjust to previously logged habitats that are now protected has important implications for conservation management strategies, such as prioritizing areas for protection, and provides insight into how extant primates, including humans, adjust to environmental change. iii For Gary Macko, my uncle and most enthusiastic supporter. iv ACKNOWLEDGMENTS It is only appropriate to start a dissertation on females with an acknowledgment of all the strong, inspiring, supportive, loving, funny, talented, intelligent women in my life. The first, of course, is my mother. Karen Macko-Milich taught me how to care for people, how to overcome obstacles, how to be independent and capable. She always supported me in all of my academic endeavors, even when she did not understand my choices or worried about my safety. I owe all of my professional success to her. My sister, Jennifer Milich, who was the quintessential older sister—teaching me how to be cool, making me tough, answering all the questions I couldn’t ask my mom, putting up with my antics, and making sure I didn’t make too many stupid mistakes along the way. I followed in her footsteps in many ways, including my love of animals, my vegetarian diet, and my bachelors in zoology. My grandmother, my Baba, Josephine Macko. While I did not inherit her love of shopping, her gorgeous blue eyes, or her adorable ability to be a proper lady, I have benefited from her tender care, her sense of humor, and her perseverance. She kept me supplied with fried egg sandwiches and haluski on all my trips home and brightened my days with weekly phone calls to check on me no matter what city I lived in. My wonderful aunts – Aunt Cathy, Aunt Lana, Aunt Pat, and Aunt Susie – who filled my childhood with many happy memories. For both my sister and me, these women have been there to celebrate our greatest successes and to sympathize with our greatest losses. My rockstar cousins, Kim, Kelly, and Jess, who were so cool and so exciting and who I idolized growing up. I believe that even to this day, Kim’s early advice on how to manage my big hair is what has kept me from looking entirely like a crazy scientist. Kelly was my first and best pen pal and a welcome confident. Jessica made me laugh endlessly every time I saw her, and to me, she was larger than life. And my Grandma Milich. I know she would be very proud of me for this accomplishment. v My academic development has been equally inspired by wonderful women. My advisor, Rebecca Stumpf, who mentored me through my moments of excitement and frustration. When I applied to graduate schools, I wanted to combine my interest in conservation with my interest in reproductive biology. Becky helped me to design a project that did just that. In my first semester of graduate school, Becky’s class on Behavioral Endocrinology provided me with the basis for my dissertation research. Her intellectual contribution not only strengthened my dissertation and graduate career, but has also made a lasting impression that will shape my approach to future research. I hope to be able to emulate how kindly and gracefully Becky deals with difficult situations. At times, she shared her personal stories of navigating the field of primatology as a woman, which was exactly the type of insight I was hoping to gain from having a female advisor. My lab advisor and close mentor, Janice Bahr, has provided me endless support in every possible way during my graduate career. She welcomed me into her lab and provided me with whatever I needed for my research. She taught me reproductive biology and lab methods in endocrinology, but she also taught me how to be an academic and a mentor. Outside of the lab, she made me a part of her family and was always there for me. When I was hobbling around on crutches in the snow, she would pick me up and take me wherever I needed to go. She has been like a mother to me. My committee member, Laura Shackelford, who provided me with valuable feedback on my dissertation and invaluable moral support during my graduate career. I am always searching for positive female role models in my field—those that are successful in their careers and happy in their lives. Laura is exactly that type of role model and she gives me hope for my life in this field. My friends, who are like family to me, include equally inspiring female figures. Amanda Byers, Angie Puertas, Beth Kostelnick, and Sue Wismar – childhood pals that still remain my vi closest girlfriends. Beth is my oldest friend and still so important in my life, Angie is the sweetest person I know and I appreciate the hope she has for me, Amanda and I can spend hours in deep discussion, and Sue is hilarious and has gone great lengths to help me out (like driving 5 hours to pick me up when I’ve been sick). Sara Critchfield is a kindred spirit who has taken on many adventures with me from our first moments as trees in a high school play to caring for me when I had typhoid in India. Daniela Atanasovski is an inspiration as a successful female nuclear engineer. Her family, most especially Marijana and Vesna, have been a lovely second family to me and help me to engage with my Eastern European roots. All of these friends are near and dear to my heart and have offered me shelter and encouragement along the way. Emily Otali and Sarah Paige were my two closest friends during field work. They are both strong, intelligent women who were always willing to help deal with logistics for my project when I was not able. More importantly, they offered much needed moral support. I must now turn my focus to the amazing male role models in my life. The person I attribute my career as a primatologist to is my grandfather, PapPap, Joseph Macko. From a young age, he showed me the beauty of the natural world – taking me fishing, letting me pick tomatoes from the garden, and spending time outside. His career as an amateur archaeologist (his large collection of Native American artifacts made him something of a local celebrity) and his love of nature somehow combined in me to spark the fire of a biological anthropologist. In many more ways than this, PapPap left a lasting impression on me and influenced the path of my life. Each of my uncles has played a very important role in my life. As a biology teacher, my Uncle Jim was never short of things to teach me about biology and the natural world. He is an outdoorsman through and through and he still provides me with endless amounts of delicious, fresh vegetables, opportunities to wander around in the forest with him, and interesting insight vii into the biological world. My Uncle Ron is without a doubt the most influential person in giving me the opportunity to travel the world. I am fortunate that he is a talented international airline captain and that he is generous with his family passes that allow me to go on many adventures around the world, including to see primates in distant habitats.
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