Do Female Spider-Monkeys Tend-And- Befriend?
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Stress and Sociality in a Patrilocal Primate: Do Female Spider-Monkeys Tend-and- Befriend? DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Michelle Amanda Rodrigues Graduate Program in Anthropology The Ohio State University 2013 Dissertation Committee: Dawn M. Kitchen, Advisor W. Scott McGraw Douglas E. Crews Randy Nelson ii Copyrighted by Michelle Amanda Rodrigues 2013 iii Abstract Stress provokes an adaptive strategy that mobilizes the body for acute physical challenges. However, chronic stress has detrimental effects that can reduce health and reproductive fitness. Thus, coping mechanisms are valuable in reducing chronic stress. One such mechanism, the “tend-and-befriend” strategy, refers to affiliation between females as an adaptive strategy to deal with stress. This mechanism is proposed to be a widespread strategy throughout the primate order, and one that underlies patterns of female bonding in humans. Although this strategy has been documented in matrilineal primates characterized by female kinship bonds, there has not been documentation of this strategy among unrelated females. Such documentation is necessary to demonstrate that this strategy is unrelated to female philopatry. Since our hominid ancestors are presumed to be male-philopatric, examining if this strategy applies to unrelated females is essential to understanding the evolutionary context of this mechanism. Here, I examine the tend- and-befriend strategy in a species characterized by fission-fusion social organization and female dispersal. I examine the patterns of female-female social relationships, male aggression, and ecological variables on glucocorticoid concentrations, a measure of physiological stress, among female black-handed spider monkeys. Behavioral, hormonal and ecological data were collected in a wild, habituated community. I validated a cortisol ii assay for black-handed spider monkeys, and determined that cortisol concentrations do not significantly vary between reproductive states. The only activity variable or ecological variable that was significantly associated was time engaged in rest, with rest and cortisol concentrations inversely related. I found that affiliative behavior was significantly correlated with cortisol concentrations. I further found that females engaged in higher rates of affiliative behavior on days when fecal samples with high cortisol concentrations were collected. Most females exhibited a pattern of low cortisol concentrations punctuated by spikes in cortisol that returned to baseline, rather than chronically elevated cortisol concentrations. I found that patterns of association and affiliation were highly variable, and that rates of affiliative behavior were significantly correlated with association indices. I conclude that these patterns indicate that female spider monkeys are engaging in high rates of affiliative behavior when they are experiencing stress, and that engaging in affiliation brings cortisol concentrations back to baseline values. This research has direct implications for understanding the evolution of the stress response, and whether bonding among unrelated females is a result of ancestral tendencies within the primate order or a more derived feature limited to certain taxa. iii For Roger Rodrigues iv Acknowledgments There are many people, organizations, and animals that have helped make this project possible. First, I have to thank Dawn Kitchen for both encouraging and challenging me. Dawn has been a great friend and mentor throughout my PhD program, and continually challenges me to improve my work, even if it means endless cycle revisions and learning new statistical tests. I also am very grateful to Scott McGraw, Douglas Crews, and Randy Nelson for serving on my committee, and teaching me about primate ecology and behavioral endocrinology, and providing feedback to strengthen this project at various stages. I am very grateful to Jill Pruetz for giving me the opportunity to first study at El Zota and supporting my research. Jill is a mentor, a colleague, and a friend, and she is responsible for the early years of research on the study of the El Zota spiders. I also owe a great deal of gratitude to Stacy Lindshield. Stacy helped me so much in establishing planning my research, and she first introduced me to the beautiful forest and the spider monkeys. Stacy has also provided feedback on this project at various stages, particularly on the ecological component. I also appreciate all of the assistance that Matt Lattanzio has given me at every stage of my research. He taught me how to identify snakes v venomous snakes, provided feedback and suggestions at the early stages of this project and has provided statistical advice whenever I am stuck on analysis. Matt has been a great colleague and friend, and I would not have made it through graduate school without his support. Many people at the El Zota Biological Field Station helped me tremendously in this research. I am eternal gratitude to Israel Mesen for facilitating so many logistical aspects of my dissertation research, especially translating everything from financial transactions to rather embarrassing medical problems. Marbeli, Tomas, Hinder, Daisy, and Abigail, Victor and Noely, Wilmara Maria and Carlos Luis, Dona Anna and Douglas, Marjorie and Joel all went out of their way to make me feel comfortable at El Zota. Marbeli, Maria, Dona Rosa, and Marjorie made an extra effort to make my favorite foods and surprise us with desserts when torrential rain got our spirits down. Maria and Luis were wonderful friends and companions, and made El Zota truly feel like home. I am also very grateful to Hiner Ramirez, Enid Ramirez, Maribel Ramirez, and their entire family for allowing me permission to work at El Zota, supporting conservation of the forest, and being wonderful hosts. I appreciate the assistance of Jessica Walz in pilot research field, and her feedback and support throughout this project. She was a fantastic assistant and companion in the field, and a great colleague and collaborator. Agnieska Sukiennik and Katy Gilbert assisted me in identifying and naming individuals. I am also grateful to Jason Ferrell and Katy for establishing the ecological transects. vi I am incredibly indebted to three wonderful assistants that went above and beyond in their dedication to finding and keeping the monkeys, even when it meant getting perpetually getting stuck in the swamp and having to crawl out. They did their best to collect fecal samples no matter what: whether they were splattered on tall leaves or the assistant’s eyelids, or if they needed to sniff it to distinguish it from rotting fruit. They then patiently sorted through fecals to remove debris and seeds, and Emily went even further with her own side project that involved sorting and washing the remaining fecals to recover and identify seeds. Each field assistant helped train the next, and they monitored transects, recorded party encounters, identified animals and collected fecals any time I needed to travel away from the field site or was not feeling well. They got very dirty They got eaten alive by mosquitoes. They motivated me when my own motivation was flagging. They walked through more spider webs than we can ever count and stayed calm even if when there were spiders in their hair. They helped me to see the forest through new eyes and appreciate so many aspects of the forest ecosystem . This project owes so much to Emily “Little Chair” Stulik, Anna “Fondles Poo” Kordek, and Lindsay “One Feather” Mahovetz. “Sings with Monkeys” is incredibly appreciative. Both Emily and Anna also worked simultaneously on side projects that I hope will further our knowledge of the Pilon community’s feeding ecology. I am also grateful to the friends and colleagues who have provided advice, feedback, and moral support throughout graduate school. Cathy Cooke, Elizabeth Hellmer, Stacy Lindshield, Matt Lattanzio, Kristina Walkup, Tracie McKinney, Erin Ehmke, Laurie Kauffman, Liz Beggrow, Ellen Furlong, Anna Yocom Laurie Reitsema, vii Jennifer Spence, Hedy Justus, Erin Kane, Dara Ulmer, Sarah Martin, Amy Eakins, Lori Critcher, Jessica Walz, Jocelyn Bryant, Darcy Hannibal, Raymond Vagell, and many others have provided advice, support, or feedback at various stages of my research. I also want to acknowledge the great female friends I rely on when I need to tend-and-befriend: Amy Laude, Angie Sansguiri, Divya Kansagra, Phillipa Soskin, Cathy Cooke, Elizabeth Hellmer, Karen Bullock, Melissa Tanouye Conger, Paulomi Shah, Danielle Van Kampen, Anna Geletka, Sabrina Ahmad McCollough, Claire Speirs, Shuba Bindra, Meredith Palmer, Agnieska Sukiennik, Tejal Chande, and Anjal Chande have all been wonderful and supportive friends. I am also grateful to Caleb Bullock, Gracie Bullock, and Nathan Cooke Moussopo for providing stress relief, and Sirius, Maise, Stitchy, and Cleo for being my furry dissertation assistants. I am also appreciative of the support of my family, including my sister, Belinda Rodrigues, and my father Roger Rodrigues. My father has been supportive of my decision to study monkeys, even though he still wishes I had gone to medical school instead. And finally, I want to thank all the spider monkeys who helped contribute to this project. Goldie, Clydette, Travis and Udi inspired me to study spider monkeys, and Rita, Marielita, Margarita, Evita, and Chita provided behavioral data and fecal samples. Most of