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Nutritional Strategy and Social Environment in Redtail Monkeys (Cercopithecus Ascanius)

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City University of New York (CUNY) CUNY Academic Works All Dissertations, Theses, and Capstone Projects Dissertations, Theses, and Capstone Projects 2-2020 Nutritional Strategy and Social Environment in Redtail Monkeys (Cercopithecus ascanius) Margaret Bryer The Graduate Center, City University of New York How does access to this work benefit ou?y Let us know! More information about this work at: https://academicworks.cuny.edu/gc_etds/3554 Discover additional works at: https://academicworks.cuny.edu This work is made publicly available by the City University of New York (CUNY). Contact: [email protected] NUTRITIONAL STRATEGY AND SOCIAL ENVIRONMENT IN REDTAIL MONKEYS (CERCOPITHECUS ASCANIUS) by MARGARET A. H. BRYER A dissertation submitted to the Graduate Faculty in Anthropology in partial fulfillment of the requirements for the degree of Doctor of Philosophy, The City University of New York 2020 i © 2020 MARGARET A. H. BRYER All Rights Reserved ii Nutritional strategy and social environment in redtail monkeys (Cercopithecus ascanius) by Margaret A. H. Bryer This manuscript has been read and accepted for the Graduate Faculty in Anthropology in satisfaction of the dissertation requirement for the degree of Doctor of Philosophy. December 6, 2019 Jessica M. Rothman Chair of Examining Committee December 6, 2019 Jeff Maskovsky Executive Officer Supervisory Committee: Larissa Swedell Andrea L. Baden Marina Cords David Raubenheimer THE CITY UNIVERSITY OF NEW YORK iii ABSTRACT Nutritional strategy and social environment in redtail monkeys (Cercopithecus ascanius) by Margaret A. H. Bryer Advisor: Jessica M. Rothman An animal’s nutritional strategy involves the complex interplay between its dynamic physiology and its environment, an environment that includes a landscape of foods that vary in nutritional composition as well as a social environment of other feeding individuals. Social behavior—cooperative or competitive, with conspecifics or with other sympatric species— influences individual feeding behavior. Investigation of social feeding by estimating individual intake of multiple nutritional components, sometimes referred to as “social nutrition,” can give insight into how social variables may lead to shifts in nutritional niche. In this study, I examined the effects of temporal shifts in diet, reproductive status and conspecific and heterospecific social factors on the nutritional intake of an arboreal guenon. This study draws from 137 full-day focal follows of adult female redtail monkeys (Cercopithecus ascanius) in three study groups in Kibale National Park, Uganda; phenological data from the monkey group home ranges; insect abundance data via malaise trap and sweep net methods; nutritional wet chemistry or near-infrared reflectance spectroscopy (NIRS) analyses of over 600 food samples; and mineral analyses via inductively coupled plasma optical emission spectroscopy (ICP-OES) of 101 food samples. I first characterized the redtail nutritional strategy as it relates to fruit in the diet, monkey group and reproductive status. I found that redtail monkeys are “food composition generalists,” iv consuming food items that are diverse in macronutrient and mineral composition. Insects were modest contributors to metabolizable energy and protein in the redtail diet, given that time spent feeding on insects was comparable to fruits, but insects contributed substantially to mineral intake. The balance of dietary nonprotein energy to available protein (NPE:AP) of redtail females was similar to other omnivorous primates. Redtail daily fat intake varied the most, while protein varied the least, indicating protein regulation. Redtail female nutritional strategy was affected by habitat variation in their home ranges, while ripe fruit in the diet or reproductive status did not have a strong effect on nutrition. One redtail group relied on the fruit and gum of Prunus africana, a high density tree in disturbed areas, which led to higher dietary NPE:AP than the other groups. Increased switching among foods was associated with increased sodium, copper and iron intake, suggesting that diet diversity and rapid food switching enable increased consumption of minerals. Second, I examined the relationship between redtail female agonism and nutritional strategy. Redtail monkey females exhibited low levels of within-group female agonism compared to other cercopithecines. Intragroup agonism was mostly in a feeding context, suggesting that some intragroup contest competition occurs. A relationship between agonism during feeding and daily nutritional intake could not be detected for multiple macronutrients and energy. Foods that female redtail monkeys contested over were diverse in food type and in macronutrient and mineral composition. Though nutritional effects of intragroup food competition were not detectable at the daily scale, future work should examine the level of the food patch when short-term nutritional costs may occur. Alternatively, group membership as it relates to being able to defend a food resource as a group may be more relevant to nutritional shortfalls than an individual’s ability to compete with another individual over food. v Third, I examined how polyspecific association affects female redtail daily nutritional intake. The redtail study groups varied in polyspecific association patterns and partners. I could not detect a relationship between polyspecific association with blue monkeys (Cercopithecus mitis) or grey-cheeked mangabeys (Lophocebus albigena) and redtail daily food intake, total metabolizable energy, nonprotein energy, sodium, or copper, regardless of shifts in dietary ripe fruit. An established interspecific dominance hierarchy by body size at feeding trees leading to spatial adjustments and mitigating interspecific competition may help explain this result. Food over which redtails and heterospecifics contested did not fit one nutritional profile and were instead diverse in macronutrient and mineral composition. I was unable to find a statistically clear relationship between red colobus monkey (Procolobus rufomitratus) polyspecific association and redtail female intake of macronutrients or energy, which was expected given redtail-red-colobus lower dietary overlap than frugivores. Though I could not detect a relationship between red colobus monkey polyspecific association and redtail daily intake of sodium from insects, future work will address questions of insect feeding efficiency and red colobus potential flushing of insects for redtails. Redtail monkeys combine foods of diverse nutritional composition and use fat, digestible fiber and nonstructural carbohydrates interchangeably as energy sources. This study characterizes the diet of a generalist forest guenon, clarifies the mineral-driven role that insects play in the redtail monkey diet, and suggests that redtail females may suffer minimal daily nutritional costs of intragroup agonism and of polyspecific association. vi ACKNOWLEDGEMENTS First, a huge thank you to my adviser Jessica Rothman for her guidance and support throughout this long process. She provided me with incredible opportunities in the field and in the nutritional chemistry laboratory. The attentive and thorough training she offered me on research and scientific writing, as well as her candid approach to advising her students in the ways of academia, have been crucial to my professional development. I am grateful for her guidance in completing three degrees over the past ten years. I am also grateful to the other members of my dissertation committee who have provided insight and feedback on my dissertation: Larissa Swedell, Andrea Baden, Marina Cords, and David Raubenheimer. I thank Larissa for her primate social behavior expertise and her feedback on my dissertation at multiple stages, including at the proposal stage. Thank you to Andrea for her thoughtful input and behavioral ecology expertise, as well as for raising landscape-level questions. Thank you to Marina for her guenon and social behavior expertise and her guidance from proposal to final product. Thank you to David for his enthusiasm in discussing my project with me and guidance on Nutritional Geometry. Thank you to additional members of my proposal committee who improved my project in preparation for grant applications: Chris Gilbert and Herman Pontzer. Thank you to Mike Steiper for his professional advice as I more recently entered the job market. I sincerely thank the Ugandan field assistants who made my project possible with their exceptional knowledge of Kibale National Park’s flora and fauna: Hillary Musinguzi and Sabiiti Richard showed tremendous dedication to the redtail monkey project. Thank you also to Richard Kaseregenyu and Patrick Ahabyoona for additional assistance with behavioral data collection, Peter Irumba for assistance in phenology data collection, and James Magaro and Francis Katuramu for assistance in field-lab work. vii I am very grateful to the Uganda Wildlife Authority and the Uganda National Council for Science and Technology for permission to conduct this research in Kibale National Park. Thank you also to Makerere University Biological Field Station for accommodations during my field seasons. This work was made possible through support from the National Science Foundation (Doctoral Dissertation Research Improvement Grant NSF BCS 1540369 and NSF BCS 1521528), Hunter College of the City University of New York, The Graduate Center of the City University of New York, and the New York Consortium in Evolutionary Anthropology
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