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Gorilla Gorilla Gorilla) A PHYSIOLOGICAL EVALUATION OF SOCIAL BONDING IN WESTERN LOWLAND GORILLAS (GORILLA GORILLA GORILLA) by CHARLES AUSTIN LEEDS Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Biology CASE WESTERN RESERVE UNIVERSITY MAY 2019 CASE WESTERN RESERVE UNIVERSITY SCHOOL OF GRADUATE STUDIES We herby approve the dissertation of Charles Austin Leeds, candidate for the degree of Doctor of Philosophy* Kristen E. Lukas, Ph.D. Committee Chair Mandi W. Schook, Ph.D. Committee Member Patricia M. Dennis, DVM, Ph.D. Committee Member Mark A. Willis, Ph.D. Committee Member Tara S. Stoinski, Ph.D. Committee Member Date of Defense: 22 Month 2019 *We also certify that written approval has been obtained for any proprietary material contained therein. Dedicated to: Washoe, Dar, Tatu and Loulis – you four changed my life and perspective for the better. I will forever be grateful for knowing you. TABLE OF CONTENTS List of Tables.......................................................................................................................ii List of Figures.....................................................................................................................iii Acknowledgements.............................................................................................................iv Abstract................................................................................................................................1 Chapter One: Introduction.................................................................................................3 Chapter Two: Validating the use of a commercial enzyme immunoassay to measure oxytocin in unextracted urine and saliva of the western lowland gorilla (Gorilla gorilla gorilla)...............................................................................................................................34 Chapter Three: Evaluating changes in salivary oxytocin and cortisol following positive reinforcement training in two adult male western lowland gorillas (Gorilla gorilla gorilla) ..............................................................................................................................69 Chapter Four: Urinary oxytocin concentrations vary by social demographic, reproductive and developmental factors in western lowland gorillas (Gorilla gorilla gorilla)...............................................................................................................................77 Chapter Five: Evaluating the relationship between animal care-staff perceptions of group-level social bonding and urinary oxytocin concentrations of western lowland gorillas (Gorilla gorilla gorilla)......................................................................................114 Chapter Six: General discussion and future directions..................................................136 References.......................................................................................................................146 i LIST OF TABLES Chapter Three: Table 3.1 Comparison of salivary oxytocin and cortisol concentration by subject and condition................................................................................................................72 Chapter Four: Table 4.1 Fixed factors tested in linear mixed models......................................................89 Table 4.2. Linear mixed model output for evaluations of uOXT in the entire study population (model 1), the female study population (model 2), the adult female study population, the entire male study population (model 4), the bachelor group study population (model 5) and the adult male in mixed-sex groups study population (model 6)..............................................................................................92 Chapter Five: Table 5.1. Survey question information..........................................................................120 Table 5.2. Comparison of mean survey scores by group type........................................125 Table 5.3. Comparison of mean survey scores within bachelor groups..........................125 Table 5.4. Comparison of mean survey scores within mixed-sex groups.......................126 ii LIST OF FIGURES Chapter Two: Figure 2.1: Parallelism of oxytocin standards and pooled samples from (A) unextracted urine, (B) extracted urine), (C) unextracted saliva and (D) extracted saliva.........50 Figure 2.2: Urinary oxytocin concentrations for samples that were simultaneously assayed using both an extraction process and without...........................................51 Figure 2.3: Urinary oxytocin concentrations prior to and following the intranasal challenge................................................................................................................52 Figure 2.4: Salivary oxytocin concentrations prior to and following the intranasal challenge................................................................................................................53 Figure 2.5: Urinary oxytocin concentrations for ten matched morning and afternoon samples ..................................................................................................................54 Figure 2.6: Diurnal variation in mean salivary oxytocin concentration (± SE) per gorilla (n =3 saliva samples per time point/gorilla)..........................................................55 Figure 2.7: Salivary oxytocin concentrations of Mokolo were compared 15 min post- breeding with an adult female gorilla to a match-control sample for each respective post-breeding sample (n = 5)................................................................56 Figure 2.8: Salivary oxytocin concentrations following two consecutive play bouts......57 Figure 2.9: Urinary oxytocin concentrations of Mokolo before and after the loss of his groupmate..............................................................................................................58 iii Chapter Three: Figure 3.1. Salivary oxytocin concentrations before and after positive reinforcement training...................................................................................................................73 Figure 3.2 Salivary cortisol concentrations of Mokolo before and after positive reinforcement training…………………………………………..………………..74 Chapter Four: Figure 4.1. Estimated marginal mean (EMM) urinary oxytocin (uOXT) concentration varied by age class and by the interaction of sex and age class.............................95 Figure 4.2. Comparison of estimated marginal mean (EMM) urinary oxytocin (uOXT) of adult female gorillas. Lactating females had significantly greater uOXT than non-lactating females (A). Females not using hormonal contraception (HC) had significantly greater uOXT than those using HC (B). Lastly, females in groups containing an adult conspecific raising an offspring had significantly lower uOXT than females in groups without an adult conspecific raising an offspring (C)..........................................................................................................................98 Figure 4.3. Group-type was a significant predictor of male urinary oxytocin (uOXT) concentration. Parwise comparisons found estimated marginal mean (EMM) concentrations were greater in males living in fission-fusion and bachelor groups than males living in mixed-sex groups or as solitary individuals (P ≤ 0.05).......100 Figure 4.4. Estimated marginal mean (EMM) urinary oxytocin (uOXT) variation in male gorillas living in bachelor groups. Male gorillas in groups containing a young silverback (YSB) had significantly lower uOXT than males in groups without a iv YSB (A). Males in mixed-generation groups, groups containing at least one male in a different age class than the rest of the group, had significantly greater uOXT than males in single-generation groups, groups containing males all in the same age class (B).........................................................................................................102 Chapter Five: Figure 5.1. Peripheral status was associated with significantly lower urinary oxytocin (pg/mg CR) concentrations in all mature (≥14 yrs) females (A) and all non- lactating, mature females (B)...............................................................................130 v ACKNOWLEDGEMENTS First and foremost I would like to thank my parents, Karen and Al, for always supporting me. I would not have been able to accomplish any of this without them. I also can’t thank my wife, Dawn, enough for all her support and patience through this process. Thank you for always being there for me. I had the amazing opportunity to work at the Chimpanzee-Human Communication Institute for six years before starting my PhD. I worked with some great people, but I can’t thank Dr. Mary Lee Jensvold enough for encouraging me to pursue graduate school. It was never a thought in my mind before we discussed it. Thank you Mary Lee for encouraging me to push myself. I had the privilege of being mentored by many zoo professionals while in Cleveland. It would take a second dissertation to properly document everything, but in short I can’t thank Dr. Elena Less, Tad Schoffner, Travis Vineyard, Andi Kornak and the Primate, Cat and Aquatics keepers enough for all they have taught me. Many thanks go to the Conservation & Science team I had the opportunity to work with. I would not have accomplished much in the endocrinology lab if it were not for the help of Laura Amendolagine. I also appreciate
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