AMBASSADOR ANIMAL WELFARE: USING BEHAVIORAL AND PHYSIOLOGICAL INDICATORS TO ASSESS THE WELL-BEING OF ANIMALS USED FOR EDUCATION PROGRAMS IN ZOOS by BONNIE ANN BAIRD Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Biology CASE WESTERN RESERVE UNIVERSITY May 2018 CASE WESTERN RESERVE UNIVERSITY SCHOOL OF GRADUATE STUDIES We hereby approve the dissertation of Bonnie Ann Baird, candidate for the degree of Doctor of Philosophy* Mandi W. Schook, Ph.D. Committee Chair Kristen E. Lukas, Ph.D. Committee Member Mark A. Willis, Ph.D. Committee Member Nadja C. Wielebnowski, Ph.D. Committee Member Christopher W. Kuhar, Ph.D. Committee Member Date of Defense: 19 March 2018 *We also certify that written approval has been obtained for any proprietary material contained therein. ii To my dad, who taught me to love and respect all creatures great and small, and raised me to believe that I could be anything. I miss you every day, but I know you’ll be with me in all my future adventures. iii TABLE OF CONTENTS List of Tables. …………………………………………………………………………… ii List of Figures. ………………………………………………………………………….. iii Acknowledgements. …………………………………………………………………….. iv Abstract. …………………………………………………………………………………. 1 Chapter One: Introduction. …………………………………………………………….. 3 Chapter Two: The influence of management role and handling on indicators of welfare in armadillos, hedgehogs, and red-tailed hawks. ………………………………. 37 Chapter Three: Personality assessment in zoo-housed cheetahs. …………………….. 75 Chapter Four: Assessing welfare in zoo-housed cheetahs in different management roles. … 93 Chapter Five: General discussion and future directions. ……………………………. 133 Appendix I: Husbandry and demographic survey used for cheetahs. ……………….. 141 Appendix II: Cheetah personality survey. …………………………………………… 143 Appendix III: Daily log form used to record human interaction, exercise, and enrichment in cheetahs. ……………………………………………………………………. 145 References. …………………………………………………………………………… 146 i LIST OF TABLES Chapter Two: Table 2.1: Husbandry and demographic factors for armadillos in Experiment One. …. 43 Table 2.2: Husbandry and demographic factors for species in Experiment Two. …….. 44 Table 2.3: A) Ethogram used for behavioral data collection on armadillos, hedgehogs, and red-tailed hawks for both Experiment One and Experiment Two. B) Modifications to the “Rest” category used when collecting behavioral data in hawks. ………………………………………………………………………….. 49 Chapter Three: Table 3.1: Subjects, raters, and institutional reliability used in the cheetah personality assessment. ……………………………………………………………………... 79 Table 3.2: Behavioral definitions of adjectives used in personality questionnaire. …… 80 Table 3.3: Factor loadings for four components of cheetah personality identified through Principal Components Analysis. ……………………………………………….. 86 Chapter Four: Table 4.1: Husbandry and demographic factors measures in 73 cheetahs. ……………. 97 Table 4.2: Broad categories used to classify human interaction, exercise, and enrichment for comparison across institutions. …………………………………………… 100 Table 4.3: Ethogram used for behavioral data collection in cheetahs. ………………. 104 Table 4.4: Fixed factors analyzed in relation to FGM and behavior using linear mixed models. ………………………………………………………………………... 108 ii LIST OF FIGURES Chapter Two: Figure 2.1: FGM concentrations in response to an ACTH injection in armadillos (A-C) and a red-tailed hawk (D) and FGM concentrations in response to a veterinary exam in a hedgehog (E). ………………………………………………………………………. 55 Figure 2.2: Box plots representing average corticosterone concentrations of education, exhibit, and off exhibit armadillos. ………………………………………………… 56 Figure 2.3: Comparison of individual behaviors between education, exhibit, and off exhibit armadillos. ……………………………………………………………… 59 Figure 2.4: Mean (+SEM) FGM concentrations for four La Plata armadillos (A, B, C, D) during the three phases of Experiment Two. ………………………………………. 61 Figure 2.5: Individual differences in mean FGM concentrations for six representative African hedgehogs in each phase of Experiment Two. …………………………………………. 63 Figure 2.6: Average (+SEM) FGM levels in two representative red-tailed hawks during each three-week phase of Experiment Two. ………………………………………………… 64 Chapter Four: Figure 4.1: Least-square mean (± 95% CI) FGM concentrations for cheetahs in different management roles. ……………………………………………………………. 114 Figure 4.2: Interaction between dominant personality and on-exhibit housing on FGM concentrations. ………………………………………………………………... 116 Figure 4.3: Box Plots representing the relationship between primary management role and behavioral diversity scores. ………………………………………………. 118 Figure 4.4: Scatter plots of behavioral diversity scores and A) average and B) baseline FGM concentrations for 39 cheetahs, separated by sex. ……………………………………. 120 iii ACKNOWLEDGEMENTS I will always be grateful to all those that guided and supported me along this journey that has been full of the highest of highs and the lowest of lows. First and foremost, I need to thank my wonderful husband, Tommy Klypchak for your unconditional love and patience for the last 15(!) years. Having you as my solid rock at home has enabled me to fly and reach for my dreams. You are truly the most caring and selfless person I have ever met, and I am so lucky to have you in my corner. There’s no one I would rather partner with on this crazy journey of life, and I can’t wait to see what the future has in store for us! I have to acknowledge my advisor, Dr. Kristen Lukas. You have played such a major role in who I am today, both personally and professionally. I am eternally grateful for your guidance and friendship, and for all of the heart to heart talks. Thanks to you, I was able to do something I never thought I would be able to – travel to Africa (three times!). Part of me still can’t believe that this girl from North Ridgeville, Ohio was able to have such an amazing opportunity and the other part can’t wait to go back. I still have to see wild elephants! Thank you for helping to make my dreams a reality and enabling me to develop my skills and use them to make a difference in the world. I have also been so fortunate to have a committee full of supportive and brilliant scientists. I’m grateful for the advice and expertise of Dr. Nadja Wielebnowski throughout this process. Despite being on the other side of the country, she has always been ready and willing to answer my endless questions, and I truly appreciate that. Dr. Mark Willis, thanks for all the great conversations and advice and for recognizing iv something in me that I didn’t even see in myself yet. Your guidance and advice has meant more to me than you know. Finally, despite technically only serving in an “advisory role” on my committee for the last 6 years, Dr. Chris Kuhar has never missed a committee meeting or failed to provide feedback on anything I’ve sent him, even with all the responsibilities of a zoo director. Thank you all for taking the time to help develop me into a professional in this field. I hope I can make you proud! None of this would have been possible without my friends and colleagues at Cleveland Metroparks Zoo. A very special thank you to Laura Amendolagine, the Endocrinology Lab Manager for your endless patience, expertise, and for always finding a place in the freezer for thousands of poop samples and making sacrifices to the Assay Gods with me. Thank you to Ingrid Rinker and Elaine Leickly for volunteering to spend your retirement years crushing fecal samples, and always smiling about it. To all the keepers and curators, especially Andi Kornak, Travis Vineyard, Tad Schoffner, Elena Less and the PCA team, and Chris Peterson and the rest of the elephant team, your leadership, passion, and dedication to your work is inspiring. I have thoroughly enjoyed working with and learning from each of you. You have all helped me to become a better scientist and a better zoo professional. I look forward to continuing to work with you all in the future. To my academic brothers and sisters that I’ve shared an office with, Dr. Grace Fuller, Dr. Jason Wark, Austin Leeds, and Laura Bernstein-Kurtycz, thank you for your personal and professional support, for the intellectual and not so intellectual conversations, and most importantly, for your friendship. To my primary advisor, Dr. Mandi Schook, I don’t think there are enough words to express how grateful I am for all you’ve done to help me grow. Thank you for taking a v chance on me and for never letting me give up. Thanks to you, I have transformed from someone who likes animals and behavior to a multidisciplinary scientist. Your guidance has helped me to accomplish things that I never thought I could, and I can’t wait to see what the future holds for me. I’m grateful to call you a colleague and a friend. Thank you for being you. Finally, I want to thank all the staff, students, and volunteers that collected data at each participating institution to make this research possible: Cleveland Metroparks Zoo, Akron Zoo, Bergan County Zoo, Binder Park Zoo, Busch Gardens Tampa, Cincinnati Zoo and Botanical Garden, Columbus Zoo and Aquarium, Denver Zoo, Florida Aquarium, Fresno Chaffee Zoo, The Good Zoo at Oglebay, Happy Hollow Park and Zoo, Jacksonville Zoo, Lincoln Park Zoo, Tampa’s Lowry Park Zoo, Memphis Zoo, Oregon Zoo, Peoria Zoo, Philadelphia Zoo, Point Defiance Zoo and Aquarium, San Antonio Zoo, Seneca Park Zoo, Smithsonian’s National Zoo and Conservation Biology Institute, Toronto Zoo, Wildlife Safari, The Wilds, Zoo Atlanta, and Zoo Miami. This research was also funded in part by the Association of Zoos and Aquariums Conservation Grants Fund. vi Ambassador Animal Welfare: Using Behavioral and Physiological Indicators to Assess the Well-Being of Animals Used for Education Programs in Zoos. By BONNIE ANN BAIRD Abstract Modern accredited zoos strive to adhere to the highest standards of animal care while simultaneously providing meaningful educational experiences for their guests. One avenue where these goals intersect is the widely employed practice of using ambassador animals in education and outreach programs.