THE NIGHT SHIFT: LIGHTING AND NOCTURNAL STREPSIRRHINE CARE IN ZOOS by GRACE FULLER Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy Dissertation Advisor: Dr. Kristen E. LuKas Department of Biology CASE WESTERN RESERVE UNIVERSITY January 2014 CASE WESTERN RESERVE UNIVERSITY SCHOOL OF GRADUATE STUDIES We hereby approve the dissertation of Grace Fuller, candidate for the Doctor of Philosophy degree*. Signed: _________________________________________________ Kristen E. Lukas, Ph.D. (chair of the committee) _________________________________________________ Mark Willis, Ph.D. _________________________________________________ Mary Ann Raghanti, Ph.D. _________________________________________________ Patricia M. Dennis, D.V.M., Ph.D. _________________________________________________ Christopher W. Kuhar, Ph.D. Date: 10 October 2013 * We also certify that written approval has been obtained for any proprietary material contained within. Dedicated to: Rene Culler, my mother and my role model; my father Charles Fuller, who would have been so proud; and all the big-eyed friends I made along the way. TABLE OF CONTENTS AcKnowledgments vii Abstract xii Chapter 1. Introduction: Light, Activity Patterns, and the Exhibition of 1 Nocturnal Primates in Zoos Chapter 2. A Survey of Husbandry Practices for Lorisid Primates in 30 North American Zoos and Related Facilities Chapter 3. A Retrospective Review of Mortality in Lorises and Pottos 57 in North American Zoos, 1980-2010 Chapter 4. Validating Actigraphy for Circadian Monitoring of Behavior 90 in the Pygmy Loris (Nycticebus pygmaeus) and Potto (Perodicticus potto) Chapter 5. Methods for Measuring Salivary Melatonin in the Potto, 113 Perodicticus potto, and Pygmy Loris, Nycticebus pygmaeus Chapter 6. A Case Study Comparing Hormonal and Behavioral 135 Responses to Red and Blue Exhibit Lighting in the Aye-Aye, Daubentonia madagascariensis Chapter 7. A Comparison of Nocturnal Strepsirrhine Behavior in 148 Exhibits Illuminated with Red and Blue Light Chapter 8. Endocrine Responses to Exhibit Lighting in the Potto, 175 Perodicticus potto Chapter 9. General Discussion 195 Appendix I. Questions for Multi-Institutional Husbandry Survey 200 Appendix II. Detailed Tables for Cause of Death in Lorisid Primates by 202 Species and Age Group References 208 i LIST OF TABLES Chapter Two Table 1. Group compositions of lorisid primates in North American facilities. 37 Table 2. Enclosure design features of lorisid primates in North American 40 facilities. Table 3. Lighting design of the primary enclosure. 43 Table 4. Animal care practices. 45 Table 5. Estimated reproductive success of lorisid primates. 49 Chapter Three Table 1. Recorded type of death for lorises and pottos in North American 63 facilities 1980-2010. Table 2. Distribution of loris and potto deaths by age class in North American 64 facilities 1980-2010. Table 3. Primary cause of death or reason for euthanasia in lorises and pottos 67 housed in North American facilities 1980-2010. Table 4. Percent of lorises and pottos with pathology diagnosed by organ 69 system upon postmortem examination 1980-2010. Table 5. Neoplasia reported for lorises and pottos in North American facilities 74 1980-2010. Table 6. Circumstances surrounding traumas related to death in lorises and 80 pottos in North American zoos 1980-2010. ii Chapter Four Table 1. Ethogram for behavioral data collection for actigraph study. 99 Chapter Six Table 1. Ethogram for behavioral data collection on the aye-aye. 138 Chapter Seven Table 1. Nocturnal strepsirrhine subjects and housing conditions for the 154 multi-zoo study. Table 2. Ethogram for behavioral data collection. 158 Chapter Eight Table 1. Nocturnal strepsirrhine subjects and housing conditions for the 181 multi-zoo study. iii LIST OF FIGURES Chapter Two Figure 1. Age pyramids for lorisid primates in North American institutions. 38 Figure 2. Primary enclosure size for lorisid primates in North American 41 facilities. Chapter Four Figure 1 a-b. a) Attaching the actigraph harness to the pygmy loris subject; b) 95 the potto wears the actigraph harness on exhibit. Figure 2. General activity budget for the potto subject with and without the 101 actigraph harness in place. Figure 3. General activity budget for the pygmy loris subject with and without 103 the actigraph harness in place. Figure 4. Actigraph data for the potto subject. 105 Figure 5. Actigraph data for the pygmy loris subject. 106 Figure 6. Mean activity counts associated with behaviors observed in a potto 107 and a pygmy loris. Chapter Five Figure 1. Collection of saliva from the female potto. 118 Figures 2 a-c. Melatonin concentrations measured following nocturnal 127 exposure to test lights in a potto (a), and pygmy lorises PSL1 (b) and iv PSL2 (c). Figure 3. 24-hour patterns of salivary melatonin expression in a potto and 130 three pygmy lorises (PSL). Chapter Six Figure 1. Daily time of emergence from the nest box by the aye-aye subject 140 based on keeper reports. Figure 2. Time spent performing active behaviors (move, feed, self-directed, or 141 object examination) by the aye-aye subject during the baseline red and experimental blue lighting conditions. Figure 3. Dark phase activity budget (1000-2200 hrs) for the aye-aye subject 142 during the baseline red and experimental blue lighting conditions. Figure 4. DarK phase salivary melatonin concentrations in the aye-aye during 144 the baseline red and experimental blue lighting conditions. Figure 5. Salivary cortisol rhythms in the aye-aye during the baseline red and 146 experimental blue conditions. Chapter Seven Figure 1 a-b. Percent of time spent performing active behaviors during the darK 162 phase by animals at Cleveland MetroparKs Zoo (a) and Cincinnati Zoo and Botanical Garden (b). Figure 2 a-d. Changes in behavior across the three study conditions (C1-3) 164 comparing red and blue light for pottos (a) and pygmy slow lorises v (b) at Cleveland MetroparKs Zoo (CMZ) and pottos (c) and a bamboo lemur (d) at Cincinnati Zoo and Botanical Garden (CZBG). Figure 3 a-c. 24-hour activity level data for potto PP2 (a) and pygmy slow 167 lorises NP1 (b) and NP2 (c) (see Table 1 for subject IDs) at Cleveland Metroparks Zoo. Chapter Eight Figure 1 a-c. Melatonin concentrations measured in potto saliva six hours after 185 dark phase onset in red and blue light. Figure 2. Scatterplot of light intensity compared to salivary melatonin 186 concentrations measured in pottos at six hours after darK phase onset. Figure 3. Salivary cortisol concentrations measured in pottos living in blue and 188 red dark phase lighting conditions. vi Acknowledgments It is humbling to looK bacK over these many years and contemplate how many people contributed to my development as a scientist as well as to the body of worK I am offering here. First and foremost, I would liKe to thanK my dissertation advisor, Dr. Kristen LuKas. Meeting Kristen inspired me to pursue a path of study examining the care of animals in captivity. Over the years she has been a mentor and a friend, and I am a better person and scientist for having Known her. All of my committee members have had a profound influence on how I see the world and have also been a source of great strength and support throughout the process of completing my dissertation research. I am grateful to Dr. Mary Ann Raghanti for her years of friendship and encouragement, for believing in me, and always reminding me to thinK liKe an anthropologist. I am grateful to Dr. Pam Dennis for pushing me to asK hard questions and for encouraging me to believe that I could acquire the sKills to answer them, and for always reminding me to stand up for the little guys. I am grateful to Dr. Chris Kuhar for pushing me to strive for both scientific rigor and practicality in my research endeavors. Not only did Dr. MarK Willis teach me to thinK liKe a scientist, he also demonstrated what it means to be a great teacher both in and outside the classroom. Finally, Dr. Mandi VicK selflessly gave me so much guidance, personally and professionally, that I will always consider her an honorary part of my committee. I looK forward to many years of friendship and collaboration with you all. I am also grateful to my academic peers and friends for their support and encouragement over these many years. Dr. Elena Less was a source of inspiration to vii me for both her worK ethic and her Kindness, and I am so grateful for all the experiences we had together as students. Jason WarK made me laugh every day, and pushed me to thinK critically and have fun doing it. Christine Cassella was also a great source of friendship and support, and an inspiration for how to live a better life. I am incredibly grateful to Austin Leeds for his assistance in collecting saliva samples for this research, as I truly could not have done it without his help. Bonnie Baird is going to do great things and I will remember that I Knew her when. I look forward to many years of friendship and collaboration with you all as well, and I cannot wait to see all the amazing contributions that you maKe to our field. Working in the Conservation and Science area at Cleveland Metroparks Zoo was amazing because literally everyone I worked with was wonderful. Laura Amendolagine is a top-notch laboratory manager and therapist and has the biggest heart of anyone I know. I will always remember fondly our time worKing in the lab together. I am also grateful to Kym Gopp for her dedication to loris conservation and for offering me opportunities to contribute, in some small way, to this goal. Finally, I am grateful that I met Sonia DiFiore there too. Of course there are many other staff members at the zoo that I would like to thanK for their assistance with my research, especially BecKy Johnson, Dawn Stone, and Andrew Smyser, who put in many, many hours of worK to assist in my research efforts all while providing exceptional care to the lorises and many other animals.