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Self-Enurination in the Domesticated Male Goat (Capra Hircus)

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Self-Enurination in the Domesticated Male Goat (Capra Hircus) SELF-ENURINATION IN THE DOMESTICATED MALE GOAT (CAPRA HIRCUS) by WILLIAM F. FRITZ JR. A dissertation submitted to the Graduate School-New Brunswick Rutgers, The State University of New Jersey In partial fulfillment of the requirements For the degree of Doctor of Philosophy Graduate Program in Endocrinology and Animal Biosciences Written under the direction of Dr. Larry S. Katz And approved by _____________________________________ _____________________________________ _____________________________________ _____________________________________ New Brunswick, New Jersey May 2017 ABSTRACT OF THE DISSERTATION SELF-ENURINATION IN THE DOMESTICATED MALE GOAT (CAPRA HIRCUS) By: WILLIAM F. FRITZ JR. Dissertation Director: Dr. Larry S. Katz The sexual behavior of the female goat has been researched extensively to solve reproductive efficiency issues in the agricultural setting. Traditionally, the sexual behavior of the male goat has not been as well understood. The male goat is often dismissed for having an insatiable sexual appetite and thus not a problem worthy of inquiry. More recently, studies on low-performing males in closely related domesticated species have opened the door for the study of sexual behavior in male ruminants. Among the less understood behaviors of the male ruminant, the male goat is known to display a behavior known as self-enurination. Self-enurination is displayed in male domesticated goats characterized by the downward turning of the head and neck to intercept the stream of urine from the erect penis resulting in the application of urine to the face, beard and posterior surface of the forelegs. While many hypotheses on the etiology of such a behavior have been proposed, none have been demonstrated through experimentation. While the behavior appears to be involved in olfactory communication, it is not clear whether the behavior is directed at females or other males of the same species. Knowing that the behavior is testosterone-dependent, displayed much more frequently during the breeding season and evoked by sexual stimuli, suggests a reproductive function. On the ii contrary, the behavior is elicited in the absence of females, so it is also believed to have social implications. By developing a set of social and physical environmental conditions capable of reliably producing bouts of self-enurination, hypotheses directed at understanding the behavior’s purpose have been tested. Findings are relevant to the production industry in the development of natural and less invasive breeding practices and also provide a better understanding of goat sexual behavior necessary to improve husbandry techniques. Also, this work contributes to the field of chemical communication through the study of a domesticated species still subject to natural selection, even after thousands of years of domestication in relatively intensely managed herds. iii DEDICATION I dedicate this to my advisor, mentor, committee member and friend, Linda Smith, who passed away in 2015. Linda was the person who inspired me to pursue a career in science and to attend Rutgers, where she had completed her Ph.D. To my parents Susan and William Fritz, for supporting me and affording me the opportunities that lead me to where I am today. They raised me to dream big, and work hard and it has made all the difference. To my wife Michelle, for her love, support, encouragement and for keeping me grounded. To my sister Jennifer, for her support and friendship To all of my extended family and friends, for their generous love and support. iv ACKNOWLEDGEMENTS I would like to express my most sincere gratitude to my graduate research advisor, Larry S. Katz for affording me the opportunity to pursue my degree working in his lab. Over the years, Larry has taught me many important lessons that apply not only in the lab, but in life. He has been an invaluable teacher, mentor and friend and I will carry his wisdom with me forever. I would also like to thank my committee members, Drs. Michael Sukhdeo, Michael Westendorf and George Wagner for their guidance and contributions. I would especially like to thank Susan Becker for the countless hours she has spent teaching me, helping me at the barn, organizing the lab, or just chatting about research and life. She has been jokingly referred to as my “lab mother,” but after five years together, I would call her a lifelong friend. A special thanks to Rebecca Potosky, Laura Comerford, Felicia Kleiman and Clint Burgher for all of their work on the farm that makes our research run smoothly. Finally, I would like to thank all of the undergraduate research students that have assisted with my work, especially Hanna Canfield, Tonya Ternova, Meg Radford, Cynthia Xue, Lena Sena, Caitlin Kober and Emily Convery. v TABLE OF CONTENTS Title ABSTRACT OF THE DISSERTATION ii DEDICATION iv ACKNOWLEDGMENTS v TABLE OF CONTENTS vi LIST OF TABLES ix LIST OF FIGURES x TABLE OF ABBREVIATIONS xiii INTRODUCTION 1 CHAPTER I Review of Literature 3 A. Purpose and scope of the literature review 4 B. Sexual behavior of the male goat 5 C. The male effect 8 D. Scent of a buck 10 E. Sebaceous gland secretions 10 F. Urine in scent-marking and sexual behavior 13 G. Caprine olfactory perception 14 H. The flehmen response 14 I. The accessory olfactory system 15 J. Taxonomic prevalence and permutations of self-enurination 17 vi TABLE OF CONTENTS (continued) K. Importance of self-enurination to the goat 19 L. Behavioral scenarios that evoke self-enurination 20 M. Endocrine influence of self-enurination 20 N. Predictions on purpose and origin of self-enurination 21 O. Relevance 25 P. Research objectives and hypotheses 26 Q. References 27 Chapter II Differential effects of androgens, estrogens and socio-sexual context on sexual behaviors in the castrated male goat (Capra hircus) A. Abstract 37 B. Introduction 39 C. Materials and Methods 43 D. Results 48 E. Discussion 50 F. Tables and Figures 56 G. References 66 Chapter III Domesticated male goats use self-enurination to present attractive olfactory cues to estrous females A. Abstract 70 B. Introduction 71 vii C. Materials and Methods 74 D. Results 77 E. Discussion 78 F. Tables and Figures 81 G. References 93 Chapter IV Effects of Simulated self-enurination on reproductive behavior and endocrinology in male goats A. Abstract 97 B. Introduction 99 C. Materials and Methods 109 D. Results 114 E. Discussion 117 F. Figures 124 G. References 136 Chapter V A. Dissertation Conclusions 141 B. References 146 viii LIST OF TABLES Table # Title Page # Chapter II Table 1 Self-enurinations more likely to occur in bucks distanced from 58 does Table 2 Courtship occurs at higher frequencies in bucks with fenceline 59 contact with does Chapter III Table 1 Mean frequency of investigative behaviors in experiment 2 86 ix LIST OF FIGURES Figure # Title Page # Chapter II Figure 1. Buck exhibiting self-enurination 56 Figure 2. Behavior test apparatus for experiment 1 57 Figure 3. Androgens activate self-enurination 60 Figure 4. Estrogens activate courtship 61 Figure 5. Opportunity to court and breed estrous does negatively affects 62 self- enurination frequency in androgen-treated wethers Figure 6. Both hormone treatment and socio-sexual conditions affect 63 courtship Figure 7. Hormone treatments do not affect mounting frequency 64 Figure 8. Hormone concentrations do not affect frequency of ejaculation 65 Chapter III Figure 1. Behavior test apparatus for experiment 1 81 Figure 2. Behavior test apparatus for experiment 2 82 Figure 3. Urine recycling fountain for experiment 2 83 Figure 4. Estrous females spent more time near ovx does carrying buck SE 84 urine than those carrying wether urine Figure 5. Estrous females prefer buck SE urine over wether urine 85 Figure 6. Estrous females spent more time near buck SE urine than wether 87 urine fountain Figure 7. Estrous females prefer buck SE urine over wether urine fountain 88 x LIST OF FIGURES (continued) Figure # Title Figure 8. Time spent near DHT-treated wether urine vs. EB-treated wether 89 urine Figure 9. Estrous females prefer DHT-treated wether urine over EB-treated 90 wether urine Figure 10. Time spent near buck SE urine vs buck plain urine 91 Figure 11. Estrous females prefer Buck plain urine over buck SE urine 92 Chapter IV Figure 1. Testosterone response to simulated SE for all bucks in experiment 124 1 Figure 2. Testosterone response to simulated SE for mature bucks in 125 experiment 1 Figure 3. Proportion of bucks displaying flehmen and mean time spent in 126 flehmen in experiment 2 Figure 4. LH response to simulated SE for bucks in experiment 2 127 Figure 5. LH response to simulated SE for mature bucks in experiment 2 128 Figure 6. Proportion of bucks displaying flehmen and mean time spent in 129 flehmen for experiment 3 during non-breeding season Figure 7. LH response to simulated SE for experiment 3 during non- 130 breeding season Figure 8. Proportion of bucks displaying flehmen and mean time spent in 131 flehmen for experiment 3 during transition into breeding season xi LIST OF FIGURES (continued) Figure # Title Figure 9. LH response to simulated SE for experiment 3 during transition 132 into breeding season Figure 10. Proportion of bucks displaying flehmen and mean time spent in 133 flehmen for experiment 4 Figure 11. LH response to simulated SE for experiment 4 134 Figure 12. T response to simulated SE for experiment 4 135 xii TABLE OF ABBREVIATIONS AOB Accessory Olfactory Bulb Buck Domesticated male goat (Capra hircus) DHT Dihydrotestosterone DHT-P Dihydrotestosterone propionate Doe Intact female domesticated goat (Capra hircus) E Estradiol EB Estradiol benzoate GnRH Gonadotropin releasing hormone HPG Hypothalamic-pituitary-gonadal IZ Incentive Zone LH Luteinizing hormone MOB Main olfactory bulb NZ Neutral zone OVX Ovariectomized SE Self-enurination T Testosterone TP Testosterone propionate VNO Vomeronasal organ Wether Prepubertally castrated male domesticated goat (Capra hircus) xiii 1 INTRODUCTION During the breeding season, the male goat (buck) urinates onto his head and front legs in a behavior known as self-enurination (SE).
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