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Investigating Chemosensory Signals in Wolf Urine Scent-Marking: Investigating chemosensory signals in wolf urine By Wendi K Wolfram Submitted to the University of Exeter As a thesis for the degree of Doctor of Philosophy in Biological Sciences In March 2013 This thesis is available for Library use on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgement. I certify that all material in this thesis which is not my own work has been identified and that no material has previously been submitted and approved for the award of a degree by this or any other University. Signature: _______________________________________________ 1 ABSTRACT Identifying the best control method for problematic wildlife is an ever present issue in wildlife management. Popular control methods have ranged from lethal techniques, extirpating the animal, to multiple non-lethal methods focused on deterring undesired behavior. In the past, lethal methods were the preferred choice. However, with increased awareness of the need for biodiversity conservation, new management methods focus on non-lethal control, with emphasis on exploiting aspects of naturally occurring organismal behaviors and ecology. Over the past decade, technological advances in extraction method’s and equipment have also developed new techniques providing a broader range of information about species biology for management use. One of the most well documented conflicts between wildlife and humans is that of the wolf. Using advanced technology and new techniques, we investigated the implication of using chemosensory signals in canid urine to modify behavior as a possible non-lethal alternative in large predator management. Here we used the SBSE method coupled with improved GC/MS equipment to analyze the volatile organic compounds in the urine of four canid species, gray wolf (Canis lupus), red wolf (Canis rufus), wolf-dog hybrids (Canis familiaris) and the domestic dog (Canis familiaris) in order to create working urinary profiles. The extraction method identified several compounds also seen in the urinary profiles of other large predators. In addition, similarities and differences were also noted between taxa and the sexes, and these can be further explored in future studies. Two identified urinary compounds, acetophenone and methyl propyl sulfide, were selected for further behavioral evaluation. We focused on these compounds and their influence as chemosensory signals triggering urine marking events in both the gray wolf and red wolf. Behavioral observations of the effects of these two chemicals indicated they elicited responses from captive wolves. At each of the three study sites, the combination of these chemicals produced urine-marking events along the territory boundary by dominant animals. As a result, the 2 investigation focused on what triggered the urine-marking events, the chemicals themselves, their combination, or the breakdown of the chemicals producing other odorants. It was found that there was no significant degradation of the chemicals over time and environmental conditions produced no significant breakdown of the acetophenone prior to the addition of methyl propyl sulfide. This posed a number of new questions and illustrated the need for additional behavioral studies. The results of this study analyzing chemosensory signals in canid urine, provides biologists with new information to aid in the development of new non-lethal management strategies for handling problematic wildlife as well as providing useful information for future research involving reproduction, predator/prey dynamics, territory maintenance, and a host of other studies focusing on animal ecology in association with chemosensory signaling. 3 ACKNOWLEGEMENTS First I would like to thank my supervisor Dr. David Hosken for his patience and support as I encountered many difficult and life altering events throughout the course of my research. His continued encouragement and guidance was much appreciated and I have been blessed tremendously through my working with him to see this project to completion. I would also like to thank additional members of my committee and academic support, Dr. Sasha Dall and Dr. John Hunt for their insight and continued follow-ups to ensure things were going well on both and academic and personal level respectively. I would like to further extend my gratitude to the Wolf Curator-Lori Schmidt, the directors, and staff of the International Wolf Center in Ely, Minnesota, USA; Tony Haighway founder and director of Wolf Watch UK, Wales; the director and staff of the Fort Worth Zoo, Fort Worth, Texas, USA; Will Waddell-Red Wolf Species Survival Plan Coordinator; Dr. David Rabon – U.S. Fish and Wildlife and director of the Red Wolf Recovery Program; Dr. James Raymer, Jocelyn Deese-Spruill, and the staff at RTI International Laboratory; the faculty and staff of Hardin-Simmons University; and the Texas Academy of Science for the volunteers, assistance, support, lab facilities, urine samples, and live animals used to facilitate this project. Finally, I thank the many friends and family who have encouraged me through the project and the many sacrifices that were made in order for me to complete the work. A special thank you to my son, Matthew Moran, who had to share his mother for the past few years as I traveled to various locations in the United States and to the United Kingdom to complete these studies. Your love and faith in me kept me going and gave me a strength and pride to continue following my dreams despite the hardships. Thank you all. I couldn’t have completed the project without each and every one of you. I am very blessed to have been graced with each of you. 4 Table of Contents Title Page: Scent-marking: Investigating chemosensory signals in wolf urine….. 1 Abstract…………………………………………………………………………………... 2 Acknowledgements……………………………………………………………………. 4 Table of Contents……………………………………………………………………… 5 Tables and Figures……………………………………………………………………. 6 Author’s Declarations…………………………………………………………………..9 Chapter One: Introduction……………………………………………………..11 Chapter Two: Analysis of volatile organics in canid urine using stir bar sorptive extraction [SBSE]………………………………………………………29 Chapter Three: Chemical analysis of volatile organics in urine of multiple canid species……………………………………………………………………..45 Chapter Four: Impact of select volatile organics from canid urinary profiles on scent-marking behaviors of wolves…..…………………………. 76 Chapter Five: Chemical air analysis of volatile organic breakdowns associated with scent-marking behaviors seen in canids………………….101 Chapter Six: General discussion: Scent-marking: Investigating chemosensory signals in wolf urine…………………………………………..123 Appendix I: Organic compounds identified in male canid urine using SBSE method…………………………………………………………………...135 Appendix II: Organic compounds identified in female canid urine using SBSE method…………………………………………………………………...139 Appendix III: Organic compounds identified in red wolf urine using SBSE method…………………………………………………………………………...142 5 Figures and Tables Chapter 1...............................................................................................................11 Box 1. Select public positions on wolf management across the globe…...16 Box 2. Lethal Control Methods………………………………………………..17 Box 3. Non-Lethal Control Methods…………………………………………..20 Chapter 2…………………………………………………………………………………29 Table 1. GC/MS Operating Parameters………………………………………35 Table 2. Check Standard Area of response………………………………....36 Figure 1. Comparison of wolf urine sample, system blank and stir bar blank……………………………………………………………………………....37 Figure 2. Reconstructed ion chromatograms from GC/MS analysis of volatile compounds found in the urine of male gray wolf…………………....38 Chapter 3………………………………………………………………………………...45 Table 1. GC/MS Operation Parameters……………………………………...51 Figure 1. Reconstructed ion chromatograms from GC/MS analysis of volatile compounds found in the urine of male gray wolf, red wolf, wolf- dog hybrid, and domestic dog……………………………………………….....53 Table 2. Compounds in male urine specific to each of the individual male canid species……………………………………………………………....54 Table 3. Organic compounds detected in male urine shared specifically between canid species……………………………………………………….....56 Table 4. Organic compounds detected in male urine in all four canid Species gray wolf, red wolf, wolf-dog hybrid, and domestic dog...………....57 Table 5. Compounds in female urine specific to each of the individual female canid species………………………………………………………….....59 Table 6. Organic compounds and retention times detected in urine of both red wolf and gray wolf female canid species.…………………………...60 Figure 2. Reconstructed ion chromatograms from GC/MS analysis of volatile compounds found in the urine of male gray wolf and female gray wolf…………………………………………………………………………….......61 6 Table 7. Organic compounds found in both gray wolf male and gray wolf female urine…………………………………………………………………........62 Table 8. Organic compounds detected in urine specific to male and female gray wolf……………………………………………………………….....63 Table 9. Gender based relationships in organic compounds detected in male and female red wolf urine profiles…………………………………….....64 Chapter 4………………………………………………………………………………...76 Figure 1. Activity levels of red wolves in the presence and absence of chemicals…………………………………………………………….………......86 Figure 2. Scent-marking behaviors of red wolves in the presence and absence of chemicals………………..………………………………………….87 Figure 3. Activity levels of gray wolves in the presence
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