HIBERNATION BIOLOGY OF RICHARDSON'S GROUND SQUIRRELS: HIBERNACULUM SYSTEMS AND ENERGY UTILIZATION T. Die Charge B.Sc. (Kin), Simon Fraser University, 1986 A Thesis Submitted to the School of Graduate Studies of the University of Lethbridge in Partial Fulfilment of the Requirements for the Degree MASTER OF SCIENCE Lethbridge, Alberta, Canada October. 2001 © T. Die Charge, 2001 DEDICATION To my first son, Nathan, who has been with me through it all. Daddy's gonna stay home tonight, and no, tiger, I don't have to work on my thesis. Wanna wrestle? And to my second son, Mackenzie, who has never known this task but has been nonetheless affected. Daddy's gonna try to stay home most nights, and no, slugger, I won't have to work on my thesis. Wanna wrestle when ya grow up a little? - iii - ABSTRACT I studied free-living Richardson's ground squirrels {Spermophilus richardsonii) using telemetry and total body electrical conductivity (TOBEC) to evaluate overwinter energy utilization and the impact of seed caching on body composition of males. I excavated 51 hibernation systems and found that 66% of 35 males cached 1 to 4 species of seed in the hibernaculum. Pre-emergent euthermy was shorter for 3 non-caching (0.7 ± 0.2 days) than for 13 caching males (4.0 ± 2.8 days), and metabolic predictions of overwinter mass loss approximated actual loss for non-caching males, but over-estimated mass loss for caching males. I concluded that caching males recouped some of the mass lost during hibernation by eating the cache during the longer period of pre-emergence euthermy. Based on TOBEC, the recouped mass included both fat and lean tissue. I suggest that caching in one year is a cost of reproduction that offsets the energetic demands of mating the following year. - iv - ACKNOWLEDGMENTS Funding for this research was provided by an American Society of Mammalogists Grant-in-Aid of Research and a Challenge Grant in Biodiversity from the University of Alberta to myself, and Natural Sciences and Engineering Research Council of Canada operating grants to Dr. Gail Michener. The purchase of the EM-Scan SA-2 small animal body composition analyzer was funded from a Natural Sciences and Engineering Research Council of Canada Equipment Grant awarded to Dr. Gail Michener and Dr. T. Andrew Hurly. I am profoundly grateful to Mark Bader and David Pankhurst for their humour and hard work during the long days of excavations and days of trapping in all types of weather. One never knows how or when such good friends cross your path, but I will always appreciate both of them for the shared experience. I am also grateful to Karen Dean, Anke-Maria Hoeffer, and Stacey Lacoste for their field and lab assistance. At the Lethbridge Agriculture and Agrifood Research Centre, I thank Brian Beres, Ron Dalton, Hugh McLean, and Dr. Stephen Morgan Jones for their gracious assistance with seed sorting, soil temperature data, and access to calibration animals. I also thank the unnamed property owner in Granum, Alberta, for access to the 2 pregnant females whose young I raised in captivity. I thank my supervisor, Dr. Gail Michener, for her guidance, financial support, and assistance in all aspects of this study. I also thank my other supervisory committee members, Dr. T. Andrew Hurly and Dr. Randall J. Weselake, for their guidance and support. I am very grateful for the logistical support and assistance of my many friends in . v - the Departments of Biological Sciences, Geography, and Psychology and Neuroscience at the University of Lethbridge, particularly Bruce McMullin and Bryan Kolb. They helped me keep the proverbial light visible and urged me to believe I should continue toward it. My parents, Betty and Glenn Charge, have expressed an unwavering faith in my ability to achieve this and many other goals. Their guidance gives me the chance to get the most out of life, and my successes are theirs. I am proud to have and return their love. Margaret Forgie has championed the care and development of our son Nathan during this time and has frequently stepped in to help me. Her support has helped me immeasurably and our boy's well-adjusted nature and early scholastic success is proof that we were right - ex-spouses can (and should) be good friends. My new daughter, Erika Montgomery, has shown me levels of understanding and compassion beyond her 13 years while she tried to get know a stepdad with his face glued to the computer. Vicki Charge has tolerated my many mood swings and fits of despair, my irregular hours, and my absences in most aspects of our young marriage. I have been astounded by (and grateful for) her patience, help, support, comfort, laughter, sympathy. I really cannot imagine reaching the end without having had her there. Her faith that, someday soon, our marriage can really begin with me as a full participant, is finally about to be realized. Finally, I thank one unnamed badger, who initially scared me into thinking that an entire year of field work was about to be lost, but who ultimately helped me learn more about these squirrels than I had planned. Who needs a shovel? TABLE OF CONTENTS Abstract iv Acknowledgements v Table of Contents vii List of Tables ix List of Figures x List of Abbreviations xii Chapter I Introduction 1 Literature Cited 4 Chapter II Estimation of lean body mass of Richardson's ground squirrels (Spermophilus richardsonii) using total body electrical conductivity (TOBEC) Abstract 7 Introduction 8 Methods 12 Results 18 Discussion 25 Literature Cited 29 Chapter III Effect of seed caches on changes in body composition of hibernating Richardson's ground squirrels {Spermophilus richardsonii) Abstract 35 Introduction 36 Methods 39 - vii - TABLE OF CONTENTS (Cont'd.) Chapter 111 Results 49 (cont'd.) Discussion 66 Literature Cited 74 Chapter IV Architecture and contents of the hibernacula of Richardson's ground squirrels (Spermophilus richardsonii) Abstract 78 Introduction 79 Methods 83 Results 90 Discussion 118 Literature Cited 132 Chapter V Summary 136 Literature Cited 139 - viii - LIST OF TABLES Chapter Table Title Page II Table 1. Semi-quantitative analysis of fluorescence in fecal 14 pellets collected at ~l-hr intervals after ingestion by 14 Richardson's ground squirrels of barley coated with fluorescent pigment. Table 2. Effects of gut filling and hydration status on body 24 composition in Richardson's ground squirrels. III Table 1. Sample size (n) of each age and sex class of 42 Richardson's ground squirrels used for the determination of body composition and overwinter energy utilization. Table 2. Comparisons of pre- and post-hibernation body 55 composition as determined by TOBEC between hibernating juvenile male Richardson's ground squirrels with (n =13) and without (n = 3) seed caches, and the changes that occurred during hibernation. Table 3. Mean ± 1 SE (range) duration and oxygen utilization 59 (V02) during different periods of hibernation for 9 radiocollared juvenile male Richardson's ground squirrels in 1997-1998 and 1998-1999 that survived to emergence. Table 4. Time to complete hibernation and changes in body mass 69 and composition in 4 species of ground squirrel (Spermophilus). IV Table 1. Immergence and maximum pre-hibernation masses of 92 radiocollared Richardson's ground squirrels and measurements ofhibernaculum systems used in 1997-1998 and 1998-1999. Table 2. Contents of hibernacula of Richardson's ground 112 squirrels pooled for 1997-1998 and 1998-1999. Table 3. Constituent seeds in hibernaculum caches of 23 male 116 Richardson's ground squirrels in 1997-1998 and 1998-1999. Table 4. Comparison ofhibernaculum characteristics for 2 120 species of ground squirrels. - ix - LIST OF FIGURES Chapter Figure Title Page II Figure 1. Relationship between TOBEC measurements of 20 19 Richardson's ground squirrels with and without eartags. Figure 2. Relationship of actual lean body mass (LBM) 20 determined by fat extraction and predicted LBM determined using TOBEC (at 37°C with eartags) and forelimb length for 30 Richardson's ground squirrels. Figure 3. The difference between TOBEC measurements at 37°C 22 and at 5 lower body temperatures (Tb), all for Richardson's ground squirrels with eartags removed. Ill Figure 1. Lean body mass (LBM) and fat body mass (FBM) 51 related to body mass of 28 Richardson's ground squirrels prior to hibernation and after either emergence, death, or exhumation. Figure 2. LBM as a function of FBM for 28 hibernating 53 Richardson's ground squirrels pre-hibernation and after either emergence, death, or exhumation. Figure 3. Mass losses during hibernation of 28 Richardson's 57 ground squirrels for which pre- and post-hibernation TOBEC readings were available. Figure 4. The percentage of total mass lost as fat (FBM) during 58 hibernation by 28 Richardson's ground squirrels for which pre- hibernation and final (at exhumation, death, or emergence) TOBEC readings were available. Figure 5. Predicted versus actual mass loss in 8 Richardson's 62 ground squirrels (5 oV, 3 ¥ ?) that did not have seed caches in the hibernaculum. Figure 6. The difference between predicted and actual mass loss 64 in 8 juvenile male Richardson's ground squirrels that survived hibernation and had seed caches, as a function of the amount of time spent euthermic at the end of hibernation prior to emergence. LIST OF FIGURES (Cont'd.) - X - Chapter Figure Title Page III Figure 7. Total mass loss during hibernation as a function of the 67 (cont'd) size of the seed cache remaining after hibernation in 8 juvenile Richardson's ground squirrels that completed hibernation. IV Figure 1. Orthographic renderings of 6 hibernation systems of 97 Richardson's ground squirrels representing one unique organization (1) and examples of the 3 basic plans (2-6).