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Open Pritchard Dissertation 2018 The Pennsylvania State University The Graduate School Department of Ecosystem Science and Management A LANDSCAPE OF FEAR: MEASURING NUTRITIONAL AND PSYCHOLOGICAL STRESS IN PREDATOR-PREY INTERACTIONS A Dissertation in Wildlife and Fisheries Science by Catharine Pritchard © 2018 Catharine Pritchard Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy December 2018 The dissertation of Catharine Pritchard was reviewed and approved* by the following: Tracy Langkilde Professor and Head of Biology, The Pennsylvania State University Dissertation Advisor C. Paola Ferreri Associate Professor of Fisheries Management, The Pennsylvania State University Chair of Committee Victoria Braithwaite Professor, The Pennsylvania State University Matthew Marshall Adjunct Assistant Professor of Wildlife Conservation, The Pennsylvania State University Michael Messina Professor and Head of Ecosystem Science and Management, The Pennsylvania State University *Signatures are on file in the Graduate School iii ABSTRACT Animals commonly respond to stimuli, including risk of predation, nutritional deficits, and disturbance through the stress response. The most commonly measured stress hormones, glucocorticoids (GCs), then generally become elevated, energy is diverted away from non- essential processes, and behavior is modified to facilitate short-term survival. Because GCs can be collected noninvasively, they are candidates for evaluating health in wild animals. However, few studies have tested critical assumptions about GCs and their relationships with other health- relevant measures in wild animals, which are commonly observed in laboratory settings. I tested if these relationships held in wild animals, using pumas (Puma concolor) and vicuñas (Vicugna vicugna) in a dyadic predator-prey system. In Chapter 2, I test the predictions that: 1) GCs in four biological matrices (blood, saliva, feces, and hair) collected during captures will be positively related, allowing different matrices to be used interchangeably, and 2) that elevated GC levels indicate poor condition by correlating with downstream health-relevant traits. I found little support for these predictions, and suggest these be validated for each species to properly interpret GC levels. In Chapter 3, I test the relationships between GC levels in different matrices and their downstream effects, collected during captures in two different habitats. I found that these relationships are not always consistent across habitat. In Chapter 4, I explore state-dependent foraging, using behavioral observations and fecal samples, from which I measured GCs and thyroid hormones to indicate levels of fear and nutritional deficits, respectively. There were no relationships between behavior and hormone concentrations, and I suggest this tradeoff may be difficult to detect in animals at baseline conditions. Lastly, in Chapter 5, I examine anti-predator behavior in response to estimates of direct and indirect risk. I report estimated home range sizes and successful chemical immobilization for vicuñas. By estimating dynamic interaction (across space and time), I found little response of vicuñas to direct risk, but found anticipatory anti- iv predatory behaviors in response to indirect risk, through diel migrations to avoid risky habitats at the riskiest time of day. These results provide a cautionary tale of GCs as physiological indicators of population health, and highlight the insights provided by quantifying dynamic interactions between species. v TABLE OF CONTENTS LIST OF FIGURES ................................................................................................................. viii LIST OF TABLES ................................................................................................................... x ACKNOWLEDGEMENTS ..................................................................................................... xi Chapter 1 Introduction ............................................................................................................ 1 The Physiological Stress Response ................................................................................. 2 The Hypothalamic-Pituitary-Thyroidal Axis .................................................................. 3 Study System ................................................................................................................... 4 Research Objectives ........................................................................................................ 6 Literature Cited ................................................................................................................ 9 Chapter 2 Lack of Correspondence Among Different Measures of Stress in a Wild Animal ............................................................................................................................. 18 Abstract ............................................................................................................................ 18 Introduction ...................................................................................................................... 19 Methods ........................................................................................................................... 21 Study System and Capture Protocol ........................................................................... 21 Glucocorticoid Sample Collection and Analysis ........................................................ 21 Downstream Effects Measurements and Analysis ..................................................... 23 Statistical Analysis ..................................................................................................... 25 Animals Ethics Statement ........................................................................................... 25 Results ............................................................................................................................. 25 Glucocorticoid Measurements .................................................................................... 25 Downstream Measurements ....................................................................................... 27 Discussion........................................................................................................................ 27 Relationships Between Matrices ................................................................................ 28 Short-Term Integrators ............................................................................................... 28 Short- and Long-Term Integrators .............................................................................. 29 Long-Term Integrators ............................................................................................... 30 Ability to Predict Downstream Effects ....................................................................... 31 Conclusions ..................................................................................................................... 35 Literature Cited ................................................................................................................ 38 Chapter 3 Few and Complex Relationships in Glucocorticoids and Fitness- Relevant Downstream Measures Between Habitats in a Wild Animal. ......................................... 62 Abstract ............................................................................................................................ 62 Introduction ...................................................................................................................... 62 Methods ........................................................................................................................... 65 Study Organism and Study Site ............................................................................. 65 Biological Sample Collection ................................................................................ 66 vi Glucocorticoid Sample Collection and Analysis ........................................... 66 Downstream Effects Measurements and Analysis ........................................ 67 Statistical Analysis ................................................................................................ 69 Animal Ethics Statement ....................................................................................... 69 Results ............................................................................................................................. 70 Discussion........................................................................................................................ 72 Conclusions ..................................................................................................................... 76 Literature Cited ................................................................................................................ 77 Chapter 4 Glucocorticoids and Triiodothyronine do not Correlate with Behavior in a Wild Mammal. .......................................................................................................................... 88 Abstract ............................................................................................................................ 88 Introduction ...................................................................................................................... 88 Methods ..........................................................................................................................
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