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Examination of the State-Dependency and Consequences of Foraging in a Low-Energy

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Examination of the State-Dependency and Consequences of Foraging in a Low-Energy Examination of the State-Dependency and Consequences of Foraging in a Low-Energy System, the Gila Monster, Heloderma Suspectum by Christian Wright A Dissertation Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy Approved April 2014 by the Graduate Supervisory Committee: Dale DeNardo, Chair Jon Harrison Kevin McGraw Brian Sullivan Blair Wolf ARIZONA STATE UNIVERSITY May 2014 ABSTRACT Foraging has complex effects on whole-organism homeostasis, and there is considerable evidence that foraging behavior is influenced by both environmental factors (e.g., food availability, predation risk) and the physiological condition of an organism. The optimization of foraging behavior to balance costs and benefits is termed state-dependent foraging (SDF) while behavior that seeks to protect assets of fitness is termed the asset protection principle (APP). A majority of studies examining SDF have focused on the role that energy balance has on the foraging of organisms with high metabolism and high energy demands ("high-energy systems" such as endotherms). In contrast, limited work has examined whether species with low energy use ("low-energy systems" such as vertebrate ectotherms) use an SDF strategy. Additionally, there is a paucity of evidence demonstrating how physiological and environmental factors other than energy balance influence foraging behavior (e.g. hydration state and free-standing water availability). Given these gaps in our understanding of SDF behavior and the APP, I examined the state-dependency and consequences of foraging in a low-energy system occupying a resource-limited environment - the Gila monster (Heloderma suspectum, Cope 1869). In contrast to what has been observed in a wide variety of taxa, I found that Gila monsters do not use a SDF strategy to manage their energy reserves and that Gila monsters do not defend their energetic assets. However, hydration state and free-standing water availability do affect foraging behavior of Gila monsters. Additionally, as Gila monsters become increasingly dehydrated, they reduce activity to defend hydration state. The SDF behavior of Gila monsters appears to be largely driven by the fact that Gila monsters i must separately satisfy energy and water demands with food and free-standing water, respectively, in conjunction with the timescale within which Gila monsters balance their energy and water budgets (supra-annually versus annually, respectively). Given these findings, the impact of anticipated changes in temperature and rainfall patterns in the Sonoran Desert are most likely going to pose their greatest risks to Gila monsters through the direct and indirect effects on water balance. ii DEDICATION I dedicate my dissertation work to the support of my many friends and my family. Thank you to my loving mother, Cyndy Wright, for all the words of encouragement, love, and support. To my brother Cory Wright, who has always pushed me to be my best and to his wife, Cathy Wright, for her continued support. To my niece Madeline Wright, whom I one day hope becomes a scientist! And especially to my grandparents, Louis and Elizabeth Headley, who always taught me to do what I loved and work hard every day. I would also like to give a special thanks to my closest friends, Dr. Zachary and Kaity Redfield-Ortiz, the Redfield/Taylor family, and Janin Polcovich, for being there throughout my entire doctoral program. iii ACKNOWLEDGMENTS This research was made possible through funding by the Graduate and Professional Students’ Association at Arizona State University (ASU), the ASU Foundation, the School of Life Sciences at ASU, College of Liberal Arts and Sciences at ASU, and the Peabody Family Memorial Graduate Fellowship. I greatly appreciate the support of Dr. Ty Hoffman, Dr. Michael Angilletta, Dr. John Sabo, Dr. Kevin McCluney, Dr. Jake Brashears, Dr. Zachary Stahlschmidt, Dr. Catriona Condon, Marin Jackson, Courtney Holden, Guillaume Demare, and Megan Murphy. Finally, I would like to extend a special thank you to my mother Cyndy Wright, my brother Cory Wright, my friends, my graduate committee, and to my graduate colleague and friend, Karla Moeller. iv TABLE OF CONTENTS Page LIST OF TABLES ............................................................................................................. ix LIST OF FIGURES ..........................................................................................................xii LIST OF SYMBOLS / NOMENCLATURE ................................................................. xiv CHAPTER 1 INTRODUCTION .................... ............................................................................ 1 2 EXAMINING COLD-ACCLIMATION METABOLIC RESPONSE AND THERMAL SENSITIVITY OF STANDARD METABOLIC RATE .............. 8 Introduction ................................................................................................ 8 Results ...................................................................................................... 10 Experiment 1 – Thermal Sensitivity of SMR ............................. 10 Experiment 2 – Acclimation of SMR to Cold Temperatures ..... 11 Discussion ................................................................................................ 11 Thermal Sensitivity of SMR ....................................................... 11 Acclimation of SMR to Cold Temperatures ............................... 13 Ecological Significance ............................................................... 15 Materials and Methods ............................................................................. 18 Experiment 1 – Thermal Sensitivity of SMR ............................. 18 Experiment 2 – Acclimation of SMR to Cold Temperatures ..... 21 Meta-analysis of Gila Monster SMR .......................................... 24 Statistical Analysis ...................................................................... 24 v CHAPTER Page 3 DO LOW ENERGY ORGANISMS PRACTICE STATE-DEPENDENT FORAGING STRATEGIES? ............................................................................. 33 Introduction .............................................................................................. 33 Results ...................................................................................................... 36 Surface Activity Estimates .......................................................... 36 Energy Expenditure per Day ....................................................... 37 Condition – Change in Tail Volume ........................................... 38 Total Body Water ........................................................................ 38 Hydration State ............................................................................ 38 Energy Expended Performing Different Activities .................... 39 Cost of Foraging .......................................................................... 40 Discussion ................................................................................................ 40 The Role of Energetics and Hydric Currencies in Satisfying Physiological Demands ............................................................... 41 Energetic State, SDF, the APP, and Possible Mechanisms Driving Foraging Behavior ....................................................................... 42 Hydration State and SDF ............................................................. 45 Ecological Implications .............................................................. 47 Materials and Methods ............................................................................. 48 Study Site and Weather Conditions ............................................ 48 Sample Sizes and Radiotelemetry ............................................... 49 Meal Supplementation ................................................................. 50 vi CHAPTER Page Body Condition and Hydration State .......................................... 50 Field Metabolic Rate and Total Body Water Estimates ............. 51 Surface Activity Estimates .......................................................... 53 Cost of Foraging .......................................................................... 54 Statistical Analysis ...................................................................... 56 4 THE IMPACT OF INDIVIDUAL VARIATION IN PHYSIOLOGICAL STATE ON FORAGING BEHAVIOR ACROSS MULTIPLE TIME SCALES: IMPLICATIONS FOR FUTURE STUDIES EXAMINING STATE-DEPENDENT FORAGING ........................................................................................................ 67 Introduction .............................................................................................. 67 Results ...................................................................................................... 72 Surface Activity and Tail Volume .............................................. 72 Surface Activity and Osmolality ................................................. 73 Tail Volume across Seasons and Years ...................................... 73 Plasma Osmolality across Seasons and Years ............................ 74 Discussion ................................................................................................ 74 Broader Contributions to SDF Theory ........................................ 74 Implications Associated with Global Climate Change .............. 78 Materials and Methods ............................................................................. 80 Study Site and Weather Conditions ...........................................
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